Nuclear FAK: A new mode of gene regulation from cellular adhesions

Molecules and Cells

Volumn 36, Issue 1, 2013, Pages 1-6

  Lim, Ssang Taek Steve ^a  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

Cell Proliferation; Fak; Ferm; Gata4; Inflammation; P53

Indexed keywords

FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR;

CELL ADHESION; CELLULAR DISTRIBUTION; CYTOSOL; FOCAL ADHESION; GENE CONTROL; INFLAMMATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL NUCLEUS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE EXPRESSION REGULATION; HUMANS; SIGNAL TRANSDUCTION;

EID: 84877772571     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-013-0139-1     Document Type: Review

References (51)

1. Ahmad, M., Theofanidis, P., and Medford, R.M. (1998). Role of activating protein-1 in the regulation of the vascular cell adhesion molecule-1 gene expression by tumor necrosis factor-Alpha. J. Biol. Chem. 273, 4616-4621.
2. Ahn, S., and Park, H. (2010). XIAP is essential for shear stressenhanced Tyr-576 phosphorylation of FAK. Biochem. Biophys. Res. Commun. 399, 256-261.
3. Aoto, H., Sasaki, H., Ishino, M., and Sasaki, T. (2002). Nuclear translocation of cell adhesion kinase beta/proline-rich tyrosine kinase 2. Cell Struct. Funct. 27, 47-61.
4. Bagi, C.M., Christensen, J., Cohen, D.P., Roberts, W.G., Wilkie, D., Swanson, T., Tuthill, T., and Andresen, C.J. (2009). Sunitinib and PF-562,271 (FAK/Pyk2 inhibitor) effectively block growth and recovery of human hepatocellular carcinoma in a rat xenograft model. Cancer Biol. Ther. 8, 856-865.
5. Braren, R., Hu, H., Kim, Y.H., Beggs, H.E., Reichardt, L.F., and Wang, R. (2006). Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 172, 151-162.
6. Cai, X., Lietha, D., Ceccarelli, D.F., Karginov, A.V., Rajfur, Z., Jacobson, K., Hahn, K.M., Eck, M.J., and Schaller, M.D. (2008). Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol. Cell. Biol. 28, 201-214.
7. Carter, R.A., and Wicks, I.P. (2001). Vascular cell adhesion molecule 1 (CD106): a multifaceted regulator of joint inflammation. Arthritis Rheum. 44, 985-994.
8. Ceccarelli, D.F., Song, H.K., Poy, F., Schaller, M.D., and Eck, M.J. (2006). Crystal structure of the FERM domain of focal adhesion kinase. J. Biol. Chem. 281, 252-259.
9. Cooper, J., Li, W., You, L., Schiavon, G., Pepe-Caprio, A., Zhou, L., Ishii, R., Giovannini, M., Hanemann, C.O., Long, S.B., et al. (2011). Merlin/NF2 functions upstream of the nuclear E3 ubiquitin ligase CRL4DCAF1 to suppress oncogenic gene expression. Sci. Signal. 4, pt6.
10. Cybulsky, M.I., Iiyama, K., Li, H., Zhu, S., Chen, M., Iiyama, M., Davis, V., Gutierrez-Ramos, J.C., Connelly, P.W., and Milstone, D.S. (2001). A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J. Clin. Invest. 107, 1255-1262.
11. Dai, Q., Zhang, C., Wu, Y., McDonough, H., Whaley, R.A., Godfrey, V., Li, H.H., Madamanchi, N., Xu, W., Neckers, L., et al. (2003). CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 22, 5446-5458.
12. Dikic, I., and Schlessinger, J. (1998). Identification of a new Pyk2 isoform implicated in chemokine and antigen receptor signaling. J. Biol. Chem. 273, 14301-14308.
13. Dong, J.M., Lau, L.S., Ng, Y.W., Lim, L., and Manser, E. (2009). Paxillin nuclear-cytoplasmic localization is regulated by phosphorylation of the LD4 motif: evidence that nuclear paxillin promotes cell proliferation. Biochem. J. 418, 173-184.
