Role of NK cells and HLA-G in endometriosis

Frontiers in Bioscience - Scholar

Volumn 4 S, Issue 4, 2012, Pages 1568-1581

  Maeda, Nagamasa ^a   Izumiya, Chiaki ^a   Taniguchi, Kayo ^a   Matsushima, Sachio ^a   Fukaya, Takao ^a  

^a KOCHI MEDICAL SCHOOL   (Japan)

Author keywords

Endometriosis; Endometrium; HLA G; ILT; NK cells; NK receptors; Retrograde menstruation; Review

Indexed keywords

CD94 ANTIGEN; HLA ANTIGEN CLASS 1; HLA E ANTIGEN; HLA G ANTIGEN; IMMUNOGLOBULIN; IMMUNOGLOBULIN LIKE TRANSCRIPT; NATURAL KILLER CELL RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CYTOTOXICITY; ENDOMETRIOSIS; ENDOMETRIUM CELL; HUMAN; IMMUNOSURVEILLANCE; MENSTRUAL CYCLE; MENSTRUATION; NATURAL KILLER CELL; PATHOGENESIS; PERITONEAL FLUID; STRESS;

EID: 84883726337     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: 10.2741/s353     Document Type: Article

References (116)

1. JA Sampson. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into peritoneal cavity. Am J Obstet Gynecol 14 422-425 (1927)
2. R Meyer. Ueber den Stand der Frage der Adenomyositis und Adenomyom im Allgemeinen und insbesonderes ueber Adenomyositis seroepithelialis und Adenomyometritis sarcomatosa. Zbl Gynaekol 36 745-750 (1919)
3. D. Oosterlynck, F. Cornillie, M Waer. M Vandeputte, PR Koninckx. Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 56 45-51 (1991)
4. D. Oosterlynck, C Meuleman. M Waer, M Vandeputte, PR Koninckx. The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril 58 290-295 (1992)
5. D Semer. K Reisler, P. MacDonald, ML Casey. Responsiveness of human endometrial stromal cells to cytokines. Ann NY Acad Sci 622 99-102 (1991)
6. S. Gilmore, S Aksel. C Hoff, RD Peterson. In vitro lymphocyte activity in women with endometriosis-an altered immuneresponse? Fertil Steril 58 1148-1152 (1992) (Pubitemid 23001286)
7. G. Garzetti, A Ciavattini. M Provinciali, N Fabris. M Cignitti, C Romanini. Natural killer cell activity in endometriosis: correlation between serum estradiol levels and cytotoxicity. Obstet Gynecol 81 665-668 (1993) (Pubitemid 23137231)
8. T. Wilson, P. Hertzog, D Angus. L Munnery, E. Wood, I Kola: Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis. Fertil Steril 62 1086-1088 (1994) (Pubitemid 24328246)
9. D Bartosik. SL Jacobs, LJ Kelly. Endometrial tissue in peritoneal fluid. Fertil Steril 46 796-800 (1986) (Pubitemid 17187648)
10. R. Kruitwagen, L. Poels, W. Willemsen, d. Ronde IJ, Ja. PH, Rolland R. Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertil Steril 55 297-303 (1991)
11. P. van der Linden, G. Dunselman, A. de Goeij, E. van der Linden, Ever. JL, Ramaekers FC. Epithelial cells in peritoneal fluid-of endometrial origin? Am J Obstet Gynecol 173 566-570 (1995)
12. A Moretta. S Sivori, M Vitale, D Pende: Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med 182 875-884 (1995)
13. A Moretta. C Bottino, M Vitale. D Pende, R Biassoni. MC Mingari, L Moretta. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol 14 619-648 (1996) (Pubitemid 26130196)
14. E. Long, D. Burshtyn, W. Clark, M Peruzzi. S Rajagopalan, S Rojo. N Wagtmann, CC Winter. Killer cell inhibitory receptors: diversity, specificity, and function. Immunol Rev 155 135-144 (1997) (Pubitemid 27076065)
15. N Maeda. C Izumiya, Y Yamamoto. H Oguri, T Kusume, T Fukaya. Increased killer inhibitory receptor KIR2DL1 expression among natural killer cells in women with pelvic endometriosis. Fertil Steril 77 297-302 (2002) (Pubitemid 34083552)
