Focal Adhesion Kinase and p53 Signaling in Cancer Cells

International Review of Cytology

Volumn 263, Issue , 2007, Pages 103-153

  Golubovskaya, Vita M ^a,b   Cance, William G ^a,b,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Apoptosis; Cancer; Focal adhesion kinase; p53; Tumorigenesis

Indexed keywords

ADVEXIN; ANTINEOPLASTIC AGENT; ANTISENSE OLIGODEOXYNUCLEOTIDE; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; COMPLEMENTARY DNA; EZRIN; FLUOROURACIL; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; GEMCITABINE; GENDICINE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IMIDAZOLE DERIVATIVE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; LEPTOMYCIN B; LUCIFERASE; NUCLEAR PROTEIN; OKADAIC ACID; ONYX 015; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN; PROTEIN GRB 7; PROTEIN P53; PROTEIN SHC; SCATTER FACTOR RECEPTOR; TAE 226; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR;

AMINO TERMINAL SEQUENCE; ANGIOGENESIS; APOPTOSIS; BINDING SITE; BRAIN TUMOR; BREAST CANCER; CANCER; CANCER CELL; CANCER GENE THERAPY; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL DEATH; CELL MIGRATION; CELL MOTILITY; CELL NUCLEUS; CHICKEN; CHO CELL; COLON CANCER; COLORECTAL CANCER; CYTOLOGY; CYTOPLASM; DRUG PROTEIN BINDING; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE AMPLIFICATION; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; HEAD AND NECK CANCER; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CANCER; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MOUSE STRAIN; MOUTH CANCER; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; OSTEOSARCOMA; OVARY CARCINOMA; PANCREAS CANCER; PHAGE DISPLAY; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CARCINOMA; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SARCOMA; SIGNAL TRANSDUCTION; STEM CELL; SUMOYLATION; THYROID CANCER; TUMOR VOLUME; UTERINE CERVIX CANCER; VIRAL GENE THERAPY;

ANIMALS; CELL ADHESION; CELL MOVEMENT; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 34548085454     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7696(07)63003-4     Document Type: Review

References (260)

1. Aarts M., Liu Y., Liu L., Besshoh S., Arundine M., Gurd J.W., Wang Y.T., Salter M.W., and Tymianski M. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298 (2002) 846-850
2. Abbi S., and Guan J.L. Focal adhesion kinase: Protein interactions and cellular functions. Histol. Histopathol. 17 (2002) 1163-1171
3. Abedi H., and Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 272 (1997) 15442-15451
4. Abu-Ghazaleh R., Kabir J., Jia H., Lobo M., and Zachary I. Src mediates stimulation by vascular endothelial growth factor of the phosphorylation of focal adhesion kinase at tyrosine 861, and migration and anti-apoptosis in endothelial cells. Biochem. J. 360 (2001) 255-264
5. Agochiya M., Brunton V.G., Owens D.W., Parkinson E.K., Paraskeva C., Keith W.N., and Frame M.C. Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 18 (1999) 5646-5653
6. Akasaka T., van Leeuwen R.L., Yoshinaga I.G., Mihm Jr. M.C., and Byers H.R. Focal adhesion kinase (p125FAK) expression correlates with motility of human melanoma cell lines. J. Invest. Dermatol. 105 (1995) 104-108
7. Akhter S.A., Luttrell L.M., Rockman H.A., Iaccarino G., Lefkowitz R.J., and Koch W.J. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science 280 (1998) 574-577
8. Aramburu J., Yaffe M.B., Lopez-Rodriguez C., Cantley L.C., Hogan P.G., and Rao A. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285 (1999) 2129-2133
9. Arold S.T., Hoellerer M.K., and Noble M.E. The structural basis of localization and signaling by the focal adhesion targeting domain. Structure 10 (2002) 319-327
10. Aronsohn M.S., Brown H.M., Hauptman G., and Kornberg L.J. Expression of focal adhesion kinase and phosphorylated focal adhesion kinase in squamous cell carcinoma of the larynx. Laryngoscope 113 (2003) 1944-1948
11. Avraham H.K., Lee T.H., Koh Y., Kim T.A., Jiang S., Sussman M., Samarel A.M., and Avraham S. Vascular endothelial growth factor regulates focal adhesion assembly in human brain microvascular endothelial cells through activation of the focal adhesion kinase and related adhesion focal tyrosine kinase. J. Biol. Chem. 278 (2003) 36661-36668
12. Avraham H.K., Jiang S., Lee T.H., Prakash O., and Avraham S. HIV-1 Tat-mediated effects on focal adhesion assembly and permeability in brain microvascular endothelial cells. J. Immunol. 173 (2004) 6228-6233
13. Avraham S., London R., Fu Y., Ota S., Hiregowdara D., Li J., Jiang S., Pasztor L.M., White R.A., Groopman J.E., et al. Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol. Chem. 270 (1995) 27742-27751
14. Bachelot C., Rameh L., Parsons T., and Cantley L.C. Association of phosphatidylinositol 3-kinase, via the SH2 domains of p85, with focal adhesion kinase in polyoma middle t-transformed fibroblasts. Biochim. Biophys. Acta 1311 (1996) 45-52
15. Baker S.J., Preisinger A.C., Jessup J.M., Paraskeva C., Markowitz S., Willson J.K., Hamilton S., and Vogelstein B. p53 gene mutations occur in combination with 17p allelic deletions as late events in colorectal tumorigenesis. Cancer Res. 50 (1990) 7717-7722
16. Benlimame N., He Q., Jie S., Xiao D., Xu Y.J., Loignon M., Schlaepfer D.D., and Alaoui-Jamali M.A. FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J. Cell Biol. 171 (2005) 505-516
17. Benoit V., de Moraes E., Dar N.A., Taranchon E., Bours V., Hautefeuille A., Taniere P., Chariot A., Scoazec J.Y., de Moura Gallo C.V., Merville M.P., and Hainaut P. Transcriptional activation of cyclooxygenase-2 by tumor suppressor p53 requires nuclear factor-kappaB. Oncogene 25 (2006) 5708-5718
18. Bergamaschi D., Gasco M., Hiller L., Sullivan A., Syed N., Trigiante G., Yulug I., Merlano M., Numico G., Comino A., Attard M., Reelfs O., et al. p53 polymorphism influences response in cancer chemotherapy via modulation of p73-dependent apoptosis. Cancer Cell 3 (2003) 387-402
19. Beviglia L., Golubovskaya V., Xu L., Yang X., Craven R.J., and Cance W.G. Focal adhesion kinase N-terminus in breast carcinoma cells induces rounding, detachment and apoptosis. Biochem. J. 373 (2003) 201-210
20. Bianco R., Melisi D., Ciardiello F., and Tortora G. Key cancer cell signal transduction pathways as therapeutic targets. Eur. J. Cancer 42 (2006) 290-294
