Effect of Progesterone on Human Mesenchymal Stem Cells

Vitamins and Hormones

Volumn 87, Issue , 2011, Pages 217-237

  Kyurkchiev, Dobroslav S ^a   Ivanova Todorova, Ekaterina ^a   Kyurkchiev, Stanimir D ^b  

^a UNIVERSITY HOSPITAL ALEXANDROVSKA   (Bulgaria)

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

Author keywords

Endometrium; Immunoregulatory molecules; Mesenchymal stem cells; Pregnancy; Progesterone

Indexed keywords

EID: 84857129806     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386015-6.00040-8     Document Type: Chapter

References (102)

1. Bainbridge D.R.J., Ellis S.A., Sargent I.L. HLA-G suppresses proliferation of CD4+ T-lymphocytes. J. Reprod. Immunol. 2000, 48:17-26.
2. Blanco O., Tirado I., Munoz-Fernandez R., Abadi{dotless}a-Molina C.A., Garci{dotless}a-Pacheco M.J., Pena J., Olivares E.G. Human decidual stromal cells express HLA-G effects of cytokines and decidualization. Hum. Reprod. 2008, 23:144-152.
3. Blaschitz A., Lenfant F., Mallet V., Hartmann M., Bensussan A., Geraghty D.E., 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.
4. 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.
5. Brosens J.J., Hayashi N., White J.O. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 1999, 140:4809-4820.
6. Castro-Malaspina H., Gay R.E., Resnick G., Kapoor N., Meyers P., Chiarieri D., McKenzie S., Broxmeyer H.H., Moore M.A. Characterisation of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 1980, 56:289-301.
7. Chan R.W.S., Schwab K.E., Garget C.E. Clonogenicity of human endometrial epithelial and stromal cells. Biol. Reproduction. 2004, 70:1738-1750.
8. Check J., Szekeres-Bartho J., O'Slaughnessy A. Progesterone induced blocking factor seen in pregnancy lymphocytes soon after implantation. Am. J. Reprod. Immunol. 1996, 35:277-280.
9. Chek J., Arwitz M., Gross J., Peymer M., Szekeres-Bartho J. Lymphocyte immunotherapy (LI) increases serum levels of (PIBF). Am. J. Reprod. Immunol. 1997, 37:17-20.
10. Chu W., Fant M.E., Geraghty D.E., Hunt J.S. Soluble HLA-G in human placentas: Synthesis in trophoblasts and interferon-g-activated macrophages but not placental fibroblasts. Hum. Immunol. 1998, 59:435-442.
11. Colter D.C., Sekiya I., Prockop D.J. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl. Acad. Sci. USA 2001, 98(14):7841-7845.
12. Condon J.C., Hardy D.B., Kovaric K., Mendelson C.R. Upregulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of NF-{kappa}B may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol. 2006, 20:764-775.
13. 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.
14. 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.
15. Dimitrov R., Kyurkchiev D., Timeva T., Yunakova M., Stamenova M., Shterev A., Kyurkchiev S. First-trimester human decidua contains a population of mesenchymal stem cells. Fertil. Steril. 2010, 93:210-219.
16. Dosiou C., Guidice L.C. Natural killer cells in pregnancy and reccurent pregnancy loss: Endocrine and immunologic perspectives. Hum. Reprod. 2001, 16:855-861.
17. Dosiou C., Guidice L.C. NK cells in pregnancy and recurrent pregnancy loss: Endocrine and immunologic perspectives. Endocr. Rev. 2005, 26:44-62.
18. Du H., Taylor H.S. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells 2007, 25(8):2082-2086.
19. Dunn C.L., Kelly R.W., Critchley H.O.D. Decidualization of the human endometrial stromal cell: An enigmatic transformation. Reprod. Biomed. Online 2003, 7:151-161.
20. Falkenstein E., Schmieding K., Lange A., Meyer C., Gerdes D., Welsch U., Wehling M. Localization of a putative progesterone membrane binding protein in porcine hepatocytes. Cell. Mol. Biol. 1998, 44(4):571-578.
