Focal Adhesion Kinase Controls Cellular Levels of p27/Kip1 and p21/Cip1 through Skp2-Dependent and -Independent Mechanisms

REFERENCES

• Abid, M. R., K. Yano, S. Guo, V. I. Patel, G. Shrikhande, K. C. Spokes, C. Ferran, and W. C. Aird. 2005. Forkhead transcription factors inhibit vascular smooth muscle cell proliferation and neointimal hyperplasia. J. Biol. Chem. 280:29864–29873. (First published 15 June 2005; 10.1074/jbc.M502149200.)
   PubMed Web of Science ®Google Scholar
• Abu-Ghazaleh, R., J. Kabir, H. Jia, M. Lobo, and I. Zachary. 2001. 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. 360:255–264.
   PubMed Web of Science ®Google Scholar
• Alavi, A., J. D. Hood, R. Frausto, D. G. Stupack, and D. A. Cheresh. 2003. Role of Raf in vascular protection from distinct apoptotic stimuli. Science 301:94–96.
   PubMed Web of Science ®Google Scholar
• Aplin, A. E., S. A. Stewart, R. K. Assoian, and R. L. Juliano. 2001. Integrin-mediated adhesion regulates ERK nuclear translocation and phosphorylation of Elk-1. J. Cell Biol. 153:273–282.
   PubMed Web of Science ®Google Scholar
• Assoian, R. K., and M. A. Schwartz. 2001. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11:48–53.
   PubMed Web of Science ®Google Scholar
• Avraham, H. K., T. H. Lee, Y. Koh, T. A. Kim, S. Jiang, M. Sussman, A. M. Samarel, and S. Avraham. 2003. 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. 278:36661–36668.
   PubMedGoogle Scholar
• Baldassarre, G., B. Belletti, P. Bruni, A. Boccia, F. Trapasso, F. Pentimalli, M. V. Barone, G. Chiappetta, M. T. Vento, S. Spiezia, A. Fusco, and G. Viglietto. 1999. Overexpressed cyclin D3 contributes to retaining the growth inhibitor p27 in the cytoplasm of thyroid tumor cells. J. Clin. Investig. 104:865–874.
   PubMed Web of Science ®Google Scholar
• Bao, W., M. Thullberg, H. Zhang, A. Onischenko, and S. Strömblad. 2002. Cell attachment to the extracellular matrix induces proteasomal degradation of p21CIP1 via Cdc42/Rac1 signaling. Mol. Cell. Biol. 22:4587–4597.
   PubMedGoogle Scholar
• Bashir, T., N. V. Dorrello, V. Amador, D. Guardavaccaro, and M. Pagano. 2004. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428:190–193.
   PubMed Web of Science ®Google Scholar
• Ben-Izhak, O., S. Lahav-Baratz, S. Meretyk, S. Ben-Eliezer, E. Sabo, M. Dirnfeld, S. Cohen, and A. Ciechanover. 2003. Inverse relationship between Skp2 ubiquitin ligase and the cyclin dependent kinase inhibitor p27Kip1 in prostate cancer. J. Urol. 170:241–245.
   PubMed Web of Science ®Google Scholar
• Blagosklonny, M. V., P. Giannakakou, L. Y. Romanova, K. M. Ryan, K. H. Vousden, and T. Fojo. 2001. Inhibition of HIF-1- and wild-type p53-stimulated transcription by codon Arg175 p53 mutants with selective loss of functions. Carcinogenesis 22:861–867.
   PubMedGoogle Scholar
• Bond, M., G. B. Sala-Newby, and A. C. Newby. 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.
   PubMedGoogle Scholar
• Bornstein, G., J. Bloom, D. Sitry-Shevah, K. Nakayama, M. Pagano, and A. Hershko. 2003. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 278:25752–25757.
   PubMed Web of Science ®Google Scholar
• Bottazzi, M. E., X. Zhu, R. M. Bohmer, and R. K. Assoian. 1999. Regulation of p21(cip1) expression by growth factors and the extracellular matrix reveals a role for transient ERK activity in G1 phase. J. Cell Biol. 146:1255–1264.
   PubMed Web of Science ®Google Scholar
• Carmeliet, P., and R. K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature 407:249–257.
