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Erschienen in: Journal of Assisted Reproduction and Genetics 7/2007

01.07.2007

HLA-G and its role in implantation (review)

verfasst von: Roumen G. Roussev, Carolyn B. Coulam

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 7/2007

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Abstract

Background

Human leukocyte antigen G (HLA-G) is thought to play a key role in implantation by modulating cytokine secretion to control trophopblastic cell invasion and to maintain a local immunotolerance.

Method of study

The literature is reviewed to provide a description of the genetic background, properties of the protein, and the function of HLA-G. Data are presented on potential clinical applications of HLA-G including the use of evaluation of HLA-G gene polymorphisms in the diagnosis of patients experiencing recurrent pregnancy loss and evaluation and testing of soluble HLA-G (sHLA-G) in embryo culture media for the selection of embryos for transfer after in vitro fertilization (IVF).

Results

The literature supports a central role of HLA-G for successful implantation. Of couples experiencing recurrent pregnancy loss, 32% demonstrated the -1725G HLA-G polymorphism. Our data showed that when embryos were selected for transfer after IVF based on culture media concentrations of sHLA-G ≥ 2 U/ml and good morphologic grade, a 65% pregnancy rate compared with a 0% pregnancy rate in those with <2 U/ml sHLA-G.

Conclusions

HLA-G is important for successful implantation in human beings. The HLA-G -725 promoter polymorphism is a risk factor for recurrent miscarriage. Measurement of sHLA-G in embryo culture media can help select embryos for transfer after IVF allowing fewer embryos to be transferred in an attempt to lower multiple gestation rates.
Literatur
1.
Zurück zum Zitat Hunt JS. HLA and maternal–fetal relationship. Austin: RG Landes Co.; 1996. Hunt JS. HLA and maternal–fetal relationship. Austin: RG Landes Co.; 1996.
2.
Zurück zum Zitat Puppo F, Ghio M, Contini P, Brenci S, Bignardi D, Filaci G, et al. Immunoregulatory role of soluble HLA molecules: a new skin for an old subject? Arch Immunol Ther Exp 1998;46:157–60. Puppo F, Ghio M, Contini P, Brenci S, Bignardi D, Filaci G, et al. Immunoregulatory role of soluble HLA molecules: a new skin for an old subject? Arch Immunol Ther Exp 1998;46:157–60.
3.
Zurück zum Zitat Chu W, Fant ME, Geraghty DE, Hunt JS. Soluble HLA-G in human placentas: synthesis in trophoblasts and in interferon-gamma-activated macrophages but not placental fibroblasts. Hum Immunol 1998;59:435–42.PubMedCrossRef Chu W, Fant ME, Geraghty DE, Hunt JS. Soluble HLA-G in human placentas: synthesis in trophoblasts and in interferon-gamma-activated macrophages but not placental fibroblasts. Hum Immunol 1998;59:435–42.PubMedCrossRef
4.
Zurück zum Zitat Ellis SA, Sargent IL, Redman CW, McMichael AJ. Evidence for a novel HLA antigen found on human extravillous trophoblast and a choriocarcinoma cell line. Immunology 1986;59:595–601.PubMed Ellis SA, Sargent IL, Redman CW, McMichael AJ. Evidence for a novel HLA antigen found on human extravillous trophoblast and a choriocarcinoma cell line. Immunology 1986;59:595–601.PubMed
5.
Zurück zum Zitat Ishitani A, Geraghty DE. Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc Natl Acad Sci USA 1992;89:3947–51.PubMedCrossRef Ishitani A, Geraghty DE. Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc Natl Acad Sci USA 1992;89:3947–51.PubMedCrossRef
6.
Zurück zum Zitat Kirszenbaum M, Moreau P, Gluckman E, Dausset J, Carosella E. An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc Natl Acad Sci USA 1994;91:4209–13.PubMedCrossRef Kirszenbaum M, Moreau P, Gluckman E, Dausset J, Carosella E. An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc Natl Acad Sci USA 1994;91:4209–13.PubMedCrossRef
