Integrins synergise to induce expression of the MRTF-A-SRF target gene ISG15 for promoting cancer cell invasion

Journal of Cell Science

Volumn 129, Issue 7, 2016, Pages 1391-1403

  Hermann, Michaela Rosemarie ^a   Jakobson, Madis ^a   Colo, Georgina P ^a   Rognoni, Emanuel ^a   Jakobson, Maili ^a   Kupatt, Christian ^b   Posern, Guido ^c   Fässler, Reinhard ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Institute of Physiological Chemistry   (Germany)

Author keywords

Cell migration; Integrin; ISG15; MRTF A; SRF

Indexed keywords

CYTOSKELETON PROTEIN; FIBRONECTIN; G ACTIN; INTEGRIN; ACTIN; BETA1 INTEGRIN; CD51 ANTIGEN; CYTOKINE; ISG15 PROTEIN, HUMAN; MKL1 PROTEIN, HUMAN; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; UBIQUITIN;

ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEOMICS; TRANSCRIPTOMICS; BREAST TUMOR; CELL ADHESION; CELL MOTION; CYTOSKELETON; FOCAL ADHESION; GENETICS; MCF-7 CELL LINE; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR INVASION;

ACTINS; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CYTOKINES; CYTOSKELETON; FOCAL ADHESIONS; HUMANS; INTEGRIN ALPHAV; INTEGRIN BETA1; MCF-7 CELLS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANS-ACTIVATORS; UBIQUITINS;

EID: 84964033541     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.177592     Document Type: Article

References (56)

