Double-stranded RNA promotes CTL-independent tumor cytolysis mediated by CD11b + Ly6G + intratumor myeloid cells through the TICAM-1 signaling pathway

Cell Death and Differentiation

Volumn 24, Issue 3, 2017, Pages 385-396

  Shime, Hiroaki ^a   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; CASPASE 3; CASPASE 8; CD11B ANTIGEN; DOUBLE STRANDED RNA; INTERLEUKIN 1 RECEPTOR; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; IFNAR1 PROTEIN, MOUSE; IPS-1 PROTEIN, MOUSE; LY ANTIGEN; LY6G ANTIGEN, MOUSE; POLYINOSINIC POLYCYTIDYLIC ACID; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER CELL LINE; CELL DEATH; CYTOTOXICITY; DENDRITIC CELL; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR CELL DESTRUCTION; TUMOR GROWTH; TUMOR REGRESSION; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; DEFICIENCY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; SPLEEN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIGENS, LY; APOPTOSIS; CASPASE 3; CASPASE 8; CD11B ANTIGEN; CELL PROLIFERATION; CELLS, CULTURED; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; POLY I-C; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; RECEPTOR, INTERFERON ALPHA-BETA; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84994761168     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.131     Document Type: Article

References (58)

1. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-322
2. Gajewski TF, Schreiber H, Fu Y-X. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14: 1014-1022
3. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12: 252-264
4. Marabelle A, Kohrt H, Caux C, Levy R. Intratumoral immunization: a new paradigm for cancer therapy. Clin Cancer Res 2014; 20: 1747-1756
5. 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 USA 2007; 104: 252-257
6. 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: 581-592
7. Matsumoto M, Funami K, Tanabe M, Oshiumi H, Shingai M, Seto Y, et al. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J Immunol 2003; 171: 3154-3162
8. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003; 4: 161-167
9. McCartney S, Vermi W, Gilfillan S, Cella M, Murphy TL, Schreiber RD, et al. Distinct and complementary functions of MDA5 and TLR3 in poly(I: C)-mediated activation of mouse NK cells. J Exp Med 2009; 206: 2967-2976
10. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12: 253-268
11. Pekarek LA, Starr BA, Toledano AY, Schreiber H. Inhibition of tumor growth by elimination of granulocytes. J Exp Med 1995; 181: 435-440
12. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA 2006; 103: 12493-12498
13. Shojaei F, Wu X, Qu X, Kowanetz M, Yu L, Tan M, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci USA 2009; 106: 6742-6747
14. Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumorbearing mice. J Immunol 2008; 181: 5791-5802
15. Dumitru CA, Lang S, Brandau S. Modulation of neutrophil granulocytes in the tumor microenvironment: mechanisms and consequences for tumor progression. Semin Cancer Biol 2013; 23: 141-148
16. Reid MD, Basturk O, Thirabanjasak D, Hruban RH, Klimstra DS, Bagci P, et al. Tumorinfiltrating neutrophils in pancreatic neoplasia. Mod Pathol 2011; 24: 1612-1619
17. Donskov F, Maase, von Der H. Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 2006; 24: 1997-2005
18. Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 2009; 182: 5693-5701
19. Raber PL, Thevenot P, Sierra R, Wyczechowska D, Halle D, Ramirez ME, et al. Subpopulations of myeloid-derived suppressor cells impair T cell responses through independent nitric oxide-related pathways. Int J Cancer 2013; 134: 2853-2864
20. Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 2007; 13: 828-835
21. Lu T, Ramakrishnan R, Altiok S, Youn J-I, Cheng P, Celis E, et al. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest 2011; 121: 4015-4029
22. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: N1 versus ?N2? TAN. Cancer Cell 2009; 16: 183-194
23. Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011; 20: 300-314
24. Finisguerra V, Di Conza G, Di Matteo M, Serneels J, Costa S, Thompson AAR, et al. MET is required for the recruitment of anti-tumoural neutrophils. Nature 2015; 522: 349-353
25. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41: 49-61
26. Zoglmeier C, Bauer H, Nörenberg D, Wedekind G, Bittner P, Sandholzer N, et al. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice. Clin Cancer Res 2011; 17: 1765-1775
27. Shirota Y, Shirota H, Klinman DM. Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells. J Immunol 2012; 188: 1592-1599
