An integrin α v Β 3-c-Src oncogenic unit promotes anchorage-independence and tumor progression

Nature Medicine

Volumn 15, Issue 10, 2009, Pages 1163-1169

  Desgrosellier, Jay S ^a   Barnes, Leo A ^a   Shields, David J ^a   Huang, Miller ^a   Lau, Steven K ^a   Prévost, Nicolas ^b   Tarin, David ^a   Shattil, Sanford J ^b   Cheresh, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; DASATINIB; FOCAL ADHESION KINASE; IMATINIB; PROTEIN TYROSINE KINASE; VITRONECTIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER INVASION; CARCINOMA CELL; CELL ANCHORAGE; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; ONCOGENE SRC; PANCREAS ADENOCARCINOMA; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUMOR GROWTH; TUMOR PROMOTION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CARCINOMA; CELL ADHESION; CELL PROLIFERATION; FEMALE; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GREEN FLUORESCENT PROTEINS; HUMANS; IN SITU NICK-END LABELING; INTEGRIN ALPHAVBETA3; KI-67 ANTIGEN; LYMPHATIC METASTASIS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; PROTEIN-TYROSINE KINASES; RNA, SMALL INTERFERING; SUBSTRATE SPECIFICITY; TIME FACTORS; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 70350574674     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2009     Document Type: Article

References (49)