1. Azioune, A., Carpi, N., Tseng, Q., Théry, M. and Piel, M. (2010). Protein micropatterns: a direct printing protocol using deep UVs. Methods Cell Biol. 97, 133-146.
2. Balza, R. O., Jr and Misra, R. P. (2006). Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. J. Biol. Chem. 281, 6498-6510.
3. Bishop, A. L. and Hall, A. (2000). Rho GTPases and their effector proteins. Biochem. J. 348, 241-255.
4. Busche, S., Descot, A., Julien, S., Genth, H. and Posern, G. (2008). Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J. Cell Sci. 121, 1025-1035.
5. Connelly, J. T., Gautrot, J. E., Trappmann, B., Tan, D. W.-M., Donati, G., Huck, W. T. S. and Watt, F. M. (2010). Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat. Cell Biol. 12, 711-718.
6. Cooper, S. J., Trinklein, N. D., Nguyen, L. and Myers, R. M. (2007). Serum response factor binding sites differ in three human cell types. Genome Res. 17, 136-144.
7. Danen, E. H. J., Sonneveld, P., Brakebusch, C., Fässler, R. and Sonnenberg, A. (2002). The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J. Cell Biol. 159, 1071-1086.
8. Desai, S. D., Haas, A. L., Wood, L. M., Tsai, Y.-C., Pestka, S., Rubin, E. H., Saleem, A., Nur-E-Kamal, A. and Liu, L. F. (2006). Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Cancer Res. 66, 921-928.
9. Desai, S. D., Reed, R. E., Burks, J., Wood, L. M., Pullikuth, A. K., Haas, A. L., Liu, L. F., Breslin, J. W., Meiners, S. and Sankar, S. (2012). ISG15 disrupts cytoskeletal architecture and promotes motility in human breast cancer cells. Exp. Biol. Med. 237, 38-49.
10. Descot, A., Hoffmann, R., Shaposhnikov, D., Reschke, M., Ullrich, A. and Posern, G. (2009). Negative regulation of the EGFR-MAPK cascade by actin-MAL-mediated Mig6/Errfi-1 induction. Mol. Cell 35, 291-304.
11. Durfee, L. A., Lyon, N., Seo, K. and Huibregtse, J. M. (2010). The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell 38, 722-732.
12. Esnault, C., Stewart, A., Gualdrini, F., East, P., Horswell, S., Matthews, N. and Treisman, R. (2014). Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev. 28, 943-958.
13. Farrell, P. J., Broeze, R. J. and Lengyel, P. (1979). Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 279, 523-525.
14. Gyorffy, B., Lanczky, A., Eklund, A. C., Denkert, C., Budczies, J., Li, Q. and Szallasi, Z. (2010). An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treatment 123, 725-731.
15. Haas, A. L., Ahrens, P., Bright, P. M. and Ankel, H. (1987). Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262, 11315-11323.
16. Hall, A. (2012). Rho family GTPases. Biochem. Soc. Trans. 40, 1378-1382.
17. Han, S.-Y., Kim, S.-H. and Heasley, L. E. (2002). Differential gene regulation by specific gain-of-function JNK1 proteins expressed in Swiss 3T3 fibroblasts. J. Biol. Chem. 277, 47167-47174.
18. Hermeking, H., Lengauer, C., Polyak, K., He, T.-C., Zhang, L., Thiagalingam, S., Kinzler, K. W. and Vogelstein, B. (1997). 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1, 3-11.
19. Hood, J. D. and Cheresh, D. A. (2002). Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2, 91-100.
20. Hoshino, D., Branch, K. M. and Weaver, A. M. (2013). Signaling inputs to invadopodia and podosomes. J. Cell Sci. 126, 2979-2989.
21. Hu, Q., Guo, C., Li, Y., Aronow, B. J. and Zhang, J. (2011). LMO7 mediates cell-specific activation of the Rho-myocardin-related transcription factor-serum response factor pathway and plays an important role in breast cancer cell migration. Mol. Cell. Biol. 31, 3223-3240.
22. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
23. Jeon, Y. J., Choi, J. S., Lee, J. Y., Yu, K. R., Kim, S. M., Ka, S. H., Oh, K. H., Kim, K. I., Zhang, D.-E., Bang, O. S. et al. (2009). ISG15 modification of filamin B negatively regulates the type I interferon-induced JNK signalling pathway. EMBO Rep. 10, 374-380.
24. Kerscher, O., Felberbaum, R. and Hochstrasser, M. (2006). Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180.
25. Kressner, C., Nollau, P., Grosse, R. and Brandt, D. T. (2013). Functional interaction of SCAI with the SWI/SNF complex for transcription and tumor cell invasion. PLoS ONE 8, e69947.
26. Legate, K. R., Wickstrom, S. A. and Fassler, R. (2009). Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 23, 397-418.
27. Leitner, L., Shaposhnikov, D., Mengel, A., Descot, A., Julien, S., Hoffmann, R. and Posern, G. (2011). MAL/MRTF-A controls migration of non-invasive cells by upregulation of cytoskeleton-associated proteins. J. Cell Sci. 124, 4318-4331.
