Immune checkpoint: The novel target for antitumor therapy

Genes and Diseases - Tập 8 - Trang 25-37 - 2021
Xianghu Jiang1, Guohong Liu2, Yirong Li1, Yunbao Pan1
1Department of Laboratory Medicine, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, Hubei, 430072, PR China
2Department of Radiology, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, Hubei, 430072, PR China

Tài liệu tham khảo

Lizée, 2013, Harnessing the power of the immune system to target cancer, Annu Rev Med, 64, 71, 10.1146/annurev-med-112311-083918 Kean, 2017, Advances in targeting co-inhibitory and co-stimulatory pathways in transplantation settings: the Yin to the Yang of cancer immunotherapy, Immunol Rev, 276, 192, 10.1111/imr.12523 Janakiram, 2017, The third group of the B7-CD28 immune checkpoint family: HHLA2, TMIGD2, B7x, and B7-H3, Immunol Rev, 276, 26, 10.1111/imr.12521 Ni, 2017, New checkpoints in cancer immunotherapy, Immunol Rev, 276, 52, 10.1111/imr.12524 Andrews, 2017, LAG3 (CD223) as a cancer immunotherapy target, Immunol Rev, 276, 80, 10.1111/imr.12519 Das, 2017, Tim-3 and its role in regulating anti-tumor immunity, Immunol Rev, 276, 97, 10.1111/imr.12520 Chen, 2004, Co-inhibitory molecules of the B7–CD28 family in the control of T-cell immunity, Nat Rev Immunol, 4, 336, 10.1038/nri1349 Nurieva, 2006, T-cell tolerance or function is determined by combinatorial costimulatory signals, EMBO J, 25, 2623, 10.1038/sj.emboj.7601146 Tsai, 2017, Cancer immunotherapy by targeting immune checkpoints: mechanism of T cell dysfunction in cancer immunity and new therapeutic targets, J Biomed Sci, 24, e35, 10.1186/s12929-017-0341-0 Blackburn, 2009, Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection, Nat Immunol, 10, 29, 10.1038/ni.1679 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466 Topalian, 2015, Immune checkpoint blockade: a common denominator approach to cancer therapy, Cancer Cell, 27, 450, 10.1016/j.ccell.2015.03.001 Ribas, 2015, Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): a randomised, controlled, phase 2 trial, Lancet Oncol, 16, 908, 10.1016/S1470-2045(15)00083-2 Anderson, 2016, Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation, Immunity, 44, 989, 10.1016/j.immuni.2016.05.001 Lucca, 2017, Co-inhibitory blockade while preserving tolerance: checkpoint inhibitors for glioblastoma, Immunol Rev, 276, 9, 10.1111/imr.12529 Tison, 2019, Safety and efficacy of immune checkpoint inhibitors in patients with cancer and preexisting autoimmune disease: a Nationwide Multicenter Cohort study, Arthritis Rheumatol, 71, 2100, 10.1002/art.41068 Zhang, 2018, Cancer immune checkpoint blockade therapy and its associated autoimmune cardiotoxicity, Acta Pharmacol Sin, 39, 1693, 10.1038/s41401-018-0062-2 Grabie, 2019, T cell checkpoint regulators in the heart, Cardiovasc Res, 115, 869, 10.1093/cvr/cvz025 Kasagi, 2011, PD-1 and autoimmunity, Crit Rev Immunol, 31, 265, 10.1615/CritRevImmunol.v31.i4.10 Zhang, 2016, Co-stimulatory and co-inhibitory pathways in autoimmunity, Immunity, 44, 1034, 10.1016/j.immuni.2016.04.017 Chen, 2013, Oncology meets immunology: the cancer-immunity cycle, Immunity, 39, 1, 10.1016/j.immuni.2013.07.012 Spranger, 2016, Mechanisms of tumor escape in the context of the T-cell-inflamed and the non-T-cell-inflamed tumor microenvironment, Int Immunol, 28, 383, 10.1093/intimm/dxw014 Maruse, 2018, Significant association of increased PD-L1 and PD-1 expression with nodal metastasis and a poor prognosis in oral squamous cell carcinoma, Int J Oral, 47, 836 Nakano, 2018, PD-1+ TIM-3+ T cells in malignant ascites predict prognosis of gastrointestinal