Non-classical MHC-E (Mamu-E) Expression in the Rhesus Monkey Placenta

Placenta

Volumn 29, Issue 1, 2008, Pages 58-70

  Dambaeva, S V ^a   Bondarenko, G I ^a   Grendell, R L ^a   Kravitz, R H ^a   Durning, M ^a   Golos, T G ^a  

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

Author keywords

HLA E; Mamu E; Placenta; Pregnancy; Rhesus monkey; Trophoblast

Indexed keywords

HLA ANTIBODY; HLA E ANTIGEN; HLA G ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; MAMU E PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHORION VILLUS; CONTROLLED STUDY; CYTOTROPHOBLAST; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GESTATION PERIOD; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOTHER FETUS RELATIONSHIP; NONHUMAN; PLACENTA; PLACENTA VILLUS; PREGNANCY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; STAINING; TROPHOBLAST; WESTERN BLOTTING;

ANIMALS; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; MACACA MULATTA; MODELS, ANIMAL; PLACENTA; PREGNANCY; RECOMBINANT PROTEINS;

EID: 37649007426     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2007.10.001     Document Type: Article

References (67)

1. Hunt J.S. Stranger in a strange land. Immunol Rev 213 (2006) 36-47
2. Moreau P., Dausset J., Carosella E.D., and Rouas-Freiss N. Viewpoint on the functionality of the human leukocyte antigen-G null allele at the fetal-maternal interface. Biol Reprod 67 (2002) 1375-1378
3. Ishitani A., Sageshima N., Lee N., Dorofeeva N., Hatake K., Marquardt H., et al. 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 (2003) 1376-1384
4. Kovats S., Main E.K., Librach C.L., Stubblenbine M., Fisher S.J., and DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248 (1990) 220-223
5. Hunt J.S., Petroff M.G., Morales P., Sedlmayr P., Geraghty D.E., and Ober C. HLA-G in reproduction: studies on the maternal-fetal interface. Hum Immunol 61 (2000) 1113-1117
6. Riteau B., Rouas-Freiss N., Menier C., Paul P., Dausset J., and Carosella E.D. HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J Immunol 166 (2001) 5018-5026
7. Shobu T., Sageshima N., Tokui H., Omura M., Saito K., Nagatsuka Y., et al. The surface expression of HLA-F on decidual trophoblast increases from mid to term gestation. J Reprod Immunol 72 (2006) 18-32
8. Lee N., and Geraghty D.E. HLA-F surface expression on B cell and monocyte cell lines is partially independent from tapasin and completely independent from TAP. J Immunol 171 (2003) 5264-5271
9. Ulbrecht M., Honka T., Person S., Johnson J.P., and Weiss E.H. The HLA-E gene encodes two differentially regulated transcripts and a cell surface protein. J Immunol 149 (1992) 2945-2953
10. Coupel S., Moreau A., Hamidou M., Horejsi V., Soulillou J.-P., and Charreau B. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood 109 (2007) 2806-2814
11. Marin R., Ruiz-Cabello F., Pedrinaci S., Mendez R., Jimenez P., Geraghty D.E., et al. Analysis of HLA-E expression in human tumors. Immunogenetics 54 (2003) 767-775
12. Derre L., Corvaisier M., Charreau B., Moreau A., Godefroy E., Moreau-Aubry A., et al. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J Immunol 177 (2006) 3100-3107
13. King A., Allan D.S., Bowen M., Powis S.J., Joseph S., Verma S., et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 30 (2000) 1623-1631
14. Ishitani A., Sageshima H., Lee N., Dorofeeva N., Hatake K., Marquardt H., et al. 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 (2003) 1376-1384
15. Lee N., Goodlett D.R., Ishitani A., Marquardt H., and Geraghty D.E. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 160 (1998) 4951-4960
16. Michaelsson J., Teixeira de Matos C., Achour A., Lanier L.L., Karre K., and Soderstrom K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 196 (2002) 1403-1414
17. Tomasec P., Braud V.M., Rickards C., Powell M.B., McSharry B.P., Gadola S., et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287 (2000) 1031-1033
18. Heinzel A., Grotzke J., Lines R., Lewinsohn D.A., McNabb A., Streblow D., et al. HLA-E-dependent presentation of Mtb-derived antigen to human CD8+ T cells. J Exp Med 196 (2002) 1473-1481
19. Lee N., Llano M., Carretero M., Ishitani A., Navarro F., Lopez-Botet M., et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 95 (1998) 5199-5304
20. Braud V.M., Allan D.S.J., O'Callaghan C.A., Soderstrom K., D'Andrea A., Ogg G.S., et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391 (1998) 795-799
