Focal adhesion kinase controls prostate cancer progression via intrinsic kinase and scaffolding functions

Anti-Cancer Agents in Medicinal Chemistry

Volumn 11, Issue 7, 2011, Pages 607-616

  Figel, Sheila ^a   Gelman, Irwin H ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Androgen independence; FAK; Focal adhesion kinase; Prostate cancer; Tyrosine kinase

Indexed keywords

3,4 DIHYDRO 6 [[4 [[[3 (METHYLSULFONYL)PHENYL]METHYL]AMINO] 5 (TRIFLUOROMETHYL) 2 PYRIMIDINYL]AMINO] 2(1H) QUINOLINONE; ANDROGEN RECEPTOR; ANTINEOPLASTIC AGENT; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; PF 562271; PF 573228; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; ARTICLE; CANCER GROWTH; CANCER MORTALITY; CARCINOGENESIS; CATALYSIS; CELL ADHESION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; DRUG STRUCTURE; ENZYME ACTIVITY; FOCAL ADHESION; HUMAN; METASTASIS; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 80051716129     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/187152011796817646     Document Type: Article

References (115)

1. Schaller, M. D.; Borgman, C. A.; Cobb, B. S.; Vines, R. R.; Reynolds, A. B.; Parsons, J. T. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. U S A, 1992, 89, 5192-5196.
2. Hanks, S. K.; Calalb, M. B.; Harper, M. C.; Patel, S. K. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Nat.l Aca.d Sci U S A, 1992, 89, 8487-8491.
3. Schlaepfer, D. D.; Hauck, C. R.; Sieg, D. J. Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol., 1999, 71, 435-478.
4. Parsons, J. T. Focal adhesion kinase: the first ten years. J. Cell Sci., 2003, 116, 1409-1416.
5. Fiedorek, F. T.; Kay, E. S. Mapping of the focal adhesion kinase (Fadk) gene to mouse chromosome 15 and human chromosome 8. Mamm. Genome, 1995, 6, 123-126.
6. Agochiya, M.; Brunton, V. G.; Owens, D. W.; Parkinson, E. K.; Paraskeva, C.; Keith, W. N.; Frame, M. C. Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene, 1999, 18, 5646-5653.
7. Pylayeva, Y.; Gillen, K. M.; Gerald, W.; Beggs, H. E.; Reichardt, L. F.; Giancotti, F. G. Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J. Clin. Invest., 2009, 119, 252-266.
8. Golubovskaya, V.; Kaur, A.; Cance, W. Cloning and characterization of the promoter region of human focal adhesion kinase gene: nuclear factor kappa B and p53 binding sites. Biochim. Biophys. Acta, 2004, 1678, 111-125.
9. Johnson, T. R.; Khandrika, L.; Kumar, B.; Venezia, S.; Koul, S.; Chandhoke, R.; Maroni, P.; Donohue, R.; Meacham, R. B.; Koul, H. K. Focal adhesion kinase controls aggressive phenotype of androgen-independent prostate cancer. Mol. Cancer Res., 2008, 6, 1639-1648.
10. Beierle, E. A.; Trujillo, A.; Nagaram, A.; Kurenova, E. V.; Finch, R.; Ma, X.; Vella, J.; Cance, W. G.; Golubovskaya, V. M. N-MYC regulates focal adhesion kinase expression in human neuroblastoma. J. Biol. Chem., 2007, 282, 12503-12516.
11. Hao, H.; Naomoto, Y.; Bao, X.; Watanabe, N.; Sakurama, K.; Noma, K.; Motoki, T.; Tomono, Y.; Fukazawa, T.; Shirakawa, Y.; Yamatsuji, T.; Matsuoka, J.; Wang, Z. G.; Takaoka, M. Focal adhesion kinase as potential target for cancer therapy (Review). Oncol. Rep., 2009, 22, 973-979.
12. Golubovskaya, V. M.; Finch, R.; Cance, W. G. Direct interaction of the N-terminal domain of focal adhesion kinase with the Nterminal transactivation domain of p53. J. Biol. Chem., 2005, 280, 25008-25021.
13. Lietha, D.; Cai, X.; Ceccarelli, D. F.; Li, Y.; Schaller, M. D.; Eck, M. J. Structural basis for the autoinhibition of focal adhesion kinase. Cell, 2007, 129, 1177-1187.
