Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein

Molecular and Cellular Biology

Volumn 24, Issue 10, 2004, Pages 4361-4371

  Kurenova, Elena ^a   Xu, Li Hui ^b   Yang, Xihui ^b   Baldwin Jr , Albert S ^b   Craven, Rolf J ^c   Hanks, Steven K ^d   Liu, Zheng Gang ^e   Cance, William G ^a,f  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f Division of Pulmonary and Critical Care Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; DEATH ASSOCIATED PROTEIN KINASE; DEATH RECEPTOR; FAS ANTIGEN; FOCAL ADHESION KINASE; RECEPTOR PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR 1; FOCAL ADHESION KINASE 1; LEUKOCYTE ANTIGEN; PROTEIN; PROTEIN TYROSINE KINASE; PTK2 PROTEIN, HUMAN; PTK2 PROTEIN, MOUSE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, HUMAN; RIPK1 PROTEIN, MOUSE; SMALL INTERFERING RNA; STAUROSPORINE; TUMOR NECROSIS FACTOR RECEPTOR;

APOPTOSIS; ARTICLE; COMPLEX FORMATION; ENZYME BINDING; ENZYME REPRESSION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BREAST TUMOR; CELL LINE; DRUG EFFECT; FEMALE; GENETICS; HUMAN; METABOLISM; MOUSE; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN BINDING; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD; APOPTOSIS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; FEMALE; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MICE; MICE, KNOCKOUT; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PROTEINS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAUROSPORINE;

EID: 2942531163     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.10.4361-4371.2004     Document Type: Article

References (44)

