Advertisement

Ovarian Follicular Growth, Ovulation and Atresia

Endocrine, Paracrine and Autocrine Regulation
  • Kelle H. Moley
  • James R. Schreiber
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 377)

Abstract

The human ovary at birth contains approximately two million primordial follicles (1). A primordial follicle consists of an oocyte arrested in prophase of meiosis I, a single layer of granulosa cells and a basement membrane, the basal lamina. Throughout life, from childhood to menopause, this pool is progressively diminished, as new cohorts of follicles daily are recruited from this large group to undergo follicular development (2). Follicular growth begins when the oocyte, which is still arrested in meiosis I, increases in size (3). The surrounding granulosa cells simultaneously undergo mitotic division. By the end of this preantral stage, four to five layers of granulosa cells surround the oocyte. Also during this stage, these follicles have developed another layer of a different cell type external to the basal lamina called the theca cell layer (3). A vascular wreath is formed within this thecal layer directly adjacent to the granulosa cell shell. The granulosa and theca cells undergo differentiation during this stage as they acquire FSH and LH receptors, respectively (4). Formation of the antrum, or fluid-filled cavity, at one pole of the follicle, signals transition to the antral follicle stage. The theca interna cells undergo final cytodifferentiation into active steroidogenic cells. The mean diameter of the follicle increases significantly during this time due to a combination of an accumulation of follicular fluid in the antrum as well as an increase in the granulosa cell number. By approximately day 5 to 7 of the follicular phase, a dominant follicle is easily recognized morphologically (5). This follicle, selected for ovulation, is the largest, contains the greatest number of granulosa cells, and has a thecal layer which is highly vascularized.

Keywords

Granulosa Cell Corpus Luteum Primordial Follicle Theca Cell Follicular Growth 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Baker TG. Oogenesis and ovarian development. In: Balin H, Glasser S, eds. Reproductive Biology. Excerpta Medica, Amsterdam, 1972;398–401.Google Scholar
  2. 2.
    Block E. Quantitative morphological investigations of the follicular system in women. Acta Anat 1952; 14: 108–123.PubMedGoogle Scholar
  3. 3.
    Koering MJ. Preantral follicle development during the menstrual cycle in the macaca mulatta ovary. Am J Anat 1983; 166: 429–443.PubMedGoogle Scholar
  4. 4.
    Richards JS, Midgley AR. Protein Hormone Action: A key to understanding ovarian follicular and luteal cell development. Biol Reprod 1976; 14: 82–94.PubMedGoogle Scholar
  5. 5.
    Koering MJ. Cyclic changes in ovarian morphology during the menstrual cycle in macaca mulatta. Am J Anat 1969; 126: 73–101.PubMedGoogle Scholar
  6. 6.
    Thibault C, Levasseur MC. Ovulation. Human Reprod 1988; 3: 513–523.Google Scholar
  7. 7.
    Pierce J, Parsons T. Glycoprotein hormones: structure and function. Ann Rev Biochem 1981; 50: 465–495.PubMedGoogle Scholar
  8. 8.
    Hsueh A, Bicsak T, Jia X-C, Dahl K, Fauser B, Galway AB, Czekala N, Pavlou S, Papkoff H, Keen J, Boime I. Granulosa cells as hormone targets: the role of biologically active follicle-stimulating hormone in reproduction. Rec Prog Horm Res 1989; 45: 209–278.PubMedGoogle Scholar
  9. 9.
    Kourides I, Landon M, Hoffman B, Weintraub B. Excess free alpha relative to beta subunits of the glycoprotein hormones in normal and abnormal human pituitary glands. Clin Endocrinol (Oxf) 1980; 12: 407–416.Google Scholar
  10. 10.
    Naylor S, Chin W, Goodman H, Lalley P, Grzeschik K-H, Sakaguchi A. Chromosome assignment of genes encoding the a and β subunits of glycoprotein hormones in man and mouse. Somat Cell Genet 1983; 9: 757–770.PubMedGoogle Scholar
  11. 11.
    Uilenbroek J, Richards J. Ovarian follicular development during the rat estrous cycle: gonadotropin receptors and follicular responsiveness. Biol Reprod 1979; 20: 1159–1165.PubMedGoogle Scholar
  12. 12.
