New concepts regarding focal adhesion kinase promotion of cell migration and proliferation

Journal of Cellular Biochemistry

Volumn 99, Issue 1, 2006, Pages 35-52

  Cox, Braden D ^a,b   Natarajan, Meera ^a,c   Stettner, Michelle R ^a,d   Gladson, Candece L ^a,b  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^d EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

CAS; FAK; Focal adhesion kinase; HEF1; Migration; Proliferation

Indexed keywords

ADAPTOR PROTEIN; CELL PROTEIN; CRK ASSOCIATED SUBSTRATE PROTEIN; CRK PROTEIN; CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FOCAL ADHESION KINASE; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; INTEGRIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN INHIBITOR; PROTEIN P53; PROTEIN TYROSINE KINASE; STEROID RECEPTOR COACTIVATOR 1; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETS B; TRANSCRIPTION FACTOR KLF8; UNCLASSIFIED DRUG; BCAR1 PROTEIN, MOUSE; SERINE;

CELL CYCLE REGULATION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME REGULATION; EXTRACELLULAR MATRIX; GENETIC TRANSCRIPTION; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR CELL; ANIMAL; BINDING SITE; CELL CYCLE; CELL MOTION; CHEMISTRY; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SRC HOMOLOGY DOMAIN;

ANIMALS; BINDING SITES; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; CRK-ASSOCIATED SUBSTRATE PROTEIN; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; SERINE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES;

EID: 33748068089     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20956     Document Type: Review

References (82)

