Combination immune checkpoint blockade as an effective therapy for mesothelioma

References

• Robinson BW, Musk AW, Lake RA Malignant mesothelioma. Lancet 2005; 366:397–408. doi:10.1016/S0140-6736(05)67025-0
   PubMed Web of Science ®Google Scholar
• Vogelzang NJ, Rusthoven JJ, Symanowski J, Denham C, Kaukel E, Ruffie P, et al. Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncol 2003; 21:2636–2644. doi:10.1200/JCO.2003.11.136
   PubMed Web of Science ®Google Scholar
• Alley EW, Lopez J, Santoro A, Morosky A, Saraf S, Piperdi B, et al. Clinical safety and activity of pembrolizumab in patients with malignant pleural mesothelioma (KEYNOTE-028): preliminary results from a non-randomised, open-label, phase 1b trial. Lancet Oncol 2017; 18:623–630. doi:10.1016/S1470-2045(17)30169-9
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015; 372:320–330. doi:10.1056/NEJMoa1412082
   PubMed Web of Science ®Google Scholar
• Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711–723. doi:10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443–2454. doi:10.1056/NEJMoa1200690
   PubMed Web of Science ®Google Scholar
• Yamada N, Oizumi S, Kikuchi E, Shinagawa N, Konishi-Sakakibara J, Ishimine A, et al. CD8+ tumor-infiltrating lymphocytes predict favorable prognosis in malignant pleural mesothelioma after resection. Cancer Immunol Immunother 2010; 59:1543–1549. doi:10.1007/s00262-010-0881-6
   PubMed Web of Science ®Google Scholar
• Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci U S A 2002; 99:12293–12297. doi:10.1073/pnas.192461099
   PubMed Web of Science ®Google Scholar
• Hegmans JP, Hemmes A, Hammad H, Boon L, Hoogsteden HC, Lambrecht BN Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur Respir J 2006; 27:1086–1095. doi:10.1183/09031936.06.00135305
   PubMed Web of Science ®Google Scholar
• Krummel MF, Allison JP CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995; 182:459–465.
   PubMed Web of Science ®Google Scholar
• Krummel MF, Allison JP CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J Exp Med 1996; 183:2533–2540.
   PubMed Web of Science ®Google Scholar
• Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008; 322:271–275. doi:10.1126/science.1160062
   PubMed Web of Science ®Google Scholar
• Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, Albacker LA, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 2006; 203:883–895. doi:10.1084/jem.20051776
   PubMed Web of Science ®Google Scholar
• Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001; 2:261–268. doi:10.1038/85330
   PubMed Web of Science ®Google Scholar
• Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192:1027–1034.
   PubMed Web of Science ®Google Scholar
• Wu L, Yun Z, Tagawa T, Rey-McIntyre K, De Perrot M CTLA-4 blockade expands infiltrating T cells and inhibits cancer cell repopulation during the intervals of chemotherapy in murine mesothelioma. Mol Cancer Ther 2012; 11:1809–1819. doi:10.1158/1535-7163.MCT-11-1014
   PubMed Web of Science ®Google Scholar
• Lesterhuis WJ, Salmons J, Nowak AK, Rozali EN, Khong A, Dick IM, et al. Synergistic effect of CTLA-4 blockade and cancer chemotherapy in the induction of anti-tumor immunity. PLoS One 2013; 8:e61895. doi:10.1371/journal.pone.0061895
   PubMed Web of Science ®Google Scholar
• Leshem Y, O’Brien J, Liu X, Bera TK, Terabe M, Berzofsky JA, et al. Combining local immunotoxins targeting mesothelin with CTLA-4 blockade synergistically eradicates murine cancer by promoting anticancer immunity. Cancer Immunol Res 2017; 5:685–694. doi:10.1158/2326-6066.CIR-16-0330
   PubMed Web of Science ®Google Scholar
• Mkrtichyan M, Najjar YG, Raulfs EC, Abdalla MY, Samara R, Rotem-Yehudar R, et al. Anti-PD-1 synergizes with cyclophosphamide to induce potent anti-tumor vaccine effects through novel mechanisms. Eur J Immunol 2011; 41:2977–2986. doi:10.1002/eji.201141639
   PubMed Web of Science ®Google Scholar
