On the role of placental major histocompatibility complex and decidual leukocytes in implantation and pregnancy success using non-human primate models

International Journal of Developmental Biology

Volumn 54, Issue 2-3, 2010, Pages 431-443

  Golos, Thaddeus G ^a,b,c   Bondarenko, Gennadiy I ^c   Dambaeva, Svetlana V ^a,c   Breburda, Edith E ^c   Durning, Maureen ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Decidua; HLA G; NK cell; Placenta

Indexed keywords

GLYCOPROTEIN; HLA G ANTIGEN; IMMUNOGLOBULIN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR; PROTEIN ANTIBODY; PROTEIN MAMU AG; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY REACTION; ANTIGEN EXPRESSION; ARTICLE; DECIDUA; FETOPLACENTAL UNIT; GENE LOCUS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LEUKOCYTE; LYMPHOCYTE TRANSFER; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NIDATION; NONHUMAN; PASSIVE IMMUNIZATION; PLACENTA; PLACENTA DEVELOPMENT; PREGNANCY; PREGNANCY OUTCOME; PREMATURE LABOR; PRIORITY JOURNAL; RHESUS MONKEY; TROPHOBLAST; ANIMAL; FEMALE; FETOMATERNAL TRANSFUSION; IMMUNOLOGY; MACACA; REVIEW;

ANIMALIA; BOS; MAMMALIA; OVIS ARIES; PRIMATES; RODENTIA; SUIDAE;

ANIMALS; DECIDUA; EMBRYO IMPLANTATION; FEMALE; LEUKOCYTES; MACACA MULATTA; MAJOR HISTOCOMPATIBILITY COMPLEX; MATERNAL-FETAL EXCHANGE; PLACENTA; PREGNANCY; PREGNANCY OUTCOME;

EID: 77950343004     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082797tg     Document Type: Article

References (94)

1. ADAMS WALDORF, K.M., PERSING, D., NOVY, M.J., SADOWSKY, D.W., GRAVETT, M.G. (2008). Pretreatment with toll-like receptor 4 antagonist inhibits lipopolysaccharid-induced preterm uterine contractability, cytokines, and prostaglandins in rhesus monkeys. Reprod. Sci. 15: 121-127.
2. ALLAN, D.S., COLONNA, M., LANIER, L.L., CHURAKOVA, T.D., ABRAMS, J.S., ELLIS, S.A., MCMICHAEL, A.J., and BRAUD, V.M. (1999). Tetrameric complexes of human histocompatibility leukocyte antigen (HLA)-G bind to peripheral blood myelomonocytic cells. J. Exp. Med. 189: 1149-1156.
3. ARNAIZ-VILLENA, A., MORALES, P., GOMEZ-CASADO, E., CASTRO, M.J., VARELA, P., ROJO-AMIGO, R., AND MARTINEZ-LASO, J. (1999). Evolution of MHC-G in primates: a different kind of molecule for each group of species. J. Reprod. Immunol. 43: 111-125.
4. ASHKAR, A.A., DISANTO, J.P., and CROY, B.A. (2000). Interferon gamma Contributes to Initiation of Uterine Vascular Modification, Decidual Integrity, and Uterine Natural Killer Cell Maturation during Normal Murine Pregnancy. J. Exp. Med. 192: 259-269.
5. BONDARENKO, G.M., DURNING, M., BURLEIGH, D., BREBURDA, E., GRENDELL, R., and GOLOS, T.G. (2007). Passive immunization against the MHC Class I molecule disrupts rhesus placental development and endometrial responses. J. Immunol. 179: 8042-8050.
6. BONDARENKO, G.I., DAMBAEVA, S.V., GRENDELL, R.L., HUGHES, A.L., DURNING, M., GARTHWAITE, M.A. and GOLOS T.G. (2009). Characterization of cynomolgus and vervet monkey placental MHC class I expression: Diversity of the nonhuman primate AG locus. Immunogenetics 61: 431-442.
