Role of the immunosuppressive microenvironment in immunotherapy

Hanahan, 2011, Hallmarks of cancer: The next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013

Boon, 1997, Cancer tumor antigens, Curr Opin Immunol, 9, 681, 10.1016/S0952-7915(97)80049-0

Dudley, 2003, Adoptive-cell-transfer therapy for the treatment of patients with cancer, Nat Rev Cancer, 3, 666, 10.1038/nrc1167

McCarthy, 2006, The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas, Iowa Orthop J, 26, 154

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

Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466

Hamid, 2013, Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma, N Engl J Med, 369, 134, 10.1056/NEJMoa1305133

Vanpouille-Box, 2017, Trial watch: Immune checkpoint blockers for cancer therapy, Oncoimmunology, 6, e1373237, 10.1080/2162402X.2017.1373237

Herbst, 2014, Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients, Nature, 515, 563, 10.1038/nature14011

Tumeh, 2014, PD-1 blockade induces responses by inhibiting adaptive immune resistance, Nature, 515, 568, 10.1038/nature13954

Crittenden, 2018, Tumor cure by radiation therapy and checkpoint inhibitors depends on pre-existing immunity, Sci Rep, 8, 7012, 10.1038/s41598-018-25482-w

Whiteside, 2008, The tumor microenvironment and its role in promoting tumor growth, Oncogene, 27, 5904, 10.1038/onc.2008.271

Zou, 2005, Immunosuppressive networks in the tumour environment and their therapeutic relevance, Nat Rev Cancer, 5, 263, 10.1038/nrc1586

Vonderheide, 2018, The immune revolution: A case for priming, not checkpoint, Cancer Cell, 33, 563, 10.1016/j.ccell.2018.03.008

Thommen, 2018, T cell dysfunction in cancer, Cancer Cell, 33, 547, 10.1016/j.ccell.2018.03.012

Gough, 2009, Combination approaches to immunotherapy: The radiotherapy example, Immunotherapy, 1, 1025, 10.2217/imt.09.64

Gough, 2012, Immune system plays an important role in the success and failure of conventional cancer therapy, Immunotherapy, 4, 125, 10.2217/imt.11.157

Apetoh, 2007, The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy, Immunol Rev, 220, 47, 10.1111/j.1600-065X.2007.00573.x

Lee, 2009, Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment, Blood, 114, 589, 10.1182/blood-2009-02-206870

Lugade, 2005, Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor, J Immunol, 174, 7516, 10.4049/jimmunol.174.12.7516

Chakraborty, 2004, External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing, Cancer Res, 64, 4328, 10.1158/0008-5472.CAN-04-0073

Wennerberg, 2017, Barriers to radiation-induced in situ tumor vaccination, Front Immunol, 8, 229, 10.3389/fimmu.2017.00229

Vesely, 2011, Natural innate and adaptive immunity to cancer, Annu Rev Immunol, 29, 235, 10.1146/annurev-immunol-031210-101324

Vajdic, 2006, Cancer incidence before and after kidney transplantation, JAMA, 296, 2823, 10.1001/jama.296.23.2823

Broz, 2014, Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity, Cancer Cell, 26, 638, 10.1016/j.ccell.2014.09.007

Demoulin, 2013, Tumor microenvironment converts plasmacytoid dendritic cells into immunosuppressive/tolerogenic cells: Insight into the molecular mechanisms, J Leukoc Biol, 93, 343, 10.1189/jlb.0812397

Chen, 2008, The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation, J Immunol, 181, 5396, 10.4049/jimmunol.181.8.5396

den Haan, 2000, CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo, J Exp Med, 192, 1685, 10.1084/jem.192.12.1685

Fuertes, 2011, Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells, J Exp Med, 208, 2005, 10.1084/jem.20101159

Hildner, 2008, Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity, Science, 322, 1097, 10.1126/science.1164206

Kim, 2007, Cancer immunoediting from immune surveillance to immune escape, Immunology, 121, 1, 10.1111/j.1365-2567.2007.02587.x

Mihm, 1996, Tumor infiltrating lymphocytes in lymph node melanoma metastases: A histopathologic prognostic indicator and an expression of local immune response, Lab Invest, 74, 43

Miescher, 1987, Clonal and frequency analyses of tumor-infiltrating T lymphocytes from human solid tumors, J Immunol, 138, 4004, 10.4049/jimmunol.138.11.4004

Fischer, 2007, Inhibitory effect of tumor cell-derived lactic acid on human T cells, Blood, 109, 3812, 10.1182/blood-2006-07-035972

Vander Heiden, 2009, Understanding the Warburg effect: The metabolic requirements of cell proliferation, Science, 324, 1029, 10.1126/science.1160809

Zhang, 2016, Starved and asphyxiated: How can CD8(+) T cells within a tumor microenvironment prevent tumor progression, Front Immunol, 7, 32, 10.3389/fimmu.2016.00032