    McFarland K, Sprengel R, Phillips H, Köhler M, Rosemblit N, Nikolics K, Segaloff D, Seeburg P. Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science 1989; 245: 494–499.PubMedGoogle Scholar
  13. 13.
    Segaloff D, Sprengel R, Nikolics K, Ascoli M. Structure of the lutropin/choriogonadotropin receptor. Rec Prog Horm Res 1990; 46: 261–303.PubMedGoogle Scholar
  14. 14.
    Meyer T, Habener J. Cyclic adenosine 3′,5′-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins. Endocr Rev 1993; 14: 269–290.PubMedGoogle Scholar
  15. 15.
    Shaw H, Hillier S, Hodges J. Developmental changes in luteinizing hormone/human chorionic gonadotropin steroidogenic responsiveness in marmoset granulosa cells: effects of follicle-stimulating hormone and androgens. Endocrinology 1989; 124; 1669–1677.PubMedGoogle Scholar
  16. 16.
    Yong E, Baird D, Hillier S. Mediation of gonadotropin-stimulated growth and differentiation of human granulosa cells by adenosine-3′,5′-monophosphate: one molecule, two messages. Clin Endocrinol 1992; 37: 51–58.Google Scholar
  17. 17.
    Magoffin D. Regulation and differentiated functions in ovarian theca cells. In: Speroff L and Schreiber J, eds., Seminars in Reproductive Endocrinology, Thieme Medical Publishers, New York, NY 1991; 9: 321–331.Google Scholar
  18. 18.
    Erickson G, Magoffin D, Dyer C, Hofeditz C. The ovarian androgen producing cells: a review of structure/function relationships. Endocr Rev 1985; 6: 371–399.PubMedGoogle Scholar
  19. 19.
    Hutchison J, Zeleznik A. The rhesus monkey corpus luteum is dependent on pituitary gonadotropin secretion throughout the luteal phase of the menstrual cycle. Endocrinology 1984; 115: 1780–1786.PubMedGoogle Scholar
  20. 20.
    Niswender G, Juengel J, McGuire W, Belfiore C, Wiltbank M. Luteal function: the estrous cycle and early pregnancy. Biol Reprod 1994; 50: 239–247.PubMedGoogle Scholar
  21. 21.
    McNatty K, Moore Smith D, Osathanondh R, Ryan K. The human antral follicle: functional correlates of growth and atresia. Ann Biol Anim Biochim Biophys 1979; 19: 1547–1558.Google Scholar
  22. 22.
    Hirshfield A. Development of follicles in the mammalian ovary. International Rev Cytol 1991; 124: 43–101.Google Scholar
  23. 23.
    Hodgen G. The dominant ovarian follicle. Fertil Steril 1982; 38: 281–300.PubMedGoogle Scholar
  24. 24.
    Mais V, Kazer R, Cetel N, Rivier J, Vale W, Yen S. The dependency of folliculogenesis and corpus luteum function on pulsatile gonadotropin secretion in cycling women using a gonadotropin-releasing hormone antagonist as a probe. J Clin Endocrinol Metab 1986; 62: 1250–1255.PubMedGoogle Scholar
  25. 25.
    Hurwitz A, Adashi E. Ovarian follicular atresia as an apoptotic process: a paradigm for programmed cell death in endocrine tissues. Molec Cellular Endocrinol 1992; 84:C19–23.Google Scholar
  26. 26.
    Erickson GF, Nakatani A, Liu X-J, Shimasaki S, Ling N. Role of insulin-like growth factors (IGF) and the IGF binding proteins in folliculogenesis. In: Findley J, ed. Cellular and Molecular Mechanisms in Female Reproduction. Academic Press, New York, NY, 1993: pp. 101–127.Google Scholar
  27. 27.
    Tsafriti A, Chun S, Reich R. Follicular rupture and ovulation. In: Adashi EY, Leung PCK, eds. The Ovary. Raven Press, New York, NY 1973:227–244.Google Scholar
  28. 28.
    Gougeon A, Chainy G. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 1987; 81: 433–442.PubMedGoogle Scholar
  29. 29.
    Erickson G. An analysis of follicle development and ovum maturation. In: Speroff L and Archer DF, eds., Seminars in Reproductive Endocrinology, Thieme, Inc, New York, NY 1986; 4: 233–254.Google Scholar
  30. 30.