14. Cai, X.; Lietha, D.; Ceccarelli, D. F.; Karginov, A. V.; Rajfur, Z.; Jacobson, K.; Hahn, K. M.; Eck, M. J.; Schaller, M. D. Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mo.l Cell. Biol., 2008, 28, 201-214.
15. Polte, T. R.; Hanks, S. K. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Nat.l Acad. Sci. U S A, 1995, 92, 10678-10682.
16. Schaller, M. D.; Borgman, C. A.; Parsons, J. T. Autonomous expression of a noncatalytic domain of the focal adhesionassociated protein tyrosine kinase pp125FAK. Mol. Cell. Biol., 1993, 13, 785-791.
17. Richardson, A.; Parsons, T. A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature, 1996, 380, 538-540.
18. Taylor, J. M.; Mack, C. P.; Nolan, K.; Regan, C. P.; Owens, G. K.; Parsons, J. T. Selective expression of an endogenous inhibitor of FAK regulates proliferation and migration of vascular smooth muscle cells. Mol. Cell Bio.l, 2001, 21, 1565-1572.
19. Xu, L. H.; Yang, X.; Craven, R. J.; Cance, W. G. The COOHterminal domain of the focal adhesion kinase induces loss of adhesion and cell death in human tumor cells. Cell Growth Differ., 1998, 9, 999-1005.
20. Schaller, M. D.; Parsons, J. T. Focal adhesion kinase and associated proteins. Curr Opin Cell Biol, 1994, 6, 705-710.
21. Schaller, M. D.; Otey, C. A.; Hildebrand, J. D.; Parsons, J. T. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J. Cel.l Biol., 1995, 130, 1181-1187.
22. Schaller, M. D.; Hildebrand, J. D.; Shannon, J. D.; Fox, J. W.; Vines, R. R.; Parsons, J. T. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol., 1994, 14, 1680-1688.
23. Calalb, M. B.; Polte, T. R.; Hanks, S. K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol., 1995, 15, 954-963.
24. Owen, J. D.; Ruest, P. J.; Fry, D. W.; Hanks, S. K. Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol. Cell. Biol., 1999, 19, 4806-4818.
25. Schlaepfer, D. D.; Hanks, S. K.; Hunter, T.; van der Geer, P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature, 1994, 372, 786- 791.
26. Luo, M.; Guan, J. L. Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett., 2010, 289, 127-139.
27. Cary, L. A.; Chang, J. F.; Guan, J. L. Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sc.i, 1996, 109 (Pt 7), 1787-1794.
28. Sieg, D. J.; Hauck, C. R.; Schlaepfer, D. D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci., 1999, 112 (Pt 16), 2677-2691.
29. Sieg, D. J.; Hauck, C. R.; Ilic, D.; Klingbeil, C. K.; Schaefer, E.; Damsky, C. H.; Schlaepfer, D. D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol., 2000, 2, 249-256.
30. Moissoglu, K.; Gelman, I. H. V-Src rescues actin-based cytoskeletal architecture and cell motility and induces enhanced anchorage independence during oncogenic transformation of focal adhesion kinase-null fibroblasts. J Biol. Chem., 2003, 278, 47946-47959.
31. Petit, V.; Boyer, B.; Lentz, D.; Turner, C. E.; Thiery, J. P.; Valles, A. M. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBTII cells. J. Cell. Biol., 2000, 148, 957-970.
32. Cary, L. A.; Han, D. C.; Polte, T. R.; Hanks, S. K.; Guan, J. L. Identification of p130Cas as a mediator of focal adhesion kinasepromoted cell migration. J. Cell. Biol., 1998, 140, 211-221.
33. Chu, P. Y.; Huang, L. Y.; Hsu, C. H.; Liang, C. C.; Guan, J. L.; Hung, T. H.; Shen, T. L. Tyrosine phosphorylation of growth factor receptor-bound protein-7 by focal adhesion kinase in the regulation of cell migration, proliferation, and tumorigenesis. J. Biol. Chem., 2009, 284, 20215-20226.
34. Hsia, D. A.; Mitra, S. K.; Hauck, C. R.; Streblow, D. N.; Nelson, J. A.; Ilic, D.; Huang, S.; Li, E.; Nemerow, G. R.; Leng, J.; Spencer, K. S.; Cheresh, D. A.; Schlaepfer, D. D. Differential regulation of cell motility and invasion by FAK. J. Cell Biol., 2003, 160, 753-767.