Topalian, 2015, Immune checkpoint blockade: A common denominator approach to cancer therapy, Cancer Cell, 27, 450, 10.1016/j.ccell.2015.03.001

Tosolini, 2011, Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer, Cancer Res, 71, 1263, 10.1158/0008-5472.CAN-10-2907

Sakaguchi, 1995, Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases, J Immunol, 155, 1151, 10.4049/jimmunol.155.3.1151

Budhu, 2017, Blockade of surface-bound TGF-beta on regulatory T cells abrogates suppression of effector T cell function in the tumor microenvironment, Sci Signal., 10, 494, 10.1126/scisignal.aak9702

Nishikawa, 2010, Regulatory T cells in tumor immunity, Int J Cancer, 127, 759, 10.1002/ijc.25429

Shang, 2015, Prognostic value of tumor-infiltrating FoxP3+ regulatory T cells in cancers: A systematic review and meta-analysis, Sci Rep, 5, 15179, 10.1038/srep15179

Feng, 2017, Multiparametric immune profiling in HPV- oral squamous cell cancer, JCI Insight, 2, 10.1172/jci.insight.93652

Ito, 2006, Tumor-derived TGFbeta-1 induces dendritic cell apoptosis in the sentinel lymph node, J Immunol, 176, 5637, 10.4049/jimmunol.176.9.5637

Weber, 2005, Transforming growth factor-beta1 immobilises dendritic cells within skin tumours and facilitates tumour escape from the immune system, Cancer Immunol Immunother, 54, 898, 10.1007/s00262-004-0652-3

Byrne, 2008, TGFbeta is responsible for skin tumour infiltration by macrophages enabling the tumours to escape immune destruction, Immunol Cell Biol, 86, 92, 10.1038/sj.icb.7100116

Thomas, 2005, TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance, Cancer Cell, 8, 369, 10.1016/j.ccr.2005.10.012

Young, 2014, TGFbeta inhibition prior to hypofractionated radiation enhances efficacy in preclinical models, Cancer Immunol Res, 2, 1011, 10.1158/2326-6066.CIR-13-0207

Vanpouille-Box, 2015, TGFbeta is a master regulator of radiation therapy-induced antitumor immunity, Cancer Res, 75, 2232, 10.1158/0008-5472.CAN-14-3511

DeNardo, 2009, CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages, Cancer Cell, 16, 91, 10.1016/j.ccr.2009.06.018

Kuang, 2009, Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1, J Exp Med, 206, 1327, 10.1084/jem.20082173

Rodriguez, 2002, Regulation of T cell receptor CD3zeta chain expression by L-arginine, J Biol Chem, 277, 21123, 10.1074/jbc.M110675200

Crittenden, 2014, Expression of arginase I in myeloid cells limits control of residual disease after radiation therapy of tumors in mice, Radiat Res, 182, 182, 10.1667/RR13493.1

Ravishankar, 2012, Tolerance to apoptotic cells is regulated by indoleamine 2,3-dioxygenase, Proc Natl Acad Sci U S A, 109, 3909, 10.1073/pnas.1117736109

Munn, 2005, GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase, Immunity, 22, 633, 10.1016/j.immuni.2005.03.013

Mezrich, 2010, An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells, J Immunol, 185, 3190, 10.4049/jimmunol.0903670

Holmgaard, 2015, Tumor-expressed IDO recruits and activates MDSCs in a Treg-dependent manner, Cell Rep, 13, 412, 10.1016/j.celrep.2015.08.077

Lob, 2009, Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees?, Nat Rev Cancer, 9, 445, 10.1038/nrc2639

Holmgaard, 2013, Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4, J Exp Med, 210, 1389, 10.1084/jem.20130066

Chen, 2005, Tumor-associated macrophages: The double-edged sword in cancer progression, J Clin Oncol, 23, 953, 10.1200/JCO.2005.12.172

Crittenden, 2016, Mertk on tumor macrophages is a therapeutic target to prevent tumor recurrence following radiation therapy, Oncotarget, 7, 78653, 10.18632/oncotarget.11823

Gough, 2013, The impact of the myeloid response to radiation therapy, Clin Dev Immunol, 2013, 281958, 10.1155/2013/281958

Xu, 2013, CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer, Cancer Res, 73, 2782, 10.1158/0008-5472.CAN-12-3981

Kalbasi, 2017, Tumor-derived CCL2 mediates resistance to radiotherapy in pancreatic ductal adenocarcinoma, Clin Cancer Res, 23, 137, 10.1158/1078-0432.CCR-16-0870

Ruffell, 2012, Differential macrophage programming in the tumor microenvironment, Trends Immunol, 33, 119, 10.1016/j.it.2011.12.001

