Immunology of placentation in eutherian mammals (original) (raw)

• Medawar, P. B. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 7, 320–338 (1953). The seminal paper that introduced the concept of the fetus as an allograft.
  Google Scholar
• Trowsdale, J. & Betz, A. G. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nature Immunol. 7, 241–246 (2006).
  Article CAS Google Scholar
• Steven, D. H. (ed) Comparative Placentation (Academic Press, New York, 1975).
  Google Scholar
• Mossman, H. W. Vertebrate fetal membranes. (Rutgers University Press, New Brunswick, 1987).
  Book Google Scholar
• Wooding, F. B. P. & Flint, A. P. F. in Marshall's Physiology of Reproduction Vol. 3 Ch. 4 (ed. Lamming, G. E.) 230–466 (Chapman and Hall, London, 1994).
  Google Scholar
• Moffett-King, A. Natural killer cells and pregnancy. Nature Rev. Immunol. 2, 656–663 (2002).
  Article CAS Google Scholar
• Johnson, M. Origins of pluriblast and trophoblast in the eutherian conceptus. Reprod. Fertil. Dev. 8, 699–709 (1996).
  CAS Google Scholar
• Moffett, A., Loke, Y. W. & McLaren, A. The Biology and Pathology of Trophoblast (Cambridge University Press, Cambridge, 2006).
  Book Google Scholar
• Blackburn, D. G. Reconstructing the evolution of viviparity and placentation. J. Theor. Biol. 192, 183–190 (1998).
  Article CAS PubMed Google Scholar
• Romer, A. S. Major steps in vertebrate evolution. Science 158, 1629–1637 (1967).
  Article CAS PubMed Google Scholar
• Luckett, W. P. in Major Patterns of Vertebrate Evolution (eds Hecht, M. K., Goody, P. C. & Hecht, B. M.) 439–516 (Plenum Press, New York 1977).
  Book Google Scholar
• Hubrecht, A. A. W. Studies in mammalian embryology. 1. The placentation of Erinaceus europaeus, with remarks on the phylogeny of the placenta. Q. J. Microsc. Sci. 119, 283–404 (1889).
  Google Scholar
• Amoroso, E. C. in Marshall's Physiology of Reproduction Vol. 2 Ch. 15 (ed.Parkes, A. S.) 127–311 (Longman, Green and Co., London, 1952).
  Google Scholar
• Vogel, P. The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta 26, 591–596 (2005).
  Article CAS PubMed Google Scholar
• Murphy, W. J. et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348–2351 (2001).
  Article CAS PubMed Google Scholar
• Kriegs, J. O. et al. Retroposed elements as archives for the evolutionary history of placental mammals. PLoS Biol. 4, e91 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Mess, A. & Carter, A. M. Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J. Exp. Zoolog. B. Mol. Dev. Evol. 306, 140–163 (2006).
  Article Google Scholar
• Enders, A. C. & Carter, A. M. What can comparative studies of placental structure tell us? — A review. Placenta 25 (Suppl. A), S3–S9 (2004).
  Article CAS PubMed Google Scholar
• Wildman, D. E. et al. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203–3208 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Clarke, C. A. Prevention of rhesus iso-immunisation. Lancet 2, 1–7 (1968).
  Article CAS PubMed Google Scholar
• Nelson, J. L. Maternal-fetal immunology and autoimmune disease. Is some autoimmune disease auto-allo or allo-auto immune? Arthritis Rheum. 39, 191–194 (1996).
  Article CAS PubMed Google Scholar
• Pijnenborg, R., Vercruysse, L. & Hanssens, M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 17 February 2006 [epub ahead of print]. The definitive paper of the placental bed based on a life-time's study.
• Jauniaux, E., Poston, L. & Burton, G. J. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum. Reprod. Update 8 May 2006 [epub ahead of print].
• King, A. et al. Uterine leukocytes and decidualization. Hum. Reprod. Update 6, 28–36 (2000).
  Article CAS PubMed Google Scholar
• Robertson, W. B. in Obstetrical and Gynaecological Pathology (ed. Fox, H.) 1149–1176 (Churchill Livingstone, 1987).
  Google Scholar
• Kirby, D. R. S. in The Early Conceptus, Normal and Abnormal (ed. Park, W. W.) 68–73 (Proceedings of Symposium, Queen's College, Dundee, 1965).
  Google Scholar
• Khong, T. Y. & Robertson, W. B. Placenta creta and placenta praevia creta. Placenta 8, 399–409 (1987).
