Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis

Advanced Drug Delivery Reviews

Volumn 63, Issue 8, 2011, Pages 610-615

  Zhao, Xiaofeng ^a   Guan, Jun Lin ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis; Cancer; Cell migration; FAK; Signal transduction

Indexed keywords

ANGIOGENESIS; CANCER; CANCER CELLS; CANCER PROGRESSION; CELL MIGRATION; CELL SURFACE RECEPTORS; CELLULAR FUNCTION; CULTURED CELL; CYTOPLASMIC TYROSINE KINASE; EMBRYONIC DEVELOPMENT; FAK; FOCAL ADHESION KINASE; HUMAN CANCER; INTRAMOLECULAR INTERACTIONS; KINASE ACTIVITY; KINASE DOMAINS; KINASE-INDEPENDENT FUNCTIONS; KNOCKOUT MICE; METASTATIC CANCERS; MOLECULAR INHIBITORS; SIGNALING PATHWAYS; SRC-FAMILY KINASE;

ADHESION; AMINO ACIDS; BACTERIOPHAGES; CELL ADHESION; CELL CULTURE; CELL MEMBRANES; DISEASE CONTROL; DISEASES; ENDOTHELIAL CELLS; MAMMALS; MOLECULAR STRUCTURE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SIGNALING;

ENZYMES;

2 [5 CHLORO 2 (2 METHOXY 4 MORPHOLINOANILINO) 4 PYRIMIDINYLAMINO] N METHYLBENZAMIDE; FOCAL ADHESION KINASE; INTEGRIN;

ANGIOGENESIS; CANCER CELL; CANCER GROWTH; CELL MIGRATION; CRYSTAL STRUCTURE; DRUG TARGETING; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; FAK GENE; FIBROBLAST; GENE CONTROL; GENE FUNCTION; HUMAN; KNOCKOUT MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTEGRINS; MICE; MICE, KNOCKOUT; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION;

EID: 79959971564     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2010.11.001     Document Type: Review

References (93)