Poon, 2014, Apoptotic cell clearance: Basic biology and therapeutic potential, Nat Rev Immunol, 14, 166, 10.1038/nri3607

Jinushi, 2009, Milk fat globule epidermal growth factor-8 blockade triggers tumor destruction through coordinated cell-autonomous and immune-mediated mechanisms, J Exp Med, 206, 1317, 10.1084/jem.20082614

Apetoh, 2008, Molecular interactions between dying tumor cells and the innate immune system determine the efficacy of conventional anticancer therapies, Cancer Res, 68, 4026, 10.1158/0008-5472.CAN-08-0427

Green, 2009, Immunogenic and tolerogenic cell death, Nat Rev Immunol, 9, 353, 10.1038/nri2545

Vanpouille-Box, 2017, DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity, Nat Commun, 8, 15618, 10.1038/ncomms15618

Tormoen, 2017, The TAM family as a therapeutic target in combination with radiation therapy, Emerging Topics Life Sci, 1, 493, 10.1042/ETLS20170066

Buque, 2016, Trial watch-small molecules targeting the immunological tumor microenvironment for cancer therapy, Oncoimmunology, 5, e1149674, 10.1080/2162402X.2016.1149674

Vacchelli, 2016, Trial watch: Immunotherapy plus radiation therapy for oncological indications, Oncoimmunology, 5, e1214790, 10.1080/2162402X.2016.1214790

Wing, 2008, CTLA-4 control over Foxp3+ regulatory T cell function, Science, 322, 271, 10.1126/science.1160062

Reeves, 2017, Antigen processing and immune regulation in the response to tumours, Immunology, 150, 16, 10.1111/imm.12675

Antonioli, 2013, Immunity, inflammation and cancer: A leading role for adenosine, Nat Rev Cancer, 13, 842, 10.1038/nrc3613

Mariathasan, 2018, TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells, Nature, 554, 544, 10.1038/nature25501

Fukumura, 2018, Enhancing cancer immunotherapy using antiangiogenics: Opportunities and challenges, Nat Rev Clin Oncol, 15, 325, 10.1038/nrclinonc.2018.29

Khan, 2018, Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa, Nat Rev Clin Oncol, 15, 310, 10.1038/nrclinonc.2018.9

Moore, 2001, Interleukin-10 and the interleukin-10 receptor, Ann Rev Immunol, 19, 683, 10.1146/annurev.immunol.19.1.683

Fiorentino, 1991, IL-10 inhibits cytokine production by activated macrophages, J Immunol, 147, 3815, 10.4049/jimmunol.147.11.3815

Dokka, 2001, Interleukin-10-mediated inhibition of free radical generation in macrophages, Am J Physiol Lung Cell Mol Physiol, 280, L1196, 10.1152/ajplung.2001.280.6.L1196

Steinbrink, 2002, CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity, Blood, 99, 2468, 10.1182/blood.V99.7.2468

Uyttenhove, 2003, Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase, Nat Med, 9, 1269, 10.1038/nm934

Kobie, 2006, T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5'-adenosine monophosphate to adenosine, J Immunol, 177, 6780, 10.4049/jimmunol.177.10.6780

Saze, 2013, Adenosine production by human B cells and B cell-mediated suppression of activated T cells, Blood, 122, 9, 10.1182/blood-2013-02-482406

Chang, 2013, Posttranscriptional control of T cell effector function by aerobic glycolysis, Cell, 153, 1239, 10.1016/j.cell.2013.05.016

Lee, 2010, Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis, Carcinogenesis, 31, 427, 10.1093/carcin/bgp326

Singer, 2011, Suppression of T-cell responses by tumor metabolites, Cancer Immunol Immunother, 60, 425, 10.1007/s00262-010-0967-1

Rodriguez, 2017, Arginine metabolism in myeloid cells shapes innate and adaptive immunity, Front Immunol, 8, 93, 10.3389/fimmu.2017.00093

Holt, 2011, Prostaglandin E(2) (PGE (2)) suppresses natural killer cell function primarily through the PGE(2) receptor EP4, Cancer Immunol Immunother, 60, 1577, 10.1007/s00262-011-1064-9

Martinet, 2010, PGE2 inhibits natural killer and gamma delta T cell cytotoxicity triggered by NKR and TCR through a cAMP-mediated PKA type I-dependent signaling, Biochem Pharmacol, 80, 838, 10.1016/j.bcp.2010.05.002

Kalinski, 2012, Regulation of immune responses by prostaglandin E2, J Immunol, 188, 21, 10.4049/jimmunol.1101029

Mao, 2014, Inhibition of tumor-derived prostaglandin-e2 blocks the induction of myeloid-derived suppressor cells and recovers natural killer cell activity, Clin Cancer Res, 20, 4096, 10.1158/1078-0432.CCR-14-0635