Loss of IFN-γ Pathway Genes in Tumor Cells as a Mechanism of Resistance to Anti-CTLA-4 Therapy

Alegre, 1998, Expression and function of CTLA-4 in Th1 and Th2 cells, J. Immunol., 161, 3347, 10.4049/jimmunol.161.7.3347 Borghaei, 2015, Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer, N. Engl. J. Med., 373, 1627, 10.1056/NEJMoa1507643 Chen, 2009, Anti-CTLA-4 therapy results in higher CD4+ICOShi T cell frequency and IFN-gamma levels in both nonmalignant and malignant prostate tissues, Proc. Natl. Acad. Sci. USA, 106, 2729, 10.1073/pnas.0813175106 Chin, 1997, Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis, Mol. Cell. Biol., 17, 5328, 10.1128/MCB.17.9.5328 Cibulskis, 2013, Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples, Nat. Biotechnol., 31, 213, 10.1038/nbt.2514 Detjen, 2001, Interferon gamma inhibits growth of human pancreatic carcinoma cells via caspase-1 dependent induction of apoptosis, Gut, 49, 251, 10.1136/gut.49.2.251 Dulos, 2012, PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer, J. Immunother., 35, 169, 10.1097/CJI.0b013e318247a4e7 Dunn, 2006, Interferons, immunity and cancer immunoediting, Nat. Rev. Immunol., 6, 836, 10.1038/nri1961 Dunn, 2005, IFN unresponsiveness in LNCaP cells due to the lack of JAK1 gene expression, Cancer Res., 65, 3447, 10.1158/0008-5472.CAN-04-4316 Fisher, 2011, A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries, Genome Biol., 12, R1, 10.1186/gb-2011-12-1-r1 Fu, 2011, The ICOS/ICOSL pathway is required for optimal antitumor responses mediated by anti-CTLA-4 therapy, Cancer Res., 71, 5445, 10.1158/0008-5472.CAN-11-1138 Gautier, 2004, Affy--analysis of Affymetrix GeneChip data at the probe level, Bioinformatics, 20, 307, 10.1093/bioinformatics/btg405 Gnirke, 2009, Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing, Nat. Biotechnol., 27, 182, 10.1038/nbt.1523 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N. Engl. J. Med., 363, 711, 10.1056/NEJMoa1003466 Ikeda, 2002, The roles of IFN gamma in protection against tumor development and cancer immunoediting, Cytokine Growth Factor Rev., 13, 95, 10.1016/S1359-6101(01)00038-7 Kaplan, 1998, Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice, Proc. Natl. Acad. Sci. USA, 95, 7556, 10.1073/pnas.95.13.7556 Liakou, 2008, CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients, Proc. Natl. Acad. Sci. USA, 105, 14987, 10.1073/pnas.0806075105 Li, 2009, Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, 25, 1754, 10.1093/bioinformatics/btp324 Liu, 2001, A transcriptional corepressor of Stat1 with an essential LXXLL signature motif, Proc. Natl. Acad. Sci. USA, 98, 3203, 10.1073/pnas.051489598 Motzer, 2015, Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma, N. Engl. J. Med., 373, 1803, 10.1056/NEJMoa1510665 Mowen, 2001, Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription, Cell, 104, 731, 10.1016/S0092-8674(01)00269-0 Olshen, 2004, Circular binary segmentation for the analysis of array-based DNA copy number data, Biostatistics, 5, 557, 10.1093/biostatistics/kxh008 Paradis, 2001, The anti-tumor activity of anti-CTLA-4 is mediated through its induction of IFN gamma, Cancer Immunol. Immunother., 50, 125, 10.1007/s002620100181 Peng, 2012, PD-1 blockade enhances T-cell migration to tumors by elevating IFN-γ inducible chemokines, Cancer Res., 72, 5209, 10.1158/0008-5472.CAN-12-1187 Quezada, 2006, CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells, J. Clin. Invest., 116, 1935, 10.1172/JCI27745 Reich, 2013, A death-promoting role for ISG54/IFIT2, J. Interferon Cytokine Res., 33, 199, 10.1089/jir.2012.0159 Robert, 2011, Ipilimumab plus dacarbazine for previously untreated metastatic melanoma, N. Engl. J. Med., 364, 2517, 10.1056/NEJMoa1104621 Rosenberg, 2016, Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial, Lancet, 387, 1909, 10.1016/S0140-6736(16)00561-4 Sharma, 2015, The future of immune checkpoint therapy, Science, 348, 56, 10.1126/science.aaa8172 Sharma, 2015, Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential, Cell, 161, 205, 10.1016/j.cell.2015.03.030 Sherry, 2001, dbSNP: the NCBI database of genetic variation, Nucleic Acids Res., 29, 308, 10.1093/nar/29.1.308 Shi, 2016, Interdependent IL-7 and IFN-γ signalling in T-cell controls tumour eradication by combined α-CTLA-4+α-PD-1 therapy, Nat. Commun., 7, 12335, 10.1038/ncomms12335 Shi, 2013, Inhibitory role of the transcription repressor Gfi1 in the generation of thymus-derived regulatory T cells, Proc. Natl. Acad. Sci. USA, 110, E3198, 10.1073/pnas.1300950110 Song, 1998, The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities, J. Biol. Chem., 273, 35056, 10.1074/jbc.273.52.35056 Szabo, 2003, Molecular mechanisms regulating Th1 immune responses, Annu. Rev. Immunol., 21, 713, 10.1146/annurev.immunol.21.120601.140942 Therasse, 2000, New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada, J. Natl. Cancer Inst., 92, 205, 10.1093/jnci/92.3.205 Van Allen, 2015, Genomic correlates of response to CTLA-4 blockade in metastatic melanoma, Science, 350, 207, 10.1126/science.aad0095 van der Heide, 2016, Down-regulation of MicroRNA-31 in CD4+ T Cells Contributes to Immunosuppression in Human Sepsis by Promoting TH2 Skewing, Anesthesiology, 124, 908, 10.1097/ALN.0000000000001031 Wang, 2010, ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data, Nucleic Acids Res., 38, e164, 10.1093/nar/gkq603 Zaretsky, 2016, Mutations associated with acquired resistance to pd-1 blockade in melanoma, N. Engl. J. Med., 10.1056/NEJMoa1604958