Nuclear-localized focal adhesion kinase regulates inflammatory VCAM-1 expression

Journal of Cell Biology

Volumn 197, Issue 7, 2012, Pages 907-919

  Lim, Ssang Taek ^a,c   Miller, Nichol L G ^a   Chen, Xiao Lei ^a   Tancioni, Isabelle ^a   Walsh, Colin T ^a,d   Lawson, Christine ^a   Uryu, Sean ^a   Weis, Sara M ^b   Cheresh, David A ^b   Schlaepfer, David D ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTH ALABAMA   (United States)

^d Explora BioLabs   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE BAND 4.1 PROTEIN; EZRIN; FOCAL ADHESION KINASE; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE; MOESIN; RADIXIN; TRANSCRIPTION FACTOR GATA 4; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; HEART MUSCLE CELL; IN VIVO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; UBIQUITINATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; FOCAL ADHESION KINASE 1; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICE, TRANSGENIC; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84863753056     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201109067     Document Type: Article

References (57)

1. Ahmad, M., P. Theofanidis, and R.M. Medford. 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. http://dx.doi.org/10.1074/jbc.273.8.4616
2. Beg, A.A., and D. Baltimore. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 274:782-784. http://dx.doi.org/10.1126/science.274.5288.782
3. Bieler, G., M. Hasmim, Y. Monnier, N. Imaizumi, M. Ameyar, J. Bamat, L. Ponsonnet, S. Chouaib, M. Grell, S.L. Goodman, et al. 2007. Distinctive role of integrin-mediated adhesion in TNF-induced PKB/Akt and NFkappaB activation and endothelial cell survival. Oncogene. 26:5722-5732. http://dx.doi.org/10.1038/sj.onc.1210354
4. Braren, R., H. Hu, Y.H. Kim, H.E. Beggs, L.F. Reichardt, and R. Wang. 2006. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 172:151-162. http://dx.doi.org/10.1083/jcb.200506184
5. Brewer, A., and J. Pizzey. 2006. GATA factors in vertebrate heart development and disease. Expert Rev. Mol. Med. 8:1-20. http://dx.doi.org/10.1017/S1462399406000093
6. Carter, R.A., and I.P. Wicks. 2001. Vascular cell adhesion molecule 1 (CD106): A multifaceted regulator of joint inflammation. Arthritis Rheum. 44:985-994. http://dx.doi.org/10.1002/1529-0131(200105)44:5<985::AID-ANR176>3.0.CO;2-P
7. Dai, Q., C. Zhang, Y. Wu, H. McDonough, R.A. Whaley, V. Godfrey, H.H. Li, N. Madamanchi, W. Xu, L. Neckers, et al. 2003. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 22:5446-5458. http://dx.doi.org/10.1093/emboj/cdg529
8. Ferdous, A., J. Morris, M.J. Abedin, S. Collins, J.A. Richardson, and J.A. Hill. 2011. Forkhead factor FoxO1 is essential for placental morphogenesis in the developing embryo. Proc. Natl. Acad. Sci. USA. 108:16307-16312. http://dx.doi.org/10.1073/pnas.1107341108
9. Fitau, J., G. Boulday, F. Coulon, T. Quillard, and B. Charreau. 2006. The adaptor molecule Lnk negatively regulates tumor necrosis factor-alpha-dependent VCAM-1 expression in endothelial cells through inhibition of the ERK1 and -2 pathways. J. Biol. Chem. 281:20148-20159. http://dx.doi.org/10.1074/jbc.M510997200
