Placenta
Volume 30, Issue 12 , Pages 1016-1022 , December 2009

Expression and Regulation by PPARγ of hCG α- and β-subunits: Comparison between Villous and Invasive Extravillous Trophoblastic Cells

  • K. Handschuh

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • ,
  • J. Guibourdenche

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • Biologie Hormonale, CHU Cochin, Paris F 75014, France
    • PremUP, Foundation, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • ,
  • M. Cocquebert

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • PremUP, Foundation, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • ,
  • V. Tsatsaris

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • AP-HP, Maternité Port-Royal, groupe hospitalier Cochin, Paris F 75014, France
    • PremUP, Foundation, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • ,
  • M. Vidaud

      Affiliations

    • Université Paris Descartes, Paris F 75006, France
    • INSERM, UMR745, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • ,
  • D. Evain-Brion

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • PremUP, Foundation, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • ,
  • T. Fournier

      Affiliations

    • INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Université Paris Descartes, Paris F 75006, France
    • AP-HP, Maternité Port-Royal, groupe hospitalier Cochin, Paris F 75014, France
    • PremUP, Foundation, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France
    • Corresponding Author InformationCorresponding author. INSERM, UMR767, Faculté des Sciences Pharmaceutiques et Biologiques, Paris F 75006, France. Tel.: +33 (1) 53 73 96 03; fax: +33 (1) 44 07 39 92.

,Accepted 18 September 2009.