7. BOYSON, J.E., MCADAM, S.N., GALLIMORE, A., GOLOS T.G., LIU, X., GOTCH, F.M., HUGHES, A.L., and WATKINS, D.I. (1995). The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41: 59-68.
8. BOYSON, J.E., IWANAGA, K.K., GOLOS, T.G., and WATKINS, D.I. (1996). Identification of the rhesus monkey HLA-G ortholog Mamu-G is a pseudogene. J. Immunol. 157: 5428-5437.
9. BOYSON, J.E., IWANAGA, K.K., GOLOS, T.G., and WATKINS, D.I. (1997). Identification of a novel MHC class I gene, Mamu-AG in the placenta of primate with an inactivated G locus. J. Immunol. 159: 3311-3321.
10. BREBURDA, E.E., DAMBAEVA, S.V., SLUKVIN, I.I., and GOLOS, T.G. (2006). Selective distribution and pregnancy specific expression of DC-SIGN at the maternal-fetal interface in the rhesus macaque: DC-SIGN is a putative marker of the recognition of pregnancy. Placenta 27: 11-21.
11. CANTONI, C., VERDIANI S., FALCO, M., PESSINO, A., CILLI, R., CONTE, R., PENDE, D., PONTE, M., MIKAELSSON, M.S., MORETTA, L., and BIASSONI, R. (1998). A putative HLA class I-specific inhibitory receptor belonging to the immunoglobulin superfamily. Eur. J. Immunol. 28: 1980-1990.
12. CAROSELLA, E.D., FAVIER, B., ROUAS-FREISS, N., MOREAU, P., AND LEMAOULT, J. (2008). Beyond the increasing complexity of the immunomodulatory HLA-G molecule. Blood 111: 4862-4870.
13. CAROSELLA, E.D., MOREAU, P., ARACTINGI, S., AND ROUAS-FREISS, N. (2001). HLA-G: a shield against inflammatory aggression. Trends. Immunol. 22:553-555.
14. CARROLL, R.L., MAH, K., FANTON, J.W., MAGINNIS, G.N., BRENNER, R.M., and SLAYDEN, O.D. (2007). Assessment of menstruation in the vervet (Cercopithecus aethiops). Am. J. Primatol. 69: 901-916.
15. CHOI, E.I., WANG, R., PETERSON, L., LETVIN, N.L. and REIMANN, K.A. (2008). Use of an anti-CD16 antibody for in vivo depletion of natural killer cells in rhesus macaques. Immunology 124: 215-222.
16. CHU, W., YANG, Y., GERAGHTY, D.E., and HUNT, J.S. (1999). Interferons enhance HLA-G nRNA and protein in transfected mouse fibroblasts. J. Repro. Immunol. 42: 1-15.
17. COSIMI, A.B., CONTI, D., DELMONICO, F.L., PREFFER, F.I, WEE, S.-L., ROTHLEIN, R., FAANES, R., and COLVIN, R.B. (1990). In vivo effects of monoclonal antibody to ICAM-1 (CD54) in nonhuman primates with renal allografts. J. Immunol. 144: 4604-4612.
18. DAMBAEVA, S.V., BONDARENKO, G.I., GRENDELL R.L., KRAVITZ, R.H., DURNING, M. and GOLOS, T.G. (2008). Nonclassical MHC-E (Mamu-E) expression in the rhesus monkey placenta. Placenta 29: 58-70.
19. DAZA-VAMENTA, R., GLUSMAN, G., ROWEN, L., GUTHRIE, B., AND GERAGHTY, D.E. (2004). Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res. 14: 1501-1515.
20. DESAI, N., FILIPOVITS, J., and GOLDFARB, J. (2006). Secretion of soluble HLAG by day 3 human embryos associated with higher pregnancy and implantation rates: assay of culture media using a new ELISA kit. Reprod. Biomed. Online 13: 272-277.