• Wu L, Wu MO, De La Maza L, Yun Z, Yu J, Zhao Y, et al. Targeting the inhibitory receptor CTLA-4 on T cells increased abscopal effects in murine mesothelioma model. Oncotarget 2015; 6:12468–12480. doi:10.18632/oncotarget.3487
   PubMedGoogle Scholar
• Maio M, Scherpereel A, Calabro L, Aerts J, Perez SC, Bearz A, et al. Tremelimumab as second-line or third-line treatment in relapsed malignant mesothelioma (DETERMINE): a multicentre, international, randomised, double-blind, placebo-controlled phase 2b trial. Lancet Oncol 2017; 18:1261–1273. doi:10.1016/S1470-2045(17)30446-1
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015; 373:23–34. doi:10.1056/NEJMoa1504030
   PubMed Web of Science ®Google Scholar
• Sabatos CA, Chakravarti S, Cha E, Schubart A, Sanchez-Fueyo A, Zheng XX, et al. Interaction of tim-3 and tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol 2003; 4:1102–1110. doi:10.1038/ni988
   PubMed Web of Science ®Google Scholar
• Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC Targeting tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010; 207:2187–2194. doi:10.1084/jem.20100643
   PubMed Web of Science ®Google Scholar
• Valzasina B, Guiducci C, Dislich H, Killeen N, Weinberg AD, Colombo MP. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood 2005; 105:2845–2851. doi:10.1182/blood-2004-07-2959
   PubMed Web of Science ®Google Scholar
• Cohen AD, Schaer DA, Liu C, Li Y, Hirschhorn-Cymmerman D, Kim SC, et al. Agonist anti-gitr monoclonal antibody induces melanoma tumor immunity in mice by altering regulatory t cell stability and intra-tumor accumulation. PLoS ONE 2010; 5:e10436. doi:10.1371/journal.pone.0010436
   PubMed Web of Science ®Google Scholar
• Ott PA, Hodi FS, Kaufman HL, Wigginton JM, Wolchok JD Combination immunotherapy: a road map. J Immunother Cancer 2017; 5:16. doi:10.1186/s40425-017-0218-5
   PubMed Web of Science ®Google Scholar
• Lesterhuis WJ, Rinaldi C, Jones A, Rozali EN, Dick IM, Khong A, et al. Network analysis of immunotherapy-induced regressing tumours identifies novel synergistic drug combinations. Scientific Reports 2015; 5:12298. doi:10.1038/srep12298
   PubMed Web of Science ®Google Scholar
• Calabro L, Morra A, Fonsatti E, Cutaia O, Fazio C, Annesi D, et al. Efficacy and safety of an intensified schedule of tremelimumab for chemotherapy-resistant malignant mesothelioma: an open-label, single-arm, phase 2 study. Lancet Respir Med 2015; 3:301–309. doi:10.1016/S2213-2600(15)00092-2
   PubMed Web of Science ®Google Scholar
• Marabelle A, Kohrt H, Sagiv-Barfi I, Ajami B, Axtell RC, Zhou G, et al. Depleting tumor-specific Tregs at a single site eradicates disseminated tumors. J Clin Invest 2013; 123:2447–2463. doi:10.1172/JCI64859
   PubMed Web of Science ®Google Scholar
• Redmond WL, Linch SN, Kasiewicz MJ Combined targeting of costimulatory (OX40) and coinhibitory (CTLA-4) pathways elicits potent effector T cells capable of driving robust antitumor immunity. Cancer Immunol Res 2014; 2:142–153. doi:10.1158/2326-6066.CIR-13-0031-T
   PubMed Web of Science ®Google Scholar
• Hu P, Arias RS, Sadun RE, Nien YC, Zhang N, Sabzevari H, et al. Construction and preclinical characterization of Fc-mGITRL for the immunotherapy of cancer. Clin Cancer Res 2008; 14:579–588. doi:10.1158/1078-0432.CCR-07-0940
   PubMed Web of Science ®Google Scholar
• Lu L, Xu X, Zhang B, Zhang R, Ji H, Wang X Combined PD-1 blockade and GITR triggering induce a potent antitumor immunity in murine cancer models and synergizes with chemotherapeutic drugs. J Transl Med 2014; 12:36. doi:10.1186/1479-5876-12-36
   PubMed Web of Science ®Google Scholar
• Ramirez-Montagut T, Chow A, Hirschhorn-Cymerman D, Terwey TH, Kochman AA, Lu S, et al. Glucocorticoid-induced TNF receptor family related gene activation overcomes tolerance/ignorance to melanoma differentiation antigens and enhances antitumor immunity. J Immunol 2006; 176:6434–6442.
