IL-33 delays metastatic peritoneal cancer progression inducing an allergic microenvironment

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics. CA Cancer J Clin. 2018;68:7–30. doi:10.3322/caac.21442.
   PubMed Web of Science ®Google Scholar
• Maringe C, Walters S, Butler J, Coleman MP, Hacker N, Hanna L, Mosgaard BJ, Nordin A, Rosen B, Engholm G, et al. Stage at diagnosis and ovarian cancer survival: evidence from the International Cancer Benchmarking Partnership. Gynecol Oncol. 2012;127:75–82. doi:10.1016/j.ygyno.2012.06.033.
   PubMed Web of Science ®Google Scholar
• Armstrong DK, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, Copeland LJ, Walker JL, Burger RA, Gynecologic Oncology G. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med. 2006;354:34–43. doi:10.1056/NEJMoa052985.
   PubMed Web of Science ®Google Scholar
• Jaaback K, Johnson N, Lawrie TA. Intraperitoneal chemotherapy for the initial management of primary epithelial ovarian cancer. Cochrane Database Syst Rev. 2016;CD005340.
   PubMed Web of Science ®Google Scholar
• Pujade-Lauraine E, Guastalla JP, Colombo N, Devillier P, Francois E, Fumoleau P, Monnier A, Nooy M, Mignot L, Bugat R, et al. Intraperitoneal recombinant interferon gamma in ovarian cancer patients with residual disease at second-look laparotomy. J Clin Oncol. 1996;14:343–350. doi:10.1200/JCO.1996.14.2.343.
   PubMed Web of Science ®Google Scholar
• Edwards RP, Gooding W, Lembersky BC, Colonello K, Hammond R, Paradise C, Kowal CD, Kunschner AJ, Baldisseri M, Kirkwood JM, et al. Comparison of toxicity and survival following intraperitoneal recombinant interleukin-2 for persistent ovarian cancer after platinum: twenty-four-hour versus 7-day infusion. J Clin Oncol. 1997;15:3399–3407. doi:10.1200/JCO.1997.15.11.3399.
   PubMed Web of Science ®Google Scholar
• Berek JS, Markman M, Stonebraker B, Lentz SS, Adelson MD, DeGeest K, Moore D. Intraperitoneal interferon-alpha in residual ovarian carcinoma: a phase II gynecologic oncology group study. Gynecol Oncol. 1999;75:10–14. doi:10.1006/gyno.1999.5532.
   PubMed Web of Science ®Google Scholar
• Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 2005;23:479–490. doi:10.1016/j.immuni.2005.09.015.
   PubMed Web of Science ®Google Scholar
• Villarreal DO, Wise MC, Walters JN, Reuschel EL, Choi MJ, Obeng-Adjei N, Yan J, Morrow MP, Weiner DB. Alarmin IL-33 acts as an immunoadjuvant to enhance antigen-specific tumor immunity. Cancer Res. 2014;74:1789–1800. doi:10.1158/0008-5472.CAN-13-2729.
   PubMed Web of Science ®Google Scholar
• Dominguez D, Ye C, Geng Z, Chen S, Fan J, Qin L, Long A, Wang L, Zhang Z, Zhang Y, et al. Exogenous IL-33 Restores Dendritic Cell Activation and Maturation in Established Cancer. J Immunol. 2017;198:1365–1375. doi:10.4049/jimmunol.1501399.
   PubMed Web of Science ®Google Scholar
• Lu Z, Wang J, Wientjes MG, Au JL. Intraperitoneal therapy for peritoneal cancer. Future Oncol. 2010;6:1625–1641. doi:10.2217/fon.10.100.
   PubMed Web of Science ®Google Scholar
• Hinds DA, McMahon G, Kiefer AK, Do CB, Eriksson N, Evans DM, St Pourcain B, Ring SM, Mountain JL, Francke U, et al. A genome-wide association meta-analysis of self-reported allergy identifies shared and allergy-specific susceptibility loci. Nat Genet. 2013;45:907–911. doi:10.1038/ng.2686.
   PubMed Web of Science ®Google Scholar
• Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, von Mutius E, Farrall M, Lathrop M, Cookson W, et al. A large-scale, consortium-based genomewide association study of asthma. N Engl J Med. 2010;363:1211–1221. doi:10.1056/NEJMoa0906312.
