Apodaca Lab Research

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Epithelial Cell
Overview

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Stretch-Regulated
Membrane Traffic

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Tight Junction
Response to Stretch

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Mechanotransduction
in Urothelium


Epithelial cell overview: Epithelial tissues are comprised of continuous sheets of adherent epithelial cells that cover the body surfaces and cavities, form glands, and line the inner and outer surfaces of sac- and tube-shaped organs. Epithelial cells characteristically have an apical-basolateral asymmetry or polarity that is marked by compositionally, functionally, and morphologically distinct membrane domains: an apical one that is contiguous with the external milieu or faces the body cavities, and a basolateral domain that abuts the underlying tissues. By separating the external environment from the internal one, a function that depends, in part, on the tight junction, adjacent epithelial cells can perform specialized functions including vectorial water, ion, and peptide transport. Furthermore, their location at the interface of the external and internal milieus makes them ideally suited to form barriers to water, ions, and pathogens, to carry out immune surveillance, and to perform sensory transduction.


Stretch-regulated membrane traffic in bladder umbrella cells: Umbrella cells are the outermost cell layer of the the urothelium, a stratified epithelium that lines the renal pelvis, ureters, and bladder. These cells form a tight barrier that prevents solute flow and toxic metabolites in the urine from entering the underlying blood supply. Components of this barrier include tight junctions and an apical membrane with a specialized lipid and protein composition. An important aspect of the umbrella cell barrier is that it must accommodate large changes in volume as the bladder fills and empties. One mechanism used by these cells is massive exocytosis of a large population of subapical discoidal/fusiform vesicles (DFVs), which significantly increases the apical surface area of the cell. Coupled with changes in cell shape and expansion of the tight junction ring, the increased apical surface area allows for increased urine storage. Upon voiding, the added apical membrane must be recovered, a process we have shown is mediated by a clathrin-independent endocytic pathway that is regulated by the dynamin GTPase, RhoA, and the beta1 integrin. Some of our current research projects include: defining the mechanosensors and signal transduction cascades that occur in response to stretch; exploring the regulatory Rab GTPases, their effectors, and how stretch regulates these Rab-dependent signaling cascades; revealing how membrane stretch is coupled to integrin signaling and stimulation of the endocytic machinery; exploring the fate of endocytosed membrane and fluid in umbrella cells.


Regulation of tight junction morphology and function in response to stretch: Tight junctions (TJs) encircle adjacent epithelial cells, forming a seal that prevents the unregulated flux of ions, organic solutes, and water across the paracellular space. TJs are formed by the close apposition of anastomosing filamentous strands between the plasma membranes of neighboring cells. Claudins, major components of the strands, promote cell-cell adhesion and control paracellular permeability by forming anion-selective, cation-selective, or occluding pores. A critical feature of TJs is that they must maintain function in the face of mechanical stretch or shear stress, forces that are commonplace as air fills the lungs, as solids move along the epithelial surfaces of the gastrointestinal tract, or as fluid passes through the nephrons of the kidney or accumulates in sac-like organs such as the bladder. At present, surprisingly little is understood about how mechanical forces affect TJ activity (i.e. permeability), remodeling, and stability. Ongoing research projects in the laboratory include identification of umbrella cell claudins and defining their contribution to the umbrella cell TJ barrier, understanding the dynamics of the TJ during bladder filling and voiding, and understanding how solute flow across the TJs controls bladder function by affecting the activity of the afferent nerve processes that innervate the urothelium.


Mechanotransduction in the urothelium: The bladder, which undergoes cycles of filling and voiding, is governed by mechanical forces including changes in wall tension (i.e., stretch force), which must be sensed and then conveyed to the CNS. At the molecular level, mechanosensation depends on mechanosensors, which are specialized molecules that undergo changes in their conformation in direct response to mechanical stimuli and upon doing so, initiate mechanotransduction cascades. While mechanosensitive afferent nerve processes are important for normal bladder sensation, other cell types and tissues within the bladder wall are also likely play a critical role in this process. This includes the urothelium, which sits directly at the interface between the bladder proper and the urinary space, and in response to stretch releases mediators/neurotransmitters that are hypothesized to activate afferent processes. The major research question that we are addressing is what are the urothelial mechanosensors? One possibility, are the PIEZO channels, a small family (PIEZO1 and PIEZO2), which are expressed at low levels in the mouse urothelium. PIEZO channels are directly gated by stretch and they are non-selective cation channels that conduct Ca2+. The entrance of calcium into the cell is thought to initiate a signal transduction cascade that in the urothelium may result in the release of mediators. To assess the role of PIEZO channels in urothelial function, we have generated urothelial conditional knockout mice. Our current experiments are focused on characterizing these mice with the ultimate goal of understanding what role, if any, urothelial expressed PIEZO channels play in normal bladder function.

Apodaca Lab Publications


Primary Research Articles:

Maples CJ, Ruiz WG, Apodaca G. Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darby canine kidney cells. J Biol Chem. 1997 Mar 7;272(10):6741-51. PubMed PMID: 9045707.

Kang PJ, Hauser AR, Apodaca G, Fleiszig SM, Wiener-Kronish J, Mostov K, Engel JN. Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol. 1997 Jun;24(6):1249-62. PubMed PMID: 9218773.

Lavelle JP, Apodaca G, Meyers SA, Ruiz WG, Zeidel ML. Disruption of guinea pig urinary bladder permeability barrier in noninfectious cystitis. Am J Physiol. 1998 Jan;274(1 Pt 2):F205-14. PubMed PMID: 9458841.

Leung SM, Chen D, DasGupta BR, Whiteheart SW, Apodaca G. SNAP-23 requirement for transferrin recycling in Streptolysin-O-permeabilized Madin-Darby canine kidney cells. J Biol Chem. 1998 Jul 10;273(28):17732-41. PubMed PMID: 9651373.

Birder LA, Apodaca G, De Groat WC, Kanai AJ. Adrenergic- and capsaicin-evoked nitric oxide release from urothelium and afferent nerves in urinary bladder. Am J Physiol. 1998 Aug;275(2 Pt 2):F226-9. PubMed PMID: 9691011.

Henkel JR, Apodaca G, Altschuler Y, Hardy S, Weisz OA. Selective perturbation of apical membrane traffic by expression of influenza M2, an acid-activated ion channel, in polarized madin-darby canine kidney cells. Mol Biol Cell. 1998 Sep;9(9):2477-90. PubMed PMID: 9725907; PubMed Central PMCID: PMC25516.

Truschel ST, Ruiz WG, Shulman T, Pilewski J, Sun TT, Zeidel ML, Apodaca G. Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. J Biol Chem. 1999 May 21;274(21):15020-9. Review. PubMed PMID:10329705.

Altschuler Y, Liu S, Katz L, Tang K, Hardy S, Brodsky F, Apodaca G, Mostov K. ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J Cell Biol. 1999 Oct 4;147(1):7-12. PubMed PMID: 10508850; PubMed Central PMCID: PMC2164974.

Leung SM, Rojas R, Maples C, Flynn C, Ruiz WG, Jou TS, Apodaca G. Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase RhoA. Mol Biol Cell. 1999 Dec;10(12):4369-84. PubMed PMID: 10588664; PubMed Central PMCID: PMC25764.

Jou TS, Leung SM, Fung LM, Ruiz WG, Nelson WJ, Apodaca G. Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell. 2000 Jan;11(1):287-304. PubMed PMID: 10637309; PubMed Central PMCID: PMC14775.

Altschuler Y, Kinlough CL, Poland PA, Bruns JB, Apodaca G, Weisz OA, Hughey RP. Clathrin-mediated endocytosis of MUC1 is modulated by its glycosylation state. Mol Biol Cell. 2000 Mar;11(3):819-31. PubMed PMID: 10712502; PubMed Central PMCID: PMC14813.

Lavelle JP, Meyers SA, Ruiz WG, Buffington CA, Zeidel ML, Apodaca G. Urothelial pathophysiological changes in feline interstitial cystitis: a human model. Am J Physiol Renal Physiol. 2000 Apr;278(4):F540-53. PubMed PMID: 10751214.

Leung SM, Ruiz WG, Apodaca G. Sorting of membrane and fluid at the apical pole of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2000 Jun;11(6):2131-50. PubMed PMID: 10848634; PubMed Central PMCID: PMC14908.

Liu SH, Towler MC, Chen E, Chen CY, Song W, Apodaca G, Brodsky FM. A novel clathrin homolog that co-distributes with cytoskeletal components functions in the trans-Golgi network. EMBO J. 2001 Jan 15;20(1-2):272-84. PubMed PMID: 11226177; PubMed Central PMCID: PMC140205.

Rojas R, Ruiz WG, Leung SM, Jou TS, Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257-74. PubMed PMID: 11514615; PubMed Central PMCID: PMC58593.

Rajasekaran SA, Palmer LG, Moon SY, Peralta Soler A, Apodaca GL, Harper JF, Zheng Y, Rajasekaran AK. Na,K-ATPase activity is required for formation of tight junctions, desmosomes, and induction of polarity in epithelial cells. Mol Biol Cell. 2001 Dec;12(12):3717-32. PubMed PMID: 11739775; PubMed Central PMCID: PMC60750.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Magyar CE, White KE, Rojas R, Apodaca G, Friedman PA. Plasma membrane Ca2+-ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am J Physiol Renal Physiol. 2002 Jul;283(1):F29-40. PubMed PMID: 12060584.

Lavelle J, Meyers S, Ramage R, Bastacky S, Doty D, Apodaca G, Zeidel ML. Bladder permeability barrier: recovery from selective injury of surface epithelial cells. Am J Physiol Renal Physiol. 2002 Aug;283(2):F242-53. PubMed PMID: 12110507.

Birder LA, Nealen ML, Kiss S, de Groat WC, Caterina MJ, Wang E, Apodaca G, Kanai AJ. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci. 2002 Sep 15;22(18):8063-70. PubMed PMID: 12223560.

Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci. 2002 Sep;5(9):856-60. PubMed PMID: 12161756.

Kanai AJ, Zeidel ML, Lavelle JP, Greenberger JS, Birder LA, de Groat WC, Apodaca GL, Meyers SA, Ramage R, Epperly MW. Manganese superoxide dismutase gene therapy protects against irradiation-induced cystitis. Am J Physiol Renal Physiol. 2002 Dec;283(6):F1304-12. PubMed PMID: 12426235.

Apodaca G, Kiss S, Ruiz W, Meyers S, Zeidel M, Birder L. Disruption of bladder epithelium barrier function after spinal cord injury. Am J Physiol Renal Physiol. 2003 May;284(5):F966-76. Epub 2003 Jan 14. PubMed PMID: 12527557.

Wang E, Truschel S, Apodaca G. Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods. 2003 Jul;30(3):207-17. PubMed PMID: 12798135.

Wang EC, Lee JM, Johnson JP, Kleyman TR, Bridges R, Apodaca G. Hydrostatic pressure-regulated ion transport in bladder uroepithelium. Am J Physiol Renal Physiol. 2003 Oct;285(4):F651-63. Epub 2003 May 27. PubMed PMID: 12770841.

Kanai A, Epperly M, Pearce L, Birder L, Zeidel M, Meyers S, Greenberger J, de Groat W, Apodaca G, Peterson J. Differing roles of mitochondrial nitric oxide synthase in cardiomyocytes and urothelial cells. Am J Physiol Heart Circ Physiol. 2004 Jan;286(1):H13-21. Erratum in: Am J Physiol Heart Circ Physiol. 2009 Feb;296(2):H536. PubMed PMID: 14684357.

Pollack AL, Apodaca G, Mostov KE. Hepatocyte growth factor induces MDCK cell morphogenesis without causing loss of tight junction functional integrity. Am J Physiol Cell Physiol. 2004 Mar;286(3):C482-94. Epub 2003 Oct 30. PubMed PMID: 14592813.

Cetin S, Ford HR, Sysko LR, Agarwal C, Wang J, Neal MD, Baty C, Apodaca G, Hackam DJ. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J Biol Chem. 2004 Jun 4;279(23):24592-600. Epub 2004 Mar 30. PubMed PMID: 15169791.

Hill WG, Mathai JC, Gensure RH, Zeidel JD, Apodaca G, Saenz JP, Kinne-Saffran E, Kinne R, Zeidel ML. Permeabilities of teleost and elasmobranch gill apical membranes: evidence that lipid bilayers alone do not account for barrier function. Am J Physiol Cell Physiol. 2004 Jul;287(1):C235-42. Epub 2004 Mar 3. PubMed PMID: 14998788.

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Zeidel JD, Mathai JC, Campbell JD, Ruiz WG, Apodaca GL, Riordan J, Zeidel ML. Selective permeability barrier to urea in shark rectal gland. Am J Physiol Renal Physiol. 2005 Jul;289(1):F83-9. Epub 2005 Feb 22. PubMed PMID: 15727989.

Hill WG, Southern NM, MacIver B, Potter E, Apodaca G, Smith CP, Zeidel ML. Isolation and characterization of the Xenopus oocyte plasma membrane: a new method for studying activity of water and solute transporters. Am J Physiol Renal Physiol. 2005 Jul;289(1):F217-24. Epub 2005 Mar 1. PubMed PMID: 15741609.

Hill WG, Almasri E, Ruiz WG, Apodaca G, Zeidel ML. Water and solute permeability of rat lung caveolae: high permeabilities explained by acyl chain unsaturation. Am J Physiol Cell Physiol. 2005 Jul;289(1):C33-41. Epub 2005 Feb 23. PubMed PMID: 15728712.

Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA, Apodaca G. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Invest. 2005 Sep;115(9):2412-22. Epub 2005 Aug 18. PubMed PMID: 16110327; PubMed Central PMCID: PMC1187935.

Ducharme NA, Hales CM, Lapierre LA, Ham AJ, Oztan A, Apodaca G, Goldenring JR. MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol Biol Cell. 2006 Aug;17(8):3625-37. Epub 2006 Jun 14. PubMed PMID: 16775013; PubMed Central PMCID: PMC1525241.

Yu W, Zacharia LC, Jackson EK, Apodaca G. Adenosine receptor expression and function in bladder uroepithelium. Am J Physiol Cell Physiol. 2006 Aug;291(2):C254-65. Epub 2006 Mar 29. PubMed PMID: 16571869.

Morimoto T, Liu W, Woda C, Carattino MD, Wei Y, Hughey RP, Apodaca G, Satlin LM, Kleyman TR. Mechanism underlying flow stimulation of sodium absorption in the mammalian collecting duct. Am J Physiol Renal Physiol. 2006 Sep;291(3):F663-9. Epub 2006 Apr 25. PubMed PMID: 16638910.

Balestreire EM, Apodaca G. Apical epidermal growth factor receptor signaling: regulation of stretch-dependent exocytosis in bladder umbrella cells. Mol Biol Cell. 2007 Apr;18(4):1312-23. Epub 2007 Feb 7. PubMed PMID: 17287395; PubMed Central PMCID: PMC1838979.

Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Ameen N, Apodaca G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic. 2007 Aug;8(8):998-1006. Epub 2007 Jun 6. PubMed PMID: 17555536.

