HLA-G expression Is up-regulated by progesterone in mesenchymal stem cells

American Journal of Reproductive Immunology

Volumn 62, Issue 1, 2009, Pages 25-33

  Ivanova todorova, Ekaterina ^a   Mourdjeva, Milena ^b   Kyurkchiev, Dobroslav ^a   Bochev, Ivan ^b   Stoyanova, Elena ^b   Dimitrov, Rumen ^b   Timeva, Tanya ^c   Yunakova, Maria ^c   Bukarev, Dimitar ^a   Shterev, Atanas ^c   Tivchev, Petar ^a   Kyurkchiev, Stanimir ^b  

^a UNIVERSITY HOSPITAL ALEXANDROVSKA   (Bulgaria)

^b BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^c University Hospital of Obstetrics and Gynecology 'Maichin Dom' Bulgaria   (Bulgaria)

Author keywords

HLA G; Immune response; Mesenchymal stem cells; Pregnancy; Progesterone

Indexed keywords

HLA G ANTIGEN; MEDROXYPROGESTERONE ACETATE; PROGESTERONE; GESTAGEN; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA-G ANTIGEN;

ADIPOSE TISSUE; ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW; CELL CULTURE; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; DECIDUA; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; MESENCHYMAL STEM CELL; PREGNANCY; PRIORITY JOURNAL; UPREGULATION; BIOSYNTHESIS; DRUG EFFECT; IMMUNOLOGY; METABOLISM; MIDDLE AGED;

ADIPOSE TISSUE; ADULT; AGED; AGED, 80 AND OVER; CELLS, CULTURED; DECIDUA; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; MESENCHYMAL STEM CELLS; MIDDLE AGED; PREGNANCY; PROGESTERONE; PROGESTINS; UP-REGULATION;

EID: 67149143142     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2009.00707.x     Document Type: Article

References (42)