7.
Zurück zum Zitat Fujii T, Ishitani A, Geraghty DE. A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 1994;153:5516–24.PubMed Fujii T, Ishitani A, Geraghty DE. A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 1994;153:5516–24.PubMed
8.
Zurück zum Zitat Paul P, Cabestre FA, Ibrahim EC, Lefebvre S, Khalil-Daher I, Vazeux G, et al. Identification of HLA-G7 as a new splice variant of the HLA-G mRNA and expression of soluble HLA-G5, -G6, and -G7 transcripts in human transfected cells. Hum Immunol 2000;61:1138–49.PubMedCrossRef Paul P, Cabestre FA, Ibrahim EC, Lefebvre S, Khalil-Daher I, Vazeux G, et al. Identification of HLA-G7 as a new splice variant of the HLA-G mRNA and expression of soluble HLA-G5, -G6, and -G7 transcripts in human transfected cells. Hum Immunol 2000;61:1138–49.PubMedCrossRef
9.
Zurück zum Zitat Loke YW, King A. Human implantation: cell biology and immunlogy. Cambridge: Cambridge University Press; 1995. Loke YW, King A. Human implantation: cell biology and immunlogy. Cambridge: Cambridge University Press; 1995.
10.
Zurück zum Zitat Hunt SJ, Petroff MG, McIntyre RH, Ober C. HLA-G and immune tolerance in pregnancy. FASEB J 2005;5:681–93.CrossRef Hunt SJ, Petroff MG, McIntyre RH, Ober C. HLA-G and immune tolerance in pregnancy. FASEB J 2005;5:681–93.CrossRef
11.
Zurück zum Zitat Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bansusan A, Geraghty DE, et al. Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol 1997;27:3380–8.PubMedCrossRef Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bansusan A, Geraghty DE, et al. Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol 1997;27:3380–8.PubMedCrossRef
12.
Zurück zum Zitat McMaster M, Zhou Y, Shorter S, Kapasi K, Geraghty D, Lim K, et al. HLA-G isoforms produced by placental cytotrophoblast and found in amniotic fluid are due to unusual glycosylation. J Immunol 1998;160:5922–8.PubMed McMaster M, Zhou Y, Shorter S, Kapasi K, Geraghty D, Lim K, et al. HLA-G isoforms produced by placental cytotrophoblast and found in amniotic fluid are due to unusual glycosylation. J Immunol 1998;160:5922–8.PubMed
13.
Zurück zum Zitat Crisa L, McMaster M, Ishii JK, Fisher S, Salomon DR. Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J Exp Med 1997;186:289–98.PubMedCrossRef Crisa L, McMaster M, Ishii JK, Fisher S, Salomon DR. Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J Exp Med 1997;186:289–98.PubMedCrossRef
14.
Zurück zum Zitat Yang Y, Chu W, Geraghty DE, Hunt S. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol 1996;156:4224–31.PubMed Yang Y, Chu W, Geraghty DE, Hunt S. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol 1996;156:4224–31.PubMed
15.
Zurück zum Zitat Parham P, Lomen CE, Lawlor DA, Ways JP, Holmes N, Coppin HL, et al. Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci USA 1988;85:4005–9.PubMedCrossRef Parham P, Lomen CE, Lawlor DA, Ways JP, Holmes N, Coppin HL, et al. Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci USA 1988;85:4005–9.PubMedCrossRef
16.
Zurück zum Zitat Shimizu Y, Geraghty DE, Koller BH, Orr HT, DeMars R. Transfer and expression of three cloned human non-HLA-A,B,C class I major histocompatibility complex genes in mutant lymphoblastoid cells. Proc Natl Acad Sci USA 1988;85:227–31.PubMedCrossRef Shimizu Y, Geraghty DE, Koller BH, Orr HT, DeMars R. Transfer and expression of three cloned human non-HLA-A,B,C class I major histocompatibility complex genes in mutant lymphoblastoid cells. Proc Natl Acad Sci USA 1988;85:227–31.PubMedCrossRef
17.
