Regulatory T cells in cancer immunotherapy

van der Bruggen, 1991, A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma, Science, 254, 1643, 10.1126/science.1840703 Kawakami, 1997, Human tumor antigens recognized by T-cells, Immunol Res, 16, 313, 10.1007/BF02786397 Scanlan, 2002, Cancer/testis antigens: an expanding family of targets for cancer immunotherapy, Immunol Rev, 188, 22, 10.1034/j.1600-065X.2002.18803.x Boon, 2006, Human T cell responses against melanoma, Annu Rev Immunol, 24, 175, 10.1146/annurev.immunol.24.021605.090733 Rosenberg, 2004, Cancer immunotherapy: moving beyond current vaccines, Nat Med, 10, 909, 10.1038/nm1100 Gnjatic, 2006, NY-ESO-1: review of an immunogenic tumor antigen, Adv Cancer Res, 95, 1, 10.1016/S0065-230X(06)95001-5 Dougan, 2009, Immune therapy for cancer, Annu Rev Immunol, 27, 83, 10.1146/annurev.immunol.021908.132544 Zou, 2006, Regulatory T cells, tumour immunity and immunotherapy, Nat Rev Immunol, 6, 295, 10.1038/nri1806 Nishikawa, 2010, Regulatory T cells in tumor immunity, Int J Cancer, 127, 759 Sharma, 2011, Novel cancer immunotherapy agents with survival benefit: recent successes and next steps, Nat Rev Cancer, 11, 805, 10.1038/nrc3153 Wing, 2010, Regulatory T cells exert checks and balances on self tolerance and autoimmunity, Nat Immunol, 11, 7, 10.1038/ni.1818 Shimizu, 1999, Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity, J Immunol, 163, 5211, 10.4049/jimmunol.163.10.5211 Sakaguchi, 2010, FOXP3+ regulatory T cells in the human immune system, Nat Rev Immunol, 10, 490, 10.1038/nri2785 Miyara, 2009, Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor, Immunity, 30, 899, 10.1016/j.immuni.2009.03.019 Curiel, 2004, Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival, Nat Med, 10, 942, 10.1038/nm1093 Sato, 2005, Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer, Proc Natl Acad Sci U S A, 102, 18538, 10.1073/pnas.0509182102 Alvaro, 2005, Outcome in Hodgkin's lymphoma can be predicted from the presence of accompanying cytotoxic and regulatory T cells, Clin Cancer Res, 11, 1467, 10.1158/1078-0432.CCR-04-1869 Badoual, 2006, Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers, Clin Cancer Res, 12, 465, 10.1158/1078-0432.CCR-05-1886 Salama, 2009, Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer, J Clin Oncol, 27, 186, 10.1200/JCO.2008.18.7229 Sugiyama, 2013, Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans, Proc Natl Acad Sci U S A, 110, 17945, 10.1073/pnas.1316796110 Faget, 2011, Early detection of tumor cells by innate immune cells leads to Treg recruitment through CCL22 production by tumor cells, Cancer Res, 71, 6143, 10.1158/0008-5472.CAN-11-0573 Facciabene, 2011, Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and Treg cells, Nature, 475, 226, 10.1038/nature10169 Redjimi, 2012, CXCR3+ T regulatory cells selectively accumulate in human ovarian carcinomas to limit type I immunity, Cancer Res, 72, 4351, 10.1158/0008-5472.CAN-12-0579 Wang, 2004, Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy, Immunity, 20, 107, 10.1016/S1074-7613(03)00359-5 Vence, 2007, Circulating tumor antigen-specific regulatory T cells in patients with metastatic melanoma, Proc Natl Acad Sci U S A, 104, 20884, 10.1073/pnas.0710557105 Lehe, 2008, The Wilms’ tumor antigen is a novel target for human CD4+ regulatory T cells: implications for immunotherapy, Cancer Res, 68, 6350, 10.1158/0008-5472.CAN-08-0050 Bonertz, 2009, Antigen-specific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma, J Clin Invest, 119, 3311 Fourcade, 2010, Human tumor antigen-specific helper and regulatory T cells share common epitope specificity but exhibit distinct T cell repertoire, J Immunol, 184, 6709, 10.4049/jimmunol.0903612 Nishikawa, 2005, Definition of target antigens for naturally occurring CD4+CD25+ regulatory T cells, J Exp Med, 201, 681, 10.1084/jem.20041959 Jordan, 2001, Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide, Nat Immunol, 2, 301, 10.1038/86302 Sakaguchi, 2004, Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses, Annu Rev Immunol, 22, 531, 10.1146/annurev.immunol.21.120601.141122 Francois, 2009, The CD4+ T-cell response of melanoma patients to a MAGE-A3 peptide vaccine involves potential regulatory T cells, Cancer Res, 69, 