35. Sieg, D. J.; Ilic, D.; Jones, K. C.; Damsky, C. H.; Hunter, T.; Schlaepfer, D. D. Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration. EMBO J., 1998, 17, 5933-5947.
36. Ren, X. D.; Kiosses, W. B.; Schwartz, M. A. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J., 1999, 18, 578-585.
37. Ren, X. D.; Kiosses, W. B.; Sieg, D. J.; Otey, C. A.; Schlaepfer, D. D.; Schwartz, M. A. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci., 2000, 113 (Pt 20), 3673-3678.
38. Lim, Y.; Lim, S. T.; Tomar, A.; Gardel, M.; Bernard-Trifilo, J. A.; Chen, X. L.; Uryu, S. A.; Canete-Soler, R.; Zhai, J.; Lin, H.; Schlaepfer, W. W.; Nalbant, P.; Bokoch, G.; Ilic, D.; Waterman- Storer, C.; Schlaepfer, D. D. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol., 2008, 180, 187-203.
39. Lim, S. T.; Chen, X. L.; Tomar, A.; Miller, N. L.; Yoo, J.; Schlaepfer, D. D. Knock-in mutation reveals an essential role for focal adhesion kinase activity in blood vessel morphogenesis and cell motility-polarity but not cell proliferation. J. Biol. Chem., 2010, 285, 21526-21536.
40. Chang, F.; Lemmon, C. A.; Park, D.; Romer, L. H. FAK potentiates Rac1 activation and localization to matrix adhesion sites: a role for betaPIX. Mol. Biol. Cell, 2007, 18, 253-264.
41. Yano, H.; Mazaki, Y.; Kurokawa, K.; Hanks, S. K.; Matsuda, M.; Sabe, H. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol., 2004, 166, 283- 295.
42. Tilghman, R. W.; Slack-Davis, J. K.; Sergina, N.; Martin, K. H.; Iwanicki, M.; Hershey, E. D.; Beggs, H. E.; Reichardt, L. F.; Parsons, J. T. Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J. Cell Sci., 2005, 118, 2613-2623.
43. Serrels, B.; Serrels, A.; Brunton, V. G.; Holt, M.; McLean, G. W.; Gray, C. H.; Jones, G. E.; Frame, M. C. Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol,. 2007, 9, 1046-1056.
44. Mitra, S. K.; Lim, S. T.; Chi, A.; Schlaepfer, D. D. Intrinsic focal adhesion kinase activity controls orthotopic breast carcinoma metastasis via the regulation of urokinase plasminogen activator expression in a syngeneic tumor model. Oncogene, 2006, 25, 4429-4440.
45. Lahlou, H.; Sanguin-Gendreau, V.; Zuo, D.; Cardiff, R. D.; McLean, G. W.; Frame, M. C.; Muller, W. J. Mammary epithelialspecific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl. Acad. Sci. U S A, 2007, 104, 20302-20307.
46. Slack-Davis, J. K.; Hershey, E. D.; Theodorescu, D.; Frierson, H. F.; Parsons, J. T. Differential requirement for focal adhesion kinase signaling in cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol. Cancer Ther., 2009, 8, 2470-2477.
47. Zeng, Z. Z.; Jia, Y.; Hahn, N. J.; Markwart, S. M.; Rockwood, K. F.; Livant, D. L. Role of focal adhesion kinase and phosphatidylinositol 3'-kinase in integrin fibronectin receptormediated, matrix metalloproteinase-1-dependent invasion by metastatic prostate cancer cells. Cancer Res., 2006, 66, 8091-8099.
48. Zheng, Y.; Xia, Y.; Hawke, D.; Halle, M.; Tremblay, M. L.; Gao, X.; Zhou, X. Z.; Aldape, K.; Cobb, M. H.; Xie, K.; He, J.; Lu, Z. FAK phosphorylation by ERK primes ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol. Cell, 2009, 35, 11-25.
49. Moissoglu, K.; Sachdev, S.; Gelman, I. H. Enhanced v-Src-induced oncogenic transformation in the absence of focal adhesion kinase is mediated by phosphatidylinositol 3-kinase. Biochem. Biophys. Res. Commun., 2005, 330, 673-684.
