Mitochondrial permeabilization engages NF-κB-dependent anti-tumour activity under caspase deficiency

Nature Cell Biology

Volumn 19, Issue 9, 2017, Pages 1116-1129

  Giampazolias, Evangelos ^a   Zunino, Barbara ^a   Dhayade, Sandeep ^a   Bock, Florian ^a   Cloix, Catherine ^a   Cao, Kai ^a   Roca, Alba ^a   Lopez, Jonathan ^a   Ichim, Gabriel ^a   Proïcs, Emma ^b   Rubio Patiño, Camila ^b   Fort, Loic ^a   Yatim, Nader ^c   Woodham, Emma ^a   Orozco, Susana ^d   Taraborrelli, Lucia ^e   Peltzer, Nieves ^e   Lecis, Daniele ^f   Machesky, Laura ^a   Walczak, Henning ^e   Albert, Matthew L ^c,g   Milling, Simon ^a   Oberst, Andrew ^d   Ricci, Jean Ehrland ^b   Ryan, Kevin M ^a   Blyth, Karen ^a   Tait, Stephen W G ^a,h   more..

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f NATIONAL CANCER INSTITUTE   (Italy)

^g GENENTECH INC   (United States)

^h CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NAVITOCLAX; NECROSTATIN1; PHOSPHOTRANSFERASE INHIBITOR; Q VD OPH; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; AUTACOID; INHIBITOR OF APOPTOSIS PROTEIN; NF-KAPPA B KINASE; PROTEIN SERINE THREONINE KINASE; SULFONAMIDE; TNFRSF1A PROTEIN, MOUSE; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER THERAPY; CELL DEATH; CELL KILLING; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; MOUSE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; REPEATED DRUG DOSE; SIGNAL TRANSDUCTION; TUMOR REGRESSION; ANIMAL; BAGG ALBINO MOUSE; COLONIC NEOPLASMS; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HELA CELL LINE; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE ACTIVATION; METABOLISM; MITOCHONDRION; NECROSIS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PERMEABILITY; PHENOTYPE; RNA INTERFERENCE; SCID MOUSE; TIME FACTOR;

ANILINE COMPOUNDS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASES; COLONIC NEOPLASMS; GENOTYPE; HELA CELLS; HUMANS; INFLAMMATION MEDIATORS; INHIBITOR OF APOPTOSIS PROTEINS; MACROPHAGE ACTIVATION; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NECROSIS; NF-KAPPA B; PERMEABILITY; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SULFONAMIDES; TIME FACTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85028669130     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3596     Document Type: Article

References (43)

