The major histocompatability complex in pregnancy: Part II. Placental HLA-G protein expression in vivo: Where and what for?

Human Reproduction Update

Volumn 5, Issue 3, 1999, Pages 223-233

  Le Bouteiller, Philippe ^a   Solier, Corinne ^a   Pröll, Johannes ^a   Aguerre Girr, Maryse ^a   Fournel, Sylvie ^a   Lenfant, Françoise ^a  

^a CHU PURPAN   (France)

Author keywords

Cytotoxic T cells; Endothelial cells; HLA G; NK cell receptors; Trophoblast

Indexed keywords

HLA A ANTIGEN; HLA B ANTIGEN; HLA G ANTIGEN; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA-G ANTIGEN; ISOPROTEIN;

AMNION CELL; AMNION FLUID; ANGIOGENESIS; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; CHORION VILLUS; CYTOTROPHOBLAST; DECIDUA; ENDOTHELIUM CELL; EPITHELIUM CELL; HUMAN; IMMUNOMODULATION; NONHUMAN; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THYMOCYTE; TROPHOBLAST; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; METABOLISM; PHYSIOLOGY;

AMNIOTIC FLUID; CHORIONIC VILLI; FEMALE; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; PLACENTA; PREGNANCY; PROTEIN ISOFORMS; TROPHOBLASTS;

EID: 0033127666     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/5.3.223     Document Type: Review

References (101)

