Phosphatidylinositol 3-kinase/Akt positively regulates Fas (CD95)-mediated apoptosis in epidermal Cl41 cells

Journal of Immunology

Volumn 176, Issue 11, 2006, Pages 6785-6793

  Lu, Bin ^a   Wang, Liying ^b   Stehlik, Christian ^c   Medan, Djordje ^a   Huang, Chuanshu ^c   Hu, Shuiying ^a   Chen, Fei ^b   Shi, Xianglin ^b   Rojanasakul, Yon ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; FAS ANTIGEN; FAS LIGAND; FLICE INHIBITORY PROTEIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRAIN; CELL STRAIN CL41; CELL SURVIVAL; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EPIDERMIS CELL; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION;

EID: 33646857103     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.11.6785     Document Type: Article

References (55)

1. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267: 1449-1456.
2. Nagata, S. 1997. Apoptosis by death factor. Cell 88: 355-365.
3. Lenardo, M., K. M. Chan, F. Hornung, H. McFarland, R. Siegel, J. Wang, and L. Zheng. 1999. Mature T lymphocyte apoptosis: immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17: 221-253.
4. Nagata, S. 1999. Fas ligand-induced apoptosis. Annu. Rev. Genet. 33: 29-55.
5. Takahashi, T., M. Tanaka, C. I. Brannan, N. A. Jenkins, N. G. Copeland, T. Suda, and S. Nagata. 1994. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76: 969-976.
6. Chervonsky, A. V., Y. Wang, F. S. Wong, I. Visintin, R. A. Flavell, C. A. Janeway, Jr., and L. A. Matis. 1997. The role of Fas in autoimmune diabetes. Cell 89: 17-24.
7. Hsu, H. C., Y. Matsuki, H. G. Zhang, T. Zhou, and J. D. Mountz. 2001. The Fas signaling connection between autoimmunity and embryonic lethality. J. Clin. Immunol. 21: 1-14.
8. Viard, I., P. Wehrli, R. Bullani, P. Schneider, N. Holler, D. Salomon, T. Hunziker, J. H. Saurat, J. Tschopp, and L. E. French. 1998. Inhibition of toxic epidermal necrolysis by blockage of CD95 with human intravenous immunoglobulin. Science 282: 490-493.
9. Guan, D. W., T. Ohshima, and T. Kondo. 2000. Immunohistochemical study on Fas and Fas ligand in skin wound healing. Histochem. J. 32: 85-91.
10. Santamaria, A. B., D. W. Davis, D. X. Nghiem, D. J. McConkey, S. E. Ullrich, M. Kapoor, G. Lozano, and N. Ananthaswamy. 2002. p53 and Fas ligand are required for psoralen and UVA-induced apoptosis in mouse epidermal cells. Cell Death Differ. 9: 549-560.
11. Westentorp, M. O., R. Frank, C. Ochsenbauer, K. Stricker, J. Dhein, H. Walczak, K. M. Debatin, and P. H. Krammer. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375: 497-500.
12. Friesen, C., I. Herr, P. H. Krammer, and K. M. Debatin. 1996. Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat. Med. 2: 574-577.
13. Muller, M., S. Strand, H. Hug, E. M. Heinemann, H. Walczak, W. J. Hofmann, W. Stremmel, P. H. Krammer, and P. R. Galle. 1997. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J. Clin. Invest. 99: 403-413.
14. Rehemtulla, A., C. A. Hamilton, A. M. Chinnaiyan, and V. M. Dixit. 1997. Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/ APO-1). J. Biol. Chem. 272: 25783-25786.
15. Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905-2927.
16. Toker, A., and A. C. Newton. 2000. Akt/Protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem. 275: 8271-8274.
17. Pastorino, J. G., M. Tafani, and J. L. Farber. 1999. Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J. Biol. Chem. 274: 19411-19416.
18. Rena, G., S. Guo, S. C. Cichy, T. G. Unterman, and P. Cohen. 1999. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274: 17179-17183.
19. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868.
20. Madrid, L. V., M. W. Mayo, J. Y. Reuther, and A. S. Baldwin, Jr. 2001. Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen-activated protein kinase p38. J. Biol. Chem. 276: 18934-18940.
21. Suhara, T., T. Mano, B. E. Oliveira, and K. Walsh. 2001. Phosphatidylinositol 3-kinase/Akt signaling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE-inhibitory protein (FLIP). Circ. Res. 89: 13-19.
22. L promote growth factor-independent survival through distinct effects on mitochondrial physiology. J. Biol. Chem. 276: 12041-12048.
23. Gulbins, E., M. Hermisson, B. Brenner, H. U. Grassme, O. Linderkamp, J. Dichgans, M. Weller, and F. Lang. 1998. Cellular stimulation via CD95 involves activation of phosphoinositide-3-kinase. Pflugers Arch. 435: 546-554.
24. Ivanov, V. N., A. Bhoumik, M. Krasilnikov, R. Raz, L. B. Owen-Schaub, D. Levy, C. M. Horvath, and Z. Ronai. 2001. Cooperation between STAT3 and c-jun suppresses Fas transcription. Mol. Cell 7: 517-528.
25. Gibson, S., S. Tu, R. Oyer, S. M. Anderson, and G. L. Johnson. 1999. Epidermal growth factor protects epithelial cells against Fas-induced apoptosis: requirement for Akt activation. J. Biol. Chem. 274: 17612-17618.
26. Ushio-Fukai, M., R. W. Alexander, M. Akers, Q. Yin, Y. Fujio, K. Walsh, and K. K. Griendling. 1999. Reactive oxygen species mediate the activation of Akt/ protein kinase B by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 274: 22699-22704.
27. Konishi, H., H. Matsuzaki, M. Tanaka, Y. Takemura, S. Kuroda, Y. Ono, and U. Kikkawa. 1997. Activation of protein kinase B (Akt/RAC-protein kinase) by cellular stress and its association with heat shock protein Hsp27. FEBS Lett. 410: 493-498.
28. Sonoda, Y., S. Watanabe, Y. Matsumoto, E. Aizu-Yokota, and T. Kasahara. 1999. FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J. Biol. Chem. 274: 10566-10570.
29. Klotz, L. O., S. M. Schieke, H. Sies, and N. J. Holbrook. 2000. Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem. J. 352: 219-225.
30. Wang, X., K. D. McCullough, T. F. Franke, and N. J. Holbrook. 2000. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275: 14624-14631.
31. 308 in mouse epidermal Cl 41 cells through hydrogen peroxide. J. Biol. Chem. 276: 40234-40240.
32. Denning, T. L., H. Takaishi, S. E. Crowe, I. Boldogh, A. Jevnikar, and P. B. Ernst. 2002. Oxidative stress induces the expression of Fas and Fas ligand and apoptosis in murine intestinal epithelial cells. Free Radic. Biol. Med. 33: 1641-1650.
33. Devadas, S., J. A. Hinshaw, L. Zaritskaya, and M. S. Williams. 2003. Fas-stimulated generation of reactive oxygen species or exogenous oxidative stress sensitizes cells to Fas-mediated apoptosis. Free Radic. Biol. Med. 35: 648-661.
34. + cells. Mol. Cell. Biol. 16: 6427-6435.
35. Chan, H., D. P. Bartos, and L. B. Owen-Schaub. 1999. Activation-dependent transcriptional regulation of the human fas promoter requires NF-κB p5-p65 recruitment. Mol. Cell. Biol. 19: 2098-2108.
36. Colburn, N. H., B. F. Former, K. A. Nelson, and S. H. Yuspa. 1979. Tumor promoter induces anchorage independence irreversibly. Nature 281: 589-591.
37. Ye, J., S. Wang, S. S. Leonard, Y. Sun, L. Butterworth, J. Antonini, M. Ding, Y. Rojanasakul, V. Vallyathan, V. Castranova, and X. Shi. 1999. Role of reactive oxygen species and p53 in chromium (VI)-induced apoptosis. J. Biol. Chem. 274: 34974-34980.