14. Frame, M.C., Patel, H., Serrels, B., Lietha, D., and Eck, M.J. (2010). The FERM domain: organizing the structure and function of FAK. Nat. Rev. Mol. Cell Biol. 11, 802-814.
15. Furuta, Y., Ilic, D., Kanazawa, S., Takeda, N., Yamamoto, T., and Aizawa, S. (1995). Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 11, 1989-1995.
16. Gurtner, G.C., Davis, V., Li, H., McCoy, M.J., Sharpe, A., and Cybulsky, M.I. (1995). Targeted disruption of the murine VCAM1 gene, essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 9, 1-14.
17. Ili?, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
18. Inman, K.E., and Downs, K.M. (2007). The murine allantois, emerging paradigms in development of the mammalian umbilical cord and its relation to the fetus. Genesis 45, 237-258.
19. Karin, M., and Gallagher, E. (2009). TNFR signaling, ubiquitin-conjugated TRAFfic signals control stop-And-go for MAPK signaling complexes. Immunol. Rev. 228, 225-240.
20. Klingbeil, C.K., Hauck, C.R., Hsia, D.A., Jones, K.C., Reider, S.R., and Schlaepfer, D.D. (2001). Targeting Pyk2 to beta 1-integrincontaining focal contacts rescues fibronectin-stimulated signaling and haptotactic motility defects of focal adhesion kinase-null cells. J. Cell Biol. 152, 97-110.
21. Kobayashi, S., Mao, K., Zheng, H., Wang, X., Patterson, C., O'Connell, T.D., and Liang, Q. (2007). Diminished GATA4 protein levels contribute to hyperglycemia-induced cardiomyocyte injury. J. Biol. Chem. 282, 21945-21952.
22. Kwee, L., Baldwin, H.S., Shen, H.M., Stewart, C.L., Buck, C., Buck, C.A., and Labow, M.A. (1995). Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121, 489-503.
23. Lawson, C., Lim, S.T., Uryu, S., Chen, X.L., Calderwood, D.A., and Schlaepfer, D.D. (2012). FAK promotes recruitment of talin to nascent adhesions to control cell motility. J. Cell Biol. 196, 223-232.
24. Lev, S., Moreno, H., Martinez, R., Canoll, P., Peles, E., Musacchio, J.M., Plowman, G.D., Rudy, B., and Schlessinger, J. (1995). Protein tyrosine kinase PYK2 involved in calcium-induced regulation of ion channel and MAP kinase functions. Nature 376, 737-745.
25. Libby, P. (2002). Inflammation in atherosclerosis. Nature 420, 868-874.
26. Libby, P., Ridker, P.M., and Maseri, A. (2002). Inflammation and atherosclerosis. Circulation 105, 1135-1143.
27. Lietha, D., Cai, X., Ceccarelli, D.F., Li, Y., Schaller, M.D., and Eck, M.J. (2007). Structural basis for the autoinhibition of focal adhesion kinase. Cell 129, 1177-1187.
28. Lim, S.T., Chen, X.L., Lim, Y., Hanson, D.A., Vo, T.T., Howerton, K., Larocque, N., Fisher, S.J., Schlaepfer, D.D., and Ilic, D. (2008a). Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell 29, 9-22.
29. Lim, S.-T., Mikolon, D., Stupack, D.G., and Schlaepfer, D.D. (2008b). FERM control of FAK function, Implications for cancer therapy. Cell Cycle 7, 2306-2314.
30. Lim, Y., Lim, S.T, Tomar, A., Gardel, M., Bernard-Trifilo, J.A., Chen, X.L., Uryu, S.A., Canete-Soler, R., Zhai, J., Lin, H., et al. (2008c). PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol. 180, 187-203.
31. Lim, S.T., Miller, N.L., Nam, J.O., Chen, X.L., Lim, Y., and Schlaepfer, D.D. (2010a). PYK2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival. J. Biol. Chem. 285, 1743-1753.
32. Lim, S.T., Chen, X.L., Tomar, A., Miller, N.L., Yoo, J., and Schlaepfer, D.D. (2010b). Knock-in mutation reveals an essential role for focal adhesion kinase activity in blood vessel morphogenesis and cell motility-polarity but not cell proliferation. J. Biol. Chem. 285, 21526-21536.