21. Bonsi L., Pierdomenico L., Biscardi M., Marchionni C., Gavazzi S., Fossati V., Ghinassi B., Alviano F., Rondelli D., Franchina M., Bagnara G.P., and Grossi A. Constitutive and stimulated production of VEGF by human megakaryoblastic cell lines: Effect on proliferation and signaling pathway. Int. J. Immunopathol. Pharmacol. 18 (2005) 445-455
22. Borkhardt A., Bojesen S., Haas O.A., Fuchs U., Bartelheimer D., Loncarevic I.F., Bohle R.M., Harbott J., Repp R., Jaeger U., Viehmann S., Henn T., et al. The human GRAF gene is fused to MLL in a unique t(5;11)(q31;q23) and both alleles are disrupted in three cases of myelodysplastic syndrome/acute myeloid leukemia with a deletion 5q. Proc. Natl. Acad. Sci. USA 97 (2000) 9168-9173
23. Bouchard M.J., Wang L., and Schneider R.J. Activation of focal adhesion kinase by hepatitis B virus HBx protein: Multiple functions in viral replication. J. Virol. 80 (2006) 4406-4414
24. Bouchet B.P., de Fromentel C.C., Puisieux A., and Galmarini C.M. p53 as a target for anti-cancer drug development. Crit. Rev. Oncol. Hematol. 58 (2006) 190-207
25. Boyanapalli M., Lahoud O.B., Messiaen L., Kim B., Anderle de Sylor M.S., Duckett S.J., Somara S., and Mikol D.D. Neurofibromin binds to caveolin-1 and regulates ras, FAK, and Akt. Biochem. Biophys. Res. Commun. 340 (2006) 1200-1208
26. Brown M.T., Andrade J., Radhakrishna H., Donaldson J.G., Cooper J.A., and Randazzo P.A. ASAP1, a phospholipid-dependent arf GTPase-activating protein that associates with and is phosphorylated by Src. Mol. Cell. Biol. 18 (1998) 7038-7051
27. Burgaya F., and Girault J.A. Cloning of focal adhesion kinase, pp125FAK, from rat brain reveals multiple transcripts with different patterns of expression. Brain Res. Mol. Brain Res. 37 (1996) 63-73
28. Caballero O.L., de Souza S.J., Brentani R.R., and Simpson A.J. Alternative spliced transcripts as cancer markers. Dis. Markers 17 (2001) 67-75
29. Calalb M.B., Polte T.R., and 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. 15 (1995) 954-963
30. Cance W.G., Harris J.E., Iacocca M.V., Roche E., Yang X., Chang J., Simkins S., and Xu L. Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: Correlation with preinvasive and invasive phenotypes. Clin. Cancer Res. 6 (2000) 2417-2423
31. Canel M., Secades P., Rodrigo J.-P., Cabanillas R., Herrero A., Suarez C., and Chiara M.-D. Overexpression of focal adhesion kinase in head and neck squamous cell carcinoma is independent of fak gene copy number. Clin. Cancer Res. 12 (2006) 3272-3279
32. Carelli S., Zadra G., Vaira V., Falleni M., Bottiglieri L., Nosotti M., Di Giulio A.M., Gorio A., and Bosari S. Up-regulation of focal adhesion kinase in non-small cell lung cancer. Lung Cancer 53 (2006) 263-271
33. Ceccarelli D.F., Song H.K., Poy F., Schaller M.D., and Eck M.J. Crystal structure of the FERM domain of focal adhesion kinase. J. Biol. Chem. 281 (2006) 252-259
34. Chae H.J., Ha H.Y., Im J.Y., Song J.Y., Park S., and Han P.L. JSAP1 is required for the cell adhesion and spreading of mouse embryonic fibroblasts. Biochem. Biophys. Res. Commun. 345 (2006) 809-816
35. Chan P.C., Liang C.C., Yu K.C., Chang M.C., Ho W.L., Chen B.H., and Chen H.C. Synergistic effect of focal adhesion kinase overexpression and hepatocyte growth factor stimulation on cell transformation. J. Biol. Chem. 277 (2002) 50373-50379
36. Chen H.C., and Guan J.L. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 91 (1994) 10148-10152
37. Chen H.C., Appeddu P.A., Parsons J.T., Hildebrand J.D., Schaller M.D., and Guan J.L. Interaction of focal adhesion kinase with cytoskeletal protein talin. J. Biol. Chem. 270 (1995) 16995-16999
38. Chen R., Kim O., Li M., Xiong X., Guan J.L., Kung H.J., Chen H., Shimizu Y., and Qiu Y. Regulation of the PH-domain-containing tyrosine kinase Etk by focal adhesion kinase through the FERM domain. Nat. Cell Biol. 3 (2001) 439-444
39. Chen S.Y., and Chen H.C. Direct interaction of focal adhesion kinase (FAK) with Met is required for FAK to promote hepatocyte growth factor-induced cell invasion. Mol. Cell. Biol. 26 (2006) 5155-5167
40. Chen Y.N., Sharma S.K., Ramsey T.M., Jiang L., Martin M.S., Baker K., Adams P.D., Bair K.W., and Kaelin Jr. W.G. Selective killing of transformed cells by cyclin/cyclin-dependent kinase 2 antagonists. Proc. Natl. Acad. Sci. USA 96 (1999) 4325-4329
41. Chipuk J.E., and Green D.R. Cytoplasmic p53: Bax and forward. Cell Cycle 3 (2004) 429-431
42. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., and Green D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303 (2004) 1010-1014
43. Choi H.S., Wang Z., Richmond W., He X., Yang K., Jiang T., Karanewsky D., Gu X.J., Zhou V., Liu Y., Che J., Lee C.C., et al. Design and synthesis of 7H-pyrrolo[2,3-d]pyrimidines as focal adhesion kinase inhibitors. Part 2. Bioorg. Med. Chem. Lett. 16 (2006) 2689-2692
44. Cooper L.A., Shen T.L., and Guan J.L. Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol. Cell. Biol. 23 (2003) 8030-8041
45. Corsi J.M., Rouer E., Girault J.A., and Enslen H. Organization and post-transcriptional processing of focal adhesion kinase gene. BMC Genomics 7 (2006) 198
46. Cox B.D., Natarajan M., Stettner M.R., and Gladson C.L. New concepts regarding focal adhesion kinase promotion of cell migration and proliferation. J. Cell. Biochem. 99 (2006) 35-52
47. Critchley D.R. Genetic, biochemical and structural approaches to talin function. Biochem. Soc. Trans. 33 (2005) 1308-1312
48. Debant A., Serra-Pages C., Seipel K., O'Brien S., Tang M., Park S.H., and Streuli M. The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. USA 93 (1996) 5466-5471
49. Duxbury M.S., Ito H., Benoit E., Zinner M.J., Ashley S.W., and Whang E.E. RNA interference targeting focal adhesion kinase enhances pancreatic adenocarcinoma gemcitabine chemosensitivity. Biochem. Biophys. Res. Commun. 311 (2003) 786-792
50. Duxbury M.S., Ito H., Zinner M.J., Ashley S.W., and Whang E.E. Focal adhesion kinase gene silencing promotes anoikis and suppresses metastasis of human pancreatic adenocarcinoma cells. Surgery 135 (2004) 555-562
51. Edwards S.J., Hananeia L., Eccles M.R., Zhang Y.F., and Braithwaite A.W. The proline-rich region of mouse p53 influences transactivation and apoptosis but is largely dispensable for these functions. Oncogene 22 (2003) 4517-4523
52. Fan R.S., Jacamo R.O., Jiang X., Sinnett-Smith J., and Rozengurt E. G protein-coupled receptor activation rapidly stimulates focal adhesion kinase phosphorylation at Ser-843. Mediation by Ca2+, calmodulin, and Ca2+/calmodulin-dependent kinase II. J. Biol. Chem. 280 (2005) 24212-24220
