The rhesus monkey analogue of human lymphocyte antigen-G is expressed primarily in villous syncytiotrophoblasts

Biology of Reproduction

Volumn 58, Issue 3, 1998, Pages 728-738

  Slukvin, Igor I ^a   Boyson, Jonathan E ^a   Watkins, David I ^b   Golos, Thaddeus G ^a,c  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; FEMALE; FETOPLACENTAL UNIT; HLA SYSTEM; IMMUNOLOGICAL TOLERANCE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; FEMALE; GENE EXPRESSION; GENES, MHC CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA MULATTA; MATERNAL-FETAL EXCHANGE; PLACENTA; POLYMERASE CHAIN REACTION; PREGNANCY; RNA, MESSENGER; SPECIES SPECIFICITY; TROPHOBLASTS;

ANIMALIA; MACACA MULATTA;

EID: 0031882757     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod58.3.728     Document Type: Article

References (47)

1. Bulmer JN, Johnson PM. Antigen expression by trophoblast populations in the human placenta and their possible immunological relevance. Placenta 1985; 6:127-140.
2. 2 microglobulin and HLA in chorionic villi of human placentae. Nature 1976; 262:799-802.
3. Goodfellow PN, Barnstable CJ, Bodmer WF, Snary DE, Crumpton MJ. Expression of HLA system antigens on placenta. Transplantation 1976; 22:595-603.
4. Redman CW, McMichael AJ, Stirrat GM, Sunderland CA, Ting A. Class I major histocompatibility complex antigens on human extravillous trophoblast. Immunology 1984; 52:457-468.
5. McMaster MT, Librach CL, Zhou Y, Lim KH, Janatpour MJ, DeMars R, Kovats S, Damsky C, Fisher S. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol 1995; 154:3771-3778.
6. Yelavarthi KK, Fishback JL, Hunt JS. Analysis of HLA-G mRNA in human placental and extraplacental membrane cells by in situ hybridization. J Immunol 1991; 146:2847-2854.
7. Chumbley G, King A, Holmes N, Loke YW. In situ hybridization and northern blot demonstration of HLA-G mRNA in human trophoblast populations by locus-specific oligonucleotide. Hum Immunol 1993; 37:17-22.
8. King A, Boocock C, Sharkey AM, Gardner L, Beretta A, Siccardi AG, Loke YW. Evidence for the expression of HLA-C class I mRNA and protein by human first trimester trophoblast. J Immunol 1996; 156:2068-2076.
9. Alizadeh M, Legras C, Semana G, Le Bouteiller P, Genetet B, Fauchet R. Evidence for a polymorphism of HLA-G gene. Hum Immunol 1993; 38:206-212.
10. Kirszenbaum M, Djoulah S, Hors J, Legall I, Deoliveira EB, Prost S, Dausset J, Carosella ED. HLA-G gene polymorphism segregation within CEPH reference families. Hum Immunol 1997; 53:140-147.
11. Morales P, Corell A, Martinez-Laso J, Martin-Villa J, Varela P, Paz-Artal E, Allende LM, Arnaiz-Villena A. Three new HLA-G alleles and their linkage disequilibria with HLA-A. Immunogenetics 1993; 38:323-331.
12. Wei X, Orr H. Differential expression of HLA-E, HLA-F, and HLA-G transcripts in human tissue. Hum Immunol 1990; 29:131-142.
13. Yamashita T, Fujii T, Watanabe Y, Tokunaga K, Tadokoro K, Juji T, Taketani Y. HLA-G gene polymorphism in a Japanese population. Immunogenetics 1996; 44:186-191.
14. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990; 248:220-223.
15. Sanders SK, Giblin PA, Kavathas P. 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 1991; 174:737-740.
16. Lee N, Malacko AR, Ishitani A, Chen MC, Bajorath J, Marquardt H, Geraghty DE. The membrane-bound and soluble forms of HLA-G bind identical sets of endogenous peptides but differ with respect to TAP association. Immunity 1995; 3:591-600.
17. Diehl M, Munz C, Keilholz W, Stevanovic S, Holmes N, Loke YW, Rammensee HG. Nonclassical HLA-G molecules are classical peptide presenters. Curr Biol 1996; 6:305-314.
18. 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; 89:2669-2673.
19. 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; 153:5516-5524.
20. Chumbley G, King A, Robertson K, Holmes N, Loke YW. Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol 1994; 155:312-322.
21. Deniz G, Christmas SE, Brew R, Johnson PM. Phenotypic and functional cellular differences between human CD3 decidual and peripheral blood leukocytes. J Immunol 1994; 152:4255-4261.
22. Le Bouteiller P, Lenfant F. Antigen-presenting function(s) of the nonclassical HLA-E, -F and -G class I molecules: the beginning of a story. Res Immunol 1996; 147:301-313.
23. Mossman HW. Vertebrate Fetal Membranes. New Brunswick: Rutgers University Press; 1987.
24. Trowsdale J. "Both man & bird & beast": comparative organization of MHC genes. Immunogenetics 1995; 41:1-17.
25. King BF, Blankenship TN. Development and organization of primate trophoblast cells. In: Soares MJ, Handwerger S, Talamantes F (eds.), Trophoblast Cells. New York: Springer-Verlag; 1993: 13-30.