   PubMed Web of Science ®Google Scholar
• Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002; 3:135–142. doi:10.1038/ni759
   PubMed Web of Science ®Google Scholar
• Ko K, Yamazaki S, Nakamura K, Nishioka T, Hirota K, Yamaguchi T, et al. Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+CD25+CD4+ regulatory T cells. J Exp Med 2005; 202:885–891.doi:10.1084/jem.20050940
   PubMed Web of Science ®Google Scholar
• Mitsui J, Nishikawa H, Muraoka D, Wang L, Noguchi T, Sato E, et al. Two distinct mechanisms of augmented antitumor activity by modulation of immunostimulatory/inhibitory signals. Clin Cancer Res 2010; 16:2781–2791. doi:10.1158/1078-0432.CCR-09-3243
   PubMed Web of Science ®Google Scholar
• Shevach EM, Stephens GL The GITR-GITRL interaction: co-stimulation or contrasuppression of regulatory activity? Nat Rev Immunol 2006; 6:613–618. doi:10.1038/nri1867
   PubMed Web of Science ®Google Scholar
• Davis MR, Manning LS, Whitaker D, Garlepp MJ, Robinson BW. Establishment of a murine model of malignant mesothelioma. Int J Cancer 1992; 52:881–886.
   PubMed Web of Science ®Google Scholar
• Fisher SA, Aston WJ, Chee J, Khong A, Cleaver AL, Solin JN, et al. Transient treg depletion enhances therapeutic anti-cancer vaccination. Immun Inflamm Dis 2017; 5:16–28. doi:10.1002/iid3.136
   PubMed Web of Science ®Google Scholar
• Sneddon S, Patch AM, Dick IM, Kazakoff S, Pearson JV, Waddell N, et al. Whole exome sequencing of an asbestos-induced wild-type murine model of malignant mesothelioma. BMC Cancer 2017; 17:396. doi:10.1186/s12885-017-3382-6
   PubMed Web of Science ®Google Scholar
• Brown SD, Warren RL, Gibb EA, Martin SD, Spinelli JJ, Nelson BH, et al. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res 2014; 24:743–750. doi:10.1101/gr.165985.113
   PubMed Web of Science ®Google Scholar
• Efremova M, Finotello F, Rieder D, Trajanoski Z Neoantigens Generated by Individual Mutations and Their Role in Cancer Immunity and Immunotherapy. Front Immunol 2017; 8:1679. doi:10.3389/fimmu.2017.01679
   PubMed Web of Science ®Google Scholar
• Hugo W, Zaretsky JM, Sun L, Song C, Moreno BH, Hu-Lieskovan S, et al. Genomic and transcriptomic features of response to anti-pd-1 therapy in metastatic melanoma. Cell 2016; 165:35–44. doi:10.1016/j.cell.2016.02.065
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015; 348:124–128. doi:10.1126/science.aaa1348
   PubMed Web of Science ®Google Scholar
• Strickland KC, Howitt BE, Shukla SA, Rodig S, Ritterhouse LL, Liu JF, et al. Association and prognostic significance of BRCA1/2-mutation status with neoantigen load, number of tumor-infiltrating lymphocytes and expression of PD-1/PD-L1 in high grade serous ovarian cancer. Oncotarget 2016; 7:13587–13598. doi:10.18632/oncotarget.7277
   PubMed Web of Science ®Google Scholar
• Bai J, Gao Z, Li X, Dong L, Han W, Nie J Regulation of PD-1/PD-L1 pathway and resistance to PD-1/PD-L1 blockade. Oncotarget 2017; 8:110693–110707. doi:10.18632/oncotarget.22690
   PubMedGoogle Scholar
• Marzo AL, Lake RA, Robinson BW, Scott B T-cell receptor transgenic analysis of tumor-specific CD8 and CD4 responses in the eradication of solid tumors. Cancer Res 1999; 59:1071–1079.
   PubMed Web of Science ®Google Scholar
• McLean M, Wallace HL, Sharma A, Hill HC, Sabel MS, Egilmez NK A BALB/c murine lung alveolar carcinoma used to establish a surgical spontaneous metastasis model. Clin Exp Metastasis 2004; 21:363369.
   Web of Science ®Google Scholar
• Lansley SM, Cheah HM, Varano Della Vergiliana JF, Chakera A, Lee YC Tissue plasminogen activator potently stimulates pleural effusion via a monocyte chemotactic protein-1-dependent mechanism. Am J Respir Cell Mol Biol 2015; 53:105–112. doi:10.1165/rcmb.2014-0017OC
   PubMed Web of Science ®Google Scholar