21. DIEHL, M., MUNZ, C., KEILHOLZ, W., STEVANOVIC, S., HOLMES, N., LOKE, Y.W., and RAMMENSEE, H.G. (1996). Nonclassical HLA-G molecules are classical peptide presenters. Curr. Biol. 6: 305-314.
22. DOSIOU, C. and GIUDICE, L. C. (2005). Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocrine Reviews 26: 44-62.
23. ENDERS, A.C. (1993). Overview of the morphology of implantation in primates. In In vitro fertilization and embryo transfer in primates (Eds. D.P. Wolf, R.L. Stouffer, and R.M. Brenner). Springer-Verlag, New York, pp. 145-157.
24. ERIKSSON, J.G., FORSEN, T., TUOMILEHTO, J., OSMOND, C., and BARKER, D.J.P. (2001). Early growth and coronary hearth disease in later life: longitudinal study. Brit. Med. J. 233: 949-953.
25. FAZLEABAS, A.T. (2007). Physiology and pathology of implantation in the human and nonhuman primate. Semin Reprod Med. 25: 405-409.
26. FONS, P., CHABOT, S., CARTWRIGHT, J.E., LENFANT, F., L'FAQIHI, F., GIUSTINIANI, J., HERAULT, J.P., GUEGUEN, G., BONO, F., SAVI, P., AGUERRE-GIRR, M., FOURNEL, S., MALECAZE, F., BENSUSSAN, A., PLOUËT, J., AND LE BOUTEILLER, P. (2006). Soluble HLA-G1 inhibits angiogenesis through an apoptotic pathway and by direct binding to CD160 receptor expressed by endothelial cells. Blood. 108: 2608-2615.
27. FOURNEL, S., AGUERRE-GIRR, M., CAMPAN, A., SALAUZE, L., BERREBI, A., LONE, Y.-C., LENFANT, F., AND LE BOUTEILLER, P. (1999). Soluble HLA-G: Purification from eukaryotic transfected cells and detection by a specific ELISA. Am. J. Reprod. Immunol. 42: 22-29s.
28. FOURNEL, S., AGUERRE-GIRR, M., HUC, X., LENFANT, F., ALAM, A., TOUBERT, A., BENSUSSAN, A., AND LE BOUTEILLER, P. (2000). Cutting Edge: Soluble HLA-G1 triggers CD95/CD95 Ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J. Immunol. 164: 6100-6104.
29. 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.
30. FUZZI, B., RIZZO, R., CRISCUOLI, L., NOCI, I., MELCHIORRI, L., SCARSELLI, B., BENCINI, E., MENICUCCI, A., and BARICORDI, O.R. (2002). HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur. J. Immunol. 32: 311-315.
31. GIAVEDONI, L.D. (2005). Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J. Immunol. Methods. 301: 89-101.
32. GOLOS, T.G. (2003). Nonhuman primate placental MHC expression: a model for exploring mechanisms of human Maternal-Fetal immune tolerance. Hum Immunol. 64: 1102-1109.
33. GONEN-GROSS, T., ACHDOUT, H., GAZT, R., HANNA, J., MIZRAHI, S., MARKEL, G., GOLDMAN-WOHL, D., YAGEL, S., HOREJSI, V., LEVY, O., BANIYASH, M., AND MANDELBOIM, O. (2003). Complexes of HLA-G protein on the cell surface are important for leukocyte Ig-like receptor-1 function. J Immunol. 171: 1343-1351.
34. GREENE, J.M., BURWITZ, B.J., BLASKY, A.J., MATTILA, T.L., HONG, J.J., RAKASZ, E.G., WISEMAN, R.W., HASENKRUG, K.J., SKINNER, P.J., O'CONNOR, S.L., AND O'CONNOR, D.H. (2008). Allogeneic lymphocytes persist and traffic in feral MHC-matched mauritian cynomolgus macaques. PLoS ONE 3: e2384.