Zurück zum Zitat Dobbe LM, Stam NJ, Neefjes JJ, Giphart MJ. Biochemical complexity of serum HLA class I molecules. Immunogenetics 1988;27:203–10.PubMedCrossRef Dobbe LM, Stam NJ, Neefjes JJ, Giphart MJ. Biochemical complexity of serum HLA class I molecules. Immunogenetics 1988;27:203–10.PubMedCrossRef
18.
Zurück zum Zitat Van Rood JJ, Van Leeuwan A, Van Santen MCT. Anti-HLA-A2 inhibitor in normal human sera. Nature 1970;226:336–67.CrossRef Van Rood JJ, Van Leeuwan A, Van Santen MCT. Anti-HLA-A2 inhibitor in normal human sera. Nature 1970;226:336–67.CrossRef
19.
Zurück zum Zitat Haga JA, She JX, Kao KJ. Biochemical characterization of 39 kDa class I histocompatibility antigen plasma. A secretable membrane protein derived from transmembrane domain deletion. J Biol Chem 1991;266:3695–701.PubMed Haga JA, She JX, Kao KJ. Biochemical characterization of 39 kDa class I histocompatibility antigen plasma. A secretable membrane protein derived from transmembrane domain deletion. J Biol Chem 1991;266:3695–701.PubMed
20.
Zurück zum Zitat LeMaoult J, Zafaranloo K, Le Danff C, Carosella ED. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen-presenting cells, NK cells, and T cells. FASEB J 2005;19:662–4.PubMed LeMaoult J, Zafaranloo K, Le Danff C, Carosella ED. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen-presenting cells, NK cells, and T cells. FASEB J 2005;19:662–4.PubMed
21.
Zurück zum Zitat Fournel S, Aguerre-Girr M, Huc X, Lenfant F, Alam A, Toubert A, et al. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J Immunol 2000;164:6100–4.PubMed Fournel S, Aguerre-Girr M, Huc X, Lenfant F, Alam A, Toubert A, et al. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J Immunol 2000;164:6100–4.PubMed
22.
Zurück zum Zitat Morales PJ, Pace JL, Platt JS, Phillips TA, Morgan K, Fazleabas AT, et al. Placental cell expression of HLA-G2 isoforms is limited to the invasive trophoblast phenotype. J Immunol 2003;171:6215–24.PubMed Morales PJ, Pace JL, Platt JS, Phillips TA, Morgan K, Fazleabas AT, et al. Placental cell expression of HLA-G2 isoforms is limited to the invasive trophoblast phenotype. J Immunol 2003;171:6215–24.PubMed
23.
Zurück zum Zitat Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999;189:1093–100.PubMedCrossRef Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999;189:1093–100.PubMedCrossRef
24.
Zurück zum Zitat van der Meer A, Lukassen HG, van Cranenbroek B, Weiss EH, Braat DD, van Lierop MJ, et al. Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod 2007;13:123–33.PubMedCrossRef van der Meer A, Lukassen HG, van Cranenbroek B, Weiss EH, Braat DD, van Lierop MJ, et al. Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod 2007;13:123–33.PubMedCrossRef
25.
Zurück zum Zitat McIntire RH, Morales PJ, Petroff MG, Colonna M, Hunt JS. Recombinant HLA-G5 and -G6 drive U937 myelomonocytic cell production of TGF-beta-1. J Leukoc Biol 2004;76:1220–8.PubMedCrossRef McIntire RH, Morales PJ, Petroff MG, Colonna M, Hunt JS. Recombinant HLA-G5 and -G6 drive U937 myelomonocytic cell production of TGF-beta-1. J Leukoc Biol 2004;76:1220–8.PubMedCrossRef
26.
Zurück zum Zitat Kanai T, Fujii T, Kozuma S, Yamashita T, Miki A, Kikuchi A, et al. Soluble HLA-G influences the release of cytokines from allogeneic peripheral blood mononuclear cells in culture. Mol Hum Reprod 2001;7:195–200.PubMedCrossRef Kanai T, Fujii T, Kozuma S, Yamashita T, Miki A, Kikuchi A, et al. Soluble HLA-G influences the release of cytokines from allogeneic peripheral blood mononuclear cells in culture. Mol Hum Reprod 2001;7:195–200.PubMedCrossRef
27.
