Inflammation, NK cells and implantation: friend and foe (the good, the bad and the ugly?): replacing placental viviparity in an evolutionary perspective

Abbondanzo, 1996, Reproduction in mice lacking a functional type 1 IL-1 receptor, Endocrinology, 137, 3598, 10.1210/en.137.8.3598 Adelman, 2004, The natural antibody repertoire of sharks and humans recognizes the potential universe of antigens, Protein J., 23, 103, 10.1023/B:JOPC.0000020077.73751.76 Adelstein, 1990, Suppressor T-cell memory, Curr. Top. Microbiol. Immunol., 159, 123, 10.1007/978-3-642-75244-5_8 Ahmed, 2010, A new mouse model to explore therapies for preeclampsia, PLoS ONE, 5, e13663, 10.1371/journal.pone.0013663 Allen, 1997, Interspecific and extraspecific pregnancies in equids: anything goes, J. Hered., 88, 384, 10.1093/oxfordjournals.jhered.a023123 Allen, 1986, Successful application of immunotherapy to a model of pregnancy failure in equids, 253 Allison, 2009, Recurrent first trimester pregnancy loss: revised definitions and novel causes, Curr. Opin. Endocrinol. Diab. Obes., 16, 446, 10.1097/MED.0b013e3283327fc5 Altincicek, 2009, Identification of immune inducible genes from the velvet worm Epiperipatus biolleyi (Onychophora), Dev. Comp. Immunol., 32, 1416, 10.1016/j.dci.2008.06.004 Arceci, 1989, The temporal expression and localisation of colony stimulating factor (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1 regulated placental development, Proc. Natl. Acad. Sci. U.S.A., 86, 8818, 10.1073/pnas.86.22.8818 Basak, 2002, Expression of pro-inflammatory cytokines in mouse blastocysts during implantation: modulation by steroid hormones, Am. J. Reprod. Immunol., 47, 2, 10.1034/j.1600-0897.2002.1o047.x Bazer, 2009, Comparative aspects of implantation, Reproduction, 138, 195, 10.1530/REP-09-0158 Blackburn, 2012, Invasive implantation and intimate placental associations in a placentotrophic African lizard, Trachylepis ivensi (scincidae), J. Morphol., 273, 137, 10.1002/jmor.11011 Bobé, 1989, Immunogenetic studies of spontaneous abortion in mice. III. Non-H-2 antigens and gestation, J. Immunogenet., 16, 223, 10.1111/j.1744-313X.1989.tb00465.x Bobé, 1987, Immunogenetic studies of spontaneous abortions in mice, 252 Chaouat, 2003, Innately moving away from the Th1/Th2 paradigm in pregnancy, Clin. Exp. Immunol., 131, 393, 10.1046/j.1365-2249.2003.02100.x Chaouat, 1985, Immunogenetic studies of spontaneous abortion in mice. Preimmunisation of the mother with allogeneic spleen cells, J. Immunol., 134, 2966, 10.4049/jimmunol.134.5.2966 Chaouat, 1995, Il-10 prevents inflammatory cytokine-mediated foetal death and is inducible by tau interferon, J. Immunol., 152, 2411 Chaouat, 1997, Immune suppression and Th1/Th2 balance in pregnancy revisited: a (very) personal tribute to Tom Wegmann, Am. J. Reprod. Immunol., 37, 427, 10.1111/j.1600-0897.1997.tb00255.x Chaouat, 2002, A brief review of recent data on some cytokine expressions at the materno–foetal interface which might challenge the classical Th1/Th2 dichotomy, J. Reprod. Immunol., 53, 241, 10.1016/S0165-0378(01)00119-X Chaouat, 2004, Th1/Th2 paradigm in pregnancy: paradigm lost? Cytokines in pregnancy/early abortion: reexamining the TH1/TH2 paradigm, Int. Arch. Allergy Immunol., 134, 93, 10.1159/000074300 Chaouat, 2005, Fourth international workshop on immunology of pre-eclampsia, December 2004, Reunion, France, J. Reprod. Immunol., 67, 103, 10.1016/j.jri.2005.09.004 Chaouat, 2005, Fourth International Workshop on immunology of pre-eclampsia, December 2004, Reunion, France, J. Reprod. Immunol., 67, 103, 10.1016/j.jri.2005.09.004 Chaouat, 