16. N Maeda. C Izumiya, T Kusum. T Masumoto, C Yamashita. Y Yamamoto, H Oguri, T Fukaya. Killer inhibitory receptor CD158a overexpression among natural killer cells in women with endometriosis is undiminished by laparoscopic surgery and gonadotropin releasing hormone agonist treatment. Am J Reprod Immunol 51 364-372 (2004) (Pubitemid 38765271)
17. S Matsuoka. N Maeda, C Izumiya. C Yamashita, Y Nishimori, T Fukaya. Expression of inhibitory-motif killer immunoglobulin-like receptor, KIR2DL1, is increased in natural killer cells from women with pelvic endometriosis. Am J Reprod Immunol 53 249-254 (2005) (Pubitemid 40542807)
18. S Rajagopalan, EO Long. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 189 1093-1100 (1999)
19. S Kovats. EK Main, C Librach. M Stubblebine, S. Fisher, R DeMars. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248 220-223 (1990) (Pubitemid 120031455)
20. K. Yelavarthi, Fishbac. JL, Hunt JS. Analysis of HLA-G mRNA in human placental and extraplacental membrane cells by in situ hybridization. J Immunol 146 2847-2854 (1991)
21. Y Yang. DE Geraghty, Hunt JS. Cytokine regulation of HLA-G expression in human trophoblast cell lines. J Reprod Immunol 29 179-195 (1995)
22. JA McIntyre. Immune recognition at the maternalfetal interface: overview. Am J Reprod Immunol 28 127-131 (1992) (Pubitemid 23044812)
23. PM Johnson. Immunobiology of the human placental trophoblast. Exp Clin Immunogenet 10 118-122 (1993) (Pubitemid 23270618)
24. IL Sargent. Maternal and fetal immune responses during pregnancy. Exp Clin Immunogenet 10 85-102 (1993) (Pubitemid 23270616)
25. E. Ibrahim, M Morange. J Dausset, E. Carosella, P Paul. Heat shock and arsenite induce expression of the nonclassical class I histocompatibility HLA-G gene in tumor cell lines. Cell Stress Chaperones 5 207-218 (2000)
26. B. Barrier, B. Kendall, C. Ryan, KL Sharpe-Timms. HLA-G is expressed by the glandular epithelium of peritoneal endometriosis but not in eutopic endometrium. Hum Reprod 21 864-869 (2006)
27. J Halme. MG Hammond, J. Hulka, S. Raj, LM Talbert. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 64 151-154 (1984) (Pubitemid 14096684)
28. E Klein. MG Masucci, G Masucci, F Vanky. Natural killer activity of human blood lymphocytes. Mol Immunol 19 1323-1329 (1982) (Pubitemid 12021069)
29. L. Holmberg, KA Ault. Characterization of natural killer cells induced in the peritoneal exudates of mice infected with Listeria monocytogenes: a study of their tumor target specificity and their expression of murine differentiation antigens and human NK-associated antigens. Cell Immunol 89 151-68 (1984) (Pubitemid 15202742)
30. E Klein. F Vánky, BM Vose. Natural killer and tumor recognizing lymphocyte activity in tumor patients. Haematologia 12 107-112 (1978) (Pubitemid 10103694)
31. M Lefkowitz. J Kornbluth, J. Tomaszewski, DK Jorkasky. Natural killer-cell activity in cyclosporinetreated renal allograft recipients. J Clin Immunol 8:121-127 (1988)
32. J. Kwak, K. Beaman, A Gilman-Sachs. JE Ruiz, D Schewitz, AE Beer. Up-regulated expression of CD56+, CD56+/CD16+, and CD19+ cells in peripheral blood lymphocytes in pregnant women with recurrent pregnancy losses. Am J Reprod Immunol 34 93-99 (1995)
33. T Werfel. P Uciechowski, P. Tetteroo, R Kurrle. H Deicher, RE Schmidt. Activation of cloned human natural killer cells via Fc gamma RIII. J Immunol 142 1102-1106 (1989) (Pubitemid 19067477)
34. T Nitta. H Yagita, K Sato, K Okumura. Involvement of CD56 (NKH-1/Leu-19 antigen) as an adhesion molecule in natural killer-target cell interaction. J Exp Med 170 1757-1761 (1989) (Pubitemid 19284573)