cancer, Cancer Sci, 109, 2986, 10.1111/cas.13723 Linsley, 1990, T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1, Proc Natl Acad Sci U S A, 87, 5031, 10.1073/pnas.87.13.5031 Walunas, 1994, CTLA-4 can function as a negative regulator of T cell activation, Immunity, 1, 405, 10.1016/1074-7613(94)90071-X Callahan, 2013, Antibodies to stimulate host immunity: lessons from ipilimumab, In: Cancer Immunotherapy. ed. Elsevier;, 287 Soskic, 2014, A transendocytosis perspective on the CD28/CTLA-4 pathway, Adv Immunol, 124, 95, 10.1016/B978-0-12-800147-9.00004-2 Azuma, 1993, B70 antigen is a second ligand for CTLA-4 and CD28, Nature, 366, 76, 10.1038/366076a0 Allemani, 2015, Global surveillance of cancer survival 1995–2009: analysis of individual data for 25 676 887 patients from 279 population-based registries in 67 countries (CONCORD-2), Lancet, 385, 977, 10.1016/S0140-6736(14)62038-9 Grosso, 2013, CTLA-4 blockade in tumor models: an overview of preclinical and translational research, Cancer Immunity Arch, 13, e5 Gubens, 2016, Phase I/II study of pembrolizumab (pembro) plus ipilimumab (Ipi) as second-line therapy for NSCLC: KEYNOTE-021 cohorts D and H, Am Soc Clin Oncol, 34 Prasad, 2018, Cancer drugs approved based on biomarkers and not tumor type—FDA approval of pembrolizumab for mismatch repair-deficient solid cancers, JAMA Oncol, 4, 157, 10.1001/jamaoncol.2017.4182 Magistrelli, 1999, A soluble form of CTLA-4 generated by alternative splicing is expressed by nonstimulated human T cells, Eur J Immunol, 29, 3596, 10.1002/(SICI)1521-4141(199911)29:11<3596::AID-IMMU3596>3.0.CO;2-Y Sato, 2004, Serum soluble CTLA-4 levels are increased in diffuse cutaneous systemic sclerosis, Rheumatology, 43, 1261, 10.1093/rheumatology/keh303 Liu, 2017, Current treatment options of T cell-associated immunotherapy in multiple myeloma, Clin Exp Med, 17, 431, 10.1007/s10238-017-0450-9 Liu, 2017, Soluble cytotoxic T-lymphocyte antigen 4: a favorable predictor in malignant tumors after therapy, OncoTargets Ther, 10, 2147, 10.2147/OTT.S128451 Pistillo, 2019, Soluble CTLA-4 as a favorable predictive biomarker in metastatic melanoma patients treated with ipilimumab: an Italian melanoma intergroup study, Cancer Immunol Immunother, 68, 97, 10.1007/s00262-018-2258-1 Ishida, 1992, Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death, EMBO J, 11, 3887, 10.1002/j.1460-2075.1992.tb05481.x Yao, 2009, PD-1 on dendritic cells impedes innate immunity against bacterial infection, Blood, 113, 5811, 10.1182/blood-2009-02-203141 Hassan, 2015, PD-1, PD-L1 and PD-L2 gene expression on T-cells and natural killer cells declines in conjunction with a reduction in PD-1 protein during the intensive phase of tuberculosis treatment, PLoS One, 10, e0137646, 10.1371/journal.pone.0137646 Wu, 2009, Kupffer cell suppression of CD8+ T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions, Cancer Res, 69, 8067, 10.1158/0008-5472.CAN-09-0901 Ma, 2011, Expression and clinical significance of PD-L1 and PD-1 in non-small cell lung cancer, J Pract Med, 27, 1551 Dzik, 2000, B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin 10 secretion, Transfus Med Rev, 3, 285 Ji, 2015, PD-1/PD-L1 pathway in non-small-cell lung cancer and its relation with EGFR mutation, J Transl Med, 13, e5, 10.1186/s12967-014-0373-0 Bigelow, 2013, Immunohistochemical staining of B7-H1 (PD-L1) on paraffin-embedded slides of pancreatic adenocarcinoma tissue, J Vis Exp, e4059 Kim, 2016, Prognostic implications of immunosuppressive protein expression in tumors as well as immune cell infiltration within the tumor microenvironment in gastric cancer, Gastric