53. Farmer G., Bargonetti J., Zhu H., Friedman P., Prywes R., and Prives C. Wild-type p53 activates transcription in vitro. Nature 358 (1992) 83-86
54. Fearon E.R., and Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 61 (1990) 759-767
55. Fiedorek Jr. F.T., and Kay E.S. Mapping of the focal adhesion kinase (Fadk) gene to mouse chromosome 15 and human chromosome 8. Mamm. Genome 6 (1995) 123-126
56. Finlayson C.A., Chappell J., Leitner J.W., Goalstone M.L., Garrity M., Nawaz S., Ciaraldi T.P., and Draznin B. Enhanced insulin signaling via Shc in human breast cancer. Metabolism 52 (2003) 1606-1611
57. Fleigel J., Sedwick J., and Kornberg L.J. Hepatocyte growth factor/scatter factor stimulates mitogenesis and migration of a head and neck squamous cell carcinoma cell line. Otolaryngol. Head Neck Surg. 127 (2002) 271-278
58. Fridman J.S., and Lowe S.W. Control of apoptosis by p53. Oncogene 22 (2003) 9030-9040
59. Frisch S.M. Evidence for a function of death-receptor-related, death-domain-containing proteins in anoikis. Curr. Biol. 9 (1999) 1047-1049
60. Frisch S.M., and Ruoslahti E. Integrins and anoikis. Curr. Opin. Cell Biol. 9 (1997) 701-706
61. Frisch S.M., and Screaton R.A. Anoikis mechanisms. Curr. Opin. Cell Biol. 13 (2001) 555-562
62. Frisch S.M., Vuori K., Ruoslahti E., and Chan-Hui P.Y. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134 (1996) 793-799
63. Fujii T., Koshikawa K., Nomoto S., Okochi O., Kaneko T., Inoue S., Yatabe Y., Takeda S., and Nakao A. Focal adhesion kinase is overexpressed in hepatocellular carcinoma and can be served as an independent prognostic factor. J. Hepatol. 41 (2004) 104-111
64. Fujimoto J., Sawamoto K., Okabe M., Takagi Y., Tezuka T., Yoshikawa S., Ryo H., Okano H., and Yamamoto T. Cloning and characterization of Dfak56, a homolog of focal adhesion kinase, in Drosophila melanogaster. J. Biol. Chem. 274 (1999) 29196-29201
65. Fujita H., Kamiguchi K., Cho D., Shibanuma M., Morimoto C., and Tachibana K. Interaction of Hic-5, a senescence-related protein, with focal adhesion kinase. J. Biol. Chem. 273 (1998) 26516-26521
66. Furuyama K., Doi R., Mori T., Toyoda E., Ito D., Kami K., Koizumi M., Kida A., Kawaguchi Y., and Fujimoto K. Clinical significance of focal adhesion kinase in resectable pancreatic cancer. World J. Surg. 30 (2006) 219-226
67. Gabarra-Niecko V., Schaller M.D., and Dunty J.M. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 22 (2003) 359-374
68. Gabriel B., Mildenberger S., Weisser C.W., Metzger E., Gitsch G., Schule R., and Muller J.M. Focal adhesion kinase interacts with the transcriptional coactivator FHL2 and both are overexpressed in epithelial ovarian cancer. Anticancer Res. 24 (2004) 921-927
69. Gan B., Melkoumian Z.K., Wu X., Guan K.L., and Guan J.L. Identification of FIP200 interaction with the TSC1-TSC2 complex and its role in regulation of cell size control. J. Cell Biol. 170 (2005) 379-389
70. Gan B., Peng X., Nagy T., Alcaraz A., Gu H., and Guan J.L. Role of FIP200 in cardiac and liver development and its regulation of TNFalpha and TSC-mTOR signaling pathways. J. Cell Biol. 175 (2006) 121-133
71. Garces C.A., Kurenova E.V., Golubovskaya V.M., and Cance W.G. Vascular endothelial growth factor receptor-3 and focal adhesion kinase bind and suppress apoptosis in breast cancer cells. Cancer Res. 66 (2006) 1446-1454
72. Giaccia A.J., and Kastan M.B. The complexity of p53 modulation, emerging patterns from divergent signals. Genes Dev. 12 (1998) 2973-2983
73. Goicoechea S.M., Tu Y., Hua Y., Chen K., Shen T.L., Guan J.L., and Wu C. Nck-2 interacts with focal adhesion kinase and modulates cell motility. Int. J. Biochem. Cell Biol. 34 (2002) 791-805
74. Golubovskaya V., Beviglia L., Xu L.H., Earp III H.S., Craven R., and Cance W. 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. 277 (2002) 38978-38987
75. Golubovskaya V.M., Gross S., Kaur A.S., Wilson R.I., Xu L.H., Yang X.H., and Cance W.G. Simultaneous inhibition of focal adhesion kinase and SRC enhances detachment and apoptosis in colon cancer cell lines. Mol. Cancer Res. 1 (2003) 755-764
76. Golubovskaya V., Kaur A., and Cance W. Cloning and characterization of the promoter region of human focal adhesion kinase gene: Nuclear factor kappa B and p53 binding sites*1. Biochim. Biophys. Acta 1678 (2004) 111-125
77. Golubovskaya V.M., Finch R., and Cance W.G. Direct interaction of the N-terminal domain of focal adhesion kinase with the N-terminal transactivation domain of p53. J. Biol. Chem. 280 (2005) 25008-25021
78. Grigera P.R., Jeffery E.D., Martin K.H., Shabanowitz J., Hunt D.F., and Parsons J.T. FAK phosphorylation sites mapped by mass spectrometry. J. Cell Sci. 118 (2005) 4931-4935
79. Grisaru-Granovsky S., Salah Z., Maoz M., Pruss D., Beller U., and Bar-Shavit R. Differential expression of protease activated receptor 1 (Par1) and pY397FAK in benign and malignant human ovarian tissue samples. Int. J. Cancer 113 (2005) 372-378
80. Guan J.L. Role of focal adhesion kinase in integrin signaling. Int. J. Biochem. Cell Biol. 29 (1997) 1085-1096
81. Han D.C., and Guan J.L. Association of focal adhesion kinase with Grb7 and its role in cell migration. J. Biol. Chem. 274 (1999) 24425-24430
82. Han E.K., McGonigal T., Wang J., Giranda V.L., and Luo Y. Functional analysis of focal adhesion kinase (FAK) reduction by small inhibitory RNAs. Anticancer Res. 24 (2004) 3899-3905
83. Han N.M., Fleming R.Y., Curley S.A., and Gallick G.E. Overexpression of focal adhesion kinase (p125FAK) in human colorectal carcinoma liver metastases: Independence from c-src or c-yes activation. Ann. Surg. Oncol. 4 (1997) 264-268
84. Hanada M., Tanaka K., Matsumoto Y., Nakatani F., Sakimura R., Matsunobu T., Li X., Okada T., Nakamura T., Takasaki M., and Iwamoto Y. Focal adhesion kinase is activated in invading fibrosarcoma cells and regulates metastasis. Clin. Exp. Metastasis 22 (2005) 485-494
85. Hanks S.K., and Polte T.R. Signaling through focal adhesion kinase. BioEssays 19 (1997) 137-145
86. Hanks S.K., Calalb M.B., Harper M.C., and Patel S.K. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl. Acad. Sci. USA 89 (1992) 8487-8491
87. Hanks S.K., Ryzhova L., Shin N.Y., and Brabek J. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front. Biosci. 8 (2003) d982-d996
88. Hauck C.R., Sieg D.J., Hsia D.A., Loftus J.C., Gaarde W.A., Monia B.P., and Schlaepfer D.D. 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 (2001) 7079-7090
