SNARE expression and localization in renal epithelial cells suggest mechanism for variability of trafficking phenotypes

American Journal of Physiology - Renal Physiology

Volumn 283, Issue 5 52-5, 2002, Pages

  Li, Xin ^a   Low, Seng Hui ^a   Miura, Masumi ^a   Weimbs, Thomas ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Cell polarity; Endobrevin; Membrane fusion; Membrane traffic; Syntaxin

Indexed keywords

SNARE PROTEIN; SYNTAXIN; SYNTAXIN 2; SYNTAXIN 3; SYNTAXIN 4; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; BASOLATERAL MEMBRANE; CELL POLARITY; CELL TYPE; KIDNEY EPITHELIUM; KIDNEY TUBULE; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

EID: 0036838541     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00185.2002     Document Type: Article

References (66)

1. Al-Awqati Q, Vijayakumar S, Hikita C, Chen J, and Takito J. Phenotypic plasticity in the intercalated cell: The hensin pathway. Am J Physiol Renal Physiol 275: F183-F190, 1998.
2. +-ATPase. Proc Natl Acad Sci USA 86: 5429-5433, 1989.
3. Antonin W, Holroyd C, Tikkanen R, Honing S, and Jahn R. The R-SNARE endobrevin/VAMP-8 mediates homotypic fusion of early endosomes and late endosomes. Mol Biol Cell 11: 3289-3298, 2000.
4. Bonilha VL, Marmorstein AD, Cohen-Gould L, and Rodriguez-Boulan E. Apical sorting of influenza hemagglutinin by transcytosis in retinal pigment epithelium. J Cell Sci 110: 1717-1727, 1997.
5. Breton S, Inoue T, Knepper MA, and Brown D. Antigen retrieval reveals widespread basolateral expression of syntaxin 3 in renal epithelia. Am J Physiol Renal Physiol 282: F523-F529, 2002.
6. Breuza L, Fransen J, and Le Bivic A. Transport and function of syntaxin 3 in human epithelial intestinal cells. Am J Physiol Cell Physiol 279: C1239-C1248, 2000.
7. Brown D. Targeting of membrane transporters in renal epithelia: When cell biology meets physiology. Am J Physiol Renal Physiol 278: F192-F201, 2000.
8. +-ATPase in opposite plasma membrane domains in kidney epithelial cell subpopulations. Nature 331: 622-624, 1988.
9. Brown D and Stow JL. Protein trafficking and polarity in kidney epithelium: From cell biology to physiology. Physiol Rev 76: 245-297, 1996.
10. Chen YA and Scheller RH. SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol 2: 98-106, 2001.
11. Christensen EI, Nielsen S, Moestrup SK, Borre C, Maunsbach AB, de Heer E, Ronco P, Hammond TG, and Verroust P. Segmental distribution of the endocytosis receptor gp330 in renal proximal tubules. Eur J Cell Biol 66: 349-364, 1995.
12. Delgrossi MH, Breuza L, Mirre C, Chavrier P, and Le Bivic A. Human syntaxin 3 is localized apically in human intestinal cells. J Cell Sci 110: 2207-2214, 1997.
13. Flaumenhaft R, Croce K, Chen E, Furie B, and Furie BC. Proteins of the exocytotic core complex mediate platelet alpha-granule secretion. Roles of vesicle-associated membrane protein, SNAP-23, and syntaxin 4. J Biol Chem 274: 2492-2501, 1999.
14. Fujimoto T and Ogawa K. Immunoelectron microscopy of fodrin in the rat uriniferous and collecting tubular epithelium. J Histochem Cytochem 37: 1345-1352, 1989.
15. Fujita H, Tuma PL, Finnegan CM, Locco L, and Hubbard AL. Endogenous syntaxins 2, 3 and 4 exhibit distinct but overlapping patterns of expression at the hepatocyte plasma membrane. Biochem J 329: 527-538, 1998.
16. Gaisano HY, Ghai M, Malkus PN, Sheu L, Bouquillon A, Bennett MK, and Trimble WS. Distinct cellular locations and protein-protein interactions of the syntaxin family of proteins in rat pancreatic acinar cells. Mol Biol Cell 7: 2019-2027, 1996.
17. Galli T, Zahraoui A, Vaidyanathan VV, Raposo G, Tian JM, Karin M, Niemann H, and Louvard D. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell 9: 1437-1448, 1998.
18. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, Scheller RH, and 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.
19. Hansen NJ, Antonin W, and Edwardson JM. Identification of SNAREs involved in regulated exocytosis in the pancreatic acinar cell. J Biol Chem 274: 22871-22876, 1999.
20. Hirai Y, Lochter A, Galosy S, Koshida S, Niwa S, and Bissell MJ. Epimorphin functions as a key morphoregulator for mammary epithelial cells. J Cell Biol 140: 159-169, 1998.
21. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, and Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 123: 35-45, 1993.
22. Ibaraki K, Horikawa HP, Morita T, Mori H, Sakimura K, Mishina M, Saisu H, and Abe T. Identification of four different forms of syntaxin 3. Biochem Biophys Res Commun 211: 997-1005, 1995.
23. Ihrke G and Hubbard AL. Control of vesicle traffic in hepatocytes. Prog Liver Dis 13: 63-99, 1995.
24. Jahn R and Sudhof TC. Membrane fusion and exocytosis. Annu Rev Biochem 68: 863-911, 1999.
25. Katafuchi K, Mori T, Toshimori K, and Iida H. Localization of a syntaxin isoform, syntaxin 2, to the acrosomal region of rodent spermatozoa. Mol Reprod Dev 57: 375-383, 2000.
26. Lafont F, Verkade P, Galli T, Wimmer C, Louvard D, and Simons K. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc Natl Acad Sci USA 96: 3734-3738, 1999.
27. Lapierre LA, Tuma PL, Navarre J, Goldenring JR, and Anderson JM. VAP-33 localizes to both an intracellular vesicle population and with occludin at the tight junction. J Cell Sci 112: 3723-3732, 1999.
28. Lehtonen S, Riento K, Olkkonen VM, and Lehtonen E. Syntaxin 3 and Munc-18-2 in epithelial cells during kidney development. Kidney Int 56: 815-826, 1999.
29. Lencer WI, Weyer P, Verkman AS, Ausiello DA, and Brown D. FITC-dextran as a probe for endosome function and localization in kidney. Am J Physiol Cell Physiol 258: C309-C317, 1990.
30. Low SH, Chapin SJ, Weimbs T, Kömüves LG, Bennett MK, and Mostov KE. Differential localization of syntaxin isoforms in polarized MDCK cells. Mol Biol Cell 7: 2007-2018, 1996.
31. Low SH, Chapin SJ, Wimmer C, Whiteheart SW, Kömüves LK, Mostov KE, and Weimbs T. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J Cell Biol 141: 1503-1513, 1998.
32. Low SH, Miura M, Roche PA, Valdez AC, Mostov KE, and Weimbs T. Intracellular redirection of plasma membrane trafficking after loss of epithelial cell polarity. Mol Biol Cell 11: 3045-3060, 2000.
33. Low SH, Roche PA, Anderson HA, van Ijzendoorn SCD, Zhang M, Mostov KE, and Weimbs T. Targeting of SNAP-23 and SNAP-25 in polarized epithelial cells. J Biol Chem 273: 3422-3430, 1998.
34. Macaulay SL, Hewish DR, Gough KH, Stoichevska V, MacPherson SF, Jagadish M, and Ward CW. Functional studies in 3T3L1 cells support a role for SNARE proteins in insulin stimulation of GLUT4 translocation. Biochem J 324: 217-224, 1997.
35. Mandon B, Chou CL, Nielsen S, and Knepper MA. Syntaxin-4 is localized to the apical plasma membrane of rat renal collecting duct cells: possible role in aquaporin-2 trafficking. J Clin Invest 98: 906-913, 1996.
36. Mandon B, Nielsen S, Kishore BK, and Knepper MA. Expression of syntaxins in rat kidney. Am J Physiol Renal Physiol 273: F718-F730, 1997.
37. Maranda B, Brown D, Bourgoin S, Casanova JE, Vinay P, Ausiello DA, and Marshansky V. Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J Biol Chem 276: 18540-18550, 2001.
38. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, Paumet F, Sollner TH, and Rothman JE. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407: 153-159, 2000.
39. Meier KE and Insel PA. Hormone receptors and response in cultured renal epithelial cell lines. In: Tissue Culture of Epithelial Cells, edited by Taub M. New York: Plenum, 1985, p. 145-178.
40. Min J, Okada S, Kanzaki M, Elmendorf JS, Coker KJ, Ceresa BP, Syu LJ, Noda Y, Saltiel AR, and Pessin JE. Synip: A novel insulin-regulated syntaxin 4-binding protein mediating GLUT4 translocation in adipocytes. Mol Cell 3: 751-760, 1999.
41. Mostov KE, Verges M, and Altschuler Y. Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol 12: 483-490, 2000.
42. Moutairou K, Hayez N, Pohl V, Pattyn G, and Pochet R. Calbindin localization in African giant rat kidney (Cricetomys gambianus). Biochim Biophys Acta 1313: 187-193, 1996.
43. Nagamatsu S, Nakamichi Y, Yamamura C, Matsushima S, Watanabe T, Ozawa S, Furukawa H, and Ishida H. Decreased expression of t-SNARE, syntaxin 1, and SNAP-25 in pancreatic beta-cells is involved in impaired insulin secretion from diabetic GK rat islets: Restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes 48: 2367-2373, 1999.