1. Abbi S, Ueda H, Zheng C, Cooper LA, Zhao J, Christopher R, Guan JL. 2002. Regulation of focal adhesion kinase by a novel protein inhibitor FIP200. Mol Biol Cell 13:3178-3191.
2. Alexandropoulos K, Baltimore D. 1996. Coordinate activation of c-Src by SH3- and SH2-binding sites on a novel p130Cas-related protein, Sin. Genes Dev 10:1341-1355.
3. Almeida EA, Ilic D, Han Q, Hauck CR, Jin F, Kawakatsu H, Schlaepfer DD, Damsky CH. 2000. Matrix survival signaling: From fibronectin via focal adhesion kinase to a Jun NH(2)-terminal kinase. J Cell Biol 149:741-754.
4. Bianchi M, De Lucchini S, Marin O, Turner DL, Hanks SK, Villa-Moruzzi E. 2005. Regulation of FAK Ser-722 phosphorylation and kinase activity by GSK3 and PP1 during cell spreading and migration. Biochem J 391:359-370.
5. Bond M, Sala-Newby GB, Newby AC. 2004. Focal adhesion kinase (FAK)-dependent regulation of S-phase kinase-associated protein-2 (Skp-2) stability. A novel mechanism regulating smooth muscle cell proliferation. J Biol Chem 279:37304-37310.
6. Brunton VG, Avizienyte E, Fincham VJ, Serrels B, Metcalf CA III, Sawyer TK, Frame MC. 2005. Identification of Src-specific phosphorylation site on focal adhesion kinase: Dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior. Cancer Res 65:1335-1342.
7. Calalb MB, Polte TR, Hanks SK. 1995. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity; a role for Src-family kinases. Mol Cell Biol 15:954-963.
8. Carragher NO, Westhoff MA, Fincham VJ, Schaller MD, Frame MC. 2003. A novel role for FAK as a protease-targeting adaptor protein: Regulation by p42 ERK and Src. Curr Biol 13:1442-1450.
9. Carrano AC, Eytan E, Hershko A, Pagano M. 1999. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1:193-199.
10. Cary LA, Han DC, Polte TR, Hanks SK, Guan JL. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 140:211-221.
11. Ceccarelli DF, Song HK, Poy F, Schaller MD, Eck MJ. 2005. Crystal structure of the FERM domain of focal adhesion kinase. J Biol Chem 281:252-259.
12. Cho SY, Klemke RL. 2000. 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.
13. Colognato H, Ramachandrappa S, Olsen IM, ffrench-Constant C. 2004. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167:365-375.
14. Cooper LA, Shen TL, Guan JL. 2003. Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol Cell Biol 23:8030-8041.
15. Craven RJ, Lightfoot H, Cance WG. 2003. A decade of tyrosine kinases: From gene discovery to therapeutics. Surg Oncol 12:39-49.
16. Ding Q, Stewart J, Jr., Olman MA, Klobe MR, Gladson CL. 2003. The pattern of enhancement of Src kinase activity on platelet-derived growth factor stimulation of glioblastoma cells is affected by the integrin engaged. J Biol Chem 278:39882-39891.
17. Ding Q, Grammer JR, Nelson MA, Guan JL, Stewart JE, Jr., Gladson CL. 2005. p27(Kip1) and cyclin D1 are necessary for focal adhesion kinase (FAK) regulation of cell cycle progression in glioblastoma cells propagated in vitro and in vivo in the scid mouse brain. J Biol Chem 280:6802-6815.
18. Dolfi F, Garcia-Guzman M, Ojaniemi M, Nakamura H, Matsuda M, Vuori K. 1998. The adaptor protein Crk connects multiple cellular stimuli to the JNK signaling pathway. Proc Natl Acad Sci USA 95:15394-15399.
19. Dunty JM, Gabarra-Niecko V, King ML, Ceccarelli DF, Eck MJ, Schaller MD. 2004. FERM domain interaction promotes FAK signaling. Mol Cell Biol 24:5353-5368.
20. Ezratty EJ, Partridge MA, Gundersen GG. 2005. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7:581-590.
21. Fashena SJ, Einarson MB, O'Neill GM, Patriotis C, Golemis EA. 2002. Dissection of HEF1-dependent functions in motility and transcriptional regulation. J Cell Sci 115:99-111.
22. Giannone G, Ronde P, Gaire M, Beaudouin J, Haiech J, Ellenberg J, Takeda K. 2004. Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J Biol Chem 279:28715-28723.
23. Golubovskaya V, Kaur A, Cance WG. 2004. Cloning and characterization of the promoter region of human focal adhesion kinase gene: Nuclear factor kappa B and p53 binding sites. Biochim Biopys Acta 1678(2-3):111-125.
24. Hanks SK, Ryzhova L, Shin NY, Brabek J. 2003. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front Biosci 8:d982-d996.
25. Harte MT, Hildebrand JD, Burnham MR, Bouton AH, Parsons JT. 1996. p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J Biol Chem 271:13649-13655.
26. Hauck CR, Sieg DJ, Hsia DA, Loftus JC, Gaarde WA, Monia BP, Schlaepfer DD. 2001. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res 61:7079-7090.
27. Hecker TP, Grammer JR, Gillespie GY, Stewart J, Jr., Gladson CL. 2002. Focal adhesion kinase enhances signaling through the Shc/extracellular signal-regulated kinase pathway in anaplastic astrocytoma tumor biopsy samples. Cancer Res 62:2699-2707.
