Nephrin regulates lamellipodia formation by assembling a protein complex that includes Ship2, Filamin and Lamellipodin

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Venkatareddy, Madhusudan ^a   Cook, Leslie ^a   Abuarquob, Kamal ^a   Verma, Rakesh ^a   Garg, Puneet ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN; LAMELLIPODIN; NCK PROTEIN; NEPHRIN; P21 ACTIVATED KINASE 1; PHOSPHATASE; SCAFFOLD PROTEIN; SH2 CONTAINING INOSITOL 5' PHOSPHATASE; UNCLASSIFIED DRUG; ACTIN; ACTIN BINDING PROTEIN; CARRIER PROTEIN; CONTRACTILE PROTEIN; FILAMINS; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; ONCOPROTEIN; P21 ACTIVATED KINASE; PAK1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4-DIPHOSPHATE; PHOSPHOTYROSINE; POLYPHOSPHOINOSITIDE; PROTAMINE; RAPH1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LAMELLIPODIUM; MOUSE; NONHUMAN; PODOCYTE; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; GENE SILENCING; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN BINDING; PSEUDOPODIUM; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CELL MEMBRANE; CONTRACTILE PROTEINS; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; ONCOGENE PROTEINS; P21-ACTIVATED KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PHOSPHOTYROSINE; PODOCYTES; PROTAMINES; PROTEIN BINDING; PSEUDOPODIA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS;

EID: 83355172822     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028710     Document Type: Article

References (61)

1. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, et al. (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354.
2. Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, et al. (1998) Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1: 575-582.
3. Holzman LB, St John PL, Kovari IA, Verma R, Holthofer H, et al. (1999) Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int 56: 1481-1491.
4. Rantanen M, Palmen T, Patari A, Ahola H, Lehtonen S, et al. (2002) Nephrin TRAP mice lack slit diaphragms and show fibrotic glomeruli and cystic tubular lesions. J Am Soc Nephrol 13: 1586-1594.
5. Hamano Y, Grunkemeyer JA, Sudhakar A, Zeisberg M, Cosgrove D, et al. (2002) Determinants of vascular permeability in the kidney glomerulus. J Biol Chem 277: 31154-31162.
6. Verma R, Wharram B, Kovari I, Kunkel R, Nihalani D, et al. (2003) Fyn binds to and phosphorylates the kidney slit diaphragm component Nephrin. J Biol Chem 278: 20716-20723.
7. Verma R, Kovari I, Soofi A, Nihalani D, Patrie K, et al. (2006) Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J Clin Invest 116: 1346-1359.
8. Jones N, Blasutig IM, Eremina V, Ruston JM, Bladt F, et al. (2006) Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440: 818-823.
9. Harita Y, Kurihara H, Kosako H, Tezuka T, Sekine T, et al. (2008) Neph1, a component of the kidney slit diaphragm, is tyrosine-phosphorylated by the Src family tyrosine kinase and modulates intracellular signaling by binding to Grb2. J Biol Chem 283: 9177-9186.
10. Zhu J, Sun N, Aoudjit L, Li H, Kawachi H, et al. (2008) Nephrin mediates actin reorganization via phosphoinositide 3-kinase in podocytes. Kidney Int 73: 556-566.
11. Harita Y, Kurihara H, Kosako H, Tezuka T, Sekine T, et al. (2009) Phosphorylation of Nephrin Triggers Ca2+ Signaling by Recruitment and Activation of Phospholipase C-{gamma}1. J Biol Chem 284: 8951-8962.
12. Asanuma K, Kim K, Oh J, Giardino L, Chabanis S, et al. (2005) Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner. J Clin Invest 115: 1188-1198.
13. Blasutig IM, New LA, Thanabalasuriar A, Dayarathna TK, Goudreault M, et al. (2008) Phosphorylated YDXV motifs and Nck SH2/SH3 adaptors act cooperatively to induce actin reorganization. Mol Cell Biol 28: 2035-2046.
14. Lehtonen S, Ryan JJ, Kudlicka K, Iino N, Zhou H, et al. (2005) Cell junction-associated proteins IQGAP1, MAGI-2, CASK, spectrins, and alpha-actinin are components of the nephrin multiprotein complex. Proc Natl Acad Sci U S A 102: 9814-9819.