Cresawn KO, Potter BA, Oztan A, Guerriero CJ, Ihrke G, Goldenring JR, Apodaca G, Weisz OA. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 2007 Aug 22;26(16):3737-48. Epub 2007 Aug 2. PubMed PMID: 17673908; PubMed Central PMCID: PMC1952228.

Ducharme NA, Williams JA, Oztan A, Apodaca G, Lapierre LA, Goldenring JR. Rab11-FIP2 regulates differentiable steps in transcytosis. Am J Physiol Cell Physiol. 2007 Sep;293(3):C1059-72. Epub 2007 Jul 11. PubMed PMID: 17626244.

Oztan A, Silvis M, Weisz OA, Bradbury NA, Hsu SC, Goldenring JR, Yeaman C, Apodaca G. Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol Biol Cell. 2007 Oct;18(10):3978-92. Epub 2007 Aug 8. PubMed PMID: 17686995; PubMed Central PMCID: PMC1995710.

Hill WG, Meyers S, von Bodungen M, Apodaca G, Dedman JR, Kaetzel MA, Zeidel ML. Studies on localization and function of annexin A4a within urinary bladder epithelium using a mouse knockout model. Am J Physiol Renal Physiol. 2008 Apr;294(4):F919-27. Epub 2008 Feb 6. PubMed PMID: 18256316; PubMed Central PMCID: PMC2603049.

Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15773-8. Epub 2008 Oct 8. PubMed PMID: 18843107; PubMed Central PMCID: PMC2572972.

Studeny S, Cheppudira BP, Meyers S, Balestreire EM, Apodaca G, Birder LA, Braas KM, Waschek JA, May V, Vizzard MA. Urinary bladder function and somatic sensitivity in vasoactive intestinal polypeptide (VIP)-/- mice. J Mol Neurosci. 2008 Nov;36(1-3):175-87. Epub 2008 Jun 17. PubMed PMID: 18561033; PubMed Central PMCID: PMC2693375.

Yu W, Khandelwal P, Apodaca G. Distinct apical and basolateral membrane requirements for stretch-induced membrane traffic at the apical surface of bladder umbrella cells. Mol Biol Cell. 2009 Jan;20(1):282-95. Epub 2008 Nov 5. PubMed PMID: 18987341; PubMed Central PMCID: PMC2613117.

Khandelwal P, Ruiz WG, Apodaca G. Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J. 2010 Jun 16;29(12):1961-75. Epub 2010 May 11. PubMed PMID:20461056.

Yu W, Hill WG, Apodaca G, Zeidel ML. Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium. Am J Physiol Renal Physiol. 2011 Jan;300(1):F49-59. Epub 2010 Oct 13. PubMed PMID: 20943764; PubMed Central PMCID: PMC3023226.

Rondanino C, Poland PA, Kinlough CL, Li H, Rbaibi Y, Myerburg MM, Al-bataineh MM, Kashlan OB, Pastor-Soler NM, Hallows KR, Weisz OA, Apodaca G, Hughey RP. Galectin-7 modulates the length of the primary cilia and wound repair in polarized kidney epithelial cells. Am J Physiol Renal Physiol. 2011 Sep;301(3):F622-33. Epub 2011 Jun 15. PubMed PMID: 21677144; PubMed Central PMCID: PMC3174547.

Butterworth MB, Edinger RS, Silvis MR, Gallo LI, Liang X, Apodaca G, Fizzell RA, Johnson JP. Rab11b regulates the trafficking and recycling of the epithelial sodium channel (ENaC). Am J Physiol Renal Physiol. 2012 Mar;302(5):F581-90. doi: 10. 1152/ ajprenal. 00304. 2011. Epub 2011 Nov 30. PubMed PMID: 22129970; PubMed Central PMCID: PMC3353647.

Lapierre LA, Avant KM, Caldwell CM, Oztan A, Apodaca G, Knowles BC, Roland JT, Ducharme NA, Goldenring JR. Phosphorylation of Rab11-FIP2 regulates polarity in MDCK cells. Mol Biol Cell. 2012 Jun;23(12):2302-2318. Epub 2012 May 2. PubMed PMID: 22553350; PubMed Central PMCID: PMC3374749..

Prakasam HS, Herrington H, Roppolo JR, Jackson EK, Apodaca G. Modulation of bladder function by luminal adenosine turnover and A1 receptor activation. Am J Physiol Renal Physiol. 2012 Jul 15;303(2):F279-92. Epub 2012 May 2. PubMed PMID: 22552934; PubMed Central PMCID: PMC3404591.

Lapierre LA, Avant KM, Caldwell CM, Oztan A, Apodaca G, Knowles BC, Roland JT, Ducharme NA, Goldenring JR. Phosphorylation of Rab11-FIP2 regulates polarity in MDCK cells. Mol Biol Cell. 2012 Jun;23(12):2302-18. Epub 2012 May 2. PubMed PMID: 22553350; PubMed Central PMCID: PMC3374749.

Mitra S, Lukianov S, Ruiz WG, Cianciolo Cosentino C, Sanker S, Traub LM, Hukriede NA, Apodaca G. Requirement for a uroplakin 3a-like protein in the development of zebrafish pronephric tubule epithelial cell function, morphogenesis, and polarity. PLoS One. 2012;7(7):e41816. Epub 2012 Jul 25. PubMed PMID: 22848617; PubMed Central PMCID: PMC3404999.

Edinger RS, Bertrand CA, Rondandino C, Apodaca G, Johnson JP, Butterworth MB. The Epithelial Sodium Channel (ENaC) Establishes a Trafficking Vesicle Pool Responsible for Its Regulation. PLoS One. 2012;7(9):e46593. doi: 10.1371/journal.pone.0046593. Epub 2012 Sep 28. PubMed PMID: 23029554; PubMed Central PMCID: PMC3460899.

Hanna-Mitchell AT, Ruiz GW, Daneshgari F, Liu G, Apodaca G, Birder LA. Impact of diabetes mellitus on bladder uroepithelial cells. Am J Physiol Regul Integr Comp Physiol. 2013 Jan 15;304(2):R84-93. doi: 10.1152/ajpregu.00129.2012. Epub 2012 Nov 21. PubMed PMID: 23174855; PubMed Central PMCID: PMC3543662.

Szalinski CM, Guerriero CJ, Ruiz WG, Docter BE, Rbaibi Y, Pastor-Soler NM, Apodaca G, Puthenveedu MA, Weisz OA. PIP5KIβ Selectively Modulates Apical Endocytosis in Polarized Renal Epithelial Cells. PLoS One. 2013;8(1):e53790. PubMed PMID: 23342003; PubMedCentral PMCID: PMC3547069.

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Chakraborty S, Umasankar PK, Preston GM, Khandelwal P, Apodaca G, Watkins SC, Traub LM. A phosphotyrosine switch for cargo sequestration at clathrin-coated buds. J Biol Chem. 2014 Jun 20;289(25):17497-514. doi: 10.1074/jbc.M114.556589. Epub 2014 May 5. PubMed PMID: 24798335; PubMed Central PMCID: PMC4067187.

Gallo LI, Liao Y, Ruiz WG, Clayton DR, Li M, Liu YJ, Jiang Y, Fukuda M, Apodaca G, Yin XM. TBC1D9B functions as a GTPase-activating protein for Rab11a in polarized MDCK cells. Mol Biol Cell. 2014 Nov 15;25(23):3779-97. doi: 10.1091/mbc.E13-10-0604. Epub 2014 Sep 17. PubMed PMID: 25232007; PubMed Central PMCID: PMC4230784.

Prakasam HS, Gallo LI, Li H, Ruiz WG, Hallows KR, Apodaca G. A1 adenosine receptor-stimulated exocytosis in bladder umbrella cells requires phosphorylation of ADAM17 Ser-811 and EGF receptor transactivation. Mol Biol Cell. 2014 Nov 15;25(23):3798-812. doi: 10.1091/mbc.E14-03-0818. Epub 2014 Sep 17. PubMed PMID: 25232008; PubMed Central PMCID: PMC4230785.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Sep 30.2015. [Epub ahead of print] PubMed PMID: 26423859.

Gallo L, Apodaca G. Measuring receptor recycling in polarized MDCK cells. Methods Cell Biol. 2015;130:247-69. Epub 2015 Jun 11. PubMed PMID: 26360039.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PubMed PMID: 26423859; PubMed Central PMCID: PMC4683306.

Sneddon WB, Ruiz GW, Gallo LI, Xiao K, Zhang Q, Rbaibi Y, Weisz OA, Apodaca GL, Friedman PA. Convergent Signaling Pathways Regulate Parathyroid Hormone and Fibroblast Growth Factor-23 Action on NPT2A-mediated Phosphate Transport. J Biol Chem. 2016 Jul 18. pii: jbc.M116.744052. [Epub ahead of print] PubMed PMID: 27432882.

Moulton DE, Sulzer V, Apodaca G, Byrne HM, Waters S. Mathematical modeling of stretch-induced traffic in bladder umbrella cells. J Theor Biol. 2016. Nov 21;409:115-132. doi: 10.1016/j.jtbi.2016.08.032. PubMed PMID: 27590325.

Dimitrion P, Zhi Y, Clayton D, Apodaca G, Wilcox MR, Johnson JW, Nimgaonkar V, D'Aiuto L. Low-Density Neuronal Cultures from Human Induced Pluripotent Stem Cells. Mol Neuropsychiatry. 2017 Jul;3(1):28-36. doi: 10.1159/000476034. Epub 2017 Jun 17. PubMed PMID: 28879199; PubMed Central PMCID: PMC5582512.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

Kullmann FA, McDonnell BM, Wolf-Johnston AS, Lynn AM, Getchell SE, Ruiz WG, Zabbarova IV, Ikeda Y, Kanai AJ, Roppolo JR, Bastacky SI, Apodaca G, Buffington CAT, Birder LA. Inflammation and Tissue Remodeling in the Bladder and Urethra in Feline Interstitial Cystitis. Front Syst Neurosci. 2018 Apr 13;12:13. doi: 10.3389/fnsys.2018.00013. eCollection 2018. PubMed PMID: 29706873; PubMed Central PMCID: PMC5908978.

D'Aiuto L, Naciri J, Radio N, Tekur S, Clayton D, Apodaca G, Di Maio R, Zhi Y, Dimitrion P, Piazza P, Demers M, Wood J, Chu C, Callio J, McClain L, Yolken R, McNulty J, Kinchington P, Bloom D, Nimgaonkar V. Generation of three-dimensional human neuronal cultures: application to modeling CNS viral infections. Stem Cell Res Ther. 2018 May 11;9(1):134. doi: 10.1186/s13287-018-0881-6. PubMed PMID: 29751846; PubMed Central PMCID: PMC5948884.

Truschel ST, Clayton DR, Beckel JM, Yabes JG, Yao Y, Wolf-Johnston A, Birder LA, Apodaca G. Age-related endolysosome dysfunction in the rat urothelium. PLoS One. 2018 Jun 8;13(6):e0198817. doi: 10.1371/journal.pone.0198817. eCollection 2018. PubMed PMID: 29883476; PubMed Central PMCID: PMC5993304.

Montalbetti N, Stocker SD, Apodaca G, Bastacky SI, Carattino MD. Urinary K(+) promotes irritative voiding symptoms and pain in the face of urothelial barrier dysfunction. Sci Rep. 2019 Apr 2;9(1):5509. doi: 10.1038/s41598-019-41971-y. PubMed PMID: 30940909; PubMed Central PMCID: PMC6445132.

Kullmann AF, Truschel ST, Wolf-Johnston AS, McDonnell BM, Lynn AM, Kanai AJ, Kessler TM, Apodaca G, Birder LA. Acute spinal cord injury is associated with mitochondrial dysfunction in mouse urothelium. Neurourol Urodyn. 2019 Aug;38(6):1551-1559. doi: 10.1002/nau.24037. Epub 2019 May 18. PubMed PMID: 31102563.

Dalghi MG, Clayton DR, Ruiz WG, Al-Bataineh MM, Satlin LM, Kleyman TR, Ricke WA, Carattino MD, Apodaca G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol. 2019 Aug 1;317(2):F303-F321. doi: 10.1152/ajprenal.00214.2019. Epub 2019 Jun 5. PubMed PMID: 31166705; PubMed Central PMCID: PMC6732449.

Eaton AF, Clayton DR, Ruiz WG, Griffiths SE, Rubio ME, Apodaca G. Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Mol Biol Cell. 2019 Jul 22;30(16):2037-2052. doi: 10.1091/mbc.E19-02-0115. Epub 2019 Jun 5. PubMed PMID: 31166831; PubMed Central PMCID: PMC6727774.

Shiwarski D, Tashman J, Eaton A, Apodaca G, Feinberg A. 3D printed biaxial stretcher compatible with live fluorescence microscopy. In: HardwareX Elsevier, 2020 7:e00095.

Dalghi MG, Ruiz WG, Clayton DR, Montalbetti N, Daugherty SL, Beckel JM, Carattino MD, Apodaca G. Functional roles for PIEZO1 and PIEZO2 in urothelial mechanotransduction and lower urinary tract interoception. JCI Insight. 2021 Oct 8;6(19):e152984. doi: 10.1172/jci.insight.152984. PMID: 34464353; PMCID: PMC8525643.
 
Montalbetti N, Dalghi MG, Bastacky SI, Clayton DR, Ruiz WG, Apodaca G, Carattino MD. Bladder infection with uropathogenic Escherichia coli increases the excitability of afferent neurons. Am J Physiol Renal Physiol. 2022 Jan 1;322(1):F1-F13. doi: 10.1152/ajprenal.00167.2021. Epub 2021 Nov 15. PMID: 34779263; PMCID: PMC8698541.
 
Porter AW, Nguyen DN, Clayton DR, Ruiz WG, Mutchler SM, Ray EC, Marciszyn AL, Nkashama LJ, Subramanya AR, Gingras S, Kleyman TR, Apodaca G, Hendershot LM, Brodsky JL, Buck TM. The molecular chaperone GRP170 protects against ER stress and acute kidney injury in mice. JCI Insight. 2022 Mar 8;7(5):e151869. doi: 10.1172/jci.insight.151869. PMID: 35104250; PMCID: PMC8983141.


Review Articles:

Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic. 2001 Mar;2(3):149-59. Review. PubMed PMID: 11260520.

Apodaca G. Modulation of membrane traffic by mechanical stimuli. Am J Physiol Renal Physiol. 2002 Feb;282(2):F179-90. Review. PubMed PMID: 11788431.

Rojas R, Apodaca G. Immunoglobulin transport across polarized epithelial cells. Nat Rev Mol Cell Biol. 2002 Dec;3(12):944-55. Review. PubMed PMID: 12461560.

Traub LM, Apodaca G. AP-1B: polarized sorting at the endosome. Nat Cell Biol. 2003 Dec;5(12):1045-7. PubMed PMID: 14647300.

Apodaca G. The uroepithelium: not just a passive barrier. Traffic. 2004 Mar;5(3):117-28. Review. PubMed PMID: 15086788.

