Polyi:C-induced, TLR3/RIP3-dependent necroptosis backs up immune effector-mediated tumor elimination in vivo

Cancer Immunology Research

Volumn 3, Issue 8, 2015, Pages 902-914

  Takemura, Ryo ^a   Takaki, Hiromi ^a   Okada, Seiji ^b   Shime, Hiroaki ^a   Akazawa, Takashi ^c   Oshiumi, Hiroyuki ^a   Matsumoto, Misako ^a   Teshima, Takanori ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CASPASE 8; GAMMA INTERFERON; INFLAMMASOME; INTERFERON; INTERLEUKIN 1BETA; MAVS PROTEIN; MDA5 PROTEIN; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; RECEPTOR INTERACTING PROTEIN KINASE 3; RNA; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BENZYLOXYCARBONYL-VALYL-ALANYL-ASPARTIC ACID; OLIGOPEPTIDE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL LINE; CELL DEATH; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF DETECTION; MOUSE; NECROPTOSIS; NONHUMAN; PROTEIN EXPRESSION; PYROPTOSIS; TUMOR GROWTH; TUMOR VOLUME; TUNEL ASSAY; UPREGULATION; WST-1 ASSAY; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HUMAN; IMMUNOLOGY; METABOLISM; NEOPLASM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HETEROGRAFTS; HUMANS; MICE; NEOPLASMS; OLIGOPEPTIDES; POLY I-C; REACTIVE OXYGEN SPECIES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TUMOR BURDEN;

EID: 84962016546     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0219     Document Type: Article

References (55)

1. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G. Viral control of mitochondrial apoptosis. PLoS Pathog 2008;4:e1000018.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
3. Criscitiello C, Esposito A, Curigliano G. Tumor-stroma crosstalk: targeting stroma in breast cancer. Curr Opin Oncol 2014;26:551-5.
4. Moriwaki K, Chan FK. RIP3: a molecular switch for necrosis and inflammation. Genes Dev 2013;27:1640-9.
5. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010;11:700-14.
6. Su Z, Yang Z, Xu Y, Chen Y, Yu Q. Apoptosis, autophagy, necroptosis, and cancer metastasis. Mol Cancer 2015;14:48.
7. Roma-Rodrigues C, Fernandes AR, Baptista PV. Exosome in tumour microenvironment: overview of the crosstalk between normal and cancer cells. Biomed Res Int 2014;2014:179486.
8. Tatematsu M, Seya T, Matsumoto M. Beyond dsRNA: Toll-like receptor 3 signalling in RNA-induced immune responses. Biochem J 2014;458:195-201.
9. Tatematsu M, Nishikawa F, Seya T, Matsumoto M. Toll-like receptor 3 recognizes incomplete stem structures in single-stranded viral RNA. Nat Commun 2013;4:1833.
10. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009;9:353-63.
11. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008;8:279-89.
12. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012;19:107-20.
13. Seya T, Shime H, Takaki H, Azuma M, Oshiumi H, Matsumoto M. TLR3/TICAM-1 signaling in tumor cell RIP3-dependent necroptosis. Oncoimmunology 2012;1:917-23.
14. Matsumoto M, Seya T. TLR3: interferon induction by double-strandedRNA including poly (I:C). Adv Drug Deliv Rev 2008;60:805-12.
15. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005;6:981-8.
16. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferonbeta induction. Nat Immunol 2003;4:161-7.
17. Kaiser WJ, Offermann MK. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J Immunol 2005;174:4942-52.
18. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, et al. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003;8:237-49.
19. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, et al. TRIF licenses caspase-11-dependent NLRP3 inflammasomeactivation by gram-negative bacteria. Cell 2012;150:606-19.
20. Seya T, Matsumoto M. The extrinsic RNA-sensing pathway for adjuvant immunotherapy of cancer. Cancer Immunol Immunother 2009;58:1175-84.
21. Akazawa T, Ebihara T, Okuno M, Okuda Y, Shingai M, Tsujimura K, et al. Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc Natl Acad Sci U S A 2007;104:252-7.
22. Ono A, Hattori S, Kariya R, Iwanaga S, Taura M, Harada H, et al. Comparative study of human hematopoietic cell engraftment into BALB/c and C57BL/6 strain of rag-2/jak3 double-deficient mice. J Biomed Biotechnol 2011;2011:539748.
23. Azuma M, Ebihara T, Oshiumi H, Matsumoto M, Seya T. Cross-priming for antitumor CTL induced by soluble Ag + polyI:C depends on the TICAM-1 pathway in mouse CD11c (+)/CD8a (+) dendritic cells. Oncoimmunology 2012;1:581-92.
24. Wu YT, Tan HL, Huang Q, Sun XJ, Zhu X, Shen HM. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFa mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ 2011;18:26-37.
25. Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW, Gough PJ, et al. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J Biol Chem 2013;288:31268-79.
26. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013;341:1246-9.
27. Thapa RJ, Nogusa S, Chen P, Maki JL, Lerro A, Andrake M, et al. Interferoninduced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc Natl Acad Sci U S A 2013;110:E3109-18.
28. Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q, Luo J, et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci U S A 2012;109:5322-7.
29. Künstle G, Leist M, Uhlig S, Revesz L, Feifel R, MacKenzie A, et al. ICEprotease inhibitors block murine liver injury and apoptosis caused by CD95 or by TNF-alpha. Immunol Lett 1997;55:5-10.
30. Jouan-Lanhouet S, Riquet F, Duprez L, Vanden Berghe T, Takahashi N, Vandenabeele P. Necroptosis, in vivo detection in experimental disease models. Semin Cell Dev Biol 2014;35:2-13.
31. Kang SJ, Wang S, Kuida K, Yuan J. Distinct downstream pathways of caspase-11 in regulating apoptosis and cytokine maturation during septic shock response. Cell Death Differ 2002;9:1115-25.
32. Nomura M, Ueno A, Saga K, Fukuzawa M, Kaneda Y. Accumulation of cytosolic calcium induces necroptotic cell death in human neuroblastoma. Cancer Res 2013;74:1056-66.
33. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, et al., The RNA helicase RIG-I has an essential function in doublestranded RNA-induced innate antiviral responses. Nat Immunol 2004;5:730-7
34. Wang X, Jiang W, Yan Y, Gong T, Han J, Tian Z, et al. RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat Immunol 2014;15:1126-33.
35. Scheffer SR, Nave H, Korangy F, Schlote K, Pabst R, Jaffee EM, et al. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int J Cancer 2003;103:205-11.
36. Goldszmid RS, Idoyaga J, Bravo AI, Steinman R, Mordoh J, Wainstok R. Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma. J Immunol 2003;171:5940-7.
37. Bartholomae WC, Rininsland FH, Eisenberg JC, Boehm BO, Lehmann PV, Tary-Lehmann M. T cell immunity induced by live, necrotic, and apoptotic tumor cells. J Immunol 2004;173:1012-22.
38. Yoon TJ, Kim JY, Kim H, Hong C, Lee H, Lee CK, et al. Anti-tumor immunostimulatory effect of heat-killed tumor cells. Exp Mol Med 2008;40:130-44.
39. Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, et al. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med 2012;18:1286-90.
40. Roderick JE, Hermance N, Zelic M, Simmons MJ, Polykratis A, Pasparakis M, et al. Hematopoietic RIPK1 deficiency results in bone marrow failure caused by apoptosis and RIPK3-mediated necroptosis. Proc Natl Acad Sci U S A 2014;111:14436-41.
41. Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C, Wachsmuth L, et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 2014;513:90-4.
42. Narayan N, Lee IH, Borenstein R, Sun J, Wong R, Tong G, et al. The NADdependent deacetylase SIRT2 is required for programmed necrosis. Nature 2012;492:199-204.
43. Matsumoto M, Tatematsu M, Nishikawa F, Azuma M, Ishii N, Morii-Sakai A, et al. Defined TLR3-specific adjuvant that induces NK and CTL activation without significant cytokine production in vivo. Nat Commun 2015;6:6280.
44. Ebihara T, Azuma M, Oshiumi H, Kasamatsu J, Iwabuchi K, Matsumoto K, et al. Identification of a polyI: C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 2010;207:2675-87.
45. Kasamatsu J, Azuma M, Oshiumi H, Morioka Y, Okabe M, Ebihara T, et al. INAM plays a critical role in IFN-g production by NK cells interacting with polyinosinic-polycytidylic acid-stimulated accessory cells. J Immunol 2014;193:5199-207.
46. Wang Y, Cella M, Gilfillan S, Colonna M. Polyinosinic: polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiationassociated protein 5 expressed in stromal cells. J Immunol 2010;184:2751-5.
47. Shime H, Matsumoto M, Oshiumi H, Tanaka S, Nakane A, Iwakura Y, et al. Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors. Proc Natl Acad Sci U S A 2012;109:2066-71.
48. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013;19:1423-37.
49. Masuda H, Saeki Y, Nomura M, Shida K, Matsumoto M, Ui M, et al. High levels of RAE-1 isoforms on mouse tumor cell lines assessed by anti-"pan" RAE-1 antibody confer tumor susceptibility to NK cells. Biochem Biophys Res Commun 2002;290:140-5.
50. Salaun B, Lebecque S, Matikainen S, Rimoldi D, Romero P. Toll-like receptor 3 expressed by melanoma cells as a target for therapy? Clin Cancer Res 2007;13:4565-74.
51. Conforti R, Ma Y, Morel Y, Paturel C, Terme M, Viaud S, et al. Opposing effects of toll-like receptor (TLR3) signaling in tumors can be therapeutically uncoupled to optimize the anticancer efficacy of TLR3 ligands. Cancer Res 2010;70:490-500.
52. Morikawa T, Sugiyama A, Kume H, Ota S, Kashima T, Tomita K, et al. Identification of Toll-like receptor 3 as a potential therapeutic target in clear cell renal cell carcinoma. Clin Cancer Res 2007;13:5703-9.
53. Salaun B, Zitvogel L, Asselin-Paturel C, Morel Y, Chemin K, Dubois C, et al. TLR3 as a biomarker for the therapeutic efficacy of double-stranded RNA in breast cancer. Cancer Res 2011;7:1607-14.
54. Mocarski ES, Upton JW, Kaiser WJ. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat Rev Immunol 2012;12:79-88.
55. Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 2013;38:209-23.