Supervillin-mediated suppression of p53 protein enhances cell survival

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7918-7929

  Fang, Zhiyou ^a   Luna, Elizabeth J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL-SUBSTRATE ADHESION; CELLULAR RESPONSE; DEUBIQUITINATING ENZYMES; DOWNSTREAM TARGET; METABOLIC ACTIVITY; REGULATORY PROTEIN; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-LIKE PROTEINS;

ADHESION; CELL DEATH; CELL PROLIFERATION; PROTEINS;

CELL SIGNALING;

CELL PROTEIN; DOXORUBICIN; ETOPOSIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN P53; PROTEIN USP7; SUMO 1 PROTEIN; SUPERVILLIN ISOFORM 1; SUPERVILLIN ISOFORM 4; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; COVALENT BOND; DNA DAMAGE; DOWN REGULATION; EXPRESSION VECTOR; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SUMOYLATION; UBIQUITINATION; UPREGULATION;

CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CLONING, MOLECULAR; CYTOSKELETON; DNA DAMAGE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENETIC VECTORS; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN THIOLESTERASE;

EID: 84875181259     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.416842     Document Type: Article

References (67)

1. Taddei, M. L., Giannoni, E., Fiaschi, T., and Chiarugi, P. (2012) Anoikis: an emerging hallmark in health and diseases. J. Pathol. 226, 380-393
2. Hu, P., and Luo, B. H. (2013) Integrin bidirectional signaling across the plasma membrane. J. Cell. Physiol. 228, 306-312
3. Wehrle-Haller, B. (2012) Structure and function of focal adhesions. Curr. Opin. Cell Biol. 24, 116-124
4. Cheng, H., Liu, P., Wang, Z. C., Zou, L., Santiago, S., Garbitt, V., Gjoerup, O. V., Iglehart, J. D., Miron, A., Richardson, A. L., Hahn, W. C., and Zhao, J. J. (2009) SIK1 couples LKB1 to p53-dependent anoikis and suppresses metastasis. Sci. Signal. 2, ra35
5. Horbinski, C., Mojesky, C., and Kyprianou, N. (2010) Live free or die: tales of homeless (cells) in cancer. Am. J. Pathol. 177, 1044-1052
6. Ilić, D., Almeida, E. A., Schlaepfer, D. D., Dazin, P., Aizawa, S., and Damsky, C. H. (1998) Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J. Cell Biol. 143, 547-560
7. Golubovskaya, V. M., and Cance, W. G. (2011) FAK and p53 protein interactions. Anticancer Agents Med. Chem. 11, 617-619
8. Weis, S. M., Lim, S. T., Lutu-Fuga, K. M., Barnes, L. A., Chen, X. L., Göthert, J. R., Shen, T. L., Guan, J. L., Schlaepfer, D. D., and Cheresh, D. A. (2008) Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J. Cell Biol. 181, 43-50
9. Lim, S. T., Miller, N. L., Nam, J. O., Chen, X. L., Lim, Y., and Schlaepfer, D. D. (2010) Pyk2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival. J. Biol. Chem. 285, 1743-1753
10. Destaing, O., Block, M. R., Planus, E., and Albiges-Rizo, C. (2011) Invadosome regulation by adhesion signaling. Curr. Opin. Cell Biol. 23, 597-606
11. Linder, S., Wiesner, C., and Himmel, M. (2011) Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27, 185-211
12. Hochgräfe, F., Zhang, L., O'Toole, S. A., Browne, B. C., Pinese, M., Porta Cubas, A., Lehrbach, G. M., Croucher, D. R., Rickwood, D., Boulghourjian, A., Shearer, R., Nair, R., Swarbrick, A., Faratian, D., Mullen, P., Harrison, D. J., Biankin, A. V., Sutherland, R. L., Raftery, M. J., and Daly, R. J. (2010) Tyrosine phosphorylation profiling reveals the signaling network characteristics of basal breast cancer cells. Cancer Res. 70, 9391-9401
13. Ren, X., Cao, C., Zhu, L., Yoshida, K., Kharbanda, S., Weichselbaum, R., and Kufe, D. (2002) Lyn tyrosine kinase inhibits nuclear export of the p53 tumor suppressor. Cancer Biol. Ther. 1, 703-708