21. 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.
22. Friedstein A.J., Petrakova K.V., Kurolesova A.I., Frolova G.P. Heterotopic transplants of bone marrow. Analysis of precursor cells for osteogenic and hematopoetic tissues. Transplantation 1968, 6:230-247.
23. Gang E.J., Bosnakovski D., Figueiredo C.A., Visser J.W., Perlingeiro R.C. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 2007, 109:1743-1751.
24. Gargett C.E. Uterine stem cells: What is the evidence?. Hum. Reprod. Update 2007, 13:87-101.
25. Gellersen B., Fernandes M.S., Brosens J.J. Non- genomic progesterone actions in female reproduction. Hum. Reprod. Update. 2009, 15:119-138.
26. Geraghty D.E., Koller B.H., Orr H.T. A human majorhistocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment. Proc. Natl. Acad. Sci. USA 1987, 84:9145-9149.
27. Graham J.D., Clarke C.L. Physiological action of progesterone in target tissues. Endocrinol Rev. 1997, 18:502-519.
28. Gronthos S., Graves S.E., Ohta S., Simmons P.J. The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 1994, 84:4164-4173.
29. Hansen P.J., Skopets B. Temporal relationship between progesterone and uterine lymphocyte-inhibitory activity in ewes. Vet. Rec. 1992, 131:371-372.
30. Henderson T.A., Saunders P.T., Moffet-King A., Grrome N.O., Critchley H.O. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2003, 88:440-449.
31. Hirshfield A.N. Stathmokinetic analysis of granulosa cell proliferation in antral follicles of cyclic rats. Biol. Reprod. 1984, 31:52-58.
32. Huang G.T.-J., Gronthos S., Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: Their biology and role in regenerative medicine. J. Dent. Res. 2009, 88:792-806.
33. Irwin J.C., Kirk D., King R.J.B., Quigley M.M., Gwatkin R.B.L. Hormonal regulation of human endometrial stromal cells in culture: And in vitro model for decidualization. Fertil. Steril. 1989, 52:761-768.
34. Irwin J.C., Utian W.H., Eckert R.L. Sex steroids and growth factors differentially regulate the growth and differentiation of cultured human endometrial stromal cells. Endocrinology 1991, 129:2385-2392.
35. Ismail P.M., Amato P., Soyal S.M., DeMayo F.J., Conneely O.M., O'Malley B.W., Lydon J.P. Progesterone involvement in breast development and tumorigenesis-As revealed by progesterone receptor " knockout" and " knockin" mouse models. Steroids 2003, 68:779-787.
36. Ivanova-Todorova E., Kyurkchiev D., Nalbanski A., Timeva T., Shterev A., Kyurkchiev S. Production and characterization of a novel monoclonal antibody against progesterone-induced blocking factor (PIBF). J. Reprod. Immunol. 2008, 78:94-101.
37. Ivanova-Todorova E., Ivan Bochev I., Mourdjeva M., Dimitrov R., Bukarev D., Kyurkchiev S., Tivchev P., Alrtankova I., Kyurkchiev D. Adipose tissue derived mesenchymal stem cells are more potent suppressors of dendritic cells differentiation copmpared with bone-marrow derived mesenchymal stem cells. Immunol. Lett. 2009, 126:37-42.
38. Ivanova-Todorova E., Mourdjeva M., Kyurkchiev D., Bochev I., Stoyanova E., Dimitrov R., Timeva T., Yunakova M., Bukarev D., Shterev A., Tivchev P., Kyurkchiev S. HLA-G expression is up-regulated by progesterone in mesenchymal stem cells. Am. J. Reprod. Immunol. 2009, 62:25-33.
39. Ivanova-Todorova E., Kyurkchiev D., Mourdjeva M., Dimitreov R., Stoyanova E., Timeva T., Yunakova M., Shterev A., Kyurkchiev S. Pre-decidual multipotent stromal cells (PreDMSC) constitutively express progesterone induced blocking factor (PIBF). C. R. Acad. Bulg. Sci. 2009, 62(12):1567-1570.