28. Shime H, Kojima A, Maruyama A, Saito Y, Oshiumi H, Matsumoto M, et al. Myeloid-derived suppressor cells confer tumor-suppressive functions on natural killer cells via polyinosinic: polycytidylic acid treatment in mouse tumor models. J Innate Immun 2014; 6: 293-305
29. 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 USA 2012; 109: 2066-2071
30. Crowder RN, El-Deiry WS. Caspase-8 regulation of TRAIL-mediated cell death. Exp Oncol 2012; 34: 160-164
31. Olsson M, Zhivotovsky B. Caspases and cancer. Cell Death Differ 2011; 18: 1441-1449
32. Estornes Y, Toscano F, Virard F, Jacquemin G, Pierrot A, Vanbervliet B, et al. dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ 2012; 19: 1482-1494
33. Takemura R, Takaki H, Okada S, Shime H, Akazawa T, Oshiumi H, et al. PolyI: C-induced, TLR3/RIP3-dependent necroptosis backs up immune effector-mediated tumor elimination in vivo. Cancer Immunol Res 2015; 3: 902-914
34. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008; 322: 1097-1100
35. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004; 6: 409-421
36. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007; 25: 911-920
37. Ren G, Zhao X, Wang Y, Zhang X, Chen X, Xu C, et al. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFa. Cell Stem Cell 2012; 11: 812-824
38. Szabó C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 2007; 6: 662-680
39. Walford GA, Moussignac R-L, Scribner AW, Loscalzo J, Leopold JA. Hypoxia potentiates nitric oxide-mediated apoptosis in endothelial cells via peroxynitrite-induced activation of mitochondria-dependent and -independent pathways. J Biol Chem 2004; 279: 4425-4432
40. Zhuang S, Simon G. Peroxynitrite-induced apoptosis involves activation of multiple caspases in HL-60 cells. Am J Physiol Cell Physiol 2000; 279: C341-C351
41. Shacka JJ, Sahawneh MA, Gonzalez JD, Ye Y-Z, D'Alessandro TL, Estévez AG. Two distinct signaling pathways regulate peroxynitrite-induced apoptosis in PC12 cells. Cell Death Differ 2006; 13: 1506-1514
42. Wu Y, Wang D, Wang X, Wang Y, Ren F, Chang D, et al. Caspase 3 is activated through caspase 8 instead of caspase 9 during H2O2-induced apoptosis in HeLa cells. Cell Physiol Biochem 2011; 27: 539-546
43. Fridlender ZG, Albelda SM. Tumor-associated neutrophils: friend or foe? Carcinogenesis 2012; 33: 949-955
44. Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin J-P, et al. Membraneassociated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010; 120: 457-471
45. Yang W-C, Ma G, Chen S-H, Pan P-Y. Polarization and reprogramming of myeloid-derived suppressor cells. J Mol Cell Biol 2013; 5: 207-209
46. Quail DF, Joyce JA.Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19: 1423-1437
47. Yu L, Wang L, Chen S. Dual character of Toll-like receptor signaling: pro-tumorigenic effects and anti-tumor functions. Biochim Biophys Acta 2013; 1835: 144-154
48. Bunt SK, Clements VK, Hanson EM, Sinha P, Ostrand-Rosenberg S. Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol 2009; 85: 996-1004
49. Maruyama A, Shime H, Takeda Y, Azuma M, Matsumoto M, Seya T. Pam2 lipopeptides systemically increase myeloid-derived suppressor cells through TLR2 signaling. Biochem Biophys Res Commun 2015; 457: 445-450
50. Hooper DC, Spitsin S, Kean RB, Champion JM, Dickson GM, Chaudhry I, et al. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc Natl Acad Sci USA 1998; 95: 675-680
51. Balavoine GG, Geletii YV. Peroxynitrite scavenging by different antioxidants. Part I: convenient assay. Nitric Oxide 1999; 3: 40-54
52. Hooper DC, Scott GS, Zborek A, Mikheeva T, Kean RB, Koprowski H, et al. Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes and tissue damage in a mouse model of multiple sclerosis. FASEB J 2000; 14: 691-698
53. Moore TC, Petro TM. IRF3 and ERK MAP-kinases control nitric oxide production from macrophages in response to poly-I: C. FEBS Lett 2013; 587: 3014-3020
54. Yang C-S, Kim J-J, Lee SJ, Hwang JH, Lee C-H, Lee M-S, et al. TLR3-triggered reactive oxygen species contribute to inflammatory responses by activating signal transducer and activator of transcription-1. J Immunol 2013; 190: 6368-6377
55. Zhang W, Kuncewicz T, Yu ZY, Zou L, Xu X, Kone BC. Protein-protein interactions involving inducible nitric oxide synthase. Acta Physiol Scand 2003; 179: 137-142
56. Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 2013; 501: 346-354
57. Oshiumi H, Okamoto M, Fujii K, Kawanishi T, Matsumoto M, Koike S, et al. The TLR3/TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection. J Immunol 2011; 187: 5320-5327
58. Tanaka H, Mori Y, Ishii H, Akedo H. Enhancement of metastatic capacity of fibroblast-tumor cell interaction in mice. Cancer Res 1988; 48: 1456-1459