14. Iqbal, M. S., Tsuyama, N., Obata, M., and Ishikawa, H. (2010) A novel signaling pathway associated with Lyn, PI3-kinase and Akt supports the proliferation of myeloma cells. Biochem. Biophys. Res. Commun. 392, 415-420
15. Mukhopadhyay, U. K., Eves, R., Jia, L., Mooney, P., and Mak, A. S. (2009) p53 suppresses Src-induced podosome and rosette formation and cellular invasiveness through the up-regulation of caldesmon. Mol. Cell. Biol. 29, 3088-3098
16. Muller, P. A., Caswell, P. T., Doyle, B., Iwanicki, M. P., Tan, E. H., Karim, S., Lukashchuk, N., Gillespie, D. A., Ludwig, R. L., Gosselin, P., Cromer, A., Brugge, J. S., Sansom, O. J., Norman, J. C., and Vousden, K. H. (2009) Mutant p53 drives invasion by promoting integrin recycling. Cell 139, 1327-1341
17. Mak, A. S. (2011) p53 regulation of podosome formation and cellular invasion in vascular smooth muscle cells. Cell Adh. Migr. 5, 144-149
18. Bhuwania, R., Cornfine, S., Fang, Z., Krüger, M., Luna, E. J., and Linder, S. (2012) Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J. Cell Sci. 125, 2300-2314
19. Crowley, J. L., Smith, T. C., Fang, Z., Takizawa, N., and Luna, E. J. (2009) Supervillin reorganizes the actin cytoskeleton and increases invadopodial efficiency. Mol. Biol. Cell 20, 948-962
20. Edelstein, L. C., Luna, E. J., Gibson, I. B., Bray, M., Jin, Y., Kondkar, A., Nagalla, S., Hadjout-Rabi, N., Smith, T. C., Covarrubias, D., Jones, S. N., Ahmad, F., Stolla, M., Kong, X. G., Fang, Z., Bergmeier, W., Shaw, C., Leal, S. M., and Bray, P. F. (2012) Human genome-wide association and mouse knockout approaches Identify platelet supervillin as an inhibitor of thrombus formation under shear stress. Circulation 125, 2762-2771
21. Nebl, T., Pestonjamasp, K. N., Leszyk, J. D., Crowley, J. L., Oh, S. W., and Luna, E. J. (2002) Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J. Biol. Chem. 277, 43399-43409
22. Smith, T. C., Fang, Z., and Luna, E. J. (2010) Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton 67, 346-364
23. Takizawa, N., Smith, T. C., Nebl, T., Crowley, J. L., Palmieri, S. J., Lifshitz, L. M., Ehrhardt, A. G., Hoffman, L. M., Beckerle, M. C., and Luna, E. J. (2006) Supervillin modulation of focal adhesions involving TRIP6/ZRP-1. J. Cell Biol. 174, 447-458
24. Wulfkuhle, J. D., Donina, I. E., Stark, N. H., Pope, R. K., Pestonjamasp, K. N., Niswonger, M. L., and Luna, E. J. (1999) Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J. Cell Sci. 112, 2125-2136
25. Mitra, S. K., Hanson, D. A., and Schlaepfer, D. D. (2005) Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68
26. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T., and Horwitz, A. F. (2004) FAK-Src signalling through paxillin: ERK and MLCK regulate adhesion disassembly. Nat. Cell Biol. 6, 154-161
27. Takizawa, N., Ikebe, R., Ikebe, M., and Luna, E. J. (2007) Supervillin slows cell spreading by facilitating myosin II activation at the cell periphery. J. Cell Sci. 120, 3792-3803
28. Fang, Z., Takizawa, N., Wilson, K. A., Smith, T. C., Delprato, A., Davidson, M. W., Lambright, D. G., and Luna, E. J. (2010) The membrane protein, supervillin, accelerates rapid integrin recycling and cell motility. Traffic 11, 782-799
29. Kuo, J. C., Han, X., Hsiao, C. T., Yates, J. R., 3rd, and Waterman, C. M. (2011) Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393
30. Gangopadhyay, S. S., Takizawa, N., Gallant, C., Barber, A. L., Je, H. D., Smith, T. C., Luna, E. J., and Morgan, K. G. (2004) Smooth muscle archvillin: a novel regulator of signaling and contractility in vascular smooth muscle. J. Cell Sci. 117, 5043-5057