Apodaca G. Synaptotagmins: mediators of Ca2+-regulated vesicle fusion. Focus on "stable gene silencing of synaptotagmin I in rat PC12 cells inhibits Ca2+-evoked release of catecholamine". Am J Physiol Cell Physiol. 2006 Aug;291(2):C234-6. Epub 2006 May 31. PubMed PMID: 16738005.

Apodaca G, Balestreire E, Birder LA. The uroepithelial-associated sensory web. Kidney Int. 2007 Nov;72(9):1057-64. Epub 2007 Aug 1. Review. PubMed PMID: 17667988.

Oztan A, Rondanino C, Apodaca G. Transcytosis of polymeric immunoglobulin a in polarized Madin-Darby canine kidney cells. Methods Mol Biol. 2008;440:157-70. PubMed PMID: 18369944; PubMed Central PMCID: PMC2603048.

Khandelwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol. 2009 Dec;297(6):F1477 501. Epub 2009 Jul 8. Review. PubMed PMID: 19587142; PubMed Central PMCID: PMC2801337

Apodaca G. Opening ahead: early steps in lumen formation revealed. Nat Cell Biol. 2010 Nov;12(11):1026-8. PubMed PMID: 21045801.

Apodaca G, Gallo LI, Bryant DM. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol. 2012 Dec;14(12):1235-43. PubMed PMID: 23196841.

Apodaca G, Brown WJ. Membrane traffic research: challenges for the next decade. Front Cell Dev Biol. 2014 Sep 17;2:52. doi: 10.3389/fcell.2014.00052. eCollection 2014. PubMed PMID: 25364759; PubMed Central PMCID: PMC4207031.

Apodaca G. Role of Polarity Proteins in the Generation and Organization of Apical Surface Protrusions. Cold Spring Harb Perspect Biol. 2018 Jan 2;10(1):a027813. doi: 10.1101/cshperspect.a027813. PMID: 28264821; PMCID: PMC5587363.

Dalghi MG, Montalbetti N, Carattino MD, Apodaca G. The Urothelium: Life in a Liquid Environment. Physiol Rev. 2020 Oct 1;100(4):1621-1705. doi: 10.1152/physrev.00041.2019. Epub 2020 Mar 19. PMID: 32191559; PMCID: PMC7717127.


Books & Chapters:

Birder, LA, DeGroat, WC, Apodaca, G. Physiology of the urothelium. In Textbook of the Neurogenic Bladder, 2nd edition, J. Corcos and E. Schick, Eds. Informa Healthcare, London, G.B. 2008, pp 19-39.

Apodaca G, Gallo LI. Epithelial Polarity. In: Colloquium series on building blocks of the cell: cell structure and function. Nabi RI editor. Morgan and Claypool Life Sciences, 2013.

Apodaca Lab Image Gallery

EHD1 (green), actin (red), and nuclei (blue) distribution in rat proximal tubule cells.
Apical brush border of MYO6 KO mice.
Endocytosis of FITC-wheatgerm agglutinin (umbrella cell borders labeled with TRITC-phalloidin).
SEM of umbrella cell
Biotinylated apical surface (detected using FITC-streptavidin), actin (red), and nuclei (blue).
Binding of uropathogenic E.coli (false-colored blue) to umbrella cells.
Primary culture of cat urothelium showing distribution of UPK3a (green), ZO-1 (red), and nuclei (blue).
Cell junctions of epithelial cells lining the surface of the zebrafish larvae.
H&E-labeled cross section of rat bladder.
Cytokeratin-20 (green) and actin distribution in urothelium.
Apical brush border of rat enterocytes.
Dab2 (green), actin (red), and nuclei (blue) in rat kidney proximal tubule epithelial cells.
ENaC gamma subunit (green), Rab11b (red), and ZO-1 (blue) in mCCD cells.
SEM of lightbug eye and adjacent antenna.
Uptake of basolaterally internalized IgA in MDCK cells expressing the pIgR.
Cross section through pronephric tubule of 72 hpf zebrafish larvae.
Claudin-4 (green) and ZO-1 (red) staining of umbrella cell layer.
Ciliated epithelia in rat trachea.
UPK3a (green), actin (red), and nuclei (blue) in bladder umbrella cells.
Distribution of Sec6 (green) and Golgi (red) in MDCK cells.
Cross section through lumen of zebrafish larval pronephric tubule. Basal bodies are found at the left, cilia are in the lumen, and microvilli are found at the upper right.
Rab11a (green), actin (red), and nuclei (blue) in umbrella cell layer.
Voiding-induced uptake of FITC-wheatgerm agglutinin (green) in umbrella cells.
Paraneurons (aka brush cells) interdigitated between adjacent urethral epithelial cells.
Distribution of CFTR (green) and nuclei (red) in dogfish rectal gland.
Apical surface of umbrella cell showing discoidal- and/or fusiform-shaped vesicles (DFVs) and multi vesicular bodies (MB). inset: asymmetric unit membrane
3D reconstruction of umbrella cell layer stained with TRITC-phalloidin (red) and nuclei (blue).
Umbrella cell layer stained with TRITC-phalloidin (red) and ToPro3 (blue).
Mouse kidney proximal tubules stained with an antibody to the organic anion tranporter OAT1 (green), rhodamine phalloidin (red), and To-Pro3 (blue)
Distribution of E-cadherin (green) and nuclei (blue) in rat umbrella cells
Uropathogenic E.coli infection of mouse urothelium
Localization of cKIT+ interstitial cells and PDGFRA+ interstitial cells in mouse colon
Isolated bladder mucosa: PDGFRA (green), phalloidin (red), nuclei (blue)
MDCK cells: ZO1 (blue), galectin-9 (green), E-cadherin (red)
Mouse urothelium: keratin-20 (green), keratin-5 (red), nuclei (blue)
bladder intermuscular interstitial cells: smooth muscle (gray), CD34 (red), PDGFRA (green), nuclei (blue)
Suburothelial lamina propria of mouse bladder
Suburothelial fibroblasts: PDGFRA (green), TNC (red), CAR3 (white)

Current Apodaca Lab Members

Professor Gerard Apodaca, Ph.D.

Appointments: Departments of Medicine and Cell Biology

Director: Pittsburgh Center for Kidney Research Kidney Imaging Core

Contact Information:
University of Pittsburgh
Renal/Electrolyte Division
980 Scaife Hall
3550 Terrace Street
Pittsburgh, PA 15261

Telephone: 412-383-8893
E-mail: gla6@pitt.edu
Website: https://apodaca2.dept-med.pitt.edu

Education and Training:

Undergraduate:
B.A., Rollins College, Winter Park, FL, 1979–1983

Graduate:
Ph.D., University of California, San Francisco, CA, Dr. James McKerrow mentor, 1983-1989

Post-Doctoral:
University of California, San Francisco, CA, Dr. Keith Mostov mentor, 1989-1995

Stacks Image 3079

Primary Research Articles:

Asahi M, Lindquist R, Fukuyama K, Apodaca G, Epstein WL, McKerrow JH. Purification and characterization of major extracellular proteinases from Trichophyton rubrum. Biochem J. 1985 Nov 15;232(1):139-44. PubMed Central PMCID: PMC1152850.

Rutka JT, Giblin JR, Apodaca G, DeArmond SJ, Stern R, Rosenblum ML. Inhibition of growth and induction of differentiation in a malignant human glioma cell line by normal leptomeningeal extracellular matrix proteins. Cancer Res. 1987 Jul 1;47(13):3515-22. PubMed PMID: 3555773.

Apodaca G, McKerrow JH. Regulation of Trichophyton rubrum proteolytic activity. Infect Immun. 1989 Oct;57(10):3081-90. PubMed PMID: 2476398; PubMed Central PMCID: PMC260773.

Apodaca G, McKerrow JH. Purification and characterization of a 27,000-Mr extracellular proteinase from Trichophyton rubrum. Infect Immun. 1989 Oct;57(10):3072-80. PubMed PMID: 2674015; PubMed Central PMCID: PMC260772.

Apodaca G, McKerrow JH. Expression of proteolytic activity by cultures of Trichophyton rubrum. J Med Vet Mycol. 1990;28(2):159-71. PubMed PMID: 1696313.

Apodaca G, Rutka JT, Bouhana K, Berens ME, Giblin JR, Rosenblum ML, McKerrow JH, Banda MJ. Expression of metalloproteinases and metalloproteinase inhibitors by fetal astrocytes and glioma cells. Cancer Res. 1990 Apr 15;50(8):2322-9. PubMed PMID: 2156617.

Casanova JE, Apodaca G, Mostov KE. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell. 1991 Jul 12;66(1):65-75. PubMed PMID: 2070419.

Banda MJ, Howard EW, Herron GS, Apodaca G. Secreted inhibitors of metalloproteinases (IMPs) that are distinct from TIMP. Matrix Suppl. 1992;1:294-8. PubMed PMID: 1480040.

Lindstedt R, Apodaca G, Barondes SH, Mostov KE, Leffler H. Apical secretion of a cytosolic protein by Madin-Darby canine kidney cells. Evidence for polarized release of an endogenous lectin by a nonclassical secretory pathway. J Biol Chem. 1993 Jun 5;268(16):11750-7. PubMed PMID: 8505302.

Apodaca G, Aroeti B, Tang K, Mostov KE. Brefeldin-A inhibits the delivery of the polymeric immunoglobulin receptor to the basolateral surface of MDCK cells. J Biol Chem. 1993 Sep 25;268(27):20380-5. PubMed PMID: 8376395.

Apodaca G, Mostov KE. Transcytosis of placental alkaline phosphatase-polymeric immunoglobulin receptor fusion proteins is regulated by mutations of Ser664. J Biol Chem. 1993 Nov 5;268(31):23712-9. PubMed PMID: 8226896.

Apodaca G, Katz LA, Mostov KE. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol. 1994 Apr;125(1):67-86. PubMed PMID: 8138576; PubMed Central PMCID: PMC2120019.

Apodaca G, Enrich C, Mostov KE. The calmodulin antagonist, W-13, alters transcytosis, recycling, and the morphology of the endocytic pathway in Madin-Darby canine kidney cells. J Biol Chem. 1994 Jul 22;269(29):19005-13. PubMed PMID: 7913467.

Song W, Apodaca G, Mostov K. Transcytosis of the polymeric immunoglobulin receptor is regulated in multiple intracellular compartments. J Biol Chem. 1994 Nov 25;269(47):29474-80. PubMed PMID: 7961930.

Apodaca G, Bomsel M, Lindstedt R, Engel J, Frank D, Mostov KE, Wiener-Kronish J. Characterization of Pseudomonas aeruginosa-induced MDCK cell injury: glycosylation-defective host cells are resistant to bacterial killing. Infect Immun. 1995 Apr;63(4):1541-51. PubMed PMID: 7890421; PubMed Central PMCID: PMC173187.

Apodaca G, Cardone MH, Whiteheart SW, DasGupta BR, Mostov KE. Reconstitution of transcytosis in SLO-permeabilized MDCK cells: existence of an NSF-dependent fusion mechanism with the apical surface of MDCK cells. EMBO J. 1996 Apr 1;15(7):1471-81. PubMed PMID: 8612570; PubMed Central PMCID: PMC450054.

Enrich C, Apodaca G, Mostov KE. Calmodulin regulates the intracellular trafficking in epithelial cells. Z Gastroenterol. 1996 Jun;34 Suppl 3:83-5. PubMed PMID: 8767473.

van Ooij C, Apodaca G, Engel J. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect Immun. 1997 Feb;65(2):758-66. PubMed PMID: 9009339; PubMed Central PMCID: PMC176122.

Maples CJ, Ruiz WG, Apodaca G. Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darby canine kidney cells. J Biol Chem. 1997 Mar 7;272(10):6741-51. PubMed PMID: 9045707.

Kang PJ, Hauser AR, Apodaca G, Fleiszig SM, Wiener-Kronish J, Mostov K, Engel JN. Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol. 1997 Jun;24(6):1249-62. PubMed PMID: 9218773.

Lavelle JP, Apodaca G, Meyers SA, Ruiz WG, Zeidel ML. Disruption of guinea pig urinary bladder permeability barrier in noninfectious cystitis. Am J Physiol. 1998 Jan;274(1 Pt 2):F205-14. PubMed PMID: 9458841.

Leung SM, Chen D, DasGupta BR, Whiteheart SW, Apodaca G. SNAP-23 requirement for transferrin recycling in Streptolysin-O-permeabilized Madin-Darby canine kidney cells. J Biol Chem. 1998 Jul 10;273(28):17732-41. PubMed PMID: 9651373.

Birder LA, Apodaca G, De Groat WC, Kanai AJ. Adrenergic- and capsaicin-evoked nitric oxide release from urothelium and afferent nerves in urinary bladder. Am J Physiol. 1998 Aug;275(2 Pt 2):F226-9. PubMed PMID: 9691011.

Henkel JR, Apodaca G, Altschuler Y, Hardy S, Weisz OA. Selective perturbation of apical membrane traffic by expression of influenza M2, an acid-activated ion channel, in polarized madin-darby canine kidney cells. Mol Biol Cell. 1998 Sep;9(9):2477-90. PubMed PMID: 9725907; PubMed Central PMCID: PMC25516.

Truschel ST, Ruiz WG, Shulman T, Pilewski J, Sun TT, Zeidel ML, Apodaca G. Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. J Biol Chem. 1999 May 21;274(21):15020-9. Review. PubMed PMID:10329705.

Altschuler Y, Liu S, Katz L, Tang K, Hardy S, Brodsky F, Apodaca G, Mostov K. ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J Cell Biol. 1999 Oct 4;147(1):7-12. PubMed PMID: 10508850; PubMed Central PMCID: PMC2164974.

Leung SM, Rojas R, Maples C, Flynn C, Ruiz WG, Jou TS, Apodaca G. Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase RhoA. Mol Biol Cell. 1999 Dec;10(12):4369-84. PubMed PMID: 10588664; PubMed Central PMCID: PMC25764.

Jou TS, Leung SM, Fung LM, Ruiz WG, Nelson WJ, Apodaca G. Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell. 2000 Jan;11(1):287-304. PubMed PMID: 10637309; PubMed Central PMCID: PMC14775.

Altschuler Y, Kinlough CL, Poland PA, Bruns JB, Apodaca G, Weisz OA, Hughey RP. Clathrin-mediated endocytosis of MUC1 is modulated by its glycosylation state. Mol Biol Cell. 2000 Mar;11(3):819-31. PubMed PMID: 10712502; PubMed Central PMCID: PMC14813.

Lavelle JP, Meyers SA, Ruiz WG, Buffington CA, Zeidel ML, Apodaca G. Urothelial pathophysiological changes in feline interstitial cystitis: a human model. Am J Physiol Renal Physiol. 2000 Apr;278(4):F540-53. PubMed PMID: 10751214.

Leung SM, Ruiz WG, Apodaca G. Sorting of membrane and fluid at the apical pole of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2000 Jun;11(6):2131-50. PubMed PMID: 10848634; PubMed Central PMCID: PMC14908.