Cancer, 19, 42, 10.1007/s10120-014-0440-5 Mittendorf, 2014, PD-L1 expression in triple-negative breast cancer, Cancer Immunol Res, 2, 361, 10.1158/2326-6066.CIR-13-0127 Gandhi, 2018, Pembrolizumab plus chemotherapy in metastatic non–small-cell lung cancer, N Engl J Med, 378, 2078, 10.1056/NEJMoa1801005 Weber, 2015, Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial, Lancet Oncol, 16, 375, 10.1016/S1470-2045(15)70076-8 Daud, 2016, Programmed death-ligand 1 expression and response to the anti–programmed death 1 antibody Pembrolizumab in melanoma, J Clin Oncol, 34, 4102, 10.1200/JCO.2016.67.2477 Wolchok, 2017, Overall survival with combined nivolumab and ipilimumab in advanced melanoma, N Engl J Med, 377, 1345, 10.1056/NEJMoa1709684 Koyama, 2016, Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints, Nat Commun, 7, e10501, 10.1038/ncomms10501 Zhou, 2017, Soluble PD-L1 as a biomarker in malignant melanoma treated with checkpoint blockade, Cancer Immunol Res, 5, 480, 10.1158/2326-6066.CIR-16-0329 Rossille, 2014, High level of soluble programmed cell death ligand 1 in blood impacts overall survival in aggressive diffuse large B-cell lymphoma: results from a French multicenter clinical trial, Leukemia, 28, 2367, 10.1038/leu.2014.137 Okuma, 2018, Soluble programmed cell death ligand 1 as a novel biomarker for nivolumab therapy for non-small-cell lung cancer, Clin Lung Cancer, 19, 410, 10.1016/j.cllc.2018.04.014 Wang, 2015, Serum levels of soluble programmed death ligand 1 predict treatment response and progression free survival in multiple myeloma, Oncotarget, 6, 41228, 10.18632/oncotarget.5682 Frigola, 2011, Identification of a soluble form of B7-H1 that retains immunosuppressive activity and is associated with aggressive renal cell carcinoma, Clin Cancer Res Off J Am Assoc Cancer Res, 17, 1915, 10.1158/1078-0432.CCR-10-0250 Schwarzenbach, 2011, Cell-free nucleic acids as biomarkers in cancer patients, Nat Rev Cancer, 11, 426, 10.1038/nrc3066 Stroun, 2001, About the possible origin and mechanism of circulating DNA: apoptosis and active DNA release, Clin Chim Acta, 313, 139, 10.1016/S0009-8981(01)00665-9 Lee, 2018, Association between circulating tumor DNA and pseudoprogression in patients with metastatic melanoma treated with anti–programmed cell death 1 antibodies, JAMA Oncol, 4, 717, 10.1001/jamaoncol.2017.5332 Lee, 2017, Circulating tumour DNA predicts response to anti-PD1 antibodies in metastatic melanoma, Ann Oncol, 28, 1130, 10.1093/annonc/mdx026 Khagi, 2017, Hypermutated circulating tumor DNA: correlation with response to checkpoint inhibitor–based immunotherapy, Clin Cancer Res, 23, 5729, 10.1158/1078-0432.CCR-17-1439 Simons, 2009, Exosomes–vesicular carriers for intercellular communication, Curr Opin Cell Biol, 21, 575, 10.1016/j.ceb.2009.03.007 Del Re, 2018, PD-L1 mRNA expression in plasma-derived exosomes is associated with response to anti-PD-1 antibodies in melanoma and NSCLC, Br J Cancer, 118, 820, 10.1038/bjc.2018.9 Chen, 2018, Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response, Nature, 560, 382, 10.1038/s41586-018-0392-8 Tucci, 2018, Serum exosomes as predictors of clinical response to ipilimumab in metastatic melanoma, OncoImmunology, 7, e1387706, 10.1080/2162402X.2017.1387706 Monney, 2002, Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease, Nature, 415, 536, 10.1038/415536a Anderson, 2016, Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation, Immunity, 44, 989, 10.1016/j.immuni.2016.05.001 Yasinska, 2019, The Tim-3-galectin-9 pathway and its regulatory mechanisms in human breast cancer, Front Immunol, 10, e1594, 