RIP1 protein-dependent assembly of a cytosolic cell death complex is required for inhibitor of apoptosis (IAP) inhibitor-mediated sensitization to lexatumumab-induced apoptosis

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38767-38777

  Basit, Farhan ^a   Humphreys, Robin ^b   Fulda, Simone ^a  

^a GOETHE UNIVERSITY   (Germany)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL LINES; CELL VIABILITY; CLONOGENIC SURVIVAL; CYTOSOLIC; CYTOSOLIC COMPLEXES; INDUCED APOPTOSIS; INHIBITOR OF APOPTOSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; RHABDOMYOSARCOMA; RNA INTERFERENCE; SMALL-MOLECULE INHIBITORS; SYNERGISTIC MANNER;

CELL CULTURE; MAGNESIUM PRINTING PLATES; MONOCLONAL ANTIBODIES; PROTEINS; RNA;

CELL DEATH;

CASPASE 3; CASPASE 8; CASPASE 9; CELL PROTEIN; DEATH RECEPTOR 4; DEATH RECEPTOR 5; FAS ASSOCIATED DEATH DOMAIN PROTEIN; LEXATUMUMAB; MAPATUMUMAB; RECEPTOR ACTIVATING PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER SURVIVAL; CELL SURVIVAL; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; INHIBITION KINETICS; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; RHABDOMYOSARCOMA; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANTIBODIES, MONOCLONAL; APOPTOSIS; CASPASES; CELL SEPARATION; CELL SURVIVAL; CYTOSOL; FLOW CYTOMETRY; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MITOCHONDRIA; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RHABDOMYOSARCOMA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84869056283     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398966     Document Type: Article

References (38)