1. Beviglia, L., V. Golubovskaya, L. Xu, X. Yang, R. J. Craven, and W. G. Cance. 2003. Focal adhesion kinase N-terminus in breast carcinoma cells induces rounding, detachment and apoptosis. Biochem. J. 373:201-210.
2. Cance, W. G., J. E. Harris, M. V. Iacocca, E. Roche, X. Yang, J. Chang, S. Simkins, and L. Xu. 2000. 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. 6:2417-2423.
3. Chinnaiyan, A. M., C. G. Tepper, M. F. Seldin, K. O'Rourke, F. C. Kischkel, S. Hellbardt, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961-4965.
4. Cusson, N., S. Oikemus, E. D. Kilpatrick, L. Cunningham, and M. Kelliher. 2002. The death domain kinase RIP protects thymocytes from tumor necrosis factor receptor type 2-induced cell death. J. Exp. Med. 196:15-26.
5. Duan, H., and V. M. Dixit. 1997. RAIDD is a new 'death' adaptor molecule. Nature 385:86-89.
6. Folkman, J., and A. Moscona. 1978. Role of cell shape in growth control. Nature 273:345-349.
7. Frisch, S. M. 1999. Evidence for a function of death-receptor-related, death-domain-containing proteins in anoikis. Curr. Biol. 9:1047-1049.
8. Frisch, S. M., and H. Francis. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:619-626.
9. Frisch, S. M., K. Vuori, E. Ruoslahti, and P. Y. Chan-Hui. 1996. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134:793-799.
10. Fujita-Yamaguchi, Y., and S. Kathuria. 1988. Characterization of receptor tyrosine-specific protein kinases by the use of inhibitors. Staurosporine is a 100-times more potent inhibitor of insulin receptor than IGF-I receptor. Biochem. Biophys. Res. Commun. 157:955-962.
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.
12. Gilmore, A. P., A. D. Metcalfe, L. H. Romer, and C. H. Streuli. 2000. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J. Cell Biol. 149:431-446.
13. 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.
14. Grimm, S., B. Z. Stanger, and P. Leder. 1996. RIP and FADD: two "death domain"-containing proteins can induce apoptosis by convergent, but dissociable, pathways. Proc. Natl. Acad. Sci. USA 93:10923-10927.
15. Grossmann, J. 2002. Molecular mechanisms of "detachment-induced apoptosis-anoikis." Apoptosis 7:247-260.
16. Hisano, C., R. Tanaka, H. Fujishima, H. Ariyama, T. Tsuchiya, T. Tatsumoto, K. Mitsugi, M. Nakamura, and S. Nakano. 2003. Suppression of anoikis by v-Src but not by activated c-H-Ras in human gallbladder epithelial cells. Cell Biol. Int. 27:415-421.
17. Hsu, H., J. Huang, H. B. Shu, V. Baichwal, and D. V. Goeddel. 1996. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4:387-396.
18. Hungerford, J. E., M. T. Compton, M. L. Matter, B. G. Hoffstrom, and C. A. Otey. 1996. Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J. Cell Biol. 135:1383-1390.
19. 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.
20. Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, et al. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
21. 2-terminal FAK in the nuclei of apoptotic glioblastoma cells. Cancer Res. 61:4978-4981.
22. Kabir, J., M. Lobo, and I. Zachary. 2002. Staurosporine induces endothelial cell apoptosis via focal adhesion kinase dephosphorylation and focal adhesion disassembly independent of focal adhesion kinase proteolysis. Biochem. J. 367:145-155.
23. Kelliher, M. A., S. Grimm, Y. Ishida, F. Kuo, B. Z. Stanger, and P. Leder. 1998. The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8:297-303.
24. Lark, A. L., C. A. Livasy, B. Calvo, L. Caskey, D. T. Moore, X. Yang, and W. G. Cance. 2003. Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clin. Cancer Res. 9:215-222.
25. Lewis, J., A. Devin, A. Miller, Y. Lin, Y. Rodriguez, L. Neckers, and Z. G. Liu. 2000. Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J. Biol. Chem. 275:10519-10526.
26. Liu, X. J., L. Yang, H. B. Wu, O. Qiang, M. H. Huang, and Y. P. Wang. 2002. Apoptosis of rat hepatic stellate cells induced by anti-focal adhesion kinase antibody. World J. Gastroenterol. 8:734-738.
27. Liu, Z. G., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87:565-576.
28. Martinon, F., N. Holler, C. Richard, and J. Tschopp. 2000. Activation of a pro-apoptotic amplification loop through inhibition of NF-kappaB-dependent survival signals by caspase-mediated inactivation of RIP. FEBS Lett. 468:134-136.
29. Mosmant, T. 1983. Rapid colorimetric assay for cellular growth and survival. J. Immunol. Methods 65:55-63.
30. Nakano, H., E. Kobayashi, I. Takahashi, T. Tamaoki, Y. Kuzuu, and H. Iba. 1987. Staurosporine inhibits tyrosine-specific protein kinase activity of Rous sarcoma virus transforming protein p60. J. Antibiot. (Tokyo) 40:706-708.
31. Owen, J. D., P. J. Ruest, D. W. Fry, and S. K. Hanks. 1999. 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. 19:4806-4818.
32. Owens, L. V., L. Xu, R. J. Craven, G. A. Dent, T. M. Weiner, L. Kornberg, E. T. Liu, and W. G. Cance. 1995. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 55:2752-2755.
33. Richardson, A., and T. Parsons. 1996. A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp125FAK. Nature 380:538-540.
34. Ruegg, U. T., and G. M. Burgess. 1989. Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol. Sci. 10:218-220.
35. Rytomaa, M., L. M. Martins, and J. Downward. 1999. Involvement of FADD and caspase-8 signalling in detachment-induced apoptosis. Curr. Biol. 9:1043-1046.
36. Secrist, J. P., I. Sehgal, G. Powis, and R. T. Abraham. 1990. Preferential inhibition of the platelet-derived growth factor receptor tyrosine kinase by staurosporine. J. Biol. Chem. 265:20394-20400.
37. Sonoda, Y., Y. Matsumoto, M. Funakoshi, D. Yamamoto, S. K. Hanks, and T. Kasahara. 2000. 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. 275:16309-16315.
38. Stanger, B. Z., P. Leder, T. H. Lee, E. Kim, and B. Seed. 1995. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 81:513-523.
39. Ting, A. T., F. X. Pimentel-Muinos, and B. Seed. 1996. RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1-initiated apoptosis. EMBO J. 15:6189-6196.
40. van De Water, B., F. Houtepen, M. Huigsloot, and I. B. Tijdens. 2001. 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. 276:36183-36193.
41. Weiner, T. M., E. T. Liu, R. J. Craven, and W. G. Cance. 1993. Expression of focal adhesion kinase gene and invasive cancer. Lancet 342:1024-1025.
42. Xu, L. H., L. V. Owens, G. C. Sturge, X. Yang, E. T. Liu, R. J. Craven, and W. G. Cance. 1996. Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ. 7:413-418.
43. Xu, L.-H., X.-H. Yang, C. A. Bradham, D. A. Brenner, A. S. Baldwin, R. J. Craven, and W. G. Cance. 2000. The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. J. Biol. Chem. 275:30597-30604.
44. 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.