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12 - Immunology of trophoblast: a reappraisal

from General discussion II

Published online by Cambridge University Press:  07 August 2009

By
Y. W. (charlie) Loke
Edited by
Ashley Moffett ,
Charlie Loke  and
Anne McLaren
Y. W. (charlie) Loke
Affiliation:
University of Cambridge, UK
Ashley Moffett
Affiliation:
University of Cambridge
Charlie Loke
Affiliation:
University of Cambridge
Anne McLaren
Affiliation:
Cancer Research, UK
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Summary

Introduction

In the light of the discovery of the major histocompatibility complex (MHC) and its role in transplantation, the seminal essay written by Medawar drew a logical comparison between an allograft and a fetus (Medawar 1953). Despite being non-self, the fetus survives while the transplant is rejected. Medawar himself pointed out that the placenta must play a central role in fetal acceptance as it is the placental trophoblast cells that interface with the mother. Now, over 50 years later, the question how the allogeneic trophoblast survives in the potentially immunological hostile uterine environment remains unanswered. Why is the solution to this problem so elusive? I would argue that comparing the placental/maternal relationship with the graft/host relationship is misleading because the analogy between the two is not as close as it appears to be.

The extent of cellular contact between trophoblast and maternal tissue will vary significantly between species depending on the type of placentation. The immunological problem is likely to be most acute in the deeply invasive haemochorial placenta used in humans so that the adaptation required and the strategy employed in human reproduction would be expected to be different from those of other species. For this reason, animal models are not very useful and extrapolation of data between species has led to much confusion. The present paper is focused on human placentation.

Type
Chapter
Information
Biology and Pathology of Trophoblast , pp. 242 - 260
Publisher: Cambridge University Press
Print publication year: 2006