15. Garg P, Verma R, Cook L, Soofi A, Venkatareddy M, et al. Actin-depolymerizing factor cofilin-1 is necessary in maintaining mature podocyte architecture. J Biol Chem 285: 22676-22688.
16. Garg P, Verma R, Nihalani D, Johnstone DB, Holzman LB, (2007) Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization. Mol Cell Biol 27: 8698-8712.
17. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
18. Bamburg JR, Bernstein BW, (2010) Roles of ADF/cofilin in actin polymerization and beyond. F1000 Biol Rep 2: 62.
19. Nakamura F, Stossel TP, Hartwig JH, (2011) The filamins: organizers of cell structure and function. Cell Adh Migr 5: 160-169.
20. Nakamura F, Osborn TM, Hartemink CA, Hartwig JH, Stossel TP, (2007) Structural basis of filamin A functions. J Cell Biol 179: 1011-1025.
21. Critchley DR, (2000) Focal adhesions- the cytoskeletal connection. Curr Opin Cell Biol 12: 133-139.
22. Dyson JM, Kong AM, Wiradjaja F, Astle MV, Gurung R, et al. (2005) The SH2 domain containing inositol polyphosphate 5-phosphatase-2: SHIP2. Int J Biochem Cell Biol 37: 2260-2265.
23. Geier SJ, Algate PA, Carlberg K, Flowers D, Friedman C, et al. (1997) The human SHIP gene is differentially expressed in cell lineages of the bone marrow and blood. Blood 89: 1876-1885.
24. Habib T, Hejna JA, Moses RE, Decker SJ, (1998) Growth factors and insulin stimulate tyrosine phosphorylation of the 51C/SHIP2 protein. J Biol Chem 273: 18605-18609.
25. Sly LM, Rauh MJ, Kalesnikoff J, Buchse T, Krystal G, (2003) SHIP, SHIP2, and PTEN activities are regulated in vivo by modulation of their protein levels: SHIP is up-regulated in macrophages and mast cells by lipopolysaccharide. Exp Hematol 31: 1170-1181.
26. Majerus PW, (1996) Inositols do it all. Genes Dev 10: 1051-1053.
27. Martin TF, (1997) Phosphoinositides as spatial regulators of membrane traffic. Curr Opin Neurobiol 7: 331-338.
28. Dyson JM, O'Malley CJ, Becanovic J, Munday AD, Berndt MC, et al. (2001) The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J Cell Biol 155: 1065-1079.
29. Smith K, Humphreys D, Hume PJ, Koronakis V, (2010) Enteropathogenic Escherichia coli recruits the cellular inositol phosphatase SHIP2 to regulate actin-pedestal formation. Cell Host Microbe 7: 13-24.
30. Campellone KG, (2010) Phosphoinositides influence pathogen surfing: EPEC rights the SHIP. Cell Host Microbe 7: 1-2.
31. Lahdenpera J, Kilpelainen P, Liu XL, Pikkarainen T, Reponen P, et al. (2003) Clustering-induced tyrosine phosphorylation of nephrin by Src family kinases. Kidney Int 64: 404-413.
32. Wary KK, Mariotti A, Zurzolo C, Giancotti FG, (1998) A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634.
33. Rivera GM, Briceno CA, Takeshima F, Snapper SB, Mayer BJ, (2004) Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization. Curr Biol 14: 11-22.
34. Byfield FJ, Wen Q, Levental I, Nordstrom K, Arratia PE, et al. (2009) Absence of filamin A prevents cells from responding to stiffness gradients on gels coated with collagen but not fibronectin. Biophys J 96: 5095-5102.
35. Garg P, Verma R, Cook L, Soofi A, Venkatareddy M, et al. (2010) Actin-depolymerizing factor cofilin-1 is necessary in maintaining mature podocyte architecture. J Biol Chem 285: 22676-22688.
36. Dyson JM, Munday AD, Kong AM, Huysmans RD, Matzaris M, et al. (2003) SHIP-2 forms a tetrameric complex with filamin, actin, and GPIb-IX-V: localization of SHIP-2 to the activated platelet actin cytoskeleton. Blood 102: 940-948.
37. Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, et al. (2002) Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol 4: 681-690.
