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Human endometrium as a neuroendocrine tissue: Expression, regulation and biological roles of endometrial corticotropin-releasing hormone (CRH) and opioid peptides

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References

  1. Vale W., Spiess J., Rivter C, Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 213: 1394, 1981.

    Article  PubMed  CAS  Google Scholar 

  2. Vale W., Rivier C, Brown M.R., Spiess J., Koob G., Swanson A. Chemical and biological characterization of corticotropin-releasing factor. Recent Prog. Horm. Res. 39: 245, 1983.

    PubMed  CAS  Google Scholar 

  3. Antoni F.A. Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor. Endocr. Rev. 7: 351, 1986.

    Article  PubMed  CAS  Google Scholar 

  4. Orth D. Corticotropin-releasing hormone in humans. Endocr. Rev. 13: 164, 1992.

    PubMed  CAS  Google Scholar 

  5. Usui T., Nakai Y., Tsukada T., Jingami H., Takahashi H., Fucada J. Expression of adrenocorticotropin-releasing hormone precursor gene in placenta and other nonhypothalamic tissues in man. Mol. Endocrinol. 2: 871, 1988.

    Article  PubMed  CAS  Google Scholar 

  6. Suda T., Tomori N., Tozawa F., Mouri T., Demoura H., Shizume K. Distribution and characterization of immunoreactive corticotropin-releasing factor in human tissues. J. Clin. Endocrinol. Metab. 59: 861, 1984.

    Article  PubMed  CAS  Google Scholar 

  7. Petrusz P., Merghenthaler I., Maderdrut L., Vigh S., Schally A. Corticotropin-releasing factor-like immunoreactivity in the vertebrate endocrine pancreas. Proc. Natl. Acad. Sci. 80: 1721, 1983.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  8. Petrusz P., Merghenthaler I., Ordronneau P., Maderdrut L., Vigh S., Schally A. Corticotropin-releasing factor-like immunoreactivity in the gastro-entero-pancreatic endocrine system. Peptides 5: 71, 1984.

    Article  PubMed  CAS  Google Scholar 

  9. Dammrich J., Ormanns W., Kahaly G., Schrezenmeir J. Multiple peptide hormone producing adenocarcinoma of lung with neurotensin and CRF-like immunoreactivity. Pathol. Res. Pract. 183: 670, 1988.

    Article  PubMed  CAS  Google Scholar 

  10. Owens M.J., Nemeroff C.B. Physiology and pharmacology of corticotropin-releasing factor. Pharmacol. Rev. 43: 425, 1991.

    PubMed  CAS  Google Scholar 

  11. Donaldson C.J., Sutton S.W., Perrin M.H., Corrigan A.Z., Lewis K.A., Rivier J.E., Vaughan J.M., Vale W.W. Cloning and characterization of human urocortin. Endocrinology 137: 2167, 1996.

    Article  PubMed  CAS  Google Scholar 

  12. Ross P.C., Kostas CM., Ramabhadran T.V. A variant of the human corticotropin-releasing factor (CRF) receptor: cloning, expression and pharmacology. Biochem. Biophys. Res. Comun. 205: 1836, 1994.

    Article  CAS  Google Scholar 

  13. Hillhouse E.W., Grammatopoulos D., Milton N.G., Quartero H.W. The identification of a human myometrial corticotropin-releasing hormone receptor that increases in affinity during pregnancy. J. Clin. Endocrinol. Metab. 76: 736, 1993.

    PubMed  CAS  Google Scholar 

  14. Smets G., Van-Gompel J., Meyer C, Abs R., de Menten Y., Kloppel G. Corticotropin-releasing hormone receptors on human pituitary cells: autoradiography at the light microscopical level, quantification and immunocyto-chemistry. Prog. Histochem. Cytochem. 26: 107, 1992.

    Article  PubMed  CAS  Google Scholar 

  15. Polymeropoulos M.H., Torres R., Yanovski J.A., Chandrasekharappa S.C., Ledbetter D.H. The human corticotropin-releasing factor receptor (CRHR) gene maps to chromosome 17q12-q22. Genomics 28: 123, 1995.

    Article  PubMed  CAS  Google Scholar 

  16. Xiong Y., Xie L.Y., Abou-Samra A.B. Signaling properties of mouse and human corticotropin-releasing factor (CRF) receptors: decreased coupling efficiency of human type II CRF receptor. Endocrinology 136: 1828, 1995.

