c-mip impairs podocyte proximal signaling and induces heavy proteinuria

Science Signaling

Volumn 3, Issue 122, 2010, Pages

  Zhang, Shao Yu ^a,b   Kamal, Maud ^a,b   Dahan, Karine ^a,b   Pawlak, André ^a,b   Ory, Virginie ^a,b   Desvaux, Dominique ^a,b   Audard, Vincent ^a,b   Candelier, Marina ^a,b   BenMohamed, Fatima ^a,b   Matignon, Marie ^a,b   Christov, Christo ^a,c   Decrouy, Xavier ^a   Bernard, Veronique ^a   Mangiapan, Gilles ^d   Lang, Philippe ^a,b,c   Guellaën, Georges ^a,b   Ronco, Pierre ^e,f,g   Sahali, Djillali ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d CENTRE HOSPITALIER INTERCOMMUNAL DE CRÉTEIL   (France)

^e Hopital   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g HÔPITAL TENON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; C MAF INDUCING PROTEIN; NCK PROTEIN; NEPHRIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN KINASE FYN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEINURIA;

ANIMALS; CARRIER PROTEINS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PODOCYTES; PROTEIN BINDING; PROTEINURIA; PROTO-ONCOGENE PROTEINS C-FYN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

MUS;

EID: 77953835378     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000678     Document Type: Article

References (44)