2009, Early regulators in abortion and implications for a preeclampsia model, J. Reprod. Immunol., 82, 131, 10.1016/j.jri.2009.08.004 Chaouat, 2011, An insight into normal and pathological pregnancies using large-scale microarrays: lessons from microarrays, J. Reprod. Immunol., 89, 163, 10.1016/j.jri.2010.12.006 Chaouat, G., Rahmati, M., Bensussan, A., Clark, D.A. Seminal plasma peptides determine maternal immune response that alters success or failure of pregnancy in the abortion-prone CBAxDBA/2 model. J. Reprod. Immunol., in this issue. Chatterjee-Hasrouni, 1979, Localization of H-2 antigens on mouse trophoblast cells, J. Exp. Med., 149, 1238, 10.1084/jem.149.5.1238 Chen, T., Darrasse-Jèze, G., Bergot, A.S., Valdivia, K., Strominger, J.L., Chaouat, G., Klatzmann, D. Self-specific memory regulatory T cells protect embryos at implantation in a manner resembling protection of nascent tumors, submitted for publication. Clark, 1995, Characterization of murine pregnancy decidua transforming growth factor beta. I. Transforming growth factor beta 2-like molecules of unusual molecular size released in bioactive form, Biol. Reprod., 52, 1380, 10.1095/biolreprod52.6.1380 Clark, 2008, Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA×DBA/2 mouse model. II. Fecal LPS levels in colonies with different basal abortion rates, Am. J. Reprod. Immunol., 60, 529, 10.1111/j.1600-0897.2008.00652.x Criscitiello, 2010, Evolutionarily conserved TCR binding sites, identification of T cells in primary lymphoid tissues, and surprising trans-rearrangements in nurse shark, J. Immunol., 184, 6950, 10.4049/jimmunol.0902774 D’Hooghe, 2006, Recombinant human TNFRSF1A (r-hTBP1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study, Biol. Reprod., 74, 131, 10.1095/biolreprod.105.043349 Dimitriadis, 2011, New generation contraceptives: interleukin 11 family cytokines as non-steroidal contraceptive targets, J. Reprod. Immunol., 88, 233, 10.1016/j.jri.2010.12.002 Ding, 2010, Attenuated oocyte fertilization and embryo development associated with altered growth factor/signal transduction induced by endometriotic peritoneal fluid, Fertil. Steril., 93, 2538, 10.1016/j.fertnstert.2009.11.011 1995, Early embryo development, uterine preparation and role of cytokines in implantation and labour Engleman, 1978, A suppressor T cell of the mixed lymphocyte reaction in man specific for the stimulating alloantigen. Evidence that identity at HLA-D between suppressor and responder is required for suppression, J. Exp. Med., 147, 137, 10.1084/jem.147.1.137 Engleman, 1978, Suppression of the mixed lymphocyte reaction in man by a soluble T-cell factor. Specificity of the factor for both responder and stimulator, J. Exp. Med., 147, 1037, 10.1084/jem.147.4.1037 Giannubilo, 2012, The involvement of inflammatory cytokines in the pathogenesis of recurrent miscarriage, Cytokine, 58, 50, 10.1016/j.cyto.2011.12.019 Girardi, 2006, The complement system in the pathophysiology of pregnancy, Mol. Immunol., 43, 68, 10.1016/j.molimm.2005.06.017 Girardi, 2011, Complement activation in animal and human pregnancies as a model for immunological recognition, Mol. Immunol., 48, 1621, 10.1016/j.molimm.2011.04.011 Gnainsky, 2010, Local injury of the endometrium induces an inflammatory response that promotes successful implantation, Fertil. Steril., 94, 2030, 10.1016/j.fertnstert.2010.02.022 Hamilton, 1987, Environmental influences on immunologically associated recurrent spontaneous abortion in CBA/J mice, J. Reprod. Immunol., 11, 237, 10.1016/0165-0378(87)90060-X Hamlett, 2005, Ultrastructure of the maternal–fetal