  Article CAS PubMed Google Scholar
• McLaren, A. in The Early Conceptus, Normal and Abnormal (ed. Park, W. W.) 27–33 (Proceedings of Symposium, Queen's College, Dundee, 1965).
  Google Scholar
• Martin, R. D. Human reproduction: a comparative background for medical hypotheses. J. Reprod. Immunol. 59, 111–135 (2003).
  Article PubMed Google Scholar
• Ramsey, E. M., Houston, M. L. & Harris, J. W. S. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am. J. Obstet. Gynecol. 124, 647–652 (1976). This paper emphasizes that, even among closely related species of primates, the ways trophoblast cells interact with maternal tissues show many differences.
  Article CAS PubMed Google Scholar
• Rockwell, L. C., Vargas, E. & Moore, L. G. Human physiological adaptation to pregnancy: inter- and intraspecific perspectives. Am. J. Hum. Biol. 15, 330–341 (2003).
  Article PubMed Google Scholar
• Chaline, J. Increased cranial capacity in hominoid evolution and preeclampsia. J. Reprod. Immunol. 59, 137–152 (2003).
  Article PubMed Google Scholar
• Baker, J. M., Bamford, A. I. & Antczak, D. F. Modulation of allospecific CTL responses during pregnancy in equids: an immunological barrier to interspecies matings? J. Immunol. 162, 4496–4501 (1999).
  CAS PubMed Google Scholar
• Davies, C. J., Eldridge, J. A., Fisher, P. J. & Schlafer, D. H. Evidence for expression of both classical and non-classical major histocompatibility complex class I genes in bovine trophoblast cells. Am. J. Reprod. Immunol. 55, 188–200 (2006).
  Article CAS PubMed Google Scholar
• Bainbridge, D. R., Sargent, I. L. & Ellis, S. A. Increased expression of major histocompatibility complex (MHC) class I transplantation antigens in bovine trophoblast cells before fusion with maternal cells. Reproduction 122, 907–913 (2001).
  Article CAS PubMed Google Scholar
• Stewart, I. J. Granulated metrial gland cells in 'minor' species. J. Reprod. Immunol. 40, 129–146 (1998).
  Article CAS PubMed Google Scholar
• Georgiades, P., Ferguson-Smith, A. C. & Burton, G. J. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3–19 (2002).
  Article CAS PubMed Google Scholar
• Ain, R., Canham, L. N. & Soares, M. J. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev. Biol. 260, 176–190 (2003).
  Article CAS PubMed Google Scholar
• Vercruysse, L., Caluwaerts, S., Luyten, C. & Pijnenborg, R. Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta 27, 22–33 (2006).
  Article CAS PubMed Google Scholar
• Hemberger, M., Nozaki, T., Masutani, M. & Cross, J. C. Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion. Dev. Dyn. 227, 185–191 (2003).
  Article CAS PubMed Google Scholar
• Croy, B. A., Chantakru, S., Esadeg, S., Ashkar, A. A. & Wei, Q. Decidual natural killer cells: key regulators of placental development (a review). J. Reprod. Immunol. 57, 151–168 (2002). Comprehensive review discussing uterine NK cells in mice.
  Article CAS PubMed Google Scholar
• Tafuri, A., Alferink, J., Moller, P., Hammerling, G. J. & Arnold, B. T cell awareness of paternal alloantigens during pregnancy. Science 270, 630–633 (1995).
  Article CAS PubMed Google Scholar
• Redline, R. W. & Lu, C. Y. Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship. Lab. Invest. 61, 27–36 (1989).
  CAS PubMed Google Scholar
• Zuckermann, F. A. & Head, J. R. Expression of MHC antigens on murine trophoblast and their modulation by interferon. J. Immunol. 137, 846–853 (1986).
  CAS PubMed Google Scholar
• Erlebacher, A., Lukens, A. K. & Glimcher, L. H. Intrinsic susceptibility of mouse trophoblasts to natural killer cell-mediated attack in vivo. Proc. Natl Acad. Sci. USA 99, 16940–16945 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Munn, D. H. et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191–1193 (1998).
  Article CAS PubMed Google Scholar
• Erlebacher, A., Zhang, D., Parlow, A. F. & Glimcher, L. H. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J. Clin. Invest. 114, 39–48 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Aluvihare, V. R. et al. Regulatory T cells mediate maternal tolerance to the fetus. Nature Immunol. 5, 266–271 (2004). Paper describing a potential role for regulatory T cells in allogeneic murine pregnancies.
  Article CAS Google Scholar
• Sollwedel, A. et al. Protection from abortion by heme oxygenase-1 up-regulation is associated with increased levels of Bag-1 and neuropilin-1 at the fetal-maternal interface. J. Immunol. 175, 4875–4885 (2005).