10. Fornaro, M., J. Plescia, S. Chheang, G. Tallini, Y.M. Zhu, M. King, D.C. Altieri, and L.R. Languino. 2003. Fibronectin protects prostate cancer cells from tumor necrosis factor-alpha-induced apoptosis via the AKT/survivin pathway. J. Biol. Chem. 278:50402-50411. http://dx.doi.org/10.1074/jbc.M307627200
11. Funakoshi-Tago, M., Y. Sonoda, S. Tanaka, K. Hashimoto, K. Tago, S. Tominaga, and T. Kasahara. 2003. Tumor necrosis factor-induced nuclear factor kappaB activation is impaired in focal adhesion kinase-deficient fibroblasts. J. Biol. Chem. 278:29359-29365. http://dx.doi.org/10.1074/jbc.M213115200
12. Golubovskaya, V.M., R. Finch, and W.G. Cance. 2005. Direct interaction of the N-terminal domain of focal adhesion kinase with the N-terminal transactivation domain of p53. J. Biol. Chem. 280:25008-25021. http://dx.doi.org/10.1074/jbc.M414172200
13. Gurtner, G.C., V. Davis, H. Li, M.J. McCoy, A. Sharpe, and M.I. Cybulsky. 1995. Targeted disruption of the murine VCAM1 gene: Essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 9:1-14. http://dx.doi.org/10.1101/gad.9.1.1
14. Hiratsuka, S., S. Goel, W.S. Kamoun, Y. Maru, D. Fukumura, D.G. Duda, and R.K. Jain. 2011. Endothelial focal adhesion kinase mediates cancer cell homing to discrete regions of the lungs via E-selectin up-regulation. Proc. Natl. Acad. Sci. USA. 108:3725-3730. http://dx.doi.org/10.1073/pnas.1100446108
15. Huang, W.C., J.J. Chen, and C.C. Chen. 2003. c-Src-dependent tyrosine phosphorylation of IKKbeta is involved in tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 expression. J. Biol. Chem. 278:9944-9952. http://dx.doi.org/10.1074/jbc.M208521200
16. Ilic, D., B. Kovacic, S. McDonagh, F. Jin, C. Baumbusch, D.G. Gardner, and C.H. Damsky. 2003. Focal adhesion kinase is required for blood vessel morphogenesis. Circ. Res. 92:300-307. http://dx.doi.org/10.1161/01.RES.0000055016.36679.23
17. Inman, K.E., and K.M. Downs. 2007. The murine allantois: Emerging paradigms in development of the mammalian umbilical cord and its relation to the fetus. Genesis. 45:237-258. http://dx.doi.org/10.1002/dvg.20281
18. Karin, M., and E. Gallagher. 2009. TNFR signaling: Ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes. Immunol. Rev. 228:225-240. http://dx.doi.org/10.1111/j.1600-065X.2008.00755.x
19. Kobayashi, S., K. Mao, H. Zheng, X. Wang, C. Patterson, T.D. O'Connell, and Q. Liang. 2007. Diminished GATA4 protein levels contribute to hyperglycemiainduced cardiomyocyte injury. J. Biol. Chem. 282:21945-21952. http://dx.doi.org/10.1074/jbc.M703048200
20. Kwee, L., H.S. Baldwin, H.M. Shen, C.L. Stewart, C. Buck, C.A. Buck, and M.A. Labow. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development. 121:489-503.
21. Lawson, M.A., D.B. Whyte, and P.L. Mellon. 1996. GATA factors are essential for activity of the neuron-specific enhancer of the gonadotropin-releasing hormone gene. Mol. Cell. Biol. 16:3596-3605.