1. Agrawal, S., Marquet, J., Freeman, G. et al. (1999) MHC class I triggering by a novel cell surface ligand costimulates proliferation of activated human T cells. J. Immunol., 162, 1223-1226.
2. Amiot, L., Onno, M., Drenou, B. et al. (1998) HLA-G class I gene expression in normal and malignant hematopoietic cells. Hum. Immunol., 59, 524-528.
3. Benirschke, K. and Kaufmann, P. (eds) (1995) Pathology of the Human Placenta. 3rd edn, Springer-Verlag, New York.
4. Bensussan, A., Mansur, I.G., Mallet, V. et al. (1995) Detection of membrane-bound HLA-G translated products with a specific monoclonal antibody. Proc. Natl Acad. Sci. USA, 92, 10292-10296.
5. Blaschitz, A., Lenfant, F., Mallet, V. et al. (1997) Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur. J. Immunol., 27, 3380-3388.
6. Borrego, F., Ulbrecht, M., Weiss, E.H. et al. (1998) Recognition of human histocompatibility leucocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med., 197, 813-818.
7. Boyson, J.E., Iwanaga, K.K., Golos, T.G. and Watkins, D.I. (1997) Identification of a novel MHC class I gene, Mamu-AG, expressed in the placenta of a primate with an inactivated G locus. J. Immunol., 159, 3311-3321.
8. Braud, V.M., Allan, D.S., O'Callaghan, C.A. et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature, 391, 795-799.
9. Cantoni, C., Verdiani, S., Falco, M. et al. (1998) p49, a putative HLA class I-specific inhibitory NK receptor belonging to the immunoglobulin superfamily. Eur. J. Immunol., 28, 1980-1990.
10. Carbone, E., Terrazano, G., Colonna, M. et al. (1996) Natural killer clones recognize specific soluble HLA class I molecules. Eur. J. Immunol., 26, 683-689.
11. Chaouat, G., Menu, E., Mognetti, B. et al. (1997) Immunopathology of early pregnancy. Infect. Dis. Obstet. Gynaecol., 5, 73-92.
12. Chu, W., Fant, M.E., Geraghty, D.E. and Hunt, J.S. (1998) Soluble HLA-G in human placentas: synthesis in trophoblast and interferon-gamma-activated macrophages but not placental fibroblasts. Hum. Immunol., 59, 435-442.
13. Chumbley, G., King, A., Robertson, K. et al. (1994) Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell. Immunol., 155, 312-322.
14. Clark, D.A. (1997) HLA-G finally does something. Am. J. Reprod. Immunol., 38, 75-78.
15. Colbern, G.T., Chiang, M.H. and Main, E.K. (1994) Expression of the nonclassic histocompatibility antigen HLA-G by preeclamptic placenta. Am. J. Obstet. Gynecol., 170, 1244-1250.
16. Colonna, M., Navarro, F., Bellon, T. et al. (1997) A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med., 186, 1809-1818.
17. Colonna, M., Samaridis, J., Cella, M. et al. (1998) Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J. Immunol., 160, 3096-3100.
18. Cosman, D., Fanger, N., Borges, L. et al. (1997) A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity, 7, 273-282.
19. Crisa, L., McMaster, M.T., Ishii, J.K. et al. (1997) Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J. Exp. Med., 186, 289-298.
20. Deniz, G., Christmas, S.E., Brew, R. and Johnson, P.M. (1994) Phenotypic and functional cellular differences between human CD3-decidual and peripheral blood leucocytes. J. Immunol., 142, 4255-4262.
21. Diehl, M., Munz, C., Keilholz, W. et al. (1996) Nonclassical HLA-G molecules are classical peptide presenters. Curr. Biol., 6, 305-314.
22. Ellis, S.A., Sargent, I.L., Redman, C.W. and McMichael, A.J. (1986) Evidence for a novel HLA antigen found on human extravillous trophoblast and a choriocarcinoma cell line. Immunology, 59, 595-601.
23. Ellis, S.A., Palmer, M.S. and McMichael, A.J. (1990) Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA class I molecule. J. Immunol., 144, 731-735.
24. Fournel, S., Aguerre-Girr, M., Campan, A. et al. (1999) Soluble HLA-G: purification from eukaryotic transfected cells and detection by a specific ELISA. Am. J. Reprod. Immunol., in press.
25. Fujii, T., Ishitani, A. and Geraghty, D.E. (1994) A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J. Immunol., 153, 5516-5524.