35. K Handa. R Suzuki, H Matsui. Y Shimizu, K Kumagai. Natural killer (NK) cells as a responder to interleukin 2 (IL-2). II. IL-2-induced interferon gamma production. J Immunol 130 988-992 (1983) (Pubitemid 13186340)
36. C. Hunter, J Timans. P Pisacane, S Menon. G Cai, W Walker. M Aste-Amezaga, R Chizzonite. JF Bazan, RA Kastelein. Comparison of the effects of interleukin-1 alpha, interleukin-1 beta and interferon-gammainducing factor on the production of interferon-gamma by natural killer. Eur J Immunol 27 2787-2792 (1997) (Pubitemid 27478344)
37. P. Peters, J. Ortaldo, M. Shalaby, L. Svedersky, G. Nedwin, T. Bringman, P. Hass, B. Aggarwal, R. Herberman, D. Goeddel, et al. Natural killer-sensitive targets stimulate production of TNF-alpha but not TNFbeta (lymphotoxin) by highly purified human peripheral blood large granular lymphocytes. J Immunol 137 2592-2598 (1986) (Pubitemid 17176617)
38. B. Lozzio, CB Lozzio. Properties and usefulness of the original K-562 human myelogenous leukemia cell line. Leuk Res 3 363-370 (1979) (Pubitemid 10145094)
39. H. Kay, R Fagnani, GD Bonnard. Cytotoxicity against the K562 erythroleukemia cell line by human natural killer (NK) cells which do not bear free Fc receptors for IgG. Int J Cancer 24 141-150 (1979) (Pubitemid 9244263)
40. K Kärre. MHC gene control of the natural killer system at the level of the target and the host. Semin Cancer Biol 2 295-309 (1991)
41. K Kärre. Natural killer cell recognition of missing self. Nat Immunol 9 477-480 (2008) (Pubitemid 351560515)
42. A Hiraki. K Kiura, H Yamane. N Nogami, M Tabata. N Takigawa, H Ueoka. M Tanimoto, M Harada. Interleukin-12 augments cytolytic activity of peripheral blood mononuclear cells against autologous lung cancer cells in combination with IL-2. Lung Cancer 35 329-333 (2002) (Pubitemid 34158668)
43. W. Carson, J. Giri, M. Lindemann, M. Linett, M Ahdieh. R Paxton, D Anderson. J Eisenmann, K Grabstein, MA Caligiuri. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 180 1395-1403 (1994) (Pubitemid 24289613)
44. Y. Son, R. Dallal, R. Mailliard, S Egawa. ZL Jonak, MT Lotze. Interleukin-18 (IL-18) synergizes with IL-2 to enhance cytotoxicity, interferon-gamma production, and expansion of natural killer cells. Cancer Res 61 884-888 (2001) (Pubitemid 32174396)
45. K Skak. KS Frederiksen, D Lundsgaard. Interleukin-21 activates human natural killer cells and modulates their surface receptor expression. Immunology 123 575-583 (2008) (Pubitemid 351280971)
46. J. Miller, F Prosper, V McCullar. Natural killer (NK) cells are functionally abnormal and NK cell progenitors are diminished in granulocyte colony-stimulating factormobilized peripheral blood progenitor cell collections. Blood 90 3098-3105 (1997) (Pubitemid 27444204)
47. P Uciechowski. T Werfel, R Leo. JE Gessner, J Schubert, RE Schmidt. Analysis of CD16+dim and CD16+bright lymphocytes-comparison of peripheral and clonal non-MHC-restricted T cells and NK cells. Immunobiology 185 28-40 (1992)
48. P Uciechowski. JE Gessner, R Schindler, RE Schmidt. Fc gamma RIII activation is different in CD16+ cytotoxic T lymphocytes and natural killer cells. Eur J Immunol 22 1635-1638 (1992)
49. F Borrego. M Ulbrecht, E. Weiss, J. Coligan, AG Brooks. Recognition of human histocompatibility leukocyte 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 187 813-818 (1998) (Pubitemid 28115198)
50. P. Posch, F Borrego. AG Brooks, JE Coligan. HLA-E is the ligand for the natural killer cell CD94/NKG2 receptors. J Biomed Sci 5 321-531 (1998)
51. V. Braud, AJ McMichael. Regulation of NK cell functions through interaction of the CD94/NKG2 receptors with the nonclassical class I molecule HLA-E. Curr Top Microbiol Immunol 244 85-95 (1999) (Pubitemid 29304672)