10.3389/fimmu.2019.01594 Tallerico, 2017, IL-15, TIM-3 and NK cells subsets predict responsiveness to anti-CTLA-4 treatment in melanoma patients, OncoImmunology, 6, e1261242, 10.1080/2162402X.2016.1261242 Shayan, 2017, Adaptive resistance to anti-PD1 therapy by Tim-3 upregulation is mediated by the PI3K-Akt pathway in head and neck cancer, OncoImmunology, 6, e1261779, 10.1080/2162402X.2016.1261779 Silva, 2017, The Tim-3-galectin-9 secretory pathway is involved in the immune escape of human acute myeloid leukemia cells, EBioMedicine, 22, 44, 10.1016/j.ebiom.2017.07.018 Triebel, 1990, LAG-3, a novel lymphocyte activation gene closely related to CD4, J Exp Med, 171, 1393, 10.1084/jem.171.5.1393 Weber, 1993, Mouse CD4 binds MHC class II with extremely low affinity, Int Immunol, 5, 695, 10.1093/intimm/5.6.695 Baixeras, 1992, Characterization of the lymphocyte activation gene 3-encoded protein. A new ligand for human leukocyte antigen class II antigens, J Exp Med, 176, 327, 10.1084/jem.176.2.327 Workman, 2002, Phenotypic analysis of the murine CD4-related glycoprotein, CD223 (LAG-3), Eur J Immunol, 32, 2255, 10.1002/1521-4141(200208)32:8<2255::AID-IMMU2255>3.0.CO;2-A Huard, 1996, T cell major histocompatibility complex class II molecules down-regulate CD4+ T cell clone responses following LAG-3 binding, Eur J Immunol, 26, 1180, 10.1002/eji.1830260533 Xu, 2014, LSECtin expressed on melanoma cells promotes tumor progression by inhibiting antitumor T-cell responses, Cancer Res, 74, 3418, 10.1158/0008-5472.CAN-13-2690 Yang, 2016, Involvement of LSECtin in the hepatic natural killer cell response, Biochem Biophys Res Commun, 476, 49, 10.1016/j.bbrc.2016.05.072 Matsuzaki, 2010, Tumor-infiltrating NY-ESO-1–specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer, Proc Natl Acad Sci U S A, 107, 7875, 10.1073/pnas.1003345107 Woo, 2012, Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape, Cancer Res, 72, 917, 10.1158/0008-5472.CAN-11-1620 Ascierto, 2017, Ann Oncol, 28 Ascierto, 2017, Initial efficacy of anti-lymphocyte activation gene-3 (anti–LAG-3; BMS-986016) in combination with nivolumab (Nivo) in Pts with melanoma (MEL) previously treated with anti–PD-1/PD-L1 therapy, Am Soc Clin Oncol, 35 Triebel, 2006, A soluble lymphocyte activation gene-3 (sLAG-3) protein as a prognostic factor in human breast cancer expressing estrogen or progesterone receptors, Cancer Lett, 235, 147, 10.1016/j.canlet.2005.04.015 Zhao, 2013, HHLA2 is a member of the B7 family and inhibits human CD4 and CD8 T-cell function, Proc Natl Acad Sci U S A, 110, 9879, 10.1073/pnas.1303524110 Janakiram, 2015, Expression, clinical significance, and receptor identification of the newest B7 family member HHLA2 protein, Clin Cancer Res Off J Am Assoc Cancer Res, 21, 2359, 10.1158/1078-0432.CCR-14-1495 Koirala, 2016, HHLA2, a member of the B7 family, is expressed in human osteosarcoma and is associated with metastases and worse survival, Sci Rep, 6, srep31154, 10.1038/srep31154 Schalper, 2017, Differential expression and significance of PD-L1, Ido-1, and B7-H4 in human lung cancer, Clin Cancer Res Off J Am Assoc Cancer Res, 23, 370, 10.1158/1078-0432.CCR-16-0150 Chapoval, 2001, B7-H3: a costimulatory molecule for T cell activation and IFN-γ production, Nat Immunol, 2, 269, 10.1038/85339 Hofmeyer, 2008, The contrasting role of B7-H3, Proc Natl Acad Sci U S A, 105, 10277, 10.1073/pnas.0805458105 Suh, 2003, The B7 family member B7-H3 preferentially down-regulates T helper type 1–mediated immune responses, Nat Immunol, 4, 899, 10.1038/ni967 Zang, 2007, B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome, Proc