   PubMed Web of Science ®Google Scholar
• Piehler D, Eschke M, Schulze B, Protschka M, Muller U, Grahnert A, Richter T, Heyen L, Kohler G, Brombacher F, et al. The IL-33 receptor (ST2) regulates early IL-13 production in fungus-induced allergic airway inflammation. Mucosal Immunol. 2016;9:937–949. doi:10.1038/mi.2015.106.
   PubMed Web of Science ®Google Scholar
• Savinko T, Karisola P, Lehtimaki S, Lappetelainen AM, Haapakoski R, Wolff H, Lauerma A, Alenius H. ST2 regulates allergic airway inflammation and T-cell polarization in epicutaneously sensitized mice. J Invest Dermatol. 2013;133:2522–2529. doi:10.1038/jid.2013.195.
   PubMed Web of Science ®Google Scholar
• Welch JS, Escoubet-Lozach L, Sykes DB, Liddiard K, Greaves DR, Glass CK. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J Biol Chem. 2002;277:42821–42829. doi:10.1074/jbc.M205873200.
   PubMed Web of Science ®Google Scholar
• Meisel C, Bonhagen K, Lohning M, Coyle AJ, Gutierrez-Ramos JC, Radbruch A, Kamradt T. Regulation and function of T1/ST2 expression on CD4+ T cells: induction of type 2 cytokine production by T1/ST2 cross-linking. J Immunol. 2001;166:3143–3150.
   PubMed Web of Science ®Google Scholar
• Ngoc PL, Gold DR, Tzianabos AO, Weiss ST, Celedon JC. Cytokines, allergy, and asthma. Curr Opin Allergy Clin Immunol. 2005;5:161–166.
   PubMed Web of Science ®Google Scholar
• Till S, Durham S, Dickason R, Huston D, Bungre J, Walker S, Robinson D, Kay AB, Corrigan C. IL-13 production by allergen-stimulated T cells is increased in allergic disease and associated with IL-5 but not IFN-gamma expression. Immunology. 1997;91:53–57.
   PubMed Web of Science ®Google Scholar
• Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol. 2008;180:5771–5777.
   PubMed Web of Science ®Google Scholar
• Judd LM, Heine RG, Menheniott TR, Buzzelli J, O'Brien-Simpson N, Pavlic D, O'Connor L, Al Gazali K, Hamilton O, Scurr M, et al. Elevated IL-33 expression is associated with pediatric eosinophilic esophagitis, and exogenous IL-33 promotes eosinophilic esophagitis development in mice. Am J Physiol Gastrointest Liver Physiol. 2016;310:G13–25. doi:10.1152/ajpgi.00290.2015.
   PubMed Web of Science ®Google Scholar
• Melichar B, Freedman RS. Immunology of the peritoneal cavity: relevance for host-tumor relation. Int J Gynecol Cancer. 2002;12:3–17.
   PubMed Web of Science ®Google Scholar
• Jiang Z, Zhu L. Update on the role of alternatively activated macrophages in asthma. J Asthma Allergy. 2016;9:101–107. doi:10.2147/JAA.S104508.
   PubMed Web of Science ®Google Scholar
• Byers DE, Holtzman MJ. Alternatively activated macrophages and airway disease. Chest. 2011;140:768–774. doi:10.1378/chest.10-2132.
   PubMed Web of Science ®Google Scholar
• Kurowska-Stolarska M, Stolarski B, Kewin P, Murphy G, Corrigan CJ, Ying S, Pitman N, Mirchandani A, Rana B, van Rooijen N, et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol. 2009;183:6469–6477. doi:10.4049/jimmunol.0901575.
   PubMed Web of Science ®Google Scholar
• Balbo P, Silvestri M, Rossi GA, Crimi E, Burastero SE. Differential role of CD80 and CD86 on alveolar macrophages in the presentation of allergen to T lymphocytes in asthma. Clin Exp Allergy. 2001;31:625–636.
   PubMed Web of Science ®Google Scholar
• Martin NT, Martin MU. Interleukin 33 is a guardian of barriers and a local alarmin. Nat Immunol. 2016;17:122–131. doi:10.1038/ni.3370.