26. Geraghty, D.E., Koller, B.H. and Orr, H.T. (1987) A human major histocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment. Proc. Natl Acad. Sci. USA, 84, 9145-9149.
27. Guillaudeux, T., Rodriguez, A.M., Girr, M. et al. (1995) Methylation status and transcriptional expression of the MHC class I loci in human trophoblast cells from term placenta. J. Immunol., 155, 3283-3299.
28. Hammer, A., Hutter, H., Blaschitz, A. et al. (1997) Amnion epithelial cells, in contrast to trophoblast cells, express all classical HLA class I molecules together with HLA-G. Am. J. Reprod. Immunol., 37, 161-171.
29. Hara, N., Fujii, T., Yamashita, T. et al. (1996) Altered expression of Human Leucocyte Antigen (HLA-G) on extravillous trophoblast in preeclampsia: immunohistological demonstration with anti-HLA-G specific antibody '87G' and anti-cytokeratin antibody 'CAMS.2'. Am. J. Reprod. Immunol., 36, 349-358.
30. Horuzsko, A., Antoniou, J., Tomlinson, P. et al. (1997) HLA-G functions as a restriction element and a transplantation antigen in mice. Int. Immunol., 9, 645-653.
31. Houlihan, J.M., Biro, P.A., Harper, H.M. et al. (1995) The human amnion is a site of MHC class Ib expression: evidence for the expression of HLA-E and HLA-G. J. Immunol., 154, 5665-5674.
32. Hunt, J.S. (ed.) (1996) HLA and the Maternal-Fetal Relationship. R.G. Landes Company, Austin, Texas.
33. Hunt, J.S., Chu, W. and Miller, L. (1998) Nonspecific immunity in the uterus and placenta. Trophoblast Res., 12, 125-134.
34. Hutter, H., Hammer, A., Blaschitz, A. et al. (1996) Expression of HLA class I molecules in human first trimester and term placenta trophoblast. Cell Tissue Res., 286, 439-447.
35. Ishitani, A. and Geraghty, D.E. (1992). Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc. Natl Acad. Sci. USA, 89, 3947-3951.
36. Jiang, S.P. and Vacchio, M.S. (1998) Multiple mechanisms of peripheral T cell tolerance to the fetal 'allograft'. J. Immunol., 160, 3086-3090.
37. Johnson, P., Vince, G.S. and Christmas, S.E. (1997) NK cells and reproduction. Immunol. Today, 18, 605.
38. Jurisicova, A., Casper, R., MacLusky, N.J. et al. (1996) HLA-G expression during preimplantation human embryo development. Proc. Natl Acad. Sci. USA, 93, 161-165.
39. Kanellopoulos-Langevin, C. (1998) Tolerance of the fetus by the maternal immune system. Curr. Concepts. Rev. Rheum., 65, 603-607.
40. King, A., Gardner, L. and Loke, Y.W. (1996) Human decidual leukocytes do not proliferate in response to either extravillous trophoblast or allogeneic peripheral blood lymphocytes. J Reprod. Immunol., 30, 67-74.
41. King, A., Hiby, S.E., Verma, S. et al. (1997) Uterine NK cells and trophoblast HLA class I molecules. Am. J. Reprod. Immunol., 37, 459-462.
42. King, A., Burrows, T., Verma, S. et al. (1998) Human uterine lymphocytes. Hum. Reprod. Update, 4, 480-485.
43. Kirszenbaum, M., Moreau, P., Gluckman, E. et al. (1994) An alternatively spliced form of HLA-G mRNA in human trophoblast and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc. Natl Acad. Sci. USA, 91, 4209-4213.
44. Kovats, S., Main, E.K., Librach, C. et al. (1990) Class I antigen, HLA-G, expressed in human trophoblast. Science, 248, 220-223.
45. Lanier, L.L (1998) NK receptors. Annu. Rev. Immunol., 16, 359-393.
46. Le Bouteiller, P. (1994) HLA class I chromosomal region, genes, and products: facts and questions. Crit. Rev. Immunol., 14, 89-129.
47. Le Bouteiller, P. and Blaschitz, A. (1999) The functionality of HLA-G is emerging. Immunol. Rev., in press.
48. Le Bouteiller, P. and Lenfant, F. (1996) Antigen-presenting function(s) of the non-classical HLA-E, -F and -G class I molecules: the beginning of a story. Res. Immunol., 147, 301-313.
49. 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.
50. Lee, N., Goodlett, D.R., Ishitani, A. et al. (1998) HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol., 160, 4951-4960.
51. Leibson, P.J. (1998) Cytotoxic lymphocyte recognition of HLA-E: utilizing a nonclassical window to peer into classical MHC. Immunity, 9, 289-294.