21. Pietra G., Romagnani C., Mazzarino P., Falco M., Millo E., Moretta A., et al. HLA-E-restricted recognition of cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes. Proc Natl Acad Sci U S A 100 (2003) 10896-10901
22. Bulmer J.N., Morrison L., Longfellow M., Ritson A., and Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 6 (1991) 791-798
23. Slukvin I.I., Watkins D.I., and Golos T.G. Phenotypic and functional characterization of rhesus monkey decidual lymphocytes: rhesus decidual large granular lymphocytes express CD56 and have cytolytic activity. J Reprod Immunol 50 (2001) 57-79
24. Cooper M.A., Fehniger T.A., Turner S.C., Chen K.S., Ghaheri B.A., Ghayur T., et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood 97 (2001) 3146-3151
25. Koopman L., Kopcow H., Rybalov B., Boyson J., Orange J., Schatz F., et al. Human decidual natural killer cells are a unique NK cells subset with immunomodulatory potential. J Exp Med 198 (2003) 1201-1212
26. Hanna J., Goldman-Wohl D., Hamani Y., Avraham I., Greenfield C., Natanson-Yaron S., et al. Decidual NK cells regulate key developmental process a the human fetal-maternal interface. Nat Med 12 9 (2006) 1065-1074
27. Daza-Vamenta R., Glusman G., Rowen L., Guthrie B., and Geraghty D.E. Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14 (2004) 1501-1515
28. Boyson J.E., Iwanaga K.K., Golos T.G., and Watkins D.I. Identification of the rhesus monkey HLA-G ortholog - Mamu-G is a pseudogene. J Immunol 157 (1996) 5428-5437
29. Boyson J.E., Iwanaga K.K., Golos T.G., and Watkins D.I. Identification of a novel MHC class I gene, Mamu-AG in the placenta of primate with an inactivated G locus. J Immunol 159 (1997) 3311-3321
30. Slukvin I., Boyson J., Watkins D., and Golos T. The rhesus monkey analogue of human lymphocyte antigen-G is expressed primarily in villous syncytiotrophoblasts. Biol Reprod 58 (1998) 728-738
31. Ryan A., Grendel R., Geraghty D., and Golos T. 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 (2002) 673-683
32. Knapp L.A., Cadavid L.F., and Watkins D.I. The MHC-E locus is the most well conserved of all known primate class I histocompatibility genes. J Immunol 160 (1998) 189-196
33. Boyson J.E., McAdam S.N., Gallimore A., Golos T.G., Liu X., Gotch F.M., et al. The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41 (1995) 59-68
34. Golos T.G., Bondarenko G.I., Breburda E.E., Dambaeva S.V., Durning M., and Slukvin I.I. Immune and trophoblast cells at the rhesus monkey maternal-fetal interface. Methods Mol Med 122 (2005) 93-108
35. Knapp L.A., Lehmann E., Piekarczyk M.S., Urvater J.A., and Watkins D.I. A high frequency of Mamu-A*01 in the rhesus macaque detected by polymerase chain reaction with sequence-specific primers and direct sequencing. Tissue Antigens 50 6 (1997) 657-661
36. Slukvin I., Lunn D., and Golos T. 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 (2000) 9104-9109
37. Menier C., Saez B., Horejsi V., Martinozzi S., Krawice-Radanne I., Bruel S., et al. Characterization of monoclonal antibodies recognizing HLA-G or HLA-E: new tools to analyze the expression of the nonclassical HLA class I molecules. Hum Immunol 64 (2003) 315-326
38. Chu W., Fant M.E., Geraghty D.E., and Hunt J.S. Soluble HLA-G in human placentas: synthesis in trophoblast and interferon-γ-activated macrophages but not placental fibroblasts. Hum Immunol 59 (1998) 435-472
39. Watkins D.I., Kannagi M., Stone M.E., and Letvin N.L. Major histocompatibility complex class I molecules of nonhuman primates. Eur J Immunol 18 (1988) 1425-1432
40. Matsunami K., Miyagawa S., Nakai R., Yamada M., and Shirakura R. Modulation of the leader peptide sequence of the HLA-E gene up-regulates its expression and down-regulates natural killer cell-mediated swine endothelial cell lysis. Transplantation 73 (2002) 1582-1589
41. Hutter H., Hammer A., Blaschitz A., Hartmann M., Ebbesen P., Gottfried D., et al. Expression of HLA class I molecules in human first trimester and term placenta trophoblast. Cell Tissue Res 286 (1996) 439-447
42. Fujii T., Ishitani A., and Geraghty D.E. A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 153 (1994) 5516-5524
43. Watkins D.I. The evolution of major histocompatibility class I genes in primates. Crit Rev Immunol 15 (1995) 1-29
44. Golos T.G. Nonhuman primate placental MHC expression: a model for exploring mechanisms of human Maternal-Fetal immune tolerance. Hum Immunol 64 (2003) 1102-1109