52. D. Oosterlynck, C Meuleman. FA Lacquet, M Waer, PR Koninckx. Flow cytometry analysis of lymphocyte subpopulations in peritoneal fluid of women with endometriosis. Am J Reprod Immunol 31 25-31 (1994) (Pubitemid 24072182)
53. H. Ho, K. Chao, H. Chen, M. Wu, Yan. YS, Lee TY. Peritoneal natural killer cytotoxicity and CD25+ CD3+ lymphocyte subpopulation are decreased in women with stage III-IV endometriosis. Hum Reprod 10 2671-2675 (1995)
54. D. Oosterlynck, C Meuleman. M Waer, PR Koninckx. CO2-laser excision of endometriosis does not improve the decreased natural killer activity. Acta Obstet Gynecol Scand 73 333-337 (1994) (Pubitemid 24121495)
55. P. van der Linden, A. de Goeij, G. Dunselman, E. van der Linden, F. Ramaekers, JL Evers. Expression of integrins and E-cadherin in cells from menstrual effluent, endometrium, peritoneal fluid, peritoneum, and endometriosis. Fertil Steril 61 85-90 (1994) (Pubitemid 24030683)
56. W. Dmowski, H Gebel, DP Braun. Decreased apoptosis and sensitivity to macrophage mediated cytolysis of endometrial cells in endometriosis. Hum Reprod Update 4 696-701 (1998) (Pubitemid 29041482)
57. H. Gebel, D. Braun, A Tambur. D Frame, N Rana, WP Dmowski. Spontaneous apoptosis of endometrial tissue is impaired in women with endometriosis. Fertil Steril 69 1042-1047 (1998) (Pubitemid 28274891)
58. G. Meresman, S Vighi. RA Buquet, O Contreras-Ortiz. M Tesone, LS Rumi. Apoptosis and expression of Bcl-2 and Bax in eutopic endometrium from women with endometriosis. Fertil Steril 74 760-766 (2000)
59. L. Lanier, B. Corliss, J Wu. C Leong, JH Phillips. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391 703-707 (1998) (Pubitemid 28113218)
60. P Bruhns. P Marchetti, W. Fridman, E Vivier, M Daëron. Differential roles of N-and C-terminal immunoreceptor tyrosine-based inhibition motifs during inhibition of cell activation by killer cell inhibitory receptors. J Immunol 162 3168-3175 (1999) (Pubitemid 29313562)
61. S Yusa. TL Catina, KS Campbell. SHP-1-and phosphotyrosine-independent inhibitory signaling by a killer cell Ig-like receptor cytoplasmic domain in human NK cells. J Immunol 168 5047-5057 (2002) (Pubitemid 34495968)
62. M López-Botet. T Bellón, M Llano. F Navarro, P García, M de Miguel. Paired inhibitory and triggering NK cell receptors for HLA class I molecules. Hum Immunol 61 7-17 (2000) (Pubitemid 30058762)
63. F Borrego. J Kabat, D. Kim, L Lieto. K Maasho, J Peña. R Solana, JE Coligan. Structure and function of major histocompatibility complex (MHC) class I specific receptors expressed on human natural killer (NK) cells. Mol Immunol 38 637-660 (2002) (Pubitemid 34168194)
64. J. Goodridge, C. Witt, F. Christiansen, HS Warren. KIR2DL4 (CD158d) genotype influences expression and function in NK cells. J Immunol 71 1768-1774 (2003) (Pubitemid 36966459)
65. J. Goodridge, L. Lathbury, N. Steiner, C. Shulse, P Pullikotil. NG Seidah, C. Hurley, F. Christiansen, CS Witt. Three common alleles of KIR2DL4 (CD158d) encode constitutively expressed, inducible and secreted receptors in NK cells. Eur J Immunol 37 199-211 (2007) (Pubitemid 46128800)
66. A Kikuchi-Maki. S Yusa, T. Catina, KS Campbell. KIR2DL4 is an IL-2-regulated NK cell receptor that exhibits limited expression in humans but triggers strong IFN-gamma production. J Immunol 171 3415-3425 (2003) (Pubitemid 37254542)
67. W. Yan, LA Fan. Residues Met76 and Gln79 in HLAG alpha1 domain involve in KIR2DL4 recognition. Cell Res 15 176-182 (2005) (Pubitemid 41653940)
