1,788
Views
8
CrossRef citations to date
0
Altmetric
Research Article

IL-17 suppresses the therapeutic activity of cancer vaccines through the inhibition of CD8+ T-cell responses

, , , ORCID Icon, , , , & ORCID Icon show all
Article: 1758606 | Received 31 Jan 2020, Accepted 07 Apr 2020, Published online: 12 May 2020

References

  • Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages 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;313:1960–14. doi:10.1126/science.1129139.
  • Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman W-H, Pagès F, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011;71(4):1263–1271. doi:10.1158/0008-5472.CAN-10-2907.
  • Zhang JP, Yan J, Xu J, Pang XH, Chen MS, Li L, Wu C, Li S-P, Zheng L. Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol. 2009;50:980–989. doi:10.1016/j.jhep.2008.12.033.
  • Conti HR, Shen F, Nayyar N, Stocum E, Sun JN, Lindemann MJ, Ho AW, Hai JH, Yu JJ, Jung JW, et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med. 2009;206:299–311. doi:10.1084/jem.20081463.
  • Abadja F, Sarraj B, Ansari MJ. Significance of T helper 17 immunity in transplantation. Curr Opin Organ Transplant. 2012;17:8–14. doi:10.1097/MOT.0b013e32834ef4e4.
  • Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, et al. Differential roles of interleukin-17A and −17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity. 2009;30(1):108–119. doi:10.1016/j.immuni.2008.11.009.
  • Veldhoen M. Th17 cells require you to chew before you swallow. Immunity. 2017;46:8–10. doi:10.1016/j.immuni.2016.12.016.
  • Tartour E, Fossiez F, Joyeux I, Galinha A, Gey A, Claret E, Sastre-Garau X, Couturier J, Mosseri V, Vives V, et al. Interleukin 17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice. Cancer Res. 1999;59:3698–3704.
  • Numasaki M, Fukushi J, Ono M, Narula SK, Zavodny PJ, Kudo T, Robbins PD, Tahara H, Lotze MT. Interleukin-17 promotes angiogenesis and tumor growth. Blood. 2003;101:2620–2627. doi:10.1182/blood-2002-05-1461.
  • Chung AS, Wu X, Zhuang G, Ngu H, Kasman I, Zhang J, Vernes J-M, Jiang Z, Meng YG, Peale FV, et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat Med. 2013;19:1114–1123. doi:10.1038/nm.3291.
  • Wang L, Yi T, Zhang W, Pardoll DM, Yu H. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 2010;70(24):10112–10120. doi:10.1158/0008-5472.CAN-10-0775.
  • Hayata K, Iwahashi M, Ojima T, Katsuda M, Iida T, Nakamori M, Ueda K, Nakamura M, Miyazawa M, Tsuji T, et al. Inhibition of IL-17A in tumor microenvironment augments cytotoxicity of tumor-infiltrating lymphocytes in tumor-bearing mice. PLoS One. 2013;8(1):e53131. doi:10.1371/journal.pone.0053131.
  • He D, Li H, Yusuf N, Elmets CA, Li J, Mountz JD, Xu H. IL-17 promotes tumor development through the induction of tumor promoting microenvironments at tumor sites and myeloid-derived suppressor cells. J Immunol. 2010;184(5):2281–2288. doi:10.4049/jimmunol.0902574.
  • Zou W, Restifo NP. T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol. 2010;10:248–256. doi:10.1038/nri2742.
  • Benchetrit F, Ciree A, Vives V, Warnier G, Gey A, Sautes-Fridman C, Fossiez F, Haicheur N, Fridman WH, Tartour E. Interleukin-17 inhibits tumor cell growth by means of a T-cell-dependent mechanism. Blood. 2002;99:2114–2121. doi:10.1182/blood.V99.6.2114.
  • Hirahara N, Nio Y, Sasaki S, Minari Y, Takamura M, Iguchi C, Dong M, Yamasawa K, Tamura K. Inoculation of human interleukin-17 gene-transfected Meth-A fibrosarcoma cells induces T cell-dependent tumor-specific immunity in mice. Oncology. 2001;61(1):79–89. doi:10.1159/000055357.
  • Gnerlich JL, Mitchem JB, Weir JS, Sankpal NV, Kashiwagi H, Belt BA, Porembka MR, Herndon JM, Eberlein TJ, Goedegebuure P, et al. Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J Immunol. 2010;185(7):4063–4071. doi:10.4049/jimmunol.0902609.
