Tumor Necrosis Factor (TNF) receptor-associated factor 7 is required for TNFα-induced Jun NH2-terminal kinase activation and promotes cell death by regulating polyubiquitination and lysosomal degradation of c-FLIP protein

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 6053-6061

  Scudiero, Ivan ^a,b   Zotti, Tiziana ^a,b   Ferravante, Angela ^a,b   Vessichelli, Mariangela ^a,b   Reale, Carla ^a,b   Masone, Maria C ^a,b   Leonardi, Antonio ^c   Vito, Pasquale ^a,b   Stilo, Romania ^a,b  

^a UNIVERSITY OF SANNIO   (Italy)

^b Grande Ospedale Metropolitano   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-APOPTOTIC PROTEIN; CELL SURVIVAL; CYTOKINES; EXPRESSION LEVELS; KINASE ACTIVATION; LYSOSOMAL DEGRADATION; POLYUBIQUITINATION; SURVIVAL FACTOR; TUMOR NECROSIS FACTORS;

CELL DEATH; CHEMICAL ACTIVATION; DEGRADATION; MACROPHAGES; PROTEINS;

GLYCOPROTEINS;

FLICE INHIBITORY PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 7; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CELL LEVEL; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOTOXICITY; EMBRYO; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC CORRELATION; HUMAN; HUMAN CELL; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; RNA INTERFERENCE; UBIQUITINATION;

CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL DEATH; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HELA CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; JURKAT CELLS; LYSOSOMES; POLYUBIQUITIN; PROTEOLYSIS; RNA, SMALL INTERFERING; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION;

EID: 84857253295     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.300137     Document Type: Article

References (43)