1. LA. Stevens, A. S. Levey, Measured GFR as a confirmatory test for estimated GFR. J. Am. Soc. Nephrol. 20, 2305-2313 (2009).
2. K. Tryggvason, J. Patrakka, J. Wartiovaara, Hereditary proteinuria syndromes and mechanisms of proteinuria. N. Engl. J. Med. 354, 1387-1401 (2006).
3. D. Kerjaschki, Caught flat-footed: Podocyte damage and the molecular bases of focal glomerulosclerosis. J. Clin. Invest. 108, 1583-1587 (2001).
4. T. Benzing, Signaling at the slit diaphragm. J. Am. Soc. Nephrol. 15, 1382-1391 (2004).
5. M. Kestilä, U. Lenkkeri, M. Mannikkö, J. Lamerdin, P. McCready, H. Putaala, V. Ruotsalainen, T. Morita, M. Nissinen, R. Herva, C. E. Kashtan, L Peltonen, C. Holmberg, A. Olsen, K. Tryggvason, Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol. Cell 1, 575-582 (1998).
6. N. Boute, O. Gribouval, S. Roselli, F. Benessy, H. Lee, A. Fuchshuber, K. Dahan, M. C. Gubler, P. Niaudet, C. Antignac, NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet. 24, 349-354 (2000).
7. J. M. Kim, H. Wu, G. Green, C. A. Winkler, J. B. Kopp, J. H. Miner, E. R. Unanue, A. S. Shaw, CD2-associated protein haploin sufficiency is linked to glomerular disease susceptibility. Science 300, 1298-1300 (2003).
8. J. M. Kaplan, S. H. Kim, K. N. North, H. Rennke, L. A. Correia, H. Q. Tong, B. J. Mathis, J. C. Rodriguez-Perez, P. G. Allen, A. H. Beggs, M. R. Pollak, Mutations in ACTN4, encoding α-actinin-4, cause familial focal segmental glomerulosclerosis. Nat. Genet. 24, 251-256 (2000).
9. J. Reiser, K. R. Polu, C. C. Moller, P. Kenlan, M. M. Altintas, C. Wei, C. Faul, S. Herbert, I. Villegas, C. Avila-Casado, M. McGee, H. Sugimoto, D. Brown, R. Kalluri, P. Mundel, P. L. Smith, D. E. Clapham, M. R. Pollak, TRPC6 is a glomerular slit diaphragm associated channel required for normal renal function. Nat. Genet. 37, 739-744 (2005).
10. B. Hinkes, R. C. Wiggins, R. Gbadegesin, C. N. Vlangos, D. Seelow, G. Nürnberg, P. Garg, R. Verma, H. Chaib, B. E. Hoskins, S. Ashraf, C. Becker, H. C. Hennies, M. Goyal, B. L. Wharram, A. D. Schachter, S. Mudumana, I. Drummond, D. Kerjaschki, R. Waldherr, A. Dietrich, F. Ozaltin, A. Bakkaloglu, R. Cleper, L. Basel-Vanagaite, M. Pohl, M. Griebel, A. N. Tsygin, A. Soylu, D. Muller, C. S. Sorli, T. D. Bunney, M. Katan, J. Liu, M. Attanasio, J. F. Otoole, K. Hasselbacher, B. Mucha, E. A. Otto, R. Airik, A. Kispert, G. G. Kelley, A. V. Smrcka, T. Gudermann, L. B. Holzman, P. Nürnberg, F. Hildebrandt, Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible. Nat. Genet. 38, 1397-1405 (2006).
11. M. Simons, K. Schwarz, W. Kriz, A. Miettinen, J. Reiser, P. Mundel, H. Holthöfer, Involvement of lipid rafts in nephrin phosphorylation and organization of the glomerular slit diaphragm. Am. J. Pathol. 159, 1069-1077 (2001).
12. R. Verma, I. Kovari, A. Soofi, D. Nihalani, K. Patrie, L. B. Holzman, Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J. Clin. Invest. 116, 1346-1359 (2006).
13. N. Jones, I. M. Blasutig, V. Eremina, J. M. Ruston, F. Bladt, H. Li, H. Huang, L. Larose, S. S. Li, T. Takano, S. E. Quaggin, T. Pawson, Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440, 818-823 (2006).
14. T. B. Huber, B. Hartleben, J. Kim, M. Schmidts, B. Schermer, A. Keil, L. Egger, R. L. Lecha, C. Borner, H. Pavenstädt, A. S. Shaw, G. Walz, T. Benzing, Nephrin and CD2AP associate with phosphoinositide 3-OH kinase and stimulate AKT-dependent signaling. Mol. Cell. Biol. 23, 4917-4928 (2003).
15. H. N. Higgs, T. D. Pollard, Regulation of actin filament network formation through ARP2/3 complex: Activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649-676 (2001).
16. S. Banin, O. Truong, D. R. Katz, M. D. Waterfield, P. M. Brickell, I. Gout, Wiskott-Aldrich syndrome protein (WASp) is a binding partner for c-Src family protein-tyrosine kinases. Curr. Biol. 6, 981-988 (1996).
17. T. B. Huber, C. Kwoh, H. Wu, K. Asanuma, M. Gödel, B. Hartleben, K. J. Blumer, J. H. Miner, P. Mundel, A. S. Shaw, Bigenic mouse models of focal segmental glomerulosclerosis involving pairwise interaction of CD2AP, Fyn, and synaptopodin. J. Clin. Invest. 116, 1337-1345 (2006).
18. D. Sahali, A. Pawlak, A. Valanciuté, P. Grimbert, P. Lang, P. Remy, A. Bensman, G. Guellaën, A novel approach to investigation of the pathogenesis of active minimalchange nephrotic syndrome using subtracted cDNA library screening. J. Am. Soc. Nephrol. 13, 1238-1247 (2002).
19. A. A. Eddy, J. M. Symons, Nephrotic syndrome in childhood. Lancet 362, 629-639 (2003).
20. C. Kitiyakara, J. B. Kopp, P. Eggers, Trends in the epidemiology of focal segmental glomerulosclerosis. Semin. Nephrol. 23, 172-182 (2003).
21. A. Meyrier, Nephrotic focal segmental glomerulosclerosis in 2004: An update. Nephrol. Dial. Transplant. 19, 2437-2444 (2004).
22. V. D. D'Agati, A. B. Fogo, J. A. Bruijn, J. C. Jennette, Pathologic classification of focal segmental glomerulosclerosis: A working proposal. Am. J. Kidney Dis. 43, 368-382 (2004).
23. P. W. Mathieson, Minimal change nephropathy and focal segmental glomerulosclerosis. Semin. Immunopathol. 29, 415-426 (2007).
24. P. Ronco, H. Debiec, Molecular pathomechanisms of membranous nephropathy: From Heymann nephritis to alloimmunization. J. Am. Soc. Nephrol. 16, 1205-1213 (2005).
25. J. P. DiNitto, D. G. Lambright, Membrane and juxtamembrane targeting by PH and PTB domains. Biochim. Biophys. Acta 1761, 850-867 (2006).
26. D. Filipp, J. Zhang, B. L. Leung, A. Shaw, S. D. Levin, A. Veillette, M. Julius, Regulation of Fyn through translocation of activated Lck into lipid rafts. J. Exp. Med. 197, 1221-1227 (2003).