  • Kryczek I, Wei S, Szeliga W, Vatan L, Zou W. Endogenous IL-17 contributes to reduced tumor growth and metastasis. Blood. 2009;114:357–359. doi:10.1182/blood-2008-09-177360.
  • Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S, Hwu P, Restifo NP, Overwijk WW, Dong C. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity. 2009;31(5):787–798. doi:10.1016/j.immuni.2009.09.014.
  • Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, Paulos CM, Palmer DC, Touloukian CE, Ptak K, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood. 2008;112(2):362–373. doi:10.1182/blood-2007-11-120998.
  • Higashi T, Takagi R, Hashimoto K, Matsushita S. Curdlan induces dendritic cell-mediated Th17 polarisation via jagged1 activation in human dendritic cells. Allergy. 2010;65:339.
  • Mori A, Oleszycka E, Sharp FA, Coleman M, Ozasa Y, Singh M, O’Hagan DT, Tajber L, Corrigan OI, McNeela EA, et al. The vaccine adjuvant alum inhibits IL-12 by promoting PI3 kinase signaling while chitosan does not inhibit IL-12 and enhances Th1 and Th17 responses. Eur J Immunol. 2012;42(10):2709–2719. doi:10.1002/eji.201242372.
  • Werninghaus K, Babiak A, Gross O, Holscher C, Dietrich H, Agger EM, Mages J, Mocsai A, Schoenen H, Finger K. Adjuvanticity of a synthetic cord factor analogue for subunit Mycobacterium tuberculosis vaccination requires FcRgamma-Syk-Card9-dependent innate immune activation. J Exp Med. 2009;206:89–97. doi:10.1084/jem.20081445.
  • Gasse P, Riteau N, Vacher R, Michel ML, Fautrel A, Di Padova F, Fick L, Charron S, Lagente V, Eberl G, et al. IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis. PLoS One. 2011;6. doi:10.1371/journal.pone.0023185.
  • Preville X, Ladant D, Timmerman B, Leclerc C. Eradication of established tumors by vaccination with recombinant Bordetella pertussis adenylate cyclase carrying the human papillomavirus 16 E7 oncoprotein. Cancer Res. 2005;65:641–649.
  • Lin KY, Guarnieri FG, Staveley-O’Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res. 1996;56:21–26.
  • Schoenen H, Bodendorfer B, Hitchens K, Manzanero S, Werninghaus K, Nimmerjahn F, Agger EM, Stenger S, Andersen P, Ruland J, et al. Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol. 2010;184:2756–2760. doi:10.4049/jimmunol.0904013.
  • Kim HS, Park KH, Lee HK, Kim JS, Kim YG, Lee JH, Kim KH, Yun J, Hwang BY, Hong JT, et al. Curdlan activates dendritic cells through dectin-1 and toll-like receptor 4 signaling. Int Immunopharmacol. 2016;39:71–78. doi:10.1016/j.intimp.2016.07.013.
  • Schlecht G, Loucka J, Najar H, Sebo P, Leclerc C. Antigen targeting to CD11b allows efficient presentation of CD4+ and CD8+ T cell epitopes and in vivo Th1-polarized T cell priming. J Immunol. 2004;173:6089–6097. doi:10.4049/jimmunol.173.10.6089.
  • Ma SB, Cheng Q, Cai YF, Gong HL, Wu Y, Yu X, Shi L, Wu D, Dong C, Liu H. IL-17A produced by gamma delta T cells promotes tumor growth in hepatocellular carcinoma. Cancer Res. 2014;74:1969–1982. doi:10.1158/0008-5472.CAN-13-2534.
  • Fabre J, Giustiniani J, Garbar C, Antonicelli F, Merrouche Y, Bensussan A, Bagot M,  Al-Dacak R. Targeting the tumor microenvironment: the protumor effects of IL-17 related to cancer type. Int J Mol Sci. 2016;17:E1433.
  • Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol. 2009;39:216–224. doi:10.1002/eji.200838475.