68. M Faure, EO Long. KIR2DL4 (CD158d), an NK cellactivating receptor with inhibitory potential. J Immunol 168 6208-6214 (2002) (Pubitemid 34620040)
69. X. Ju, C Hacker. B Scherer, V Redecke. T Berger, G Schuler. H Wagner, G. Lipford, M Zenke. Immunoglobulin-like transcripts ILT2, ILT3 and ILT7 are expressed by human dendritic cells and down-regulated following activation. Gene 331 159-64 (2004) (Pubitemid 38501603)
70. N Maeda. C Izumiya, H Oguri. T Kusume, Y Yamamoto, T Fukaya. Aberrant expression of intercellular adhesion molecule-1 and killer inhibitory receptors induces immune tolerance in women with pelvic endometriosis. Fertil Steril 77 679-683 (2002) (Pubitemid 34275343)
71. C Zhang. N Maeda, C Izumiya. Y Yamamoto, T Kusume. H Oguri, C Yamashita. Y Nishimori, K Hayashi. J Luo, T Fukaya. Killer immunoglobulin-like receptor and human leukocyte antigen expression as immunodiagnostic parameters for pelvic endometriosis. Am J Reprod Immunol 55 106-114 (2006) (Pubitemid 43329485)
72. J Kitawaki. B Xu, H Ishihara. M Fukui, G Hasegawa. N Nakamura, S Mizuno. M Ohta, H Obayashi, H Honjo. Association of killer cell immunoglobulin-like receptor genotypes with susceptibility to endometriosis. Am J Reprod Immunol 58 481-486 (2007) (Pubitemid 350091184)
73. M Kawashima. N Maeda, Y Adachi. T Takeuchi, Y Yamamoto. C Izumiya, K Hayashi. M Furihata, K Udaka, T Fukaya. Human leukocyte antigen-G, a ligand for the natural killer receptor KIR2DL4, is expressed by eutopic endometrium only in the menstrual phase. Fertil Steril 91 343-349 (2009)
74. E. Petrie, C. Clements, J Lin. LC Sullivan, D Johnson. T Huyton, A Heroux. HL Hoare, T Beddoe. HH Reid, M. Wilce, A. Brooks, J Rossjohn. CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J Exp Med 205 725-735 (2008) (Pubitemid 351439316)
75. L. Sullivan, C. Clements, T Beddoe. D Johnson, H. Hoare, J Lin. T Huyton, E. Hopkins, H. Reid, M. Wilce, J Kabat. F Borrego, J. Coligan, J Rossjohn, AG Brooks. The heterodimeric assembly of the CD94-NKG2 receptor family and implications for human leukocyte antigen-E recognition. Immunity 27 900-911 (2007) (Pubitemid 50013980)
76. M Carretero. C Cantoni, T Bellón. C Bottino, R Biassoni. A Rodríguez, J. Pérez-Villar, L Moretta. A Moretta, M López-Botet. The CD94 and NKG2-A C-type lectins covalently assemble to form a natural killer cell inhibitory receptor for HLA class I molecules. Eur J Immunol 27 563-567 (1997) (Pubitemid 27085264)
77. M Carretero. M Llano, F Navarro. T Bellón, M López-Botet. Mitogen-activated protein kinase activity is involved in effector functions triggered by the CD94/NKG2-C NK receptor specific for HLA-E. Eur J Immunol 30 2842-2848 (2000)
78. M Valés-Gómez. HT Reyburn, R. Erskine, M López. Botet, JL Strominger. 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 4250-4260 (1999)
79. A King. DS Allan, M Bowe. SJ Powis, S Joseph. S Verma, S. Hiby, A. McMichael, Y. Loke, VM Braud. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 30 1623-1631 (2000) (Pubitemid 30342804)
80. R Galandrini. MG Porpora, A Stoppacciaro. F Micucci, C Capuano. I Tassi, A Di Felice. Increased frequency of human leukocyte antigen-E inhibitory receptor
81. M Shiroishi. K Tsumoto, K Amano. Y Shirakihara, M Colonna. VM Braud, D. Allan, A Makadzange. Rowland-Jones S, Willco. B, Jone. EY, va. der Merwe PA, Kumaga. I, Maenaka K. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci U S A 100 8856-8861 (2003) (Pubitemid 36899188)