    PubMed  CAS  Google Scholar 

  17. Perrin M., Donaldson C, Chen R., Blount A., Berggren T., Bilezikjian L., Sawchenko P., Vale W. Identification of a second corticotropin-releasing factor receptor gene and characterization of a cDNA expressed in heart. Proc. Natl. Acad. Sci. 92: 2969, 1995.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  18. Kishimoto T., Pearse R.V. 2nd, Lin C.R., Rosenfeld M.G. A sauvagine/corticotropin-releasing factor receptor expressed in heart and skeletal muscle. Proc. Natl. Acad. Sci. USA 92: 1108, 1995.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  19. Lovenberg T.W., Liaw C.W., Grigoriadis D.E., Clevenger W., Chalmers D.T., De Souza E.B., Oltersdorf T. Cloning and characterization of a functionally distinct corticotropin-releasing factor receptor subtype from rat brain. Proc. Natl. Acad. Sci. USA 92: 836, 1995.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  20. Grigoriadis D.E., Heroux J.A., De Souza E.B. Characterization and regulation of corticotropin-releasing factor receptors in the central nervous, endocrine and immune systems. Ciba Found. Symp. 172: 85, discussion 101–7, 1993.

    PubMed  CAS  Google Scholar 

  21. Chang CP., Pearse R.V. 2d, O’Connell S., Rosenfeld M.G. Identification of a seven transmembrane helix receptor for corticotropin-releasing factor and sauvagine in mammalian brain. Neuron. 11: 1187, 1993.

    Article  PubMed  CAS  Google Scholar 

  22. Chen R., Lewis K.A., Perrin M.H., Vale W.W. Expression cloning of a human corticotropin-releasing-factor receptor. Proc. Natl. Acad. Sci. 90: 8967, 1993.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  23. Hughes J. Isolation of an endogenous compound from the brain with pharmacological properties similar to morphine. Brain Res. 88: 295, 1975.

    Article  PubMed  CAS  Google Scholar 

  24. Hughes J., Smith T.W., Kosterlitz H.G., Fothergill L.A., Morgan B.A., Morris H.R. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 258: 577, 1975.

    Article  PubMed  CAS  Google Scholar 

  25. Lynch D.R., Snyder S.H. Neuropeptides: Multiple molecular forms, metabolic pathways and receptors. Ann. Rev. Biochem. 55: 773, 1986.

    Article  PubMed  CAS  Google Scholar 

  26. Lord J.A.H., Waterfield A.A., Hughes J., Kosterlitz H.W. Endogenous opioid peptides:multiple agonists and receptors. Nature 267: 495, 1977.

    Article  PubMed  CAS  Google Scholar 

  27. Numa S. Opioid peptide precursors and their genes. In: Gross E., Meienhofer J. (Eds.), The peptides. Academic Press, New York, 1984, vol. 6, p. 1.

    Google Scholar 

  28. Chavkin C, Goldstein A. Demonstration of a specific dynorphin receptor in guinea pig ileum myenteric plexus. Nature 297: 591, 1981.

    Article  Google Scholar 

  29. Shultz R., Wüster M., Herz A. Endogenous ligands for k-opiate receptors. Peptides 3: 973, 1982.

    Article  Google Scholar 

  30. Chavkin C, James J., Goldstein A. Dynorphin is a specific endogenous ligand of kappa opioid receptor. Science 275: 413, 1982.

    Article  Google Scholar 

  31. Atweh S.F, Kuhar M.J. Distribution and significance of opioid receptors in the brain. Br. Med. Bull. 39: 47, 1983.

    PubMed  CAS  Google Scholar 

  32. Atweh S.F., Kuhar M.J. Autoradiographic localization of opiate receptors in rat brain spinal cord and lower medulla. Brain Res. 124: 53, 1977.

    Article  PubMed  CAS  Google Scholar 

  33. Atweh S.R, Kuhar M.J. Autoradiographic localization of opiate receptors in rat brain stem II. The brain stem. Brain Res. 129: 1, 1977.

    Article  PubMed  CAS  Google Scholar 

  34. Atweh S.F., Kuhar M.J. Autoradiographic localization of opiate receptors in rat brain III. The telencephalon. Brain Res. 134: 393, 1977.

    Article  PubMed  CAS  Google Scholar 

  35. Wüster M., Schultz R., Herz A. Multiple opiate receptors in peripheral tissue preparations. Biochem Pharmacol. 30: 1883, 1981.

    Article  PubMed  Google Scholar 

  36. Yoon D.J., Sklar C., David R. Presence of immunoreactive corticotropin-releasing factor in rat testis. Endocrinology 122: 759, 1988.