89. Hayasaka H., Simon K., Hershey E.D., Masumoto K.H., and Parsons J.T. FRNK, the autonomously expressed C-terminal region of focal adhesion kinase, is uniquely regulated in vascular smooth muscle: Analysis of expression in transgenic mice. J. Cell. Biochem. 95 (2005) 1248-1263
90. Hayashi I., Vuori K., and Liddington R.C. The focal adhesion targeting (FAT) region of focal adhesion kinase is a four-helix bundle that binds paxillin. Nat. Struct. Biol. 9 (2002) 101-106
91. Hecker T.P., Grammer J.R., Gillespie G.Y., Stewart Jr. J., and Gladson C.L. Focal adhesion kinase enhances signaling through the Shc/extracellular signal-regulated kinase pathway in anaplastic astrocytoma tumor biopsy samples. Cancer Res. 62 (2002) 2699-2707
92. Hecker T.P., Ding Q., Rege T.A., Hanks S.K., and Gladson C.L. Overexpression of FAK promotes Ras activity through the formation of a FAK/p120RasGAP complex in malignant astrocytoma cells. Oncogene 23 (2004) 3962-3971
93. Hess A.R., and Hendrix M.J. Focal adhesion kinase signaling and the aggressive melanoma phenotype. Cell Cycle 5 (2006) 478-480
94. Hildebrand J.D., Schaller M.D., and Parsons J.T. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 123 (1993) 993-1005
95. Hildebrand J.D., Taylor J.M., and Parsons J.T. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell. Biol. 16 (1996) 3169-3178
96. Hoffman W.H., Biade S., Zilfou J.T., Chen J., and Murphy M. Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J. Biol. Chem. 277 (2002) 3247-3257
97. Hollstein M., Hergenhahn M., Yang Q., Bartsch H., Wang Z.Q., and Hainaut P. New approaches to understanding p53 gene tumor mutation spectra. Mutat. Res. 431 (1999) 199-209
98. Huang Y.T., Lee L.T., Lee P.P., Lin Y.S., and Lee M.T. Targeting of focal adhesion kinase by flavonoids and small-interfering RNAs reduces tumor cell migration ability. Anticancer Res. 25 (2005) 2017-2025
99. Hunger-Glaser I., Salazar E.P., Sinnett-Smith J., and Rozengurt E. Bombesin, lysophosphatidic acid, and epidermal growth factor rapidly stimulate focal adhesion kinase phosphorylation at Ser-910: Requirement for ERK activation. J. Biol. Chem. 278 (2003) 22631-22643
100. Hunger-Glaser I., Fan R.S., Perez-Salazar E., and Rozengurt E. PDGF and FGF induce focal adhesion kinase (FAK) phosphorylation at Ser-910: Dissociation from Tyr-397 phosphorylation and requirement for ERK activation. J. Cell. Physiol. 200 (2004) 213-222
101. Ilic D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T., and Aizawa S. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377 (1995) 539-544
102. Ilic D., Kanazawa S., Furuta Y., Yamamoto T., and Aizawa S. Impairment of mobility in endodermal cells by FAK deficiency. Exp. Cell Res. 222 (1996) 298-303
103. Ilic D., Almeida E.A., Schlaepfer D.D., Dazin P., Aizawa S., and Damsky C.H. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J. Cell Biol. 143 (1998) 547-560
104. Imaizumi M., Nishimura M., Takeuchi S., Murase M., and Hamaguchi M. Role of tyrosine specific phosphorylation of cellular proteins, especially EGF receptor and p125FAK in human lung cancer cells. Lung Cancer 17 (1997) 69-84
105. Ishino K., Kaneyama J.K., Shibanuma M., and Nose K. Specific decrease in the level of Hic-5, a focal adhesion protein, during immortalization of mouse embryonic fibroblasts, and its association with focal adhesion kinase. J. Cell. Biochem. 76 (2000) 411-419
106. Jacamo R., Jiang X., Lunn J.A., and Rozengurt E. FAK phosphorylation at Ser-843 inhibits Tyr-397 phosphorylation, cell spreading and migration. J. Cell. Physiol. 210 (2007) 436-444
107. Jenq W., Cooper D.R., and Ramirez G. Integrin expression on cell adhesion function and up-regulation of P125FAK and paxillin in metastatic renal carcinoma cells. Connect. Tissue Res. 34 (1996) 161-174
108. Jiang T., Guo Z., Dai B., Kang M., Ann D.K., Kung H.J., and Qiu Y. Bi-directional regulation between tyrosine kinase Etk/BMX and tumor suppressor p53 in response to DNA damage. J. Biol. Chem. 279 (2004) 50181-50189
109. Johnsen J.I., Aurelio O.N., Kwaja Z., Jorgensen G.E., Pellegata N.S., Plattner R., Stanbridge E.J., and Cajot J.F. p53-mediated negative regulation of stathmin/Op18 expression is associated with G(2)/M cell-cycle arrest. Int. J. Cancer 88 (2000) 685-691
110. Jones G., and Stewart G. Nuclear import of N-terminal FAK by activation of the FcepsilonRI receptor in RBL-2H3 cells. Biochem. Biophys. Res. Commun. 314 (2004) 39-45
111. Jones G., Machado Jr. J., and Merlo A. Loss of focal adhesion kinase (FAK) inhibits epidermal growth factor receptor-dependent migration and induces aggregation of nh(2)-terminal FAK in the nuclei of apoptotic glioblastoma cells. Cancer Res. 61 (2001) 4978-4981
112. Jones R.J., Brunton V.G., and Frame M.C. Adhesion-linked kinases in cancer; emphasis on src, focal adhesion kinase and PI 3-kinase. Eur. J. Cancer 36 (2000) 1595-1606
113. Judson P.L., He X., Cance W.G., and Van Le L. Overexpression of focal adhesion kinase, a protein tyrosine kinase, in ovarian carcinoma. Cancer 86 (1999) 1551-1556
114. Kadare G., Toutant M., Formstecher E., Corvol J.C., Carnaud M., Boutterin M.C., and Girault J.A. PIAS1-mediated sumoylation of focal adhesion kinase activates its autophosphorylation. J. Biol. Chem. 278 (2003) 47434-47440
115. Kahana O., Micksche M., Witz I.P., and Yron I. The focal adhesion kinase (P125FAK) is constitutively active in human malignant melanoma. Oncogene 21 (2002) 3969-3977
116. Kasahara T., Koguchi E., Funakoshi M., Aizu-Yokota E., and Sonoda Y. Antiapoptotic action of focal adhesion kinase (FAK) against ionizing radiation. Antioxid. Redox Signal. 4 (2002) 491-499
117. Kilpatrick T.J., Ortuno D., Bucci T., Lai C., and Lemke G. Rat oligodendroglia express c-met and focal adhesion kinase, protein tyrosine kinases implicated in regulating epithelial cell motility. Neurosci. Lett. 279 (2000) 5-8
118. Kim B., van Golen C.M., and Feldman E.L. Degradation and dephosphorylation of focal adhesion kinase during okadaic acid-induced apoptosis in human neuroblastoma cells. Neoplasia 5 (2003) 405-416
119. Kim S.J., Park J.W., Yoon J.S., Mok J.O., Kim Y.J., Park H.K., Kim C.H., Byun D.W., Lee Y.J., Jin S.Y., Suh K.I., and Yoo M.H. Increased expression of focal adhesion kinase in thyroid cancer: Immunohistochemical study. J. Korean Med. Sci. 19 (2004) 710-715
120. Kim Y.M., Hwang S., Kim Y.M., Pyun B.J., Kim T.Y., Lee S.T., Gho Y.S., and Kwon Y.G. Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 277 (2002) 27872-27879