  Article CAS PubMed Google Scholar
• Zhu, X. Y. et al. 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, 338–345 (2005).
  Article CAS PubMed Google Scholar
• Zenclussen, A. C. et al. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur. J. Immunol. 36, 82–94 (2006).
  Article CAS PubMed Google Scholar
• Xu, C. et al. A critical role for murine complement regulator crry in fetomaternal tolerance. Science 287, 498–501 (2000).
  Article CAS PubMed Google Scholar
• Hunt, J. S., Vassmer, D., Ferguson, T. A. & Miller, L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J. Immunol. 158, 4122–4128 (1997).
  CAS PubMed Google Scholar
• Guleria, I. et al. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 202, 231–237 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Krishnan, L., Guilbert, L. J., Wegmann, T. G., Belosevic, M. & Mosmann, T. R. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-γ and TNF and reduced IL-10 production by placental cells. J. Immunol. 156, 653–662 (1996).
  CAS PubMed Google Scholar
• Fallon, P. G. et al. IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 17, 7–17 (2002).
  Article CAS PubMed Google Scholar
• Baban, B. et al. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol. 61, 67–77 (2004).
  Article CAS PubMed Google Scholar
• Somerset, D. A., Zheng, Y., Kilby, M. D., Sansom, D. M. & Drayson, M. T. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+CD4+ regulatory T-cell subset. Immunology 112, 38–43 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Sasaki, Y. et al. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10, 347–353 (2004).
  Article CAS PubMed Google Scholar
• Grabowska, A. Placental antigenicity and maternal immunoregulation in human and murine pregnancy. Ph.D. Thesis, Univ. Cambridge (1989).
• Ostensen, M. Sex hormones and pregnancy in rheumatoid arthritis and systemic lupus erythematosus. Ann. NY Acad. Sci. 876, 131–144 (1999).
  Article CAS PubMed Google Scholar
• Buyon, J. P. The effects of pregnancy on autoimmune diseases. J. Leukoc. Biol. 63, 281–287 (1998).
  Article CAS PubMed Google Scholar
• Gardner, L. & Moffett, A. Dendritic cells in the human decidua. Biol. Reprod. 69, 1438–1446 (2003).
  Article CAS Google Scholar
• Shao, L., Jacobs, A. R., Johnson, V. V. & Mayer, L. Activation of CD8+ regulatory T cells by human placental trophoblasts. J. Immunol. 174, 7539–7547 (2005).
  Article CAS PubMed Google Scholar
• Shiroishi, M. et al. Efficient leukocyte Ig-like receptor signaling and crystal structure of disulfide-linked HLA-G dimer. J. Biol. Chem. 281, 10439–10447 (2006).
  Article CAS PubMed Google Scholar
• Chang, C. C. et al. Tolerization of dendritic cells by TS cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nature Immunol. 3, 237–243 (2002).
  Article CAS Google Scholar
• Velten, F. W., Duperrier, K., Bohlender, J., Metharom, P. & Goerdt, S. A gene signature of inhibitory MHC receptors identifies a BDCA3+ subset of IL-10-induced dendritic cells with reduced allostimulatory capacity in vitro. Eur. J. Immunol. 34, 2800–2811 (2004).
  Article CAS PubMed Google Scholar
• Ristich, V., Liang, S., Zhang, W., Wu, J. & Horuzsko, A. Tolerization of dendritic cells by HLA-G. Eur. J. Immunol. 35, 1133–1142 (2005).
  Article CAS PubMed Google Scholar
• Sherman, M. E., Mazur, M. T. & Kurman, R. J. in Blaustain's Pathology of the Female Genital Tract (ed. Kurman, R. J.) 428 (Springer, New York, 2002).
  Google Scholar
• Ryan, A. F., Grendell, R. L., Geraghty, D. E. & Golos, T. G. A soluble isoform of the rhesus monkey nonclassical MHC class I molecule Mamu-AG is expressed in the placenta and the testis. J. Immunol. 169, 673–683 (2002).
  Article CAS PubMed Google Scholar
• Stern, P. L. et al. Class I-like MHC molecules expressed by baboon placental syncytiotrophoblast. J. Immunol. 138, 1088–1091 (1987).
  CAS PubMed Google Scholar
• King, A., et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30, 1623–1631 (2000).
  Article CAS PubMed Google Scholar
• Rajagopalan, S. et al. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS. Biol. 4, e9 (2006). A careful study describing stimulation of NK cells by soluble HLA-G that is endocytosed by KIR2DL4.