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References

Akira, S. & Hemmi, H. (2003). Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett., 85, 85–95.CrossRefGoogle ScholarPubMed
Bieche, I., Laurent, A., Laurendeau, I.et al. (2003). Placenta-specific INSL4 expression is mediated by a human endogenous retrovirus element. Biol. Reprod., 68, 1422–9.CrossRefGoogle ScholarPubMed
Billingham, R. E., Brent, L. & Medawar, P. B. (1953). ‘Actively acquired tolerance’ of foreign cells. Nature, 172, 603–6.CrossRefGoogle Scholar
Blond, J. L., Lavillette, D., Cheynet, V.et al. (2000). An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J. Virol., 74, 3321–9.CrossRefGoogle ScholarPubMed
Burnet, F. M. (1959). The Clonal Selection Theory of Acquired Immunity. Nashville, Tennessee: Vanderbilt University Press.CrossRefGoogle Scholar
Crisa, L., McMaster, M. T., Ishii, J. K., Fisher, S. J. & Salomon, D. R. (1997). Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J. Exp. Med., 186, 289–98.CrossRefGoogle ScholarPubMed
Crocker, P. R. & Varki, A. (2001). Siglecs, sialic acids and innate immunity. Trends Immunol., 22, 337–42.CrossRefGoogle ScholarPubMed
Davies, B., Hiby, S. E., Gardner, L., Loke, Y. W. & King, A. (2001). HLA-G expression by tumors. Am. J. Reprod. Immunol., 45, 103–7.CrossRefGoogle ScholarPubMed
Devergne, O., Coulomb-L'Hermine, A., Capel, F., Moussa, M. & Capron, F. (2001). Expression of Epstein-Barr virus-induced gene 3, an interleukin-12 p40-related molecule, throughout human pregnancy. Am. J. Pathol. 159, 1763–76.CrossRefGoogle ScholarPubMed
Fox, D. (1999). Why we don't lay eggs. New Scientist, 162, 27–31.Google Scholar
Frendo, J. L., Olivier, D., Cheynet, V.et al. (2003). Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol. Cell. Biol., 23, 3566–74.CrossRefGoogle Scholar
Frumento, G., Franchello, S., Palmisano, G. L.et al. (2000). Melanoma and melanoma cell lines do not express HLA-G, and the expression cannot be induced by gamma-IFN treatment. Tissue Antigens, 56, 30–7.CrossRefGoogle ScholarPubMed
Guidotti, L. G. & Chisari, F. V. (2001). Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol., 19, 65–91.CrossRefGoogle ScholarPubMed
Harris, J. R. (1998). Placental endogenous retrovirus ERV: structural, functional and evolutionary significance. BioEssays, 20, 307–16.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Hiby, S. E., King, A., Sharkey, A. M. & Loke, Y. W. (1997). Human uterine NK cells have a similar repertoire of Killer Inhibitory and Activatory receptors to those found in blood, as demonstrated by RT-PCR and sequencing. Mol. Immunol., 34, 419–30.CrossRefGoogle ScholarPubMed
Hiby, S. E., King, A., Sharkey, A. M. & Loke, Y. W. (1999). Molecular studies of trophoblast HLA-G: polymorphism, isoforms, imprinting and expression in pre-implantation embryo. Tissue Antigens, 53, 1–13.CrossRefGoogle Scholar
Karre, K., Ljunggren, H. G., Piontek, G. & Kiessling, R. (1986). Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature, 319, 675–8.CrossRefGoogle ScholarPubMed
Kaufmann, P. & Burton, G. (1994). Anatomy and genesis of the placenta. In Knobil, E. & Neill, J. D., eds., Physiology of Reproduction, 2nd edn. New York: Raven Press, pp. 441–83.Google Scholar
King, A. & Loke, Y. W. (1991). On the nature and function of human uterine granular lymphocytes. Immunol. Today, 12, 432–5.CrossRefGoogle ScholarPubMed
King, A., Boocock, C., Sharkey, A., Gardner, L. & Loke, Y. W. (1996). Evidence for the expression of HLA-C class I mRNA and protein by human first trimester trophoblast. J. Immunol., 156, 2068–76.Google Scholar
King, A., Allan, D. S. J., Joseph, S.et al. (2000a). HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol., 30, 1623–31.3.0.CO;2-M>CrossRefGoogle Scholar
King, A., Burrows, T. D., Hiby, S. E.et al. (2000b). Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta, 21, 376–87.CrossRefGoogle Scholar
Koopman, L. A., Kopcow, H. D., Rybalov, B.et al. (2003). Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med., 198, 1201–12.CrossRefGoogle ScholarPubMed
Lee, N., Malacko, A. R., Ishitani, A.et al. (1995). The membrane-bound and soluble forms of HLA-G bind identical sets of endogenous peptides but differ with respect to TAP association. Immunity, 3, 591–600.CrossRefGoogle ScholarPubMed
Lee, N., Goodlett, D. R., Ishitani, A., Marquardt, H. & Geraghty, D. E. (1998a). HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol., 160, 4951–60.Google Scholar