121. Kitajo H., Shibata T., Nagayasu H., Kawano T., Hamada J., Yamashita T., and Arisue M. Rho regulates the hepatocyte growth factor/scatter factor-stimulated cell motility of human oral squamous cell carcinoma cells. Oncol. Rep. 10 (2003) 1351-1356
122. Kodama K., Ishii G., Miyamoto S., Goya M., Zhang S.C., Sangai T., Yoshikawa T., Hasebe T., Hitomi Y., Izumi K., and Ochiai A. Laminin 5 expression protects against anoikis at aerogenous spread and lepidic growth of human lung adenocarcinoma. Int. J. Cancer 116 (2005) 876-884
123. Kornberg L.J. Focal adhesion kinase expression in oral cancers. Head Neck 20 (1998) 634-639
124. Kornberg L.J. Adenovirus-mediated transfer of FRNK augments drug-induced cytotoxicity in cultured SCCHN cells. Anticancer Res. 25 (2005) 4349-4356
125. Kornberg L. Ad-fRNK and Ad-p53 cooperate to augment drug-induced death of a transformed cell line. Anticancer Res. 26 (2006) 3025-3031
126. Kornberg L.J., Shaw L.C., Spoerri P.E., Caballero S., and Grant M.B. Focal adhesion kinase overexpression induces enhanced pathological retinal angiogenesis. Invest. Ophthalmol. Vis. Sci. 45 (2004) 4463-4469
127. Krause K., Wasner M., Reinhard W., Haugwitz U., Dohna C.L., Mossner J., and Engeland K. The tumour suppressor protein p53 can repress transcription of cyclin B. Nucleic Acids Res. 28 (2000) 4410-4418
128. Kume A., Nishiura H., Suda J., and Suda T. Focal adhesion kinase upregulated by granulocyte-macrophage colony-stimulating factor but not by interleukin-3 in differentiating myeloid cells. Blood 89 (1997) 3434-3442
129. Kurenova E., Xu L.-H., Yang X., Baldwin Jr. A.S., Craven R.J., Hanks S.K., Liu Z.-G., and Cance W.G. Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol. Cell. Biol. 24 (2004) 4361-4371
130. Lacroix M., Toillon R.A., and Leclercq G. p53 and breast cancer, an update. Endocr. Relat. Cancer 13 (2006) 293-325
131. Lark A.L., Livasy C.A., Calvo B., Caskey L., Moore D.T., Yang X., and Cance W.G. Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: Immunohistochemistry and real-time PCR analyses. Clin. Cancer Res. 9 (2003) 215-222
132. Lark A.L., Livasy C.A., Dressler L., Moore D.T., Millikan R.C., Geradts J., Iacocca M., Cowan D., Little D., Craven R.J., and Cance W. High focal adhesion kinase expression in invasive breast carcinomas is associated with an aggressive phenotype. Mod. Pathol. 18 (2005) 1289-1294
133. Le Boeuf F., Houle F., Sussman M., and Huot J. Phosphorylation of FAK on Ser732 is induced by ROCK and is essential for Pyk2-mediated phosphorylation of FAK on Tyr407 in response to VEGF. Mol. Biol. Cell 17 (2006) 3508-3520
134. Lev S., Moreno H., Martinez R., Canoll P., Peles E., Musacchio J.M., Plowman G.D., Rudy B., and Schlessinger J. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376 (1995) 737-745
135. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 88 (1997) 323-331
136. Lightfoot Jr. H.M., Lark A., Livasy C.A., Moore D.T., Cowan D., Dressler L., Craven R.J., and 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. 88 (2004) 109-116
137. Ling K., Doughman R.L., Iyer V.V., Firestone A.J., Bairstow S.F., Mosher D.F., Schaller M.D., and Anderson R.A. Tyrosine phosphorylation of type Igamma phosphatidylinositol phosphate kinase by Src regulates an integrin-talin switch. J. Cell Biol. 163 (2003) 1339-1349
138. Liu B., Liao J., Rao X., Kushner S.A., Chung C.D., Chang D.D., and Shuai K. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95 (1998) 10626-10631
139. Liu Y., Loijens J.C., Martin K.H., Karginov A.V., and Parsons J.T. 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 13 (2002) 2147-2156
140. Livasy C.A., Moore D., Cance W.G., and Lininger R.A. Focal adhesion kinase overexpression in endometrial neoplasia. Appl. Immunohistochem. Mol. Morphol. 12 (2004) 342-345
141. Lobo M., and Zachary I. Nuclear localization and apoptotic regulation of an amino-terminal domain focal adhesion kinase fragment in endothelial cells. Biochem. Biophys. Res. Commun. 276 (2000) 1068-1074
142. Lowe S.W., Ruley H.E., Jacks T., and Housman D.E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74 (1993) 957-967
143. Lowe S.W., Jacks T., Housman D.E., and Ruley H.E. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. USA 91 (1994) 2026-2030
144. Madan R., Smolkin M.B., Cocker R., Fayyad R., and Oktay M.H. Focal adhesion proteins as markers of malignant transformation and prognostic indicators in breast carcinoma. Hum. Pathol. 37 (2006) 9-15
145. Matkowskyj K.A., Keller K., Glover S., Kornberg L., Tran-Son-Tay R., and Benya R.V. Expression of GRP and its receptor in well-differentiated colon cancer cells correlates with the presence of focal adhesion kinase phosphorylated at tyrosines 397 and 407. J. Histochem. Cytochem. 51 (2003) 1041-1048
146. Maulik G., Kijima T., Ma P.C., Ghosh S.K., Lin J., Shapiro G.I., Schaefer E., Tibaldi E., Johnson B.E., and Salgia R. Modulation of the c-Met/hepatocyte growth factor pathway in small cell lung cancer. Clin. Cancer Res. 8 (2002) 620-627
147. Maung K., Easty D.J., Hill S.P., and Bennett D.C. Requirement for focal adhesion kinase in tumor cell adhesion. Oncogene 18 (1999) 6824-6828
148. May M.J., D'Acquisto F., Madge L.A., Glockner J., Pober J.S., and Ghosh S. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science 289 (2000) 1550-1554
149. McCormack S.J., Brazinski S.E., Moore Jr. J.L., Werness B.A., and Goldstein D.J. Activation of the focal adhesion kinase signal transduction pathway in cervical carcinoma cell lines and human genital epithelial cells immortalized with human papillomavirus type 18. Oncogene 15 (1997) 265-274
150. McLean G.W., Carragher N.O., Avizienyte E., Evans J., Brunton V.G., and Frame M.C. The role of focal-adhesion kinase in cancer-a new therapeutic opportunity. Nat. Rev. Cancer 5 (2005) 505-515
151. Medley Q.G., Buchbinder E.G., Tachibana K., Ngo H., Serra-Pages C., and Streuli M. Signaling between focal adhesion kinase and trio. J. Biol. Chem. 278 (2003) 13265-13270
152. Melkoumian Z.K., Peng X., Gan B., Wu X., and Guan J.L. Mechanism of cell cycle regulation by FIP200 in human breast cancer cells. Cancer Res. 65 (2005) 6676-6684
153. Mitra S.K., and Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18 (2006) 516-523
154. Mitra S.K., Mikolon D., Molina J.E., Hsia D.A., Hanson D.A., Chi A., Lim S.T., Bernard-Trifilo J.A., Ilic D., Stupack D.G., Cheresh D.A., and Schlaepfer D.D. Intrinsic FAK activity and Y925 phosphorylation facilitate an angiogenic switch in tumors. Oncogene 25 (2006) 5969-5984