1. Erickson C.A. Cell migration in the embryo and adult organism. Curr. Opin. Cell Biol. 1990, 2(1):67-74.
2. Stoker M., Gherardi E. Regulation of cell movement: the motogenic cytokines. Biochim. Biophys. Acta 1991, 1072(1):81-102.
3. Ridley A.J., et al. Cell migration: integrating signals from front to back. Science 2003, 302(5651):1704-1709.
4. Lauffenburger D.A., Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 1996, 84(3):359-369.
5. Hynes R. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110(6):673-687.
6. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell Sci. 2003, 116(Pt 8):1409-1416.
7. Schlaepfer D.D., Mitra S.K. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 2004, 14(1):92-101.
8. Siesser P.M., Hanks S.K. The signaling and biological implications of FAK overexpression in cancer. Clin. Cancer Res. 2006, 12(11 Pt 1):3233-3237.
9. Schaller M.D. Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 2001, 1540(1):1-21.
10. Cohen L.A., Guan J.L. Mechanisms of focal adhesion kinase regulation. Curr. Cancer Drug Targets 2005, 5(8):629-643.
11. Guan J.L., Trevithick J.E., Hynes R.O. Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 1991, 2(11):951-964.
12. Kornberg L.J., et al. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins. Proc. Natl Acad. Sci. USA 1991, 88(19):8392-8396.
13. Kanner S.B., et al. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc. Natl Acad. Sci. USA 1990, 87(9):3328-3332.
14. Schaller M.D., et al. pp 125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl Acad. Sci. USA 1992, 89(11):5192-5196.
15. Guan J.L., Shalloway D. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 1992, 358(6388):690-692.
16. Golubovskaya V.M., Cance W.G. Focal adhesion kinase and p53 signaling in cancer cells. Int. Rev. Cytol. 2007, 263:103-153.
17. McLean G.W., et al. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer 2005, 5(7):505-515.
18. Zhao J., Guan J.L. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 2009, 28(1-2):35-49.
19. Lim S.T., et al. FERM control of FAK function: implications for cancer therapy. Cell Cycle 2008, 7(15):2306-2314.
20. Parsons J.T., et al. Focal adhesion kinase: targeting adhesion signaling pathways for therapeutic intervention. Clin. Cancer Res. 2008, 14(3):627-632.
21. Hanks S.K., et al. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl Acad. Sci. USA 1992, 89(18):8487-8491.
22. Andre E., Becker-Andre M. Expression of an N-terminally truncated form of human focal adhesion kinase in brain. Biochem. Biophys. Res. Commun. 1993, 190(1):140-147.
23. Zhang X., Wright C.V., Hanks S.K. Cloning of a Xenopus laevis cDNA encoding focal adhesion kinase (FAK) and expression during early development. Gene 1995, 160(2):219-222.
24. 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(2):123-126.
25. Chishti A.H., et al. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci. 1998, 23(8):281-282.
26. Girault J.A., et al. The N-termini of FAK and JAKs contain divergent band 4.1 domains. Trends Biochem. Sci. 1999, 24(2):54-57.
27. Chen R., et al. Regulation of the PH-domain-containing tyrosine kinase Etk by focal adhesion kinase through the FERM domain. Nat. Cell Biol. 2001, 3(5):439-444.
28. Golubovskaya V., et al. Dual inhibition of focal adhesion kinase and epidermal growth factor receptor pathways cooperatively induces death receptor-mediated apoptosis in human breast cancer cells. J. Biol. Chem. 2002, 277(41):38978-38987.
29. Poullet P., et al. Ezrin interacts with focal adhesion kinase and induces its activation independently of cell-matrix adhesion. J. Biol. Chem. 2001, 276(40):37686-37691.
30. Schaller M.D., et al. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J. Cell Biol. 1995, 130(5):1181-1187.
31. Sieg D.J., et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2000, 2(5):249-256.
32. Cooper L.A., Shen T.L., Guan J.L. Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol. Cell. Biol. 2003, 23(22):8030-8041.
33. Cohen L.A., Guan J.L. Residues within the first subdomain of the FERM-like domain in focal adhesion kinase are important in its regulation. J. Biol. Chem. 2005, 280(9):8197-8207.
34. Lietha D., et al. Structural basis for the autoinhibition of focal adhesion kinase. Cell 2007, 129(6):1177-1187.
35. Polte T.R., Hanks S.K. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Natl Acad. Sci. USA 1995, 92(23):10678-10682.
36. Wu X., et al. FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell 2005, 9(2):185-196.
37. Hildebrand J.D., Taylor J.M., Parsons J.T. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell. Biol. 1996, 16(6):3169-3178.
38. Liu Y., et al. The association of ASAP1, an ADP ribosylation factor-GTPase activating protein, with focal adhesion kinase contributes to the process of focal adhesion assembly. Mol. Biol. Cell 2002, 13(6):2147-2156.
39. Klemke R.L., et al. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 1998, 140(4):961-972.
40. Liu Y., et al. Mislocalization or reduced expression of Arf GTPase-activating protein ASAP1 inhibits cell spreading and migration by influencing Arf1 GTPase cycling. J. Biol. Chem. 2005, 280(10):8884-8892.
41. Dunty J.M., et al. FERM domain interaction promotes FAK signaling. Mol. Cell. Biol. 2004, 24(12):5353-5368.
42. Romer L.H., et al. Tyrosine kinase activity, cytoskeletal organization, and motility in human vascular endothelial cells. Mol. Biol. Cell 1994, 5(3):349-361.
43. Gates R.E., et al. Potential role for focal adhesion kinase in migrating and proliferating keratinocytes near epidermal wounds and in culture. Cell Growth Differ. 1994, 5(8):891-899.
44. Weiner T.M., et al. Expression of focal adhesion kinase gene and invasive cancer. Lancet 1993, 342(8878):1024-1025.
45. Owens L.V., et al. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 1995, 55(13):2752-2755.
