Co-Signaling Molecules in Maternal–Fetal Immunity

Trowsdale, 2006, Mother's little helpers: mechanisms of maternal–fetal tolerance, Nat. Immunol., 7, 241, 10.1038/ni1317 Rai, 2006, Recurrent miscarriage, Lancet, 368, 601, 10.1016/S0140-6736(06)69204-0 Tian, 2016, The PD-1/PD-L1 inhibitory pathway is altered in pre-eclampsia and regulates T cell responses in pre-eclamptic rats, Sci. Rep., 6, 27683, 10.1038/srep27683 Inoue, 2016, Activation of Nod1 signaling induces fetal growth restriction and death through fetal and maternal vasculopathy, J. Immunol., 196, 2779, 10.4049/jimmunol.1500295 Williams, 2012, Inducing tolerance to pregnancy, N. Engl. J. Med., 367, 1159, 10.1056/NEJMcibr1207279 Mekinian, 2016, Unexplained recurrent miscarriage and recurrent implantation failure: is there a place for immunomodulation?, Am. J. Reprod. Immunol., 76, 8, 10.1111/aji.12493 Chen, 2013, Molecular mechanisms of T cell co-stimulation and co-inhibition, Nat. Rev. Immunol., 13, 227, 10.1038/nri3405 Lee, 2013, The influence of T cell Ig mucin-3 signaling on central nervous system autoimmune disease is determined by the effector function of the pathogenic T cells, J. Immunol., 190, 4991, 10.4049/jimmunol.1300083 Koirala, 2016, Immune infiltration and PD-L1 expression in the tumor microenvironment are prognostic in osteosarcoma, Sci. Rep., 6, 30093, 10.1038/srep30093 Shi, 2016, Counter-regulation of rejection activity against human liver grafts by donor PD-L1 and recipient PD-1 interaction, J. Hepatol., 64, 1274, 10.1016/j.jhep.2016.02.034 Hirayama, 2016, Anti-PD-L1 treatment enhances antitumor effect of everolimus in a mouse model of renal cell carcinoma, Cancer Sci., 10.1111/cas.13099 Reck, 2016, Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer, N. Engl. J. Med., 375, 1823, 10.1056/NEJMoa1606774 Poulet, 2016, An evaluation of the impact of PD-1 pathway blockade on reproductive safety of therapeutic PD-1 inhibitors, Birth Defects Res. B Dev. Reprod. Toxicol., 107, 108, 10.1002/bdrb.21176 Wang, 2016, Programmed cell death-1 (PD-1) and T-cell immunoglobulin mucin-3 (TIM-3) regulate CD4+ T cells to induce Type 2 helper T cell (Th2) bias at the maternal–fetal interface, Hum. Reprod., 31, 700, 10.1093/humrep/dew019 Ceeraz, 2013, B7 family checkpoint regulators in immune regulation and disease, Trends Immunol., 34, 556, 10.1016/j.it.2013.07.003 Choi, 2011, ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6, Immunity, 34, 932, 10.1016/j.immuni.2011.03.023 Nabekura, 2014, Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection, Immunity, 40, 225, 10.1016/j.immuni.2013.12.011 Huang, 2015, CEACAM1 regulates TIM-3-mediated tolerance and exhaustion, Nature, 517, 386, 10.1038/nature13848 Fu, 2014, Trophoblasts and decidual stromal cells regulate decidual NK cell functions via interaction between collagen and LAIR-1, Am. J. Reprod. Immunol., 71, 368, 10.1111/aji.12211 Yu, 2008, LPS-induced murine abortions require C5 but not C3, and are prevented by upregulating expression of the CD200 tolerance signaling molecule, Am. J. Reprod. Immunol., 60, 135, 10.1111/j.1600-0897.2008.00605.x Ndhlovu, 2012, TIM-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity, Blood, 119, 3734, 10.1182/blood-2011-11-392951 Yang, 2016, Enhanced expression of T-cell immunoglobulin and mucin domain protein 3 in endothelial cells facilitates intracellular killing of Rickettsia heilongjiangensis, J. Infect. Dis., 213, 71, 10.1093/infdis/jiv463 Burton, 2015, What is the placenta?, Am. J. Obstet. Gynecol., 213 Arck, 2013, Fetomaternal immune cross-talk and its consequences for maternal and offspring's health, Nat. Med., 19, 548, 10.1038/nm.3160 Houser, 2011, Two unique human decidual macrophage populations, J. Immunol., 186, 2633, 10.4049/jimmunol.1003153 Adams, 2010, Dynamic changes in fetal microchimerism in maternal peripheral blood mononuclear