IL-36γ Transforms the Tumor Microenvironment and Promotes Type 1 Lymphocyte-Mediated Antitumor Immune Responses

Cancer Cell

Volumn 28, Issue 3, 2015, Pages 296-306

  Wang, Xuefeng ^a,b   Zhao, Xin ^a,g   Feng, Chao ^b   Weinstein, Aliyah ^a   Xia, Rui ^a,b   Wen, Wen ^b   Lv, Quansheng ^b   Zuo, Shuting ^a,k   Tang, Peijun ⁱ   Yang, Xi ^a,h   Chen, Xiaojuan ^a,g   Wang, Hongrui ^e   Zang, Shayang ^a,b   Stollings, Lindsay ^f   Denning, Timothy L ^j   Jiang, Jingting ^d   Fan, Jie ^a,l   Zhang, Guangbo ^g   Zhang, Xueguang ^b   Zhu, Yibei ^b   Storkus, Walter ^a   Lu, Binfeng ^a,c   more..

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d THE THIRD AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^e XIAMEN UNIVERSITY   (China)

^f UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^g THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^h Tsinghua University   (China)

ⁱ The Affiliated Infectious Diseases Hospital of Soochow University   (China)

^j GEORGIA STATE UNIVERSITY   (United States)

^k THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^l VETERANS AFFAIRS MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 36GAMMA; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CANCER VACCINE; IL36G PROTEIN, HUMAN; INTERLEUKIN 1; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CANCER GROWTH; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENICITY; IMMUNOREGULATION; INFLAMMATION; INTERFERON PRODUCTION; LUNG CANCER; LYMPHOCYTE; MELANOMA; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; EXPERIMENTAL MELANOMA; IMMUNOLOGY; IMMUNOTHERAPY; LUNG TUMOR; NATURAL KILLER CELL; PROCEDURES; TUMOR CELL CULTURE;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-1; INTERLEUKIN-12; KILLER CELLS, NATURAL; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84942365848     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.07.014     Document Type: Article

References (38)