46. Ilic D., et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995, 377(6549):539-544.
47. Gilmore A.P., Romer L.H. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell 1996, 7(8):1209-1224.
48. 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 Sci. 1996, 109(Pt 7):1787-1794.
49. 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.
50. Owen J.D., et al. 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(7):4806-4818.
51. Cary L.A., et al. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 1998, 140(1):211-221.
52. 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. 2000, 149(1):223-236.
53. Cheresh D.A., Leng J., Klemke R.L. Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J. Cell Biol. 1999, 146(5):1107-1116.
54. Turner C.E. Paxillin interactions. J. Cell Sci. 2000, 113(Pt 23):4139-4140.
55. Turner C.E., et al. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat. ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 1999, 145(4):851-863.
56. West K.A., et al. The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J. Cell Biol. 2001, 154(1):161-176.
57. Han D.C., Guan J.L. Association of focal adhesion kinase with Grb7 and its role in cell migration. J. Biol. Chem. 1999, 274(34):24425-24430.
58. Han D.C., Shen T.L., Guan J.L. Role of Grb7 targeting to focal contacts and its phosphorylation by focal adhesion kinase in regulation of cell migration. J. Biol. Chem. 2000, 275(37):28911-28917.
59. Reiske H.R., et al. Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration. J. Biol. Chem. 1999, 274(18):12361-12366.
60. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 2005, 6(1):56-68.
61. Shen T.L., Han D.C., Guan J.L. Association of grb7 with phosphoinositides and its role in the regulation of cell migration. J. Biol. Chem. 2002, 277(32):29069-29077.
62. Ren X.D., et al. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 2000, 113(Pt 20):3673-3678.
63. Hsia D.A., et al. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 2003, 160(5):753-767.
64. Chen B.H., et al. Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J. Biol. Chem. 2002, 277(37):33857-33863.
65. Zhai J., et al. Direct interaction of focal adhesion kinase with p190RhoGEF. J. Biol. Chem. 2003, 278(27):24865-24873.
66. Lim Y., et al. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol. 2008, 180(1):187-203.
67. Wu X., et al. Focal adhesion kinase regulation of N-WASP subcellular localization and function. J. Biol. Chem. 2004, 279(10):9565-9576.
68. Shibata K., et al. Both focal adhesion kinase and c-Ras are required for the enhanced matrix metalloproteinase 9 secretion by fibronectin in ovarian cancer cells. Cancer Res. 1998, 58(5):900-903.
69. Polte T.R., Naftilan A.J., Hanks S.K. Focal adhesion kinase is abundant in developing blood vessels and elevation of its phosphotyrosine content in vascular smooth muscle cells is a rapid response to angiotensin II. J. Cell. Biochem. 1994, 55(1):106-119.
70. Qi J.H., Claesson-Welsh L. VEGF-induced activation of phosphoinositide 3-kinase is dependent on focal adhesion kinase. Exp. Cell Res. 2001, 263(1):173-182.
71. Kim I., et al. Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ. Res. 2000, 86(9):952-959.
72. Brooks P.C., Clark R.A., Cheresh D.A. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 1994, 264(5158):569-571.
73. Brooks P.C., et al. Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J. Clin. Invest. 1995, 96(4):1815-1822.
74. Eliceiri B.P., Cheresh D.A. The role of alphav integrins during angiogenesis: insights into potential mechanisms of action and clinical development. J. Clin. Invest. 1999, 103(9):1227-1230.
75. Eliceiri B.P., et al. Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signaling. J. Cell Biol. 2002, 157(1):149-160.
76. Peng X., et al. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc. Res. 2004, 64(3):421-430.
77. Shen T.L., et al. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 2005, 169(6):941-952.
78. Braren R., et al. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 2006, 172(1):151-162.
79. Corsi J.M., et al. Autophosphorylation-independent and -dependent functions of focal adhesion kinase during development. J. Biol. Chem. 2009, 284(50):34769-34776.
80. Lim S.T., et al. 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(28):21526-21536.
81. Gabarra-Niecko V., Schaller M.D., Dunty J.M. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 2003, 22(4):359-374.
82. Mitra S.K., et al. Intrinsic FAK activity and Y925 phosphorylation facilitate an angiogenic switch in tumors. Oncogene 2006, 25(44):5969-5984.
83. Hauck C.R., Hsia D.A., Schlaepfer D.D. The focal adhesion kinase-a regulator of cell migration and invasion. IUBMB Life 2002, 53(2):115-119.
84. Hanks S.K., et al. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front. Biosci. 2003, 8:d982-d996.
85. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 2006, 18(5):516-523.
86. Lim S.T., et al. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell 2008, 29(1):9-22.
87. Zhao X., et al. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol. 2010, 189(6):955-965.
88. Liotta L.A., Kleinerman J., Saidel G.M. Quantitative relationships of intravascular tumor cells, tumor vessels, and pulmonary metastases following tumor implantation. Cancer Res. 1974, 34(5):997-1004.
89. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2(8):563-572.
90. Roberts W.G., et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562, 271. Cancer Res. 2008, 68(6):1935-1944.
91. Shi Q., et al. A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol. Carcinog. 2007, 46(6):488-496.
92. Slack-Davis J.K., et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 2007, 282(20):14845-14852.
93. Halder J., et al. Therapeutic efficacy of a novel focal adhesion kinase inhibitor TAE226 in ovarian carcinoma. Cancer Res. 2007, 67(22):10976-10983.