Liu SH, Towler MC, Chen E, Chen CY, Song W, Apodaca G, Brodsky FM. A novel clathrin homolog that co-distributes with cytoskeletal components functions in the trans-Golgi network. EMBO J. 2001 Jan 15;20(1-2):272-84. PubMed PMID: 11226177; PubMed Central PMCID: PMC140205.

Rojas R, Ruiz WG, Leung SM, Jou TS, Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257-74. PubMed PMID: 11514615; PubMed Central PMCID: PMC58593.

Rajasekaran SA, Palmer LG, Moon SY, Peralta Soler A, Apodaca GL, Harper JF, Zheng Y, Rajasekaran AK. Na,K-ATPase activity is required for formation of tight junctions, desmosomes, and induction of polarity in epithelial cells. Mol Biol Cell. 2001 Dec;12(12):3717-32. PubMed PMID: 11739775; PubMed Central PMCID: PMC60750.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Magyar CE, White KE, Rojas R, Apodaca G, Friedman PA. Plasma membrane Ca2+-ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am J Physiol Renal Physiol. 2002 Jul;283(1):F29-40. PubMed PMID: 12060584.

Lavelle J, Meyers S, Ramage R, Bastacky S, Doty D, Apodaca G, Zeidel ML. Bladder permeability barrier: recovery from selective injury of surface epithelial cells. Am J Physiol Renal Physiol. 2002 Aug;283(2):F242-53. PubMed PMID: 12110507.

Birder LA, Nealen ML, Kiss S, de Groat WC, Caterina MJ, Wang E, Apodaca G, Kanai AJ. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci. 2002 Sep 15;22(18):8063-70. PubMed PMID: 12223560.

Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci. 2002 Sep;5(9):856-60. PubMed PMID: 12161756.

Kanai AJ, Zeidel ML, Lavelle JP, Greenberger JS, Birder LA, de Groat WC, Apodaca GL, Meyers SA, Ramage R, Epperly MW. Manganese superoxide dismutase gene therapy protects against irradiation-induced cystitis. Am J Physiol Renal Physiol. 2002 Dec;283(6):F1304-12. PubMed PMID: 12426235.

Apodaca G, Kiss S, Ruiz W, Meyers S, Zeidel M, Birder L. Disruption of bladder epithelium barrier function after spinal cord injury. Am J Physiol Renal Physiol. 2003 May;284(5):F966-76. Epub 2003 Jan 14. PubMed PMID: 12527557.

Wang E, Truschel S, Apodaca G. Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods. 2003 Jul;30(3):207-17. PubMed PMID: 12798135.

Wang EC, Lee JM, Johnson JP, Kleyman TR, Bridges R, Apodaca G. Hydrostatic pressure-regulated ion transport in bladder uroepithelium. Am J Physiol Renal Physiol. 2003 Oct;285(4):F651-63. Epub 2003 May 27. PubMed PMID: 12770841.

Kanai A, Epperly M, Pearce L, Birder L, Zeidel M, Meyers S, Greenberger J, de Groat W, Apodaca G, Peterson J. Differing roles of mitochondrial nitric oxide synthase in cardiomyocytes and urothelial cells. Am J Physiol Heart Circ Physiol. 2004 Jan;286(1):H13-21. Erratum in: Am J Physiol Heart Circ Physiol. 2009 Feb;296(2):H536. PubMed PMID: 14684357.

Pollack AL, Apodaca G, Mostov KE. Hepatocyte growth factor induces MDCK cell morphogenesis without causing loss of tight junction functional integrity. Am J Physiol Cell Physiol. 2004 Mar;286(3):C482-94. Epub 2003 Oct 30. PubMed PMID: 14592813.

Cetin S, Ford HR, Sysko LR, Agarwal C, Wang J, Neal MD, Baty C, Apodaca G, Hackam DJ. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J Biol Chem. 2004 Jun 4;279(23):24592-600. Epub 2004 Mar 30. PubMed PMID: 15169791.

Hill WG, Mathai JC, Gensure RH, Zeidel JD, Apodaca G, Saenz JP, Kinne-Saffran E, Kinne R, Zeidel ML. Permeabilities of teleost and elasmobranch gill apical membranes: evidence that lipid bilayers alone do not account for barrier function. Am J Physiol Cell Physiol. 2004 Jul;287(1):C235-42. Epub 2004 Mar 3. PubMed PMID: 14998788.

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Zeidel JD, Mathai JC, Campbell JD, Ruiz WG, Apodaca GL, Riordan J, Zeidel ML. Selective permeability barrier to urea in shark rectal gland. Am J Physiol Renal Physiol. 2005 Jul;289(1):F83-9. Epub 2005 Feb 22. PubMed PMID: 15727989.

Hill WG, Southern NM, MacIver B, Potter E, Apodaca G, Smith CP, Zeidel ML. Isolation and characterization of the Xenopus oocyte plasma membrane: a new method for studying activity of water and solute transporters. Am J Physiol Renal Physiol. 2005 Jul;289(1):F217-24. Epub 2005 Mar 1. PubMed PMID: 15741609.

Hill WG, Almasri E, Ruiz WG, Apodaca G, Zeidel ML. Water and solute permeability of rat lung caveolae: high permeabilities explained by acyl chain unsaturation. Am J Physiol Cell Physiol. 2005 Jul;289(1):C33-41. Epub 2005 Feb 23. PubMed PMID: 15728712.

Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA, Apodaca G. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Invest. 2005 Sep;115(9):2412-22. Epub 2005 Aug 18. PubMed PMID: 16110327; PubMed Central PMCID: PMC1187935.

Ducharme NA, Hales CM, Lapierre LA, Ham AJ, Oztan A, Apodaca G, Goldenring JR. MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol Biol Cell. 2006 Aug;17(8):3625-37. Epub 2006 Jun 14. PubMed PMID: 16775013; PubMed Central PMCID: PMC1525241.

Yu W, Zacharia LC, Jackson EK, Apodaca G. Adenosine receptor expression and function in bladder uroepithelium. Am J Physiol Cell Physiol. 2006 Aug;291(2):C254-65. Epub 2006 Mar 29. PubMed PMID: 16571869.

Morimoto T, Liu W, Woda C, Carattino MD, Wei Y, Hughey RP, Apodaca G, Satlin LM, Kleyman TR. Mechanism underlying flow stimulation of sodium absorption in the mammalian collecting duct. Am J Physiol Renal Physiol. 2006 Sep;291(3):F663-9. Epub 2006 Apr 25. PubMed PMID: 16638910.

Balestreire EM, Apodaca G. Apical epidermal growth factor receptor signaling: regulation of stretch-dependent exocytosis in bladder umbrella cells. Mol Biol Cell. 2007 Apr;18(4):1312-23. Epub 2007 Feb 7. PubMed PMID: 17287395; PubMed Central PMCID: PMC1838979.

Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Ameen N, Apodaca G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic. 2007 Aug;8(8):998-1006. Epub 2007 Jun 6. PubMed PMID: 17555536.

Cresawn KO, Potter BA, Oztan A, Guerriero CJ, Ihrke G, Goldenring JR, Apodaca G, Weisz OA. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 2007 Aug 22;26(16):3737-48. Epub 2007 Aug 2. PubMed PMID: 17673908; PubMed Central PMCID: PMC1952228.

Ducharme NA, Williams JA, Oztan A, Apodaca G, Lapierre LA, Goldenring JR. Rab11-FIP2 regulates differentiable steps in transcytosis. Am J Physiol Cell Physiol. 2007 Sep;293(3):C1059-72. Epub 2007 Jul 11. PubMed PMID: 17626244.

Oztan A, Silvis M, Weisz OA, Bradbury NA, Hsu SC, Goldenring JR, Yeaman C, Apodaca G. Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol Biol Cell. 2007 Oct;18(10):3978-92. Epub 2007 Aug 8. PubMed PMID: 17686995; PubMed Central PMCID: PMC1995710.

Hill WG, Meyers S, von Bodungen M, Apodaca G, Dedman JR, Kaetzel MA, Zeidel ML. Studies on localization and function of annexin A4a within urinary bladder epithelium using a mouse knockout model. Am J Physiol Renal Physiol. 2008 Apr;294(4):F919-27. Epub 2008 Feb 6. PubMed PMID: 18256316; PubMed Central PMCID: PMC2603049.

Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15773-8. Epub 2008 Oct 8. PubMed PMID: 18843107; PubMed Central PMCID: PMC2572972.

Studeny S, Cheppudira BP, Meyers S, Balestreire EM, Apodaca G, Birder LA, Braas KM, Waschek JA, May V, Vizzard MA. Urinary bladder function and somatic sensitivity in vasoactive intestinal polypeptide (VIP)-/- mice. J Mol Neurosci. 2008 Nov;36(1-3):175-87. Epub 2008 Jun 17. PubMed PMID: 18561033; PubMed Central PMCID: PMC2693375.

Yu W, Khandelwal P, Apodaca G. Distinct apical and basolateral membrane requirements for stretch-induced membrane traffic at the apical surface of bladder umbrella cells. Mol Biol Cell. 2009 Jan;20(1):282-95. Epub 2008 Nov 5. PubMed PMID: 18987341; PubMed Central PMCID: PMC2613117.

Khandelwal P, Ruiz WG, Apodaca G. Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J. 2010 Jun 16;29(12):1961-75. Epub 2010 May 11. PubMed PMID:20461056.

Yu W, Hill WG, Apodaca G, Zeidel ML. Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium. Am J Physiol Renal Physiol. 2011 Jan;300(1):F49-59. Epub 2010 Oct 13. PubMed PMID: 20943764; PubMed Central PMCID: PMC3023226.

Rondanino C, Poland PA, Kinlough CL, Li H, Rbaibi Y, Myerburg MM, Al-bataineh MM, Kashlan OB, Pastor-Soler NM, Hallows KR, Weisz OA, Apodaca G, Hughey RP. Galectin-7 modulates the length of the primary cilia and wound repair in polarized kidney epithelial cells. Am J Physiol Renal Physiol. 2011 Sep;301(3):F622-33. Epub 2011 Jun 15. PubMed PMID: 21677144; PubMed Central PMCID: PMC3174547.

Butterworth MB, Edinger RS, Silvis MR, Gallo LI, Liang X, Apodaca G, Fizzell RA, Johnson JP. Rab11b regulates the trafficking and recycling of the epithelial sodium channel (ENaC). Am J Physiol Renal Physiol. 2012 Mar;302(5):F581-90. doi: 10. 1152/ ajprenal. 00304. 2011. Epub 2011 Nov 30. PubMed PMID: 22129970; PubMed Central PMCID: PMC3353647.

Lapierre LA, Avant KM, Caldwell CM, Oztan A, Apodaca G, Knowles BC, Roland JT, Ducharme NA, Goldenring JR. Phosphorylation of Rab11-FIP2 regulates polarity in MDCK cells. Mol Biol Cell. 2012 Jun;23(12):2302-2318. Epub 2012 May 2. PubMed PMID: 22553350; PubMed Central PMCID: PMC3374749..

Prakasam HS, Herrington H, Roppolo JR, Jackson EK, Apodaca G. Modulation of bladder function by luminal adenosine turnover and A1 receptor activation. Am J Physiol Renal Physiol. 2012 Jul 15;303(2):F279-92. Epub 2012 May 2. PubMed PMID: 22552934; PubMed Central PMCID: PMC3404591.

Lapierre LA, Avant KM, Caldwell CM, Oztan A, Apodaca G, Knowles BC, Roland JT, Ducharme NA, Goldenring JR. Phosphorylation of Rab11-FIP2 regulates polarity in MDCK cells. Mol Biol Cell. 2012 Jun;23(12):2302-18. Epub 2012 May 2. PubMed PMID: 22553350; PubMed Central PMCID: PMC3374749.

Mitra S, Lukianov S, Ruiz WG, Cianciolo Cosentino C, Sanker S, Traub LM, Hukriede NA, Apodaca G. Requirement for a uroplakin 3a-like protein in the development of zebrafish pronephric tubule epithelial cell function, morphogenesis, and polarity. PLoS One. 2012;7(7):e41816. Epub 2012 Jul 25. PubMed PMID: 22848617; PubMed Central PMCID: PMC3404999.

Edinger RS, Bertrand CA, Rondandino C, Apodaca G, Johnson JP, Butterworth MB. The Epithelial Sodium Channel (ENaC) Establishes a Trafficking Vesicle Pool Responsible for Its Regulation. PLoS One. 2012;7(9):e46593. doi: 10.1371/journal.pone.0046593. Epub 2012 Sep 28. PubMed PMID: 23029554; PubMed Central PMCID: PMC3460899.

Hanna-Mitchell AT, Ruiz GW, Daneshgari F, Liu G, Apodaca G, Birder LA. Impact of diabetes mellitus on bladder uroepithelial cells. Am J Physiol Regul Integr Comp Physiol. 2013 Jan 15;304(2):R84-93. doi: 10.1152/ajpregu.00129.2012. Epub 2012 Nov 21. PubMed PMID: 23174855; PubMed Central PMCID: PMC3543662.

Szalinski CM, Guerriero CJ, Ruiz WG, Docter BE, Rbaibi Y, Pastor-Soler NM, Apodaca G, Puthenveedu MA, Weisz OA. PIP5KIβ Selectively Modulates Apical Endocytosis in Polarized Renal Epithelial Cells. PLoS One. 2013;8(1):e53790. PubMed PMID: 23342003; PubMedCentral PMCID: PMC3547069.

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Chakraborty S, Umasankar PK, Preston GM, Khandelwal P, Apodaca G, Watkins SC, Traub LM. A phosphotyrosine switch for cargo sequestration at clathrin-coated buds. J Biol Chem. 2014 Jun 20;289(25):17497-514. doi: 10.1074/jbc.M114.556589. Epub 2014 May 5. PubMed PMID: 24798335; PubMed Central PMCID: PMC4067187.

Gallo LI, Liao Y, Ruiz WG, Clayton DR, Li M, Liu YJ, Jiang Y, Fukuda M, Apodaca G, Yin XM. TBC1D9B functions as a GTPase-activating protein for Rab11a in polarized MDCK cells. Mol Biol Cell. 2014 Nov 15;25(23):3779-97. doi: 10.1091/mbc.E13-10-0604. Epub 2014 Sep 17. PubMed PMID: 25232007; PubMed Central PMCID: PMC4230784.

Prakasam HS, Gallo LI, Li H, Ruiz WG, Hallows KR, Apodaca G. A1 adenosine receptor-stimulated exocytosis in bladder umbrella cells requires phosphorylation of ADAM17 Ser-811 and EGF receptor transactivation. Mol Biol Cell. 2014 Nov 15;25(23):3798-812. doi: 10.1091/mbc.E14-03-0818. Epub 2014 Sep 17. PubMed PMID: 25232008; PubMed Central PMCID: PMC4230785.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Sep 30.2015. [Epub ahead of print] PubMed PMID: 26423859.

Gallo L, Apodaca G. Measuring receptor recycling in polarized MDCK cells. Methods Cell Biol. 2015;130:247-69. Epub 2015 Jun 11. PubMed PMID: 26360039.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PubMed PMID: 26423859; PubMed Central PMCID: PMC4683306.

