Neurexin-1, a presynaptic adhesion molecule, localizes at the slit diaphragm of the glomerular podocytes in kidneys

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 2, 2011, Pages

  Saito, Akira ^a,b   Miyauchi, Naoko ^a   Hashimoto, Taeko ^a   Karasawa, Tamaki ^a   Han, Gi Dong ^a,c   Kayaba, Mutsumi ^a   Sumi, Tomoyuki ^a   Tomita, Masayuki ^a   Ikezumi, Yohei ^a   Suzuki, Kenji ^a   Koitabashi, Yasushi ^b   Shimizu, Fujio ^d   Kawachi, Hiroshi ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Yeungnam University   (South Korea)

^d NIIGATA SEIRYO UNIVERSITY   (Japan)

Author keywords

Nephrin; Nephrotic syndrome; Proteinuria

Indexed keywords

CD2 ASSOCIATED PROTEIN; MESSENGER RNA; NEPHRIN; NEUREXIN; NEUREXIN 1ALPHA; NEUREXIN 1BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CELL LYSATE; CYTOPLASM; DISEASE SEVERITY; FEMALE; GLOMERULUS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KIDNEY; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEINURIA; RAT; STAINING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMAL STRUCTURES; ANIMALS; CEREBRUM; CYTOSKELETAL PROTEINS; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION; GLYCOPROTEINS; GUANYLATE KINASE; KIDNEY GLOMERULUS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NEPHROTIC SYNDROME; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PODOCYTES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEINURIA; RATS; RATS, WISTAR; RECEPTORS, CELL SURFACE; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 79551533801     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00640.2009     Document Type: Article

References (49)