1. Guo, W. & Giancotti, F.G. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5, 816-826 (2004).
2. Schlaepfer, D.D., Mitra, S.K. & Ilic, D. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692, 77-102 (2004).
3. Roberts, W.G. et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 68, 1935-1944 (2008).
4. Pylayeva, Y. et al. Ras-and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J. Clin. Invest. 119, 252-266 (2009).
5. Lahlou, H. et al. Mammary epithelial-specifc disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl. Acad. Sci. USA 104, 20302-20307 (2007).
6. Eide, B.L., Turck, C.W. & Escobedo, J.A. Identifcation of Tyr-397 as the primary site of tyrosine phosphorylation and pp60Src association in the focal adhesion kinase, pp125FAK. Mol. Cell. Biol. 15, 2819-2827 (1995).
7. Ishizawar, R. & Parsons, S.J. c-Src and cooperating partners in human cancer. Cancer Cell 6, 209-214 (2004).
8. Brábek, J. et al. Crk-associated substrate tyrosine phosphorylation sites are critical for invasion and metastasis of SRC-transformed cells. Mol. Cancer Res. 3, 307-315 (2005).
9. Klemke, R.L. et al. CAS/Crk coupling serves as a 'molecular switch' for induction of cell migration. J. Cell Biol. 140, 961-972 (1998).
10. Cho, S.Y. & Klemke, R.L. Extracellular-regulated kinase activation and CAS/Crk coupling regulate cell migration and suppress apoptosis during invasion of the extracellular matrix. J. Cell Biol. 149, 223-236 (2000).
11. Albelda, S.M. et al. Integrin distribution in malignant melanoma: association of the p3 subunit with tumor progression. Cancer Res. 50, 6757-6764 (1990).
12. Hsu, M.Y. et al. Adenoviral gene transfer of p3 integrin subunit induces conversion from radial to vertical growth phase in primary human melanoma. Am. J. Pathol. 153, 1435-1442 (1998).
13. McCabe, N.P., De, S., Vasanji, A., Brainard, J. & Byzova, T.V. Prostate cancer specifc integrin avp3 modulates bone metastatic growth and tissue remodeling. Oncogene 26, 6238-6243 (2007).
14. Takayama, S. et al. The relationship between bone metastasis from human breast cancer and integrin avp3 expression. Anticancer Res. 25, 79-83 (2005).
15. Sloan, E.K. et al. Tumor-specifc expression of avp3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res. 8, R20 (2006).
16. Felding-Habermann, B. et al. Integrin activation controls metastasis in human breast cancer. Proc. Natl. Acad. Sci. USA 98, 1853-1858 (2001).
17. Gruber, G. et al. Correlation between the tumoral expression of p3-integrin and outcome in cervical cancer patients who had undergone radiotherapy. Br. J. Cancer 92, 41-46 (2005).
18. Hosotani, R. et al. Expression of integrin avp3 in pancreatic carcinoma: relation to MMP-2 activation and lymph node metastasis. Pancreas 25, e30-e35 (2002).
19. Giancotti, F.G. & Ruoslahti, E. Elevated levels of the a5p1 fbronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell 60, 849-859 (1990).
20. Varner, J.A., Emerson, D.A. & Juliano, R.L. Integrin a5p1 expression negatively regulates cell growth: reversal by attachment to fbronectin. Mol. Biol. Cell 6, 725-740 (1995).
21. Stupack, D.G., Puente, X.S., Boutsaboualoy, S., Storgard, CM. & Cheresh, D.A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J. Cell Biol. 155, 459-470 (2001).
22. Stupack, D.G. et al. Potentiation of neuroblastoma metastasis by loss of caspase-8. Nature 439, 95-99 (2006).
23. Ginsberg, M.H., Partridge, A. & Shattil, S.J. Integrin regulation. Curr. Opin. Cell Biol. 17, 509-516 (2005).
24. Arias-Salgado, E.G. et al. Src kinase activation by direct interaction with the integrin p cytoplasmic domain. Proc. Natl. Acad. Sci. USA 100, 13298-13302 (2003).
25. Tsatsanis, C. & Spandidos, D.A. Oncogenic kinase signaling in human neoplasms. Ann. NY Acad. Sci. 1028, 168-175 (2004).
26. Simpson, CD., Anyiwe, K. & Schimmer, A.D. Anoikis resistance and tumor metastasis. Cancer Lett. 272, 177-185 (2008).
27. Leavesley, D.I., Ferguson, G.D., Wayner, E.A. & Cheresh, D.A. Requirement of the integrin p3 subunit for carcinoma cell spreading or migration on vitronectin and fbrinogen. J. Cell Biol. 117, 1101-1107 (1992).
28. Miyauchi, A. et al. Recognition of osteopontin and related peptides by an a5p3 integrin stimulates immediate cell signals in osteoclasts. J. Biol. Chem. 266, 20369-20374 (1991).
29. 3 integrin mutation abolishes ligand binding and alters divalent cation-dependent conformation. Science 249, 915-918 (1990).
30. Shin, N.Y. et al. Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are suffcient to promote cell migration. J. Biol. Chem. 279, 38331-38337 (2004).
31. Summy, J.M. & Gallick, G.E. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 22, 337-358 (2003).
32. Reddig, P.J. & Juliano, R.L. Clinging to life: cell to matrix adhesion and cell survival. Cancer Metastasis Rev. 24, 425-439 (2005).
33. Westhoff, M.A., Serrels, B., Fincham, V.J., Frame, M.C. & Carragher, N.O. SRC-mediated phosphorylation of focal adhesion kinase couples actin and adhesion dynamics to survival signaling. Mol. Cell. Biol. 24, 8113-8133 (2004).
34. Uhm, J.H., Dooley, N.P., Kyritsis, A.P., Rao, J.S. & Gladson, C.L. Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin. Cancer Res. 5, 1587-1594 (1999).
35. De, S. et al. VEGF-integrin interplay controls tumor growth and vascularization. Proc. Natl. Acad. Sci. USA 102, 7589-7594 (2005).
36. Matter, M.L. & Ruoslahti, E. A signaling pathway from the a5p1 and avp3 integrins that elevates bcl-2 transcription. J. Biol. Chem. 276, 27757-27763 (2001).
37. Bao, W. & Stromblad, S. Integrin av-mediated inactivation of p53 controls a MEK1-dependent melanoma cell survival pathway in three-dimensional collagen. J. Cell Biol. 167, 745-756 (2004).
38. Scatena, M. et al. NF-kappaB mediates avp3 integrin-induced endothelial cell survival. J. Cell Biol. 141, 1083-1093 (1998).
39. Charo, I.F., Nannizzi, L., Smith, J.W. & Cheresh, D.A. The vitronectin receptor αvβ3 binds fbronectin and acts in concert with α5β1 in promoting cellular attachment and spreading on fbronectin. J. Cell Biol. 111, 2795-2800 (1990).
40. Cabodi, S. et al. p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res. 66, 4672-4680 (2006).
41. Bouton, A.H., Riggins, R.B. & Bruce-Staskal, P.J. Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene 20, 6448-6458 (2001).
42. Sakai, R. et al. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13, 3748-3756 (1994).
43. Honda, H. et al. Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat. Genet. 19, 361-365 (1998).
44. Jove, R. & Hanafusa, H. Cell transformation by the viral Src oncogene. Annu. Rev. Cell Biol. 3, 31-56 (1987).
45. Huveneers, S. et al. Integrin a5 p3 controls activity and oncogenic potential of primed c-Src. Cancer Res. 67, 2693-2700 (2007).
46. Huveneers, S., Arslan, S., van de Water, B., Sonnenberg, A. & Danen, E.H. Integrins uncouple Src-induced morphological and oncogenic transformation. J. Biol. Chem. 283, 13243-13251 (2008).
47. Nip, J., Shibata, H., Loskutoff, D.J., Cheresh, D.A. & Brodt, P. Human melanoma cells derived from lymphatic metastases use integrin a5 p3 to adhere to lymph node vitronectin. J. Clin. Invest. 90, 1406-1413 (1992).
48. Allan, A.L. et al. Role of the integrin-binding protein osteopontin in lymphatic metastasis of breast cancer. Am. J. Pathol. 169, 233-246 (2006).
49. Reinmuth, N. et al. avp3 integrin antagonist S247 decreases colon cancer metastasis and angiogenesis and improves survival in mice. Cancer Res. 63, 2079-2087 (2003)