50. Chan, K. T.; Cortesio, C. L.; Huttenlocher, A. FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J. Cell Biol., 2009, 185, 357-370.
51. Ilic, D.; Almeida, E. A.; Schlaepfer, D. D.; Dazin, P.; Aizawa, S.; Damsky, C. H. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J. Cell Biol., 1998, 143, 547-560.
52. Almeida, E. A.; Ilic, D.; Han, Q.; Hauck, C. R.; Jin, F.; Kawakatsu, H.; Schlaepfer, D. D.; Damsky, C. H. Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH(2)-terminal kinase. J. Cell Biol., 2000, 149, 741-754.
53. Frisch, S. M.; Vuori, K.; Ruoslahti, E.; Chan-Hui, P. Y. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol., 1996, 134, 793-799.
54. Zouq, N. K.; Keeble, J. A.; Lindsay, J.; Valentijn, A. J.; Zhang, L.; Mills, D.; Turner, C. E.; Streuli, C. H.; Gilmore, A. P. FAK engages multiple pathways to maintain survival of fibroblasts and epithelia: differential roles for paxillin and p130Cas. J. Cell Sci., 2009, 122, 357-367.
55. Lim, S. T.; Chen, X. L.; Lim, Y.; Hanson, D. A.; Vo, T. T.; Howerton, K.; Larocque, N.; Fisher, S. J.; Schlaepfer, D. D.; Ilic, D. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell, 2008, 29, 9-22.
56. Xu, L. H.; Owens, L. V.; Sturge, G. C.; Yang, X.; Liu, E. T.; Craven, R. J.; Cance, W. G. Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ., 1996, 7, 413-418.
57. Xu, L. H.; Yang, X.; Bradham, C. A.; Brenner, D. A.; Baldwin, A. S.,; Craven, R. J.; Cance, W. G. The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. Involvement of death receptor-related signaling pathways. J. Biol. Chem., 2000, 275, 30597-30604.
58. Sonoda, Y.; Kasahara, T.; Yokota-Aizu, E.; Ueno, M.; Watanabe, S. A suppressive role of p125FAK protein tyrosine kinase in hydrogen peroxide-induced apoptosis of T98G cells. Biochem. Biophys. Res. Commun., 1997, 241, 769-774.
59. Halder, J.; Landen, C. N., Jr.; Lutgendorf, S. K.; Li, Y.; Jennings, N. B.; Fan, D.; Nelkin, G. M.; Schmandt, R.; Schaller, M. D.; Sood, A. K. Focal adhesion kinase silencing augments docetaxelmediated apoptosis in ovarian cancer cells. Clin. Cancer Res., 2005, 11, 8829-8836.
60. van Nimwegen, M. J.; Huigsloot, M.; Camier, A.; Tijdens, I. B.; van de Water, B. Focal adhesion kinase and protein kinase B cooperate to suppress doxorubicin-induced apoptosis of breast tumor cells. Mol. Pharmacol., 2006, 70, 1330-1339.
61. Sonoda, Y.; Watanabe, S.; Matsumoto, Y.; Aizu-Yokota, E.; Kasahara, T. FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J. Biol. Chem., 1999, 274, 10566-10570.
62. Kurenova, E.; Xu, L. H.; Yang, X.; Baldwin, A. S., Jr.; Craven, R. J.; Hanks, S. K.; Liu, Z. G.; Cance, W. G. Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptorinteracting protein. Mol. Cell Biol., 2004, 24, 4361-4371.
63. Claesson-Welsh, L.; Welsh, M.; Ito, N.; Anand-Apte, B.; Soker, S.; Zetter, B.; O'Reilly, M.; Folkman, J. Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD. Proc. Natl. Acad. Sci U S A, 1998, 95, 5579-5583.
64. Zhao, J. H.; Reiske, H.; Guan, J. L. Regulation of the cell cycle by focal adhesion kinase. J. Cell Biol., 1998, 143, 1997-2008.
65. Ding, Q.; Grammer, J. R.; Nelson, M. A.; Guan, J. L.; Stewart, J. E.,; Gladson, C. L. P27KIP1 and cyclin D1 are necessary for focal adhesion kinase regulation of cell cycle progression in glioblastoma cells propagated in vitro and in vivo in the scid mouse brain. J. Biol. Chem., 2005, 280, 6802-6815.