38. Ravid D, Chuderland D, Landsman L, Lavie Y, Reich R, et al. (2008) Filamin A is a novel caveolin-1-dependent target in IGF-I-stimulated cancer cell migration. Exp Cell Res 314: 2762-2773.
39. Flanagan LA, Chou J, Falet H, Neujahr R, Hartwig JH, et al. (2001) Filamin A, the Arp2/3 complex, and the morphology and function of cortical actin filaments in human melanoma cells. J Cell Biol 155: 511-517.
40. Prasad N, Topping RS, Decker SJ, (2002) Src family tyrosine kinases regulate adhesion-dependent tyrosine phosphorylation of 5'-inositol phosphatase SHIP2 during cell attachment and spreading on collagen I. J Cell Sci 115: 3807-3815.
41. Rameh LE, Cantley LC, (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274: 8347-8350.
42. Hogan A, Yakubchyk Y, Chabot J, Obagi C, Daher E, et al. (2004) The phosphoinositol 3,4-bisphosphate-binding protein TAPP1 interacts with syntrophins and regulates actin cytoskeletal organization. J Biol Chem 279: 53717-53724.
43. Krause M, Leslie JD, Stewart M, Lafuente EM, Valderrama F, et al. (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev Cell 7: 571-583.
44. Chang C, Adler CE, Krause M, Clark SG, Gertler FB, et al. (2006) MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin. Curr Biol 16: 854-862.
45. Reiser J, von Gersdorff G, Loos M, Oh J, Asanuma K, et al. (2004) Induction of B7-1 in podocytes is associated with nephrotic syndrome. J Clin Invest 113: 1390-1397.
46. Saarikangas J, Zhao H, Lappalainen P, (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90: 259-289.
47. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, et al. (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401: 926-929.
48. Marchand JB, Moreau P, Paoletti A, Cossart P, Carlier MF, et al. (1995) Actin-based movement of Listeria monocytogenes: actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J Cell Biol 130: 331-343.
49. Goosney DL, de Grado M, Finlay BB, (1999) Putting E. coli on a pedestal: a unique system to study signal transduction and the actin cytoskeleton. Trends Cell Biol 9: 11-14.
50. Gruenheid S, DeVinney R, Bladt F, Goosney D, Gelkop S, et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3: 856-859.
51. Tikhmyanova N, Little JL, Golemis EA, (2010) CAS proteins in normal and pathological cell growth control. Cell Mol Life Sci 67: 1025-1048.
52. Defilippi P, Di Stefano P, Cabodi S, (2006) p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol 16: 257-263.
53. Prasad N, Topping RS, Decker SJ, (2001) SH2-containing inositol 5'-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading. Mol Cell Biol 21: 1416-1428.
54. Takala H, Nurminen E, Nurmi SM, Aatonen M, Strandin T, et al. (2008) Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding. Blood 112: 1853-1862.
55. Kiema T, Lad Y, Jiang P, Oxley CL, Baldassarre M, et al. (2006) The molecular basis of filamin binding to integrins and competition with talin. Mol Cell 21: 337-347.
56. Xu Y, Bismar TA, Su J, Xu B, Kristiansen G, et al. (2010) Filamin A regulates focal adhesion disassembly and suppresses breast cancer cell migration and invasion. J Exp Med 207: 2421-2437.
57. Onji T, Takagi M, Shibata N, (1987) Calpain abolishes the effect of filamin on the actomyosin system in platelets. Biochim Biophys Acta 912: 283-286.
58. Prasad NK, (2009) SHIP2 phosphoinositol phosphatase positively regulates EGFR-Akt pathway, CXCR4 expression, and cell migration in MDA-MB-231 breast cancer cells. Int J Oncol 34: 97-105.
59. Jimenez C, Portela RA, Mellado M, Rodriguez-Frade JM, Collard J, et al. (2000) Role of the PI3K regulatory subunit in the control of actin organization and cell migration. J Cell Biol 151: 249-262.
60. Prasad NK, Decker SJ, (2005) SH2-containing 5'-inositol phosphatase, SHIP2, regulates cytoskeleton organization and ligand-dependent down-regulation of the epidermal growth factor receptor. J Biol Chem 280: 13129-13136.
61. Weiger MC, Wang CC, Krajcovic M, Melvin AT, Rhoden JJ, et al. (2009) Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts. J Cell Sci 122: 313-323.