Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling

Journal of Clinical Investigation

Volumn 119, Issue 2, 2009, Pages 252-266

  Pylayeva, Yuliya ^a,b,d   Gillen, Kelly M ^a,b   Gerald, William ^a   Beggs, Hilary E ^c   Reichardt, Louis F ^c   Giancotti, Filippo G ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FOCAL ADHESION KINASE; MESSENGER RNA; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; RAS PROTEIN; BCAR1 PROTEIN, MOUSE; VIRUS T ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; BREAST TUMOR; CANCER GROWTH; CANCER INHIBITION; CELL AGING; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; GENE AMPLIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC CODE; HUMAN; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CANCER INVASION; ENZYMOLOGY; EXPERIMENTAL NEOPLASM; LUNG TUMOR; METASTASIS; ONCOGENE RAS; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; BREAST NEOPLASMS; CELL AGING; CRK-ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENES, RAS; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION;

EID: 61749094852     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI37160     Document Type: Article

References (60)

1. Weinstein, I.B. 2002. Cancer. Addiction to oncogenes - the Achilles heal of cancer. Science. 297:63-64.
2. Forbes, S., et al. 2006. Cosmic 2005. Br. J. Cancer. 94:318-322.
3. Saal, L.H., et al. 2005. PIK3CA mutations correlate with hormone receptors, node metastasis, and ERBB2, and are mutually exclusive with PTEN loss in human breast carcinoma. Cancer Res. 65:2554-2559.
4. Carpten, J.D., et al. 2007. A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature. 448:439-444.
5. Elenbaas, B., et al. 2001. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15:50-65.
6. Zhao, J.J., et al. 2005. The oncogenic properties of mutant p110alpha and p110beta phosphatidylinositol 3-kinases in human mammary epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 102:18443-18448.
7. Giancotti, F.G., and Tarone, G. 2003. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell Dev. Biol. 19:173-206.
8. Guo, W., et al. 2006. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell. 126:489-502.
9. Schwartz, M.A. 1997. Integrins, oncogenes, and anchorage independence. J. Cell Biol. 139:575-578.
10. Hood, J.D., and Cheresh, D.A. 2002. Role of integrins in cell invasion and migration. Nat. Rev. Cancer. 2:91-100.
11. Guo, W., and Giancotti, F.G. 2004. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5:816-826.
12. White, D.E., et al. 2004. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell. 6:159-170.
13. Parsons, J.T. 2003. Focal adhesion kinase: the first ten years. J. Cell. Sci. 116:1409-1416.
14. 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.
15. Ilic, D., et al. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 377:539-544.
16. Schober, M., et al. 2007. Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J. Cell Biol. 176:667-680.
17. Beggs, H.E., et al. 2003. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron. 40:501-514.
18. Shen, T.L., et al. 2005. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169:941-952.
19. Lim, Y., et al. 2008. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol. 180:187-203.
20. Weis, S.M., et al. 2008. Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J. Cell Biol. 181:43-50.
21. Pirone, D.M., et al. 2006. An inhibitory role for FAK in regulating proliferation: a link between limited adhesion and RhoA-ROCK signaling. J. Cell Biol. 174:277-288.
22. Lim, S.T., et al. 2008. Nuclear FAK promotes cell proliferation and survival through FERMenhanced p53 degradation. Mol. Cell. 29:9-22.
23. Hauck, C.R., Hsia, D.A., Puente, X.S., Cheresh, D.A., and Schlaepfer, D.D. 2002. FRNK blocks v-Srcstimulated invasion and experimental metastases without effects on cell motility or growth. EMBO J. 21:6289-6302.
24. Hsia, D.A., et al. 2003. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 160:753-767.
25. McLean, G.W., et al. 2004. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev. 18:2998-3003.
26. Lahlou, H., et al. 2007. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl. Acad. Sci. U. S. A. 104:20302-20307.
27. Benlimame, N., et al. 2005. FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J. Cell Biol. 171:505-516.
28. Mitra, S.K., Lim, S.T., Chi, A., and Schlaepfer, D.D. 2006. Intrinsic focal adhesion kinase activity controls orthotopic breast carcinoma metastasis via the regulation of urokinase plasminogen activator expression in a syngeneic tumor model. Oncogene. 25:4429-4440.