35. GRENDELL, R.L., HUGHES, A.L., and GOLOS, T.G. (2001). Cloning of rhesus monkey killer-cell Ig-like receptors (KIRs) from early pregnancy decidua. Tissue Antigens 58:329-334.
36. HAMAI, Y., FUJII, T., MIKI, A., GERAGHTY, D.E., HARADA, I., TAKAI, Y., KOZUMA, S., TSUTSUMI, O., and TAKETANI, Y. (1999). Quantitative assessment of human leukocyte antigen-G protein in amniotic fluid by a doubledeterminant enzyme-linked immunosorbent assay using anti-human leukocyte antigen-G-specific antibody «87G». Am. J. Reprod. Immunol. 41: 293-295.
37. HANNA, J., GOLDMAN-WOHL, D., HAMANI, Y., AVRAHAM, I., GREENFIELD, C., NATANSON-YARON, S., PRUS, D., COHEN-DANIEL, L., ARNON, T.I., MANASTER, I., GAZIT, R., YUTKIN, V., BENHARROCH, D., PORGADOR, A., KESHET, E., YAGEL, S., AND MANDELBOIM, O. (2006). Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12: 1065-1074.
38. HODGEN, G.D., TULLNER, W.W., VAITUKAITIS, J.L., WARD, D.N., and ROSS, G.T. (1974). Specific radioimmunoassay of chorionic gonadotropin during implantation in rhesus monkeys. J. Clin. Endocrinol. Metab. 39: 457-464.
39. HODGES, J.K., and HEARN, J.P. (1977). Effects of immunisation against luteinising hormone releasing hormone on reproduction of the marmoset monkey Callithrixjacchus. Nature. 265: 746-748.
40. HUNT, J.S. (2006). Stranger in a strange land. Immunol. Rev. 213: 36-47.
41. HUNT, J.S., JADHAV, L., CHU, W., GERAGHTY, D.E., and OBER, C. (2000). Soluble HLA-G circulates in maternal blood during pregnancy. Am. J. Obstet. Gynecol. 183: 682-688.
42. 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: 2669-2673.
43. ISHITANI, A., SAGESHIMA, N., LEE, N., DOROFEEVA, N., HATAKE, K., MARQUARDT, H., and GERAGHTY, D.E. (2003). Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J. Immunol., 171: 1376-1384.
44. JONKER, M., VAN LAMBALGEN, R., MITCHELL, D.J., DURHAM, S.K., and STEINMAN, L. (1988). Successful treatment of EAE in rhesus monkeys with MHC class II specific monoclonal antibodies. J. Autoimmun. 1: 399-414.
45. KING, A., ALLAN, D.S., BOWEN, M., POWIS, S.J., JOSEPH, S., VERMA, S., HIBY, S.E., MCMICHAEL, A.J., LOKE, Y.W., and Braudt, V.M. (2000). HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 30:1623-1631.
46. KOOPMAN, L.A., KOPCOW, H.D., RYBALOV, B., BOYSON, J.E., ORANGE, J.S., SCHATZ, F., MASCH, R., LOCKWOOD, C.J., SCHACHTER, A.D., PARK, P.J., and STROMINGER, J.L. (2003). Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198: 1201-1212.
47. KOVATS, S., MAIN, E.K., LIBRACH, C., STUBBLEBINE, M., FISHER, S.J., and DEMARS, R. (1990). A class I antigen, HLA-G, expressed in human trophoblasts. Science 248: 220-223.
48. KRAVITZ, R.H., GRENDELL, R.L., SLUKVIN, I.I., and GOLOS, T.G. (2001). Selective expression of NKG2-A and NKG2-C mRNAs and novel alternative splicing of 5' exons in rhesus monkey decidua. Immunogenetics 53: 69-73.
49. KWAK-KIM, J., KIM, J.W., AND GILMAN-SACHS, A. (2004). Immunology and pregnancy losses: HLA, autoantibodies and cellular immunity. In Immunology of Pregnancy (Ed. G. Mor), Landes Bioscience/Eurekah.com, Georgetown, TX, pp. 122-134.