82. M Vernet-Tomá. Mdel, C. Pérez-Ares, N Verdú. JL Molinero, M. Fernández-Figueras, R Carreras. The endometria of patients with endometriosis show higher expression of class I human leukocyte antigen than the endometria of healthy women. Fertil Steril 85 78-83 (2006) (Pubitemid 43063426)
83. H Heinrichs, HT Orr. HLA non-A, B, C class I genes: their structure and expression. Immunol Res 9 265-274 (1990)
84. J. Rodgers, RG Cook. "MHC CLASS IB MOLECULES BRIDGE INNATE AND ACQUIRED IMMUNITY". Nat Rev Immunol 5 459-471 (2005) (Pubitemid 40835034)
85. C. O'Callaghan, JI Bell. Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLAG. Immunol Rev 163 129-138 (1998) (Pubitemid 28327866)
86. J. Hunt, M. Petroff, R. McIntire, C Ober. HLA-G and immune tolerance in pregnancy. FASEB J 19 681-693 (2005) (Pubitemid 40617373)
87. C. Clements, L Kjer-Nielsen. J McCluskey, J Rossjohn. Structural studies on HLA-G: implications for ligand and receptor binding. Hum Immunol 68 220-226 (2007) (Pubitemid 46497514)
88. J LeMaoult. K Zafaranloo, C L. Danff, ED Carosella. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J 19 662-664 (2005) (Pubitemid 40471278)
89. S Kovats. EK Main, C Librach. M Stubblebine, S. Fisher, R DeMars. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248 220-223 (1990). (Pubitemid 120031455)
90. A Blaschitz. H Hutter, G Dohr. HLA Class I protein expression in the human placenta. Early Pregnancy 5 67-69 (2001)
91. C. Clements, L Kjer-Nielsen. L Kostenko, H. Hoare, M. Dunstone, E Moses, et al. Crystal structure of HLA-G: a nonclassical MHC class I molecule expressed at the fetalmaternal interface. Proc Natl Acad Sci U S A 102 3360-3365 (2005) (Pubitemid 40328050)
92. O. Baricordi, M Stignani. L Melchiorri, R Rizzo. HLA-G and inflammatory diseases. Inflamm Allergy Drug Targets 7 67-74 (2008)
93. P Moreau. F Adrian-Cabestre, C Menier. V Guiard, L Gourand. J Dausset, E. Carosella, P Paul. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 11 803-811 (1999) (Pubitemid 29237771)
94. C Creput. G Le Friec, R Bahri. L Amiot, B Charpentier. E Carosella, N Rouas-Freiss, A Durrbach. Detection of HLA-G in serum and graft biopsy associated with fewer acute rejections following combined liver-kidney transplantation: possible implications for monitoring patients. Hum Immunol 64 1033-1038 (2003) (Pubitemid 37413711)
95. P Paul. N Rouas-Freiss, I Khalil-Daher. P Moreau, B Riteau. FA Le Gal, M. Avril, J Dausset. JG Guillet, ED Carosella. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci U S A 95 4510-4515 (1998) (Pubitemid 28207943)
96. F Adriá. Cabestré, P Moreau. B Riteau, E. Ibrahim, C L. Danff, J Dausset. N Rouas-Freiss, E. Carosella, P Paul. HLA-G expression in human melanoma cells: protection from NK cytolysis. J Reprod Immunol 43 183-193 (1999) (Pubitemid 29349682)
97. E. Ibrahim, N Guerra. MJ Lacombe, E Angevin. S Chouaib, E. Carosella, A Caignard, P Paul. Tumorspecific up-regulation of the nonclassical class I HLA-G antigen expression in renal carcinoma. Cancer Res 61 6838-6845 (2001) (Pubitemid 32896508)
98. J. Lozano, R González. JM Kindelán, N Rouas. Freiss, R Caballos. J Dausset, E. Carosella, J Peña. Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule. AIDS 16 347-351 (2002) (Pubitemid 34165365)
99. C. Clements, L Kjer-Nielsen. L Kostenko, H. Hoare, M. Dunstone, E Moses. K Freed, A. Brooks, J Rossjohn, McCluskey J. Crystal structure of HLA-G: a nonclassical MHC class I molecule expressed at the fetal-maternal interface. Proc Natl Acad Sci U S A 102 3360-3365 (2005) (Pubitemid 40328050)