    Tureck R, Strauss J. Progesterone synthesis by luteinized human granulosa cells in culture: the role of de novo sterol synthesis and lipoprotein-carried sterol. J Clin Endocrinol Metab 1982; 54: 367–373.PubMedGoogle Scholar
  31. 31.
    Carr B, McDonald P, Simpson E. The role of lipoproteins in the regulation of progesterone secretion by the human corpus luteum. Fertil Steril 1982; 38: 303–311.PubMedGoogle Scholar
  32. 32.
    Adashi EY. The intraovarian insulin-like growth factor system. In: Adashi EY, Leung PCK, eds. The Ovary. Raven Press, Ltd., New York, NY, 1993: 319–335).Google Scholar
  33. 33.
    Blundell TL, Humbel RE. Hormone families: Pancreatic hormones and homologous growth factors. Nature 1980; 287: 781–787.PubMedGoogle Scholar
  34. 34.
    Geisthovel F, Moretti-Rojas I, Asch RH, Rojas FJ. Expression of insulin-like growth factor-II (IGF-II) messenger ribonucleic acid (mRNA), but not IGF-I mRNA, in human preovulatory granulosa cells. Human Reprod 1989; 4: 899–902.Google Scholar
  35. 35.
    Adashi EY, Resnick CE, Hernandez ER, Svoboda ME, Van Wyk JJ. Characterization and regulation of a specific cell membrane receptor for somatomedin-C/insulin-like growth factor I in cultured rat granulosa cells. Endocrinology 1988; 122: 194–201.PubMedGoogle Scholar
  36. 36.
    Poretsky L, Grigorescu F, Seibel M, Moses AC, Flier JS. Distribution and characterization of insulin and insulin-like growth factor I receptors in normal human ovary. J Clin Endocrinol Metab 1985; 61: 728–734.PubMedGoogle Scholar
  37. 37.
    Adashi EY, Resnick CE, Svoboda ME, Van Wyk JJ. Somatomedin-C as an amplifier of follicle-stimulating hormone action: Enhanced accumulation of adenosine 3′,5′-monophosphate. Endocrinology 1986; 118: 149–155.PubMedGoogle Scholar
  38. 38.
    Adashi EY, Resnick CE, Hernandez ER, May JV, Knecht M, Svoboda ME, Van Wyk JJ. Insulin-like growth factor-I as an amplifier of follicle-stimulating hormone action: Studies on mechanism(s) and site(s) of action in cultured rat granulosa cells. Endocrinology 1988; 122: 1583–1591.PubMedGoogle Scholar
  39. 39.
    Baranao JLS, Hammond JM. Comparative effects of insulin and insulin-like growth factors on DNA synthesis and differentiation of porcine granulosa cells. Biochem Biophys Res Comm 1984; 124: 484–490.PubMedGoogle Scholar
  40. 40.
    Adashi EY, Resnick CE, Svoboda ME, Van Wyk JJ. Somatomedin-C synergizes with follicle-stimulating hormone in the acquisition of progestin biosynthetic capacity by cultured rat granulosa cells. Endocrinology 1985; 116: 2135–2142.PubMedGoogle Scholar
  41. 41.
    Adashi EY, Resnick CE, Brodie AMH, Svoboda ME, Van Wyk JJ. Somatomedin-C-mediated potentiation of follicle-stimulating hormone-induced aromatase activity of cultured rat granulosa cells. Endocrinology 1985; 117: 2313–2320.PubMedGoogle Scholar
  42. 42.
    Veldhuis JD, Rodgers RJ, Dee A, Simpson ER. The insulin-like growth factor, somatomedin C, induces the synthesis of cholesterol side-chain cleavage cytochrome P-450 and adrenodoxin in ovarian cells. J Biol Chem 1986; 261: 2499–2502.PubMedGoogle Scholar
  43. 43.
    Veldhuis JD, Nestler JE, Strauss JE. The insulin-like growth factor, somatomedin-C, modulates low density lipoprotein metabolism by swine granulosa cells. Endocrinology 1987; 121: 340–346.PubMedGoogle Scholar
  44. 44.