  • Hamai A, Pignon P, Raimbaud I, Duperrier-Amouriaux K, Senellart H, Hiret S, Douillard J-Y, Bennouna J, Ayyoub M, Valmori D. Human T(H)17 immune cells specific for the tumor antigen MAGE-A3 convert to IFN-gamma-secreting cells as they differentiate into effector T cells in vivo. Cancer Res. 2012;72:1059–1063. doi:10.1158/0008-5472.CAN-11-3432.
  • Gagliani N, Vesely MCA, Iseppon A, Brockmann L, Xu H, Palm NW, de Zoete MR, Licona-Limón P, Paiva RS, Ching T, et al. TH17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature. 2015;523:221–225. doi:10.1038/nature14452.
  • Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol. 2008;83:64–70. doi:10.1189/jlb.0407247.
  • Ng LG, Ostuni R, Hidalgo A. Heterogeneity of neutrophils. Nat Rev Immunol. 2019;19:255–265. doi:10.1038/s41577-019-0141-8.
  • Schwarzenberger P, Huang WT, Ye P, Oliver P, Manuel M, Zhang ZL, Bagby G, Nelson S, Kolls JK. Requirement of endogenous stem cell factor and granulocyte-colony-stimulating factor for IL-17-mediated granulopoiesis. J Immunol. 2000;164(9):4783–4789. doi:10.4049/jimmunol.164.9.4783.
  • Wu P, Wu D, Ni C, Ye J, Chen W, Hu G, Wang Z, Wang C, Zhang Z, Xia W, et al. gamma delta T17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity. 2014;40:785–800. doi:10.1016/j.immuni.2014.03.013.
  • Gabrilovich DI. Myeloid-derived suppressor cells. Cancer Immunol Res. 2017;5:3–8. doi:10.1158/2326-6066.CIR-16-0297.
  • Zhou J, Nefedova Y, Lei AH, Gabrilovich D. Neutrophils and PMN-MDSC: their biological role and interaction with stromal cells. Semin Immunol. 2018;35:19–28. doi:10.1016/j.smim.2017.12.004.
  • Coffelt SB, Kersten K, Doornebal CW, Weiden J, Vrijland K, Hau CS, Verstegen NJM, Ciampricotti M, Hawinkels LJAC, Jonkers J, et al. IL-17-producing gamma delta T cells and neutrophils conspire to promote breast cancer metastasis. Nature. 2015;522:345–348. doi:10.1038/nature14282.
  • Vono M, Lin A, Norrby-Teglund A, Koup RA, Liang F, Lore K. Neutrophils acquire the capacity for antigen presentation to memory CD4(+) T cells in vitro and ex vivo. Blood. 2017;129:1991–2001. doi:10.1182/blood-2016-10-744441.
  • Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPM, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079–1084. doi:10.1126/science.aad1329.
  • Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, Clement O, Marcheteau E, Gey A, Fraisse G, et al. Mucosal imprinting of vaccine-induced CD8(+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med. 2013;5:172ra20.
  • Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–498. doi:10.1016/j.cell.2009.09.033.
  • Goto Y, Panea C, Nakato G, Cebula A, Lee C, Diez MG, Laufer T, Ignatowicz L, Ivanov I. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity. 2014;40(4):594–607. doi:10.1016/j.immuni.2014.03.005.
  • Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by gamma delta T cells rather than CD4 T cells during mycobacterium tuberculosis infection. J Immunol. 2006;177:4662–4669. doi:10.4049/jimmunol.177.7.4662.
  • Flannigan KL, Ngo VL, Geem D, Harusato A, Hirota SA, Parkos CA, Lukacs NW, Nusrat A, Gaboriau-Routhiau V, Cerf-Bensussan N, et al. IL-17A-mediated neutrophil recruitment limits expansion of segmented filamentous bacteria. Mucosal Immunol. 2017;10:673–684. doi:10.1038/mi.2016.80.
  • Reppert S, Boross I, Koslowski M, Tureci O, Koch S, Lehr HA, Finotto S. A role for T-bet-mediated tumour immune surveillance in anti-IL-17A treatment of lung cancer. Nat Commun. 2011;2:600.
  • Ma YF, Chen C, Li DQ, Liu M, Lv ZW, Ji YH, Xu J. Targeting of interleukin (IL)-17A inhibits PDL1 expression in tumor cells and induces anticancer immunity in an estrogen receptor-negative murine model of breast cancer. Oncotarget. 2017;8:7614–7624. doi:10.18632/oncotarget.13819.