Sneddon WB, Ruiz GW, Gallo LI, Xiao K, Zhang Q, Rbaibi Y, Weisz OA, Apodaca GL, Friedman PA. Convergent Signaling Pathways Regulate Parathyroid Hormone and Fibroblast Growth Factor-23 Action on NPT2A-mediated Phosphate Transport. J Biol Chem. 2016 Jul 18. pii: jbc.M116.744052. [Epub ahead of print] PubMed PMID: 27432882.

Moulton DE, Sulzer V, Apodaca G, Byrne HM, Waters S. Mathematical modeling of stretch-induced traffic in bladder umbrella cells. J Theor Biol. 2016. Nov 21;409:115-132. doi: 10.1016/j.jtbi.2016.08.032. PubMed PMID: 27590325.

Dimitrion P, Zhi Y, Clayton D, Apodaca G, Wilcox MR, Johnson JW, Nimgaonkar V, D'Aiuto L. Low-Density Neuronal Cultures from Human Induced Pluripotent Stem Cells. Mol Neuropsychiatry. 2017 Jul;3(1):28-36. doi: 10.1159/000476034. Epub 2017 Jun 17. PubMed PMID: 28879199; PubMed Central PMCID: PMC5582512.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

Kullmann FA, McDonnell BM, Wolf-Johnston AS, Lynn AM, Getchell SE, Ruiz WG, Zabbarova IV, Ikeda Y, Kanai AJ, Roppolo JR, Bastacky SI, Apodaca G, Buffington CAT, Birder LA. Inflammation and Tissue Remodeling in the Bladder and Urethra in Feline Interstitial Cystitis. Front Syst Neurosci. 2018 Apr 13;12:13. doi: 10.3389/fnsys.2018.00013. eCollection 2018. PubMed PMID: 29706873; PubMed Central PMCID: PMC5908978.

D'Aiuto L, Naciri J, Radio N, Tekur S, Clayton D, Apodaca G, Di Maio R, Zhi Y, Dimitrion P, Piazza P, Demers M, Wood J, Chu C, Callio J, McClain L, Yolken R, McNulty J, Kinchington P, Bloom D, Nimgaonkar V. Generation of three-dimensional human neuronal cultures: application to modeling CNS viral infections. Stem Cell Res Ther. 2018 May 11;9(1):134. doi: 10.1186/s13287-018-0881-6. PubMed PMID: 29751846; PubMed Central PMCID: PMC5948884.

Truschel ST, Clayton DR, Beckel JM, Yabes JG, Yao Y, Wolf-Johnston A, Birder LA, Apodaca G. Age-related endolysosome dysfunction in the rat urothelium. PLoS One. 2018 Jun 8;13(6):e0198817. doi: 10.1371/journal.pone.0198817. eCollection 2018. PubMed PMID: 29883476; PubMed Central PMCID: PMC5993304.

Montalbetti N, Stocker SD, Apodaca G, Bastacky SI, Carattino MD. Urinary K(+) promotes irritative voiding symptoms and pain in the face of urothelial barrier dysfunction. Sci Rep. 2019 Apr 2;9(1):5509. doi: 10.1038/s41598-019-41971-y. PubMed PMID: 30940909; PubMed Central PMCID: PMC6445132.

Kullmann AF, Truschel ST, Wolf-Johnston AS, McDonnell BM, Lynn AM, Kanai AJ, Kessler TM, Apodaca G, Birder LA. Acute spinal cord injury is associated with mitochondrial dysfunction in mouse urothelium. Neurourol Urodyn. 2019 Aug;38(6):1551-1559. doi: 10.1002/nau.24037. Epub 2019 May 18. PubMed PMID: 31102563.

Dalghi MG, Clayton DR, Ruiz WG, Al-Bataineh MM, Satlin LM, Kleyman TR, Ricke WA, Carattino MD, Apodaca G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol. 2019 Aug 1;317(2):F303-F321. doi: 10.1152/ajprenal.00214.2019. Epub 2019 Jun 5. PubMed PMID: 31166705; PubMed Central PMCID: PMC6732449.

Eaton AF, Clayton DR, Ruiz WG, Griffiths SE, Rubio ME, Apodaca G. Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Mol Biol Cell. 2019 Jul 22;30(16):2037-2052. doi: 10.1091/mbc.E19-02-0115. Epub 2019 Jun 5. PubMed PMID: 31166831; PubMed Central PMCID: PMC6727774.

Shiwarski D, Tashman J, Eaton A, Apodaca G, Feinberg A. 3D printed biaxial stretcher compatible with live fluorescence microscopy. In: HardwareX Elsevier, 2020 7:e00095.

Dalghi MG, Ruiz WG, Clayton DR, Montalbetti N, Daugherty SL, Beckel JM, Carattino MD, Apodaca G. Functional roles for PIEZO1 and PIEZO2 in urothelial mechanotransduction and lower urinary tract interoception. JCI Insight. 2021 Oct 8;6(19):e152984. doi: 10.1172/jci.insight.152984. PMID: 34464353; PMCID: PMC8525643.
 
Montalbetti N, Dalghi MG, Bastacky SI, Clayton DR, Ruiz WG, Apodaca G, Carattino MD. Bladder infection with uropathogenic Escherichia coli increases the excitability of afferent neurons. Am J Physiol Renal Physiol. 2022 Jan 1;322(1):F1-F13. doi: 10.1152/ajprenal.00167.2021. Epub 2021 Nov 15. PMID: 34779263; PMCID: PMC8698541.
 
Porter AW, Nguyen DN, Clayton DR, Ruiz WG, Mutchler SM, Ray EC, Marciszyn AL, Nkashama LJ, Subramanya AR, Gingras S, Kleyman TR, Apodaca G, Hendershot LM, Brodsky JL, Buck TM. The molecular chaperone GRP170 protects against ER stress and acute kidney injury in mice. JCI Insight. 2022 Mar 8;7(5):e151869. doi: 10.1172/jci.insight.151869. PMID: 35104250; PMCID: PMC8983141.


Review Articles:

Rutka JT, Apodaca G, Stern R, Rosenblum M. The extracellular matrix of the central and peripheral nervous systems: structure and function. J Neurosurg. 1988 Aug;69(2):155-70. Review. PubMed PMID: 3292716.

Apodaca G, Bomsel M, Arden J, Breitfeld PP, Tang K, Mostov KE. The polymeric immunoglobulin receptor. A model protein to study transcytosis. J Clin Invest. 1991 Jun;87(6):1877-82. Review. PubMed PMID: 2040683; PubMed Central PMCID: PMC296937.

Mostov K, Apodaca G, Aroeti B, Okamoto C. Plasma membrane protein sorting in polarized epithelial cells. J Cell Biol. 1992 Feb;116(3):577-83. Review. PubMed PMID: 1730769; PubMed Central PMCID: PMC2289323.

Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic. 2001 Mar;2(3):149-59. Review. PubMed PMID: 11260520.

Apodaca G. Modulation of membrane traffic by mechanical stimuli. Am J Physiol Renal Physiol. 2002 Feb;282(2):F179-90. Review. PubMed PMID: 11788431.

Rojas R, Apodaca G. Immunoglobulin transport across polarized epithelial cells. Nat Rev Mol Cell Biol. 2002 Dec;3(12):944-55. Review. PubMed PMID: 12461560.

Traub LM, Apodaca G. AP-1B: polarized sorting at the endosome. Nat Cell Biol. 2003 Dec;5(12):1045-7. PubMed PMID: 14647300.

Apodaca G. The uroepithelium: not just a passive barrier. Traffic. 2004 Mar;5(3):117-28. Review. PubMed PMID: 15086788.

Apodaca G. Synaptotagmins: mediators of Ca2+-regulated vesicle fusion. Focus on "stable gene silencing of synaptotagmin I in rat PC12 cells inhibits Ca2+-evoked release of catecholamine". Am J Physiol Cell Physiol. 2006 Aug;291(2):C234-6. Epub 2006 May 31. PubMed PMID: 16738005.

Apodaca G, Balestreire E, Birder LA. The uroepithelial-associated sensory web. Kidney Int. 2007 Nov;72(9):1057-64. Epub 2007 Aug 1. Review. PubMed PMID: 17667988.

Oztan A, Rondanino C, Apodaca G. Transcytosis of polymeric immunoglobulin a in polarized Madin-Darby canine kidney cells. Methods Mol Biol. 2008;440:157-70. PubMed PMID: 18369944; PubMed Central PMCID: PMC2603048.

Khandelwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol. 2009 Dec;297(6):F1477 501. Epub 2009 Jul 8. Review. PubMed PMID: 19587142; PubMed Central PMCID: PMC2801337

Apodaca G. Opening ahead: early steps in lumen formation revealed. Nat Cell Biol. 2010 Nov;12(11):1026-8. PubMed PMID: 21045801.

Apodaca G, Gallo LI, Bryant DM. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol. 2012 Dec;14(12):1235-43. PubMed PMID: 23196841.

Apodaca G, Brown WJ. Membrane traffic research: challenges for the next decade. Front Cell Dev Biol. 2014 Sep 17;2:52. doi: 10.3389/fcell.2014.00052. eCollection 2014. PubMed PMID: 25364759; PubMed Central PMCID: PMC4207031.

Apodaca G. Role of Polarity Proteins in the Generation and Organization of Apical Surface Protrusions. Cold Spring Harb Perspect Biol. 2018 Jan 2;10(1):a027813. doi: 10.1101/cshperspect.a027813. PMID: 28264821; PMCID: PMC5587363.

Dalghi MG, Montalbetti N, Carattino MD, Apodaca G. The Urothelium: Life in a Liquid Environment. Physiol Rev. 2020 Oct 1;100(4):1621-1705. doi: 10.1152/physrev.00041.2019. Epub 2020 Mar 19. PMID: 32191559; PMCID: PMC7717127.



Books & Book Chapters:

Birder, LA, DeGroat, WC, Apodaca, G. Physiology of the urothelium. In Textbook of the Neurogenic Bladder, 2nd edition, J. Corcos and E. Schick, Eds. Informa Healthcare, London, G.B. 2008, pp 19-39.

Apodaca G, Gallo LI. Epithelial Polarity. In: Colloquium series on building blocks of the cell: cell structure and function. Nabi RI editor. Morgan and Claypool Life Sciences, 2013.

W. Giovanni Ruiz

Appointments: Department of Medicine

Contact Information:
University of Pittsburgh
Renal/Electrolyte Division
984 Scaife Hall
3550 Terrace Street
Pittsburgh, PA 15261

Telephone: 412-383-8892
E-mail: ruizw@pitt.edu

Education and Training:

Undergraduate:
Instituto Technico Agricultura, Barcenas Villa Nueva, Guatemala, 1974-1979

Stacks Image 3089

Primary Research Articles:

Maples CJ, Ruiz WG, Apodaca G. Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darby canine kidney cells. J Biol Chem. 1997 Mar 7;272(10):6741-51. PubMed PMID: 9045707.

Lavelle JP, Apodaca G, Meyers SA, Ruiz WG, Zeidel ML. Disruption of guinea pig urinary bladder permeability barrier in noninfectious cystitis. Am J Physiol. 1998 Jan;274(1 Pt 2):F205-14. PubMed PMID: 9458841.

Truschel ST, Ruiz WG, Shulman T, Pilewski J, Sun TT, Zeidel ML, Apodaca G. Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. J Biol Chem. 1999 May 21;274(21):15020-9. Review. PubMed PMID:10329705.

Leung SM, Rojas R, Maples C, Flynn C, Ruiz WG, Jou TS, Apodaca G. Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase RhoA. Mol Biol Cell. 1999 Dec;10(12):4369-84. PubMed PMID: 10588664; PubMed Central PMCID: PMC25764.

Jou TS, Leung SM, Fung LM, Ruiz WG, Nelson WJ, Apodaca G. Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell. 2000 Jan;11(1):287-304. PubMed PMID: 10637309; PubMed Central PMCID: PMC14775.

Lavelle JP, Meyers SA, Ruiz WG, Buffington CA, Zeidel ML, Apodaca G. Urothelial pathophysiological changes in feline interstitial cystitis: a human model. Am J Physiol Renal Physiol. 2000 Apr;278(4):F540-53. PubMed PMID: 10751214.

Leung SM, Ruiz WG, Apodaca G. Sorting of membrane and fluid at the apical pole of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2000 Jun;11(6):2131-50. PubMed PMID: 10848634; PubMed Central PMCID: PMC14908.

Rojas R, Ruiz WG, Leung SM, Jou TS, Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257-74. PubMed PMID: 11514615; PubMed Central PMCID: PMC58593.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Magyar CE, White KE, Rojas R, Apodaca G, Friedman PA. Plasma membrane Ca2+-ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am J Physiol Renal Physiol. 2002 Jul;283(1):F29-40. PubMed PMID: 12060584.

Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci. 2002 Sep;5(9):856-60. PubMed PMID: 12161756.

Apodaca G, Kiss S, Ruiz W, Meyers S, Zeidel M, Birder L. Disruption of bladder epithelium barrier function after spinal cord injury. Am J Physiol Renal Physiol. 2003 May;284(5):F966-76. Epub 2003 Jan 14. PubMed PMID: 12527557.

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Zeidel JD, Mathai JC, Campbell JD, Ruiz WG, Apodaca GL, Riordan J, Zeidel ML. Selective permeability barrier to urea in shark rectal gland. Am J Physiol Renal Physiol. 2005 Jul;289(1):F83-9. Epub 2005 Feb 22. PubMed PMID: 15727989.

Hill WG, Almasri E, Ruiz WG, Apodaca G, Zeidel ML. Water and solute permeability of rat lung caveolae: high permeabilities explained by acyl chain unsaturation. Am J Physiol Cell Physiol. 2005 Jul;289(1):C33-41. Epub 2005 Feb 23. PubMed PMID: 15728712.

Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA, Apodaca G. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Invest. 2005 Sep;115(9):2412-22. Epub 2005 Aug 18. PubMed PMID: 16110327; PubMed Central PMCID: PMC1187935.

Morimoto T, Liu W, Woda C, Carattino MD, Wei Y, Hughey RP, Apodaca G, Satlin LM, Kleyman TR. Mechanism underlying flow stimulation of sodium absorption in the mammalian collecting duct. Am J Physiol Renal Physiol. 2006 Sep;291(3):F663-9. Epub 2006 Apr 25. PubMed PMID: 16638910.

Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15773-8. Epub 2008 Oct 8. PubMed PMID: 18843107; PubMed Central PMCID: PMC2572972.

Khandelwal P, Ruiz WG, Apodaca G. Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J. 2010 Jun 16;29(12):1961-75. Epub 2010 May 11. PubMed PMID:20461056

Mitra S, Lukianov S, Ruiz WG, Cianciolo Cosentino C, Sanker S, Traub LM, Hukriede NA, Apodaca G. Requirement for a uroplakin 3a-like protein in the development of zebrafish pronephric tubule epithelial cell function, morphogenesis, and polarity. PLoS One. 2012;7(7):e41816. Epub 2012 Jul 25. PubMed PMID: 22848617; PubMed Central PMCID: PMC3404999.