Natl Acad Sci U S A, 104, 19458, 10.1073/pnas.0709802104 Altan, 2017, B7-H3 expression in NSCLC and its association with B7-H4, PD-L1 and tumor-infiltrating lymphocytes, Clin Cancer Res, 23, 5202, 10.1158/1078-0432.CCR-16-3107 Zhang, 2008, Soluble CD276 (B7-H3) is released from monocytes, dendritic cells and activated T cells and is detectable in normal human serum, Immunology, 123, 538, 10.1111/j.1365-2567.2007.02723.x Lin, 2019, Skint8, a novel B7 family-related molecule, negatively regulates T cell responses, J Immunol, 203, 400, 10.4049/jimmunol.1800639 Zang, 2007, The B7 family and cancer therapy: costimulation and coinhibition, Clin Cancer Res, 13, 5271, 10.1158/1078-0432.CCR-07-1030 Quandt, 2011, B7-h4 expression in human melanoma: its association with patients' survival and antitumor immune response, Clin Cancer Res, 17, 3100, 10.1158/1078-0432.CCR-10-2268 Krambeck, 2006, B7-H4 expression in renal cell carcinoma and tumor vasculature: associations with cancer progression and survival, Proc Natl Acad Sci U S A, 103, 10391, 10.1073/pnas.0600937103 Wu, 2016, B7-H4 expression indicates poor prognosis of oral squamous cell carcinoma, Cancer Immunol Immunother, 65, 1035, 10.1007/s00262-016-1867-9 Thompson, 2008, Serum-soluble B7x is elevated in renal cell carcinoma patients and is associated with advanced stage, Cancer Res, 68, 6054, 10.1158/0008-5472.CAN-08-0869 Simon, 2006, B7-h4 is a novel membrane-bound protein and a candidate serum and tissue biomarker for ovarian cancer, Cancer Res, 66, 1570, 10.1158/0008-5472.CAN-04-3550 Wang, 2016, Prognostic values of B7-H4 in non-small cell lung cancer, Biomarkers, 1 Zhang, 2015, Diagnostic value of serum B7-H4 for hepatocellular carcinoma, J Surg Res, 197, 301, 10.1016/j.jss.2015.04.034 Dong, 2015, B7-H4 expression is associated with tumor progression and prognosis in patients with osteosarcoma, BioMed Res Int, 2015, 156432, 10.1155/2015/156432 Azuma, 2018, Serum soluble B7-H4 is a prognostic marker for patients with non-metastatic clear cell renal cell carcinoma, PLoS One, 13, e0199719, 10.1371/journal.pone.0199719 He, 2017, Remarkably similar CTLA-4 binding properties of therapeutic ipilimumab and tremelimumab antibodies, Oncotarget, 8, 67129, 10.18632/oncotarget.18004 Padda, 2018, Ipilimumab induced digital vasculitis, J Immunother Cancer, 6, e12, 10.1186/s40425-018-0321-2 Larkin, 2015, Combined nivolumab and ipilimumab or monotherapy in untreated melanoma, N Engl J Med, 373, 23, 10.1056/NEJMoa1504030 Motzer, 2018, Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma, N Engl J Med, 378, 1277, 10.1056/NEJMoa1712126 Cella, 2019, Patient-reported outcomes of patients with advanced renal cell carcinoma treated with nivolumab plus ipilimumab versus sunitinib (CheckMate 214): a randomised, phase 3 trial, Lancet Oncol, 20, 297, 10.1016/S1470-2045(18)30778-2 Lenz, 2018, LBA18_PR Durable clinical benefit with nivolumab (NIVO) plus low-dose ipilimumab (IPI) as first-line therapy in microsatellite instability-high/mismatch repair deficient (MSI-H/dMMR) metastatic colorectal cancer (mCRC), Ann Oncol, 29 Force, 2017, First-line treatment of metastatic melanoma: role of nivolumab, ImmunoTargets Ther, 6, 1, 10.2147/ITT.S110479 Robert, 2015, Nivolumab in previously untreated melanoma without BRAF mutation, N Engl J Med, 372, 320, 10.1056/NEJMoa1412082 Long, 2015, Nivolumab Improved Survival vs Dacarbazine in Patients with Untreated Advanced Melanoma, J Transl Med, 13, 06, 10.1186/1479-5876-13-S1-O6 Griffin, 2017, BRAF inhibitors: resistance and the promise of combination treatments for melanoma, Oncotarget, 8, 78174, 