1. Tait, S. W., & Green, D. R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11, 621-632 (2010
2. Tait, S. W., Ichim, G., & Green, D. R. Die another way-non-apoptotic mechanisms of cell death. J. Cell Sci. 127, 2135-2144 (2014
3. Lopez, J., & Tait, S. W. Mitochondrial apoptosis: killing cancer using the enemy within. Br. J. Cancer 112, 957-962 (2015
4. Ichim, G., & Tait, S. W. A fate worse than death: apoptosis as an oncogenic process. Nat. Rev. Cancer 16, 539-548 (2016
5. Labi, V., & Erlacher, M. How cell death shapes cancer. Cell Death Dis. 6, e1675 (2015
6. Ichim, G., et al. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol. Cell 57, 860-872 (2015
7. Lovric, M. M., & Hawkins, C. J. TRAIL treatment provokes mutations in surviving cells. Oncogene 29, 5048-5060 (2010
8. Liu, X., et al. Caspase-3 promotes genetic instability and carcinogenesis. Mol. Cell 58, 284-296 (2015
9. Tait, S. W., et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep. 5, 878-885 (2013
10. Oltersdorf, T., et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 (2005
11. Wallach, D., Kang, T. B., Dillon, C. P., & Green, D. R. Programmed necrosis in inflammation: toward identification of the effector molecules. Science 352, aaf2154 (2016
12. Lopez, J., et al. Mito-priming as a method to engineer Bcl-2 addiction. Nat. Commun. 7, 10538 (2016
13. Kim, K. W., et al. Caspase cleavage product lacking amino-terminus of I Bβ sensitizes resistant cells to TNF-β and TRAIL-induced apoptosis. J. Cell. Biochem. 85, 334-345 (2002
14. Van Antwerp, D. J., Martin, S. J., Kafri, T., Green, D. R., & Verma, I. M. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274, 787-789 (1996
15. Varfolomeev, E., et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNF α-dependent apoptosis. Cell 131, 669-681 (2007
16. Vince, J. E., et al. IAP antagonists target cIAP1 to induce TNF α-dependent apoptosis. Cell 131, 682-693 (2007
17. Martins, L. M., et al. Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol. Cell. Biol. 24, 9848-9862 (2004
18. Abulwerdi, F., et al. A novel small-molecule inhibitor of mcl-1 blocks pancreatic cancer growth in vitro and in vivo. Mol. Cancer Ther. 13, 565-575 (2014
19. Verhagen, A. M., et al. Identification of mammalian mitochondrial proteins that interact with IAPs via N-terminal IAP binding motifs. Cell Death Differ. 14, 348-357 (2007
20. Zhuang, M., Guan, S., Wang, H., Burlingame, A. L., & Wells, J. A. Substrates of IAP ubiquitin ligases identified with a designed orthogonal E3 ligase, the NEDDylator. Mol. Cell 49, 273-282 (2013
21. Silke, J., et al. The anti-apoptotic activity of XIAP is retained upon mutation of both the caspase 3-and caspase 9-interacting sites. J. Cell Biol. 157, 115-124 (2002
22. Rongvaux, A., et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 159, 1563-1577 (2014
23. White, M. J., et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell 159, 1549-1562 (2014
24. Biswas, S. K., & Mantovani, A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11, 889-896 (2010
25. Aaes, T. L., et al. Vaccination with necroptotic cancer cells induces efficient antitumor immunity. Cell Rep. 15, 274-287 (2016
26. Li, J., et al. TCPA: a resource for cancer functional proteomics data. Nat. Methods 10, 1046-1047 (2013
27. Lartigue, L., et al. Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol. Biol. Cell 20, 4871-4884 (2009
28. Hayden, M. S., & Ghosh, S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26, 203-234 (2012
29. Dondelinger, Y., et al. NF-κB-independent role of IKKα/IKKβ in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol. Cell 60, 63-76 (2015
30. Ramakrishnan, P., Wang, W., & Wallach, D. Receptor-specific signaling for both the alternative and the canonical NF-κB activation pathways by NF-κB-inducing kinase. Immunity 21, 477-489 (2004
31. Zarnegar, B., Yamazaki, S., He, J. Q., & Cheng, G. Control of canonical NF-κB activation through the NIK-IKK complex pathway. Proc. Natl Acad. Sci. USA 105, 3503-3508 (2008
32. Demchenko, Y. N., et al. Classical and/or alternative NF-κB pathway activation in multiple myeloma. Blood 115, 3541-3552 (2010
33. Cheung, H. H., et al. SMG1 and NIK regulate apoptosis induced by Smac mimetic compounds. Cell Death Dis. 2, e146 (2011
34. Kim, K. W., Moretti, L., & Lu, B. M867, a novel selective inhibitor of caspase-3 enhances cell death and extends tumor growth delay in irradiated lung cancer models. PLoS ONE 3, e2275 (2008
35. Werthmoller, N., Frey, B., Wunderlich, R., Fietkau, R., & Gaipl, U. S. Modulation of radiochemoimmunotherapy-induced B16 melanoma cell death by the pan-caspase inhibitor zVAD-fmk induces anti-tumor immunity in a HMGB1-, nucleotide-and T-cell-dependent manner. Cell Death Dis. 6, e1761 (2015
36. Yatim, N., et al. RIPK1 and NF-κB signaling in dying cells determines cross-priming of CD8(C) T cells. Science 350, 328-334 (2015
37. Koo, G. B., et al. Methylation-dependent loss of RIP3 expression in cancer represses programmed necrosis in response to chemotherapeutics. Cell Res. 25, 707-725 (2015
38. Lecis, D., et al. Dimeric Smac mimetics/IAP inhibitors as in vivo-active pro-apoptotic agents. Part II: Structural and biological characterization. Bioorg. Med. Chem. 20, 6709-6723 (2012
39. Shalem, O., et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343, 84-87 (2014
40. Sanjana, N. E., Shalem, O., & Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11, 783-784 (2014
41. Graczyk, D., White, R. J., & Ryan, K. M. Involvement of RNA polymerase III in immune responses. Mol. Cell. Biol. 35, 1848-1859 (2015
42. Peltzer, N., et al. HOIP deficiency causes embryonic lethality by aberrant TNFR1-mediated endothelial cell death. Cell Rep. 9, 153-165 (2014
43. Werner, A. B., de Vries, E., Tait, S. W., Bontjer, I., & Borst, J. Bcl-2 family member Bfl-1/A1 sequesters truncated bid to inhibit is collaboration with pro-apoptotic Bak or Bax. J. Biol. Chem. 277, 22781-22788 (2002