4335, 10.1158/0008-5472.CAN-08-3726 Chen, 1997, A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening, Proc Natl Acad Sci U S A, 94, 1914, 10.1073/pnas.94.5.1914 Danke, 2004, Autoreactive T cells in healthy individuals, J Immunol, 172, 5967, 10.4049/jimmunol.172.10.5967 Nishikawa, 2005, CD4+CD25+ regulatory T cells control the induction of antigen-specific CD4+ helper T cell responses in cancer patients, Blood, 106, 1008, 10.1182/blood-2005-02-0607 Nishikawa, 2006, Influence of CD4+CD25+ regulatory T cells on low/high-avidity CD4+ T cells following peptide vaccination, J Immunol, 176, 6340, 10.4049/jimmunol.176.10.6340 Sakaguchi, 1995, Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases, J Immunol, 155, 1151, 10.4049/jimmunol.155.3.1151 Onizuka, 1999, Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor α) monoclonal antibody, Cancer Res, 59, 3128 Attia, 2005, Inability of a fusion protein of IL-2 and diphtheria toxin (Denileukin Diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma, J Immunother, 28, 582, 10.1097/01.cji.0000175468.19742.10 Dannull, 2005, Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells, J Clin Invest, 115, 3623, 10.1172/JCI25947 Jacobs, 2010, Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients, Clin Cancer Res, 16, 5067, 10.1158/1078-0432.CCR-10-1757 Rech, 2012, CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients, Sci Transl Med, 4, 134ra162, 10.1126/scitranslmed.3003330 Williams, 2007, Effector and memory CTL differentiation, Annu Rev Immunol, 25, 171, 10.1146/annurev.immunol.25.022106.141548 Shimizu, 2002, Stimulation of CD25+CD4+ regulatory T cells through GITR breaks immunological self-tolerance, Nat Immunol, 3, 135, 10.1038/ni759 Ko, 2005, Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+CD25+CD4+ regulatory T cells, J Exp Med, 202, 885, 10.1084/jem.20050940 Mitsui, 2010, Two distinct mechanisms of augmented antitumor activity by modulation of immunostimulatory/inhibitory signals, Clin Cancer Res, 16, 2781, 10.1158/1078-0432.CCR-09-3243 Valzasina, 2005, 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, 105, 2845, 10.1182/blood-2004-07-2959 Piconese, 2008, OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection, J Exp Med, 205, 825, 10.1084/jem.20071341 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 Leach, 1996, Enhancement of antitumor immunity by CTLA-4 blockade, Science, 271, 1734, 10.1126/science.271.5256.1734 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 Bulliard, 2013, Activating Fcγ receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies, J Exp Med, 210, 1685, 10.1084/jem.20130573 Mark, 2013, Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regualtory T cells, Cancer Immunol Res, 1, 32, 10.1158/2326-6066.CIR-13-0013 Simpson, 2013, Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma, J Exp Med, 210, 1695, 10.1084/jem.20130579 Hodi, 2008, Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients, Proc Natl Acad Sci U S A, 105, 3005, 10.1073/pnas.0712237105 Liakou, 2008, CTLA-4 blockade increases IFNγ-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients, Proc Natl Acad Sci U S A, 105, 14987, 10.1073/pnas.0806075105 Wing, 2008, CTLA-4 control over Foxp3+ regulatory T cell function, Science, 322, 271, 10.1126/science.1160062 Ise, 2010, CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsic mechanisms, Nat Immunol, 11, 129, 10.1038/ni.1835 Brahmer, 2012, Safety and activity of anti-PD-L1 antibody in patients with advanced cancer, N Engl J Med, 366, 2455, 10.1056/NEJMoa1200694 Topalian, 2012, Safety, activity, and immune correlates of anti-PD-1 antibody in cancer, N Engl J Med, 366, 2443, 10.1056/NEJMoa1200690 Hamid, 2013, Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma, N Engl J Med, 369, 134, 10.1056/NEJMoa1305133 Kryczek, 2009, FOXP3 defines regulatory T cells in human tumor and autoimmune disease, Cancer Res, 69, 3995, 10.1158/0008-5472.CAN-08-3804 Berger, 2008, Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies, Clin Cancer Res, 14, 3044, 10.1158/1078-0432.CCR-07-4079 Beyer, 2005, Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine, Blood, 106, 2018, 10.1182/blood-2005-02-0642 Walter, 2011, Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival, Nat Med, 17, 1094