27. 2 of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J. Cell Biol. 150, 1311-1320 (2000).
28. D. Kerjaschki, T. J. Neale, Molecular mechanisms of glomerular injury in rat experimental membranous nephropathy (Heymann nephritis). J. Am. Soc. Nephrol. 7, 2518-2526 (1996).
29. L. H. Noel, M. Zanetti, D. Droz, C. Barbanel, Long-term prognosis of idiopathic membranous glomerulonephritis. Study of 116 untreated patients. Am. J. Med. 66, 82-90 (1979).
30. P. L. Leenaerts, B. M. Hall, B. J. Van Damme, M. R. Daha, Y. F. Vanrenterghem, Active Heymann nephritis in complement component C6 deficient rats. Kidney Int. 47, 1604-1614 (1995).
31. S. T. Spicer, G. T. Tran, M. C. Killingsworth, N. Carter, D. A. Power, K. Paizis, R. Boyd, S. J. Hodgkinson, B. M. Hall, Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J. Immunol. 179, 172-178 (2007).
32. S. P. Makker, J. J. Kanalas, Course of transplanted Heymann nephritis kidney in normal host. Implications for mechanism of proteinuria in membranous glomerulonephropathy. J. Immunol. 142, 3406-3410 (1989).
33. S. Doublier, V. Ruotsalainen, G. Salvidio, E. Lupia, L. Biancone, P. G. Conaldi, P. Reponen, K. Tryggvason, G. Camussi, Nephrin redistribution on podocytes is a potential mechanism for proteinuria in patients with primary acquired nephrotic syndrome. Am. J. Pathol. 158, 1723-1731 (2001).
34. N. Y. Shih, J. Li, V. Karpitskii, A. Nguyen, M. L. Dustin, O. Kanagawa, J. H. Miner, A. S. Shaw, Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286, 312-315 (1999).
35. C. C. Yu, T. S. Yen, C. A. Lowell, A. L. DeFranco, Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases Lyn and Fyn. Curr. Biol. 11, 34-38 (2001).
36. I. Quack, L. C. Rump, P. Gerke, I. Walther, T. Vinke, O. Vonend, T. Grunwald, L. Sellin, β-Arrestin2 mediates nephrin endocytosis and impairs slit diaphragm integrity. Proc. Natl. Acad. Sci. U. S. A. 03, 4110-14115 (2006).
37. N. Jones, L. A. New, M. A. Fortino, V. Eremina, J. Ruston, I. M. Blasutig, L. Aoudjit, Y. Zou, X. Liu, G. L. Yu, T. Takano, S. E. Quaggin, T. Pawson, Nck proteins maintain the adult glomerular filtration barrier. J. Am. Soc. Nephrol. 20, 1533-1543 (2009).
38. J. Reiser, G. von Gersdorff, M. Loos, J. Oh, K. Asanuma, L. Giardino, M. P. Rastaldi, N. Calvaresi, H. Watanabe, K. Schwarz, C. Faul, M. Kretzler, A. Davidson, H. Sugimoto, R. Kalluri, A. H. Sharpe, J. A. Kreidberg, P. Mundel, Induction of B7-1 in podocytes is associated with nephrotic syndrome. J. Clin. Invest. 113, 1390-1397 (2004).
39. Y. Sun, L. He, M. Takemoto, J. Patrakka, T. Pikkarainen, G. Genové, J. Norlin, K. Truvé, K. Tryggvason, C. Betsholtz, Glomerular transcriptome changes associated with lipopolysaccharide-induced proteinuria. Am. J. Nephrol. 29, 558-570 (2009).
40. S. Y. Zhang, A. Marlier, O. Gribouval, T. Gilbert, L. Heidet, C. Antignac, M. C. Gubler, In vivo expression of podocyte slit diaphragm-associated proteins in nephrotic patients with NPHS2 mutation. Kidney Int. 66, 945-954 (2004).
41. P. Mundel, J. Reiser, A. Zúñiga Mejía Borja, H. Pavenstädt, G. R. Davidson, W. Kriz, R. Zeller, 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).
42. S. K. Bronson, E. G. Plaehn, K. D. Kluckman, J. R. Hagaman, N. Maeda, O. Smithies, Single-copy transgenic mice with chosen-site integration. Proc. Natl. Acad. Sci. U. S. A. 93, 9067-9072 (1996).
43. J. L. Michaud, L. I. Lemieux, M. Dube, B. C. Vanderhyden, S. J. Robertson, C. R. Kennedy, Focal and segmental glomerulosclerosis in mice with podocyte-specific expression of mutant α-actinin-4. J. Am. Soc. Nephrol. 14, 1200-1211 (2003).
44. Acknowledgments: We thank C. R. J. Kennedy (Ottawa Health Research Institute, Ontario, Canada) for providing the nephrin promoter; M. D. Resh (Department of Cell Biology and Genetics, Memorial Sloan-Kettering Cancer Center, New York, NY), and J. Huot (Centre de recherche de L'Hötel-Dieu de Québec, Canada) for providing the Fyn plasmids; P. Mundel (Mount Sinai School of Medicine, New York, NY) for providing the podocyte cell line; T. Benzing (Renal Division, University Hospital Freiburg, Freiburg, Germany) for providing the nephrin plasmid; C. Antignac (INSERM U574, Höpital Necker Enfant-Malades, Paris, France) for providing the antibody against podocin; L. Holzman (Medical Science Research, Ann Arbor, MI) for providing the antibody against phosphorylated nephrin; X. de Mollerat (Invitrogen) for technical assistance with RNAi experiments and for providing the cyclophilin-targeting siRNA; Liliane (Biochemistry Department, Henri Mondor Hospital) for biochemical determinations; L. Kheuang, V. Fataccioli, and A. Manceau (Pathology Department) for technical assistance with electron microscopy; Y. Allory (Pathology Department) for providing renal samples; and R. Souktani (the animal facility laboratory at the Institut Mondor de Recherche Biomédicale, Créteil) for assistance with microinjection experiments in mice. Funding: This work was supported in part by an Avenir Program from INSERM, a grant from the French Kidney Foundation, Association pour l'Utilisation du Rein Artificiel (AURA), and Assistance Publique des Höpitaux de Paris (AP-HP, Programme hospitalier de recherche clinique). Author contributions: S.-Y. Z., M. K., K. D., A. P., V. O., V. A., M. C., F. B. M., M. M., C. C., X. D., and V. B. performed the experiments. G. M. collected clinical data. P. L., G. G., P. R., and D. S. wrote the paper. D. S. supervised the project. All authors discussed the results and participated in writing the paper. Competing interests: The authors declare that they do not have any competing financial, personal, or professional interests.