28. Hecker TP, Ding Q, Rege TA, Hanks SK, Gladson CL. 2004. Overexpression of FAK promotes Ras activity through the formation of a FAK/p120RasGAP complex in malignant astrocytoma cells. Oncogene 23:3962-3971.
29. Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin CH, Westermark B, Nister M. 1992. Platelet-derived growth factor and its receptors in human glioma tissue: Expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52:3213-3219.
30. Honda H, Oda H, Nakamoto T, Honda Z, Sakai R, Suzuki T, Saito T, Nakamura K, Nakao K, Ishikawa T, Katsuki M, Yazaki Y, Hirai H. 1998. Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat Genet 19:361-365.
31. Hynes RO. 2002. Integrins: Bidirectional, allosteric signaling machines. Cell 110:673-687.
32. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
33. Ishino M, Ohba T, Sasaki H, Sasaki T. 1995. Molecular cloning of a cDNA encoding a phosphoprotein, Efs, which contains a Src homology 3 domain and associates with Fyn. Oncogene 11:2331-2338.
34. Ivanchuk SM, Mondal S, Dirks PB, Rutka JT. 2001. The INK4A/ARF locus: Role in cell cycle control and apoptosis and implications for glioma growth. J Neurooncol 51:219-229.
35. Kiyaokawa E, Hashimoto Y, Kobayashi S, Sugimura H, Kurata T, Matsuda M. 1998. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev 12:3331-3336.
36. Klemke RL, Leng J, Molander R, Brooks PC, Vuori K, Cheresh DA. 1998. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J Cell Biol 140:961-972.
37. Lavoie JN, L'Allemain G, Brunet A, Muller R, Pouyssegur J. 1996. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem 271:20608-20616.
38. Law SF, Estojak J, Wang B, Mysliwiec T, Kruh G, Golemis EA. 1996. Human enhancer of filamentation 1, a novel p130cas-like docking protein, associates with focal adhesion kinase and induces pseudohyphal growth in Saccharomyces cerevisiae. Mol Cell Biol 16:3327-3337.
39. Law SF, O'Neill GM, Fashena SJ, Einarson MB, Golemis EA. 2000. The docking protein HEF1 is an apoptotic mediator at focal adhesion sites. Mol Cell Biol 20:5184-5195.
40. Lim Y, Han I, Jeon J, Park H, Bahk YY, Oh ES. 2004. Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for ras transformation of fibroblasts. J Biol Chem 279:29060-29065.
41. Ma A, Richardson A, Schaefer EM, Parsons JT. 2001. Serine phosphorylation of focal adhesion kinase in interphase and mitosis: A possible role in modulating binding to p130(Cas). Mol Biol Cell 12:1-12.
42. Manie SN, Beck AR, Astier A, Law SF, Canty T, Hirai H, Druker BJ, Avraham H, Haghayeghi N, Sattler M, Salgia R, Griffin JD, Golemis EA, Freedman AS. 1997. Involvement of p130(Cas) and p105(HEF1), a novel Cas-like docking protein, in a cytoskeleton-dependent signaling pathway initiated by ligation of integrin or antigen receptor on human B cells. J Biol Chem 272:4230-4236.
43. Melkoumian ZK, Peng X, Gan B, Wu X, Guan JL. 2005. Mechanism of cell cycle regulation by FIP200 in human breast cancer cells. Cancer Res 65:6676-6684.
44. Merrill RA, See AW, Wertheim ML, Clagett-Dame M. 2004. Crk-associated substrate (Cas) family member, NEDD9, is regulated in human neuroblastoma cells and in the embryonic hindbram in all-trans retinoic acid. Dev Dyn 231:564-575.
45. Minegishi M, Tachibana K, Sato T, Iwata S, Nojima Y, Morimoto C. 1996. Structure and function of Cas-L, a 105-kD Crk-associated substrate-related protein that is involved in beta 1 integrin-mediated signaling in lymphocytes. J Exp Med 184:1365-1375.
46. Nakamoto T, Sakai R, Honda H, Ogawa S, Ueno H, Suzuki T, Aizawa S, Yazaki Y, Hirai H. 1997. Requirements for localization of p130cas to focal adhesions. Mol Cell Biol 17:3884-3897.
47. Nakamura K, Yano H, Schaefer E, Sabe H. 2001. Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration: Analysis of specific phosphorylation events using site-directed antibodies. Oncogene 20:2626-2635.
48. Natarajan M, Stewart JE, Golemis EA, Pugacheva EN, Alexandropoulos K, Cox BD, Wang W, Grammer JR, Gladson CL. 2006. HEF1 is a necessary and specific downstream effector of FAK that promotes the migration of glioblastoma cells. Oncogene 25:1721-1732.
49. Nho RS, Sheaff RJ. 2003. p27kip1 contributions to cancer. Prog Cell Cycle Res 5:249-259.
50. O'Neill GM, Fashena SJ, Golemis EA. 2000. Integrin signalling: A new Cas(t) of characters enters the stage. Trends Cell Biol 10:111-119.
51. Osterhout DJ, Wolven A, Wolf RM, Resh MD, Chao MV. 1999. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145:1209-1218.
52. Parsons JT. 2003. Focal adhesion kinase: The first ten years. J Cell Sci 116:1409-1416.
