Exocyst Sec10 protects epithelial barrier integrity and enhances recovery following oxidative stress, by activation of the MAPK pathway

American Journal of Physiology - Renal Physiology

Volumn 298, Issue 3, 2010, Pages

  Park, Kwon Moo ^a,c   Fogelgren, Ben ^a   Zuo, Xiaofeng ^a   Kim, Jinu ^c   Chung, Daniel C ^b   Lipschutz, Joshua H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Kyungpook National University School of Medicine   (South Korea)

Author keywords

Exoc5; Ischemia; Reperfusion

Indexed keywords

EXOCYST; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SEC10; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; KIDNEY EPITHELIUM; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; SECRETORY VESICLE;

EID: 77649129103     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00596.2009     Document Type: Article

References (41)

1. Anderson NJ, Yeaman C. Sec3-containing Exocyst complex is required for desmosome assembly in mammalian epithelial cells. Mol Cell Biol 21: 152-164, 2010.
2. Bonventre JV. Mechanisms of ischemic acute renal failure. Kidney Int 43: 1160-1178, 1993.
3. Charron AJ, Nakamura S, Bacallao R, Wandinger-Ness A. Compromised cytoarchitecture and polarized trafficking in autosomal dominant polycystic kidney disease cells. J Cell Biol 149: 111-124, 2000.
4. Chertow GM, Levy EM, Hammermeister KE, Grover F, Daley J. Independent association between acute renal failure and mortality following cardiac surgery. Am J Med 104: 343-348, 1998.
5. di Mari JF, Davis R, Safirstein RL. MAPK activation determines renal epithelial cell survival during oxidative injury. Am J Physiol Renal Physiol 277: F195-F203, 1999.
6. Dobashi K, Ghosh B, Orak JK, Singh I, Singh AK. Kidney ischemiareperfusion: modulation of antioxidant defenses. Mol Cell Biochem 205: 1-11, 2000.
7. Gonzalez JE, Digeronimo RJ, Arthur DE, King JM. Remodeling of the tight junction during recovery from exposure to hydrogen peroxide in kidney epithelial cells. Free Radic Biol Med 47: 1561-1569, 2009.
8. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, Scheller RH, Nelson WJ. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93: 731-740, 1998.
9. Guo W, Roth D, Gatti E, De Camilli P, Novick P. Identification and characterization of homologues of the exocyst component Sec10p. FEBS Lett 404: 135-139, 1997.
10. Guo W, Roth D, Walch-Solimena C, Novick P. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18: 1071-1080, 1999.
11. Hellman NE, Greco AJ, Rogers KK, Kanchagar C, Balkovetz DF, Lipschutz JH. Activated extracellular signal-regulated kinases are necessary and sufficient to initiate tubulogenesis in renal tubular MDCK strain I cell cysts. Am J Physiol Renal Physiol 289: F777-F785, 2005.
12. Hellman NE, Spector J, Robinson J, Zuo X, Saunier S, Antignac C, Tobias JW, Lipschutz JH. Matrix metalloproteinase 13 (MMP13) and tissue inhibitor of matrix metalloproteinase 1 (TIMP1), regulated by the MAPK pathway, are both necessary for Madin-Darby canine kidney tubulogenesis. J Biol Chem 283: 4272-4282, 2008.
13. Hsu S, Ting AE, Hazuka CD, Davanger S, Kenny JW, Kee Y, Scheller RH. The mammalian brain rsec6/8 complex. Neuron 17: 1209-1219, 1996.
14. Hung CC, Ichimura T, Stevens JL, Bonventre JV. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J Biol Chem 278: 29317-29326, 2003.
15. 2: distinct responses of Caco-2 and Madin-Darby canine kidney (MDCK) strains. Cell Mol Biol 49: 101-112, 2003.
16. Kiely B, Feldman G, Ryan MP. Modulation of renal epithelial barrier function by mitogen-activated protein kinases (MAPKs): mechanism of cyclosporine A-induced increase in transepithelial resistance. Kidney Int 63: 908-916, 2003.
17. Kim J, Park JW, Park KM. Increased superoxide formation induced by irradiation preconditioning triggers kidney resistance to ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 296: F1202-F1211, 2009.