Zurück zum Zitat Kapasi K, Albert SE, Yie S, Zavazava N, Librach CL. HLA-G has concentration-dependent effect on the generation of an allo-CTL response. Immunology 2000;101:191–200.PubMedCrossRef Kapasi K, Albert SE, Yie S, Zavazava N, Librach CL. HLA-G has concentration-dependent effect on the generation of an allo-CTL response. Immunology 2000;101:191–200.PubMedCrossRef
28.
Zurück zum Zitat Roussev RG, Ng SC, Coulam CB. Natural killer cell functional activity suppression by intravenous immunoglobulin, intralipid and soluble human leucocyte antigen-G. Am J Reprod Immunol 2007;57:262–9.PubMedCrossRef Roussev RG, Ng SC, Coulam CB. Natural killer cell functional activity suppression by intravenous immunoglobulin, intralipid and soluble human leucocyte antigen-G. Am J Reprod Immunol 2007;57:262–9.PubMedCrossRef
29.
Zurück zum Zitat Marchal-Bras-Goncalves R, Rouas-Freiss N, Connan F, Choppin J, Dausset J, Carosella ED, et al. A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant Proc 2001;33:2355–9.PubMedCrossRef Marchal-Bras-Goncalves R, Rouas-Freiss N, Connan F, Choppin J, Dausset J, Carosella ED, et al. A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant Proc 2001;33:2355–9.PubMedCrossRef
30.
Zurück zum Zitat Hackmon R, Hallak M, Krup M, Weitzman D, Sheiner E, Kaplan B, et al. HLA-G antigen and parturition: maternal serum, fetal serum and amniotic fluid levels during pregnancy. Fetal Diagn Ther 2004;19:404–9.PubMedCrossRef Hackmon R, Hallak M, Krup M, Weitzman D, Sheiner E, Kaplan B, et al. HLA-G antigen and parturition: maternal serum, fetal serum and amniotic fluid levels during pregnancy. Fetal Diagn Ther 2004;19:404–9.PubMedCrossRef
31.
Zurück zum Zitat Ober C, Aldrich C, Rosinsky B, Robertson A, Walker MA, Willadsen S, et al. HLA-G1 protein expression is not essential for fetal survival. Placenta 1998;19:127–32.PubMedCrossRef Ober C, Aldrich C, Rosinsky B, Robertson A, Walker MA, Willadsen S, et al. HLA-G1 protein expression is not essential for fetal survival. Placenta 1998;19:127–32.PubMedCrossRef
32.
Zurück zum Zitat Aldrich CL, Stephenson MD, Karrison T, Odem RR, Branch DW, Scott JR, et al. HLA-G genotypes and pregnancy outcome in couples with unexplained recurrent miscarriage. Mol Hum Reprod 2001;7:1167–72.PubMedCrossRef Aldrich CL, Stephenson MD, Karrison T, Odem RR, Branch DW, Scott JR, et al. HLA-G genotypes and pregnancy outcome in couples with unexplained recurrent miscarriage. Mol Hum Reprod 2001;7:1167–72.PubMedCrossRef
33.
Zurück zum Zitat Pfeiffer KA, Fimmers R, Engels G, van der Ven H, van der Ven K. The HLA-G genotype is potentially associated with idiopathic recurrent spontaneous abortion. Mol Hum Reprod 2001;7:373–8.PubMedCrossRef Pfeiffer KA, Fimmers R, Engels G, van der Ven H, van der Ven K. The HLA-G genotype is potentially associated with idiopathic recurrent spontaneous abortion. Mol Hum Reprod 2001;7:373–8.PubMedCrossRef
34.
Zurück zum Zitat Hviid TV, Sorensen S, Morling N. Polymorphism in the regulatory region located more than 1.1 kilobases 5′ to the start site of transcription, the promoter region, and exon 1 of the HLA-G gene. Hum Immunol 1999;60:1237–44.PubMedCrossRef Hviid TV, Sorensen S, Morling N. Polymorphism in the regulatory region located more than 1.1 kilobases 5′ to the start site of transcription, the promoter region, and exon 1 of the HLA-G gene. Hum Immunol 1999;60:1237–44.PubMedCrossRef
35.
Zurück zum Zitat Ober C, Aldrich CL, Chervoneva I, Billstrend C, Rahimov F, Gray HL, et al. Variation in the HLA-G promoter region influences miscarriage rates. Am J Hum Genet 2003;72:1425–35.PubMedCrossRef Ober C, Aldrich CL, Chervoneva I, Billstrend C, Rahimov F, Gray HL, et al. Variation in the HLA-G promoter region influences miscarriage rates. Am J Hum Genet 2003;72:1425–35.PubMedCrossRef
36.