   PubMed Web of Science ®Google Scholar
• Carrano, A. C., and M. Pagano. 2001. Role of the F-box protein Skp2 in adhesion-dependent cell cycle progression. J. Cell Biol. 153:1381–1390.
   PubMed Web of Science ®Google Scholar
• Chen, C. S., M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber. 1997. Geometric control of cell life and death. Science 276:1425–1428.
   PubMed Web of Science ®Google Scholar
• Chen, X., Y. Chi, A. Bloecher, R. Aebersold, B. E. Clurman, and J. M. Roberts. 2004. N-acetylation and ubiquitin-independent proteasomal degradation of p21(Cip1). Mol. Cell 16:839–847.
   PubMedGoogle Scholar
• Cheng, M., P. Olivier, J. A. Diehl, M. Fero, M. F. Roussel, J. M. Roberts, and C. J. Sherr. 1999. The p21(Cip1) and p27(Kip1) CDK ‘inhibitors’ are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18:1571–1583.
   PubMed Web of Science ®Google Scholar
• DeGregori, J., T. Kowalik, and J. R. Nevins. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell. Biol. 15:4215–4224.
   PubMed Web of Science ®Google Scholar
• Deshaies, R. J. 1999. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15:435–467.
   PubMed Web of Science ®Google Scholar
• Drobnjak, M., J. Melamed, S. Taneja, K. Melzer, R. Wieczorek, B. Levinson, A. Zeleniuch-Jacquotte, D. Polsky, J. Ferrara, R. Perez-Soler, C. Cordon-Cardo, M. Pagano, and I. Osman. 2003. Altered expression of p27 and Skp2 proteins in prostate cancer of African-American patients. Clin. Cancer Res. 9:2613–2619.
   PubMed Web of Science ®Google Scholar
• el-Deiry, W. S., J. W. Harper, P. M. O'Connor, V. E. Velculescu, C. E. Canman, J. Jackman, J. A. Pietenpol, M. Burrell, D. E. Hill, Y. Wang, et al. 1994. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1169–1174.
   PubMed Web of Science ®Google Scholar
• Eliceiri, B. P., X. S. Puente, J. D. Hood, D. G. Stupack, D. D. Schlaepfer, X. Z. Huang, D. Sheppard, and D. A. Cheresh. 2002. Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signaling. J. Cell Biol. 157:149–160.
   PubMed Web of Science ®Google Scholar
• Folkman, J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1:27–31.
   PubMed Web of Science ®Google Scholar
• Folkman, J., and A. Moscona. 1978. Role of cell shape in growth control. Nature 273:345–349.
   PubMed Web of Science ®Google Scholar
• Gilmore, A. P., and L. H. Romer. 1996. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell 7:1209–1224.
   PubMed Web of Science ®Google Scholar
• He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
   PubMed Web of Science ®Google Scholar
• Hecker, T. P., J. R. Grammer, G. Y. Gillespie, J. Stewart, Jr., and C. L. Gladson. 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.
   PubMed Web of Science ®Google Scholar
• Heidkamp, M. C., A. L. Bayer, J. A. Kalina, D. M. Eble, and A. M. Samarel. 2002. GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ. Res. 90:1282–1289.
   PubMedGoogle Scholar
• Holinstat, M., N. Knezevic, M. Broman, A. M. Samarel, A. B. Malik, and D. Mehta. 2005. Suppression of RhoA activity by focal adhesion kinase-induced activation of p190RhoGAP: role in regulation of endothelial permeability. J. Biol. Chem. 281:2296–2305. (First published 24 November 2005; 10.1074/jbc.M511248200.)
   PubMedGoogle Scholar
• Huang, S., C. S. Chen, and D. E. Ingber. 1998. Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol. Biol. Cell 9:3179–3193.
   PubMed Web of Science ®Google Scholar
• Ilic, D., E. A. Almeida, D. D. Schlaepfer, P. Dazin, S. Aizawa, and C. H. Damsky. 1998. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J. Cell Biol. 143:547–560.
   PubMed Web of Science ®Google Scholar
• Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539–544.