31. Gangopadhyay, S. S., Kengni, E., Appel, S., Gallant, C., Kim, H. R., Leavis, P., DeGnore, J., and Morgan, K. G. (2009) Smooth muscle archvillin is an ERK scaffolding protein. J. Biol. Chem. 284, 17607-17615
32. Nicholson, B., and Suresh Kumar, K. G. (2011) The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 60, 61-68
33. Oh, S. W., Pope, R. K., Smith, K. P., Crowley, J. L., Nebl, T., Lawrence, J. B., and Luna, E. J. (2003) Archvillin, a muscle-specific isoform of supervillin, is an early expressed component of the costameric membrane skeleton. J. Cell Sci. 116, 2261-2275
34. Pope, R. K., Pestonjamasp, K. N., Smith, K. P., Wulfkuhle, J. D., Strassel, C. P., Lawrence, J. B., and Luna, E. J. (1998) Cloning, characterization, and chromosomal localization of human supervillin (SVIL). Genomics 52, 342-351
35. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
36. Dantuma, N. P., Groothuis, T. A., Salomons, F. A., and Neefjes, J. (2006) A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 173, 19-26
37. Kamitani, T., Kito, K., Nguyen, H. P., and Yeh, E. T. (1997) Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem. 272, 28557-28562
38. Fu, C., Ahmed, K., Ding, H., Ding, X., Lan, J., Yang, Z., Miao, Y., Zhu, Y., Shi, Y., Zhu, J., Huang, H., and Yao, X. (2005) Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 24, 5401-5413
39. van de Loosdrecht, A. A., Beelen, R. H., Ossenkoppele, G. J., Broekhoven, M. G., and Langenhuijsen, M. M. (1994)Atetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. J. Immunol. Methods 174, 311-320
40. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
41. Pestonjamasp, K. N., Pope, R. K., Wulfkuhle, J. D., and Luna, E. J. (1997) Supervillin (p205): a novel membrane-associated, F-actin-binding protein in the villin/gelsolin superfamily. J. Cell Biol. 139, 1255-1269
42. Davoli, T., and de Lange, T. (2011) The causes and consequences of polyploidy in normal development and cancer. Annu. Rev. Cell Dev. Biol. 27, 585-610
43. Kannan, K., Amariglio, N., Rechavi, G., Jakob-Hirsch, J., Kela, I., Kaminski, N., Getz, G., Domany, E., and Givol, D. (2001) DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene 20, 2225-2234
44. Andoh, T. (2000) Signal transduction pathways leading to cell cycle arrest and apoptosis induced by DNA topoisomerase poisons. Cell Biochem. Biophys. 33, 181-188
45. Komarov, P. G., Komarova, E. A., Kondratov, R. V., Christov-Tselkov, K., Coon, J. S., Chernov, M. V., and Gudkov, A. V. (1999)Achemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285, 1733-1737
46. Strom, E., Sathe, S., Komarov, P. G., Chernova, O. B., Pavlovska, I., Shyshynova, I., Bosykh, D. A., Burdelya, L. G., Macklis, R. M., Skaliter, R., Komarova, E. A., and Gudkov, A. V. (2006) Small-molecule inhibitor of p53 binding to mitochondria protects mice from γ radiation. Nat. Chem. Biol. 2, 474-479
47. Dinkel, H., Michael, S., Weatheritt, R. J., Davey, N. E., Van Roey, K., Altenberg, B., Toedt, G., Uyar, B., Seiler, M., Budd, A., Jödicke, L., Dammert, M. A., Schroeter, C., Hammer, M., Schmidt, T., Jehl, P., McGuigan, C., Dymecka, M., Chica, C., Luck, K., Via, A., Chatr-Aryamontri, A., Haslam, N., Grebnev, G., Edwards, R. J., Steinmetz, M. O., Meiselbach, H., Diella, F., and Gibson, T. J. (2012) ELM: the database of eukaryotic linear motifs. Nucleic Acids Res. 40, D242-251
48. Li, M., Brooks, C. L., Kon, N., and Gu, W. (2004)Adynamic role ofHAUSP in the p53-Mdm2 pathway. Mol. Cell 13, 879-886