66. Reiske, H. R.; Zhao, J.; Han, D. C.; Cooper, L. A.; Guan, J. L. Analysis of FAK-associated signaling pathways in the regulation of cell cycle progression. FEBS Lett, 2000, 486, 275-280.
67. Schlaepfer, D. D.; Jones, K. C.; Hunter, T. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell Biol., 1998, 18, 2571-2585.
68. Ilic, D.; Furuta, Y.; Kanazawa, S.; Takeda, N.; Sobue, K.; Nakatsuji, N.; Nomura, S.; Fujimoto, J.; Okada, M.; Yamamoto, T. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature, 1995, 377, 539-544.
69. Richardson, A.; Malik, R. K.; Hildebrand, J. D.; Parsons, J. T. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol.Cell Biol., 1997, 17, 6906-6914.
70. Schlaepfer, D. D.; Broome, M. A.; Hunter, T. Fibronectinstimulated signaling from a focal adhesion kinase-c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol. Cel.l Biol., 1997, 17, 1702-1713.
71. Bellis, S. L.; Miller, J. T.; Turner, C. E. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem., 1995, 270, 17437-17441.
72. Tachibana, K.; Urano, T.; Fujita, H.; Ohashi, Y.; Kamiguchi, K.; Iwata, S.; Hirai, H.; Morimoto, C. Tyrosine phosphorylation of Crk-associated substrates by focal adhesion kinase. A putative mechanism for the integrin-mediated tyrosine phosphorylation of Crk-associated substrates. J. Biol. Chem., 1997, 272, 29083-29090.
73. Sachdev, S.; Bu, Y.; Gelman, I. H. Paxillin-Y118 phosphorylation contributes to the control of Src-induced anchorage-independent growth by FAK and adhesion. BMC Cancer, 2009, 9, 12.
74. Karginov, A. V.; Ding, F.; Kota, P.; Dokholyan, N. V.; Hahn, K. M. Engineered allosteric activation of kinases in living cells. Nat Biotechnol., 2010, 28, 743-747.
75. Slack-Davis, J. K.; Martin, K. H.; Tilghman, R. W.; Iwanicki, M.; Ung, E. J.; Autry, C.; Luzzio, M. J.; Cooper, B.; Kath, J. C.; Roberts, W. G.; Parsons, J. T. Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem., 2007, 282, 14845-14852.
76. Roberts, W. G.; Ung, E.; Whalen, P.; Cooper, B.; Hulford, C.; Autry, C.; Richter, D.; Emerson, E.; Lin, J.; Kath, J.; Coleman, K.; Yao, L.; Martinez-Alsina, L.; Lorenzen, M.; Berliner, M.; Luzzio, M.; Patel, N.; Schmitt, E.; LaGreca, S.; Jani, J.; Wessel, M.; Marr, E.; Griffor, M.; Vajdos, F. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res., 2008, 68, 1935-1944.
77. Vuori, K.; Hirai, H.; Aizawa, S.; Ruoslahti, E. Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell Biol., 1996, 16, 2606-2613.
78. Zhao, X.; Peng, X.; Sun, S.; Park, A. Y.; Guan, J. L. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol., 2010, 189, 955-965.
79. Songyang, Z.; Blechner, S.; Hoagland, N.; Hoekstra, M. F.; Piwnica-Worms, H.; Cantley, L. C. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol., 1994, 4, 973-982.
80. Songyang, Z.; Cantley, L. C. Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem. Sci., 1995, 20, 470-475.
81. Edison, A. M.; Barker, S. C.; Kassel, D. B.; Luther, M. A.; Knight, W. B. Exploration of the sequence specificity of pp60c-src tyrosine kinase. Minimal peptide sequence required for maximal activity. J. Biol. Chem., 1995, 270, 27112-27115.
82. Lock, P.; Abram, C. L.; Gibson, T.; Courtneidge, S. A. A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J., 1998, 17, 4346-4357.
83. Amanchy, R.; Zhong, J.; Molina, H.; Chaerkady, R.; Iwahori, A.; Kalume, D. E.; Gronborg, M.; Joore, J.; Cope, L.; Pandey, A. Identification of c-Src tyrosine kinase substrates using mass spectrometry and peptide microarrays. J. Proteome Res., 2008, 7, 3900-3910.
