Rapid up-regulation of c-FLIP expression by BCR signaling through the PI3K/Akt pathway inhibits simultaneously induced Fas-mediated apoptosis in murine B lymphocytes

Immunology Letters

Volumn 109, Issue 1, 2007, Pages 36-46

  Moriyama, Hiroyuki ^a   Yonehara, Shin ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Apoptosis; B cells; c FLIP; Fas; PI3K Akt

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTIGEN; BREAKPOINT CLUSTER REGION PROTEIN; CASPASE 8; FAS ANTIGEN; FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE; PROTEIN KINASE 13; PROTEIN KINASE B; PROTEIN P85; PROTEIN SUBUNIT; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL PROTECTION; CELL STIMULATION; CELL SURVIVAL; CROSS LINKING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REPRESSION; IMMUNOSTIMULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPLEEN CELL; TUMOR CELL LINE; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD95; APOPTOSIS; B-LYMPHOCYTES; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 3; CASPASE 8; CELL LINE, TUMOR; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; ENZYME ACTIVATION; LYMPHOMA, B-CELL; MICE; NF-KAPPA B; ONCOGENE PROTEIN V-AKT; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 33847684318     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2006.12.009     Document Type: Article

References (47)

1. Cambier J.C. Antigen and Fc receptor signaling. The awesome power of the immunoreceptor tyrosine-based activation motif (ITAM). J Immunol 155 (1995) 3281-3285
2. Gold M.R., Law D.A., and DeFranco A.L. Stimulation of protein tyrosine phosphorylation by the B-lymphocyte antigen receptor. Nature 345 (1990) 810-813
3. Nagata S., and Golstein P. The Fas death factor. Science 267 (1995) 1449-1456
4. Yonehara S., Ishii A., and Yonehara M. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med 169 (1989) 1747-1756
5. Tsubata T., Wu J., and Honjo T. B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364 (1993) 645-648
6. Tsubata T. Apotosis of mature B cells. Int Rev Immunol 18 (1999) 347-365
7. Krammer P.H. CD95's deadly mission in the immune system. Nature 407 (2000) 789-795
8. Bras A., Martinez A.C., and Baixeras E. B cell receptor cross-linking prevents Fas-induced cell death by inactivating the IL-1 beta-converting enzyme protease and regulating Bcl-2/Bcl-x expression. J Immunol 159 (1997) 3168-3177
9. Catlett I.M., and Bishop G.A. Cutting edge: a novel mechanism for rescue of B cells from CD95/Fas-mediated apoptosis. J Immunol 163 (1999) 2378-2381
10. Hinshaw J.A., Mueller C.M., Scott D.W., and Williams M.S. B cell receptor signaling mediates immediate protection from Fas-induced apoptosis upstream of caspase activation through an atypical protein kinase C isozyme and de novo protein synthesis. Eur J Immunol 33 (2003) 2490-2500
11. Rothstein T.L., Wang J.K., Panka D.J., Foote L.C., Wang Z., Stanger B., et al. Protection against Fas-dependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature 374 (1995) 163-165
12. Wang J., Lobito A.A., Shen F., Hornung F., Winoto A., and Lenardo M.J. Inhibition of Fas-mediated apoptosis by the B cell antigen receptor through c-FLIP. Eur J Immunol 30 (2000) 155-163
13. Schneider T.J., Grillot D., Foote L.C., Nunez G.E., and Rothstein T.L. Bcl-x protects primary B cells against Fas-mediated apoptosis. J Immunol 159 (1997) 4834-4839
14. Shimizu S., Narita M., and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483-487
15. Tsujimoto Y., Cossman J., Jaffe E., and Croce C.M. Involvement of the bcl-2 gene in human follicular lymphoma. Science 228 (1985) 1440-1443
16. Inohara N., Koseki T., Hu Y., Chen S., and Nunez G. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis. Proc Natl Acad Sci USA 94 (1997) 10717-10722
17. Irmler M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., et al. Inhibition of death receptor signals by cellular FLIP. Nature 388 (1997) 190-195
18. Rasper D.M., Vaillancourt J.P., Hadano S., Houtzager V.M., Seiden I., Keen S.L., et al. Cell death attenuation by 'Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ 5 (1998) 271-288
19. Scaffidi C., Schmitz I., Krammer P.H., and Peter M.E. The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 274 (1999) 1541-1548
20. Budd R.C., Yeh W.C., and Tschopp J. cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 6 (2006) 196-204
21. Kerbauy D.M., Lesnikov V., Abbasi N., Seal S., Scott B., and Deeg H.J. NF-kappaB and FLIP in arsenic trioxide (ATO)-induced apoptosis in myelodysplastic syndromes (MDSs). Blood 106 (2005) 3917-3925
22. Todaro M., Zerilli M., Triolo G., Iovino F., Patti M., Accardo-Palumbo A., et al. NF-kappaB protects Behcet's disease T cells against CD95-induced apoptosis up-regulating antiapoptotic proteins. Arthritis Rheum 52 (2005) 2179-2191
