Predictive biomarkers for checkpoint inhibitor-based immunotherapy

Hanahan, 2011, Hallmarks of cancer: the next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013 Chen, 2013, Oncology meets immunology: the cancer-immunity cycle, Immunity, 39, 1, 10.1016/j.immuni.2013.07.012 Gajewski, 2013, Innate and adaptive immune cells in the tumor microenvironment, Nat Immunol, 14, 1014, 10.1038/ni.2703 Spranger, 2013, Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells, Sci Transl Med, 5, 200ra116, 10.1126/scitranslmed.3006504 Atkins, 1999, High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993, J Clin Oncol, 17, 2105, 10.1200/JCO.1999.17.7.2105 Rosenberg, 2011, Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy, Clin Cancer Res, 17, 4550, 10.1158/1078-0432.CCR-11-0116 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466 Robert, 2011, Ipilimumab plus dacarbazine for previously untreated metastatic melanoma, N Engl J Med, 364, 2517, 10.1056/NEJMoa1104621 Schadendorf, 2015, Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma, J Clin Oncol, 33, 1889, 10.1200/JCO.2014.56.2736 Borghaei, 2015, Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer, N Engl J Med, 373, 1627, 10.1056/NEJMoa1507643 Brahmer, 2015, Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer, N Engl J Med, 373, 123, 10.1056/NEJMoa1504627 Garon, 2015, Pembrolizumab for the treatment of non-small-cell lung cancer, N Engl J Med, 372, 2018, 10.1056/NEJMoa1501824 Larkin, 2015, Combined nivolumab and ipilimumab or monotherapy in untreated melanoma, N Engl J Med, 373, 23, 10.1056/NEJMoa1504030 Robert, 2015, Nivolumab in previously untreated melanoma without BRAF mutation, N Engl J Med, 372, 320, 10.1056/NEJMoa1412082 Motzer, 2015, Nivolumab versus everolimus in advanced renal-cell carcinoma, N Engl J Med, 373, 1803, 10.1056/NEJMoa1510665 Homet Moreno, 2015, Anti-programmed cell death protein-1/ligand-1 therapy in different cancers, Br J Cancer, 112, 1421, 10.1038/bjc.2015.124 Hammers, 2015, Expanded cohort results from CheckMate 016: a phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC), Proc Am Soc Clin Oncol, 33 Hellmann, 2016, CheckMate 012: safety and efficacy of first-line (1L) nivolumab (nivo; N) and ipilimumab (ipi; I) in advanced (adv) NSCLC, Proc Am Soc Clin Oncol, 34 Topalian, 2012, Safety, activity, and immune correlates of anti-PD-1 antibody in cancer, N Engl J Med, 366, 2443, 10.1056/NEJMoa1200690 Mahoney, 2014, Prognostic and predictive markers for the new immunotherapies, Oncology, 28 Chen, 2016, Regulation of PD-L1: a novel role of pro-survival signalling in cancer, Ann Oncol, 27, 409, 10.1093/annonc/mdv615 Ansell, 2015, PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma, N Engl J Med, 372, 311, 10.1056/NEJMoa1411087 Mansfield, 2016, Heterogeneity of programmed cell death ligand 1 expression in multifocal lung cancer, Clin Cancer Res, 22, 2177, 10.1158/1078-0432.CCR-15-2246 Patel, 2015, PD-L1 Expression as a predictive biomarker in cancer immunotherapy, Mol Cancer Ther, 14, 847, 10.1158/1535-7163.MCT-14-0983 Wolchock JD, Chiarion-Sileni V, Gonzalez R, et al. Updated results from a phase III trial of nivolumab (NIVO) combined with ipilimumab (IPI) in treatment-naive patients (pts) with advanced melanoma (MEL) (CheckMate 067). 2016 ASCO Annual Meeting; Chicago, IL; June 3–7, 2016. Abstr 9505. Hamid, 2011, A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma, J Transl Med, 9, 204, 10.1186/1479-5876-9-204 Tumeh, 2014, PD-1 blockade induces responses by inhibiting adaptive immune resistance, Nature, 515, 568, 10.1038/nature13954 Chen, 2016, Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade, Cancer Discov, 6, 827, 10.1158/2159-8290.CD-15-1545 Le, 2015, PD-1 blockade in tumors with mismatch-repair deficiency, N Engl J Med, 372, 2509, 10.1056/NEJMoa1500596 Le, 2016, Programmed death-1 blockade in mismatch repair deficient colorectal cancer, Proc Am Soc Clin Oncol, 34 Snyder, 2014, Genetic basis for clinical response to CTLA-4 blockade in melanoma, N Engl J Med, 371, 2189, 10.1056/NEJMoa1406498 Van Allen, 2015, Genomic correlates of response to CTLA-4 blockade in metastatic melanoma, Science, 350, 207, 10.1126/science.aad0095 Rizvi, 2015, Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer, Science, 348, 124, 10.1126/science.aaa1348 Johnson, 2016, Hybrid capture-based next-generation sequencing (HC NGS) in melanoma to identify markers of response to anti-PD-1/PD-L1, Proc Am Soc Clin Oncol, 34 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 Hugo, 2016, Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma, Cell, 165, 35, 10.1016/j.cell.2016.02.065 McGranahan, 2016, Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade, Science, 351, 1463, 10.1126/science.aaf1490 Ji, 2012, An immune-active tumor microenvironment favors clinical response to ipilimumab, Cancer Immunol Immunother, 61, 1019, 10.1007/s00262-011-1172-6 Ribas, 2015, Association of response to programmed death receptor 1 (PD-1) blockade with