   PubMed Web of Science ®Google Scholar
• Imaki, H., K. Nakayama, S. Delehouzee, H. Handa, M. Kitagawa, T. Kamura, and K. I. Nakayama. 2003. Cell cycle-dependent regulation of the Skp2 promoter by GA-binding protein. Cancer Res. 63:4607–4613.
   PubMedGoogle Scholar
• Ingber, D. E. 1990. Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc. Natl. Acad. Sci. USA 87:3579–3583.
   PubMed Web of Science ®Google Scholar
• Joseph, B., M. Orlian, and H. Furneaux. 1998. p21(waf1) mRNA contains a conserved element in its 3′-untranslated region that is bound by the Elav-like mRNA-stabilizing proteins. J. Biol. Chem. 273:20511–20516.
   PubMedGoogle Scholar
• Kim, S. Y., A. Herbst, K. A. Tworkowski, S. E. Salghetti, and W. P. Tansey. 2003. Skp2 regulates Myc protein stability and activity. Mol. Cell 11:1177–1188.
   PubMed Web of Science ®Google Scholar
• King, R. W., R. J. Deshaies, J. M. Peters, and M. W. Kirschner. 1996. How proteolysis drives the cell cycle. Science 274:1652–1659.
   PubMed Web of Science ®Google Scholar
• Kornberg, L., H. S. Earp, J. T. Parsons, M. Schaller, and R. L. Juliano. 1992. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267:23439–23442.
   PubMed Web of Science ®Google Scholar
• Koshiji, M., Y. Kageyama, E. A. Pete, I. Horikawa, J. C. Barrett, and L. E. Huang. 2004. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J. 23:1949–1956.
   PubMed Web of Science ®Google Scholar
• Kullmann, M., U. Gopfert, B. Siewe, and L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev. 16:3087–3099.
   PubMed Web of Science ®Google Scholar
• LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847–862.
   PubMed Web of Science ®Google Scholar
• Ledford, A. W., J. G. Brantley, G. Kemeny, T. L. Foreman, S. E. Quaggin, P. Igarashi, S. M. Oberhaus, M. Rodova, J. P. Calvet, and G. B. Vanden Heuvel. 2002. Deregulated expression of the homeobox gene Cux-1 in transgenic mice results in downregulation of p27(kip1) expression during nephrogenesis, glomerular abnormalities, and multiorgan hyperplasia. Dev. Biol. 245:157–171.
   PubMedGoogle Scholar
• Li, S., M. Kim, Y. L. Hu, S. Jalali, D. D. Schlaepfer, T. Hunter, S. Chien, and J. Y. Shyy. 1997. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J. Biol. Chem. 272:30455–30462.
   PubMed Web of Science ®Google Scholar
• Madri, J. A., B. M. Pratt, and J. Yannariello-Brown. 1988. Matrix-driven cell size change modulates aortic endothelial cell proliferation and sheet migration. Am. J. Pathol. 132:18–27.
   PubMed Web of Science ®Google Scholar
• Mammoto, A., S. Huang, K. Moore, P. Oh, and D. E. Ingber. 2004. Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J. Biol. Chem. 279:26323–26330.
   PubMed Web of Science ®Google Scholar
• McMullen, M. E., P. W. Bryant, C. C. Glembotski, P. A. Vincent, and K. M. Pumiglia. 2005. Activation of p38 has opposing effects on the proliferation and migration of endothelial cells. J. Biol. Chem. 280:20995–21003.
   PubMed Web of Science ®Google Scholar
• Meadows, K. N., P. Bryant, and K. Pumiglia. 2001. Vascular endothelial growth factor induction of the angiogenic phenotype requires Ras activation. J. Biol. Chem. 276:49289–49298.
   PubMed Web of Science ®Google Scholar
• Meadows, K. N., P. Bryant, P. A. Vincent, and K. M. Pumiglia. 2004. Activated Ras induces a proangiogenic phenotype in primary endothelial cells. Oncogene 23:192–200.
   PubMed Web of Science ®Google Scholar
• Melendez, J., S. Welch, E. Schaefer, C. S. Moravec, S. Avraham, H. Avraham, and M. A. Sussman. 2002. Activation of pyk2/related focal adhesion tyrosine kinase and focal adhesion kinase in cardiac remodeling. J. Biol. Chem. 277:45203–45210.