  Article CAS PubMed Google Scholar
• Redman, C. W. & Sargent, I. L. Preeclampsia and the systemic inflammatory response. Semin. Nephrol. 24, 565–570 (2004).
  Article PubMed Google Scholar
• Parham, P. MHC class I molecules and KIRs in human history, health and survival. Nature Rev. Immunol. 5, 201–214 (2005). A comprehensive reference covering all aspects of KIRs.
  Article CAS Google Scholar
• Hiby, S. E. et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200, 957–965 (2004). This paper provides genetic evidence for a role for NK cells in regulating trophoblast-cell invasion.
  Article CAS PubMed PubMed Central Google Scholar
• Verma, S., King, A. & Loke, Y. W. Expression of killer-cell inhibitory receptors (KIR) on human uterine NK cells. Eur. J. Immunol. 27, 979–983 (1997).
  Article CAS PubMed Google Scholar
• Martin, M. P. & Carrington, M. Immunogenetics of viral infections. Curr. Opin. Immunol. 17, 510–516 (2005).
  Article CAS PubMed Google Scholar
• Abi-Rached, L. & Parham, P. Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J. Exp. Med. 201, 1319–1332 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• LaBonte, M. L., Hershberger, K. L., Korber, B. & Letvin, N. L. The KIR and CD94/NKG2 families of molecules in the rhesus monkey. Immunol. Rev. 183, 25–40 (2001).
  Article CAS PubMed Google Scholar
• Guethlein, L. A., Flodin, L. R., Adams, E. J. & Parham, P. NK cell receptors of the orangutan (Pongo pygmaeus): a pivotal species for tracking the coevolution of killer cell Ig-like receptors with MHC-C. J. Immunol. 169, 220–229 (2002).
  Article CAS PubMed Google Scholar
• Rajalingam, R., Parham, P. & Abi-Rached, L. Domain shuffling has been the main mechanism forming new hominoid killer cell Ig-like receptors. J. Immunol. 172, 356–369 (2004).
  Article CAS PubMed Google Scholar
• Khakoo, S. I. et al. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12, 687–698 (2000).
  Article CAS PubMed Google Scholar
• Emes, R. D., Goodstadt, L., Winter, E. E. & Ponting, C. P. Comparison of the genomes of human and mouse lays the foundation of genome zoology. Hum. Mol. Genet. 12, 701–709 (2003).
  Article CAS PubMed Google Scholar
• Selwood, L. & Johnson, M. H. Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins. BioEssays 28, 128–145 (2006).
  Article PubMed Google Scholar
• Koopman, L. A. et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198, 1201–1212 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Bulmer, J. N. & Lash, G. E. Human uterine natural killer cells: a reappraisal. Mol. Immunol. 42, 511–521 (2005).
  Article CAS PubMed Google Scholar
• Li, X. F. et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 86, 1823–1834 (2001).
  CAS PubMed Google Scholar
• Moffett, A., Regan, L. & Braude, P. Natural killer cells, miscarriage, and infertility. BMJ 329, 1283–1285 (2004).
  Article PubMed PubMed Central Google Scholar
• Pijnenborg, R., Robertson, W. B. & Brosens, I. The arterial migration of trophoblast in the uterus of the golden hamster, Mesocricetus auratus. J. Reprod. Fertil. 40, 269–280 (1974).
  Article CAS PubMed Google Scholar
• Nanaev, A. et al. Physiological dilation of uteroplacental arteries in the guinea pig depends on nitric oxide synthase activity of extravillous trophoblast. Cell Tissue Res. 282, 407–421 (1995).
  Article CAS PubMed Google Scholar
• Pijnenborg, R., Robertson, W. B., Brosens, I. & Dixon, G. Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2, 71–91 (1981).
  Article CAS PubMed Google Scholar
• Finn, C. Menstruation: a nonadaptive consequence of uterine evolution. Q. Rev. Biol. 73, 163–173 (1998).
  Article CAS PubMed Google Scholar
• Blankenship, T. N. & Enders, A. C. Modification of uterine vasculature during pregnancy in macaques. Microsc. Res. Tech. 60, 390–401 (2003).
  Article PubMed Google Scholar
• Pijnenborg, R., D'Hooghe, T., Vercruysse, L. & Bambra, C. Evaluation of trophoblast invasion in placental bed biopsies of the baboon, with immunohistochemical localisation of cytokeratin, fibronectin and laminin. J. Med. Primatol. 25, 272–281 (1996).
  Article CAS PubMed Google Scholar