   PubMed Web of Science ®Google Scholar
• Roy A, Ganesh G, Sippola H, Bolin S, Sawesi O, Dagalv A, Schlenner SM, Feyerabend T, Rodewald HR, Kjellen L, et al. Mast cell chymase degrades the alarmins heat shock protein 70, biglycan, HMGB1, and interleukin-33 (IL-33) and limits danger-induced inflammation. J Biol Chem. 2014;289:237–250. doi:10.1074/jbc.M112.435156.
   PubMed Web of Science ®Google Scholar
• Cohen ES, Scott IC, Majithiya JB, Rapley L, Kemp BP, England E, Rees DG, Overed-Sayer CL, Woods J, Bond NJ, et al. Oxidation of the alarmin IL-33 regulates ST2-dependent inflammation. Nat Commun. 2015;6:8327. doi:10.1038/ncomms9327.
   PubMed Web of Science ®Google Scholar
• Bessa J, Meyer CA, de Vera Mudry MC, Schlicht S, Smith SH, Iglesias A, Cote-Sierra J. Altered subcellular localization of IL-33 leads to non-resolving lethal inflammation. J Autoimmun. 2014;55:33–41. doi:10.1016/j.jaut.2014.02.012.
   PubMed Web of Science ®Google Scholar
• Nabe T, Wakamori H, Yano C, Nishiguchi A, Yuasa R, Kido H, Tomiyama Y, Tomoda A, Kida H, Takiguchi A, et al. Production of interleukin (IL)-33 in the lungs during multiple antigen challenge-induced airway inflammation in mice, and its modulation by a glucocorticoid. Eur J Pharmacol. 2015;757:34–41. doi:10.1016/j.ejphar.2015.03.015.
   PubMed Web of Science ®Google Scholar
• Prefontaine D, Nadigel J, Chouiali F, Audusseau S, Semlali A, Chakir J, Martin JG, Hamid Q. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol. 2010;125:752–754. doi:10.1016/j.jaci.2009.12.935.
   PubMed Web of Science ®Google Scholar
• Bahrami Mahneh S, Movahedi M, Aryan Z, Bahar MA, Rezaei A, Sadr M, Rezaei N, Universal Scientific E, Research N. Serum IL-33 Is Elevated in Children with Asthma and Is Associated with Disease Severity. Int Arch Allergy Immunol. 2015;168:193–196. doi:10.1159/000442413.
   PubMed Web of Science ®Google Scholar
• Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer. 2005;5:263–274. doi:10.1038/nrc1586.
   PubMed Web of Science ®Google Scholar
• Scarlett UK, Cubillos-Ruiz JR, Nesbeth YC, Martinez DG, Engle X, Gewirtz AT, Ahonen CL, Conejo-Garcia JR. In situ stimulation of CD40 and Toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res. 2009;69:7329–7337. doi:10.1158/0008-5472.CAN-09-0835.
   PubMed Web of Science ®Google Scholar
• Scarlett UK, Rutkowski MR, Rauwerdink AM, Fields J, Escovar-Fadul X, Baird J, Cubillos-Ruiz JR, Jacobs AC, Gonzalez JL, Weaver J, et al. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J Exp Med. 2012;209:495–506. doi:10.1084/jem.20111413.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Zha Y, Gajewski TF. Molecular regulation of T-cell anergy. EMBO Rep. 2008;9:50–55. doi:10.1038/sj.embor.7401138.
   PubMed Web of Science ®Google Scholar
• Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12:492–499.
   PubMed Web of Science ®Google Scholar
• Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell. 2014;159:1312–1326. doi:10.1016/j.cell.2014.11.018.
   PubMed Web of Science ®Google Scholar
• Lavin Y, Mortha A, Rahman A, Merad M. Regulation of macrophage development and function in peripheral tissues. Nat Rev Immunol. 2015;15:731–744. doi:10.1038/nri3920.
   PubMed Web of Science ®Google Scholar
• Joshi AD, Oak SR, Hartigan AJ, Finn WG, Kunkel SL, Duffy KE, Das A, Hogaboam CM, et al. Interleukin-33 contributes to both M1 and M2 chemokine marker expression in human macrophages. BMC Immunol. 2010;11:52. doi:10.1186/1471-2172-11-52.