Lee, N., Llano, M., Carretero, M.et al. (1998b). HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. U.S.A., 95, 199–204.CrossRefGoogle Scholar
Loke, Y. W. & King, A. (1995). Human Implantation: Cell Biology and Immunology. Cambridge: Cambridge University Press.Google Scholar
Loke, Y. W. & King, A. (2000). Decidual NK cell interaction with trophoblast: cytolysis or cytokine production?Biochem. Soc. Trans., 28, 196–8.CrossRefGoogle ScholarPubMed
Loke, Y. W. & King, A. (2001). HLA class I molecules in implantation. In Fetal and Maternal Medicine Review 12. Cambridge: Cambridge University Press, pp. 299–314.Google Scholar
Loke, Y. W., King, A. & Burrows, T.et al. (1997). Evaluation of trophoblast HLA-G antigen with a specific monoclonal antibody. Tissue Antigens, 50, 135–46.CrossRefGoogle ScholarPubMed
Loke, Y. W., Hiby, S. & King, A. (1999). Human leukocyte antigen-G and reproduction. J. Reprod. Immunol., 43, 235–42.CrossRefGoogle ScholarPubMed
Mallet, V., Blaschitz, A., Crisa, L.et al. (1999). HLA-G in the human thymus: a subpopulation of medullary epithelial but not CD83+ dendritic cells express HLA-G membrane-bound and soluble protein. Int. Immunol., 11, 889–98.CrossRefGoogle Scholar
Matzinger, P. (1994). Tolerance, danger and the extended family. Annu. Rev. Immunol., 12, 991–1045.CrossRefGoogle ScholarPubMed
Medawar, P. B. (1953). Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. In Society for Experimental Biology. New York: Academic Press, pp. 320–38.Google Scholar
Medzhitov, R. & Janeway, C. A. (2002). Decoding the patterns of self and nonself by the innate immune system. Science, 296, 298–300.CrossRefGoogle ScholarPubMed
Mi, S., Lee, X., Li, X.et al. (2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature, 403, 715–17.CrossRefGoogle ScholarPubMed
Moffett, A. & Loke, Y. W. (2004). The immunological paradox of pregnancy: a reappraisal. Placenta, 25, 1–8.CrossRefGoogle ScholarPubMed
Moffett-King, A. (2002). Natural killer cells and pregnancy. Nat. Rev. Immunol., 2, 656–63.CrossRefGoogle Scholar
Muir, A., Lever, A. M. L. & Moffett, A. (2004). Expression and functions of human endogenous retroviruses in the placenta: an update. Placenta, 25 (Suppl. A), S16–25.CrossRefGoogle ScholarPubMed
Ober, C., Aldrich, C., Rosinsky, B.et al. (1998). HLA-G1 protein expression is not essential for fetal survival. Placenta, 19, 127–32.CrossRefGoogle Scholar
Oldenburg, P.-A., Zhelezynak, A., Fang, Y.-F.et al. (2000). Role of CD47 as a marker of self on red blood cells. Science, 288, 2051–4.CrossRefGoogle Scholar
Robertson, W. B. (1987). Pathology of the pregnant uterus. In Fox, H., ed., Obstetrical and Gynaecological Pathology. London: Churchill Livingstone, pp. 1149–76.Google Scholar
Schulte, A. M., Malerczyk, C., Cabal-Manzano, R.et al. (2000). Influence of the human endogenous retrovirus-like element HERV-E.PTN on the expression of growth factor pleiotrophin: a critical role of retroviral Sp1-binding site. Oncogene, 19, 3988–98.CrossRefGoogle ScholarPubMed
Slukvin, I. I., Lunn, D. P., Watkins, D. I. & Golos, T. G. (2000). Placental expression of the nonclassical MHC class I molecule Mamu-AG at implantation in the rhesus monkey. Proc. Natl. Acad. Sci. U.S.A., 97, 9104–9.CrossRefGoogle ScholarPubMed
Stoye, J. P. & Coffin, J. M. (2000). A provirus put to work. Nature, 403, 715–17.CrossRefGoogle ScholarPubMed
Sverdlov, E. D. (2000). Retroviruses and primate evolution. BioEssays, 22, 161–71.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Vilches, C. & Parham, P. (2002). KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol., 20, 217–51.CrossRefGoogle ScholarPubMed
Aluvihare, V. R., Kallikourdis, M. & Betz, A. G. (2004). Regulatory T cells mediate maternal tolerance to the foetus. Nat. Immun., 5, 266–71.CrossRefGoogle Scholar
Croy, B. A., Ashkar, A. A., Minhas, K. & Greenwood, J. D. (2000). Can murine uterine natural killer cells give insights into the pathogenesis of preeclampsia?J. Soc. Gynecol. Invest., 7, 12–20.CrossRefGoogle ScholarPubMed
Munn, D. H., Zhou, M., Attwood, J. T.et al. (1998). Prevention of allogeneic fetal rejection by tryptophan catabolism. Science, 281, 1191–3.CrossRefGoogle ScholarPubMed
Regan, L., Braude, P. R. & Hill, D. P. (1991). A prospective study of the incidence, time of appearance and significance of anti-paternal lymphocytotoxic antibodies in human pregnancy. Hum. Reprod., 6, 294–8.CrossRefGoogle ScholarPubMed

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