Hanna-Mitchell AT, Ruiz GW, Daneshgari F, Liu G, Apodaca G, Birder LA. Impact of diabetes mellitus on bladder uroepithelial cells. Am J Physiol Regul Integr Comp Physiol. 2013 Jan 15;304(2):R84-93. doi: 10.1152/ajpregu.00129.2012. Epub 2012 Nov 21. PubMed PMID: 23174855; PubMed Central PMCID: PMC3543662.

Szalinski CM, Guerriero CJ, Ruiz WG, Docter BE, Rbaibi Y, Pastor-Soler NM, Apodaca G, Puthenveedu MA, Weisz OA. PIP5KIβ Selectively Modulates Apical Endocytosis in Polarized Renal Epithelial Cells. PLoS One. 2013;8(1):e53790. PubMed PMID: 23342003; PubMedCentral PMCID: PMC3547069

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Gallo LI, Liao Y, Ruiz WG, Clayton DR, Li M, Liu YJ, Jiang Y, Fukuda M, Apodaca G, Yin XM. TBC1D9B functions as a GTPase-activating protein for Rab11a in polarized MDCK cells. Mol Biol Cell. 2014 Nov 15;25(23):3779-97. doi: 10.1091/mbc.E13-10-0604. Epub 2014 Sep 17. PubMed PMID: 25232007; PubMed Central PMCID: PMC4230784.

Prakasam HS, Gallo LI, Li H, Ruiz WG, Hallows KR, Apodaca G. A1 adenosine receptor-stimulated exocytosis in bladder umbrella cells requires phosphorylation of ADAM17 Ser-811 and EGF receptor transactivation. Mol Biol Cell. 2014 Nov 15;25(23):3798-812. doi: 10.1091/mbc.E14-03-0818. Epub 2014 Sep 17. PubMed PMID: 25232008; PubMed Central PMCID: PMC4230785.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Sep 30.2015. [Epub ahead of print] PubMed PMID: 26423859.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PubMed PMID: 26423859; PubMed Central PMCID: PMC4683306.

Sneddon WB, Ruiz GW, Gallo LI, Xiao K, Zhang Q, Rbaibi Y, Weisz OA, Apodaca GL, Friedman PA. Convergent Signaling Pathways Regulate Parathyroid Hormone and Fibroblast Growth Factor-23 Action on NPT2A-mediated Phosphate Transport. J Biol Chem. 2016 Jul 18. pii: jbc.M116.744052. [Epub ahead of print] PubMed PMID: 27432882.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

Kullmann FA, McDonnell BM, Wolf-Johnston AS, Lynn AM, Getchell SE, Ruiz WG, Zabbarova IV, Ikeda Y, Kanai AJ, Roppolo JR, Bastacky SI, Apodaca G, Buffington CAT, Birder LA. Inflammation and Tissue Remodeling in the Bladder and Urethra in Feline Interstitial Cystitis. Front Syst Neurosci. 2018 Apr 13;12:13. doi: 10.3389/fnsys.2018.00013. eCollection 2018. PubMed PMID: 29706873; PubMed Central PMCID: PMC5908978.

Dalghi MG, Clayton DR, Ruiz WG, Al-Bataineh MM, Satlin LM, Kleyman TR, Ricke WA, Carattino MD, Apodaca G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol. 2019 Aug 1;317(2):F303-F321. doi: 10.1152/ajprenal.00214.2019. Epub 2019 Jun 5. PubMed PMID: 31166705; PubMed Central PMCID: PMC6732449.

Eaton AF, Clayton DR, Ruiz WG, Griffiths SE, Rubio ME, Apodaca G. Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Mol Biol Cell. 2019 Jul 22;30(16):2037-2052. doi: 10.1091/mbc.E19-02-0115. Epub 2019 Jun 5. PubMed PMID: 31166831; PubMed Central PMCID: PMC6727774.

Dalghi MG, Ruiz WG, Clayton DR, Montalbetti N, Daugherty SL, Beckel JM, Carattino MD, Apodaca G. Functional roles for PIEZO1 and PIEZO2 in urothelial mechanotransduction and lower urinary tract interoception. JCI Insight. 2021 Oct 8;6(19):e152984. doi: 10.1172/jci.insight.152984. PMID: 34464353; PMCID: PMC8525643.
 
Montalbetti N, Dalghi MG, Bastacky SI, Clayton DR, Ruiz WG, Apodaca G, Carattino MD. Bladder infection with uropathogenic Escherichia coli increases the excitability of afferent neurons. Am J Physiol Renal Physiol. 2022 Jan 1;322(1):F1-F13. doi: 10.1152/ajprenal.00167.2021. Epub 2021 Nov 15. PMID: 34779263; PMCID: PMC8698541.
 
Porter AW, Nguyen DN, Clayton DR, Ruiz WG, Mutchler SM, Ray EC, Marciszyn AL, Nkashama LJ, Subramanya AR, Gingras S, Kleyman TR, Apodaca G, Hendershot LM, Brodsky JL, Buck TM. The molecular chaperone GRP170 protects against ER stress and acute kidney injury in mice. JCI Insight. 2022 Mar 8;7(5):e151869. doi: 10.1172/jci.insight.151869. PMID: 35104250; PMCID: PMC8983141.

Dennis Clayton

Appointments: Department of Medicine

Contact Information:
University of Pittsburgh
Renal/Electrolyte Division
982 Scaife Hall
3550 Terrace Street
Pittsburgh, PA 15261

Telephone: 412-383-8892
E-mail: drc43@pitt.edu

Education and Training:

Undergraduate:
A.A., Pittsburgh Art Institute, Pittsburgh, PA

Stacks Image 3095

Primary Research Articles:

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Gallo LI, Liao Y, Ruiz WG, Clayton DR, Li M, Liu YJ, Jiang Y, Fukuda M, Apodaca G, Yin XM. TBC1D9B functions as a GTPase-activating protein for Rab11a in polarized MDCK cells. Mol Biol Cell. 2014 Nov 15;25(23):3779-97. doi: 10.1091/mbc.E13-10-0604. Epub 2014 Sep 17. PubMed PMID: 25232007; PubMed Central PMCID: PMC4230784.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Sep 30.2015. [Epub ahead of print] PubMed PMID: 26423859.

Gallo L, Apodaca G. Measuring receptor recycling in polarized MDCK cells. Methods Cell Biol. 2015;130:247-69. Epub 2015 Jun 11. PubMed PMID: 26360039.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PubMed PMID: 26423859; PubMed Central PMCID: PMC4683306.

Dimitrion P, Zhi Y, Clayton D, Apodaca G, Wilcox MR, Johnson JW, Nimgaonkar V, D'Aiuto L. Low-Density Neuronal Cultures from Human Induced Pluripotent Stem Cells. Mol Neuropsychiatry. 2017 Jul;3(1):28-36. doi: 10.1159/000476034. Epub 2017 Jun 17. PubMed PMID: 28879199; PubMed Central PMCID: PMC5582512.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

D'Aiuto L, Naciri J, Radio N, Tekur S, Clayton D, Apodaca G, Di Maio R, Zhi Y, Dimitrion P, Piazza P, Demers M, Wood J, Chu C, Callio J, McClain L, Yolken R, McNulty J, Kinchington P, Bloom D, Nimgaonkar V. Generation of three-dimensional human neuronal cultures: application to modeling CNS viral infections. Stem Cell Res Ther. 2018 May 11;9(1):134. doi: 10.1186/s13287-018-0881-6. PubMed PMID: 29751846; PubMed Central PMCID: PMC5948884.

Truschel ST, Clayton DR, Beckel JM, Yabes JG, Yao Y, Wolf-Johnston A, Birder LA, Apodaca G. Age-related endolysosome dysfunction in the rat urothelium. PLoS One. 2018 Jun 8;13(6):e0198817. doi: 10.1371/journal.pone.0198817. eCollection 2018. PubMed PMID: 29883476; PubMed Central PMCID: PMC5993304.

Dalghi MG, Clayton DR, Ruiz WG, Al-Bataineh MM, Satlin LM, Kleyman TR, Ricke WA, Carattino MD, Apodaca G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol. 2019 Aug 1;317(2):F303-F321. doi: 10.1152/ajprenal.00214.2019. Epub 2019 Jun 5. PubMed PMID: 31166705; PubMed Central PMCID: PMC6732449.

Eaton AF, Clayton DR, Ruiz WG, Griffiths SE, Rubio ME, Apodaca G. Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Mol Biol Cell. 2019 Jul 22;30(16):2037-2052. doi: 10.1091/mbc.E19-02-0115. Epub 2019 Jun 5. PubMed PMID: 31166831; PubMed Central PMCID: PMC6727774.

Dalghi MG, Ruiz WG, Clayton DR, Montalbetti N, Daugherty SL, Beckel JM, Carattino MD, Apodaca G. Functional roles for PIEZO1 and PIEZO2 in urothelial mechanotransduction and lower urinary tract interoception. JCI Insight. 2021 Oct 8;6(19):e152984. doi: 10.1172/jci.insight.152984. PMID: 34464353; PMCID: PMC8525643.
 
Montalbetti N, Dalghi MG, Bastacky SI, Clayton DR, Ruiz WG, Apodaca G, Carattino MD. Bladder infection with uropathogenic Escherichia coli increases the excitability of afferent neurons. Am J Physiol Renal Physiol. 2022 Jan 1;322(1):F1-F13. doi: 10.1152/ajprenal.00167.2021. Epub 2021 Nov 15. PMID: 34779263; PMCID: PMC8698541.
 
Porter AW, Nguyen DN, Clayton DR, Ruiz WG, Mutchler SM, Ray EC, Marciszyn AL, Nkashama LJ, Subramanya AR, Gingras S, Kleyman TR, Apodaca G, Hendershot LM, Brodsky JL, Buck TM. The molecular chaperone GRP170 protects against ER stress and acute kidney injury in mice. JCI Insight. 2022 Mar 8;7(5):e151869. doi: 10.1172/jci.insight.151869. PMID: 35104250; PMCID: PMC8983141.

Marianela Dalghi, M.Sc., Ph.D.

Appointments: Department of Medicine

Contact Information:
University of Pittsburgh
Renal/Electrolyte Division
982 Scaife Hall
3550 Terrace Street
Pittsburgh, PA 15261

Telephone: 412-383-8892
E-mail: mgd29@pitt.edu

Education and Training:

Undergraduate:
B.S., University of Buenos Aires, School of Pharmacy and Biochemistry, 2001-2008

Graduate:
M.Sc., University of Buenos Aires & Albert-Ludwigs-Universität, Freiberg, Germany, Dr. Juan Pablo Rossi mentor, 2008-2010
Ph.D., University of Buenos Aires, School of Pharmacy and Biochemistry, Dr. Juan Pablo Rossi mentor, 2010-2013

Postdoctoral:
University of Bern, Institute of Biochemistry and Molecular Medicine, Dr. Jürg Gertsch mentor, 2013-2015
University of Pittsburgh School of Medicine, Renal-Electrolyte Division, Dr. Gerard Apodaca mentor, 2016 - present

Fellowships:
Marianela received a postdoctoral fellowship from the American Urological Association

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Primary Research Articles:

Ossani G, Dalghi M, Repetto M. Oxidative damage lipid peroxidation in the kidney of choline-deficient rats. Front Biosci. 2007 Jan 1;12:1174-83. PubMed PMID: 17127370.

Montalbetti N, Cantero MR, Dalghi MG, Cantiello HF. Reactive oxygen species inhibit polycystin-2 (TRPP2) cation channel activity in term human syncytiotrophoblast. Placenta. 2008 Jun;29(6):510-8. doi: 10.1016/j.placenta.2008.02.015. PubMed PMID: 18417208.

Vanagas L, de La Fuente MC, Dalghi M, Ferreira-Gomes M, Rossi RC, Strehler EE, Mangialavori IC, Rossi JP. Differential effects of G- and F-actin on the plasma
membrane calcium pump activity. Cell Biochem Biophys. 2013 May;66(1):187-98. doi: 10.1007/s12013-012-9467-6. PubMed PMID: 23152090; PubMed Central PMCID: PMC3894748.

Dalghi MG, Fernández MM, Ferreira-Gomes M, Mangialavori IC, Malchiodi EL, Strehler EE, Rossi JP. Plasma membrane calcium ATPase activity is regulated by
actin oligomers through direct interaction. J Biol Chem. 2013 Aug 9;288(32):23380-93. doi: 10.1074/jbc.M113.470542. PubMed PMID: 23803603; PubMed Central PMCID: PMC3743507.

Montalbetti N, Simonin A, Dalghi MG, Kovacs G, Hediger MA. Development and Validation of a Fast and Homogeneous Cell-Based Fluorescence Screening Assay for
Divalent Metal Transporter 1 (DMT1/SLC11A2) Using the FLIPR Tetra. J Biomol Screen. 2014 Jul;19(6):900-8. doi: 10.1177/1087057114521663. PubMed PMID: 24505080.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

Dalghi MG, Clayton DR, Ruiz WG, Al-Bataineh MM, Satlin LM, Kleyman TR, Ricke WA, Carattino MD, Apodaca G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol. 2019 Aug 1;317(2):F303-F321. doi: 10.1152/ajprenal.00214.2019. Epub 2019 Jun 5. PubMed PMID: 31166705; PubMed Central PMCID: PMC6732449.

Dalghi MG, Ruiz WG, Clayton DR, Montalbetti N, Daugherty SL, Beckel JM, Carattino MD, Apodaca G. Functional roles for PIEZO1 and PIEZO2 in urothelial mechanotransduction and lower urinary tract interoception. JCI Insight. 2021 Oct 8;6(19):e152984. doi: 10.1172/jci.insight.152984. PMID: 34464353; PMCID: PMC8525643.
 
Montalbetti N, Dalghi MG, Bastacky SI, Clayton DR, Ruiz WG, Apodaca G, Carattino MD. Bladder infection with uropathogenic Escherichia coli increases the excitability of afferent neurons. Am J Physiol Renal Physiol. 2022 Jan 1;322(1):F1-F13. doi: 10.1152/ajprenal.00167.2021. Epub 2021 Nov 15. PMID: 34779263; PMCID: PMC8698541.
 


Review Articles:

Dalghi MG, Montalbetti N, Carattino MD, Apodaca G. The Urothelium: Life in a Liquid Environment. Physiol Rev. 2020 Oct 1;100(4):1621-1705. doi: 10.1152/physrev.00041.2019. Epub 2020 Mar 19. PMID: 32191559; PMCID: PMC7717127.



Previous Lab Members

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Steven Truschel, Ph.D.

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Amity Eaton, Ph.D.

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Sandeep Prakasam, Ph.D.

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Brady Bushover

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Luciana Gallo, Ph.D.

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Shalini Mitra, Ph.D.

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Puneet Khandelwal, Ph.D.

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Christina Rondanino, Ph.D.

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Asli Oztan, Ph.D.

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Elena Balestreire, M.D., Ph.D.

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Weiqun Yu, Ph.D.

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Edward Wang, Ph.D.

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Som-Ming Lueng, Ph.D.

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Raul Rojas, Ph.D.