pembrolizumab (MK-3475) with an interferon-inflammatory immune gene signature, Proc Am Soc Clin Oncol, 33 Huh, 2012, Prognostic significance of tumor-infiltrating lymphocytes for patients with colorectal cancer, Arch Surg, 147, 366, 10.1001/archsurg.2012.35 Thomas, 2013, Tumor-infiltrating lymphocyte grade in primary melanomas is independently associated with melanoma-specific survival in the population-based genes, environment and melanoma study, J Clin Oncol, 31, 4252, 10.1200/JCO.2013.51.3002 Zeng, 2016, Prognostic and predictive value of tumor-infiltrating lymphocytes for clinical therapeutic research in patients with non-small cell lung cancer, Oncotarget, 7, 13765, 10.18632/oncotarget.7282 Messina, 2012, 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy?, Sci Rep, 2, 765, 10.1038/srep00765 Tokito, 2016, Predictive relevance of PD-L1 expression combined with CD8+ TIL density in stage III non-small cell lung cancer patients receiving concurrent chemoradiotherapy, Eur J Cancer, 55, 7, 10.1016/j.ejca.2015.11.020 Castle, 2012, Exploiting the mutanome for tumor vaccination, Cancer Res, 72, 1081, 10.1158/0008-5472.CAN-11-3722 Matsushita, 2012, Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting, Nature, 482, 400, 10.1038/nature10755 Rooney, 2015, Molecular and genetic properties of tumors associated with local immune cytolytic activity, Cell, 160, 48, 10.1016/j.cell.2014.12.033 Schumacher, 2015, Neoantigens in cancer immunotherapy, Science, 348, 69, 10.1126/science.aaa4971 Ferrucci, 2016, Baseline neutrophils and derived neutrophil-to-lymphocyte ratio: prognostic relevance in metastatic melanoma patients receiving ipilimumab, Ann Oncol, 27, 732, 10.1093/annonc/mdw016 Martens, 2016, Baseline peripheral blood biomarkers associated with clinical outcome of advanced melanoma patients treated with ipilimumab, Clin Cancer Res, 22, 2908, 10.1158/1078-0432.CCR-15-2412 Delyon, 2013, Experience in daily practice with ipilimumab for the treatment of patients with metastatic melanoma: an early increase in lymphocyte and eosinophil counts is associated with improved survival, Ann Oncol, 24, 1697, 10.1093/annonc/mdt027 Ku, 2010, Single-institution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: lymphocyte count after 2 doses correlates with survival, Cancer, 116, 1767, 10.1002/cncr.24951 Simeone, 2014, Immunological and biological changes during ipilimumab treatment and their potential correlation with clinical response and survival in patients with advanced melanoma, Cancer Immunol Immunother, 63, 675, 10.1007/s00262-014-1545-8 Weide, 2016, Baseline biomarkers for outcome of melanoma patients treated with pembrolizumab, Clin Cancer Res, 10.1158/1078-0432.CCR-16-0127 Weber, 2013, Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma, J Clin Oncol, 31, 4311, 10.1200/JCO.2013.51.4802 Gibney, 2015, Safety, correlative markers, and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma, Clin Cancer Res, 21, 712, 10.1158/1078-0432.CCR-14-2468 Postow, 2015, Peripheral T cell receptor diversity is associated with clinical outcomes following ipilimumab treatment in metastatic melanoma, J Immunother Cancer, 3, 23, 10.1186/s40425-015-0070-4 Johnson, 2016, Melanoma-specific MHC-II expression represents a tumour-autonomous phenotype and predicts response to anti-PD-1/PD-L1 therapy, Nat Commun, 7, 10582, 10.1038/ncomms10582 Yuan, 2016, Novel technologies and emerging biomarkers for personalized cancer immunotherapy, J Immunother Cancer, 4, 3, 10.1186/s40425-016-0107-3 Feng, 2015, Multispectral imaging of formalin-fixed tissue predicts ability to generate tumor-infiltrating lymphocytes from melanoma, J Immunother Cancer, 3, 47, 10.1186/s40425-015-0091-z Kluger, 2015, Characterization of PD-L1 expression and associated T-cell infiltrates in metastatic melanoma samples from variable anatomic sites, Clin Cancer Res, 21, 3052, 10.1158/1078-0432.CCR-14-3073 Taube, 2014, Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy, Clin Cancer Res, 20, 5064, 10.1158/1078-0432.CCR-13-3271 Matsushita, 2016, Neoantigen load, antigen presentation machinery, and immune signatures determine prognosis in clear cell renal cell carcinoma, Cancer Immunol Res, 4, 463, 10.1158/2326-6066.CIR-15-0225 Taube, 2015, Differential expression of immune-regulatory genes associated with PD-L1 display in melanoma: implications for PD-1 pathway blockade, Clin Cancer Res, 21, 3969, 10.1158/1078-0432.CCR-15-0244 Higgs, 2016, Relationship of baseline tumoral IFNγ mRNA and PD-L1 protein expression to overall survival in durvalumab-treated NSCLC patients, Proc Am Soc Clin Oncol, 34 Higgs BW, Robbins PB, Blake-Haskins JA et al. High tumoral IFNγ mRNA, PD-L1 protein, and combined IFNγ mRNA/PD-L1 protein expression associates with response to durvalumab (anti-PD-L1) monotherapy in NSCLC patients. European Cancer Congress 2015; Vienna; Sept 25–29. Abstr 15LBA. Spranger, 2015, Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity, Nature, 523, 231, 10.1038/nature14404