   PubMed Web of Science ®Google Scholar
• He R, Yin H, Yuan B, Liu T, Luo L, Huang P, Dai L, Zeng K. IL-33 improves wound healing through enhanced M2 macrophage polarization in diabetic mice. Mol Immunol. 2017;90:42–49. doi:10.1016/j.molimm.2017.06.249.
   PubMed Web of Science ®Google Scholar
• Lee JS, Seppanen E, Patel J, Rodero MP, Khosrotehrani K. ST2 receptor invalidation maintains wound inflammation, delays healing and increases fibrosis. Exp Dermatol. 2016;25:71–74. doi:10.1111/exd.12833.
   PubMed Web of Science ®Google Scholar
• Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp LL, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science. 2011;331:1612–1616. doi:10.1126/science.1198443.
   PubMed Web of Science ®Google Scholar
• Wu L, Deng Z, Peng Y, Han L, Liu J, Wang L, Li B, Zhao J, Jiao S, Wei H. Ascites-derived IL-6 and IL-10 synergistically expand CD14(+)HLA-DR(-/low) myeloid-derived suppressor cells in ovarian cancer patients. Oncotarget. 2017;8:76843–76856. doi:10.18632/oncotarget.20164.
   PubMedGoogle Scholar
• Loercher AE, Nash MA, Kavanagh JJ, Platsoucas CD, Freedman RS. Identification of an IL-10-producing HLA-DR-negative monocyte subset in the malignant ascites of patients with ovarian carcinoma that inhibits cytokine protein expression and proliferation of autologous T cells. J Immunol. 1999;163:6251–6260.
   PubMed Web of Science ®Google Scholar
• Biswas SK, Gangi L, Paul S, Schioppa T, Saccani A, Sironi M, Bottazzi B, Doni A, Vincenzo B, Pasqualini F, et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood. 2006;107:2112–2122. doi:10.1182/blood-2005-01-0428.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Koma MK. Interleukin-33 Triggers B1 Cell Expansion and Its Release of Monocyte/Macrophage Chemoattractants and Growth Factors. Scand J Immunol. 2015;82:118–124. doi:10.1111/sji.12312.
   PubMed Web of Science ®Google Scholar
• Komai-Koma M, Gilchrist DS, McKenzie AN, Goodyear CS, Xu D, Fy L. IL-33 activates B1 cells and exacerbates contact sensitivity. J Immunol. 2011;186:2584–2591. doi:10.4049/jimmunol.1002103.
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Yanaba K, Tedder TF. B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J Immunol. 2010;184:4006–4016. doi:10.4049/jimmunol.0903009.
   PubMed Web of Science ®Google Scholar
• Dai M, Wei H, Yip YY, Feng Q, He K, Popov V, Hellstrom I, Hellstrom KE. Long-lasting complete regression of established mouse tumors by counteracting Th2 inflammation. J Immunother. 2013;36:248–257. doi:10.1097/CJI.0b013e3182943549.
   PubMed Web of Science ®Google Scholar
• Conejo-Garcia JR, Benencia F, Courreges MC, Kang E, Mohamed-Hadley A, Buckanovich RJ, Holtz DO, Jenkins A, Na H, Zhang L, et al. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat Med. 2004;10:950–958. doi:10.1038/nm1097.
   PubMed Web of Science ®Google Scholar
• Perales-Puchalt A, Svoronos N, Rutkowski MR, Allegrezza MJ, Tesone AJ, Payne KK, Wickramasinghe J, Nguyen JM, O’Brien SW, Gumireddy K, et al. Follicle-Stimulating Hormone Receptor Is Expressed by Most Ovarian Cancer Subtypes and Is a Safe and Effective Immunotherapeutic Target. Clin Cancer Res. 2015;521:99–104.
   Google Scholar
• Carmi Y, Spitzer MH, Linde IL, Burt BM, Prestwood TR, Perlman N, Davidson MG, Kenkel JA, Segal E, Pusapati GV, et al. Allogeneic IgG combined with dendritic cell stimuli induce antitumour T-cell immunity. Nature. 2015;521:99–104. doi:10.1038/nature14424.
   PubMed Web of Science ®Google Scholar