1. Wajant, H., Pfizenmaier, K., and Scheurich, P. (2003) Tumor necrosis factor signaling. Cell Death Differ. 10, 45-65
2. Peter, M. E., and Krammer, P. H. (2003) The CD95 (APO-1/Fas) DISC and beyond. Cell Death Differ. 10, 26-35
3. Boatright, K. M., Renatus, M., Scott, F. L., Sperandio, S., Shin, H., Pedersen, I. M., Ricci, J. E., Edris, W. A., Sutherlin, D. P., Green, D. R., and Salvesen, G. S. (2003) A unified model for apical caspase activation. Mol. Cell 11, 529-541
4. Chang, D. W., Xing, Z., Capacio, V. L., Peter, M. E., and Yang, X. (2003) Interdimer processing mechanism of procaspase-8 activation. EMBO J. 22, 4132-4142
5. Donepudi, M., Mac Sweeney, A., Briand, C., and Grütter, M. G. (2003) Insights into the regulatory mechanism for caspase-8 activation. Mol. Cell 11, 543-549
6. Micheau, O. (2003) Cellular FLICE-inhibitory protein: an attractive therapeutic target? Exp. Opin. Ther. Targets 7, 559-573
7. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J. L., Schröter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L. E., and Tschopp, J. (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388, 190-195
8. Krueger, A., Schmitz, I., Baumann, S., Krammer, P. H., and Kirchhoff, S. (2001) Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276, 20633-20640
9. Golks, A., Brenner, D., Fritsch, C., Krammer, P. H., and Lavrik, I. N. (2005) c-FLIPR, a new regulator of death receptor-induced apoptosis. J. Biol. Chem. 280, 14507-14513
10. Shirley, S., and Micheau, O. T. (2010) Cancer Lett., in press
11. Yang, J. K. (2008) FLIP as an anti-cancer therapeutic target. Yonsei Med. J. 29, 19-27
12. Olsson, A., Diaz, T., Aguilar-Santelises, M., Osterborg, A., Celsing, F., Jondal, M., and Osorio, L. M. (2001) Sensitization to TRAIL-induced apoptosis and modulation of FLICE-inhibitory protein in B chronic lymphocytic leukemia by actinomycin D. Leukemia 15, 1868-1877
13. MacFarlane, M., Harper, N., Snowden, R. T., Dyer, M. J., Barnett, G. A., Pringle, J. H., and Cohen, G. M. (2002) Mechanisms of resistance to TRAIL-induced apoptosis in primary B cell chronic lymphocytic leukaemia. Oncogene 21, 6809-6818
14. Korkolopoulou, P., Goudopoulou, A., Voutsinas, G., Thomas-Tsagli, E., Kapralos, P., Patsouris, E., and Saetta, A. A. (2004) c-FLIP expression in bladder urothelial carcinomas. Its role in resistance to Fas-mediated apoptosis and clinicopathologic correlations. Urology 63, 1198-1204
15. Salon, C., Eymin, B., Micheau, O., Chaperot, L., Plumas, J., Brambilla, C., Brambilla, E., and Gazzeri, S. (2006) E2F1 induces apoptosis and sensitizes human lung adenocarcinoma cells to death-receptor-mediated apoptosis through specific downregulation of c-FLIP(short). Cell Death Differ. 13, 260-272
16. Zong, H., Yin, B., Chen, J., Ma, B., Cai, D., and He, X. (2009) Over-expression of c-FLIP confers the resistance to TRAIL-induced apoptosis on gallbladder carcinoma. J. Exp. Med. 217, 203-208
17. Okano, H., Shiraki, K., Inoue, H., Kawakita, T., Yamanaka, T., Deguchi, M., Sugimoto, K., Sakai, T., Ohmori, S., Fujikawa, K., Murata, K., and Nakano, T. (2003) Cellular FLICE/caspase-8-inhibitory protein as a principal regulator of cell death and survival in human hepatocellular carcinoma. Lab. Invest. 83, 1033-1043
18. Djerbi, M., Screpanti, V., Catrina, A. I., Bogen, B., Biberfeld, P., and Grandien, A. (1999) The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med. 190, 1025-1032
19. Micheau, O., Lens, S., Gaide, O., Alevizopoulos, K., and Tschopp, J. (2001) NF-κB signals induce the expression of c-FLIP. Mol. Cell Biol. 21, 5299-5305
20. Kreuz, S., Siegmund, D., Scheurich, P., and Wajant, H. (2001) NF-κB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell Biol. 21, 3964-3973
21. Bartke, T., Siegmund, D., Peters, N., Reichwein, M., Henkler, F., Scheurich, P., and Wajant, H. (2001) p53 upregulates cFLIP, inhibits transcription of NF-κB-regulated genes and induces caspase-8-independent cell death in DLD-1 cells. Oncogene 20, 571-580
22. Tran, S. E., Meinander, A., Holmström, T. H., Rivero-Müller, A., Heiskanen, K. M., Linnau, E. K., Courtney, M. J., Mosser, D. D., Sistonen, L., and Eriksson, J. E. (2003) Heat stress downregulates FLIP and sensitizes cells to Fas receptor-mediated apoptosis. Cell Death Differ. 10, 1137-1147