44. Nelson WJ and Yeaman C. Protein trafficking in the exocytic pathway of polarized epithelial cells. Trends Cell Biol 11: 483-486, 2001.
45. Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, and Harris HW. Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90: 11663-11667, 1993.
46. Nielsen S, Terris J, Smith CP, Hediger MA, Ecelbarger CA, and Knepper MA. Cellular and subcellular localization of the vasopressin-regulated urea transporter in rat kidney. Proc Natl Acad Sci USA 93: 5495-5500, 1996.
47. Obermuller N, Kranzlin B, Blum WF, Gretz N, and Witzgall R. An endocytosis defect as a possible cause of proteinuria in polycystic kidney disease. Am J Physiol Renal Physiol 280: F244-F253, 2001.
48. Olkkonen VM and Ikonen E. Genetic defects of intracellular-membrane transport. N Engl J Med 343: 1095-1104, 2000.
49. Olson AL, Knight JB, and Pessin JE. Syntaxin 4, VAMP2, and/or VAMP3/cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Mol Cell Biol 17: 2425-2435, 1997.
50. Paumet F, Le Mao J, Martin S, Galli T, David B, Blank U, and Roa M. Soluble NSF attachment protein receptors (SNAREs) in RBL-2H3 mast cells: Functional role of syntaxin 4 in exocytosis and identification of a vesicle-associated membrane protein 8-containing secretory compartment. J Immunol 164: 5850-5857, 2000.
51. +-ATPase. J Biol Chem 271: 3324-3327, 1996.
52. Pollack AL, Runyan RB, and Mostov KE. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev Biol 204: 64-79, 1998.
53. Quinones B, Riento K, Olkkonen VM, Hardy S, and Bennett MK. Syntaxin 2 splice variants exhibit differential expression patterns, biochemical properties and subcellular localizations. J Cell Sci 112: 4291-4304, 1999.
54. Riento K, Galli T, Jansson S, Ehnholm C, Lehtonen E, and Olkkonen VM. Interaction of munc-18-2 with syntaxin 3 controls the association of apical SNAREs in epithelial cells. J Cell Sci 111: 2681-2688, 1998.
55. Rodger J, Davis S, Laroche S, Mallet J, and Hicks A. Induction of long-term potentiation in vivo regulates alternate splicing to alter syntaxin 3 isoform expression in rat dentate gyrus. J Neurochem 71: 666-675, 1998.
56. Scales SJ, Chen YA, Yoo BY, Patel SM, Doung YC, and Scheller RH. SNAREs contribute to the specificity of membrane fusion. Neuron 26: 457-464, 2000.
57. Snider MD and Rogers OC. Membrane traffic in animal cells: Cellular glycoproteins return to the site of Golgi mannosidase I. J Cell Biol 103: 265-275, 1986.
58. Steegmaier M, Lee KC, Prekeris R, and Scheller RH. SNARE protein trafficking in polarized MDCK cells. Traffic 1: 553-560, 2000.
59. Steinman RM, Mellman IS, Muller WA, and Cohn ZA. Endocytosis and the recycling of plasma membrane. J Cell Biol 96: 1-27, 1983.
60. Tellam JT, Macaulay SL, McIntosh S, Hewish DR, Ward CW, and James DE. Characterization of Munc-18c and syntaxin-4 in 3T3-L1 adipocytes. Putative role in insulin-dependent movement of GLUT-4. J Biol Chem 272: 6179-6186, 1997.
61. Weber E, Berta G, Tousson A, St. John P, Green MW, Gopalokrishnan U, Jilling T, Sorscher EJ, Elton TS, Abrahamson DR, and Kirk KL. Expression and polarized targeting of a rab3 isoform in epithelial cells. J Cell Biol 125: 583-594, 1994.
62. Weimbs T, Low SH, Chapin SJ, and Mostov KE. Apical targeting in polarized epithelial cells: There's more afloat than rafts. Trends Cell Biol 7: 393-399, 1997.
63. Yang C, Coker KJ, Kim JK, Mora S, Thurmond DC, Davis AC, Yang B, Williamson RA, Shulman GI, and Pessin JE. Syntaxin 4 heterozygous knockout mice develop muscle insulin resistance. J Clin Invest 107: 1311-1318, 2001.
64. Zahraoui A, Joberty G, Arpin M, Fontaine JJ, Hellio R, Tavitian A, and Louvard D. A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J Cell Biol 124: 101-115, 1994.
65. Zolotnitskaya A and Satlin LM. Developmental expression of ROMK in rat kidney. Am J Physiol Renal Physiol 276: F825-F836, 1999.
66. Zurzolo C, Le Bivic A, Quaroni A, Nitsch L, and Rodriguez-Boulan E. Modulation of transcytotic and direct targeting pathways in a polarized thyroid cell line. Embo J 11: 2337-2344, 1992.