   PubMedGoogle Scholar
• Mettouchi, A., S. Klein, W. Guo, M. Lopez-Lago, E. Lemichez, J. K. Westwick, and F. G. Giancotti. 2001. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol. Cell 8:115–127.
   PubMed Web of Science ®Google Scholar
• Mirza, A. M., S. Gysin, N. Malek, K.-I. Nakayama, J. M. Roberts, and M. McMahon. 2004. Cooperative regulation of the cell division cycle by the protein kinases RAF and AKT. Mol. Cell. Biol. 24:10868–10881.
   PubMed Web of Science ®Google Scholar
• Morrison, T. B., J. J. Weis, and C. T. Wittwer. 1998. Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. BioTechniques 24:954–958, 960, 962.
   PubMed Web of Science ®Google Scholar
• Nakayama, K. I., S. Hatakeyama, and K. Nakayama. 2001. Regulation of the cell cycle at the G1-S transition by proteolysis of cyclin E and p27Kip1. Biochem. Biophys. Res. Commun. 282:853–860.
   PubMed Web of Science ®Google Scholar
• Natarajan, M., T. P. Hecker, and C. L. Gladson. 2003. FAK signaling in anaplastic astrocytoma and glioblastoma tumors. Cancer J. 9:126–133.
   PubMedGoogle Scholar
• Pagano, M., S. W. Tam, A. M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P. R. Yew, G. F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269:682–685.
   PubMed Web of Science ®Google Scholar
• Potente, M., B. Fisslthaler, R. Busse, and I. Fleming. 2003. 11,12-Epoxyeicosatrienoic acid-induced inhibition of FOXO factors promotes endothelial proliferation by down-regulating p27Kip1. J. Biol. Chem. 278:29619–29625.
   PubMed Web of Science ®Google Scholar
• Pumiglia, K. M., and S. J. Decker. 1997. Cell cycle arrest mediated by the MEK/mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA 94:448–452.
   PubMed Web of Science ®Google Scholar
• Richardson, A., and T. Parsons. 1996. A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 380:538–540.
   PubMed Web of Science ®Google Scholar
• Richardson, P. 2003. Clinical update: proteasome inhibitors in hematologic malignancies. Cancer Treat. Rev. 29(Suppl. 1):33–39.
   PubMedGoogle Scholar
• Risau, W. 1997. Mechanisms of angiogenesis. Nature 386:671–674.
   PubMed Web of Science ®Google Scholar
• Sa, G., and D. W. Stacey. 2004. P27 expression is regulated by separate signaling pathways, downstream of Ras, in each cell cycle phase. Exp. Cell Res. 300:427–439.
   PubMedGoogle Scholar
• Schulze, A., K. Zerfass-Thome, J. Bergès, S. Middendorp, P. Jansen-Dürr, and B. Henglein. 1996. Anchorage-dependent transcription of the cyclin A gene. Mol. Cell. Biol. 16:4632–4638.
   PubMedGoogle Scholar
• Schwartz, M. A., and R. K. Assoian. 2001. Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 114:2553–2560.
   PubMed Web of Science ®Google Scholar
• Sheaff, R. J., J. D. Singer, J. Swanger, M. Smitherman, J. M. Roberts, and B. E. Clurman. 2000. Proteasomal turnover of p21Cip1 does not require p21Cip1 ubiquitination. Mol. Cell 5:403–410.
   PubMed Web of Science ®Google Scholar
• Shen, T. L., A. Y. Park, A. Alcaraz, X. Peng, I. Jang, P. Koni, R. A. Flavell, H. Gu, and J. L. Guan. 2005. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169:941–952.
   PubMed Web of Science ®Google Scholar
• Shen, Y., and M. D. Schaller. 1999. Focal adhesion targeting: the critical determinant of FAK regulation and substrate phosphorylation. Mol. Biol. Cell 10:2507–2518.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149–1163.
   PubMed Web of Science ®Google Scholar
• Sieg, D. J., C. R. Hauck, and D. D. Schlaepfer. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112:2677–2691.