1. Asanuma K, Mundel P. The role of podocytes in glomerular pathobiology. Clin Exp Nephrol 7: 255-259, 2003.
2. Biederer T, Sudhof TC. Mints as adaptors: direct binding to neurexins and recruitment of Munc18. J Biol Chem 275: 39803-39806, 2000.
3. Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α- and β-neurexins. Neuron 48: 229-236, 2005.
4. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C. NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354, 2000.
5. Dean C, Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 1-9, 2006.
6. Donoviel DB, Freed DD, Vogel H, Potter DG, Hawkins E, Barrish JP, Mathur BN, Turner CA, Geske R, Montgomery CA, Starbuck M, Brandt M, Gupta A, Ramirez-Solis R, Zambrowicz BP, Powell DR. Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol 21: 4829-4836, 2001.
7. Fukasawa H, Bornheimer S, Kudlicka K, Farquhar MG. Slit diaphragms contain tight junction proteins. J Am Soc Nephrol 20: 1491-1503, 2009.
8. Giardino L, Armelloni S, Corbelli A, Mattinzoli D, Zennaro C, Guerrot D, Tourrel F, Ikehata M, Li M, Berra S, Carraro M, Messa P, Rastaldi MP. Podocyte glutamatergic signaling contributes to the function of the glomerular filtration barrier. J Am Soc Nephrol 20: 1929-1940, 2009.
9. Han GD, Suzuki K, Koike H, Suzuki K, Yoneyama H, Narumi S, Shimizu F, Kawachi H. IFN-inducible protein-10 plays a pivotal role in maintaining slit-diaphragm function by regulating podocyte cell-cycle balance. J Am Soc Nephrol 17: 442-453, 2006.
10. Hashimoto T, Karasawa T, Saito A, Miyauchi N, Han GD, Hayasaka K, Shimizu F, Kawachi H. Ephrin-B1 localizes at the slit diaphragm of the glomerular podocyte. Kidney Int 72: 954-964, 2007.
11. Hata Y, Davletov B, Petrenko AG, Jahn R, Sudhof TC. Interaction of synaptotagmin with the cytoplasmic domains of neurexins. Neuron 10: 307-315, 1993.
12. Hata Y, Butz S, Sudhof TC. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16: 2488-2494, 1996.
13. Hirabayashi S, Mori H, Kansaku A, Kurihara H, Sakai T, Shimizu F, Kawachi H, Hata Y. MAGI-1 is a component of the glomerular slit diaphragm that is tightly associated with nephrin. Lab Invest 85: 1528-1543, 2005.
14. + cells in the prolonged mesangial proliferative glomerulonephritis. Kidney Int 61: 2044-2057, 2002.
15. Kawachi H, Orikasa M, Matsui K, Iwanaga T, Toyabe S, Oite T, Shimizu F. Epitope-specific induction of mesangial lesions with proteinuria by a MoAb against mesangial cell surface antigen. Clin Exp Immunol 88: 399-404, 1992.
16. Kawachi H, Shimizu F. Molecular composition and function of the slit diaphragm: nephrin, the molecule responsible for proteinuria. Clin Exp Nephrol 4: 161-172, 2000.
17. Kawachi H, Koike H, Kurihara H, Yaoita E, Orikasa M, Shia MA, Sakai T, Yamamoto T, Salant DJ, Shimizu F. Cloning of rat nephrin: expression in developing glomeruli and in proteinuric states. Kidney Int 57: 1949-1961, 2000.
18. Kawachi H, Koike H, Kurihara H, Sakai T, Shimizu F. Cloning of rat homologue of podocin: expression in proteinuric states and in developing glomeruli. J Am Soc Nephrol 13: 46-56, 2003.
19. Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K. Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1: 575-582, 1998.
20. Kobayashi N, Mundel P. A role of microtubules during the formation of cell processes in neuronal and non-neuronal cells. Cell Tissue Res 291: 163-174, 1998.
21. Krakower CA, Greenspon SA. Localization of the nephrotoxic antigen within the isolated renal glomerulus. AMA Arch Pathol 51:629-639, 1951.
22. Kriz W, Kobayashi N, Elger M. New aspects of podocyte structure, function, and pathology. Clin Exp Nephrol 2: 85-99, 1998.
23. Lehtonen S, Lehtonen E, Kudlicka K, Holthofer H, Farquhar MG. Nephrin forms a complex with adherens junction proteins and CASK in podocytes and in Madin-Darby canine kidney cells expressing nephrin. Am J Pathol 165: 923-936, 2004.
24. Luimula P, Sandstrom N, Novikov D, Holthofer H. Podocyte-associated molecules in puromycin aminonucleoside nephrosis of the rat. Lab Invest 82: 713-718, 2002.
25. Missler M, Fernandez-Chacon R, Sudhof TC. The making of neurexins. J Neurochem 71: 1339-1347, 1998.
26. Missler M, Sudhof TC. Neurexins: three genes and 1001 products. Trends Genet 14: 20-26, 1998.
27. Miyauchi N, Saito A, Karasawa T, Harita Y, Suzuki K, Koike H, Han GD, Shimizu F, Kawachi H. Synaptic vesicle protein 2B (SV2B) is expressed in podocyte, and its expression is altered in proteinuric glomeruli. J Am Soc Nephrol 17: 2748-2759, 2006.
28. Mundel P, Reiser J, Zuniga Mejia Borja A, Pavenstadt H, Davidson GR, Kriz W, Zeller R. Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res 236: 248-258, 1997.
29. Mundel P, Shankland SJ. Podocyte biology and response to injury. J Am Soc Nephrol 13: 3005-3015, 2002.
30. Nakatsue T, Koike H, Han GD, Suzuki K, Miyauchi N, Yuan H, Salant DJ, Gejyo F, Shimizu F, Kawachi H. Nephrin and podocin dissociate at the onset of proteinuria in experimental membranous nephropathy. Kidney Int 67: 2239-2253, 2005.
31. Orikasa M, Matsui K, Oite T, Shimizu F. Massive proteinuria induced in rats by a single intravenous injection of a monoclonal antibody. J Immunol 141: 807-814, 1988.
32. Otaki Y, Miyauchi N, Higa M, Takada A, Kuroda T, Gejyo F, Shimizu F, Kawachi H. Dissociation of neph1 from nephrin is involved in development of a rat model of focal segmental glomerulosclerosis. Am J Physiol Renal Physiol 295: F1376-F1387, 2008.
33. Pavenstadt H, Kriz W, Kretzler M. Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2002.
34. Perin MS. The COOH terminus of synaptotagmin mediates interaction with the neurexins. J Biol Chem 269: 8576-8581, 1994.
35. Rastaldi MP, Armelloni S, Berra S, Li M, Pesaresi M, Poczewski H, Langer B, Kerjaschki D, Henger A, Blattner SM, Kretzler M, Wanke R, D'Amico G. Glomerular podocytes possess the synaptic vesicle molecule Rab3A and its specific effector Rabphilin-3a. Am J Pathol 163: 889-899, 2003.
36. Reiser J, Kriz W, Kretzler M, Mundel P. The glomerular slit diaphragm is a modified adherens junction. J Am Soc Nephrol 11: 1-8, 2000.
37. Reiser J, Polu KR, Möller CC, Kenlan P, Altintas MM, Wei C, Faul C, Herbert S, Villegas I, Avila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR. TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37: 739-744, 2005.
38. Rodewald R, Karnovsky MJ. Porous substructure of the glomerular slit diaphragm in the rat and mouse. J Cell Biol 60: 423-433, 1974.
39. Rowen L, Young J, Birditt B, Kaur A, Madan A, Philipps DL, Qin S, Minx P, Wilson RK, Hood L, Graveley BR. Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity. Genomics 79: 587-597, 2002.
40. Ruotsalainen V, Ljungberg P, Wartiovaara J, Lenkkeri U, Kestila M, Jalanko H, Holmberg C, Tryggvason K. Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci USA 96: 7962-7967, 1999.
41. Schwarz K, Simons M, Reiser J, Saleem MA, Faul C, Kriz W, Shaw AS, Holzman LB, Mundel P. Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin. J Clin Invest 108: 1621-1629, 2001.
42. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O, Miner JH, Shaw AS. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286: 312-315, 1999.
43. Tabuchi K, Sudhof TC. Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 79: 849-859, 2002.
44. Topham PS, Kawachi H, Haydar SA, Chugh S, Addona TA, Charron KB, Holzman LB, Shia M, Shimizu F, Salant DJ. Nephritogenic mAb 5-1-6 is directed at the extracellular domain of rat nephrin. J Clin Invest 104: 1559-1566, 1999.
45. Ullrich B, Ushkaryov YA, Sudhof TC. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 14: 497-507, 1995.
46. Ushkaryov YA, Petrenko AG, Geppert M, Sudhof TC. Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin. Science 257: 50-56, 1992.
47. Ushkaryov YA, Hata Y, Ichtchenko K, Moomaw C, Afendis S, Slaughter CA, Sudhof TC. Conserved domain structure of β-neurexins. J Biol Chem 269: 11987-11992, 1994.
48. Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howell DN, Vance JM, Rosenberg PB. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308: 1801-1804, 2005.
49. Zhang Y, Luan Z, Liu A, Hu G. The scaffolding protein CASK mediates the interaction between rabphilin3a and β-neurexins. FEBS Lett 497: 99-102, 2001.