Zurück zum Zitat Jurisicova A, Casper RF, MacLusky NJ, Mills GB, Librach CL. HLA-G expression during pre-implantation human embryo development. Proc Natl Acad Sci USA 1996;93:161–5.PubMedCrossRef Jurisicova A, Casper RF, MacLusky NJ, Mills GB, Librach CL. HLA-G expression during pre-implantation human embryo development. Proc Natl Acad Sci USA 1996;93:161–5.PubMedCrossRef
37.
Zurück zum Zitat Menicucci A, Noci I, Fuzzi B, Criscuoli L, Scarselli G, Baricordi O, et al. Non-classic sHLA class I in human oocyte culture medium. Hum Immunol 1999;60:1054–7.PubMedCrossRef Menicucci A, Noci I, Fuzzi B, Criscuoli L, Scarselli G, Baricordi O, et al. Non-classic sHLA class I in human oocyte culture medium. Hum Immunol 1999;60:1054–7.PubMedCrossRef
38.
Zurück zum Zitat McElhinny AS, Exley GE, Warner CM. Painting Qa-2 onto Ped slow preimplantation embryos increases the rate of cleavage. Am J Reprod Immunol 2000;44:52–8.PubMedCrossRef McElhinny AS, Exley GE, Warner CM. Painting Qa-2 onto Ped slow preimplantation embryos increases the rate of cleavage. Am J Reprod Immunol 2000;44:52–8.PubMedCrossRef
39.
Zurück zum Zitat Fuzzi B, Rizzo R, Criscuoli L, Noci I, Melchiorri L, Scarselli B, et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002;32:311–5.PubMedCrossRef Fuzzi B, Rizzo R, Criscuoli L, Noci I, Melchiorri L, Scarselli B, et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002;32:311–5.PubMedCrossRef
40.
Zurück zum Zitat Roussev RG, Keskintepe L, Coulam CB, Sher G, Maasarani G. Soluble HLA-G (sHLA-G) in human embryo culture media: a useful marker for assessing embryo quality and implantation potential for IVF. Fertil Steril 2003;80(Suppl 3):S12.CrossRef Roussev RG, Keskintepe L, Coulam CB, Sher G, Maasarani G. Soluble HLA-G (sHLA-G) in human embryo culture media: a useful marker for assessing embryo quality and implantation potential for IVF. Fertil Steril 2003;80(Suppl 3):S12.CrossRef
41.
Zurück zum Zitat Sher G, Keskintepe L, Nouriani M, Roussev R, Batzofin J. Expression of sHLA-G in supernatants of individually cultured 46-h embryos: a potentially valuable indicator of ‘embryo competency’ and IVF outcome. Reprod Biomed Online 2004;9:74–8.PubMedCrossRef Sher G, Keskintepe L, Nouriani M, Roussev R, Batzofin J. Expression of sHLA-G in supernatants of individually cultured 46-h embryos: a potentially valuable indicator of ‘embryo competency’ and IVF outcome. Reprod Biomed Online 2004;9:74–8.PubMedCrossRef
42.
Zurück zum Zitat Roussev RG, Coulam CB. Detection of soluble HLA-G levels in embryo culture media is predictive for embryo quality and successful pregnancy in IVF. Am J Reprod Immunol 2004;51:471–2. Roussev RG, Coulam CB. Detection of soluble HLA-G levels in embryo culture media is predictive for embryo quality and successful pregnancy in IVF. Am J Reprod Immunol 2004;51:471–2.
43.
Zurück zum Zitat Sergent IL. Does ‘soluble’ HLA-G really exist? Another twist to the tale. Mol Hum Reprod 2005;11:695–8.CrossRef Sergent IL. Does ‘soluble’ HLA-G really exist? Another twist to the tale. Mol Hum Reprod 2005;11:695–8.CrossRef
44.
Zurück zum Zitat Menezo Y, Elder K, Viville S. Soluble HLA-G release by the human embryo: an interesting artefact? Reprod Biomed Online 2006;13:763–4.PubMedCrossRef Menezo Y, Elder K, Viville S. Soluble HLA-G release by the human embryo: an interesting artefact? Reprod Biomed Online 2006;13:763–4.PubMedCrossRef
45.
Zurück zum Zitat Yie SM, Li LH, Li YM, Librach C. HLA-G protein concentrations in maternal serum and placental tissue are decreased in preeclampsia. Am J Obstet Gynecol 2004;191:525–9.PubMedCrossRef Yie SM, Li LH, Li YM, Librach C. HLA-G protein concentrations in maternal serum and placental tissue are decreased in preeclampsia. Am J Obstet Gynecol 2004;191:525–9.PubMedCrossRef