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Prasad Acharya, M.D.

Sandeep Prakasam, Ph.D.

Education and Training:


Undergraduate:
B.S., Zoology, Loyola college, Chennai, India, 2003

Graduate:
M.S., Molecular Biology, Department of Genetics, University of Madras, India, 2008
Ph.D., Program in Integrative Molecular Biology, University of Pittsburgh, Gerard Apodaca mentor (2009-2013)

Current Position: Scientist, Prescient Life Sciences

Primary Research Articles:

Prakasam HS, Herrington H, Roppolo JR, Jackson EK, Apodaca G. Modulation of bladder function by luminal adenosine turnover and A1 receptor activation. Am J Physiol Renal Physiol. 2012 Jul 15;303(2):F279-92. Epub 2012 May 2. PubMed PMID: 22552934; PubMed Central PMCID: PMC3404591.

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Prakasam HS, Gallo LI, Li H, Ruiz WG, Hallows KR, Apodaca G. A1 adenosine receptor-stimulated exocytosis in bladder umbrella cells requires phosphorylation of ADAM17 Ser-811 and EGF receptor transactivation. Mol Biol Cell. 2014 Nov 15;25(23):3798-812. doi: 10.1091/mbc.E14-03-0818. Epub 2014 Sep 17. PubMed PMID: 25232008; PubMed Central PMCID: PMC4230785.

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA, Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PubMed PMID: 26423859; PubMed Central PMCID: PMC4683306.

Amity Eaton, Ph.D.

Education and Training:

Undergraduate:
B.A., Emory University, Atlanta, GA, 2005-2009.

Graduate:
Ph.D. University of Pittsburgh, Interdisciplinary Biomedical Graduate Program, Cell Biology and Molecular Physiology, 2014 - 2019

Fellowships: Amity was supported by an NIH National Research Service Award Pre-doctoral Fellowship

Current Position: Postdoctoral Fellow, Dennis Brown Laboratory, Massachusetts General Hospital, Harvard University

Primary Research Articles:

Montalbetti N, Rued AC, Clayton DR, Ruiz WG, Bastacky SI, Prakasam HS, Eaton AF, Kullmann FA Apodaca G, Carattino MD. Increased urothelial paracellular transport promotes cystitis. Am J Physiol Renal Physiol. 2015 Dec 15;309(12):F1070-81. doi: 10.1152/ajprenal.00200.2015. Epub 2015 Sep 30. PMID: 26423859; PMCID: PMC4683306.

Eaton AF, Clayton DR, Ruiz WG, Griffiths SE, Rubio ME, Apodaca G. Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Mol Biol Cell. 2019 Jul 22;30(16):2037-2052. doi: 10.1091/mbc.E19-02-0115. Epub 2019 Jun 5. PubMed PMID: 31166831; PubMed Central PMCID: PMC6727774.

Shiwarski D, Tashman J, Eaton A, Apodaca G, Feinberg A. 3D printed biaxial stretcher compatible with live fluorescence microscopy. In: HardwareX Elsevier, 2020 7:e00095.

Steven Truschel, Ph.D.

Appointments: Department of Cell Biology

Contact Information:
University of Pittsburgh
Department of Cell Biology
Telephone: 412-648-9409
E-mail: stt39@pitt.edu

Education and Training:

Undergraduate:
B.S., Pennsylvania State University, University Park, PA, 1990-1994

Graduate:
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 1996-2003

Postdoctoral:
University of Pennsylvania, Department of Pathology, Dr. Michael Marks mentor
Carnegie Mellon University, Department of Biological Sciences, Dr. Adam Linstedt, mentor

Current Position: Assistant Professor, University of Pittsburgh School of Medicine, Department of Cell Biology, 2018 - present

Primary Research Articles:

Truschel ST, Ruiz WG, Shulman T, Pilewski J, Sun TT, Zeidel ML, Apodaca G. Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. J Biol Chem. 1999 May 21;274(21):15020-9. Review. PubMed PMID:10329705.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Wang E, Truschel S, Apodaca G. Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods. 2003 Jul;30(3):207-17. PubMed PMID: 12798135.

Theos AC, Truschel ST, Raposo G, Marks MS. The Silver locus product Pmel17/gp100/Silv/ME20: controversial in name and in function. Pigment Cell Res. 2005 Oct;18(5):322-36. Review. PubMed PMID: 16162173; PubMed Central PMCID: PMC2788625.

Theos AC, Truschel ST, Tenza D, Hurbain I, Harper DC, Berson JF, Thomas PC, Raposo G, Marks MS. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev Cell. 2006 Mar;10(3):343-54. PubMed PMID: 16516837; PubMed Central PMCID: PMC1773005.

Setty SR, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC, Lamoreux ML, Di Pietro SM, Starcevic M, Bennett DC, Dell'Angelica EC, Raposo G, Marks MS. BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol Biol Cell. 2007 Mar;18(3):768-80. PubMed PMID: 17182842; PubMed Central PMCID: PMC1805088.

Truschel ST, Simoes S, Setty SR, Harper DC, Tenza D, Thomas PC, Herman KE, Sackett SD, Cowan DC, Theos AC, Raposo G, Marks MS. ESCRT-I function is required for Tyrp1 transport from early endosomes to the melanosome limiting membrane. Traffic. 2009 Sep;10(9):1318-36. doi: 10.1111/j.1600-0854.2009.00955.x. PubMed PMID: 19624486; PubMed Central PMCID: PMC2747296.

Truschel ST, Sengupta D, Foote A, Heroux A, Macbeth MR, Linstedt AD. Structure of the membrane-tethering GRASP domain reveals a unique PDZ ligand interaction that mediates Golgi biogenesis. J Biol Chem. 2011 Jun 10;286(23):20125-9. doi: 10.1074/jbc.C111.245324. PubMed PMID: 21515684; PubMed Central PMCID: PMC3121478.

Truschel ST, Zhang M, Bachert C, Macbeth MR, Linstedt AD. Allosteric regulation of GRASP protein-dependent Golgi membrane tethering by mitotic phosphorylation. J Biol Chem. 2012 Jun 8;287(24):19870-5. doi: 10.1074/jbc.M111.326256. PubMed PMID: 22523075; PubMed Central PMCID: PMC3370171.

Truschel ST, Clayton DR, Beckel JM, Yabes JG, Yao Y, Wolf-Johnston A, Birder LA, Apodaca G. Age-related endolysosome dysfunction in the rat urothelium. PLoS One. 2018 Jun 8;13(6):e0198817. doi: 10.1371/journal.pone.0198817. eCollection 2018. PubMed PMID: 29883476; PubMed Central PMCID: PMC5993304.

Kullmann AF, Truschel ST, Wolf-Johnston AS, McDonnell BM, Lynn AM, Kanai AJ, Kessler TM, Apodaca G, Birder LA. Acute spinal cord injury is associated with mitochondrial dysfunction in mouse urothelium. Neurourol Urodyn. 2019 Aug;38(6):1551-1559. doi: 10.1002/nau.24037. Epub 2019 May 18. PubMed PMID: 31102563

Brady Bushover

Education and Training:

Undergraduate:
B.S., University of Pittsburgh,

Current Position:
Graduate Student in the Graduate School of Public Health

Elena Balestreire, Ph.D.

Education and Training:

Undergraduate:
B.S., Computer Science and Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, 1997-2001

Graduate:
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 2003-2007
M.D., University of Pittsburgh, School of Medicine, 2009. Residency, Dermatology, Massachusetts General Hospital

Fellowships: Elena was supported by an NIH National Research Service Award Pre-doctoral Fellowship

Current Position: Assistant Professor of Dermatology, Massachusetts General Hospital, Harvard Medical School

Primary Research Articles:

Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA, Apodaca G. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Invest. 2005 Sep;115(9):2412-22. Epub 2005 Aug 18. PubMed PMID: 16110327; PubMed Central PMCID: PMC1187935.

Balestreire EM, Apodaca G. Apical epidermal growth factor receptor signaling: regulation of stretch-dependent exocytosis in bladder umbrella cells. Mol Biol Cell. 2007 Apr;18(4):1312-23. Epub 2007 Feb 7. PubMed PMID: 17287395; PubMed Central PMCID: PMC1838979.

Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15773-8. Epub 2008 Oct 8. PubMed PMID: 18843107; PubMed Central PMCID: PMC2572972.

Asli Oztan, Ph.D.

Education and Training:


Undergraduate:
B.Sc., Bogazici University, Istanbul, Turkey, 1992-1997

Graduate:
M.S., Bilkent University, Ankara, Turkey, 1997 - 1999
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 2007

Fellowships:
Asli was supported by an American Heart Association Predoctoral Fellowship

Current Position: Biomedical Informatics Scientist at Foundation Medicine

Primary Research Articles:

Ducharme NA, Hales CM, Lapierre LA, Ham AJ, Oztan A, Apodaca G, Goldenring JR. MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol Biol Cell. 2006 Aug;17(8):3625-37. Epub 2006 Jun 14. PubMed PMID: 16775013; PubMed Central PMCID: PMC1525241.

Cresawn KO, Potter BA, Oztan A, Guerriero CJ, Ihrke G, Goldenring JR, Apodaca G, Weisz OA. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 2007 Aug 22;26(16):3737-48. Epub 2007 Aug 2. PubMed PMID: 17673908; PubMed Central PMCID: PMC1952228.

Ducharme NA, Williams JA, Oztan A, Apodaca G, Lapierre LA, Goldenring JR. Rab11-FIP2 regulates differentiable steps in transcytosis. Am J Physiol Cell Physiol. 2007 Sep;293(3):C1059-72. Epub 2007 Jul 11. PubMed PMID: 17626244.

Oztan A, Silvis M, Weisz OA, Bradbury NA, Hsu SC, Goldenring JR, Yeaman C, Apodaca G. Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol Biol Cell. 2007 Oct;18(10):3978-92. Epub 2007 Aug 8. PubMed PMID: 17686995; PubMed Central PMCID: PMC1995710.

Methods Articles:


Oztan A, Rondanino C, Apodaca G. Transcytosis of polymeric immunoglobulin a in polarized Madin-Darby canine kidney cells. Methods Mol Biol. 2008;440:157-70. PubMed PMID: 18369944; PubMed Central PMCID: PMC2603048.

Weiqun Yu, Ph.D.

Education and Training:

Graduate:
M.D., Zhejiang University, School of Medicine, PRC 1993
M.S., Chongging University, National Key Laboratory of Tissue Engineering, PRC 1998
Ph.D., University of Pittsburgh, Program in Bio Engineering, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 2008

Fellowships: Weiqun was sponsored by an American Heart Association Predoctoral Fellowship

Current Position: Assistant Professor of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School

Primary Research Articles:

Yu W, Zacharia LC, Jackson EK, Apodaca G. Adenosine receptor expression and function in bladder uroepithelium. Am J Physiol Cell Physiol. 2006 Aug;291(2):C254-65. Epub 2006 Mar 29. PubMed PMID: 16571869.

Yu W, Khandelwal P, Apodaca G. Distinct apical and basolateral membrane requirements for stretch-induced membrane traffic at the apical surface of bladder umbrella cells. Mol Biol Cell. 2009 Jan;20(1):282-95. Epub 2008 Nov 5. PubMed PMID: 18987341; PubMed Central PMCID: PMC2613117.

Yu W, Hill WG, Apodaca G, Zeidel ML. Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium. Am J Physiol Renal Physiol. 2011 Jan;300(1):F49-59. Epub 2010 Oct 13. PubMed PMID: 20943764

Luciana Gallo, Ph.D.

Education and Training:

Undergraduate:
Licentiate in Biological Sciences, School of Exact and Natural Sciences, University of Buenos Aires, Argentina, 2004.

Graduate:
Ph.D., Cell Biology. School of Exact and Natural Sciences, University of Buenos Aires, Argentina, 2009.

Postdoctoral training in Apodaca lab.

Current position: Assistant Professor at the University of Buenos Aires, Argentina

Primary Research Articles:

Butterworth MB, Edinger RS, Silvis MR, Gallo LI, Liang X, Apodaca G, Fizzell RA, Johnson JP. Rab11b regulates the trafficking and recycling of the epithelial sodium channel (ENaC). Am J Physiol Renal Physiol. 2012 Mar;302(5):F581-90. doi: 10. 1152/ ajprenal. 00304. 2011. Epub 2011 Nov 30. PubMed PMID: 22129970; PubMed Central PMCID: PMC3353647.

Prakasam HS, Herrington H, Roppolo JR, Jackson EK, Apodaca G. Modulation of bladder function by luminal adenosine turnover and A1 receptor activation. Am J Physiol Renal Physiol. 2012 Jul 15;303(2):F279-92. Epub 2012 May 2. PubMed PMID: 22552934; PubMed Central PMCID: PMC3404591.

Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, Lukianov S, Peränen J, Goldenring JR, Apodaca G. A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell. 2013 Apr;24(7):1007-19. Epub 2013 Feb 6. PubMed Central PMCID: PMC3608489.

Carattino MD, Prakasam HS, Ruiz WG, Clayton DR, McGuire M, Gallo LI, Apodaca G. Bladder filling and voiding affect umbrella cell tight junction organization and function. Am J Physiol Renal Physiol. 2013 Oct;305(8):F1158-F1168. Epub 2013 Jul 24. PubMed PMID: 23884145.

Gallo LI, Liao Y, Ruiz WG, Clayton DR, Li M, Liu YJ, Jiang Y, Fukuda M, Apodaca G, Yin XM. TBC1D9B functions as a GTPase-activating protein for Rab11a in polarized MDCK cells. Mol Biol Cell. 2014 Nov 15;25(23):3779-97. doi: 10.1091/mbc.E13-10-0604. Epub 2014 Sep 17. PubMed PMID: 25232007; PubMed Central PMCID: PMC4230784.

Prakasam HS, Gallo LI, Li H, Ruiz WG, Hallows KR, Apodaca G. A1 adenosine receptor-stimulated exocytosis in bladder umbrella cells requires phosphorylation of ADAM17 Ser-811 and EGF receptor transactivation. Mol Biol Cell. 2014 Nov 15;25(23):3798-812. doi: 10.1091/mbc.E14-03-0818. Epub 2014 Sep 17. PubMed PMID: 25232008; PubMed Central PMCID: PMC4230785.

Gallo L, Apodaca G. Measuring receptor recycling in polarized MDCK cells. Methods Cell Biol. 2015;130:247-69. Epub 2015 Jun 11. PubMed PMID: 26360039.

Sneddon WB, Ruiz GW, Gallo LI, Xiao K, Zhang Q, Rbaibi Y, Weisz OA, Apodaca GL, Friedman PA. Convergent Signaling Pathways Regulate Parathyroid Hormone and Fibroblast Growth Factor-23 Action on NPT2A-mediated Phosphate Transport. J Biol Chem. 2016 Jul 18. pii: jbc.M116.744052. [Epub ahead of print] PubMed PMID: 27432882.