1. Ashkenazi, A. (2008) Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat. Rev. Drug Discov. 7, 1001-1012
2. Fulda, S., Galluzzi, L., and Kroemer, G. (2010) Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov. 9, 447-464
3. Fulda, S. (2009) Tumor resistance to apoptosis. Int. J. Cancer 124, 511-515
4. LaCasse, E. C., Mahoney, D. J., Cheung, H. H., Plenchette, S., Baird, S., and Korneluk, R. G. (2008) IAP-targeted therapies for cancer. Oncogene 27, 6252-6275
5. Varfolomeev, E., Blankenship, J. W., Wayson, S. M., Fedorova, A. V., Kayagaki, N., Garg, P., Zobel, K., Dynek, J. N., Elliott, L. O., Wallweber, H. J., Flygare, J. A., Fairbrother, W. J., Deshayes, K., Dixit, V. M., and Vucic, D. (2007) IAP antagonists induce autoubiquitination of cIAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681
6. Vince, J. E., Wong, W. W., Khan, N., Feltham, R., Chau, D., Ahmed, A. U., Benetatos, C. A., Chunduru, S. K., Condon, S. M., McKinlay, M., Brink, R., Leverkus, M., Tergaonkar, V., Schneider, P., Callus, B. A., Koentgen, F., Vaux, D. L., and Silke, J. (2007) IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693
7. Bertrand, M. J., Milutinovic, S., Dickson, K. M., Ho, W. C., Boudreault, A., Durkin, J., Gillard, J. W., Jaquith, J. B., Morris, S. J., and Barker, P. A. (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700
8. Varfolomeev, E., Wayson, S. M., Dixit, V. M., Fairbrother, W. J., and Vucic, D. (2006) The inhibitor of apoptosis protein fusion cIAP2·MALT1 stimulates NF-κB activation independently of TRAF1 and TRAF2. J. Biol. Chem. 281, 29022-29029
9. Dagher, R., and Helman, L. (1999) Rhabdomyosarcoma: an overview. Oncologist 4, 34-44
10. Hayes-Jordan, A., and Andrassy, R. (2009) Rhabdomyosarcoma in children. Curr. Opin. Pediatr. 21, 373-378
11. Humphreys, R. C., and Halpern, W. (2008) TRAIL receptors: targets for cancer therapy. Adv. Exp. Med. Biol. 615, 127-158
12. Oost, T. K., Sun, C., Armstrong, R. C., Al-Assaad, A. S., Betz, S. F., Deckwerth, T. L., Ding, H., Elmore, S. W., Meadows, R. P., Olejniczak, E. T., Oleksijew, A., Oltersdorf, T., Rosenberg, S. H., Shoemaker, A. R., Tomaselli, K. J., Zou, H., and Fesik, S. W. (2004) Discovery of potent antagonists of the anti-apoptotic protein XIAP for the treatment of cancer. J. Med. Chem. 47, 4417-4426
13. Chao, B., Deckwerth, T. L., Furth, P., S., Linton, S., D., Spada, A., P., Ullman, B., R., and Weinhouse, M. I. (February 16, 2006) U.S. Patent PCT/US2005/024700
14. Löder, S., Fakler, M., Schoeneberger, H., Cristofanon, S., Leibacher, J., Vanlangenakker, N., Bertrand, M. J., Vandenabeele, P., Jeremias, I., Debatin, K. M., and Fulda, S. (2012) RIP1 is required for IAP inhibitor-mediated sensitization of childhood acute leukemia cells to chemotherapy-induced apoptosis. Leukemia 26, 1020-1029
15. Fulda, S., Sieverts, H., Friesen, C., Herr, I., and Debatin, K. M. (1997) The CD95 (APO-1/Fas) system mediates drug-induced apoptosis in neuroblastoma cells. Cancer Res. 57, 3823-3829
16. Chou, T. C. (1991) in Synergism and Antagonism in Chemotherapy (Chou, T. C., ed) pp. 61-102, Academic Press, San Diego, CA
17. Kang, Z., Chen, J. J., Yu, Y., Li, B., Sun, S. Y., Zhang, B., and Cao, L. (2011) Drozitumab, a human antibody to death receptor 5, has potent antitumor activity against rhabdomyosarcoma with the expression of caspase-8 predictive of response. Clin. Cancer Res. 17, 3181-3192
18. Stadel, D., Mohr, A., Ref, C., MacFarlane, M., Zhou, S., Humphreys, R., Bachem, M., Cohen, G., Möller, P., Zwacka, R. M., Debatin, K. M., and Fulda, S. (2010) TRAIL-induced apoptosis is preferentially mediated via TRAIL receptor 1 in pancreatic carcinoma cells and profoundly enhanced by XIAP inhibitors. Clin. Cancer Res. 16, 5734-5749
19. Varfolomeev, E., Goncharov, T., Fedorova, A. V., Dynek, J. N., Zobel, K., Deshayes, K., Fairbrother, W. J., and Vucic, D. (2008) cIAP1 and cIAP2 are critical mediators of tumor necrosis factor α (TNFα)-induced NF-κB activation. J. Biol. Chem. 283, 24295-24299
20. Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G. D., Mitchison, T. J., Moskowitz, M. A., and Yuan, J. (2005) Chemical inhibitor of non-apoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112-119
21. Fulda, S., Küfer, M. U., Meyer, E., van Valen, F., Dockhorn-Dworniczak, B., and Debatin, K. M. (2001) Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer. Oncogene 20, 5865-5877
22. van Noesel, M. M., van Bezouw, S., VoÛte, P. A., Herman, J. G., Pieters, R., and Versteeg, R. (2003) Clustering of hypermethylated genes in neuroblastoma. Genes Chromosomes Cancer 38, 226-233
23. Wang, L., Du, F., and Wang, X. (2008) TNFα induces two distinct caspase-8 activation pathways. Cell 133, 693-703
24. Petersen, S. L., Wang, L., Yalcin-Chin, A., Li, L., Peyton, M., Minna, J., Harran, P., and Wang, X. (2007) Autocrine TNFα signaling renders human cancer cells susceptible to Smac mimetic-induced apoptosis. Cancer Cell 12, 445-456
25. Biton, S., and Ashkenazi, A. (2011) NEMO and RIP1 control cell fate in response to extensive DNA damage via TNFα feedforward signaling. Cell 145, 92-103
26. Tenev, T., Bianchi, K., Darding, M., Broemer, M., Langlais, C., Wallberg, F., Zachariou, A., Lopez, J., MacFarlane, M., Cain, K., and Meier, P. (2011) The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43, 432-448
27. Feoktistova, M., Geserick, P., Kellert, B., Dimitrova, D. P., Langlais, C., Hupe, M., Cain, K., MacFarlane, M., Häcker, G., and Leverkus, M. (2011) cIAPs block Ripoptosome formation, a RIP1/caspase-8-containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43, 449-463
28. Geserick, P., Hupe, M., Moulin, M., Wong, W. W., Feoktistova, M., Kellert, B., Gollnick, H., Silke, J., and Leverkus, M. (2009) Cellular IAPs inhibit a cryptic CD95-induced cell death by limiting RIP1 kinase recruitment. J. Cell Biol. 187, 1037-1054
29. Hitomi, J., Christofferson, D. E., Ng, A., Yao, J., Degterev, A., Xavier, R. J., and Yuan, J. (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135, 1311-1323
30. Vanlangenakker, N., Vanden Berghe, T., and Vandenabeele, P. (2012) Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 19, 75-86
31. Smith, M. A., Morton, C. L., Kolb, E. A., Gorlick, R., Keir, S. T., Carol, H., Lock, R., Kang, M. H., Reynolds, C. P., Maris, J. M., Watkins, A. E., and Houghton, P. J. (2010) Initial testing (stage 1) of mapatumumab (HGSRIP1 ETR1) by the pediatric preclinical testing program. Pediatr. Blood Cancer 54, 307-310
32. Houghton, P. J., Kang, M. H., Reynolds, C. P., Morton, C. L., Kolb, E. A., Gorlick, R., Keir, S. T., Carol, H., Lock, R., Maris, J. M., Billups, C. A., and Smith, M. A. (2012) Initial testing (stage 1) of LCL161, a Smac mimetic, by the Pediatric Preclinical Testing Program. Pediatr. Blood Cancer 58, 636-639
33. Fox, N. L., Humphreys, R., Luster, T. A., Klein, J., and Gallant, G. (2010) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) receptor 1 and receptor 2 agonists for cancer therapy. Expert Opin. Biol. Ther. 10, 1-18
34. Fulda, S., and Vucic, D. (2012) Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 11, 109-124
35. Vogler, M., Walczak, H., Stadel, D., Haas, T. L., Genze, F., Jovanovic, M., Bhanot, U., Hasel, C., Möller, P., Gschwend, J. E., Simmet, T., Debatin, K. M., and Fulda, S. (2009) Small-molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res. 69, 2425-2434
36. Loeder, S., Zenz, T., Schnaiter, A., Mertens, D., Winkler, D., Döhner, H., Debatin, K. M., Stilgenbauer, S., and Fulda, S. (2009) A novel paradigm to trigger apoptosis in chronic lymphocytic leukemia. Cancer Res. 69, 8977-8986
37. Fakler, M., Loeder, S., Vogler, M., Schneider, K., Jeremias, I., Debatin, K. M., and Fulda, S. (2009) Small-molecule XIAP inhibitors cooperate with TRAIL to induce apoptosis in childhood acute leukemia cells and overcome Bcl-2-mediated resistance. Blood 113, 1710-1722
38. Abhari, B. A., Cristofanon, S., Kappler, R., von Schweinitz, D., Humphreys, R., and Fulda, S. (2012) RIP1 is required for IAP inhibitor-mediated sensitization for TRAIL-induced apoptosis via a RIP·FADD·caspase-8 cell death complex. Oncogene, in press