46.
Zurück zum Zitat Emmer PM, Steegers EA, van Lierop MJ, Steegers-Theunissen RP, Loke YW, Joosten I. Amniotic fluid soluble human leukocyte antigen G is markedly decreased in offspring with neural tube defects. Early Hum Dev 2002;66:101–5.PubMedCrossRef Emmer PM, Steegers EA, van Lierop MJ, Steegers-Theunissen RP, Loke YW, Joosten I. Amniotic fluid soluble human leukocyte antigen G is markedly decreased in offspring with neural tube defects. Early Hum Dev 2002;66:101–5.PubMedCrossRef
47.
Zurück zum Zitat Fuzzi B, Rizzo R, Criscuoli L, Noci I, Melchiorri L, Scarselli B, et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002;32:311–5.PubMedCrossRef Fuzzi B, Rizzo R, Criscuoli L, Noci I, Melchiorri L, Scarselli B, et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002;32:311–5.PubMedCrossRef
48.
Zurück zum Zitat Rebmann V, Pfeiffer K, Passler M, Ferrone S, Maier S, Weiss E, et al. Detection of soluble HLA-G molecules in plasma and amniotic fluid. Tissue Antigens 1999;53:14–22.PubMedCrossRef Rebmann V, Pfeiffer K, Passler M, Ferrone S, Maier S, Weiss E, et al. Detection of soluble HLA-G molecules in plasma and amniotic fluid. Tissue Antigens 1999;53:14–22.PubMedCrossRef
49.
Zurück zum Zitat Sebti Y, Le Friec G, Pangault C, Gros F, Drenou B, Guilloux V, et al. Soluble HLA-G molecules are increased in lymphoproliferative disorders. Hum Immunol 2003;64:1093–101.PubMedCrossRef Sebti Y, Le Friec G, Pangault C, Gros F, Drenou B, Guilloux V, et al. Soluble HLA-G molecules are increased in lymphoproliferative disorders. Hum Immunol 2003;64:1093–101.PubMedCrossRef
50.
Zurück zum Zitat Hunt JS, Jadhav L, Chu W, Geraghty DE, Ober C. Soluble HLA-G circulates in maternal blood during pregnancy. Am J Obstet Gynecol 2000;183:682–8.PubMedCrossRef Hunt JS, Jadhav L, Chu W, Geraghty DE, Ober C. Soluble HLA-G circulates in maternal blood during pregnancy. Am J Obstet Gynecol 2000;183:682–8.PubMedCrossRef
51.
Zurück zum Zitat Rebmann V, Lamaoult J, Rouas-Freiss N, Carosella ED, Grosse-Wilde H. Report of the wet workshop for quantification of soluble HLA-G in Essen, 2004. Hum Immunol 2005;66:853–63.PubMedCrossRef Rebmann V, Lamaoult J, Rouas-Freiss N, Carosella ED, Grosse-Wilde H. Report of the wet workshop for quantification of soluble HLA-G in Essen, 2004. Hum Immunol 2005;66:853–63.PubMedCrossRef
52.
Zurück zum Zitat Pfeiffer KA, Rebman V, Passier M, van der Ven K, van der Ven H, Krebs D, et al. Soluble HLA levels in early pregnancy after in vitro fertilization. Hum Immunol 2000;61:559–64.PubMedCrossRef Pfeiffer KA, Rebman V, Passier M, van der Ven K, van der Ven H, Krebs D, et al. Soluble HLA levels in early pregnancy after in vitro fertilization. Hum Immunol 2000;61:559–64.PubMedCrossRef
53.
Zurück zum Zitat Van Lierop MJ, Wijnands F, Loke YW, Emmer PM, Lukassen HG, Braat DD, et al. Detection of HLA-G by a specific sandwich ELISA using monoclonal antibodies 6233 and 56B. Mol Hum Reprod 2002;8:776–84.PubMedCrossRef Van Lierop MJ, Wijnands F, Loke YW, Emmer PM, Lukassen HG, Braat DD, et al. Detection of HLA-G by a specific sandwich ELISA using monoclonal antibodies 6233 and 56B. Mol Hum Reprod 2002;8:776–84.PubMedCrossRef
54.
Zurück zum Zitat Lim KH, Zhou Y, Janatpour M, McMaster M, Bass K, Chun SH, et al. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol 1997;151:1809–18.PubMed Lim KH, Zhou Y, Janatpour M, McMaster M, Bass K, Chun SH, et al. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol 1997;151:1809–18.PubMed
55.
Zurück zum Zitat Pijnenborg R, Dixon G, Robertson WB, Brosens I. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980;1:3–19.PubMedCrossRef Pijnenborg R, Dixon G, Robertson WB, Brosens I. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980;1:3–19.PubMedCrossRef