52. Lenfant, F., Fort, M., Rodriguez, A.M. et al. (1998) Absence of imprinting of HLA class Ia genes leads to co-expression of biparental alleles on term human trophoblast cells upon IFN-γ induction. Immunogenetics, 47, 297-304.
53. Ljunggren, H.G. and Karre, K. (1990) In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today, 11, 237-244.
54. Llano, M., Lee, N., Navarro, F. et al. (1998) HLA-E bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol., 28, 2854-2863.
55. Loke, Y.W. and King, A. (1995) Human Implantation: Cell Biology and Immunology. Cambridge University Press, Cambridge.
56. Loke, Y.W., King, A., Burrows, T. et al. (1997) Evaluation of trophoblast HLA-G antigen with a specific monoclonal antibody. Tissue Antigens, 50, 135-146.
57. Maejima, M., Fujii, T., Kozuma, S. et al. (1997) Presence of HLA-G-expressing cells modulates the ability of peripheral blood mononuclear cells to release cytokines. Am. J. Reprod. Immunol., 38, 79-82.
58. 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 as membrane-bound and soluble protein. Int. Immunol., in press.
59. McMaster, M.T., Librach, C.L., Zhou, Y. et al. (1995) Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol., 154, 3771-3778.
60. McMaster, M., Zhou, Y., Shorter, S. et al. (1998) HLA-G isoforms produced by placental cytotrophoblast and found in amniotic fluid are due to unusual glycosylation. J. Immunol., 160, 5922-5928.
61. Mitsuishi, Y., Miyazawa, K., Sonada, A. and Terzaki, P.I. (1997) Cellular function of soluble HLA-G. In Charron, D. (ed.), Genetic Diversity of HLA. Functional and Medical Implication. EDK Publisher, France, pp. 251-253.
62. Moreau, P., Carosella, E., Teyssier, M. et al. (1995) Soluble HLA-G molecule. An alternatively spliced HLA-G mRNA form candidate to encode it in peripheral blood mononuclear cells and human trophoblasts. Hum. Immunol., 43, 231-236.
63. Moretta, A., Biassoni, R., Bottino, C. et al. (1997) Major Histocompatibility Complex class I-specific receptors on human natural killer and T lymphocytes. Immunol. Rev., 155, 105-117.
64. Munn, D.H., Zhou, M., Attwood, J.T. et al. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science, 281, 1191-1193.
65. Nahmias, A.J. and Kourtis, A.P. (1997) The great balancing acts. The pregnant woman, placenta, fetus and infectious agents. Clin. Perinatol., 24, 497-521.
66. Navarro, F., Llano, M., Bellon, T. et al. (1999) The ILT2/LIR1 and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol., 29, 277-283.
67. Ober, C. (1998) Immunogenetics '98. HLA and pregnancy: the paradox of the fetal allograft. Am. J. Hum. Genet., 62, 1-5.
68. Ober, C. and Aldrich, C.L. (1997) HLA-G polymorphisms: neutral evolution or novel function? J. Reprod. Immunol., 36, 1-21.
69. Ober, C., Aldrich, C., Rosinsky, B. et al. (1998) HLA-G1 protein expression is not essential for fetal survival. Placenta, 19, 127-132.
70. O'Callaghan, C. and Bell, J.I. (1998) Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLA-G. Immunol. Rev., 163, 129-138.
71. Onno, M., Guillaudeux, T., Amiot, L. et al. (1994) The HLA-G gene is expressed at a low mRNA level in different human cells and tissues. Hum. Immunol., 41, 79-86.
72. Pende, D., Sivori, S., Accame, L. et al. (1997) HLA-G recognition by human natural killer cells. Involvement of CD94 both as inhibitory and as activatory receptor complex. Eur. J. Immunol., 27, 1875-1880.
73. Pérez-Villar, J.J., Melero, I., Navarro, F. et al. (1997) The CD94/NKG2-A inhibitory receptor complex is involved in NK cell-mediated recognition of cells expressing HLA-G1. J. Immunol., 158, 5736-5743.
74. Pröll, J., Blaschitz, A., Hartmann, M. et al. (1997) Cytokeratin 17 as an immunohistochemical marker for intramural cytotrophoblast in human first trimester uteroplacental arteries. Cell Tissue Res., 288, 335-343.
75. Pröll, J., Blaschitz, A., Hutter, H. and Dohr, G. (1999) First trimester human trophoblast cells express both HLA-C and HLA-G. Am. J. Reprod. Immunol., in press.
76. Puppo, F., Costa, M., Contini, P. et al. (1999) Quantitation of soluble HLA-G and HLA-A, -B, -C molecules in pregnancy. J. Reprod. Immunol., in press.