10.18632/oncotarget.19836 Hu-Lieskovan, 2015, Improved antitumor activity of immunotherapy with BRAF and MEK inhibitors in BRAFV600E melanoma, Sci Transl Med, 7, 10.1126/scitranslmed.aaa4691 Motzer, 2015, Nivolumab versus everolimus in advanced renal-cell carcinoma, N Engl J Med, 373, 1803, 10.1056/NEJMoa1510665 Borghaei, 2015, Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer, N Engl J Med, 373, 1627, 10.1056/NEJMoa1507643 Ferris, 2016, Nivolumab for recurrent squamous-cell carcinoma of the head and neck, N Engl J Med, 375, 1856, 10.1056/NEJMoa1602252 Ansell, 2015, PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma, J N Engl J Med, 372, 311, 10.1056/NEJMoa1411087 McDermott, 2015, Pembrolizumab: PD-1 inhibition as a therapeutic strategy in cancer, Drugs Today, 51, 7, 10.1358/dot.2015.51.1.2250387 Martin-Liberal, 2015, Safety of pembrolizumab for the treatment of melanoma, Expert Opin Drug Saf, 14, 957, 10.1517/14740338.2015.1021774 Antonia, 2016, Safety and antitumour activity of durvalumab plus tremelimumab in non-small cell lung cancer: a multicentre, phase 1b study, Lancet Oncol, 17, 299, 10.1016/S1470-2045(15)00544-6 Barone, 2017, FDA approval summary: pembrolizumab for the treatment of patients with unresectable or metastatic melanoma, Clin Cancer Res, 23, 5661, 10.1158/1078-0432.CCR-16-0664 Fashoyin-Aje, 2019, FDA approval summary: pembrolizumab for recurrent locally advanced or metastatic gastric or gastroesophageal junction adenocarcinoma expressing PD-L1, Oncologist, 24, 103, 10.1634/theoncologist.2018-0221 Lim, 2016 Syn, 2017, De-novo and acquired resistance to immune checkpoint targeting, Lancet Oncol, 18, e731, 10.1016/S1470-2045(17)30607-1 Redman, 2018, 719 Liu, 2017, Cardiogenic shock in a patient being treated with atezolizumab for metastatic non-small cell lung cancer, Lung Cancer, 114, 106, 10.1016/j.lungcan.2017.07.028 Riudavets, 2018 Sullivan, 2019, Atezolizumab plus cobimetinib and vemurafenib in BRAF-mutated melanoma patients, Nat Med, 25, 929, 10.1038/s41591-019-0474-7 Hwu, 2016, Preliminary safety and clinical activity of atezolizumab combined with cobimetinib and vemurafenib in BRAF V600-mutant metastatic melanoma, Eur Soc Med Oncol, 27 Bendell, 2016, Clinical activity and safety of cobimetinib (Cobi) and atezolizumab in colorectal cancer (CRC), Am Soc Clin Oncol, 34 Syed, 2017, Durvalumab: first global approval, Drugs, 77, 1369, 10.1007/s40265-017-0782-5 Stewart, 2015, Identification and characterization of MEDI4736, an antagonistic anti–PD-L1 monoclonal antibody, Cancer Immunol Res, 3, 1052, 10.1158/2326-6066.CIR-14-0191 Antonia, 2017, Durvalumab after chemoradiotherapy in stage III non–small-cell lung cancer, N Engl J Med, 377, 1919, 10.1056/NEJMoa1709937 Planchard, 2016, A phase III study of durvalumab (MEDI4736) with or without tremelimumab for previously treated patients with advanced NSCLC: Rationale and Protocol design of the ARCTIC study, Clin Lung Cancer, 17, 232, 10.1016/j.cllc.2016.03.003 Kim, 2017, Avelumab: first global approval, Drugs, 77, 929, 10.1007/s40265-017-0749-6 Ferris, 2018, Rationale for combination of therapeutic antibodies targeting tumor cells and immune checkpoint receptors: Harnessing innate and adaptive immunity through IgG1 isotype immune effector stimulation, Cancer Treat Rev, 63, 48, 10.1016/j.ctrv.2017.11.008 Larroquette, 2019, Which place for avelumab in the management of urothelial carcinoma?, Expert Opin Biol Ther, 863, 10.1080/14712598.2019.1637412 Baker, 2018, Avelumab: a new standard for treating metastatic Merkel cell carcinoma, Expert Rev Anticancer Ther, 18, 319, 10.1080/14737140.2018.1445528