84. Jemal, A.; Siegel, R.; Xu, J.; Ward, E. Cancer statistics, 2010. CA Cancer J Clin, 2010, 60, 277-300.
85. Golubovskaya, V. M.; Kweh, F. A.; Cance, W. G. Focal adhesion kinase and cancer. Histol. Histopathol., 2009, 24, 503-510.
86. Rovin, J. D.; Frierson, H. F., Jr.; Ledinh, W.; Parsons, J. T.; Adams, R. B. Expression of focal adhesion kinase in normal and pathologic human prostate tissues. Prostate, 2002, 53, 124-132.
87. Goldstein, A. S.; Huang, J.; Guo, C.; Garraway, I. P.; Witte, O. N. Identification of a cell of origin for human prostate cancer. Science, 2010, 329, 568-571.
88. Tremblay, L.; Hauck, W.; Aprikian, A. G.; Begin, L. R.; Chapdelaine, A.; Chevalier, S. Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int. J. Cancer, 1996, 68, 164-171.
89. Slack, J. K.; Adams, R. B.; Rovin, J. D.; Bissonette, E. A.; Stoker, C. E.; Parsons, J. T. Alterations in the focal adhesion kinase/Src signal transduction pathway correlate with increased migratory capacity of prostate carcinoma cells. Oncogene, 2001, 20, 1152- 1163.
90. McLean, G. W.; Komiyama, N. H.; Serrels, B.; Asano, H.; Reynolds, L.; Conti, F.; Hodivala-Dilke, K.; Metzger, D.; Chambon, P.; Grant, S. G.; Frame, M. C. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev., 2004, 18, 2998-3003.
91. Golubovskaya, V. M.; Zheng, M.; Zhang, L.; Li, J. L.; Cance, W. G. The direct effect of focal adhesion kinase (FAK), dominantnegative FAK, FAK-CD and FAK siRNA on gene expression and human MCF-7 breast cancer cell tumorigenesis. BMC Cancer, 2009, 9, 280.
92. Lightfoot, H. M., Jr.; Lark, A.; Livasy, C. A.; Moore, D. T.; Cowan, D.; Dressler, L.; Craven, R. J.; Cance, W. G. Upregulation of focal adhesion kinase (FAK) expression in ductal carcinoma in situ (DCIS) is an early event in breast tumorigenesis. Breast Cancer Res. Treat., 2004, 88, 109-116.
93. Greenberg, N. M.; DeMayo, F.; Finegold, M. J.; Medina, D.; Tilley, W. D.; Aspinall, J. O.; Cunha, G. R.; Donjacour, A. A.; Matusik, R. J.; Rosen, J. M. Prostate cancer in a transgenic mouse. Proc. Natl. Acad. Sci U S A, 1995, 92, 3439-3443.
94. Hiscox, S.; Barnfather, P.; Hayes, E.; Bramble, P.; Christensen, J.; Nicholson, R. I.; Barrett-Lee, P. Inhibition of focal adhesion kinase suppresses the adverse phenotype of endocrine-resistant breast cancer cells and improves endocrine response in endocrinesensitive cells. Breast Cancer Res. Treat., 2011, 125, 659-669.
95. Lim, Y.; Han, I.; Jeon, J.; Park, H.; Bahk, Y. Y.; Oh, E. S. Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J. Biol. Chem., 2004, 279, 29060-29065.
96. Desgrosellier, J. S.; Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer, 2010, 10, 9-22.
97. Cooper, C. R.; Chay, C. H.; Pienta, K. J. The role of alpha(v)beta(3) in prostate cancer progression. Neoplasia, 2002, 4, 191-194.
98. Zheng, D. Q.; Woodard, A. S.; Fornaro, M.; Tallini, G.; Languino, L. R. Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res., 1999, 59, 1655-1664.
99. Feldman, B. J.; Feldman, D. The development of androgenindependent prostate cancer. Nat Rev Cancer, 2001, 1, 34-45.
100. Sun, Y.; Niu, J.; Huang, J. Neuroendocrine differentiation in prostate cancer. Am. J. Transl. Res., 2009, 1, 148-162.
101. Aprikian, A. G.; Tremblay, L.; Han, K.; Chevalier, S. Bombesin stimulates the motility of human prostate-carcinoma cells through tyrosine phosphorylation of focal adhesion kinase and of integrinassociated proteins. Int J Cancer, 1997, 72, 498-504.
