Myeloid-derived suppressor cells confer tumor-suppressive functions on natural killer cells via polyinosinic:polycytidylic acid treatment in mouse tumor models

Journal of Innate Immunity

Volumn 6, Issue 3, 2014, Pages 293-305

  Shime, Hiroaki ^a   Kojima, Ayako ^a   Maruyama, Akira ^a   Saito, Yusuke ^a   Oshiumi, Hiroyuki ^a   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Double stranded RNA; Mitochondrial antiviral signaling protein; Myeloid derived suppressor cells; Tumor immunotherapy

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; CD69 ANTIGEN; GAMMA INTERFERON; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; MONOCLONAL ANTIBODY; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG; CD11B ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 18; TOLL LIKE RECEPTOR 3; ALPHA BETA INTERFERON RECEPTOR; GROWTH INHIBITOR; IFNAR1 PROTEIN, MOUSE; IPS-1 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; C57BL 6 MOUSE; CANCER INHIBITION; CELL ACTIVATION; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IN VIVO STUDY; MELANOMA B16; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; TUMOR GROWTH; ANTIGEN EXPRESSION; ANTIPROLIFERATIVE ACTIVITY; BONE MARROW CELL; CANCER SIZE; CELL ISOLATION; CELL MATURATION; GENE EXPRESSION; LUNG CANCER; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MELANOMA; MYELOID DERIVED SUPPRESOR CELL; PROTEIN EXPRESSION; THYMOMA; TUMOR IMMUNITY; TUMOR MODEL; ADOPTIVE IMMUNOTHERAPY; ANIMAL; C57BL MOUSE; CELL COMMUNICATION; CELL GROWTH; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; SKIN NEOPLASMS; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL COMMUNICATION; CELL GROWTH PROCESSES; DISEASE MODELS, ANIMAL; GROWTH INHIBITORS; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; POLY I-C; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; UP-REGULATION;

EID: 84898597440     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000355126     Document Type: Article

References (40)

1. Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautès-Fridman C, et al: Trial watch: experimental Toll-like receptor agonists for cancer therapy. Oncoimmunol 2012; 1: 699-716.
2. Desmet CJ, Ishii KJ: Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 2012; 12: 479-491.
3. Seya T, Shime H, Ebihara T, Oshiumi H, Matsumoto M: Pattern recognition receptors of innate immunity and their application to tumor immunotherapy. Cancer Sci 2010; 101: 313-320.
4. 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.
5. Miyake T, Kumagai Y, Kato H, Guo Z, Matsushita K, Satoh T, et al: Poly I:C-induced activation of NK cells by CD8 alpha+ dendritic cells via the IPS-1 and TRIF-dependent pathways. J Immunol 2009; 183: 2522-2528.
6. Salem ML, El-Naggar SA, Kadima A, Gillanders WE, Cole DJ: The adjuvant effects of the Toll-like receptor 3 ligand polyinosinic-cytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 2006; 24: 5119-5132.
7. 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.
8. Azuma M, Ebihara T, Oshiumi H, Matsumoto M, Seya T: Cross-priming for antitumor CTL induced by soluble Ag + poly I:C depends on the TICAM-1 pathway in mouse CD11c+/CD8?+ dendritic cells. Oncoimmunol 2012; 1: 581-592.
9. Gauzzi MC, Del Corno M, Gessani S: Dissecting TLR3 signalling in dendritic cells. Immunobiology 2010; 215: 713-723.
10. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T: TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nat Immunol 2003; 4: 161-167.
11. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, et al: Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 2003; 301: 640-643.
12. Seth RB, Sun L, Ea C-K, Chen ZJ: Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-?B and IRF3. Cell 2005; 122: 669-682.
13. Honda K, Takaoka A, Taniguchi T: Type I inteferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 2006; 25: 349-360.
14. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, Yamamoto M, et al: Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 2004; 5: 1061-1068.
15. Seya T, Kasamatsu J, Azuma M, Shime H, Matsumoto M: Natural killer cell activation secondary to innate pattern sensing. J Innate Immun 2011; 3: 264-273.
16. Zamai L, Ponti C, Mirandola P, Gobbi G, Papa S, Galeotti L, et al: NK cells and cancer. J Immunol 2007; 178: 4011-4016.
17. Takeda K, Nakayama M, Sakaki M, Hayakawa Y, Imawari M, Ogasawara K, et al: IFN-γ production by lung NK cells is critical for the natural resistance to pulmonary metastasis of B16 melanoma in mice. J Leukoc Biol 2011; 90: 777-785.
18. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S: Functions of natural killer cells. Nat Immunol 2008; 9: 503-510.
19. Hayakawa Y, Takeda K, Yagita H, Smyth MJ, Van Kaer L, Okumura K, et al: IFN-?-mediated inhibition of tumor angiogenesis by natural killer T-cell ligand, ?-galactosylceramide. Blood 2002; 100: 1728-1733.
20. Kakuta S, Tagawa Y-I, Shibata S, Nanno M, Iwakura Y: Inhibition of B16 melanoma experimental metastasis by interferon-gamma through direct inhibition of cell proliferation and activation of antitumour host mechanisms. Immunology 2002; 105: 92-100.
21. Newman K, Riley E: Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat Rev Immunol 2007; 7: 279-291.
22. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V: Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12: 253-268.
23. Ostrand-Rosenberg S, Sinha P: Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009; 182: 4499-4506.
24. Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, et al: Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci USA 2012; 109: 2491-2496.
25. Ostrand-Rosenberg S: Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 2010; 59: 1593-1600.
26. Li H, Han Y, Guo Q, Zhang M, Cao X: Cancer- expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane- bound TGF-β1. J Immunol 2009; 182: 240-249.
27. Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, et al: Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009; 50: 799-807.
28. Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, et al: Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor- bearing host. Blood 2007; 109: 4336-4342.
29. Nausch N, Galani IE, Schlecker E, Cerwenka A: Mononuclear myeloid-derived 'suppressor' cells express RAE-1 and activate natural killer cells. Blood 2008; 112: 4080-4089.
30. 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.
31. 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.
32. Ebihara T, Azuma M, Oshiumi H, Kasamatsu J, Iwabuchi K, Matsumoto K, et al: Identification of a poly(I:C)-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 2010; 207: 2675-2687.
33. 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.
34. Takeda K, Oshima H, Hayakawa Y, Akiba H, Atsuta M, Kobata T, et al: CD27-mediated activation of murine NK cells. J Immunol 2000; 164: 1741-1745.
35. Chan CJ, Andrews DM, Mclaughlin NM, Yagita H, Gilfillan S, Colonna M, et al: DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases. J Immunol 2010; 184: 902-911.
36. Navabi H, Jasani B, Reece A, Clayton A, Tabi Z, Donninger C, et al: A clinical grade poly I:C-analogue (Ampligen) promotes optimal DC maturation and Th1-type T cell responses of healthy donors and cancer patients in vitro. Vaccine 2009; 27: 107-115.
37. 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.
38. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, et al: Innate lymphoid cells - a proposal for uniform nomenclature. Nat Rev Immunol 2013; 13: 145-149.
39. Arany I, Fleischmann CM, Tyring SK, Fleischmann WR: Interferon regulates expression of mda-6/WAF1/CIP1 and cyclin-dependent kinases independently from p53 in B16 murine melanoma cells. Biochem Biophys Res Commun 1997; 233: 678-680.
40. Ugel S, Delpozzo F, Desantis G, Papalini F, Simonato F, Sonda N, et al: Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol 2009; 9: 470-481.