45. Langat D.K., Morales P.J., Fazleabas A.T., Mwenda J.M., and Hunt J.S. Baboon placentas express soluble and membrane-bound Paan-AG proteins encoded by alternatively spliced transcripts of the class Ib major histocompatibility complex gene, Paan-AG. Immunogenetics 54 (2002) 164-173
46. Moretta L., Romagnani C., Pietra G., Moretta A., and Mingari M.C. NK-CTLs, a novel HLA-E-restricted T-cell subset. Trends Immunol 24 (2003) 136-143
47. Farag S., Fehniger T.A., Ruggeri L., Velardi A., and Caligiuri M.A. Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood 100 (2002) 1935-1947
48. Wada H., Matsumoto N., Maenaka K., Suzuki K., and Yamamoto K. The inhibitory NK cell receptor CD94/NKG2C bind the top of HLA-E through mostly shared but partly distinct sets of HLA-E residues. Eur J Immunol 34 (2004) 81-90
49. Kravitz R.H., Grendell R.L., Slukvin I.I., and Golos T.G. Selective expression of NKG2-A and NKG2-C mRNAs and novel alternative splicing of 5′ exons in rhesus monkey decidua. Immunogenetics 53 (2001) 69-73
50. LaBonte M.L., Hershberger K.L., Korber B., Letvin N.L., and The K.I.R. CD94/NKG2 families in the rhesus. Immunol Rev 183 (2001) 25-40
51. Llano M., Lee N., Navarro F., Garcia P., Albar J.P., Geraghty D.E., et al. 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 (1998) 2854-2863
52. Vales-Gomez M., Reyburn H.T., Erskine R.A., Lopez-Botet M., and Strominger J.L. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 18 (1999) 4250-4260
53. Loke Y.W., and King A. Decidual natural-killer-cell interaction with trophoblast: cytolysis or cytokine production?. Biochem Soc Trans 28 (2000) 196-198
54. Davies A., Kalb S., Liang B., Aldrich C.J., Lemonnier F.A., Jiang H., et al. A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. J Immunol 170 (2003) 5027-5033
55. Ziegert M., Witkin S.S., Sziller I., Alexander H., Brylla E., and Hartig W. Heat shock proteins and heat shock protein-antibody complexes in placental tissues. Infect Dis Obstet Gynecol 7 (1999) 180-185
56. Giacomelli R., Cipriani P., Fulminis A., Nelson J.L., and Matucci-Cerinic M. Gamma/delta T cells in placenta and skin: their different function may support the paradigm of microchimerism in systemic sclerosis. Clin Exp Rheumatol 22 3 Suppl. 33 (2004) S28-S30
57. Wataba K., Saito T., Takeuchi M., Nakayama M., Suehara N., and Kudo R. Changed expression of heat shock proteins in various pathological findings in placentas with intrauterine fetal growth restriction. Med Electron Microsc 37 (2004) 170-176
58. Rieger L., Hofmeister V., Probe C., Dietl J., Weiss E.H., Steck T., et al. Th1- and Th3-like cytokines production by first trimester decidual large lymphocytes is influenced by HLA-G and HLA-E. Mol Hum Reprod 8 (2002) 255-261
59. Apps R., Gardner L., Sharkey A.M., Holmes N., and Moffett A. A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1. Eur J Immunol 37 (2007) 1924-1937
60. Rajagopalan S., Fu J., and Long E.O. Induction of IFN-γ production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J Immunol 167 (2001) 1877-1881
61. Van der Meer A., Lukassen H., Van Lierop M., Wijnands F., Mosselman S., Braat D., et al. Membrane-bound HLA-G activates proliferation and interferon-γ production by uterine natural killer cells. Mol Hum Reprod 10 (2004) 189-195
62. Hu Y., Dutz J.P., MacCalman C.D., Yong P., Tan R., and Von Dadelszen P. Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: role for IFN-γ. J Immunol 177 (2006) 8522-8530
63. Ashkar A., Di Santo J., and Croy A. Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 192 (2000) 259-269
64. Gustafson K., and Ginder G. Interferon-γ induction of the human leukocyte antigen-E gene is mediated through binding of a complex containing STAT1α to a distinct interferon-γ-responsible element. J Biol Chem 271 (1996) 20035-20046
65. Ulbrecht M., Modrow S., Srivastava R., Peterson P.A., and Weiss E.H. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J Immunol 160 (1998) 4375-4385
66. Soloski M.J., Szperka M.E., Davies A., and Wooden S.L. Host immune response to intracellular bacteria: a role for MHC-linked class-Ib antigen-presenting molecules. Proc Soc Exp Biol Med 224 (2000) 231-239
67. Miller J.D., Weber D.A., Ibegbu C., Pohl J., Altman J.D., and Jensen P.E. Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2. J Immunol 171 (2003) 1369-1375