1. Ascierto P.A., Kalos M., Schaer D.A., Callahan M.K., Wolchok J.D. Biomarkers for immunostimulatory monoclonal antibodies in combination strategies for melanoma and other tumor types. Clin. Cancer Res. 2013, 19:1009-1020.
2. Bachmann M., Scheiermann P., Härdle L., Pfeilschifter J., Mühl H. IL-36γ/IL-1F9, an innate T-bet target in myeloid cells. J. Biol. Chem. 2012, 287:41684-41696.
3. Balkwill F., Montfort A., Capasso M. B regulatory cells in cancer. Trends Immunol. 2013, 34:169-173.
4. Blankenstein T., Coulie P.G., Gilboa E., Jaffee E.M. The determinants of tumour immunogenicity. Nat. Rev. Cancer 2012, 12:307-313.
5. Blumberg H., Dinh H., Trueblood E.S., Pretorius J., Kugler D., Weng N., Kanaly S.T., Towne J.E., Willis C.R., Kuechle M.K., et al. Opposing activities of two novel members of the IL-1 ligand family regulate skin inflammation. J. Exp. Med. 2007, 204:2603-2614.
6. Brahmer J.R., Tykodi S.S., Chow L.Q., Hwu W.J., Topalian S.L., Hwu P., Drake C.G., Camacho L.H., Kauh J., Odunsi K., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 2012, 366:2455-2465.
7. Chen L.J., Zheng X., Shen Y.P., Zhu Y.B., Li Q., Chen J., Xia R., Zhou S.M., Wu C.P., Zhang X.G., et al. Higher numbers of T-bet(+) intratumoral lymphoid cells correlate with better survival in gastric cancer. Cancer Immunol. Immunother. 2013, 62:553-561.
8. Chustz R.T., Nagarkar D.R., Poposki J.A., Favoreto S., Avila P.C., Schleimer R.P., Kato A. Regulation and function of the IL-1 family cytokine IL-1F9 in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 2011, 45:145-153.
9. Debets R., Timans J.C., Homey B., Zurawski S., Sana T.R., Lo S., Wagner J., Edwards G., Clifford T., Menon S., et al. Two novel IL-1 family members, IL-1 delta and IL-1 epsilon, function as an antagonist and agonist of NF-kappa B activation through the orphan IL-1 receptor-related protein 2. J. Immunol. 2001, 167:1440-1446.
10. Derer A., Groetsch B., Harre U., Böhm C., Towne J., Schett G., Frey S., Hueber A.J. Blockade of IL-36 receptor signaling does not prevent from TNF-induced arthritis. PLoS ONE 2014, 9:e101954.
11. Foster A.M., Baliwag J., Chen C.S., Guzman A.M., Stoll S.W., Gudjonsson J.E., Ward N.L., Johnston A. IL-36 promotes myeloid cell infiltration, activation, and inflammatory activity in skin. J. Immunol. 2014, 192:6053-6061.
12. Fourcade J., Sun Z., Benallaoua M., Guillaume P., Luescher I.F., Sander C., Kirkwood J.M., Kuchroo V., Zarour H.M. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 2010, 207:2175-2186.
13. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
14. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pagès C., Tosolini M., Camus M., Berger A., Wind P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-1964.
15. Gao X., Zhu Y., Li G., Huang H., Zhang G., Wang F., Sun J., Yang Q., Zhang X., Lu B. TIM-3 expression characterizes regulatory T cells in tumor tissues and is associated with lung cancer progression. PLoS ONE 2012, 7:e30676.
16. Gresnigt M.S., van de Veerdonk F.L. Biology of IL-36 cytokines and their role in disease. Semin. Immunol. 2013, 25:458-465.
17. Gresnigt M.S., Rösler B., Jacobs C.W., Becker K.L., Joosten L.A., van der Meer J.W., Netea M.G., Dinarello C.A., van de Veerdonk F.L. The IL-36 receptor pathway regulates Aspergillus fumigatus-induced Th1 and Th17 responses. Eur. J. Immunol. 2013, 43:416-426.
18. Guo Z.S., Liu Z., Bartlett D.L. Oncolytic Immunotherapy: Dying the Right Way is a Key to Eliciting Potent Antitumor Immunity. Front. Oncol. 2014, 4:74.
19. He Q., Chen H.X., Li W., Wu Y., Chen S.J., Yue Q., Xiao M., Li J.W. IL-36 cytokine expression and its relationship with p38 MAPK and NF-κB pathways in psoriasis vulgaris skin lesions. J. Huazhong Univ. Sci. Technolog. Med. Sci. 2013, 33:594-599.
20. Johnston A., Xing X., Guzman A.M., Riblett M., Loyd C.M., Ward N.L., Wohn C., Prens E.P., Wang F., Maier L.E., et al. IL-1F5, -F6, -F8, and -F9: a novel IL-1 family signaling system that is active in psoriasis and promotes keratinocyte antimicrobial peptide expression. J. Immunol. 2011, 186:2613-2622.