38. Ivanov, V. N., M. Krasilnikov, and Z. Ronai. 2002. Regulation of Fas expression by STAT3 and c-Jun is mediated by phosphatidylinositol 3-kinase-AKT signaling. J. Biol. Chem. 277: 4932-4944.
39. Sulciner, D. J., K. Irani, Z. X. Yu, V. J. Ferrans, P. Goldschmidt-Claermont, and T. Finkel. 1996. Rac1 regulates a cytokine-stimulated redox-dependent pathway necessary for NF-κB activation. Mol. Cell. Biol. 16: 7115-7121.
40. Sulciner, D. J., Z. X. Yu, V. J. Ferrans, K. Gutkindm, K. Irani, P. Goldschmidt-Clermont, and T. Finkel. 1996. Rac1 regulates reactive oxygen species generation in fibroblasts. Biochem. J. 318: 379-382.
41. Deshpande, S. S., P. Angkeow, J. Huang, M. Ozaki, and K. Irani. 2000. Rac1 inhibits TNF-α-induced endothelial cell apoptosis: dual regulation by reactive oxygen species. FASEB J. 14: 1705-1714.
42. Chen, X. L., Q. Zhang, R. Zhao, X. Ding, P. E. Tummala, and R. M. Medford. 2003. Rac1 and superoxide are required for the expression of cell adhesion molecules induced by tumor necrosis factor-α in endothelial cells. J. Pharmacol. Exp. Ther. 305: 573-580.
43. Franke, T. F., D. R. Kaplan, and L. C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88: 435-437.
44. Moule, S. K., G. I. Welsh, N. J. Edgell, E. J. Foulstone, C. G. Proud, and R. M. Denton. 1997. Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and β-adrenergic agonists in rat epididymal fat cells: activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. J. Biol. Chem. 272: 7713-7719.
45. Sable, C. L., N. Filippa, B. Hemmings, and E. Van Obberghen. 1997. cAMP stimulates protein kinase B in a wortmannin-insensitive manner. FEBS Lett. 409: 253-257.
46. Konishi, H., H. Matsuzaki, M. Tanaka, Y. Ono, C. Tokunaga, S. Kuroda, and U. Kikkawa. 1996. Activation of RAC-protein kinase by heat shock and hyperosmolarity stress through a pathway independent of phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 93: 7639-7643.
47. Griendling, K. K., C. A. Minieri, J. D. Ollerenshaw, and R. W. Alexander. 1994. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74: 1141-1148.
48. Brenner, B., U. Koppenhoefer, C. Weinstock, O. Linderkamp, F. Lang, and E. Gulbins. 1997. Fas- or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J. Biol. Chem. 272: 22173-23321.
49. Rubbo, H., V. Darley-Usmar, and B. A. Freeman. 1996. Nitric oxide regulation of tissue free radical injury. Chem. Res. Toxicol. 9: 809-820.
50. Chanvorachote, P., U. Nimmannit, L. Wang, C. Stehlik, B. Lu, N. Azad, and Y. Rojanasakul. 2005. Nitric oxide negatively regulates Fas (CD95)-induced apoptosis through inhibition of ubiquitin-proteasome mediated degradation of FLIP. J. Biol. Chem. 280: 42044-42050.
51. phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J. Biol. Chem. 271: 23317-23321.
52. Hatano, E., and D. A. Brenner. 2001. Akt protects mouse hepatocytes from TNF-α- and Fas-mediated apoptosis through NF-κB activation. Am. J. Physiol. 281: G1357-G1368.
53. Panka, D. J., T. Mano, T. Suhara, K. Walsh, and J. W. Mier. 2001. Phosphatidylinositol 3-kinase/Akt activity regulates c-FLIP expression in tumor cells. J. Biol. Chem. 276: 6893-6896.
54. Osaki, M., S. Kase, K. Adachi, A. Takeda, K. Hashimoto, and H. Ito. 2004. Inhibition of the PI3K-Akt signaling pathway enhances the sensitivity of Fas-mediated apoptosis in human gastric carcinoma cell line, MKN-45. J. Cancer Res. Clin. Oncol. 130: 8-14.
55. Kwon, T., D. Y. Kwon, J. Chun, J. H. Kim, and S. S. Kang. 2000. Akt protein kinase inhibits Rac1-GTP binding through phosphorylation at serine 71 of Rac1. J. Biol. Chem. 275: 423-428.