References 

  1. Pierce JG, Parsons TF. Glycoprotein hormones: structure and function. Annu Rev Biochem. 1981;50:465–495
  2. Hartree AS, Renwick AGC. Molecular structures of glycoprotein hormones and functions of their carbohydrate components. Biochem J. 1992;287:665–679
  3. Bo M, Boime I. Identification of the transcriptionally active genes of the chorionic gonadotropin β gene cluster in vivo. J Biol Chem. 1992;267:3179–3184
  4. Miller-Lindholm AK, LaBenz CJ, Ramey J, Bedows E, Ruddon RW. Human chorionic gonadotropin-gene expression in first trimester placenta. Endocrinology. 1997;138:5459–5465
  5. Rull K, Laan M. Expression of – subunit of human chorionic gonadotropin genes during the normal and failed pregnancy. Hum Reprod. 2005;20:3360–3368
  6. Jaffe RB, Lee PA, Midgley AR. Serum gonadotropins before, at the inception of, and following human pregnancy. J Clin Endocrinol Metab. 1969;29:1281–1283
  7. Hay DL, Lopata A. Chorionic gonadotropin secretion by human embryos in vitro. J Clin Endocrinol Metab. 1988;67:1322–1324
  8. Jameson JL, Hollenberg AN. Regulation of chorionic gonadotropin gene expression. Endocr Rev. 1993;14:203–221
  9. Yang M, Lei ZM, Rao ChV. The central role of human chorionic gonadotropin in the formation of human placental syncytium. Endocrinology. 2003;144:1108–1120
  10. Malassine A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9:531–539
  11. Cronier L, Bastide B, Herve JC, Deleze J, Malassine A. Gap junctional communication during human trophoblast differentiation: influence of human chorionic gonadotropin. Endocrinology. 1994;135:402–408
  12. Keryer G, Alsat E, Tasken K, Evain-Brion D. Cyclic AMP-dependent protein kinases and human trophoblast cell differentiation in vitro. J Cell Sci. 1998;111:995–1004
  13. Loke YW, King A. Human implantation. Cell biology and immunology. Cambridge University Press; 1995;
  14. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest. 2004;114:744–754
  15. Handschuh K, Guibourdenche J, Tsatsaris V, Guesnon M, Laurendeau I, Evain-Brion D, et al. Human chorionic gonadotropin expression in human trophoblasts from early placenta: comparative study between villous and extravillous trophoblastic cells. Placenta. 2007;28:175–184
  16. Handschuh K, Guibourdenche J, Tsatsaris V, Guesnon M, Laurendeau I, Evain-Brion D, et al. Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor-gamma. Endocrinology. 2007;148:5011–5019
  17. Tarrade A, Schoonjans K, Guibourdenche J, Bidart JM, Vidaud M, Auwerx J, et al. PPAR gamma/RXR α heterodimers are involved in human CG β synthesis and human trophoblast differentiation. Endocrinology. 2001;142:4504–4514
  18. Schaiff WT, Carlson MG, Smith SD, Levy R, Nelson DM, Sadovsky Y. Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab. 2000;85:3874–3881
  19. Tarrade A, Schoonjans K, Pavan L, Auwerx J, Rochette-Egly C, Evain-Brion D, et al. PPARgamma/RXRα heterodimers control human trophoblast invasion. J Clin Endocrinol Metab. 2001;86:5017–5024
  20. Tarrade A, Lai Kuen R, Malassine A, Tricottet V, Blain P, Vidaud M, et al. Characterization of human villous and extravillous trophoblasts isolated from first trimester placenta. Lab Invest. 2001;81:1199–1211
  21. Handschuh K, Guibourdenche J, Guesnon M, Laurendeau I, Evain-Brion D, Fournier T. Modulation of PAPP-A expression by PPARgamma in human first trimester trophoblast. Placenta. 2006;27(Suppl. A):S127–S134
  22. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology. 1986;118:1567–1582
  23. Bieche I, Parfait B, Le Doussal V, Olivi M, Rio MC, Lidereau R, et al. Identification of CGA as a novel estrogen receptor-responsive gene in breast cancer: an outstanding candidate marker to predict the response to endocrine therapy. Cancer Res. 2001;61:1652–1658
  24. Frendo JL, Vidaud M, Guibourdenche J, Luton D, Muller F, Bellet D, et al. Defect of villous cytotrophoblast differentiation into syncytiotrophoblast in Down's syndrome. J Clin Endocrinol Metab. 2000;85:3700–3707
  25. Frendo JL, Therond P, Guibourdenche J, Bidart JM, Vidaud M, Evain-Brion D. Modulation of copper/zinc superoxide dismutase expression and activity with in vitro differentiation of human villous cytotrophoblasts. Placenta. 2000;21:773–781
  26. Massin N, Frendo JL, Guibourdenche J, Luton D, Giovangrandi Y, Muller F, et al. Defect of syncytiotrophoblast formation and human chorionic gonadotropin expression in Down's syndrome. Placenta. 2001;22(Suppl. A):S93–S97
  27. Braunstein GD, Rasor JL, Engvall E, Wade ME. Interrelationships of human chorionic gonadotropin, human placental lactogen, and pregnancy-specific β 1-glycoprotein throughout normal human gestation. Am J Obstet Gynecol. 1980;138:1205–1213
  28. Moy E, Kimzey LM, Nelson LM, Blithe DL. Glycoprotein hormone α-subunit functions synergistically with progesterone to stimulate differentiation of cultured human endometrial stromal cells to decidualized cells: a novel role for free α-subunit in reproduction. Endocrinology. 1996;137:1332–1339
  29. Knofler M, Saleh L, Bauer S, Vasicek R, Griesinger G, Strohmer H, et al. Promoter elements and transcription factors involved in differentiation-dependent human chorionic gonadotrophin-α messenger ribonucleic acid expression of term villous trophoblasts. Endocrinology. 2000;141:3737–3748
  30. Feinman MA, Kliman HJ, Caltabiano S, Strauss JF. 8-Bromo-3′,5'-adenosine monophosphate stimulates the endocrine activity of human cytotrophoblasts in culture. J Clin Endocrinol Metab. 1986;63:1211–1217
  31. Hussa RO, Pattillo RA, Ruckert AC, Scheuermann KW. Effects of butyrate and dibutyryl cyclic AMP on hCG-secreting trophoblastic and non-trophoblastic cells. J Clin Endocrinol Metab. 1978;46:69–76
  32. Knofler M, Saleh L, Strohmer H, Husslein P, Wolschek MF. Cyclic AMP- and differentiation-dependent regulation of the proximal α HCG gene promoter in term villous trophoblasts. Mol Hum Reprod. 1999;5:573–580
  33. Malassiné A, Frendo JL, Evain-Brion D. Trisomy 21- affected placentas highlight prerequisite factors for human trophoblast fusion and differentiation. Int J Dev Biol, in press.
  34. Ringler GE, Kallen CB, Strauss JF. Regulation of human trophoblast function by glucocorticoids: dexamethasone promotes increased secretion of chorionic gonadotropin. Endocrinology. 1989;124:1625–1631
  35. Morrish DW, Bhardwaj D, Dabbagh LK, Marusyk H, Siy O. Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. J Clin Endocrinol Metab. 1987;65:1282–1290
  36. Matsuzaki N, Li Y, Masuhiro K, Jo T, Shimoya K, Taniguchi T, et al. Trophoblast-derived transforming growth factor-β 1 suppresses cytokine-induced, but not gonadotropin-releasing hormone-induced, release of human chorionic gonadotropin by normal human trophoblasts. J Clin Endocrinol Metab. 1992;74:211–216
  37. Andersen B, Milsted A, Kennedy G, Nilson JH. Cyclic AMP and phorbol esters interact synergistically to regulate expression of the chorionic gonadotropin genes. J Biol Chem. 1988;263:15578–15583
  38. Alsat E, Wyplosz P, Malassine A, Guibourdenche J, Porquet D, Nessmann C, et al. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J Cell Physiol. 1996;168:346–353
  39. Guibourdenche J, Alsat E, Soncin F, Rochette-Egly C, Evain-Brion D. Retinoid receptors expression in human term placenta: involvement of RXR α in retinoid induced-hCG secretion. J Clin Endocrinol Metab. 1998;83:1384–1387
  40. Leisser C, Saleh L, Haider S, Husslein H, Sonderegger S, Knöfler M. Tumour necrosis factor-α impairs chorionic gonadotrophin β-subunit expression and cell fusion of human villous cytotrophoblast. Mol Hum Reprod. 2006;12:601–609
  41. Haider S, Knöfler M. Human tumour necrosis factor: physiological and pathological roles in placenta and endometrium. Placenta. 2009;30:111–123
  42. Heckert LL, Schultz K, Nilson JH. The cAMP response elements of the α subunit gene bind similar proteins in trophoblasts and gonadotropes but have distinct functional sequence requirements. J Biol Chem. 1996;271:31650–31656
  43. Knofler M, Saleh L, Bauer S, Galos B, Rotheneder H, Husslein P, et al. Transcriptional regulation of the human chorionic gonadotropin β gene during villous trophoblast differentiation. Endocrinology. 2004;145:1685–1694

☆ This work was supported by “la Caisse d'Assurance Maladie des Professions Libérales-Province”, CAMPLP, Paris la Défense, 92042, France.

PII: S0143-4004(09)00302-6

doi: 10.1016/j.placenta.2009.09.006

Placenta
Volume 30, Issue 12 , Pages 1016-1022 , December 2009

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