    Article  PubMed  CAS  Google Scholar 

  37. Audhya T., Hollander C.S., Schlesinger D.H., Hutchinson B. Structural characterization and localization of corticotropin-releasing factor in testis. Biochim. Biophys. Acta 995: 10, 1989.

    Article  PubMed  CAS  Google Scholar 

  38. Fabbri A., Tinajero J.C, Dufau M.L. Corticotropin-releasing factor is produced by rat Leydig cells and has a major local antireproductive role in the testis. Endocrinology 127: 1541, 1990.

    Article  PubMed  CAS  Google Scholar 

  39. Dufau M.L, Tinajero J.C, Fabbri A. Corticotropin-releasing factor: an antireproductive hormone of the testis. FASEB J 7: 299, 1993.

    PubMed  CAS  Google Scholar 

  40. Huang B.M., Stocco D.M., Hutson J.C., Norman R.L. Corticotropin-releasing hormone stimulates steroidogenesis in mouse Leydig cells. Biol. Reprod. 53: 620, 1995.

    Article  PubMed  CAS  Google Scholar 

  41. Mastorakos G., Webster E., Friedman T., Chrousos G. Immunoreactive corticotropin-releasing hormone and its binding in the rat ovaries. J. Clin. Invest 92: 961, 1993.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  42. Mastorakos G., Scopa C., Vryonidou A., Friedman T., Kattis D., Phenekos C, Merino M., Chrousos G. Presence of immunoreactive corticotropin-releasing hormone in normal and polycystic human ovaries. J. Clin. Endocrinol. Metab. 79: 1191, 1994.

    PubMed  CAS  Google Scholar 

  43. Grino M., Chrousos G., Margioris A. The corticotropin-releasing hormone gene is expressed in human placenta. Biochem. Biophys. Res. Commn. 148: 1208, 1987.

    Article  CAS  Google Scholar 

  44. Margioris A.N. Corticotropin releasing hormone and the placenta and fetal membranes. In: Brennecke S., Rice G. (Eds.), Molecular aspects of placental and fetal membrane autacoids. CRC Press (publs) 1993, vol 12, p. 277.

  45. Linton E.A., Perkins A.V., Woods R.J., Eben F., Wolfe CD., Behan D.P., Potter E., Vale W.W., Lowry P.J. Corticotropin releasing hormone-binding protein (CRH-BP): plasma levels decrease during the third trimester of normal human pregnancy. J. Clin. Endocrinol. Metab. 76: 260, 1993.

    PubMed  CAS  Google Scholar 

  46. Campbell E.A., Linton E.A., Wolfe CD., Scraggs P.P., Jones M.T., Lowry P.J. Plasma corticotropin-releasing hormone concentrations during pregnancy and parturition. J. Clin. Endocrinol. Metab. 64: 1054, 1987.

    Article  PubMed  CAS  Google Scholar 

  47. Frim D., Emanuel P., Robinson B., Smas C., Adler G., Majzoub J. Characterization and gestational regulation of corticotropin-releasing hormone mRNA in human placenta. J. Clin. Invest. 82: 287, 1988.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  48. Petraglia F., Sawchenko P.E., Rivier J., Vale W. Evidence for local stimulation of ACTH secretion by corticotropin-releasing factor in human placenta. Nature 328: 717, 1987.

    Article  PubMed  CAS  Google Scholar 

  49. Robinson B., Emanuel R., Frim D., Majzoub J. Glucocorticoid stimulates expression of corticotropin-releasing hormone gene in human placenta. Proc. Natl. Acad. Sci. 85: 5244, 1988.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  50. Margioris A.N., Grino M., Protos P., Gold P., Chrousos G. Corticotropin-releasing hormone and oxytocin stimulate the release of placental proopiomelanocortin peptides. J. Clin. Endocrinol. Metab. 66: 922, 1988.

    Article  PubMed  CAS  Google Scholar 

  51. Petraglia F., Potter E., Cameron V.A., Sutton S., Behan D.P., Woods R.J., Sawchenko P.E., Lowry P.J., Vale W. Corticotropin-releasing factor-binding protein is produced by human placenta and intrauterine tissues. J. Clin. Endocrinol. Metab. 77: 919, 1993.

    PubMed  CAS  Google Scholar 

  52. Coukos G., Monzani A., Saletti C, Petraglia F. Noradrenaline and interleukin-1 stimulate CRF secretion from human placental cells in culture. Medicina 8: 441, 1988.