    Adashi EY, Resnick CE, Svoboda ME, Van Wyk JJ. Somatomedin-C enhances induction of luteinizing hormone receptors by follicle-stimulating hormone in cultured rat granulosa cells. Endocrinology 1985; 116: 2369–2375.PubMedGoogle Scholar
  45. 45.
    Zhiwen Z, Carson RS, Herington AC, Lee VWK, Burger HG. Follicle-stimulating hormone and somatomedin-C stimulate inhibin production by rat granulosa cells in vitro. Endocrinology 1987; 120: 1633–1638.Google Scholar
  46. 46.
    Adashi EY, Resnick CE, Svoboda ME, Van Wyk JJ, Hascall VC, Yanagishita M. Independent and synergistic actions of somatomedin-C in the stimulation of proteoglycan biosynthesis by cultured rat granulosa cells. Endocrinology 1986; 118: 567–458.Google Scholar
  47. 47.
    Magoffin DA, Kurtz KM, Erickson GF. Insulin-like growth factor-I selectively stimulates cholesterol side-chain cleavage expression in ovarian theca-interstitial cells. Mol Endo 1990; 4: 489–496.Google Scholar
  48. 48.
    Obasiolu CCW, Khan-Dawood FS, Dawood MY. Insulin-like growth factor I receptors in human corpora lutea. Fertil Steril 1992; 57: 1235–40.PubMedGoogle Scholar
  49. 49.
    Adashi EY, Resnick CE, Svoboda ME, Van Wyk JJ. Follicle-stimulating hormone enhances somatomedin C binding to cultured rat granulosa cells. J Biol Chem 1986; 261: 3923–3926.PubMedGoogle Scholar
  50. 50.
    Giudice LC, Milki AA, Milkowski DA, Danasouri IE. Human granulosa contain messenger ribonucleic acids encoding insulin-like growth factor-binding proteins (IGFBPs) and secrete IGFBPs in culture. Fertil Steril 1991; 56: 475–480.PubMedGoogle Scholar
  51. 51.
    Samaras SE, Guthrie HD, Barber JA, Hammond HM. Expression of the mRNAs for the insulin-like growth factors and their binding proteins during development of porcine ovarian follicles. Endocrinol 1993; 133: 2395–2398.Google Scholar
  52. 52.
    Adashi EY, Resnick CE, Hurwitz A, Ricciarelli E, Hernandez ER, Rosenfeld RG. Ovarian granulosa cell-derived insulin-like growth factor binding proteins: Modulatory role of follicle-stimulating hormone. Endocrinology 1991; 128: 754–760.PubMedGoogle Scholar
  53. 53.
    Erickson GF, Nakatani A, Ling N, Shimasaki S. Localization of insulin-like growth factor-binding protein-5 messenger ribonucleic acid in rat ovaries during the estrous cycle. Endocrinology 1992; 130: 1867–1878.PubMedGoogle Scholar
  54. 54.
    Bicsak TA, Shimonaka M, Malkowski M, Ling N. Insulin-like growth factor-binding protein (IGF-BP) inhibition of granulosa cell function: Effect on cyclic adenosine 3′,5′-monophosphate, deoxyribonucleic acid synthesis, and comparison with the effect of an IGF-I antibody. Endocrinology 1990; 126: 2184–2189.PubMedGoogle Scholar
  55. 55.
    Gospodarowicz D, Bialecki H. Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology 1979; 104: 757–764.PubMedGoogle Scholar
  56. 56.
    Tilly JL, LaPolt PS, Hsueh AJW. Hormonal regulation of follicle-stimulating-hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 1992; 130: 1296–1302.PubMedGoogle Scholar
  57. 57.
    Lobb DK, Kobrin MS, Kudlow JE, Dorrington JH. Transforming growth factor-alpha in the adult bovine ovary: Identification in growing ovarian follicles. Biol Reprod 1989; 40: 1087–1093.PubMedGoogle Scholar
  58. 58.
    Chabot J-G, St-Arnaud R, Walker P, Pelletier G. Distribution of epidermal growth factor receptors in the rat ovary. Molec Cellular Endocrinol 1986; 44: 99–108.Google Scholar
  59. 59.
    Downs SM. Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol Reprod 1989; 41: 371–379.PubMedGoogle Scholar
  60. 60.