interface of the yolk sac placenta in sharks, Ital. J. Anat. Embryol., 10, 175 Hedley, 1989, Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse, J. Immunol., 142, 46, 10.4049/jimmunol.142.11.4046 Hill, 1995, T helper 1 immunity to trophoblast: evidence for a new immunological mechanism for recurrent abortion in women, Hum. Reprod., 10, 114, 10.1093/humrep/10.suppl_2.114 Holder, 2012, Immune cell activation by trophoblast-derived microvesicles is mediated by syncytin 1, Immunology, 136, 184, 10.1111/j.1365-2567.2012.03568.x Horgan, 2011, In the extremes – traumatic insemination, Mol. Reprod. Dev., 78, 10.1002/mrd.21322 Kachkache, 1991, Hormonal and local factors control the immuno histochemical distribution of immunocytes in the rat uterus before conceptus implantation: effects of ovariectomy. Fallopian tube section and RU 486 injection, Biol. Reprod., 45, 860, 10.1095/biolreprod45.6.860 Kaye, 1972, Immunology and placentation in viviparous invertebrates, J. Reprod. Fertil., 31, 335, 10.1530/jrf.0.0310335 Kolomiets, 2005, The effect of mutation dominant spotting-Yurlovo (KitW-Y) on spermatogenesis, early embryogenesis, and fertility of C57BL/6JY mice, Genetika, 41, 1377 Komine-Aizawa, 2011, The therapeutic potential of the recombinant antigen from Dirofilaria immitis (rDiAg) for immune-mediated pregnancy loss, J. Reprod. Immunol., 92, 21, 10.1016/j.jri.2011.07.003 Kumasawa, 2011, Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model, Proc. Natl. Acad. Sci. U.S.A., 108, 1451, 10.1073/pnas.1011293108 Laissue, 2009, Identification of quantitative trait loci responsible for embryonic lethality in mice assessed by ultrasonography, Int. J. Dev. Biol., 53b, 623, 10.1387/ijdb.082613pl Lebovic, 2010, Peroxisome proliferator-activated receptor-(gamma) receptor ligand partially prevents the development of endometrial explants in baboons: a prospective, randomized, placebo-controlled study, Endocrinology, 151, 1846, 10.1210/en.2009-1076 Lédée-Bataille, 2005, Role of the endometrial tripod interleukin-18-15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure, Fertil. Steril., 83, 598, 10.1016/j.fertnstert.2004.11.021 Lédée-Bataille, 2006, Detectable levels of interleukin-18 in uterine luminal secretions at oocyte retrieval predict failure of the embryo transfer, Hum. Reprod., 19, 1968, 10.1093/humrep/deh356 Legac, 1996, Primitive cytokines and cytokine receptors in invertebrates: the sea star Asterias rubens as a model of study, Scand. J. Immunol., 44, 375, 10.1046/j.1365-3083.1996.d01-322.x Lightner, 2008, The fetal allograft revisited: does the study of an ancient invertebrate species shed light on the role of natural killer cells at the maternal–fetal interface?, Clin. Dev. Immunol., 2008, 631920, 10.1155/2008/631920 Litjens, 2012, Identification of circulating human antigen-reactive CD4+ FOXP3+ natural regulatory T cells, J. Immunol., 188, 1083, 10.4049/jimmunol.1101974 Loblay, 1978, Suppressor T-cell memory. Suppressor T-cell memory, Nature, 272, 620, 10.1038/272620a0 Loke, 1991, Recent developments in the human maternal-fetal immune interaction, Curr. Opin. Immunol., 5, 762, 10.1016/0952-7915(91)90110-M Loke, 1995 Loke, 1996, Immunology of human implantation: an evolutionary perspective, Hum. Reprod., 11, 283, 10.1093/HUMREP/11.2.283 Long, 2008, Live birth in the Devonian period, Nature, 453, 650, 10.1038/nature06966 Luo, 2011, A Jurassic eutherian mammal and divergence of marsupials and placentals, Nature, 476, 442, 10.1038/nature10291 MacMaster, 1992, Activation and distribution of inflammatory cells in the mouse uterus during the pre-implantation