    PubMed  CAS  Google Scholar 

  53. Margioris A.N., Grino M., Rabin D., Chrousos G.P. Human placenta and the hypothalamic-pituitary-adrenal axis. Adv. Exp. Med. Biol. 245: 389, 1988.

    Article  PubMed  CAS  Google Scholar 

  54. Hatzoglou A., Margioris A.N., Bakogeorgou E., Gravanis A., Castanas E. Identification, characterization and localization of corticotropin-releasing hormone receptors in human placenta. Life Sci. 59: 1871, 1996.

    Article  PubMed  CAS  Google Scholar 

  55. Quartero H.W., Fry CH. Placental corticotrophin releasing factor may modulate human parturition. Placenta 10: 439, 1989.

    Article  PubMed  CAS  Google Scholar 

  56. Sasaki A., Tempst P., Liotta A.S., Margioris A.N., Hood L.E., Kent S.B., Sato S., Shinkawa O., Yoshinaga K., Krieger D.T. Isolation and characterization of a corticotropin-re leasing hormone-like peptide from human placenta. J. Clin. Endocrinol. Metab. 67: 768, 1988.

    Article  PubMed  CAS  Google Scholar 

  57. Cox B., Rosenberg J.G., Douglass J. Chromatographic characterization of dynorphin and (leu5)enkephalin immunoreactivity in guinea pig and rat testis. Regul. Pept. 19: 17, 1987.

    Article  Google Scholar 

  58. Pintar J.E., Schachter B.S., Herman A.B., Durgerian S., Krieger D.T. Characterization and localization of proopiomelanocortin messenger RNA in the adult rat testis. Science 225: 632, 1984.

    Article  PubMed  CAS  Google Scholar 

  59. Eskeland N.L., Molineaux C.J., Schacter B.S. Regulation of β-endorphin secretion by corticotropin-releasing factor in the intact rat testis. Endocrinology 130: 1173, 1992.

    PubMed  CAS  Google Scholar 

  60. Fabri A., Tsai Morris C.H., Luna S., Fraioli F., Dufau M.L. Opiate receptors are present in rat testis. Identification and localization in Sertoli cells. Endocrinology 117: 2544, 1985.

    Article  Google Scholar 

  61. Sharpe P.M., Cooper I. Comparison of the effects of the purified Leydig cells of four hormones (oxytocin, vasopressin, opiates and LHRH) with suggested paracrine roles in the testis. J. Endocrinol. 113: 89, 1987.

    Article  PubMed  CAS  Google Scholar 

  62. Margioris A.N., Sasaki A., Liotta A.S. Presence and preliminary characterization of immunoreactive dynorphin in human testis. (Abstract). Annual Meeting of The Endocrine Society, 1985: 511.

  63. McMurray C.T., Devi L., Calavetta L., Douglass J.O. Regulated expression of prodynorphin gene in the R2C Leydig tumor cell line. Endocrinology 124: 49, 1988.

    Article  Google Scholar 

  64. Chen C., Chang C, Krieger D.T., Bardin C.W. Expression and regulation of proopiomelanocortin-like gene in the ovary and placenta: comparison with the testis. Endocrinology 118: 2382, 1986.

    Article  PubMed  CAS  Google Scholar 

  65. Kilpatrick D.L., Howell R.D., Noe M., Bailey C.I., Udenfriend S. Expression of preproenkephalin-like mRNA and its peptide products in mammalian testis and ovary. Proc. Natl. Acad. Sci. 82: 7467, 1985.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  66. Lim A.T., Lolait S., Barlow J.W., Wai Sum O., Zos I., Toh B.H., Funder J.W. Immunoreactive b-endorphine in sheep ovary. Nature 303: 709, 1983.

    Article  PubMed  CAS  Google Scholar 

  67. Lolait S.J., Autelitano D.J., Lim A.T.W., Smith A.I., Toh B.H., Funder J.W. Ovarian immunoreactive β-endorphin and estrus-cycle in the rat. Endocrinology 117: 161, 1985.

    Article  PubMed  CAS  Google Scholar 

  68. Facchineti F., Storchi A.R., Petraglia F., Volpe A., Genazzani A.R. Expression of proopiomelanocortin-related peptides in human follicular fluid. Peptides 9: 1089, 1988.

    Article  Google Scholar 

  69. Sanders S.L., Meiner M.H., Curry Jr T.E. Cellular localization of ovarian proopiomelanocortin messenger RNA during follicular and luteal development in the rat. Mol. Endocrinol. 4: 1311, 1990.