100. M Shiroishi. K Kuroki, L Rasubala. K Tsumoto, I Kumagai. E Kurimoto, K Kato. D Kohda, K Maenaka. Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d) . Proc Natl Acad Sci U S A 103 16412-16417 (2006) (Pubitemid 44715210)
101. A King. SE Hiby, L Gardner. S Joseph, J. Bowen, S Verma. TD Burrows, YW Loke. Recognition of trophoblast HLA class I molecules by decidual NK cell receptors-a review. Placenta 21 81-85 (2000)
102. B Favier. J Lemaoult, E Lesport, ED Carosella. ILT2/HLA-G interaction impairs NK-cell functions through the inhibition of the late but not the early events of the NKcell activating synapse. The FASEB Journal 24 689-699 (2010)
103. S Rajagopala. S, J Fu, EO Long: Cutting edge: induction of IFN-. production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting cells. J Immunol 167 1877-1881 (2001) (Pubitemid 32747490)
104. J. Boyson, R Erskine. MC Whitman, M Chiu. JM Lau, L. Koopman, M. Valter, P Angelisova. V Horejsi, JL Strominger. Disulfide bond-mediated dimerization of HLA-G on the cell surface. Proc. Natl. Acad. Sci. U S A 99 16180-16185 (2002) (Pubitemid 35462769)
105. V Hofmeister, EH Weiss. HLA-G modulates immune responses by diverse receptor interactions. Semin Cancer Biol 13 317-23 (2003) (Pubitemid 38160930)
106. D Hornung. E Fujii, K. Lim, J. Vigne, M. McMaster, RN Taylor. Histocompatibility leukocyte antigen-G is not expressed by endometriosis or endometrial tissue. Fertil Steril 75 814-817 (2001) (Pubitemid 32273521)
107. G. Spaggiari, P Contini. R Carosio, M Arvigo. M Ghio, D Oddone. A Dondero, M. Zocchi, F Puppo. F Indiveri, A Poggi. Soluble HLA class I molecules induce natural killer cell apoptosis through the engagement of CD8: evidence for a negative regulation exerted by members of the inhibitory receptor superfamily. Blood 99 1706-1714 (2002) (Pubitemid 34533045)
108. P Contini. M Ghio, A Poggi. G Filaci, F Indiveri. S Ferrone, F Puppo. Soluble HLA-A, -B, -C and-G molecules induce apoptosis in T and NK CD8+ cells and inhibit cytotoxic T cell activity through CD8 ligation. Eur J Immunol 33 125-134 (2003) (Pubitemid 36157650)
109. A Lindaman. A Dowden, N Zavazava. Soluble HLAG molecules induce apoptosis in natural killer cells. Am J Reprod Immunol 56 68-76 (2006) (Pubitemid 43871640)
110. A Naji. S Le Rond, A Durrbach. I Krawice-Radanne, C Creput. M Daouya, J Caumartin. J LeMaoult, E. Carosella, N Rouas-Freiss. CD3+CD4low and CD3+CD8low are induced by HLA-G: novel human peripheral blood suppressor T-cell subsets involved in transplant acceptance. Blood 110 3936-48 (2007) (Pubitemid 350248449)
111. A Eidukaite, V Tamosiunas. Soluble HLA-G in the peritoneal fluid of women with endometriosis. Fertil Steril 89 465-467 (2008) (Pubitemid 351215387)
112. P Mach. P Blecharz, P Basta. P Marianowski, J Skret. Magierlo, Z Kojs. M Grabiec, L Wicherek. Differences in the soluble HLA-G blood serum concentration levels in patients with ovarian cancer and ovarian and deep endometriosis. Am J Reprod Immunol 63 387-395 (2010)
113. LM Joseph. A healthy menstrual cycle. Clin Nutr Ins 5 1-7 (1997)
114. M Okazaki. T Matsuyama, T Kohno. H Shindo, T Koji. Y Morimoto, T Ishimaru. Induction of epithelial cell apoptosis in the uterus by a mouse uterine ischemiareperfusion model: possible involvement of tumor necrosis factor-alpha. Biol Reprod 72 1282-1288 (2005) (Pubitemid 40547994)
115. K. Khan, M Kitajima. T Imamura, K Hiraki. A Fujishita, I Sekine. T Ishimaru, H Masuzaki. Toll-like receptor 4-mediated growth of endometriosis by human heat-shock protein 70. Hum Reprod 23 2210-2219 (2008)
116. Khan K. Kitajima M. Hiraki K. Fujishita A. Sekine I. Ishimaru T. Masuzaki H. 2009 Gynecol Obstet Invest 68 40-52.