period, J. Immunol., 148, 1699, 10.4049/jimmunol.148.6.1699 Madeja, 2011, Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth, Proc. Natl. Acad. Sci. U.S.A., 108, 4012, 10.1073/pnas.1005342108 Mangeney, 2007, Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins, Proc. Natl. Acad. Sci. U.S.A., 104, 20534, 10.1073/pnas.0707873105 Martal, 1998, IFN-tau: a novel subtype I IFN1. Structural characteristics, non-ubiquitous expression, structure–function relationships, a pregnancy hormonal embryonic signal and cross-species therapeutic potentialities, Biochimie, 80, 755, 10.1016/S0300-9084(99)80029-7 Mas, 2008, Immune regulation at the interface during early steps of murine implantation: involvement of two new cytokines of the IL-12 family (IL-23 and IL-27) and of TWEAK, Am. J. Reprod. Immunol., 59, 323, 10.1111/j.1600-0897.2007.00567.x Matzinger, 1994, Tolerance, danger, and the extended family, Annu. Rev. Immunol., 12, 991, 10.1146/annurev.iy.12.040194.005015 Medawar, 1953, Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates, Symp. Soc. Exp. Biol., 7, 320 Meisser, 1999, Effects of tumour necrosis factor-alpha, interleukin-1 alpha, macrophage colony stimulating factor and transforming growth factor beta on trophoblastic matrix metalloproteinases, Mol. Hum. Reprod., 5, 252, 10.1093/molehr/5.3.252 Mellor, 2000, Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression, Annu. Rev. Immunol., 18, 367, 10.1146/annurev.immunol.18.1.367 Mellor, 2001, Tryptophan catabolism prevents maternal T cells from activating lethal anti-fetal immune responses, J. Reprod. Immunol., 52, 5, 10.1016/S0165-0378(01)00118-8 Menzies, 2012, Mast cells reside in myometrium and cervix, but are dispensable in mice for successful pregnancy and labor, Immunol. Cell Biol., 90, 321, 10.1038/icb.2011.40 Mitra, 2010, Identification and characterization of the transcription factors involved in T-cell development, t-bet, stat6 and foxp3, within the zebrafish, Danio rerio, FEBS J., 277, 128, 10.1111/j.1742-4658.2009.07460.x Moffett, 2006, Immunology of placentation in eutherian mammals, Nat. Rev. Immunol., 6, 584, 10.1038/nri1897 Mohamed, 2005, Uterine Wnt/beta-catenin signaling is required for implantation, Proc. Natl. Acad. Sci. U.S.A., 102, 8579, 10.1073/pnas.0500612102 Nakashima, 2012, The balance of the immune system between T cells and NK cells in miscarriage, Am. J. Reprod. Immunol., 67, 304, 10.1111/j.1600-0897.2012.01115.x Oftedal, 2012, The evolution of milk secretion and its ancient origins, Animal, 6, 355, 10.1017/S1751731111001935 Paldi, 1991, Genomic imprinting and feto maternal relationship, 61 Parham, 2012, Review: Immunogenetics of human placentation, Placenta, 33, S71, 10.1016/j.placenta.2011.11.020 Parham, 2012, Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules, Philos. Trans. R. Soc. Lond. B: Biol. Sci., 367, 800, 10.1098/rstb.2011.0266 Park, 2012, NODAL in the uterus is necessary for proper placental development and maintenance of pregnancy, Biol. Reprod., 86, 194, 10.1095/biolreprod.111.098277 Petitbarat, 2011, TWEAK appears as a modulator of endometrial IL-18 related cytotoxic activity of uterine natural killers, PLoS ONE, 6, e14497, 10.1371/journal.pone.0014497 Petrányi, 2002, The complexity of immune and alloimmune response, Transpl. Immunol., 10, 91, 10.1016/S0966-3274(02)00054-0 Pires, 2010, The evolution of placentas and superfetation in the fish genus Poecilia (Cyprinodontiformes: Poeciliidae: subgenera Micropoecilia and Acanthocephalus), Biol. J. Linnean Soc., 99, 784, 10.1111/j.1095-8312.2010.01391.x Quintana, 2010, Adaptive autoimmunity and