cells, CD4+ and CD8+ cells in normal pregnancy, Placenta, 31, 589, 10.1016/j.placenta.2010.04.013 Petroff, 2002, B7 Family Molecules: Novel Immunomodulators at the Maternal–fetal Interface, Placenta, 23, S95, 10.1053/plac.2002.0813 Petroff, 2002, B7 family molecules are favorably positioned at the human maternal–fetal interface, Biol. Reprod., 68, 1496, 10.1095/biolreprod.102.010058 Sayama, 2013, Human decidual macrophages suppress IFN-γ production by T cells through costimulatory B7-H1:PD-1 signaling in early pregnancy, J. Reprod. Immunol., 100, 109, 10.1016/j.jri.2013.08.001 Petroff, 2005, The immunomodulatory proteins B7-DC, B7-H2, and B7-H3 are differentially expressed across gestation in the human placenta, Am. J. Pathol., 167, 465, 10.1016/S0002-9440(10)62990-2 Taglauer, 2008, Expression and function of PDCD1 at the human maternal–fetal interface, Biol. Reprod., 79, 562, 10.1095/biolreprod.107.066324 Nagamatsu, 2011, The regulation of T-cell cytokine production by ICOS-B7H2 interactions at the human fetomaternal interface, Immunol. Cell Biol., 89, 417, 10.1038/icb.2010.101 Galazka, 2009, Changes in the subpopulation of CD25+ CD4+ and FOXP3+ regulatory T cells in decidua with respect to the progression of labor at term and the lack of analogical changes in the subpopulation of suppressive B7-H4 macrophages--a preliminary report, Am. J. Reprod. Immunol., 61, 136, 10.1111/j.1600-0897.2008.00674.x Wang, 2015, TIM-3 protects decidual stromal cells from toll-like receptor-mediated apoptosis and inflammatory reactions and promotes Th2 bias at the maternal–fetal interface, Sci. Rep., 5, 9013, 10.1038/srep09013 Li, 2016, The Galectin-9/TIM-3 pathway is involved in the regulation of NK cell function at the maternal–fetal interface in early pregnancy, Cell Mol. Immunol., 13, 73, 10.1038/cmi.2014.126 Wang, 2015, PD-1 and TIM-3 pathways are associated with regulatory CD8+ T–cell function in decidua and maintenance of normal pregnancy, Cell Death Dis., 6, e1738, 10.1038/cddis.2015.112 Vacca, 2008, Regulatory role of NKp44, NKp46, DNAM-1 and NKG2D receptors in the interaction between NK cells and trophoblast cells. Evidence for divergent functional profiles of decidual versus peripheral NK cells, Int. Immunol., 20, 1395, 10.1093/intimm/dxn105 Wu, 2015, Soluble costimulatory molecule sTim3 regulates the differentiation of Th1 and Th2 in patients with unexplained recurrent spontaneous abortion, Int J. Clin. Exp. Med., 8, 8812 Jin, 2009, The CD4+CD25bright regulatory T cells and CTLA-4 expression in peripheral and decidual lymphocytes are down-regulated in human miscarriage, Clin. Immunol., 133, 402, 10.1016/j.clim.2009.08.009 Huang, 2016, Association of peripheral blood dendritic cells with recurrent pregnancy loss: a case-controlled study, Am. J. Reprod. Immunol., 76, 326, 10.1111/aji.12550 Tilburgs, 2008, Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy, J. Immunol., 180, 5737, 10.4049/jimmunol.180.8.5737 Tilburgs, 2010, Human decidual tissue contains differentiated CD8+ effector-memory T cells with unique properties, J. Immunol., 185, 4470, 10.4049/jimmunol.0903597 Clark, 2003, Placental trophoblast from successful human pregnancies expresses the tolerance signaling molecule, CD200 (OX-2), Am. J. Reprod. Immunol., 50, 187, 10.1034/j.1600-0897.2003.00086.x Nagamatsu, 2009, Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions, Hum. Reprod., 24, 3160, 10.1093/humrep/dep308 Fu, 2014, Trophoblasts and decidual stromal cells regulate dNK functions via interaction between collagen and LAIR-1, Am. J. Reprod. Immunol., 71, 368, 10.1111/aji.12211 Sun, 2016, TIM-3 is upregulated in NK cells during early pregnancy and inhibits NK cytotoxicity toward trophoblast in galectin- 9 dependent pathway, PLoS One, 11, e147186 Markel, 2002, Pivotal role of CEACAM1 protein in the inhibition of activated decidual