50. LABONTE, M. L., LEVY, D. B., and LETVIN, N. L. (2000). Characterization of rhesus monkey CD94/NKG2 family members and identification of novel transmembrane-deleted forms of NKG2-A, B, C, and D. Immunogenetics 51: 496-499.
51. LACHAPELLE, M.H., MIRON, P., HEMMINGS, R., and ROY, D.C. (1996). Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J. Immunol. 156: 4027-4034.
52. LANGAT, D.K., FAZLEABAS, A.T., and HUNT, J.S. (2006). Methods for evaluating histocompatibility antigen gene expression in the baboon. In Placenta and Trophoblast: Methods and Protocols (Vol. 2) (Eds. M. J. Soares and J. S. Hunt). Humana Press, New Jersey, pp. 165-180.
53. LEBOUTEILLER, P. (2000). HLA-G in the human placenta: expression and potential functions. Biochem. Soc. Trans. 28: 208-212.
54. LEE, N., MALACKO, A.R., ISHITANI, A., CHEN, M.C., BAJORATH, J., MARQUARDT, H., and GERAGHTY, D.E. (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.
55. LI, X.F., CHARNOCK-JONES, D.S., ZHANG, E., HIBY, S., MALIK, S., DAY, K., LICENCE, D., BOWEN, J.M., GARDNER, L., KING, A., LOKE, Y.W., AND SMITH, S.K. (2001). Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 86: 1823-1834.
56. LOKE, Y.W., KING, A., BURROWS, T., GARDNER, L., BOWEN, M., HIBY, S., HOWLETT, S., HOLMES, N., and JACOBS, D. (1997). Evaluation of trophoblast HLA-G antigen with specific monoclonal antibody. Tissue Antigens 50: 135-146.
57. MAYHEW, T.M., CHARNOCK-JONES, D.S., AND KAUFMANN, P. (2004a). Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta. 25: 127-139.
58. MAYHEW, T.M., WIJESEKARA, J., BAKER, P.N., and ONG, S.S. (2004b). Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta. 25: 829-833.
59. MCINTIRE, R.H., MORALES, P.J., PETROFF, M.G., COLONNA, M., and HUNT, J.S. (2004). Recombinant HLA-G5 and -G6 drive U937 myelomonocytic cell production of TGF-b1. J Leukocyte Biol. 76: 1220-1223.
60. MEDHAMURTHY, R., ABEYAWARDENE, S.A., CULLER, M.D., NEGRO-VILAR, A., AND PLANT, T.M. (1990). Immunoneutralization of circulating inhibin in the hypophysiotropically clamped male rhesus monkey (Macaca mulatta) results in a selective hypersecretion of follicle-stimulating hormone. Endocrinol. 126: 2116-2124.
61. MEDHAMURTHY, R., CULLER, M.D., GAY, V.L., NEGRO-VILAR, A., AND PLANT, T.M. (1991). Evidence that inhibit plays a major role in the regulation of folliclestimulating hormone secretion in the fully adult male rhesus monkey (Macaca mulatta). Endocrinol. 129: 389-395.
62. MELLOR, A. L., CHANDLER, P., LEE, G.K., JOHNSON, T., KESKIN, D.B., LEE, J., and MUNN, D.H. (2002). Indoleamine 2,3-dioxygenase, immunosuppression and pregnancy. J. Repro. Immunol. 57: 143-150.
63. MOFFETT-KING, A. (2002). Natural Killer cells and pregnancy. Nat. Rev. Immunol. 2: 656-663.
64. NAVARRO, F., LLANO, M., BELLON, T., COLONNA, M., GERAGHTY, D.E., and LOPEZ-BOTET, M. (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: 277-83.
65. PACE, J.L., MORALES, P.J., PHILLIPS, T.A., and HUNT, J.S. (2006). Analysis of the soluble isoforms of HLA-G: mRNAs and Proteins. In Placenta and Trophoblast: Methods and Protocols (Vol. 2) (Eds. M. J. Soares and J. S. Hunt). Humana Press, New Jersey, pp. 181-203.