Foxp3-based immunoregulation in zebrafish, PLoS ONE, 5, e9478, 10.1371/journal.pone.0009478 Reznick, 2002, Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis, Science, 298, 1018, 10.1126/science.1076018 Ryland, 1990, Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum, Mar. Ecol. Prog. Ser., 61, 125, 10.3354/meps061125 Sabri, 2011, Placenta-like structure of the aphid endoparasitic wasp Aphidius ervi: a strategy of optimal resources acquisition, PLoS ONE, 6, e18847, 10.1371/journal.pone.0018847 Sacks, 2003, Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells, Clin. Exp. Immunol., 131, 490, 10.1046/j.1365-2249.2003.02082.x Sakaguchi, 2010, FOXP3+ regulatory T cells in the human immune system, Nat. Rev. Immunol., 10, 490, 10.1038/nri2785 Samstein, 2012, Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict, Cell, 150, 29, 10.1016/j.cell.2012.05.031 Sanford, 1992, Expression of colony stimulating factors and inflammatory cytokines in the uterus if CD1 mice during days 1 to days 3 of pregnancy, J. Reprod. Fertil., 94, 213, 10.1530/jrf.0.0940213 Sargent, 2006, NK cells and human pregnancy – an inflammatory view, Trends Immunol., 27, 399, 10.1016/j.it.2006.06.009 Shi, 2004, Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus, J. Exp. Med., 199, 1379, 10.1084/jem.20032207 Simon, 1994, Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist, Endocrinology, 134, 521, 10.1210/en.134.2.521 Simpson, 1981, A model of T-cell unresponsiveness using the male-specific antigen, H-Y, Cell Immunol., 2, 251, 10.1016/0008-8749(81)90323-3 Smith, 1977, The adoptive transfer of pregnancy-induced unresponsiveness to male skin grafts with thymus-dependent cells, J. Exp. Med., 146, 899, 10.1084/jem.146.3.899 Stewart, 1992, Blastocyst implantation depends on maternal expression of leukemia inhibitory factor, Nature, 359, 76, 10.1038/359076a0 Stilley, 2010, Neutralizing TIMP1 restores fecundity in a rat model of endometriosis and treating control rats with TIMP1 causes anomalies in ovarian function and embryo development, Biol. Reprod., 83, 185, 10.1095/biolreprod.109.083287 Stilley, 2012, Cellular and molecular basis for endometriosis-associated infertility, Cell Tissue Res., 349, 849, 10.1007/s00441-011-1309-0 Vatin, 2012, Refined mapping of a quantitative trait locus on chromosome 1 responsible for mouse embryonic death, PLoS ONE, 7, e43356, 10.1371/journal.pone.0043356 Wegmann, 1984, Fetal protection against abortion: is it immuno suppression or immuno stimulation?, Ann. Immunol. (Inst. Pasteur.), 135D, 309, 10.1016/S0769-2625(84)81196-4 Wegmann, 1993, Bidirectional cytokines interactions in the materno fetal relationship: is successful allopregnancy a Th2 phenomenon?, Immunol. Today, 14, 353, 10.1016/0167-5699(93)90235-D Wen, 2011, Identification of Treg-like cells in Tetraodon: insight into the origin of regulatory T subsets during early vertebrate evolution, Cell. Mol. Life Sci., 68, 2615, 10.1007/s00018-010-0574-5 Wible, 2007, Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary, Nature, 447, 1003, 10.1038/nature05854 Wordinger, 1986, Implantation, deciduoma formation and live births in mast cell-deficient mice (W/Wv), J. Reprod. Fertil., 77, 471, 10.1530/jrf.0.0770471 Zhang, 2011, Molecular cloning and characterization of Foxp3 in Atlantic salmon (Salmo salar), Fish Shellfish Immunol., 30, 902, 10.1016/j.fsi.2011.01.012 Zhu, 2012, Origin of immunoglobulin isotype switching, Curr. Biol., 22, 872, 10.1016/j.cub.2012.03.060 Zourbas, 2001, Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy, Clin. Exp. Immunol., 126, 519, 10.1046/j.1365-2249.2001.01607.x