155. Miyazaki T., Kato H., Nakajima M., Sohda M., Fukai Y., Masuda N., Manda R., Fukuchi M., Tsukada K., and Kuwano H. FAK overexpression is correlated with tumour invasiveness and lymph node metastasis in oesophageal squamous cell carcinoma. Br. J. Cancer 89 (2003) 140-145
156. Murphy M., Hinman A., and Levine A.J. Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev. 10 (1996) 2971-2980
157. Natarajan M., Stewart J.E., Golemis E.A., Pugacheva E.N., Alexandropoulos K., Cox B.D., Wang W., Grammer J.R., and Gladson C.L. HEF1 is a necessary and specific downstream effector of FAK that promotes the migration of glioblastoma cells. Oncogene 25 (2006) 1721-1732
158. Nishimura M., Machida K., Imaizumi M., Abe T., Umeda T., Takeshima E., Watanabe T., Ohnishi Y., Takagi K., and Hamaguchi M. Tyrosine phosphorylation of 100-130 kDa proteins in lung cancer correlates with poor prognosis. Br. J. Cancer 74 (1996) 780-787
159. Nowakowski J., Cronin C.N., McRee D.E., Knuth M.W., Nelson C.G., Pavletich N.P., Rogers J., Sang B.C., Scheibe D.N., Swanson R.V., and Thompson D.A. Structures of the cancer-related Aurora-A, FAK, and EphA2 protein kinases from nanovolume crystallography. Structure 10 (2002) 1659-1667
160. Okamoto H., Yasui K., Zhao C., Arii S., and Inazawa J. PTK2 and EIF3S3 genes may be amplification targets at 8q23-q24 and are associated with large hepatocellular carcinomas. Hepatology 38 (2003) 1242-1249
161. O'Neill G.M., Fashena S.J., and Golemis E.A. Integrin signalling: A new Cas(t) of characters enters the stage. Trends Cell Biol. 10 (2000) 111-119
162. Oren M. Decision making by p53: Life, death and cancer. Cell Death Differ. 10 (2003) 431-442
163. Owen J.D., Ruest P.J., Fry D.W., and 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. 19 (1999) 4806-4818
164. Owens L.V., Xu L., Craven R.J., Dent G.A., Weiner T.M., Kornberg L., Liu E.T., and Cance W.G. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 55 (1995) 2752-2755
165. Owens L.V., Xu L., Dent G.A., Yang X., Sturge G.C., Craven R.J., and Cance W.G. Focal adhesion kinase as a marker of invasive potential in differentiated human thyroid cancer. Ann. Surg. Oncol. 3 (1996) 100-105
166. Owens L.V., Xu L., Marston W.A., Yang X., Farber M.A., Iacocca M.V., Cance W.G., and Keagy B.A. Overexpression of the focal adhesion kinase (p125FAK) in the vascular smooth muscle cells of intimal hyperplasia. J. Vasc. Surg. 34 (2001) 344-349
167. Park H.B., Xu L.-H., Yang X., and Cance W.G. Activated c-Src rescues cell rounding and loss of adhesion caused by attenuation of the focal adhesion kinase in human breast cancer cells. Surg. Forum L (1999) 346-347
168. Park H.B., Golubovskaya V., Xu L., Yang X., Lee J.W., Scully II S., Craven R.J., and Cance W.G. Activated Src increases adhesion, survival and alpha2-integrin expression in human breast cancer cells. Biochem. J. 378 (2004) 559-567
169. Parsons J.T. Focal adhesion kinase: The first ten years. J. Cell Sci. 116 (2003) 1409-1416
170. Peng X., Ueda H., Zhou H., Stokol T., Shen T.L., Alcaraz A., Nagy T., Vassalli J.D., and Guan J.L. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc. Res. 64 (2004) 421-430
171. Peruzzi B., and Bottaro D.P. Targeting the c-Met signaling pathway in cancer. Clin. Cancer Res. 12 (2006) 3657-3660
172. Poulikakos P.I., Xiao G.H., Gallagher R., Jablonski S., Jhanwar S.C., and Testa J.R. Re-expression of the tumor suppressor NF2/merlin inhibits invasiveness in mesothelioma cells and negatively regulates FAK. Oncogene 25 (2006) 5960-5968
173. Poullet P., Gautreau A., Kadare G., Girault J.A., Louvard D., and Arpin M. Ezrin interacts with focal adhesion kinase and induces its activation independently of cell-matrix adhesion. J. Biol. Chem. 276 (2001) 37686-37691
174. Prutzman K.C., Gao G., King M.L., Iyer V.V., Mueller G.A., Schaller M.D., and Campbell S.L. The focal adhesion targeting domain of focal adhesion kinase contains a hinge region that modulates tyrosine 926 phosphorylation. Structure 12 (2004) 881-891
175. Ratnikov B.I., Partridge A.W., and Ginsberg M.H. Integrin activation by talin. J. Thromb. Haemost. 3 (2005) 1783-1790
176. Ravichandran K.S. Signaling via Shc family adapter proteins. Oncogene 20 (2001) 6322-6330
177. Reiske H.R., Kao S.C., Cary L.A., Guan J.L., Lai J.F., and Chen H.C. Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration. J. Biol. Chem. 274 (1999) 12361-12366
178. Reiske H.R., Zhao J., Han D.C., Cooper L.A., and Guan J.L. Analysis of FAK-associated signaling pathways in the regulation of cell cycle progression. FEBS Lett. 486 (2000) 275-280
179. Richardson A., and Parsons J.T. Signal transduction through integrins: A central role for focal adhesion kinase?. BioEssays 17 (1995) 229-236
180. Salasznyk R.M., Klees R.F., Boskey A., and Plopper G.E. Activation of FAK is necessary for the osteogenic differentiation of human mesenchymal stem cells on laminin-5. J. Cell. Biochem. 100 (2007) 499-514
181. Salasznyk R.M., Klees R.F., Williams W.A., Boskey A., and Plopper G.E. Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp. Cell Res. 313 (2007) 22-37
182. Sasaki H., Nagura K., Ishino M., Tobioka H., Kotani K., and Sasaki T. Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270 (1995) 21206-21219
183. Schaller M.D. Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 1540 (2001) 1-21
184. Schaller M.D. FAK and paxillin: Regulators of N-cadherin adhesion and inhibitors of cell migration?. J. Cell Biol. 166 (2004) 157-159
185. Schaller M.D., and Parsons J.T. Focal adhesion kinase and associated proteins. Curr. Opin. Cell Biol. 6 (1994) 705-710
186. Schaller M.D., Borgman C.A., Cobb B.S., Vines R.R., Reynolds A.B., and Parsons J.T. pp125fak a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89 (1992) 5192-5196
187. Schaller M.D., Hildebrand J.D., Shannon J.D., Fox J.W., Vines R.R., and Parsons J.T. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14 (1994) 1680-1688
188. Schaller M.D., Otey C.A., Hildebrand J.D., and Parsons J.T. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J. Cell Biol. 130 (1995) 1181-1187
189. Schaller M.D., Hildebrand J.D., and Parsons J.T. Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases. Mol. Biol. Cell 10 (1999) 3489-3505
190. Schlaepfer D.D., and Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16 (1996) 5623-5633
191. Schlaepfer D.D., and Mitra S.K. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14 (2004) 92-101