21. Kontermann R.E. Antibody-cytokine fusion proteins. Arch. Biochem. Biophys. 2012, 526:194-205.
22. Lewis J.D., Shearer M.H., Kennedy R.C., Bright R.K. Surrogate tumor antigen vaccination induces tumor-specific immunity and the rejection of spontaneous metastases. Cancer Res. 2005, 65:2938-2946.
23. Lian L.H., Milora K.A., Manupipatpong K.K., Jensen L.E. The double-stranded RNA analogue polyinosinic-polycytidylic acid induces keratinocyte pyroptosis and release of IL-36γ. J. Invest. Dermatol. 2012, 132:1346-1353.
24. Lu B., Chen L., Liu L., Zhu Y., Wu C., Jiang J., Zhang X. T-cell-mediated tumor immune surveillance and expression of B7 co-inhibitory molecules in cancers of the upper gastrointestinal tract. Immunol. Res. 2011, 50:269-275.
25. Mutamba S., Allison A., Mahida Y., Barrow P., Foster N. Expression of IL-1Rrp2 by human myelomonocytic cells is unique to DCs and facilitates DC maturation by IL-1F8 and IL-1F9. Eur. J. Immunol. 2012, 42:607-617.
26. Ngoi S.M., St Rose M.C., Menoret A.M., Smith D.E., Tovey M.G., Adler A.J., Vella A.T. Presensitizing with a Toll-like receptor 3 ligand impairs CD8 T-cell effector differentiation and IL-33 responsiveness. Proc. Natl. Acad. Sci. USA 2012, 109:10486-10491.
27. Overwijk W.W., Theoret M.R., Finkelstein S.E., Surman D.R., de Jong L.A., Vyth-Dreese F.A., Dellemijn T.A., Antony P.A., Spiess P.J., Palmer D.C., et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 2003, 198:569-580.
28. Pagès F., Berger A., Camus M., Sanchez-Cabo F., Costes A., Molidor R., Mlecnik B., Kirilovsky A., Nilsson M., Damotte D., et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 2005, 353:2654-2666.
29. Robinson D., Shibuya K., Mui A., Zonin F., Murphy E., Sana T., Hartley S.B., Menon S., Kastelein R., Bazan F., O'Garra A. IGIF does not drive Th1 development but synergizes with IL-12 for interferon-gamma production and activates IRAK and NFkappaB. Immunity 1997, 7:571-581.
30. Sakuishi K., Apetoh L., Sullivan J.M., Blazar B.R., Kuchroo V.K., Anderson A.C. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 2010, 207:2187-2194.
31. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 2012, 366:2443-2454.
32. Tortola L., Rosenwald E., Abel B., Blumberg H., Schäfer M., Coyle A.J., Renauld J.C., Werner S., Kisielow J., Kopf M. Psoriasiform dermatitis is driven by IL-36-mediated DC-keratinocyte crosstalk. J. Clin. Invest. 2012, 122:3965-3976.
33. Vigne S., Palmer G., Lamacchia C., Martin P., Talabot-Ayer D., Rodriguez E., Ronchi F., Sallusto F., Dinh H., Sims J.E., Gabay C. IL-36R ligands are potent regulators of dendritic and T cells. Blood 2011, 118:5813-5823.
34. Vigne S., Palmer G., Martin P., Lamacchia C., Strebel D., Rodriguez E., Olleros M.L., Vesin D., Garcia I., Ronchi F., et al. IL-36 signaling amplifies Th1 responses by enhancing proliferation and Th1 polarization of naive CD4+ T cells. Blood 2012, 120:3478-3487.
35. Vos J.B., van Sterkenburg M.A., Rabe K.F., Schalkwijk J., Hiemstra P.S., Datson N.A. Transcriptional response of bronchial epithelial cells to Pseudomonas aeruginosa: identification of early mediators of host defense. Physiol. Genomics 2005, 21:324-336.
36. Willimsky G., Czéh M., Loddenkemper C., Gellermann J., Schmidt K., Wust P., Stein H., Blankenstein T. Immunogenicity of premalignant lesions is the primary cause of general cytotoxic T lymphocyte unresponsiveness. J. Exp. Med. 2008, 205:1687-1700.
37. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., Segal N.H., Ariyan C.E., Gordon R.A., Reed K., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 2013, 369:122-133.
38. Yang Q., Li G., Zhu Y., Liu L., Chen E., Turnquist H., Zhang X., Finn O.J., Chen X., Lu B. IL-33 synergizes with TCR and IL-12 signaling to promote the effector function of CD8+ T cells. Eur. J. Immunol. 2011, 41:3351-3360.