1. Geraghty DE, Koller BH, Orr HT: A human major histocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment. Proc Natl Acad Sci USA 1987; 84: 9145-9149.
2. Le Bouteiller P: HLA class I chromosomal region, genes, and products: facts and questions. Crit Rev Immunol 1994; 14: 89-105.
3. McMaster MT, Librach CL, Zhou Y, Lim KH, Janatpour MJ, DeMars R, Kovats S, Damsky C, Fisher SJ: Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol 1995; 154: 3771-3778.
4. Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bensussan A, Geraghty DE, Le Bouteiller P, Dohr G: Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol 1997; 27: 3380-3386.
5. Chu W, Fant ME, Geraghty DE, Hunt JS: Soluble HLA-G in human placentas: synthesis in trophoblasts and interferon-g-Activated Macrophages But Not Placental Fibroblasts. Hum Immunol 1998; 59: 435-442.
6. Mallet V, Blaschitz A, Crisa L, Schmitt C, Fournel S, King A, Loke YW, Dohr G, Le BouteillerAPH: HLA-G in the human thymus: a subpopulation of medullary epithelial but not CD83F dendritic cells expresses HLA-G as a membrane-bound and soluble protein. Int Immunol 1999; 11: 889-898.
7. Le Bouteiller P, Solier C, Pröll J, Aguerre-Girr M, Fournel S, Lenfant F: The major histocompatibility complex in pregnancy: Part II. Placental HLA-G protein expression in vivo: Where and what for?. Hum Reprod Update 1999; 5: 223-233.
8. Bainbridge DRJ, Ellis SA, Sargent IL: HLA-G suppresses proliferation of CD4+ T-lymphocytes. J Reprod Immunol 2000; 48: 17-26.
9. Fournel S, Aguerre-Girr M, Huc X, Lenfant F, Alam A, Toubert A, Bensussan A, Le Bouteiller P: Soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD81 cells by interacting with CD81. J Immunol 2000; 164: 6100-6104.
10. Marchal-Bras-Goncalves R, Rouas-Freiss N, Connan F, Choppin J, Dausset J, Carosella ED, Kirszenbaum M, Guillet J-G: A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant Proc 2001; 33: 2355-2359.
11. Moreau P, Adrian-Cabestre F, Menier C, Guiard V, Gourand L, Dausset J, Carosella ED, Paul P: IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 1999; 11: 803-811.
12. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finazzi-AgròA: Progesterone up-regulates anandamide hydrolase in human lymphocytes: Role of cytokines and implications for fertility. J Immunol, 2001; 166: 7183-7189.
13. Wira CR, Sandoe CP: Hormonal regulItion of immunoglobulins: influence of estradiol in immunoglobulins A and G in the rat uterus. Endocrinology 1980; 106: 1020-1026.
14. Moriyama I, Sugawa T: Progesterone facilitates implantation of xenogeneic cultured cells in hamster uterus. Nat New Biol 1972; 236: 150-152.
15. Mori T, Kobayashi H, Nashimoto H, Suzuki A, Nishimura T: Inhibitory effect of progesterone and 20-alpha hydroxypregn4-n-3-one on the phytohaemagglutinin-induced transformation of human lymphocytes. Am J Obstet Gynecol 1977; 127: 151-157.
16. Szekeres-Bartho J, Hadnagy J, Pacsa AS: The suppressive effect of progesterone on lymphocyte cytotoxicity: Unique progesterone sensitivity of pregnancy lymphocytes. J Reprod Immunol 1985; 7: 121-128.
17. Polgar B, Kispal G, Lachmann M, Paar G, Nagy E, Csere P, Miko E, Szereday L, Varga P, Szekeres-Bartho J: Molecular cloning and immunologic characterization of a novel cDNA coding for progesterone-induced blocking factor. J Immunol 2003; 171: 5956-5963.
18. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L: Progesterone as an immunomodulatory molecule. Int Immunopharmacol 2001; 1: 1037-1048.
19. Maccarrone M, Bari M, Di Rienzo M, Finazzi-Agro A, Rossi A: Progesterone activates fatty acid amide hydrolase (FAAH) promoter in human T lymphocytes through the transcription factor Ikaros. Evidence for a synergistic effect of leptin. J Biol Chem 2003; 278: 32726-32732.
20. Dai D, Wolf DM, Litman ES, White MJ, Leslie KK: Progesterone inhibits human endometrial cancer cell growth and invasiveness: Down-regulation of cellular adhesion molecules through progesterone B receptors. Cancer Res 2002; 62: 881-886.
21. Arruvito L, Giulianelli S, Flores AC, Paladino N, Barboza M, Lanari C, Fainboim L: NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J Immunol 2008; 180: 5746-5753.
22. Dimitrov R, Timeva T, Kyurkchiev D, Stamenova M, Shterev A, Kostova P, Zlatkov V, Kehayov I, Kyurkchiev S: Characterization of clonogenic stromal cells isolated from human endometrium. Reproduction 2008; 135: 551-558.
23. Dimitrov R, Kyurkchiev DS, Timeva TN, Yunakova M, Stamenova M, Shterev AD, Kyurkchiev SD: Human pre-decidual stromal cells have the characteristics of mesenchymal stem cells. Fertil Steril 2009, (in press).
24. McIntosh K, Bartholomew A: Stromal cell modulation of the immune system. Graft 2000; 3: 324-328
25. Di Nicola M, Carlostella C, Magni M, Milanesi M, Longoni PD, Matteucci R, Gisanti S, Giann AM: Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99: 3838-3843.
26. Le Blanc K, Tammik C, Sundberg B, Haynesworth S, Ringdén O: Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility system. Scand J Immunol 2003; 57: 11-20.
27. Zhang W, Ge W, Li C, You S, Liao L, Han Q, Deng W, Zhao RCH: Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 2004; 13: 263-271.
28. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD, Mao N: Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005; 105: 4120-4126.
29. Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M: Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006;24: 74-85.
30. Bochev I, Elmadjian G, Kyurkchiev D, Tzvetanov L, Altankova I, Tivchev P, Kyurkchiev S: Mesenchymal stem cells from human bone marrow or adipose tissue differently modulate mitogen-stimulated B-cell immunoglobulin production in vitro. Cell Biol Int 2008; 32: 384-393.
31. Paul P, Cabestre AF, Gal FA, Khalil-Daher I, Danff C, Schmid M, Mercier S, Avril M-F, Dausset J, Guillet J-G, Carosella ED: Heterogeneity of HLA-G gene transcription and protein expression in malignant melanoma biopsies. Cancer Res 1999; 59: 1954-1960.
32. Moreau P, Mouillot G, Rousseau P, Marcou C, Dausset J, Carosella ED: HLA-G gene repression is reversed by demethylation. Proc Natl Acad Sci USA 2003; 100: 1191-1196.
33. 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.
34. Yang Y, Chu W, Geraghty DE, Hunt JS: Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol 1996; 156: 4224-4231.
35. Wiendl H, Mitsdoerffer M, Hofmeister V, Wischhusen J, Bornemann A, Meyermann R, Weiss EH, Melms A, Weller M: A functional role of HLA-G expression in human gliomas: An alternative strategy of immune escape. J Immunol 2002; 168: 4772-4780.
36. Torres MI, López-Casado MA, Luque J, Peña J, Ríos A: New advances in coeliac disease: Serum and intestinal expression of HLA-G. Int Immunol 2006; 18: 713-718.
37. Lafon M, Prehaud C, Megret F, Lafage M, Mouillot G, Roa M, Moreau P, Rouas-Freiss N, Carosella ED: Modulation of HLA-G expression in human neural cells after neurotropic viral infections. J Virol 2005; 79: 15226-15237.
38. Derrien M, Pizzato N, Dolcini G, Menu E, Chaouat G, Lenfant F, Barré-Sinoussi F, Le Bouteiller P: Human immunodeficiency virus 1 downregulates cell surface expression of the non-classical major histocompatibility class I molecule HLA-G1. J Gen Virol 2004; 85: 1945-1954.
39. Urosevic M, Willers J, Mueller B, Kempf W, Burg G, Dummer R: HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood 2002; 99: 609-617.
40. Sheshgiri R, Rao V, Tumiati LC, Xiao R, Prodger JL, Badiwala M, Librach C, Delgado DH: Progesterone induces human leukocyte antigen-G expression in vascular endothelial and smooth muscle cells. Circulation 2008; 118: S58-S64.
41. Yie S, Li L, Li G, Xiao R, Librach CL: Progesterone enhances HLA-G gene expression in JEG-3 choriocarcinoma cells and human cytotrophoblasts in vitro. Hum Reprod 2006; 21: 46-51.
42. Blanco O, Tirado I, Munoz-Fernandez R, Clara Abadia-Molina A, Marcos Garcia-Pacheco J, Pena J, Olivares EG: Human decidual stromal cells express HLA-G effects of cytokines and decidualization. Hum Reprod 2008; 23: 144-152.