Proteasomal degradation of Nck1 but not Nck2 regulates RhoA activation and actin dynamics

Nature Communications

Volumn 4, Issue , 2013, Pages

  Buvall, Lisa ^a   Rashmi, Priyanka ^a,d   Lopez Rivera, Esther ^b   Andreeva, Svetlana ^a   Weins, Astrid ^a,c   Wallentin, Hanna ^a   Greka, Anna ^a   Mundel, Peter ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CBL PROTEIN; CYCLIN D1; LYSINE; NCK PROTEIN; PROTEASOME; PROTEIN NCK1; PROTEIN NCK2; PROTEIN SH3; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SYNAPTOPODIN; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID; GENE EXPRESSION; PROTEIN;

ARTICLE; BINDING SITE; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; KIDNEY DEVELOPMENT; PODOCYTE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRESS FIBER; UBIQUITINATION; UPREGULATION;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CYTOSKELETON; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; ONCOGENE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-CBL; RHOA GTP-BINDING PROTEIN; UBIQUITINATION;

EID: 84889239217     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3863     Document Type: Article

References (41)

1. Buday, L., Wunderlich, L. & Tamas, P. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal. 14, 723-731 (2002). (Pubitemid 34597179)
2. Lettau, M., Pieper, J. & Janssen, O. Nck adapter proteins: functional versatility in T cells. Cell commun. Signal. 7, 1 (2009).
3. Rohatgi, R., Nollau, P., Ho, H. Y., Kirschner, M. W. & Mayer, B. J. Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276, 26448-26452 (2001).
4. Yamaguchi, H. et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452 (2005). (Pubitemid 40205066)
5. Lu, W., Katz, S., Gupta, R. & Mayer, B. J. Activation of Pak by membrane localization mediated by an SH3 domain from the adaptor protein Nck. Curr. Biol. 7, 85-94 (1997). (Pubitemid 27155617)
6. Greka, A. & Mundel, P. Cell biology and pathology of podocytes. Ann. Rev. Physiol. 74, 299-323 (2012).
7. Faul, C., Asanuma, K., Yanagida-Asanuma, E., Kim, K. & Mundel, P. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol. 17, 428-437 (2007). (Pubitemid 47499042)
8. Verma, R. et al. Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J. Clin. Invest. 116, 1346-1359 (2006).
9. Jones, N. et al. Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440, 818-823 (2006).
10. Jones, N. et al. Nck proteins maintain the adult glomerular filtration barrier. J. Am. Soc. Nephrol. 20, 1533-1543 (2009).
11. Mundel, P. et al. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J. Cell Biol. 139, 193-204 (1997). (Pubitemid 27444091)
12. Asanuma, K. et al. Synaptopodin regulates the actin-bundling activity of alphaactinin in an isoform-specific manner. J. Clin. Invest. 115, 1188-1198 (2005). (Pubitemid 40629037)
13. Asanuma, K. et al. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol. 8, 485-491 (2006).
14. Yanagida-Asanuma, E. et al. Synaptopodin protects against proteinuria by disrupting Cdc42:IRSp53:Mena signaling complexes in kidney podocytes. Am. J. Pathol. 171, 415-427 (2007). (Pubitemid 47344675)
15. Wong, J. S. et al. Rescue of tropomyosin deficiency in Drosophila and human cancer cells by synaptopodin reveals a role of tropomyosin alpha in RhoA stabilization. EMBO J. 31, 1028-1040 (2012).
16. Huber, T. B. et al. Bigenic mouse models of focal segmental glomerulosclerosis involving pairwise interaction of CD2AP, Fyn, and synaptopodin. J. Clin. Invest. 116, 1337-1345 (2006).
17. Mundel, P. et al. 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). (Pubitemid 27452369)
18. Wunderlich, L., Goher, A., Farago, A., Downward, J. & Buday, L. Requirement of multiple SH3 domains of Nck for ligand binding. Cell Signal. 11, 253-262 (1999). (Pubitemid 29185127)