53. Petch LA, Bockholt SM, Bouton A, Parsons JT, Burridge K. 1995. Adhesion-induced tyrosine phosphorylation of the p130 src substrate. J Cell Sci 108:1371-1379.
54. Pietenpol JA, Stewart ZA. 2002. Cell cycle checkpoint signaling: Cell cycle arrest versus apoptosis. Toxicology 181-182:475-481.
55. Polte TR, Hanks SK. 1995. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc Natl Acad Sci USA 92:10678-10682.
56. Pugacheva EN, Golemis EA. 2005. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat Cell Biol 7:937-946.
57. Rodriguez-Fernandez JL, Gomez M, Luque A, Hogg N, Sanchez-Madrid F, Cabanas C. 1999. The interaction of activated integrin lymphocyte function-associated antigen 1 with ligand intercellular adhesion molecule 1 induces activation and redistribution of focal adhesion kinase and proline-rich tyrosine kinase 2 in T lymphocytes. Mol Biol Cell 10:1891-1907.
58. Sakai R, Iwamatsu A, Hirano N, Ogawa S, Tanaka T, Mano H, Yazaki Y, Hirai H. 1994. 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.
59. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB, Parsons JT. 1992. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 89:5192-5196.
60. Schaller MD, Hildebrand JD, Shannon JD, Fox JW, Vines RR, Parsons JT. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol Cell Biol 14:1680-1688.
61. Schlaepfer DD, Hunter T. 1997. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J Biol Chem 272:13189-13195.
62. Schlaepfer DD, Mitra SK. 2004. Multiple connections link FAK to cell motility and invasion. Curr Opin Genet Dev 14:92-101.
63. Sieg DJ, Hauck CR, Ilic D, Klingbeil CL, Schaefer E, Damsky CH, Schlaepfer DD. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2:249-256.
64. Slingerland J, Pagano M. 2000. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 183:10-17.
65. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U, Krek W. 1999. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1:207-214.
66. Tachibana K, Urano T, Fujita H, Ohashi Y, Kamiguchi K, Iwata S, Hirai H, Morimoto C. 1997. 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 272:29083-29090.
67. Takino T, Nakada M, Miyamori H, Watanabe Y, Sato T, Gantulga D, Yoshioka K, Yamada KM, Sato H. 2005. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J Biol Chem 280:37772-37781.
68. Thomas SM, Brugge JS. 1997. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
69. van Seventer FA, Salmen HJ, Law SF, O'Neill GM, Mullen MM, Franz AM, Kanner SB, Golemis EA, van Seventer JM. 2001. Focal adhesion kinase regulates betal integrin-dependent T cell migration through an HEF1 effector pathway. Eur J Immunol 31:1417-1427.
70. Vuori K, Hirai H, Aizawa S, Ruoslahti E. 1996. Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: A role for Src family kinases. Mol Cell Biol 16:2606-2613.
71. Wang D, Grammer R, Cobbs CS, Stewart JE, Jr., Liu Z, Rhoden R, Hecker TP, Ding Q, Gladson CL. 2000. p125 focal adhesion kinase promotes malignant astrocytoma cell proliferation in vivo. J Cell Sci 113:4221-4230.
72. Wasylyk B, Hagman J, Gutierrez-Hartmann A. 1998. Ets transcription factors: Nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci 23:213-216.
73. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6:154-161.
74. Wu X, Suetsugu S, Cooper LA, Takenawa T, Guan JL. 2004. Focal adhesion kinase regulation of N-WASP subcellular localization and function. J Biol Chem 279:9565-9576.
75. Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH. 2003. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114:469-482.
76. Yamakita Y, Totsukawa G, Yamashiro S, Fry D, Zhang X, Hanks SK, Matsumura F. 1999. Dissociation of FAK/p130(CAS)/c-Src complex during mitosis: Role of mitosis-specific serine phosphorylation of FAK. J Cell Biol 144:315-324.
77. Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, Zhong H, Simons JW, Holash J, Wiegand SJ, Yancopoulos GD. 2000. Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33:49-55.
78. Zhai J, Lin H, Nie Z, Wu J, Canete-Soler R, Schlaepfer WW, Schlaepfer DD. 2003. Direct interaction of focal adhesion kinase with p190RhoGEF. J Biol Chem 278:24865-24873.
79. Zhang H, Kobayashi R, Galaktionov K, Beach D. 1995. p19Skp1 and p45Skp2 are essential elements of the cyclin A-CDK2 S phase kinase. Cell 82:915-925.
80. Zhao JH, Reiske H, Guan JL. 1998. Regulation of the cell cycle by focal adhesion kinase. J Cell Biol 143:1997-2008.
81. Zhao J, Pestell R, Guan JL. 2001. Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol Biol Cell 12:4066-4077.
82. Zhao J, Bian ZC, Yee K, Chen BP, Chien S, Guan JL. 2003. Identification of transcription factor KLF8 as a downstream target of focal adhesion kinase in its regulation of cyclin D1 and cell cycle progression. Mol Cell 11:1503-1515.