28. Lenschow, D. J., Giannakopoulos, N. V., Gunn, L. J., Johnston, C., O'Guin, A. K., Schmidt, R. E., Levine, B. and Virgin, H. W.IV. (2005). Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79, 13974-13983.
29. Liu, M., Li, X.-L. and Hassel, B. A. (2003). Proteasomes modulate conjugation to the ubiquitin-like protein, ISG15. J. Biol. Chem. 278, 1594-1602.
30. Lock, C., Hermans, G., Pedotti, R., Brendolan, A., Schadt, E., Garren, H., Langer-Gould, A., Strober, S., Cannella, B., Allard, J. et al. (2002). Genemicroarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8, 500-508.
31. Loeb, K. R. and Haas, A. L. (1992). The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267, 7806-7813.
32. Malakhov, M. P., Malakhova, O. A., Kim, K. I., Ritchie, K. J. and Zhang, D.-E. (2002). UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277, 9976-9981.
33. Malakhova, O. A. and Zhang, D.-E. (2008). ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Biol. Chem. 283, 8783-8787.
34. Medjkane, S., Perez-Sanchez, C., Gaggioli, C., Sahai, E. and Treisman, R. (2009). Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 11, 257-268.
35. Miralles, F., Posern, G., Zaromytidou, A.-I. and Treisman, R. (2003). Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342.
36. Morales, D. J. and Lenschow, D. J. (2013). The antiviral activities of ISG15. J. Mol. Biol. 425, 4995-5008.
37. Murphy, D. A. and Courtneidge, S. A. (2011). The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426.
38. Neve, R. M., Chin, K., Fridlyand, J., Yeh, J., Baehner, F. L., Fevr, T., Clark, L., Bayani, N., Coppe, J.-P., Tong, F. et al. (2006). A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515-527.
39. Okumura, F., Zou, W. and Zhang, D.-E. (2007). ISG15 modification of the eIF4E cognate 4EHP enhances cap structure-binding activity of 4EHP. Genes Dev. 21, 255-260.
40. Okumura, A., Pitha, P. M. and Harty, R. N. (2008). ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. USA 105, 3974-3979.
41. Okumura, F., Okumura, A. J., Uematsu, K., Hatakeyama, S., Zhang, D.-E. and Kamura, T. (2013). Activation of double-stranded RNA-activated protein kinase (PKR) by interferon-stimulated gene 15 (ISG15) modification down-regulates protein translation. J. Biol. Chem. 288, 2839-2847.
42. Olson, E. N. and Nordheim, A. (2010). Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 11, 353-365.
43. Philippar, U., Schratt, G., Dieterich, C., Müller, J. M., Galgóczy, P., Engel, F. B., Keating, M. T., Gertler, F., Schüle, R., Vingron, M. et al. (2004). The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol. Cell 16, 867-880.
44. Plessner, M., Melak, M., Chinchilla, P., Baarlink, C. and Grosse, R. (2015). Nuclear F-actin formation and reorganization upon cell spreading. J. Biol. Chem. 290, 11209-11216.
45. Posern, G. and Treisman, R. (2006). Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16, 588-596.
46. Schiller, H. B., Hermann, M.-R., Polleux, J., Vignaud, T., Zanivan, S., Friedel, C. C., Sun, Z., Raducanu, A., Gottschalk, K.-E., Théry, M. et al. (2013). beta1-and alphav-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 15, 625-636.
47. Selvaraj, A. and Prywes, R. (2004). Expression profiling of serum inducible genes identifies a subset of SRF target genes that areMKL dependent. BMC Mol. Biol. 5, 13.
48. Small, J.-V., Rottner, K., Hahne, P. and Anderson, K. I. (1999). Visualising the actin cytoskeleton. Microsc. Res. Tech. 47, 3-17.
49. Sotiropoulos, A., Gineitis, D., Copeland, J. and Treisman, R. (1999). Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169.
50. Sun, Q., Chen, G., Streb, J. W., Long, X., Yang, Y., Stoeckert, C. J., Jr and Miano, J. M. (2006). Defining the mammalian CArGome. Genome Res. 16, 197-207.
51. van der Veen, A. G. and Ploegh, H. L. (2012). Ubiquitin-like proteins. Annu. Rev. Biochem. 81, 323-357.
52. Vartiainen, M. K., Guettler, S., Larijani, B. and Treisman, R. (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752.
53. Vicente-Manzanares, M., Choi, C. K. and Horwitz, A. R. (2009). Integrins in cell migration-the actin connection. J. Cell Sci. 122, 199-206.
54. Winograd-Katz, S. E., Fässler, R., Geiger, B. and Legate, K. R. (2014). The integrin adhesome: from genes and proteins to human disease. Nat. Rev. Mol. Cell Biol. 15, 273-288.
55. Yuan, W. and Krug, R. M. (2001). Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20, 362-371.
56. Zhang, S. X., Garcia-Gras, E., Wycuff, D. R., Marriot, S. J., Kadeer, N., Yu, W., Olson, E. N., Garry, D. J., Parmacek, M. S. and Schwartz, R. J. (2005). Identification of direct serum-response factor gene targets during Me2SO-induced P19 cardiac cell differentiation. J. Biol. Chem. 280, 19115-19126.