66. PONTE, M., CANTONI, C., BIASSONI, R., TRADORI-CAPPAI, A., BENTIVOGLIO, G., VITALE, C., BERTONE, S., MORETTA, A., AND MINGARI, M.C. (1999). Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc. Natl. Acad. Sci. USA 96: 5343-5345.
67. PROLL, J, BLASCHITZ, A., HARTMANN, M., THALHAMER, J., DO HR, G. (1996). Human first-trimester placenta intra-arterial trophoblast cells express the neural cell adhesion molecule. Early Pregnancy 2:271-275.
68. RAJAGOPALAN, S. and LONG, E.O. (1999). A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J. Exp. Med. 189: 1093-1099.
69. RAJAGOPALAN, S. and LONG, E.O. (2001). Activation of Resting NK Cells by the Killer-Cell IG-Like Receptor KIR2DL4. Amer. J. of Repro. Immunol. 45: 347-348.
70. RAJAGOPALAN, S., BRYCESON, Y.T., KUPPUSAMY, S.P., GERAGHTY, D.E., VAN DER MEER, A., JOOSTEN, I., and LONG, E.O. (2006). Activation of NK cells by an endocytosed receptor for soluble HLA-G. PloS Biol. 4: 70-86.
71. REBMANN, V., PFEIFFER, K., PASSLER, M., FERRONE, S., MAIER, S., WEISS, E., AND GROSSE-WILDE, H. (1999). Detection of soluble HLA-G molecules in plasma and amniotic fluid. Tissue Antigens 53: 14-22.
72. ROUAS-FREISS, N., LEMAOULT, J., MOREAU, P., DAUSSET, J., AND CAROSELLA, E.D. (2003). HLA-G in transplantation: a relevant molecule for inhibition of grant rejection. Am. J. Transplant. 3: 11-16.
73. RYAN, A.F., GRENDELL, R.G., GERAGHTY, D.E., and GOLOS, T.G. (2002). 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.
74. SADOWSKY, D.W., ADAMS, K.M., GRAVETT, M.G., WITKIN, S.S. and NOVY, M.J. (2006). Preterm labor is induced by intraamniotic infusions of interleukin1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol. 195: 1578-1589.
75. SANDERS, S.K., GIBLIN, P.A., and KAVATHAS, P. (1991). Cell-cell adhesion mediated by CD8 and human histocompatibility leukocyte antigen G, a nonclassical major histocompatibility complex class I molecule on cytotrophoblasts. J. Exp. Med. 174: 737-740.
76. SANTONI, A., CARLINO, C., STABILE, H., GISMONDI, A. (2008). Mechanisms underlying recruitment and accumulation of decidual NK cells in uterus during pregnancy. Am. J. Reprod. Immunol. 59: 417-424.
77. SCHMITZ, J.E., SIMON, M.A., KURODA, M.J., LIFTON, M.A., OLLERT, M.W., VOGEL, C.W., RACZ, P., TENNER-RACZ, K., SCALLON, B.J., DALESANDRO, M., GHRAYEB, J., RIEBER, E.P., SASSEVILLE, V.G., AND REIMANN, K.A. (1999). A nonhuman primate model for selective elimination of CD8+ lymphocytes using a mouse-human chimeric monoclonal antibody. Am. J. Pathol. 154: 1923-1932.
78. SHER, G., KESKINTEPE, L., FISCH, J.D., ACACIO, B.A., AHLERING, P., BATZOFIN, J., and GINSBURG, M. (2005). Soluble human leukocyte antigen G expression in phase I culture media at 46 hours after fertilization predicts pregnancy and implantation from day 3 embryo transfer. Fertil. Steril. 83: 1410-1413.