19. Catic, A., Collins, C., Church, G. M. & Ploegh, H. L. Preferred in vivo ubiquitination sites. Bioinformatics 20, 3302-3307 (2004). (Pubitemid 40136763)
20. Waterman, H., Levkowitz, G., Alroy, I. & Yarden, Y. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J. Biol. Chem. 274, 22151-22154 (1999).
21. Faul, C. et al. Promotion of importin {alpha}-mediated nuclear import by the phosphorylation-dependent binding of cargo protein to 14-3-3. J. Cell Biol. 169, 415-424 (2005). (Pubitemid 40686692)
22. Gong, C., Stoletov, K. V. & Terman, B. I. VEGF treatment induces signaling pathways that regulate both actin polymerization and depolymerization. Angiogenesis 7, 313-321 (2004). (Pubitemid 40767933)
23. Ruusala, A., Pawson, T., Heldin, C. H. & Aspenstrom, P. Nck adapters are involved in the formation of dorsal ruffles, cell migration, and Rho signaling downstream of the platelet-derived growth factor beta receptor. J. Biol. Chem. 283, 30034-30044 (2008).
24. Nolen, B. J. et al. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034 (2009).
25. Rizvi, S. A. et al. Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chem. Biol. 16, 1158-1168 (2009).
26. Uehata, M. et al. Calcium sensitization of smooth muscle mediated by a Rhoassociated protein kinase in hypertension. Nature 389, 990-994 (1997). (Pubitemid 27485693)
27. Yang, Q., Zhang, X. F., Pollard, T. D. & Forscher, P. Arp2/3 complexdependent actin networks constrain myosin II function in driving retrograde actin flow. J. Cell Biol. 197, 939-956 (2012).
28. Jaffe, A. B. & Hall, A. RHO GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269 (2005). (Pubitemid 41740635)
29. Rivero-Lezcano, O. M., Sameshima, J. H., Marcilla, A. & Robbins, K. C. Physical association between Src homology 3 elements and the protein product of the c-cbl proto-oncogene. J. Biol. Chem. 269, 17363-17366 (1994). (Pubitemid 24218003)
30. Miyoshi-Akiyama, T., Aleman, L. M., Smith, J. M., Adler, C. E. & Mayer, B. J. Regulation of Cbl phosphorylation by the Abl tyrosine kinase and the Nck SH2/SH3 adaptor. Oncogene 20, 4058-4069 (2001). (Pubitemid 32681611)
31. Adler, C. E. et al. Abl family kinases and Cbl cooperate with the Nck adaptor to modulate Xenopus development. J. Biol. Chem. 275, 36472-36478 (2000).
32. Swaminathan, G. & Tsygankov, A. Y. The Cbl family proteins: ring leaders in regulation of cell signaling. J. Cell Physiol. 209, 21-43 (2006). (Pubitemid 44318665)
33. Tian, D. et al. Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci. Signal. 3, ra77 (2010).
34. Faul, C. et al. The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat. Med. 14, 931-938 (2008).
35. Suetsugu, S. et al. Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem. J. 384, 1-8 (2004). (Pubitemid 39564155)
36. Cestra, G., Toomre, D., Chang, S. & De Camilli, P. The Abl/Arg substrate ArgBP2/nArgBP2 coordinates the function of multiple regulatory mechanisms converging on the actin cytoskeleton. Proc. Natl Acad. Sci. USA 102, 1731-1736 (2005). (Pubitemid 40209236)
37. Thevenot, E. et al. p21-Activated kinase 3 (PAK3) protein regulates synaptic transmission through its interaction with the Nck2/Grb4 protein adaptor. J. Biol. Chem. 286, 40044-40059 (2011).
38. Chen, M. et al. Identification of Nck family genes, chromosomal localization, expression, and signaling specificity. J. Biol. Chem. 273, 25171-25178 (1998). (Pubitemid 28443277)
39. Bladt, F. et al. The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol. Cell Biol. 23, 4586-4597 (2003). (Pubitemid 36734748)
40. Boulter, E. et al. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat. Cell Biol. 12, 477-483 (2010).
41. Chen, Y. et al. Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell 35, 841-855 (2009).