192. Schlaepfer D.D., Hanks S.K., Hunter T., and van der Geer P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372 (1994) 786-791
193. Schlaepfer D.D., Broome M.A., and Hunter T. Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: Involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol. Cell. Biol. 17 (1997) 1702-1713
194. Schlaepfer D.D., Mitra S.K., and Ilic D. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692 (2004) 77-102
195. Schmidt D., and Muller S. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. USA 99 (2002) 2872-2877
196. Schmidt D., and Muller S. PIAS/SUMO: New partners in transcriptional regulation. Cell. Mol. Life Sci. 60 (2003) 2561-2574
197. Schmitz K.J., Grabellus F., Callies R., Otterbach F., Wohlschlaeger J., Levkau B., Kimmig R., Schmid K.W., and Baba H.A. High expression of focal adhesion kinase (p125FAK) in node-negative breast cancer is related to overexpression of HER-2/neu and activated Akt kinase but does not predict outcome. Breast Cancer Res. 7 (2005) R194-R203
198. Schneider G.B., Kurago Z., Zaharias R., Gruman L.M., Schaller M.D., and Hendrix M.J. Elevated focal adhesion kinase expression facilitates oral tumor cell invasion. Cancer 95 (2002) 2508-2515
199. Schroder A., Delling G., and Kaiser E.A. [Expression analysis of protein tyrosine kinases of the FAK (focal adhesion kinase) family in osteosarcoma]. Pathologe 23 (2002) 361-366
200. Scott G., and Liang H. pp125fak in human melanocytes and melanoma: Expression and phosphorylation. Exp. Cell Res. 219 (1995) 197-203
201. Shen T.L., Han D.C., and Guan J.L. Association of Grb7 with phosphoinositides and its role in the regulation of cell migration. J. Biol. Chem. 277 (2002) 29069-29077
202. Shi Q., Hjelmeland A.B., Keir S.T., Song L., Wickman S., Jackson D., Ohmori O., Bigner D.D., Friedman H.S., and Rich J.N. A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol. Carcinog. (2007) Jan. 11 [Epub ahead of print]
203. Sidransky D., Mikkelsen T., Schwechheimer K., Rosenblum M.L., Cavanee W., and Vogelstein B. Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature 355 (1992) 846-847
204. Sieg D.J., Hauck C.R., and Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112 (1999) 2677-2691
205. Sieg D.J., Hauck C.R., Ilic D., Klingbeil C.K., Schaefer E., Damsky C.H., and Schlaepfer D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2 (2000) 249-256
206. Smith C.S., Golubovskaya V.M., Peck E., Xu L.H., Monia B.P., Yang X., and Cance W.G. Effect of focal adhesion kinase (FAK) downregulation with FAK antisense oligonucleotides and 5-fluorouracil on the viability of melanoma cell lines. Melanoma Res. 15 (2005) 357-362
207. Sonoda Y., Matsumoto Y., Funakoshi M., Yamamoto D., Hanks S.K., and Kasahara T. Anti-apoptotic role of focal adhesion kinase (FAK). Induction of inhibitor-of-apoptosis proteins and apoptosis suppression by the overexpression of FAK in a human leukemic cell line, HL-60. J. Biol. Chem. 275 (2000) 16309-16315
208. Sood A.K., Coffin J.E., Schneider G.B., Fletcher M.S., DeYoung B.R., Gruman L.M., Gershenson D.M., Schaller M.D., and Hendrix M.J. Biological significance of focal adhesion kinase in ovarian cancer: Role in migration and invasion. Am. J. Pathol. 165 (2004) 1087-1095
209. Stewart A., Ham C., and Zachary I. The focal adhesion kinase amino-terminal domain localises to nuclei and intercellular junctions in HEK 293 and MDCK cells independently of tyrosine 397 and the carboxy-terminal domain. Biochem. Biophys. Res. Commun. 299 (2002) 62-73
210. Stoklsa T., and Golab J. Prospects for p53-based cancer therapy. Acta Biochim. Pol. 52 (2005) 321-328
211. Takahashi N., Seko Y., Noiri E., Tobe K., Kadowaki T., Sabe H., and Yazaki Y. Vascular endothelial growth factor induces activation and subcellular translocation of focal adhesion kinase (p125FAK) in cultured rat cardiac myocytes. Circ. Res. 84 (1999) 1194-1202
212. Takino T., Yoshioka K., Miyamori H., Yamada K.M., and Sato H. A scaffold protein in the c-Jun N-terminal kinase signaling pathway is associated with focal adhesion kinase and tyrosine-phosphorylated. Oncogene 21 (2002) 6488-6497
213. Takino T., Nakada M., Miyamori H., Watanabe Y., Sato T., Gantulga D., Yoshioka K., Yamada K.M., and Sato H. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J. Biol. Chem. 280 (2005) 37772-37781
214. Tamura M., Gu J., Matsumoto K., Aota S., Parsons R., and Yamada K.M. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280 (1998) 1614-1617
215. Tamura M., Gu J., Danen E.H., Takino T., Miyamoto S., and 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. 274 (1999) 20693-20703
216. Tamura M., Gu J., Takino T., and Yamada K.M. Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: Differential involvement of focal adhesion kinase and p130Cas. Cancer Res. 59 (1999) 442-449
217. Taylor J.M., Macklem M.M., and Parsons J.T. Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho. J. Cell Sci. 112 Pt. 2 (1999) 231-242
218. Taylor W.R., and Stark G.R. Regulation of the G2/M transition by p53. Oncogene 20 (2001) 1803-1815
219. Thakar J., Schleinkofer K., Borner C., and Dandekar T. RIP death domain structural interactions implicated in TNF-mediated proliferation and survival. Proteins 63 (2006) 413-423
220. Theocharis S.E., Kouraklis G.P., Kakisis J.D., Kanelli H.G., Apostolakou F.E., Karatzas G.M., and Koutselinis A.S. Focal adhesion kinase expression is not a prognostic predictor in colon adenocarcinoma patients. Eur. J. Surg. Oncol. 29 (2003) 571-574
221. Thomas J.W., Ellis B., Boerner R.J., Knight W.B., White II G.C., and Schaller M.D. SH2- and SH3-mediated interactions between focal adhesion kinase and Src. J. Biol. Chem. 273 (1998) 577-583
222. Tilghman R.W., Slack-Davis J.K., Sergina N., Martin K.H., Iwanicki M., Hershey E.D., Beggs H.E., Reichardt L.F., and Parsons J.T. Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J. Cell Sci. 118 (2005) 2613-2623
223. Tremblay L., Hauck W., Aprikian A.G., Begin L.R., Chapdelaine A., and Chevalier S. Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int. J. Cancer 68 (1996) 164-171
224. Turner C.E. Paxillin. Int. J. Biochem. Cell Biol. 30 (1998) 955-959
225. Turner C.E. Paxillin interactions. J. Cell Sci. 113 Pt. 23 (2000) 4139-4140
226. van De Water B., Houtepen F., Huigsloot M., and Tijdens I.B. Suppression of chemically induced apoptosis but not necrosis of renal proximal tubular epithelial (LLC-PK1) cells by focal adhesion kinase (FAK). Role of FAK in maintaining focal adhesion organization after acute renal cell injury. J. Biol. Chem. 276 (2001) 36183-36193