79. SHIROISHI, M., TSUMOTO, K., AMANO, K., SHIRAKIHARA, Y., COLONNA, M., BRAUD, V.M., ALLAN, D.S., MAKADZANGE, A., ROWLAND-JONES, S., WILLCOX, B., JONES, E.Y., VAN DER MERWE, P.A., KUMAGAI, I., AND MAENAKA, K. (2003). Human inhibitory receptors Ig-like transcript (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLAG. Proc Natl Acad Sci USA 100: 8856-8861.
80. SLUKVIN, I, BREBURDA, E.E., and GOLOS, T.G. (2004). Dynamic changes in primate endometrial leukocyte populations: differential distribution of macrophages and natural killer cells at the rhesus monkey implantation site and in early pregnancy. Placenta 25: 297-307.
81. SLUKVIN, I.I., WATKINS, D.I., and GOLOS, T.G. (1999). Tissue distribution of the mRNA for a rhesus monkey class Ib molecule, Mamu-AG. Tissue Antigens 53: 282-291.
82. SLUKVIN, I.I., WATKINS, D.I., and GOLOS, T.G. (2001). Phenotypic and functional characterization of rhesus monkey decidual lymphocytes: rhesus decidual large granular lymphocytes express CD56 and have cytolytic activity. J. Reprod. Immunol. 50: 57-79.
83. SLUKVIN, I.I., LUNN, D.P., WATKINS, D.I., and 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. USA 97: 9104-9109.
84. SLUKVIN, I.I., BOYSON, J.E., WATKINS, D.I., and GOLOS, T.G. (1998). The rhesus monkey analog of HLA-G is expressed primarily in villous syncytiotrophoblasts. Biol. Reprod. 58: 728-738.
85. STERN, P.L., BERESFORD, N., FRIEDMAN, C.I., STEVENS, V.C., RISK, J.M., and JOHNSON, P.M. (1987). Class I-like MHC molecules expressed by baboon placental syncytiotrophoblast. J. Immunol. 138: 1088-1091.
86. UGUREL, S., REINHOLD, U., and TILGEN, W. (2002). HLA-G in melanoma: A new strategy to escape from immunosurveillance? Onkologie, 25: 129-134.
87. UROSEVIC, M., and DUMMER, R. (2003). HLA-G in skin cancer: a wolf in sheep's clothing? Human Immunol. 64: 1073-1080.
88. WATKINS, D.I. (1995). The evolution of major histocompatibility class I genes in primates. Crit. Rev. Immunol. 15: 1-29.
89. WIENDL, H., MITSDOERFFER, M., HOFMEISTER, V., WISCHHUSEN, J., BORNEMANN, A., MEYERMANN, R., WEISS, E.H., MELMS, A., and WELLER, M. (2002). A functional role of HLA-G expression in human gliomas: an alternative strategy of immune escape. J. Immunol. 168: 4772-4780.
90. WILCZYNSKI, J.R. (2006). Immunological analogy between allograft rejection, recurrent abortion and pre-eclampsia the same basic mechanism? Human Immunol. 67: 492-511.
91. WOODS, L.L., WEEKS, D.A., and RASCH, R. (2004). Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 65: 1339-1348.
92. YIE, S.M., BALAKIER, H., MOTAMEDI, G., and LIBRACH, C.L. (2005). Secretion of human leukocyte antigen-G by human embryos is associated with a higher in vitro fertilization pregnancy rate. Fertil. Steril. 83: 30-36.
93. YOSHINAGA, K. (2008). Review of factors essential for blastocyst implantation for their modulating effects on the maternal immune system. Semin. Cell Dev. Biol. 19:161-169.
94. ZELEZNIK, A.J., HUTCHINSON, J.S., and SCHULER, H.M. (1987). Passive immunization with anti-oestradiol antibodies during the luteal phase of the menstrual cycle potentiates the perimenstrual rise in serum gonadotrophin concentrations and stimulates follicular growth in the cynomolgus monkey (Macaca fascicularis). J. Reprod. Fertil. 80: 403-410.