Gallo LI, Dalghi MG, Clayton DR, Ruiz WG, Khandelwal P, Apodaca G. RAB27B requirement for stretch-induced exocytosis in bladder umbrella cells. Am J Physiol Cell Physiol. 2018 Mar 1;314(3):C349-C365. doi: 10.1152/ajpcell.00218.2017. Epub 2017 Nov 22. PubMed PMID: 29167152.

Review Articles:

Apodaca G, Gallo LI, Bryant DM. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol. 2012 Dec;14(12):1235-43. PubMed PMID: 23196841.

Books:


Apodaca G, Gallo LI. Epithelial Polarity. In: Colloquium series on building blocks of the cell: cell structure and function. Nabi RI editor. Morgan and Claypool Life Sciences, 2013.

Christina Rondanino, Ph.D.

Education and Training:


Undergraduate:
B.Sc., University of Tours, Tours, France, 1997

Graduate:
M.S., Biochemistry, University of Tours, Tours, France, 1998
Ph.D., Molecular and Cellular Biology and Biophysics, University of Orleans, Orleans, France, 2003

Postdoctoral Training in Apodaca lab.

Fellowships: Christine was supported by an American Heart Association Postdoctoral Fellowship

Current Position: Assistant Professor, University of Rouen, France

Primary Research Articles:


Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Rondanino C, Poland PA, Kinlough CL, Li H, Rbaibi Y, Myerburg MM, Al-bataineh MM, Kashlan OB, Pastor-Soler NM, Hallows KR, Weisz OA, Apodaca G, Hughey RP. Galectin-7 modulates the length of the primary cilia and wound repair in polarized kidney epithelial cells. Am J Physiol Renal Physiol. 2011 Sep;301(3):F622-33. Epub 2011 Jun 15. PubMed PMID: 21677144; PubMed Central PMCID: PMC3174547.

Review Articles:

Oztan A, Rondanino C, Apodaca G. Transcytosis of polymeric immunoglobulin a in polarized Madin-Darby canine kidney cells. Methods Mol Biol. 2008;440:157-70. PubMed PMID: 18369944; PubMed Central PMCID: PMC2603048.

Edward Wang, Ph.D.

Education and Training:

Undergraduate:
B.S., University of Washington, Seattle, WA, 1993-1997

Graduate:
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 1997-2004

Current Position: Senior Director of Medical Affairs and Head, Global Publications & Scientific Communication Strategy, Quest Diagnostics

Primary Research Articles:

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Birder LA, Nealen ML, Kiss S, de Groat WC, Caterina MJ, Wang E, Apodaca G, Kanai AJ. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci. 2002 Sep 15;22(18):8063-70. PubMed PMID: 12223560.

Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci. 2002 Sep;5(9):856-60. PubMed PMID: 12161756.

Wang E, Truschel S, Apodaca G. Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods. 2003 Jul;30(3):207-17. PubMed PMID: 12798135.

Wang EC, Lee JM, Johnson JP, Kleyman TR, Bridges R, Apodaca G. Hydrostatic pressure-regulated ion transport in bladder uroepithelium. Am J Physiol Renal Physiol. 2003 Oct;285(4):F651-63. Epub 2003 May 27. PubMed PMID: 12770841.

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA, Apodaca G. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Invest. 2005 Sep;115(9):2412-22. Epub 2005 Aug 18. PubMed PMID: 16110327; PubMed Central PMCID: PMC1187935.

Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Shalini Mitra, Ph.D.

Education and Training:


Undergraduate:
B.S., Physiology, Presidency College, University of Calcutta, Kolkata, India, 2000

Graduate:
M.S., Life Sciences, Jawaharlal Nehru University, Delhi, India, 2003
Ph.D., Biochemistry and Molecular biology, University of Nebraska, Omaha, NE, 2008

Postdoctoral training in Apodaca lab.

Current Position:
Clinical Scientist at Novum Pharmaceuticals

Primary Research Articles:

Mitra S, Lukianov S, Ruiz WG, Cianciolo Cosentino C, Sanker S, Traub LM, Hukriede NA, Apodaca G. Requirement for a uroplakin 3a-like protein in the development of zebrafish pronephric tubule epithelial cell function, morphogenesis, and polarity. PLoS One. 2012;7(7):e41816. Epub 2012 Jul 25. PubMed PMID: 22848617; PubMed Central PMCID: PMC3404999.

Som-Ming Leung Ph.D.

Education and Training:

Undergraduate:

B.S., Carnegie Mellon University, Pittsburgh, PA, 1991-1995

Graduate:
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 1995-2001
M.B.A., Rutgers University, NJ, 2010

Current Position: Director, Program Management at Edge Therapeutics, Inc.

Primary Research Articles:

Leung SM, Chen D, DasGupta BR, Whiteheart SW, Apodaca G. SNAP-23 requirement for transferrin recycling in Streptolysin-O-permeabilized Madin-Darby canine kidney cells. J Biol Chem. 1998 Jul 10;273(28):17732-41. PubMed PMID: 9651373.

Leung SM, Rojas R, Maples C, Flynn C, Ruiz WG, Jou TS, Apodaca G. Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase RhoA. Mol Biol Cell. 1999 Dec;10(12):4369-84. PubMed PMID: 10588664; PubMed Central PMCID: PMC25764.

Jou TS, Leung SM, Fung LM, Ruiz WG, Nelson WJ, Apodaca G. Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell. 2000 Jan;11(1):287-304. PubMed PMID: 10637309; PubMed Central PMCID: PMC14775.

Leung SM, Ruiz WG, Apodaca G. Sorting of membrane and fluid at the apical pole of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2000 Jun;11(6):2131-50. PubMed PMID: 10848634; PubMed Central PMCID: PMC14908.

Rojas R, Ruiz WG, Leung SM, Jou TS, Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257-74. PubMed PMID: 11514615; PubMed Central PMCID: PMC58593.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Raul Rojas, Ph.D.

Education and Training:


Undergraduate:
B.S., University of Costa Rica, Costa Rica, CA

Graduate:
Ph.D., University of Pittsburgh, Program in Cell Biology and Molecular Physiology, Pittsburgh, PA, Dr. Gerard Apodaca mentor, 1997-2004

Postdoctoral training with Juan Bonafacino, NIH.

Fellowships: Raul was supported by an American Heart Association Predoctoral Fellowship

Current Position: Scientific Review Office, NIH, Bethesda, MD

Primary Research Articles:


Rondanino C, Rojas R, Ruiz WG, Wang E, Hughey RP, Dunn KW, Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic. 2007 Jul;8(7):932-49. Epub 2007 Jun 4. PubMed PMID: 17547697.

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Magyar CE, White KE, Rojas R, Apodaca G, Friedman PA. Plasma membrane Ca2+-ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am J Physiol Renal Physiol. 2002 Jul;283(1):F29-40. PubMed PMID: 12060584.

Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, Lavelle J, Zeidel M, Stoffer D, Apodaca G. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell. 2002 Mar;13(3):830-46. PubMed PMID: 11907265; PubMed Central PMCID: PMC99602.

Rojas R, Ruiz WG, Leung SM, Jou TS, Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257-74. PubMed PMID: 11514615; PubMed Central PMCID: PMC58593.

Leung SM, Rojas R, Maples C, Flynn C, Ruiz WG, Jou TS, Apodaca G. Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase RhoA. Mol Biol Cell. 1999 Dec;10(12):4369-84. PubMed PMID: 10588664; PubMed Central PMCID: PMC25764.

Review Articles:

Rojas R, Apodaca G. Immunoglobulin transport across polarized epithelial cells. Nat Rev Mol Cell Biol. 2002 Dec;3(12):944-55. Review. PubMed PMID: 12461560.

Prasad Acharya, Ph.D.

Education and Training:


Undergraduate:
B.A. in Biology, Johns Hopkins University, 1990-1994

Graduate:

M.D., University of Pittsburgh, 1994-1998

Current Position: Currently a physician in private practice.

Primary Research Articles:

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305-18. Epub 2004 Apr 6. PubMed PMID: 15068973.

Puneet Khandelwal, Ph.D.

Education and Training:


Undergraduate:
B.S., Microbiology, Delhi University, New Delhi, India, 1996

Graduate:
M.S., Department of Biotechnology, Panjab University India, 1999
Ph.D., Department of Biotechnology, Jawaharlal Nehru University, New Delhi, India, 2004

Postdoctoral training in the Apodaca lab.

Fellowships:
Puneet was supported by an American Heart Association Postdoctoral Fellowship and Career Development Award

Current Position: Scientist and Group Leader, Global Bioassays and Technology, Teva Pharmaceuticals R&D

Primary Research Articles:

Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15773-8. Epub 2008 Oct 8. PubMed PMID: 18843107; PubMed Central PMCID: PMC2572972.

Yu W, Khandelwal P, Apodaca G. Distinct apical and basolateral membrane requirements for stretch-induced membrane traffic at the apical surface of bladder umbrella cells. Mol Biol Cell. 2009 Jan;20(1):282-95. Epub 2008 Nov 5. PubMed PMID: 18987341; PubMed Central PMCID: PMC2613117.

Khandelwal P, Ruiz WG, Apodaca G. Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J. 2010 Jun 16;29(12):1961-75. Epub 2010 May 11. PubMed PMID:20461056.

Chakraborty S, Umasankar PK, Preston GM, Khandelwal P, Apodaca G, Watkins SC, Traub LM. A phosphotyrosine switch for cargo sequestration at clathrin-coated buds. J Biol Chem. 2014 Jun 20;289(25):17497-514. doi: 10.1074/jbc.M114.556589. Epub 2014 May 5. PubMed PMID: 24798335; PubMed Central PMCID: PMC4067187.

Review Articles:

Khandelwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol. 2009 Dec;297(6):F1477 501. Epub 2009 Jul 8. Review. PubMed PMID: 19587142; PubMed Central PMCID: PMC2801337

Predoctoral and Postdoctoral Training in the Apodaca Lab

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The Apodaca laboratory:
Our laboratory provides a dynamic and exciting environment for predoctoral (Ph.D.) and postdoctoral training. In addition to obtaining instruction at the benchtop, trainees participate in weekly research seminars, lab meetings, a cell biology journal club, the annual Local Traffic symposium on intracellular membrane traffic, and national meetings. Furthermore, trainees interface with a large group of investigators interested in membrane traffic, epithelial biology, and bladder physiology here at the University of Pittsburgh. See our Environment in the next section of this website below to learn more about the City of Pittsburgh, the University, and the Apodaca lab.

Ph.D. Training:
Prospective students interested in Ph.D. training are encouraged to apply to the following Ph.D. training programs: 

The Interdisciplinary Biomedical Graduate Program (www.gradbiomed.pitt.edu), with an emphasis in Cell Biology and Molecular Physiology (www.cbmp.pitt.edu). 

Integrative Systems Biology (www.isb.pitt.edu).

Students interested in laboratory rotations can learn the following techniques:
Confocal and electron microscopy, cell culture, use of animal models to study tissues ex vivo and in vivo, biochemistry, measurement of protein-protein interactions, protein purification, mutagenesis of DNA and transfection/transduction of polarized cells including use of in vivo methods, and electrophysiological methods to analyze membrane traffic. 

Post-Doctoral Training:
The training of post-doctoral fellows for independent research careers is a major goal of the laboratory. Applicants with prior training in cell, molecular, or developmental biology or biochemistry are particularly encouraged to apply. To apply for a post-doctoral fellowship in the laboratory, please provide: A detailed curriculum vitae that includes training and degrees (include pending degrees); a list of papers published, in press, and in preparation; a statement of citizenship, permanent residency, or Visa status; and the names and addresses of at least 3 referees. Please also include a statement of your reason for interest in the lab and your goals for a post-doctoral fellowship.

Fellowships:
An important skill that all trainees must learn is how to write a successful research grant. The following lab members (past and present) have been awarded competitive research fellowships:

Marianela Dalghi - postdoctoral fellowship from the American Urological Association
Amity Eaton - predoctoral NRSA from the National Institutes of Health
Puneet Khandelwal
- postdoctoral fellowships from the National Kidney Foundation and American Heart Association
Luciana Gallo - postdoctoral fellowship from the American Heart Association
Asli Oztan - predoctoral fellowship from the American Heart Association
Elena Balestreire-Hawryluk - predoctoral NRSA from the National Institutes of Health
Christine Rondanino - postdoctoral fellowship from the American Heart Association
Weiqun Yu - predoctoral fellowship from the American Heart Association
Raul Rojas - predoctoral fellowship from the American Heart Association

Trainees in my laboratory are eligible to apply for an NIH T32 grant-sponsored training fellowship. In addition, pre-doctoral students can participate as a teaching assistant in medical school tissue courses and labs.

Undergraduate research training:
The Apodaca laboratory also participates in the University of Pittsburgh School of Medicine Summer Undergraduate Research Program. Click here to learn more about this program.

Environment

The City of Pittsburgh:

The Pittsburgh metropolitan area population is 2.4 million, although only 300,000 residents live within the city itself. The city was once the center of the steel industry; however, it has now shed its outdated industrial image and is gaining recognition worldwide for its advanced medical facilities, major universities, myriad cultural institutions, and start-up technology companies. Pittsburgh has one of the countries most dynamic visual and performing arts and music scene, and the city contains appealing vistas, large parks and recreational facilities, and beautiful neighborhoods. Pittsburgh has been rated as the nation’s “most livable” city by Places Rated Almanac, Forbes and The Economist.

The University:

The University of Pittsburgh is and urban campus located in the Oakland District of the city of Pittsburgh. It is in the top cluster of U.S. public research universities and ranks 5th among all research universities in competitive grants awarded to its faculty by the National Institutes of Health. The University has a large and growing number of world-class science programs covering a broad spectrum of disciplines including: molecular biology, cellular biology, developmental biology, structural biology, drug discovery and design, immunology, neuroscience, organ and tissue engineering, regenerative medicine, cancer diagnostics and treatment, cardiology, gene therapy, bioinformatics and computational biology, nanoscience, and medical device development. The University also has numerous research centers that support cell and molecular biology research at the University. Use the "Links" tab above to learn more about these centers.

The Apodaca Laboratory:

The Apodaca laboratory is housed in the University of Pittsburgh School of Medicine, Department of Medicine, Renal-Electrolyte Division. The laboratory is located in rooms 982 and 984 of Scaife Hall on the main campus of the University (click here to see our lab location and to get a map of the campus). We are one of 11 basic-science laboratories in our Division and also maintain close ties with laboratories in the Department of Cell Biology & Physiology and the Departments of Biological Sciences at the University of Pittsburgh and the Carnegie Mellon University. The Division is home to the NIH-sponsored George M. O'Brien Pittsburgh Center for Kidney Research, one of nine such centers in the nation. Dr. Apodaca is director of the center's Urinary Tract Epithelial Imaging Core.

Contact

Professor Gerard Apodaca, Ph.D.

Appointments: Departments of Medicine and Cell Biology

Director: Pittsburgh Center for Kidney Research Kidney Imaging Core

Contact Information:
University of Pittsburgh
Renal/Electrolyte Division
980 Scaife Hall
3550 Terrace Street
Pittsburgh, PA 15261

Telephone: 412-383-8893
E-mail: gla6@pitt.edu

© 2022 Apodaca Lab - website design by Dennis Clayton

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