77. Redman, C.W.G., McMichael, A.J., Stirrat, G.M. et al. (1984) Class I major histocompatibility complex antigens on human extravillous trophoblast. Immunology, 52, 457-468.
78. Reyburn, H., Mandelboim, O., Valès-Gomèz, M. et al. (1997) Human NK cells: their ligands, receptors and functions. Immunol. Rev., 155, 119-125.
79. Rouas-Freiss, N., Marchal-Bras Goncalves, R. et al. (1997) Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl Acad. Sci. USA, 94, 11520-11525.
80. Sanders, S.K., Giblin, P.A. and Kavathas, P. (1991) Cell-cell adhesion mediated by CD8 and HLA-G, a nonclassical MHC class I molecule on cytotrophoblasts. J. Exp. Med., 174, 737-740.
81. Schmidt, C.M., Garrett, E. and Orr, H.T. (1997) Cytotoxic T lymphocyte recognition of HLA-G in mice. Hum. Immunol., 55, 127-139.
82. Schust, D.J., Hill, A.B. and Ploegh, H.L. (1996) Herpes simplex virus blocks intracellular transport of HLA-G in placentally derived human cells. J. Immunol., 157, 3375-3380.
83. Schust, D.J., Tortorella, D., Seebach, J. et al. (1998) Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J. Exp. Med., 188, 497-503.
84. Sernee, M.F., Ploegh, H.L. and Schust, D.J. (1998) Why certain antibodies cross-react with HLA-A and HLA-G: epitope mapping of two common MHC class I reagents. Mol. Immunol., 35, 177-188.
85. Sipes, S.L., Medaglia, M.V., Stabley, D.L. et al. (1996) A new major histocompatibility complex class I b gene expressed in the mouse blastocyst and placenta. Immunogenetics, 45, 108-120.
86. Slukvin, I.I., Boyson, J.E., Watkins, D.I. et al. (1998) The Rhesus monkey analogue of HLA-G is expressed primarily in villous syncytiotrophoblast. Biol. Reprod., 58, 728-738.
87. Söderstrom, K., Corliss, B., Lanier, L.L. et al. (1997) CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J. Immunol., 159, 1072-1075.
88. Stroynowski, I. and Tabaczewski, P. (1996) Multiple products of class Ib Qa-2 genes: which ones are functional? Res. Immunol., 147, 290-301.
89. Tafuri, A., Alferink, J., Moller, P. et al. (1995) T cell awareness of paternal alloantigens during pregnancy. Science, 270, 630-633.
90. Taylor, R.N. (1997) Review: immunobiology of preeclampsia. Am. J. Reprod. Immunol., 37, 79-86.
91. Vance, R.E., Kraft, J.R., Altman, J.D. et al. (1998) Mouse CD94/NKG2A is a Natural Killer cell receptor for the nonclassical Major Histocompatibility Complex (MHC) class I molecule Qa-1b. J. Exp. Med., 188, 1841-1848.
92. Verma, S., King, A. and Loke, Y.W. (1997) Expression of killer cell inhibitory receptors on human uterine natural killer cells. Eur. J. Immunol., 27, 979-983.
93. Warner, C.M., Cao, W., Exley, G.E. et al. (1998) Genetic regulation of egg and embryo survival. Hum. Reprod., 13(suppl. 3), 178-196.
94. Webb, B., Bochan, M., Montel, A. et al. (1994) The lack of NK cytotoxicity associated with fresh HUCB may be due to the presence of soluble HLA in the serum. Cell. Immunol., 159, 246-261.
95. Wei, X. and Orr, H.T. (1990) Differential expression of HLA-E, HLA-F, and HLA-G transcripts in human tissue. Hum. Immunol., 29, 131-142.
96. Wolf, P.R. and Cook, R.G. (1995) The class I-b molecule Qa-1 forms heterodimers with H-2Ld and a novel 50-kD glycoprotein encoded centromeric to I-E beta. J. Exp. Med., 181, 657-668.
97. Yang, Y., Chu, W., Geraghty, D.E. and Hunt, J.S. (1996) Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J. Immunol., 156, 4224-4231.
98. Yelavarthi, K.K., Fishback, J.L. and Hunt, J.S. (1991) Analysis of HLA-G mRNA in human placental and extraplacental membrane cells by in situ hybridization. J. Immunol., 146, 2847-2854.
99. Yokoyama, W.M. (1997) The mother-child union: the case of missing-self and protection of the fetus. Proc. Natl Acad. Sci. USA, 94, 5998-6000.
100. Zavazava, N. and Kronke, M. (1996) Soluble HLA class I molecules induce apoptosis in alloreactive cytotoxic T lymphocytes. Nature Med., 2, 1005-1010.
101. Zhou, M. and Mellor, A.L. (1998) Expanded cohorts of maternal CD8+ T cells specific for paternal MHC class I accumulate during pregnancy. J. Reprod. Immunol., 40, 47-62.