33. Lim, S.T., Miller, N.L., Chen, X.L., Tancioni, I., Walsh, C.T., Lawson, C., Uryu, S., Weis, S.M., Cheresh, D.A., and Schlaepfer, D.D. (2012). Nuclear-localized focal adhesion kinase regulates inflammatory VCAM-1 expression. J. Cell Biol. 197, 907-919.
34. Luo, S.W., Zhang, C., Zhang, B., Kim, C.H., Qiu, Y.Z., Du, Q.S., Mei, L., and Xiong, W.C. (2009). Regulation of heterochromatin remodelling and myogenin expression during muscle differentiation by FAK interaction with MBD2. EMBO J. 28, 2568-2582.
35. McLean, G.W., Carragher, N.O., Avizienyte, E., Evans, J., Brunton, V.G., and Frame, M.C. (2005). The role of focal-Adhesion kinase in cancer -A new therapeutic opportunity. Nat. Rev. Cancer 5, 505-515.
36. Mei, L., and Xiong, W.C. (2010). FAK interaction with MBD2, A link from cell adhesion to nuclear chromatin remodeling? Cell Adh. Migr. 4, 77-80.
37. Minami, T., and Aird, W.C. (2001). Thrombin stimulation of the vascular cell adhesion molecule-1 promoter in endothelial cells is mediated by tandem nuclear factor-kappa B and GATA motifs. J. Biol. Chem. 276, 47632-47641.
38. Mitra, S.K., Hanson, D.A., and Schlaepfer, D.D. (2005). Focal adhesion kinase, in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68.
39. Molkentin, J.D. (2000). The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. J. Biol. Chem. 275, 38949-38952.
40. Ossovskaya, V., Lim, S.T., Ota, N., Schlaepfer, D.D., and Ilic, D. (2008). FAK nuclear export signal sequences. FEBS Lett. 582, 2402-2406.
41. Pober, J.S. (2002). Endothelial activation, intracellular signaling pathways. Arthritis Res. 4 Suppl 3, S109-116.
42. Roberts, W.G., Ung, E., Whalen, P., Cooper, B., Hulford, C., Autry, C., Richter, D., Emerson, E., Lin, J., Kath, J., et al. (2008). Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 68, 1935-1944.
43. Schaller, M.D. (2010). Cellular functions of FAK kinases, insight into molecular mechanisms and novel functions. J. Cell Sci. 123, 1007-1013.
44. Schlaepfer, D.D., and Hunter, T. (1996). 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, 5623-5633.
45. Schlaepfer, D.D., Mitra, S.K., and Ilic, D. (2004). Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692, 77-102.
46. Shen, T.L., Park, A.Y.J., Alcaraz, A., Peng, X., Jang, I., Koni, P., Flavell, R.A., Gu, H., and Guan. J.L. (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.
47. Stokes, J.B., Adair, S.J., Slack-Davis, J.K., Walters, D.M., Tilghman, R.W., Hershey, E.D., Lowrey, B., Thomas, K.S., Bouton, A.H., Hwang, R.F., et al. (2011). Inhibition of focal adhesion kinase by PF-562,271 inhibits the growth and metastasis of pancreatic cancer concomitant with altering the tumor microenvironment. Mol. Cancer Ther. 10, 2135-2145.
48. Walsh, C., Tanjoni, I., Uryu, S., Tomar, A., Nam, J.O., Luo, H., Phillips, A., Patel, N., Kwok, C., McMahon, G., et al. (2010). Oral delivery of PND-1186 FAK inhibitor decreases spontaneous breast to lung metastasis in pre-clinical tumor models. Cancer Biol. Ther. 9, 776-788.
49. Wang, Y., and Gilmore, T.D. (2003). Zyxin and paxillin proteins, focal adhesion plaque LIM domain proteins go nuclear. Biochim. Biophys. Acta 1593, 115-120.
50. Weis, S.M., Lim, S.T., Lutu-Fuga, K.M., Barnes, L.A., Chen, X.L., Göthert, J.R., Shen, T.L., Guan, J.L., Schlaepfer, D.D., and Cheresh, D.A. (2008). Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J. Cell Biol. 181, 43-50.
51. Zhao, X., Peng, X., Sun, S., Park, A.Y., and Guan, J.L. (2010). Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol. 189, 955-965.