40. Jones R.A., Straszynski L., Meredith D.M., Markham A.F., Jack A., Emery P., McGonagle D. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002, 46:3349-3360.
41. van Kaer L., Wu M., Ichikawa Y., Ito K., Bouneville M., Ostrand-Rosenberg S., Murphy D.B., Tonegawa S. Recognition of MHC TL gene products by gd T cells. Immunol Rev. 1991, 120:89-115.
42. Karystinou A., Dell'Accio F., Kurth T.B., Wackerhage H., Khan I.M., Archer C.W., Jones E.A., Mitsiadis T.A., De Bari C. Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology 2009, 48:1057-1064.
43. Kato K., Yoshimoto M., Keiji Kato, Adachi1 S., Yamayoshi1 A., Arima T., Asanoma K., Kyo S., Nakahata T., Wake N. Characterization of side-population cells in human normal endometrium. Hum. Reprod. 2007, 22(5):1214-1223.
44. Kovats S., Main E.K., Librach C., Stubblebine M., Fisher S.J., DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990, 248:220-223.
45. Kozma N., Halasz M., Polgar B., Poehlmann T.G., Markert U.R., Palkovics T., Keszei M., Par G., Kiss K., Szeberenyi J., Grama L., Szekeres-Bartho J. Progesterone-induced blocking factor ctivates STAT6 via binding to a novel IL-4 receptor. J. Immunol. 2006, 176:819-826.
46. Kyurkchiev D., Ivanova-Todorova E., Kyurkchiev S. New target cells of the immunomodulatory effects of progesterone. Reprod. Biomed. Online 2010, 21:304-311.
47. Lafon M., Prehaud C., Megret F., Lafage M., Mouillot G., Roa M., Moreau P., Rouas-Freiss N., Carosella E.D. Modulation of HLA-G expression in human neural cells after neurotropic viral infections. J. Virol. 2005, 79:15226-15237.
48. Le Bouteiller P. HLA class I chromosomal region, genes, and products: Facts and questions. Crit. Rev. Immunol. 1994, 14:89-105.
49. Le Bouteiller P., Solier C., Pro'll J., Aguerre-Girr M., Fournel S., Lenfant F. Mini symposium. 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.
50. Li X., O'Malley B.W. Unfolding the action of progesterone receptors. J. Biol. Chem. 2003, 278:39261-39264.
51. Lockwood C.J., Krikun G., Runic R., Schwartz L.B., Mesia A.F., Schatz F. Progestin-epidermal growth factor regulation of tissue factor expression during decidualization of human endometrial stromal cells. J. Clin. Endocrinol. Metab. 2000, 85:297-301.
52. Losel R.M., Falkenstein E., Feuring M., Schultz A., Tillmann H.-C., Rossol-Haseroth K., Wehling M. Nongenomic steroid action: Controversies, questions, and answers. Physiol. Rev. 2003, 83:965-1016.
53. Losel R.M., Besonga D., Peluso J.J., Wehlinga M. Progesterone receptor membrane component 1-Many tasks for a versatile protein. Steroids 2008, 73:929-934.
54. Mallet V., Blaschitz A., Crisa L., Schmitt C., Fournel S., King A., Loke Y.W., Dohr G., Le Bouteiller P.H. 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.
55. Marchal-Bras-Goncalves R., Rouas-Freiss N., Connan F., Choppin J., Dausset J., Carosella E.D., Kirszenbaum M., Guillet J.-G. A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant. Proc. 2001, 33:2355-2359.
56. McMaster M.T., Librach C.L., Zhou Y., Lim K.H., Janatpour M.J., DeMars R., Kovats S., Damsky C., Fisher S.J. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol. 1995, 154:3771-3778.
57. Meirelles L.D.S., Chagastelles P.C., Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006, 119(11):2204-2213.
58. Meizel S., Turner K.O., Nuccitelli R. Progesterone triggers a wave of increased free calcium during the human sperm acrosome reaction. Dev. Biol. 1997, 182:67-75.
59. Meng X., Ichim T.E., Zhong J., Rogers A., Yin Z., Jackson J., Wang H., Ge W., Bogin V., Chan K.W., Thébaud B., Neil H.R. Endometrial regenerative cells: A novel stem cell population. J. Transl. Med. 2007, 5:57-67.