lymphocyte functions, J. Clin. Invest., 110, 943, 10.1172/JCI0215643 Abumaree, 2012, Trophoblast debris modulates the expression of immune proteins in macrophages: a key to maternal tolerance of the fetal allograft?, J. Reprod. Immunol., 94, 131, 10.1016/j.jri.2012.03.488 Zhao, 2009, Human pregnancy up-regulates TIM-3 in innate immune cells for systemic immunity, J. Immunol., 182, 6618, 10.4049/jimmunol.0803876 James, 2005, Cytotrophoblast differentiation in the first trimester of pregnancy: evidence for separate progenitors of extravillous trophoblasts and syncytiotrophoblast, Reproduction, 130, 95, 10.1530/rep.1.00723 Zhang, 2011, Natural killer cell-triggered vascular transformation: maternal care before birth?, Cell Mol. Immunol., 8, 1, 10.1038/cmi.2010.38 Bamberger, 2000, The adhesion molecule CEACAM1 (CD66a, C-CAM, BGP) is specifically expressed by the extravillous intermediate trophoblast, Am. J. Pathol., 156, 1165, 10.1016/S0002-9440(10)64985-1 Jin, 2005, Blockade of CD80 and CD86 at the time of implantation inhibits maternal rejection to the allogeneic fetus in abortion-prone matings, J. Reprod. Immunol., 65, 133, 10.1016/j.jri.2004.08.009 Zhu, 2005, Blockade of CD86 Signaling Facilitates a Th2 Bias at the Maternal–fetal Interface and Expands Peripheral CD4+CD25+ Regulatory T Cells to Rescue Abortion-Prone Fetuses, Biol. Reprod., 72, 338, 10.1095/biolreprod.104.034108 Li, 2013, Adenovirus mediated CTLA4Ig transgene therapy alleviates abortion by inhibiting spleen lymphocyte proliferation and regulating apoptosis in the feto-placental unit, J. Reprod. Immunol., 97, 167, 10.1016/j.jri.2013.01.002 Jin, 2004, Adoptive transfer of paternal antigen-hyporesponsive T cells induces maternal tolerance to the allogeneic fetus in abortion-prone matings, J. Immunol., 173, 3612, 10.4049/jimmunol.173.6.3612 Gleria, 2005, A critical role for the programmed death ligand 1 in fetomaternal tolerance, J. Exp. Med., 202, 231, 10.1084/jem.20050019 Habicht, 2007, A link between PDL1 and T regulatory cells in fetomaternal tolerance, J. Immunol., 179, 5211, 10.4049/jimmunol.179.8.5211 Wafula, 2009, PD-1 but not CTLA-4 blockage abrogates the protective effect of regulatory T cells in a pregnancy murine model, Am. J. Reprod. Immunol., 62, 283, 10.1111/j.1600-0897.2009.00737.x D’Addio, 2011, The Link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance, J. Immunol., 187, 4530, 10.4049/jimmunol.1002031 Taglauer, 2009, Maternal PD-1 regulates accumulation of fetal antigen-specific CD8+ T cells in pregnancy, J. Reprod. Immunol., 80, 12, 10.1016/j.jri.2008.12.001 Riella, 2013, B7h (ICOS-L) maintains tolerance at the fetomaternal interface, Am. J. Pathol., 182, 2204, 10.1016/j.ajpath.2013.02.014 Chabtini, 2013, TIM-3 regulates innate immune cells to induce fetomaternal tolerance, J. Immunol., 190, 88, 10.4049/jimmunol.1202176 Gupta, 2012, Allograft rejection is restrained by short-lived TIM-3+PD-1+Foxp3+ Tregs, J. Clin. Invest., 122, 2395, 10.1172/JCI45138 Hofmeyer, 2011, The PD-1/PD-L1 (B7-H1) pathway in chronic infection–induced cytotoxic T lymphocyte exhaustion, J. Biomed. Biotechnol., 2011, 451694, 10.1155/2011/451694 Jin, 2010, Cooperation of TIM-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection, Proc. Natl. Acad. Sci. U.S.A., 107, 14733, 10.1073/pnas.1009731107 Takano, 2016, An increased number of PD-1+ and TIM-3+ CD8+ T cells is involved in immune evasion in gastric cancer, Surg. Today, 46, 1341, 10.1007/s00595-016-1305-9 Fourcade, 2010, Upregulation of TIM-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients, J. Exp. Med., 207, 2175, 10.1084/jem.20100637 Sakuishi, 2010, Targeting TIM-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity, J. Exp. Med., 207, 2187, 10.1084/jem.20100643 Wherry, 2011, T cell exhaustion, Nat. Immunol., 12, 492, 10.1038/ni.2035 Ghebeh, 2008, FOXP3+ Tregs and B7-H1+/PD-1+ T lymphocytes co-infiltrate the tumor tissues of high–risk breast cancer patients: Implication for immunotherapy, BMC Cancer, 8, 57, 10.1186/1471-2407-8-57 Khoja, 2016, Patterns of response to anti-PD-1 treatment: an exploratory comparison of four radiological response criteria and associations with overall survival in metastatic melanoma patients, Br. J. Cancer, 115, 1186, 10.1038/bjc.2016.308 Ye, 2016, Synergistic transcutaneous immunotherapy enhances antitumor immune responses through delivery of checkpoint inhibitors, ACS Nano, 10, 8956, 10.1021/acsnano.6b04989 Baghdadi, 2014, The impact of the TIM gene family on tumor immunity and immunosuppression, Cell Mol. Immunol., 11, 41, 10.1038/cmi.2013.57 Sehrawat, 2010, Galectin-9/TIM-3 interaction regulates virus–specific primary and memory CD8 T cell response, PLoS Pathog., 6, e1000882, 10.1371/journal.ppat.1000882 Jayaraman, 2010, Tim3 binding to galectin-9 stimulates antimicrobial immunity, J. Exp. Med., 207, 2343, 10.1084/jem.20100687 Li, 2012, TIM-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma, Hepatology, 56, 1342, 10.1002/hep.25777 Cao, 2013, TIM–3 expression in cervical cancer promotes tumor metastasis, PLoS One, 8, e53834, 10.1371/journal.pone.0053834 Yang, 2012, IL-12 upregulatesTIM-3 expression and induces T cell exhaustion in patients with follicular B cell non-Hodgkin lymphoma, J. Clin. Invest., 122, 1271, 10.1172/JCI59806 Zhu, 2016, TIM-3 identifies exhausted follicular helper T cells in breast cancer patients, Immunobiology, 221, 986, 10.1016/j.imbio.2016.04.005 Ozkazanc, 2016, Functional exhaustion of CD4+ T cells induced by co-stimulatory signals from myeloid leukaemia cells, Immunology, 149, 460, 10.1111/imm.12665 Kim, 2016, Combination therapy with anti-PD-1, anti-TIM–3, and focal radiation results in regression of murine gliomas, Clin. Cancer Res. Liu, 2016, Targeting PD-1 and TIM-3 pathways to reverse CD8 T-cell exhaustion and enhance ex vivo T-cell responses to autologous dendritic/tumor vaccines, J. Immunother., 39, 171, 10.1097/CJI.0000000000000122 Wu, 2014, Alteration of Th17 and Treg cells in patients with unexplained recurrent spontaneous abortion before and after lymphocyte immunization therapy, Reprod. Biol. Endocrinol., 12, 74, 10.1186/1477-7827-12-74 Ning, 2016, The role of decidual macrophages during normal and pathological pregnancy, Am. J. Reprod. Immunol., 75, 298, 10.1111/aji.12477 O’Neill, 2016, A metabolic roadblock in inflammatory macrophages, Cell Rep., 17, 625, 10.1016/j.celrep.2016.09.085 Guo, 2010, Thymic stromal lymphopoietin from trophoblasts induces dendritic cell-mediated regulatory TH2 bias in the decidua during early gestation in humans, Blood, 116, 2061, 10.1182/blood-2009-11-252940 Du, 2014, Embryonic trophoblasts induce decidual regulatory T cell differentiation and maternal-fetal tolerance through thymic stromal lymphopoietin instructing dendritic cells, J. Immunol., 192, 1502, 10.4049/jimmunol.1203425 Triggianese, 2016, Innate immune system at the maternal–fetal interface: mechanisms of disease and targets of therapy in pregnancy syndromes, Am. J. Reprod. Immunol., 76, 245, 10.1111/aji.12509 Soldevilla, 2016, MRP1-CD28 bi-specific oligonucleotide aptamers: target costimulation to drug-resistant melanoma cancer stem cells, Oncotarget, 7, 23182, 10.18632/oncotarget.8095 Gao, 2016, Loss of IFN-gamma pathway genes in tumor cells as a mechanism of resistance to anti-CTLA-4 therapy, Cell, 167, 397, 10.1016/j.cell.2016.08.069 Ahrends, 2016, CD27 agonism plus PD-1 blockade recapitulates CD4+ T-cell help in therapeutic anticancer vaccination, Cancer Res., 76, 2921, 10.1158/0008-5472.CAN-15-3130 Ragonnaud, 2016, An adenoviral cancer vaccine co-encoding a tumor associated antigen together with secreted 4-1BBL leads to delayed tumor progression, Vaccine, 34, 2147, 10.1016/j.vaccine.2015.06.087