22. Lee, J., A.K. Borboa, H.B. Chun, A. Baird, and B.P. Eliceiri. 2010. Conditional deletion of the focal adhesion kinase FAK alters remodeling of the bloodbrain barrier in glioma. Cancer Res. 70:10131-10140. http://dx.doi.org/10.1158/0008-5472.CAN-10-2740
23. Libby, P. 2002. Inflammation in atherosclerosis. Nature. 420:868-874. http://dx.doi.org/10.1038/nature01323
24. Lietha, D., X. Cai, D.F. Ceccarelli, Y. Li, M.D. Schaller, and M.J. Eck. 2007. Structural basis for the autoinhibition of focal adhesion kinase. Cell. 129:1177-1187. http://dx.doi.org/10.1016/j.cell.2007.05.041
25. Lim, S.T., X.L. Chen, Y. Lim, D.A. Hanson, T.T. Vo, K. Howerton, N. Larocque, S.J. Fisher, D.D. Schlaepfer, and D. Ilic. 2008. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell. 29:9-22. http://dx.doi.org/10.1016/j.molcel.2007.11.031
26. Lim, S.T., X.L. Chen, A. Tomar, N.L. Miller, J. Yoo, and D.D. Schlaepfer. 2010a. 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. http://dx.doi.org/10.1074/jbc.M110.129999
27. Lim, S.T., N.L. Miller, J.O. Nam, X.L. Chen, Y. Lim, and D.D. Schlaepfer. 2010b. Pyk2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival. J. Biol. Chem. 285:1743-1753. http://dx.doi.org/10.1074/jbc.M109.064212
28. Liu, J., X. He, S.A. Corbett, S.F. Lowry, A.M. Graham, R. Fässler, and S. Li. 2009. Integrins are required for the differentiation of visceral endoderm. J. Cell Sci. 122:233-242. http://dx.doi.org/10.1242/jcs.037663
29. Luo, S.W., C. Zhang, B. Zhang, C.H. Kim, Y.Z. Qiu, Q.S. Du, L. Mei, and W.C. Xiong. 2009. Regulation of heterochromatin remodelling and myogenin expression during muscle differentiation by FAK interaction with MBD2. EMBO J. 28:2568-2582. http://dx.doi.org/10.1038/emboj.2009.178
30. MacEwan, D.J. 2002. TNF ligands and receptors-a matter of life and death. Br. J. Pharmacol. 135:855-875. http://dx.doi.org/10.1038/sj.bjp.0704549
31. May, M.J., C.P. Wheeler-Jones, and J.D. Pearson. 1996. Effects of protein tyrosine kinase inhibitors on cytokine-induced adhesion molecule expression by human umbilical vein endothelial cells. Br. J. Pharmacol. 118:1761-1771.
32. Minami, T., and W.C. Aird. 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. http://dx.doi.org/10.1074/jbc.M108363200
33. Mitra, S.K., D.A. Hanson, and D.D. Schlaepfer. 2005. Focal adhesion kinase: In command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6:56-68. http://dx.doi.org/10.1038/nrm1549
34. 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. http://dx.doi.org/10.1074/jbc.R000029200
35. Osborn, L., C. Hession, R. Tizard, C. Vassallo, S. Luhowskyj, G. Chi-Rosso, and R. Lobb. 1989. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell. 59:1203-1211. http://dx.doi.org/10.1016/0092-8674(89)90775-7
36. Ossovskaya, V., S.T. Lim, N. Ota, D.D. Schlaepfer, and D. Ilic. 2008. FAK nuclear export signal sequences. FEBS Lett. 582:2402-2406. http://dx.doi.org/10.1016/j.febslet.2008.06.004
37. Owen, K.A., F.J. Pixley, K.S. Thomas, M. Vicente-Manzanares, B.J. Ray, A.F. Horwitz, J.T. Parsons, H.E. Beggs, E.R. Stanley, and A.H. Bouton. 2007. Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J. Cell Biol. 179:1275-1287. http://dx.doi.org/10.1083/jcb.200708093
38. Pober, J.S. 2002. Endothelial activation: Intracellular signaling pathways. Arthritis Res. 4(Suppl 3):S109-S116. http://dx.doi.org/10.1186/ar576
39. Roberts, W.G., E. Ung, P. Whalen, B. Cooper, C. Hulford, C. Autry, D. Richter, E. Emerson, J. Lin, J. Kath, et al. 2008. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 68:1935-1944. http://dx.doi.org/10.1158/0008-5472.CAN-07-5155
40. Schaller, M.D. 2010. Cellular functions of FAK kinases: Insight into molecular mechanisms and novel functions. J. Cell Sci. 123:1007-1013. http://dx.doi.org/10.1242/jcs.045112
41. Schlaepfer, D.D., and S.K. Mitra. 2004. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14:92-101. http://dx.doi.org/10.1016/j.gde.2003.12.002
42. Schlaepfer, D.D., S. Hou, S.T. Lim, A. Tomar, H. Yu, Y. Lim, D.A. Hanson, S.A. Uryu, J. Molina, and S.K. Mitra. 2007. Tumor necrosis factor-alpha stimulates focal adhesion kinase activity required for mitogen-activated kinase-associated interleukin 6 expression. J. Biol. Chem. 282:17450-17459. http://dx.doi.org/10.1074/jbc.M610672200
43. Schultze, A., and W. Fiedler. 2010. Therapeutic potential and limitations of new FAK inhibitors in the treatment of cancer. Expert Opin. Investig. Drugs. 19:777-788. http://dx.doi.org/10.1517/13543784.2010.489548
44. Schwartz, M.A. 2001. Integrin signaling revisited. Trends Cell Biol. 11:466-470. http://dx.doi.org/10.1016/S0962-8924(01)02152-3
45. Shen, T.-L., A.Y.J. 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. http://dx.doi.org/10.1083/jcb.200411155
46. Short, S.M., G.A. Talbott, and R.L. Juliano. 1998. Integrin-mediated signaling events in human endothelial cells. Mol. Biol. Cell. 9:1969-1980.