    Article  PubMed  CAS  Google Scholar 

  70. Chen C.L.C. Expression and regulation of proopiomelanocortin gene and its physiological function in reproductive tissues. In: Martini L., Grong W.F. (Eds.), Frontiers in Neuroendocrinology, Gulyas B.J. Raven Press, Ltd., New York, 1988, vol. 99.

    Google Scholar 

  71. Genazzani A.R., Petraglia F., Di Meo G., Santoro V., Facchineti F., Sgre A. Prostaglandin-induced mid-pregnancy abortion increases plasma and amniotic fluid levels of β-lipotropin and β-endorphin. Gynecol. Obstet. Invest. 24: 23, 1987.

    Article  PubMed  CAS  Google Scholar 

  72. Lemaire S., Vallete A., Chounard L., Dupuis N., Day R., Porthe G., Gros J. Purification and identification of multiple forms of dynorphin in human placenta. Neuropeptides 3: 181, 1983.

    Article  PubMed  CAS  Google Scholar 

  73. Ahmed M.S., Randall L.W., Sibai B., Dass C., Fridland G., Desiderio D.M., Tolun E. Identification of dynorphin (1–8) in human placenta by mass spectrometry. Life Sci. 40: 2067, 1987.

    Article  PubMed  CAS  Google Scholar 

  74. Porthe G., Vallete A., Cros J. Kappa opiate binding sites in human placenta. Biochem. Biophys. Res. Com. 101: 1, 1981.

    Article  PubMed  CAS  Google Scholar 

  75. Valette A., Tafani M., Porthe G., Pontonnier G., Cros J. Placental Kappa binding sites: interaction with dynorphin and its possible implication in hCG secretion. Life Sci. 33: 523, 1983.

    Article  PubMed  CAS  Google Scholar 

  76. Ahmed M.S. Characterization of solubilized opiate receptors from human placenta. Membr. Biochem. 5: 35, 1983.

    Article  PubMed  CAS  Google Scholar 

  77. Belisle S., Petit A., Gallo-Payet N., Bellabarda D., Lehoux J.G., Lemaire S. Functional opioid receptor sites in human placentas. J. Clin. Endocrinol. Metab. 66: 283, 1988.

    Article  PubMed  CAS  Google Scholar 

  78. Makrigiannakis A., Zoumakis E., Margioris A.N., Theodoropoulos P., Stournaras C., Gravanis A. The corticotropin-releasing hormone in normal and tumoral epithelial cells of human endometrium. J. Clin. Endocrinol. Metab. 80: 185, 1995.

    PubMed  CAS  Google Scholar 

  79. Mastorakos G., Scopa C.D., Kao L.C, Vryonidou A., Friedman T.C., Kattis D., Phenekos C, Rabin D., Chrousos G.P. Presence of immunoreactive corticotropin-releasing hormone in human endometrium. J. Clin. Endocrinol. Metab. 81: 1046, 1996.

    PubMed  CAS  Google Scholar 

  80. Makrigiannakis A., Margioris A.N., LeGoascogne C, Zoumakis E., Nikas G., Stournaras C, Psychoyos A., Gravanis A. Corticotropin-releasing hormone (CRH) is expressed at the implantation sites of early pregnant rat uterus. Life Sci. 57: 1869, 1995.

    Article  PubMed  CAS  Google Scholar 

  81. Zoumakis E., Makrigiannakis A., Margioris A.N., Stournaras C, Gravanis A. Endometrial corticotropin releasing hormone (CRH): its potential autocrine — paracrine actions. Ann. N. Y. Acad. Sci. 1997 In press.

  82. Zoumakis E., Makrigiannakis A., Margioris A.N., Stournaras C, Gravanis A. Corticotropin-releasing hormone (CRH) in normal and pregnant uterus: physiological implications. Frontiers in Bioscience 1: 1, 1996.

    Google Scholar 

  83. Petraglia F., Tabanelli S., Galassi C., Garuti G.C., Mancini A., Genazzani A., Gurpide E. Human decidua and in vitro decidualized endometrial stromal cells at term contain immunoreactive CRF and CRF mRNA. J. Clin. Endocrinol. Metab. 74: 1427, 1992.

    PubMed  CAS  Google Scholar 

  84. Makrigiannakis A., Zoumakis E., Margioris A.N., Stournaras C, Chrousos G.P., Gravanis A. Regulation of the promoter of the human corticotropin-releasing hormone gene in transfected human endometrial cells. Neuroendocrinology 64: 85, 1996.