60. Minguelli J.J., Erices A., Conget P. Mesenchymal stem cells. Exp. Biol. Med. 2001, 226:507-520.
61. Moreau P., Adrian-Cabestre F., Menier C., Guiard V., Gourand L., Dausset J., Carosella E.D., Paul P. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int. Immunol. 1999, 11:803-811.
62. Mourdjeva M., Ivanova-Todorova E., Kyurkchiev D., Bochev I., Stoyanova E., Dimitrov R., Kyurkchiev S. Progesterone enhances the HLA-G expression in mesenchymal stem cells. C. R. Acad. Bulg. Sci. 2009, 62(12):1567-1570.
63. Mulac-Jericevic B., Mullinax R.A., DeMayo F.J., Lydon J.P., Conneely O.M. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 2000, 289:1751-1754.
64. Navarrete M.A., Maier C.M., Falzoni R., Cuadros L.G., Lima G.R., Baracat E.C., Nazario A.C. Assessment of the proliferative, apoptotic and cellular renovation indices of the human mammary epithelium during the follicular and luteal phases of the menstrual cycle. Breast Cancer Res. 2005, 7(3):306-313.
65. Norman A.W., Mizwicki M.T., Norman D.P. Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat. Rev. Drug Discov. 2004, 3:27-41.
66. Olivares E.G., Montes M.J., Oliver C., Galindo J.A., Riuz C. Cultured human decidual stromal cells express B7-1 (CD80) and stimulate allogenic T cells. Biology of Reproduction 1997, 5709-615:6.
67. Owen M. Marrow stromal cells. J. Cell Sci. Suppl. 1988, 10:63-76.
68. Patel A.N., Park E., Kuzman M., Benetti F., Silva F.J., Allickson J.G. Multipotent menstrual blood stromal stem cells: isolation, characterization and differentiation. Cell Transplantation. 2008, 17:303-311.
69. Peluso J. Multiplicity of progesterone's actions and receptors in the mammalian ovary. Biol. Reprod. 2006, 75:2-8.
70. Piva M., Flieger O., Rider V. Growth factor control of cultured rat uterine stromal cell proliferation is progesterone dependent. Biol. Reprod. 1996, 55:1333-1342.
71. Prianishnikov V.A. On the concept of stem cell and a model of functional-morphological structure of the endometrium. Contraception 1978, 18:213-223.
72. Quirici N., Soligo D., Bossolasco P., Servida F., Lumini C., Deliliers G.L. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp. Hematol. 2002, 30:783-791.
73. Reyes M., Dudek A., Jahagirdar B., Koodie L., Marker P.H., Verfaillie C.M. Origin of endothelial progenitors in human postnatal bone marrow. J. Clin. Invest. 2002, 109(3):337-346.
74. Rosen J.M. Hormone receptor patterning plays a critical role in normal lobuloalveolar development and breast cancer progression. Breast Dis. 2003, 18:3-9.
75. Rothchild I. The corpus luteum revisited: Are the paradoxical effects of RU486 a clue to how progesterone stimulates its own secretion?. Biol. Reprod. 1996, 55:1-4.
76. Schumacher M., Guennoun R., Ghoumari A., Massaad C., Robert F., El-Etr M., Akwa Y., Rajkowski K., Baulieu E.E. Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr. Rev. 2007, 28:387-439.
77. Schüring A.N., Schulte N., Kelsch R., Ropke A., Kiesel L., Gotte M. Characterization of endometrial mesenchymal stem-like cells obtained by endometrial biopsy during routine diagnostics. Fertil. Steril. 2011, 95:423-426.
78. Schwab K.E., Gargett C.E. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum. Reprod. 2007, 22:2903-2911.
79. Schwab K.E., Chan R.W., Gargett C.E. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil. Steril. 2005, 84:1124-1130.
80. Schwab K.E., Hutchinson P., Gargett C.E. Identification of surface markers for prospective isolation of human endometrial stromal colony-forming cells. Hum. Reprod. 2008, 23:934-943.