18. Lipschutz JH, Guo W, O'Brien LE, Nguyen YH, Novick P, Mostov KE. Exocyst is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol Biol Cell 11: 4259-4275, 2000.
19. Lipschutz JH, Li S, Arisco A, Balkovetz DF. Extracellular signal-regulated kinases 1/2 control claudin-2 expression in Madin-Darby canine kidney strain I and II cells. J Biol Chem 280: 3780-3788, 2005.
20. Lipschutz JH, Lingappa VR, Mostov KE. The exocyst affects protein synthesis by acting on the translocation machinery of the endoplasmic reticulum. J Biol Chem 278: 20954-20960, 2003.
21. Lipschutz JH, O'Brien LE, Altschuler Y, Avrahami D, Nguyen Y, Tang K, Mostov KE. Analysis of membrane traffic in polarized epithelial cells. Curr Protoc Cell Biol: Chapt. 15: Unit 15, 2001.
22. Liu Z, Greco AJ, Hellman NE, Spector J, Robinson J, Tang OT, Lipschutz JH. Intracellular signaling via ERK/MAPK completes the pathway for tubulogenic fibronectin in MDCK cells. Biochem Biophys Res Comm 353: 793-798, 2007.
23. Liu ZX, Nickel CH, Cantley LG. HGF promotes adhesion of ATP-depleted renal tubular epithelial cells in a MAPK-dependent manner. Am J Physiol Renal Physiol 281: F62-F70, 2001.
24. Meyer TN, Schwesinger C, Ye J, Denker BM, Nigam SK. Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity. J Biol Chem 276: 22048-22055, 2001.
25. +-ATPase that redistributes to apical membrane during ATP depletion remains functional. Am J Physiol Renal Fluid Electrolyte Physiol 265: F693-F697, 1993.
26. Molitoris BA, Falk SA, Dahl RH. Ischemia-induced loss of epithelial polarity. Role of the tight junction. J Clin Invest 84: 1334-1339, 1989.
27. Molitoris BA, Sandoval R, Sutton TA. Endothelial injury and dysfunction in ischemic acute renal failure. Crit Care Med 30: S235-240, 2002.
28. Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. The exocyst is a Ral effector complex. Nat Cell Biol 4: 66-72, 2002.
29. O'Brien LE, Tang K, Kats ES, Schutz-Geschwender A, Lipschutz JH, Mostov KE. ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev Cell 7: 21-32, 2004.
30. Padanilam BJ. Cell death induced by acute renal injury: a perspective on the contributions of apoptosis and necrosis. Am J Physiol Renal Physiol 284: F608-F627, 2003.
31. Park KM, Chen A, Bonventre JV. Prevention of kidney ischemia/ reperfusion-induced functional injury and JNK, p38, and MAPK kinase activation by remote ischemic pretreatment. J Biol Chem 276: 11870-11876, 2001.
32. Park KM, Kim JI, Ahn Y, Bonventre AJ, Bonventre JV. Testosterone is responsible for enhanced susceptibility of males to ischemic renal injury. J Biol Chem 279: 52282-52292, 2004.
33. Prozialeck WC, Edwards JR. Cell adhesion molecules in chemicallyinduced renal injury. Pharmacol Ther 114: 74-93, 2007.
34. Rogers KK, Jou TS, Guo W, Lipschutz JH. The Rho family of small GTPases is involved in epithelial cystogenesis and tubulogenesis. Kidney Int 63: 1632-1644, 2003.
35. Shipitsin M, Feig LA. RalA but not RalB enhances polarized delivery of membrane proteins to the basolateral surface of epithelial cells. Mol Cell Biol 24: 5746-5756, 2004.
36. TerBush DR, Maurice T, Roth D, Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15: 6483-6494, 1996.
37. Thadhani R, Pascual M, Bonventre JV. Acute rénal fêlure. N Engl J Med 334: 1448-1460, 1996.
38. Vega IE, Hsu SC. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J Neurosci 21: 3839-3848, 2001.
39. Waikar SS, Liu KD, Chertow GM. The incidence and prognostic significance of acute kidney injury. Curr Opin Nephrol Hypertens 16: 227-236, 2007.
40. Yeaman C, Grindstaff KK, Nelson WJ. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79: 73-98, 1999.
41. Zuo X, Guo W, Lipschutz JH. The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol Biol Cell 20: 2522-2529, 2009.