    Article  PubMed  CAS  Google Scholar 

  85. Makrigiannakis A., Psychoyos A., Zoumakis E., Margioris A.N., Stournaras C, Gravanis A. Endometrial corticotropin-releasing hormone (CRH): expression, regulation and potential physiological implications. Ann. N. Y. Acad. Sci. 1997. In press.

  86. Makrigiannakis A., Margioris A.N., Stournaras C., Gravanis A. Opioid peptides in the female reproductive system. Physiological implications. Biomed. Rev. 4: 71, 1995.

    Article  CAS  Google Scholar 

  87. Makrigiannakis A., Margioris A., Markogiannakis E., Stournaras C, Gravanis A. Steroid hormones regulate the release of immunoreactive β-endorphin from Ishikawa human endometrial cell line. J. Clin. Endocrinol. Metab. 75: 584, 1992.

    PubMed  CAS  Google Scholar 

  88. Gravanis A., Makrigiannakis A., Stournaras C, Margioris A. Interactions between steroid hormones and endometrial opioid peptides. Ann. N.Y. Acad. Sci. 734: 245, 1994.

    Article  PubMed  CAS  Google Scholar 

  89. Hatzoglou A., Gravanis A., Margioris AN., Zoumakis E., Castanas E. Identification and characterization of opioid-binding sites present in the Ishikawa human endometrial adenocarcinoma cell line. J. Clin. Endocrinol. Metab. 80: 418, 1995.

    PubMed  CAS  Google Scholar 

  90. Karalis K., Sane H., Redwine J., Listwark S., Wilder R., Chrousos G. Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 254; 421, 1991.

    Article  PubMed  CAS  Google Scholar 

  91. Markiewitz L., Gravanis A., Schatz F., Holinka C, Gurpide E. Prostaglandin production by human endometrial adenocarcinoma. In: Baulieu E.E., Jacobeli S, McGuire W.L. (Eds.), Endocrinology and Malignancy Parthenon, New Jersey, 1986, p. 420.

  92. Simon C, Frances A., Piquette G., Danasouri I., Zurawski G., Dang W., Polan M. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 134: 521, 1994.

    PubMed  CAS  Google Scholar 

  93. Sheth K.V., Roca G.L., Al-Sedairy S., Parhar R., Hamilton G., Al-Abdul Jabbar F. Prediction of successful embryo implantation by measuring interleukin-1-alpha and immunosuppressive factor(s) in preimplantation. Fertil. Steril. 55: 952, 1991.

    PubMed  CAS  Google Scholar 

  94. Ferrari A., Petraglia F., Gurpide E. Corticotropin releasing factor decidualizes human endometrial stromal cells in vitro. Interaction with progestin. J. Steroid. Biochem. Mol. Biol. 54: 251, 1995.

    Article  PubMed  CAS  Google Scholar 

  95. Grunt M., Glaser J., Schmidhuber H., Pauschinger P., Born J. Effects of corticotropin-releasing factor on isolated rat heart activity. Am. J. Physiol. 264: H1124, 1993.

    PubMed  CAS  Google Scholar 

  96. Grammatopoulos D., Thompson S., Hillhouse E.W. The human myometrium expresses multiple isoforms of the corticotropin-releasing hormone receptor. J. Clin. Endocrinol. Metab. 80: 2388, 1995.

    PubMed  CAS  Google Scholar 

  97. Grammatopoulos D., Stirrat G.M., Williams S.A., Hillhouse E.W. The biological activity of the corticotropin-releasing hormone receptor-adenylate cyclase complex in human myometrium is reduced at the end of pregnancy. J. Clin. Endocrinol. Metab. 81: 745, 1996.

    PubMed  CAS  Google Scholar 

  98. Grammatopoulos D., Milton N.G., Hillhouse E.W. The human myometrial CRH receptor: G proteins and second messengers. Mol. Cell. Endocrinol. 99: 245, 1994.

    Article  PubMed  CAS  Google Scholar 

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This work was supported by grants to AG from the General Secretariat of Research and Technology (PENED94) and Medicon Hellas.

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Zoumakis, E., Margioris, A.N., Makrigiannakis, A. et al. Human endometrium as a neuroendocrine tissue: Expression, regulation and biological roles of endometrial corticotropin-releasing hormone (CRH) and opioid peptides. J Endocrinol Invest 20, 158–167 (1997). https://doi.org/10.1007/BF03346896

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