227. van Nimwegen M.J., Verkoeijen S., van Buren L., Burg D., and van de Water B. Requirement for focal adhesion kinase in the early phase of mammary adenocarcinoma lung metastasis formation. Cancer Res. 65 (2005) 4698-4706
228. van Nimwegen M.J., Huigsloot M., Camier A., Tijdens I.B., and van de Water B. Focal adhesion kinase and protein kinase B cooperate to suppress doxorubicin-induced apoptosis of breast tumor cells. Mol. Pharmacol. 70 (2006) 1330-1339
229. van Rooij E., Doevendans P.A., de Theije C.C., Babiker F.A., Molkentin J.D., and de Windt L.J. Requirement of nuclear factor of activated T-cells in calcineurin-mediated cardiomyocyte hypertrophy. J. Biol. Chem. 277 (2002) 48617-48626
230. Vassilev L.T. p53 Activation by small molecules: Application in oncology. J. Med. Chem. 48 (2005) 4491-4499
231. Venables J.P. Unbalanced alternative splicing and its significance in cancer. Bioessays 28 (2006) 378-386
232. von Sengbusch A., Gassmann P., Fisch K.M., Enns A., Nicolson G.L., and Haier J. Focal adhesion kinase regulates metastatic adhesion of carcinoma cells within liver sinusoids. Am. J. Pathol. 166 (2005) 585-596
233. Vousden K.H., and Woude G.F. The ins and outs of p53. Nat. Cell Biol. 2 (2000) E178-E180
234. Wade R., and Vande Pol S. Minimal features of paxillin that are required for the tyrosine phosphorylation of focal adhesion kinase. Biochem. J. 393 (2006) 565-573
235. Wang W., Rastinejad F., and El-Deiry W.S. Restoring p53-dependent tumor suppression. Cancer Biol. Ther. 2 (2003) S55-S63
236. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., Liu J., Zhao X.D., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 124 (2006) 207-219
237. Weiner T.M., Liu E.T., Craven R.J., and Cance W.G. Expression of focal adhesion kinase gene and invasive cancer. Lancet 342 (1993) 1024-1025
238. Weiner T.M., Liu E.T., Craven R.J., and Cance W.G. Expression of growth factor receptors, the focal adhesion kinase, and other tyrosine kinases in human soft tissue tumors. Ann. Surg. Oncol. 1 (1994) 18-27
239. Whitney G.S., Chan P.Y., Blake J., Cosand W.L., Neubauer M.G., Aruffo A., and Kanner S.B. Human T and B lymphocytes express a structurally conserved focal adhesion kinase, pp125FAK. DNA Cell Biol. 12 (1993) 823-830
240. Willis A.C., and Chen X. The promise and obstacle of p53 as a cancer therapeutic agent. Curr. Mol. Med. 2 (2002) 329-345
241. Windham T.C., Parikh N.U., Siwak D.R., Summy J.M., McConkey D.J., Kraker A.J., and Gallick G.E. Src activation regulates anoikis in human colon tumor cell lines. Oncogene 21 (2002) 7797-7807
242. Wu Y., Mehew J.W., Heckman C.A., Arcinas M., and Boxer L.M. Negative regulation of bcl-2 expression by p53 in hematopoietic cells. Oncogene 20 (2001) 240-251
243. Xie Z., Sanada K., Samuels B.A., Shih H., and Tsai L.H. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114 (2003) 469-482
244. Xing Z., Chen H.C., Nowlen J.K., Taylor S.J., Shalloway D., and Guan J.L. Direct interaction of v-Src with the focal adhesion kinase mediated by the Src SH2 domain. Mol. Biol. Cell 5 (1994) 413-421
245. Xu L.H., Owens L.V., Sturge G.C., Yang X., Liu E.T., Craven R.J., and Cance W.G. Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ. 7 (1996) 413-418
246. Xu L.H., Yang X., Craven R.J., and Cance W.G. The COOH-terminal domain of the focal adhesion kinase induces loss of adhesion and cell death in human tumor cells. Cell Growth Differ. 9 (1998) 999-1005
247. Xu L.-H., Yang X.-H., Bradham C.A., Brenner D.A., Baldwin A.S., Craven R.J., and Cance W.G. The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. J. Biol. Chem. 275 (2000) 30597-30604
248. Yang T.H., Chen C.T., Wang C.P., and Lou P.J. Photodynamic therapy suppresses the migration and invasion of head and neck cancer cells in vitro. Oral Oncol. 43 (2006) 358-365
249. Yeo M.G., Partridge M.A., Ezratty E.J., Shen Q., Gundersen G.G., and Marcantonio E.E. Src SH2 arginine 175 is required for cell motility: Specific focal adhesion kinase targeting and focal adhesion assembly function. Mol. Cell. Biol. 26 (2006) 4399-4409
250. Yonish-Rouach E., Resnitzky D., Lotem J., Sachs L., Kimchi A., and Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 352 (1991) 345-347
251. Yu H., Chen J.K., Feng S., Dalgarno D.C., Brauer A.W., and Schreiber S.L. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76 (1994) 933-945
252. Yu H.G., Schrader H., Otte J.M., Schmidt W.E., and Schmitz F. Rapid tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130Cas by gastrin in human colon cancer cells. Biochem. Pharmacol. 67 (2004) 135-146
253. Yu H.G., Tong S.L., Ding Y.M., Ding J., Fang X.M., Zhang X.F., Liu Z.J., Zhou Y.H., Liu Q.S., Luo H.S., and Yu J.P. Enhanced expression of cholecystokinin-2 receptor promotes the progression of colon cancer through activation of focal adhesion kinase. Int. J. Cancer 119 (2006) 2724-2732
254. Zeng Z.Z., Jia Y., Hahn N.J., Markwart S.M., Rockwood K.F., and Livant D.L. Role of focal adhesion kinase and phosphatidylinositol 3′-kinase in integrin fibronectin receptor-mediated, matrix metalloproteinase-1-dependent invasion by metastatic prostate cancer cells. Cancer Res. 66 (2006) 8091-8099
255. Zhai J., Lin H., Nie Z., Wu J., Canete-Soler R., Schlaepfer W.W., and Schlaepfer D.D. Direct interaction of focal adhesion kinase with p190RhoGEF. J. Biol. Chem. 278 (2003) 24865-24873
256. Zhang W., Kadam S., Emerson B.M., and Bieker J.J. Site-specific acetylation by p300 or CREB binding protein regulates erythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol. Cell. Biol. 21 (2001) 2413-2422
257. Zhang X., Wright C.V., and Hanks S.K. Cloning of a Xenopus laevis cDNA encoding focal adhesion kinase (FAK) and expression during early development. Gene 160 (1995) 219-222
258. Zhang Y., Lu H., Dazin P., and Kapila Y.L. Squamous cell carcinoma cell aggregates escape suspension-induced, p53-mediated anoikis: Fibronectin and integrin (alpha)v mediate survival signals through focal adhesion kinase. J. Biol. Chem. 279 (2004) 48342-48349
259. Zhao L.Y., Colosimo A.L., Liu Y., Wan Y., and Liao D. Adenovirus E1B 55-kilodalton oncoprotein binds to Daxx and eliminates enhancement of p53-dependent transcription by Daxx. J. Virol. 77 (2003) 11809-11821
260. Zheng D.Q., Woodard A.S., Fornaro M., Tallini G., and Languino L.R. Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res. 59 (1999) 1655-1664