29. Watermann, D.O., et al. 2005. Specific induction of pp125 focal adhesion kinase in human breast cancer. Br. J. Cancer. 93:694-698.
30. Madan, R., Smolkin, M.B., Cocker, R., Fayyad, R., and Oktay, M.H. 2006. Focal adhesion proteins as markers of malignant transformation and prognostic indicators in breast carcinoma. Hum. Pathol. 37:9-15.
31. Jain, A.N., et al. 2001. Quantitative analysis of chromosomal CGH in human breast tumors associates copy number abnormalities with p53 status and patient survival. Proc. Natl. Acad. Sci. U. S. A. 98:7952-7957.
32. Naylor, T.L., et al. 2005. High resolution genomic analysis of sporadic breast cancer using array-based comparative genomic hybridization. Breast Cancer Res. 7:R1186-R1198.
33. Chang, H.Y., et al. 2005. Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc. Natl. Acad. Sci. U. S. A. 102:3738-3743.
34. Wagner, K.U., et al. 2001. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res. 10:545-553.
35. Klingbeil, C.K., et al. 2001. Targeting Pyk2 to beta 1-integrin- containing focal contacts rescues fibronectin-stimulated signaling and haptotactic motility defects of focal adhesion kinase-null cells. J. Cell Biol. 152:97-110.
36. Nagy, T., et al. 2007. Mammary epithelial-specific deletion of the focal adhesion kinase gene leads to severe lobulo-alveolar hypoplasia and secretory immaturity of the murine mammary gland. J. Biol. Chem. 282:31766-31776.
37. Lin, E.Y., et al. 2003. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 163:2113-2126.
38. Maglione, J.E., et al. 2001. Transgenic Polyoma middle-T mice model premalignant mammary disease. Cancer Res. 61:8298-8305.
39. Kouros-Mehr, H., et al. 2008. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell. 13:141-152.
40. Blasberg, R.G., and Tjuvajev, J.G. 2003. Moleculargenetic imaging: current and future perspectives. J. Clin. Invest. 111:1620-1629.
41. Chodniewicz, D., and Klemke, R.L. 2004. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim. Biophys. Acta. 1692:63-76.
42. Neve, R.M., et al. 2006. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 10:515-527.
43. Konecny, G.E., et al. 2006. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res. 66:1630-1639.
44. Mariotti, A., et al. 2001. EGF-R signaling through Fyn kinase disrupts the function of integrin alpha-6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J. Cell Biol. 155:447-458.
45. Campisi, J., and d'Adda di Fagagna, F. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
46. Reya, T., Morrison, S.J., Clarke, M.F., and Weissman, I.L. 2001. Stem cells, cancer, and cancer stem cells. Nature. 414:105-111.
47. Honda, H., et al. 1998. Cardiovascular anomaly, impaired actin bundling and resistance to Srcinduced transformation in mice lacking p130Cas. Nat. Genet. 19:361-365.
48. Cabodi, S., et al. 2006. p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res. 66:4672-4680.
49. Feller, S.M., Ren, R., Hanafusa, H., and Baltimore, D. 1994. SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Abl. Trends Biochem. Sci. 19:453-458.
50. Sawada, Y., et al. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell. 127:1015-1026.
51. Paszek, M.J., et al. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8:241-254.
52. Wozniak, M.A., Desai, R., Solski, P.A., Der, C.J., and Keely, P.J. 2003. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163:583-595.
53. Sarkisian, C.J., et al. 2007. Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat. Cell Biol. 9:493-505.
54. Olsen, C.L., Gardie, B., Yaswen, P., and Stampfer, M.R. 2002. Raf-1-induced growth arrest in human mammary epithelial cells is p16-independent and is overcome in immortal cells during conversion. Oncogene. 21:6328-6339.
55. Solimini, N.L., Luo, J., and Elledge, S.J. 2007. Nononcogene addiction and the stress phenotype of cancer cells. Cell. 130:986-988.
56. Guy, C.T., Cardiff, R.D., and Muller, W.J. 1992. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12:954-961.
57. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70-71.
58. Walker, R.A., et al. 2008. HER2 testing in the UK: further update to recommendations. J. Clin. Pathol. 61:818-824.
59. Ory, D.S., Neugeboren, B.A., and Mulligan, R.C. 1996. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc. Natl. Acad. Sci. U. S. A. 93:11400-11406.
60. Provenzano, P.P., Inman, D.R., Eliceiri, K.W., Beggs, H.E., and Keely, P.J. 2008. Mammary epithelial-specific disruption of focal adhesion kinase retards tumor formation and metastasis in a transgenic mouse model of human breast cancer. Am. J. Pathol. 173:1551-1565.