102. Lee, L. F.; Guan, J.; Qiu, Y.; Kung, H. J. Neuropeptide-induced androgen independence in prostate cancer cells: roles of nonreceptor tyrosine kinases Etk/Bmx, Src, and focal adhesion kinase. Mol. Cell Biol., 2001, 21, 8385-8397.
103. Sumitomo, M.; Shen, R.; Walburg, M.; Dai, J.; Geng, Y.; Navarro, D.; Boileau, G.; Papandreou, C. N.; Giancotti, F. G.; Knudsen, B.; Nanus, D. M. Neutral endopeptidase inhibits prostate cancer cell migration by blocking focal adhesion kinase signaling. J. Clin. Invest., 2000, 106, 1399-1407.
104. Lacoste, J.; Aprikian, A. G.; Chevalier, S. Focal adhesion kinase is required for bombesin-induced prostate cancer cell motility. Mol. Cell. Endocrinol., 2005, 235, 51-61.
105. Dai, B.; Chen, H.; Guo, S.; Yang, X.; Linn, D. E.; Sun, F.; Li, W.; Guo, Z.; Xu, K.; Kim, O.; Kong, X.; Melamed, J.; Qiu, S.; Qiu, Y. Compensatory upregulation of tyrosine kinase Etk/BMX in response to androgen deprivation promotes castration-resistant growth of prostate cancer cells. Cancer Res., 2010, 70, 5587-5596.
106. Lee, L. F.; Louie, M. C.; Desai, S. J.; Yang, J.; Chen, H. W.; Evans, C. P.; Kung, H. J. Interleukin-8 confers androgenindependent growth and migration of LNCaP: differential effects of tyrosine kinases Src and FAK. Oncogene, 2004, 23, 2197-2205.
107. Tamura, M.; Gu, J.; Matsumoto, K.; Aota, S.; Parsons, R.; Yamada, K. M. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science, 1998, 280, 1614-1617.
108. Tamura, M.; Gu, J.; Danen, E. H.; Takino, T.; Miyamoto, S.; Yamada, K. M. PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem., 1999, 274, 20693-20703.
109. Senapati, S.; Rachagani, S.; Chaudhary, K.; Johansson, S. L.; Singh, R. K.; Batra, S. K. Overexpression of macrophage inhibitory cytokine-1 induces metastasis of human prostate cancer cells through the FAK-RhoA signaling pathway. Oncogene, 2010, 29, 1293-1302.
110. Liu, W.; Bloom, D. A.; Cance, W. G.; Kurenova, E. V.; Golubovskaya, V. M.; Hochwald, S. N. FAK and IGF-IR interact to provide survival signals in human pancreatic adenocarcinoma cells. Carcinogenesis, 2008, 29, 1096-1107.
111. Benlimame, N.; He, Q.; Jie, S.; Xiao, D.; Xu, Y. J.; Loignon, M.; Schlaepfer, D. D.; Alaoui-Jamali, M. A. FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J. Cell Biol., 2005, 171, 505-516.
112. Di Lorenzo, G.; Tortora, G.; D'Armiento, F. P.; De Rosa, G.; Staibano, S.; Autorino, R.; D'Armiento, M.; De Laurentiis, M.; De Placido, S.; Catalano, G.; Bianco, A. R.; Ciardiello, F. Expression of epidermal growth factor receptor correlates with disease relapse and progression to androgen-independence in human prostate cancer. Clin Cancer Res., 2002, 8, 3438-3444.
113. Lorenzo, G. D.; Bianco, R.; Tortora, G.; Ciardiello, F. Involvement of growth factor receptors of the epidermal growth factor receptor family in prostate cancer development and progression to androgen independence. Clin Prostate Cancer, 2003, 2, 50-57.
114. Nickerson, T.; Chang, F.; Lorimer, D.; Smeekens, S. P.; Sawyers, C. L.; Pollak, M. In vivo progression of LAPC-9 and LNCaP prostate cancer models to androgen independence is associated with increased expression of insulin-like growth factor I (IGF-I) and IGF-I receptor (IGF-IR). Cancer Res., 2001, 61, 6276-6280.
115. Craft, N.; Shostak, Y.; Carey, M.; Sawyers, C. L. A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat. Med., 1999, 5, 280-285.