49. Li, M., Chen, D., Shiloh, A., Luo, J., Nikolaev, A. Y., Qin, J., and Gu, W. (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-653
50. Praefcke, G. J., Hofmann, K., and Dohmen, R. J. (2012) SUMO playing tag with ubiquitin. Trends Biochem. Sci. 37, 23-31
51. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R. R., Mohan, A., Heyen, J. W., Goebl, M. G., and Iakoucheva, L. M. (2010) Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78, 365-380
52. Moody, C. A., and Laimins, L. A. (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10, 550-560
53. Muratani, M., Gerlich, D., Janicki, S. M., Gebhard, M., Eils, R., and Spector, D. L. (2002) Metabolic-energy-dependent movement of PML bodies within the mammalian cell nucleus. Nat. Cell Biol. 4, 106-110
54. Hock, A., and Vousden, K. H. (2010) Regulation of the p53 pathway by ubiquitin and related proteins. Int. J. Biochem. Cell Biol. 42, 1618-1621
55. Fabbro, M., and Henderson, B. R. (2003) Regulation of tumor suppressors by nuclear-cytoplasmic shuttling. Exp. Cell Res. 282, 59-69
56. Fernández-Montalvan, A., Bouwmeester, T., Joberty, G., Mader, R., Mahnke, M., Pierrat, B., Schlaeppi, J. M., Worpenberg, S., and Gerhartz, B. (2007) Biochemical characterization of USP7 reveals post-translational modification sites and structural requirements for substrate processing and subcellular localization. FEBS J. 274, 4256-4270
57. Ting, H. J., Yeh, S., Nishimura, K., and Chang, C. (2002) Supervillin associates with androgen receptor and modulates its transcriptional activity. Proc. Natl. Acad. Sci. U.S.A. 99, 661-666
58. Lim, S. T., Chen, X. L., Lim, Y., Hanson, D. A., Vo, T. T., Howerton, K., Larocque, N., Fisher, S. J., Schlaepfer, D. D., and Ilic, D. (2008) Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell 29, 9-22
59. -/- fibroblasts are defective in their ability to disassemble focal adhesions in response to phorbol ester/hyaluronan treatment. Cell Commun. Adhes. 9, 273-283
60. Nagano, M., Hoshino, D., Koshikawa, N., Akizawa, T., and Seiki, M. (2012) Turnover of focal adhesions and cancer cell migration. Int. J. Cell Biol. 2012, 310616
61. Ezratty, E. J., Partridge, M. A., and Gundersen, G. G. (2005) Microtubuleinduced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590
62. Westhoff, M. A., Serrels, B., Fincham, V. J., Frame, M. C., and Carragher, N. O. (2004) SRC-mediated phosphorylation of focal adhesion kinase couples actin and adhesion dynamics to survival signaling. Mol. Cell. Biol. 24, 8113-8133
63. Janouskova, H., Maglott, A., Leger, D. Y., Bossert, C., Noulet, F., Guerin, E., Guenot, D., Pinel, S., Chastagner, P., Plenat, F., Entz-Werle, N., Lehmann-Che, J., Godet, J., Martin, S., Teisinger, J., and Dontenwill, M. (2012) Integrin α5β1 plays a critical role in resistance to temozolomide by interfering with the p53 pathway in high-grade glioma. Cancer Res. 72, 3463-3470
64. Schaefer, A., Nethe, M., and Hordijk, P. L. (2012) Ubiquitin links to cytoskeletal dynamics, cell adhesion and migration. Biochem. J. 442, 13-25
65. Buus, R., Faronato, M., Hammond, D. E., Urbé, S., and Clague, M. J. (2009) Deubiquitinase activities required for hepatocyte growth factor-induced scattering of epithelial cells. Curr. Biol. 19, 1463-1466
66. Forbes, S. A., Bindal, N., Bamford, S., Cole, C., Kok, C. Y., Beare, D., Jia, M., Shepherd, R., Leung, K., Menzies, A., Teague, J. W., Campbell, P. J., Stratton, M. R., and Futreal, P. A. (2011) COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39, D945-950
67. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Meth. 9, 671-675