23. Chang, L., Kamata, H., Solinas, G., Luo, J. L., Maeda, S., Venuprasad, K., Liu, Y. C., and Karin, M. (2006) The E3 ubiquitin ligase itch couples JNK activation to TNFα-induced cell death by inducing c-FLIP(L) turnover. Cell 124, 601-613
24. Fukazawa, T., Fujiwara, T., Uno, F., Teraishi, F., Kadowaki, Y., Itoshima, T., Takata, Y., Kagawa, S., Roth, J. A., Tschopp, J., and Tanaka, N. (2001) Accelerated degradation of cellular FLIP protein through the ubiquitin-proteasome pathway in p53-mediated apoptosis of human cancer cells. Oncogene 20, 5225-5231
25. Sánchez-Pérez, T., Ortiz-Ferrón, G., and López-Rivas, A. (2010) Mitotic arrest and JNK-induced proteasomal degradation of FLIP and Mcl-1 are key events in the sensitization of breast tumor cells to TRAIL by antimicrotubule agents. Cell Death Differ. 17, 883-894
26. Son, Y. G., Kim, E. H., Kim, J. Y., Kim, S. U., Kwon, T. K., Yoon, A. R., Yun, C. O., and Choi, K. S., (2007) Cancer Res. 67, 8274-8284
27. Zou, W., Chen, S., Liu, X., Yue, P., Sporn, M. B., Khuri, F. R, and Sun, S. Y. (2007) c-FLIP downregulation contributes to apoptosis induction by the novel synthetic triterpenoid methyl-2-cyano-3,12-dioxooleana-1,9-dien- 28-oate (CDDO-Me) in human lung cancer cells. Cancer Biol. Ther. 6, 1614-1620
28. Bouwmeester, T., Bauch, A., Ruffner, H., Angrand, P. O., Bergamini, G., Croughton, K., Cruciat, C., Eberhard, D., Gagneur, J., Ghidelli, S., Hopf, C., Huhse, B., Mangano, R., Michon, A. M., Schirle, M., Schlegl, J., Schwab, M., Stein, M. A., Bauer, A., Casari, G., Drewes, G., Gavin, A. C., Jackson, D. B., Joberty, G., Neubauer, G., Rick, J., Kuster, B., and Superti-Furga, G. (2004) A physical and functional map of the human TNF-α/NF-κB signal transduction pathway. Nat. Cell Biol. 6, 97-105
29. Xu, L. G., Li, L. Y., and Shu, H. B. (2004) TRAF7 potentiates MEKK3-induced AP1 and CHOP activation and induces apoptosis. J. Biol. Chem. 279, 17278-17282
30. Zotti, T., Vito, P., and Stilo, R. (2011) J. Cell. Physiol., in press
31. Zotti, T., Uva, A., Ferravante, A., Vessichelli, M., Scudiero, I., Ceccarelli, M., Vito, P., and Stilo, R. (2011) TRAF7 protein promotes Lys-29-linked polyubiquitination of IkB kinase (IKKγ)/NF-kB essential modulator (NEMO) and p65/RelA protein and represses NF-kB activation. J. Biol. Chem. 286, 22924-22933
32. Yeh, W. C., Shahinian, A., Speiser, D., Kraunus, J., Billia, F., Wakeham, A., de la Pompa, J. L., Ferrick, D., Hum, B., Iscove, N., Ohashi, P., Rothe, M., Goeddel, D. V., and Mak, T. W. (1997) Early lethality, functional NF-kB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7, 715-725
33. Tournier, C., Hess, P., Yang, D. D., Xu, J., Turner, T. K., Nimnual, A., Bar-Sagi, D., Jones, S. N., Flavell, R. A., and Davis, R. J. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870-874
34. De Smaele, E., Zazzeroni, F., Papa, S., Nguyen, D. U., Jin, R., Jones, J., Cong, R., and Franzoso, G. (2001) Induction of gadd45β by NF-kB downregulates pro-apoptotic JNK signalling. Nature 414, 308-313
35. Herr, I., Krilleke, D., and Debatin, K. M. (2000) A sensitive, non-radioactive and fast method for detection of JNK/SAPK activity in leukemic T cells. Leukemia 14, 1859-1860
36. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J., Slaughter, C., Pickart, C., and Chen, Z. J. (2000) Activation of the IkB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361
37. Chastagner, P., Israël, A., and Brou, C. (2006) Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep. 7, 1147-1153
38. -/- cells from TNF-induced apoptosis. Cell Death Differ. 9, 138-144
39. Beg, A. A., and Baltimore, D. (1996) An essential role for NF-kB in preventing TNF-α-induced cell death. Science 274, 782-784
40. Karin, M., and Lin, A. (2002) NF-kB at the crossroads of life and death. Nat. Immunol. 3, 221-227
41. Longley, D. B., Wilson, T. R., McEwan, M., Allen, W. L., McDermott, U., Galligan, L., and Johnston, P. G. (2006) c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene 25, 838-848
42. Chawla-Sarkar, M., Bae, S. I., Reu, F. J., Jacobs, B. S., Lindner, D. J., and Borden, E. C. (2004) Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ. 11, 915-923
43. Galligan, L., Longley, D. B., McEwan, M., Wilson, T. R., McLaughlin, K., and Johnston, P. G. (2005) Chemotherapy and TRAIL-mediated colon cancer cell death. The roles of p53, TRAIL receptors, and c-FLIP. Mol. Cancer Ther. 4, 2026-2036