26. Boyson JE, Shufflebotham C, Cadavid LF, Urvater JA, Knapp LA, Hughes AL, Watkins DI. The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 1996; 156:4656-4665.
27. Watkins DI. The evolution of major histocompatibility class I genes in primates. Crit Rev Immunol 1995; 15:1-29.
28. Castro MJ, Morales P, Fernandez-Soria V, Suarez B, Recio MJ, Alvarez M, Martin-Villa M, Arnaiz-Villena A. Allelic diversity at the primate Mhc-G locus: exon 3 bears stop codons in all Cercopithecinae sequences. Immunogenetics 1996; 43:327-336.
29. Otting N, Bontrop RE. Characterization of the rhesus macaque (Macaca mulatta) equivalent of HLA-F. Immunogenetics 1993; 38:141-145.
30. Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of the rhesus monkey HLA-G ortholog - Mamu-G is a pseudogene. J Immunol 1996; 157:5428-5437.
31. Boyson JE, McAdam SN, Gallimore A, Golos TG, Liu X, Gotch FM, Hughes AL, Watkins DI. The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 1995; 41:59-68.
32. Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of a novel MHC class I gene, Mamu-AG in the placenta of primate with an inactivated G locus. J Immunol 1997; 159:3311-3321.
33. Golos TG, Handrow RR, Durning M, Fisher JM, Rilling JK. Regulation of chorionic gonadotropin-alpha and chorionic somatomammotropin messenger ribonucleic acid expression by 8-bromo-adenosine 3′,5′-monophosphate and dexamethasone in cultured rhesus monkey syncytiotrophoblasts. Endocrinology 1992; 131:89-100.
34. Golos TG, Krugner-Higby LA, Williams CS, Fisher JM, Johnson KJ, Durning M, Schultz KT. Primary cultures of rhesus placental syncytiotrophoblasts are permissive for SIV infection. J Med Primatol 1994; 23:66-74.
35. Reimann KA, Waite BC, Lee-Parritz DE, Lin W, Uchanska-Ziegler B, O'Connell MJ, Letvin N. Use of human leukocyte-specific monoclonal antibodies for clinically immunophenotyping lymphocytes of rhesus monkeys. Cytometry 1994; 17:102-108.
36. Watkins DI, Kannagi M, Stone ME, Letvin NL. Major histocompatibility complex class I molecules of nonhuman primates. Eur J Immunol 1988; 18:1425-1432.
37. Stern PL, Beresford NA, Friedman CA, Stevens VC, Risk JM, Johnson PM. Class I-like MHC molecules expressed by baboon placental syncytiotrophoblast. J Immunol 1987; 138:1088-1091.
38. Enders AC. Overview of the morphology of implantation in primates. In: Wolf DP, Stouffer RL, Brenner RM (eds.), In Vitro Fertilization and Embryo Transfer in Primates. New York: Springer-Verlag; 1993: 145-157.
39. Guillaudeux T, Rodriguez AM, Girr M, Mallet V, Ellis SA, Sargent IL, Fauchet R, Alsat E, Le Bouteiller P. Methylation status and transcriptional expression of the MHC class I loci in human trophoblast cells from term placenta. J Immunol 1995; 157:3283-3289.
40. Odum N, Ledbetter JA, Martin P, Geraghty D, Tsu T, Hansen JA, Gladstone P. Homotypic aggregation of human cell lines by HLA class II-, class Ia-and HLA-G-specific monoclonal antibodies. Eur J Immunol 1991; 21:2121-2131.
41. Pazmany L, Mandelboim O, Valesgomez M, Davis DM, Reyburn HT, Strominger JL. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science 1996; 274:792-795.
42. Munz C, Holmes N, King A, Loke YW, Colonna M, Schild H, Rammensee HG. Human histocompatibility leukocyte antigen (HLA)-G molecules inhibit NKAT3 expressing natural killer cells. J Exp Med 1997; 185:385-391.
43. Pende D, Sivori S, Accame L, Pareti L, Falco M, Geraghty D, Lebouteiller P, Moretta L, Moretta A. HLA-G recognition by human natural killer cells - involvement of CD94 both as inhibitory and as activating receptor complex. Eur J Immunol 1997; 27:1875-1880.
44. Rouasfreiss N, Marchal RE, Kirszenbaum M, Dausset J, Carosella ED. The alpha(1) domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells - is HLA-G the public ligand for natural killer inhibitory receptors. Proc Natl Acad Sci USA 1997; 94:5249-5254.
45. Mandelboim O, Reyburn HT, Valesgomez M, Pazmany L, Colonna M. Borsellino G, Strominger JL. Protection from lysis by natural killer cells of group 1 and 2 specifity mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J Exp Med 1996; 184:913-922.
46. Cella M, Longo A, Battista Ferrara G, Strominger JL, Colonna M. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J Exp Med 1994; 180:1235-1242.
47. Luque I, Solana R, Galiani MD, Gonzalez R, Garcia F, Decastro JAL, Pena J. Threonine 80 on HLA-27 confers protection against lysis by a group of natural killer cells. Eur J Immunol 1996; 26:1974-1977.