47. Takada, Y., and B.B. Aggarwal. 2004. TNF activates Syk protein tyrosine kinase leading to TNF-induced MAPK activation, NF-kappaB activation, and apoptosis. J. Immunol. 173:1066-1077.
48. Tanjoni, I., C. Walsh, S. Uryu, A. Tomar, J.O. Nam, A. Mielgo, S.T. Lim, C. Liang, M. Koenig, C. Sun, et al. 2010. PND-1186 FAK inhibitor selectively promotes tumor cell apoptosis in three-dimensional environments. Cancer Biol. Ther. 9:764-777. http://dx.doi.org/10.4161/cbt.9.10.11434
49. Tavora, B., S. Batista, L.E. Reynolds, S. Jadeja, S. Robinson, V. Kostourou, I. Hart, M. Fruttiger, M. Parsons, and K.M. Hodivala-Dilke. 2010. Endothelial FAK is required for tumour angiogenesis. EMBO Mol Med. 2:516-528. http://dx.doi.org/10.1002/emmm.201000106
50. Tremblay, J.J., and R.S. Viger. 2003. Transcription factor GATA-4 is activated by phosphorylation of serine 261 via the cAMP/protein kinase a signaling pathway in gonadal cells. J. Biol. Chem. 278:22128-22135. http://dx.doi.org/10.1074/jbc.M213149200
51. van Berlo, J.H., J.W. Elrod, B.J. Aronow, W.T. Pu, and J.D. Molkentin. 2011. Serine 105 phosphorylation of transcription factor GATA4 is necessary for stress-induced cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. USA. 108:12331-12336. http://dx.doi.org/10.1073/pnas.1104499108
52. Walsh, C., I. Tanjoni, S. Uryu, A. Tomar, J.O. Nam, H. Luo, A. Phillips, N. Patel, C. Kwok, G. McMahon, et al. 2010. Oral delivery of PND-1186 FAK inhibitor decreases tumor growth and spontaneous breast to lung metastasis in pre-clinical models. Cancer Biol. Ther. 9:778-790. http://dx.doi.org/10.4161/cbt.9.10.11433
53. Weber, C., E. Negrescu, W. Erl, A. Pietsch, M. Frankenberger, H.W. Ziegler-Heitbrock, W. Siess, and P.C. Weber. 1995. Inhibitors of protein tyrosine kinase suppress TNF-stimulated induction of endothelial cell adhesion molecules. J. Immunol. 155:445-451.
54. Weis, S.M., and D.A. Cheresh. 2011. Tumor angiogenesis: Molecular pathways and therapeutic targets. Nat. Med. 17:1359-1370. http://dx.doi.org/10.1038/nm.2537
55. Weis, S.M., S.T. Lim, K.M. Lutu-Fuga, L.A. Barnes, X.L. Chen, J.R. Göthert, T.L. Shen, J.L. Guan, D.D. Schlaepfer, and D.A. Cheresh. 2008. Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J. Cell Biol. 181:43-50. http://dx.doi.org/10.1083/jcb.200710038
56. Young, S.R., R. Gerard-O'Riley, M. Harrington, and F.M. Pavalko. 2010. Activation of NF-kappaB by fluid shear stress, but not TNF-alpha, requires focal adhesion kinase in osteoblasts. Bone. 47:74-82. http://dx.doi.org/10.1016/j.bone.2010.03.014
57. Zhao, X., X. Peng, S. Sun, A.Y. Park, and J.L. Guan. 2010. Role of kinaseindependent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol. 189:955-965. http://dx.doi.org/10.1083/jcb.200912094