23. Zhang N., and He Y.W. An essential role for c-FLIP in the efficient development of mature T lymphocytes. J Exp Med 202 (2005) 395-404
24. Golks A., Brenner D., Krammer P.H., and Lavrik I.N. The c-FLIP-NH2 terminus (p22-FLIP) induces NF-kappaB activation. J Exp Med 203 (2006) 1295-1305
25. Kondo G., Iwase M., Watanabe H., Uchida M., Takaoka S., Ohashi M., et al. Enhancement of susceptibility to Fas-mediated apoptosis in HL-60 cells through down-regulation of cellular FLICE-inhibitory protein by phosphatidylinositol 3-kinase inhibitors. Oncol Rep 14 (2005) 1215-1222
26. Lu B., Wang L., Stehlik C., Medan D., Huang C., Hu S., et al. Phosphatidylinositol 3-kinase/Akt positively regulates Fas (CD95)-mediated apoptosis in epidermal Cl41 cells. J Immunol 176 (2006) 6785-6793
27. Nam S.Y., Jung G.A., Hur G.C., Chung H.Y., Kim W.H., Seol D.W., et al. Upregulation of FLIP(S) by Akt, a possible inhibition mechanism of TRAIL-induced apoptosis in human gastric cancers. Cancer Sci 94 (2003) 1066-1073
28. Osaki M., Kase S., Adachi K., Takeda A., Hashimoto K., and Ito H. 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 (2004) 8-14
29. Panka D.J., Mano T., Suhara T., Walsh K., and Mier J.W. Phosphatidylinositol 3-kinase/Akt activity regulates c-FLIP expression in tumor cells. J Biol Chem 276 (2001) 6893-6896
30. Perlman H., Pagliari L.J., Nguyen N., Bradley K., Liu H., and Pope R.M. The Fas-FasL death receptor and PI3K pathways independently regulate monocyte homeostasis. Eur J Immunol 31 (2001) 2421-2430
31. Sakata S., Sakamaki K., Watanabe K., Nakamura N., Toyokuni S., Nishimune Y., et al. Involvement of death receptor Fas in germ cell degeneration in gonads of Kit-deficient Wv/Wv mutant mice. Cell Death Differ 10 (2003) 676-686
32. Okamoto K., Fujisawa J., Reth M., and Yonehara S. Human T-cell leukemia virus type-I oncoprotein tax inhibits Fas-mediated apoptosis by inducing cellular FLIP through activation of NF-kappaB. Genes Cells 11 (2006) 177-191
33. Nishimura Y., Ishii A., Kobayashi Y., Yamasaki Y., and Yonehara S. Expression and function of mouse Fas antigen on immature and mature T cells. J Immunol 154 (1995) 4395-4403
34. Ohgushi M., Kuroki S., Fukamachi H., O'Reilly L.A., Kuida K., Strasser A., et al. Transforming growth factor beta-dependent sequential activation of Smad, Bim, and caspase-9 mediates physiological apoptosis in gastric epithelial cells. Mol Cell Biol 25 (2005) 10017-10028
35. Lee K.K., Ohyama T., Yajima N., Tsubuki S., and Yonehara S. MST, a physiological caspase substrate, highly sensitizes apoptosis both upstream and downstream of caspase activation. J Biol Chem 276 (2001) 19276-19285
36. Nakagiri S., Murakami A., Takada S., Akiyama T., and Yonehara S. Viral FLIP enhances Wnt signaling downstream of stabilized beta-catenin, leading to control of cell growth. Mol Cell Biol 25 (2005) 9249-9258
37. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14 (1995) 5579-5588
38. Mitsiades C.S., Mitsiades N., Poulaki V., Schlossman R., Akiyama M., Chauhan D., et al. Activation of NF-kappaB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 21 (2002) 5673-5683
39. Foote L.C., Schneider T.J., Fischer G.M., Wang J.K., Rasmussen B., Campbell K.A., et al. Intracellular signaling for inducible antigen receptor-mediated Fas resistance in B cells. J Immunol 157 (1996) 1878-1885
40. de Thonel A., Bettaieb A., Jean C., Laurent G., and Quillet-Mary A. Role of protein kinase C zeta isoform in Fas resistance of immature myeloid KG1a leukemic cells. Blood 98 (2001) 3770-3777
41. Suhara T., Mano T., Oliveira B.E., and Walsh K. Phosphatidylinositol 3-kinase/Akt signaling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE-inhibitory protein (FLIP). Circ Res 89 (2001) 13-19
42. Krueger A., Schmitz I., Baumann S., Krammer P.H., and Kirchhoff S. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J Biol Chem 276 (2001) 20633-20640
43. Medema J.P., Scaffidi C., Kischkel F.C., Shevchenko A., Mann M., Krammer P.H., et al. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J 16 (1997) 2794-2804
44. Antony P., Petro J.B., Carlesso G., Shinners N.P., Lowe J., and Khan W.N. B cell receptor directs the activation of NFAT and NF-kappaB via distinct molecular mechanisms. Exp Cell Res 291 (2003) 11-24
45. Bone H., and Williams N.A. Antigen-receptor cross-linking and lipopolysaccharide trigger distinct phosphoinositide 3-kinase-dependent pathways to NF-kappa B activation in primary B cells. Int Immunol 13 (2001) 807-816
46. Shou Y., Li N., Li L., Borowitz J.L., and Isom G.E. NF-kappaB-mediated up-regulation of Bcl-X(S) and Bax contributes to cytochrome c release in cyanide-induced apoptosis. J Neurochem 81 (2002) 842-852
47. Zender L., Hutker S., Mundt B., Waltemathe M., Klein C., Trautwein C., et al. NFkappaB-mediated upregulation of bcl-xl restrains TRAIL-mediated apoptosis in murine viral hepatitis. Hepatology 41 (2005) 280-288