81. Setty S.L., Mills T.M. The effects of progesterone on follicular growth in the rabbit ovary. Biol. Reprod. 1987, 36:1247-1252.
82. Sheshgiri R., Rao V., Tumiati L.C., Xiao R., Prodger J.L., Badiwala M., Librach C., Delgado D.H. Progesterone induces human leukocyte antigen-G expression in vascular endothelial and smooth muscle cells. Circulation 2008, 118:58-64.
83. Simmons P.J., Torok-Storb B. Identification of stromal cells precursors in human bone marrow by a novel monoclonal antibody STRO-1. Blood 1991, 78:55-62.
84. Singh M. Progesterone-induced neuroprotection. Endocrine 2006, 29:271-274.
85. Szekeres-Bartho J., Wegmann T.G. A progesterone-dependent immunomodulatory protein alters the Th1/Th2 balance. J. Reprod. Immunol. 1996, 31:81-95.
86. Szekeres-Bartho J., Hadnagy J., Pacsa A.S. The suppressive effect of progesterone on lymphocyte cytotoxicity: Unique progesterone sensitivity of pregnancy lymphocytes. J. Reprod. Immunol. 1985, 7:121-128.
87. Szekeres-Bartho J., Autran B., Debre P., Andreu G., Denver L., Chaouat G. Immunoregulatory effects of a suppressor factor from healthy pregnant women's lymphocytes after progesterone induction. Cell. Immunol. 1989, 122:281-294.
88. Szekeres-Bartho J., Szekeres G.Y., Dedre P., Autran B., Chaouat G. Reactivity of lymphocytes to a progesterone receptor-specific monoclonal antibody. Cell. Immunol. 1990, 125:273-283.
89. Szekeres-Bartho J., Faust Zs, Varga P. The expression of a progesterone-induced immunomodulatory protein in pregnancy lymphocytes. Am. J. Reprod. Immunol. 1995, 34:342-348.
90. Szekeres-Bartho J., Barakonyi A., Miko E., Polgar B., Palkovics T. The role of gamma/delta T cells in the feto-maternal relationship. Semin. Immunol. 2001, 13:229-233.
91. Szekeres-Bartho J., Barakonyi A., Par G., Polgar B., Palkovics T., Szereday L. Progesterone as an immunomodulatory molecule. Int. Immunopharmacol. 2001, 1:1037-1048.
92. Taylor H.S. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004, 292:81-85.
93. Torres M.I., Lopez-Casado M.A., Luque J., Peña J., Ri{dotless}os A. New advances in coeliac disease: Serum and intestinal expression of HLA-G. Int. Immunol. 2006, 18:713-718.
94. 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.
95. Welm B.E., Tepera S.B., Venezia T., Graubert T.A., Rosen J.M., Goodell M.A. Sca-1 (pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev. Biol. 2002, 245:42-56.
96. Wiendl H., Mitsdoerffer M., Hofmeister V., Wischhusen J., Bornemann A., Meyermann R., Weiss E.H., 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.
97. Wright D.W., Kellermann A.L., Hertzberg V.S., Clark P.L., Frankel M., Goldstein F.C., Salomone J.P., Dent L.L., Harris O.A., Ander D.S., Lowery D.W., Patel M.M., et al. ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury. Ann. Emerg. Med. 2007, 49:391-402.
98. Xiao G., Wei J., Yan W., Wang W., Lu Z. Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: A randomized controlled trial. Crit. Care 2008, 12:153-163.
99. Xin L., Lawson D.A., Witte O.N. The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc. Natl. Acad. Sci. USA 2005, 102:6942-6947.
100. Yang Y., Chu W., Geraghty D.E., Hunt J.S. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J. Immunol. 1996, 156:4224-4231.
101. Yie S., Li L., Li G., Xiao R., Librach C.L. Progesterone enhances HLA-G gene expression in JEG-3 choriocarcinoma cells and human cytotrophoblasts in vitro. Hum. Reprod. 2006, 21:46-51.
102. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., Alfonso Z.C., Fraser J.K., Benhaim P., Hedrick M.H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 2002, 13:4279-4295.