   PubMed Web of Science ®Google Scholar
• Sood, A. K., J. E. Coffin, G. B. Schneider, M. S. Fletcher, B. R. DeYoung, L. M. Gruman, D. M. Gershenson, M. D. Schaller, and M. J. Hendrix. 2004. Biological significance of focal adhesion kinase in ovarian cancer: role in migration and invasion. Am. J. Pathol. 165:1087–1095.
   PubMed Web of Science ®Google Scholar
• Stewart, S. A., D. Kothapalli, Y. Yung, and R. K. Assoian. 2004. Antimitogenesis linked to regulation of Skp2 gene expression. J. Biol. Chem. 279:29109–29113.
   PubMedGoogle Scholar
• Sutterluty, H., E. Chatelain, A. Marti, C. Wirbelauer, M. Senften, U. Muller, and W. Krek. 1999. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat. Cell Biol. 1:207–214.
   PubMed Web of Science ®Google Scholar
• Takuwa, N., and Y. Takuwa. 1997. Ras activity late in G1 phase required for p27kip1 downregulation, passage through the restriction point, and entry into S phase in growth factor-stimulated NIH 3T3 fibroblasts. Mol. Cell. Biol. 17:5348–5358.
   PubMed Web of Science ®Google Scholar
• Tanner, F. C., M. Boehm, L. M. Akyurek, H. San, Z. Y. Yang, J. Tashiro, G. J. Nabel, and E. G. Nabel. 2000. Differential effects of the cyclin-dependent kinase inhibitors p27(Kip1), p21(Cip1), and p16(Ink4) on vascular smooth muscle cell proliferation. Circulation 101:2022–2025.
   PubMedGoogle Scholar
• Touitou, R., J. Richardson, S. Bose, M. Nakanishi, J. Rivett, and M. J. Allday. 2001. A degradation signal located in the C-terminus of p21WAF1/CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. EMBO J. 20:2367–2375.
   PubMed Web of Science ®Google Scholar
• Tyers, M., and P. Jorgensen. 2000. Proteolysis and the cell cycle: with this RING I do thee destroy. Curr. Opin. Genet. Dev. 10:54–64.
   PubMed Web of Science ®Google Scholar
• Vermeulen, K., D. R. Van Bockstaele, and Z. N. Berneman. 2003. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 36:131–149.
   PubMed Web of Science ®Google Scholar
• Wang, F., R. K. Hansen, D. Radisky, T. Yoneda, M. H. Barcellos-Hoff, O. W. Petersen, E. A. Turley, and M. J. Bissell. 2002. Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J. Natl. Cancer Inst. 94:1494–1503.
   PubMedGoogle Scholar
• Wei, W., N. G. Ayad, Y. Wan, G. J. Zhang, M. W. Kirschner, and W. G. Kaelin, Jr. 2004. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428:194–198.
   PubMed Web of Science ®Google Scholar
• Weintraub, S. J., C. A. Prater, and D. C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358:259–261.
   PubMed Web of Science ®Google Scholar
• Zeng, H., H. F. Dvorak, and D. Mukhopadhyay. 2001. Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) receptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 276:26969–26979.
   PubMed Web of Science ®Google Scholar
• Zhang, L., and C. Wang. 5 December 2005, posting date. F-box protein Skp2: a novel transcriptional target of E2F. Oncogene [Online.] 10.1038/sj.onc.1209286.
   Google Scholar
• Zhao, J., R. Pestell, and J. L. Guan. 2001. Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol. Biol. Cell 12:4066–4077.
   PubMed Web of Science ®Google Scholar
• Zhao, J. H., H. Reiske, and J. L. Guan. 1998. Regulation of the cell cycle by focal adhesion kinase. J. Cell Biol. 143:1997–2008.
   PubMed Web of Science ®Google Scholar
• Zhu, N. W., C. M. Perks, A. R. Burd, and J. M. Holly. 1999. Changes in the levels of integrin and focal adhesion kinase (FAK) in human melanoma cells following 532 nm laser treatment. Int. J. Cancer 82:353–358.
   PubMedGoogle Scholar
• Zhu, X., M. Ohtsubo, R. M. Bohmer, J. M. Roberts, and R. K. Assoian. 1996. Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J. Cell Biol. 133:391–403.
   PubMed Web of Science ®Google Scholar