56.
Zurück zum Zitat Redman CW. Immunology of preeclampsia. Semin Perinatol 1991;15:257–62.PubMed Redman CW. Immunology of preeclampsia. Semin Perinatol 1991;15:257–62.PubMed
57.
Zurück zum Zitat Hara N, Fujii T, Yamashita T, Kozuma S, Okai T, Taketani Y. Altered expression of human leukocyte antigen G (HLA-G) on extravillous trophoblasts in preeclampsia: immunohistological demonstration with anti-HLA-G specific antibody “87G” and anti-cytokeratin antibody “CAM5.2”. Am J Reprod Immunol 1996;36:349–58.PubMed Hara N, Fujii T, Yamashita T, Kozuma S, Okai T, Taketani Y. Altered expression of human leukocyte antigen G (HLA-G) on extravillous trophoblasts in preeclampsia: immunohistological demonstration with anti-HLA-G specific antibody “87G” and anti-cytokeratin antibody “CAM5.2”. Am J Reprod Immunol 1996;36:349–58.PubMed
58.
Zurück zum Zitat Singer G, Rebmann V, Chen YC, Liu HT, Ali SZ, Reinsberg J, et al. HLA-G is a potential tumor marker in malignant ascites. Clin Cancer Res 2000;9:4460–4. Singer G, Rebmann V, Chen YC, Liu HT, Ali SZ, Reinsberg J, et al. HLA-G is a potential tumor marker in malignant ascites. Clin Cancer Res 2000;9:4460–4.
59.
Zurück zum Zitat Ugurel S, Rebmann V, Ferrone S, Tilgen W, Grosse-Wilde H, Reinhold U. Soluble human leukocyte antigen-G serum level is elevated in melanoma patients and is further increased by interferon-alpha immunotherapy. Cancer 2001;92:369–76.PubMedCrossRef Ugurel S, Rebmann V, Ferrone S, Tilgen W, Grosse-Wilde H, Reinhold U. Soluble human leukocyte antigen-G serum level is elevated in melanoma patients and is further increased by interferon-alpha immunotherapy. Cancer 2001;92:369–76.PubMedCrossRef
60.
Zurück zum Zitat Nuckel H, Rebmann V, Durig J, Duhrsen U, Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood 2005;105:1694–8.PubMedCrossRef Nuckel H, Rebmann V, Durig J, Duhrsen U, Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood 2005;105:1694–8.PubMedCrossRef
61.
Zurück zum Zitat Creput C, Durrbach A, Menier C, Guettier C, Samuel D, Dausset J, et al. Human leukocyte antigen-G (HLA-G) expression in biliary epithelial cells is associated with allograft acceptance in liver-kidney transplantation. J Hepatol 2003;39:587–94.PubMedCrossRef Creput C, Durrbach A, Menier C, Guettier C, Samuel D, Dausset J, et al. Human leukocyte antigen-G (HLA-G) expression in biliary epithelial cells is associated with allograft acceptance in liver-kidney transplantation. J Hepatol 2003;39:587–94.PubMedCrossRef
62.
Zurück zum Zitat Lila N, Carpentier A, Amrein C, Khalil-Daher I, Dausset J, Carosella ED. Implication of HLA-G molecule in heart-graft acceptance. Lancet 2000;355:2138–42.PubMedCrossRef Lila N, Carpentier A, Amrein C, Khalil-Daher I, Dausset J, Carosella ED. Implication of HLA-G molecule in heart-graft acceptance. Lancet 2000;355:2138–42.PubMedCrossRef
63.
Zurück zum Zitat Lila N, Amrein C, Guillemain R, Chevalier P, Latremouille C, Fabiani JN, et al. Human leukocyte antigen-G expression after heart transplantation is associated with a reduced incidence of rejection. Circulation 2002;105:1949–54.PubMedCrossRef Lila N, Amrein C, Guillemain R, Chevalier P, Latremouille C, Fabiani JN, et al. Human leukocyte antigen-G expression after heart transplantation is associated with a reduced incidence of rejection. Circulation 2002;105:1949–54.PubMedCrossRef
Metadaten
Titel
HLA-G and its role in implantation (review)
verfasst von
Roumen G. Roussev
Carolyn B. Coulam
Publikationsdatum
01.07.2007
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 7/2007
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-007-9148-3

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