    Adashi EY, Resnick CE. Antagonistic interactions of transforming growth factors in the regulation of granulosa cell differentiation. Endocrinology 1986; 119: 1879–1881.PubMedGoogle Scholar
  61. 61.
    Adashi EY, Resnick CE, Hernandez ER, May JV, Purchio AF, Twardzik DR. Ovarian transforming growth factor-β (TGFβ): Cellular site(s), and mechanism(s) of action. Molec Cellular Endocrinol 1989; 61: 247–256.Google Scholar
  62. 62.
    Knecht M, Feng P, Catt K. Bifunctional role of transforming growth factor-β during granulosa cell development. Endocrinology 1987; 120: 1243–1249.PubMedGoogle Scholar
  63. 63.
    Feng P, Catt KJ, Knecht M. Transforming growth factor-β stimulates meiotic maturation of the rat oocyte. Endocrinology 1988; 122: 181–186.PubMedGoogle Scholar
  64. 64.
    Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant inhibin on androgen synthesis in cultured human thecal cells. Molec Cellular Endocrinol 1991; 75:R1–R6.Google Scholar
  65. 65.
    Xiao S, Robertson DM, Findlay JK. Effects of activin and follicle-stimulating hormone (FSH)-suppressing protein/follistatin on FSH receptors and differentiation of cultured rat granulosa cells. Endocrinology 1992; 131: 1009–1016.PubMedGoogle Scholar
  66. 66.
    Shukovski L, Findlay JK. Activin-A inhibits oxytocin and progesterone production by preovulatory bovine granulosa cells in vitro. Endocrinology 1990; 126: 2222–2224.PubMedGoogle Scholar
  67. 67.
    Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant activin on androgen synthesis in cultured human thecal cells. J Clin Endocrinol Metab 1991; 72: 1206–1211.PubMedGoogle Scholar
  68. 68.
    Itoh M, Igarashi M, Yamada K, Hasegawa Y, Seki M, Eto Y, Shibai H. Activin A stimulates meiotic maturation of the rat oocyte in vitro. Biochem Biophys Res Comm 1990; 166: 1479–1484.PubMedGoogle Scholar
  69. 69.
    Xiao S, Findlay JK. Interactions between activin and follicle-stimulating hormone-suppressing protein and their mechanisms of action on cultured rat granulosa cells. Molec Cellular Endocrinol 1991; 79: 99–107.Google Scholar
  70. 70.
    Kokia E, Adashi EY. Potential role for cytokines in ovarian physiology: The case for interleukin-1. In: Adashi EY, Leung PCK, eds. The Ovary. Raven Press, Ltd., New York, NY, 1993: 383–394).Google Scholar
  71. 71.
    Kokia E, Hurwitz A, Ricciarelli E, Tedeschi C, Resnick CE, Mitchell MD, Adashi EY. Interleukin-1 stimulates ovarian prostaglandin biosynthesis: Evidence for heterologous contact-independent cell-cell interaction. Endocrinology 1992; 130: 3095–3097.PubMedGoogle Scholar
  72. 72.
    Hurwitz A, Loukides J, Ricciarelli E, Botero L, Katz E, McAllister JM, Garcia JE, Rohan R, Adashi EY, Hernandez ER. Human intraovarian interleukin-1 (IL-1) system: Highly compartmentalized and hormonally dependent regulation of the genes encoding IL-1, its receptor, and its receptor antagonist. J Clin Invest 1992; 89: 1746–1754.PubMedGoogle Scholar
  73. 73.
    Simon C, Frances A, Piquette G, Polan ML. Immunohistochemical localization of the interleukin-1 system in the mouse ovary during follicular growth, ovulation, and luteinization. Biol Reprod 1994; 50: 449–457.PubMedGoogle Scholar
  74. 74.
    Ellman C, Corbett JA, Misko TP, McDaniel M, Beckerman KP. Nitric oxide mediates interleukin-1-induced cellular cytotoxicity in the rat ovary: A potential role for nitric oxide in the ovulatory process. J Clin Invest 1993; 92: 3053–3056.PubMedGoogle Scholar
  75. 75.
    Ben-Shlomo I, Kokia E, Jackson MJ, Adashi EY, Payne DW. Interleukin-1β stimulates nitrite production in the rat ovary: Evidence for heterologous cell-cell interaction and for insulin-mediated regulation of the inducible isoform of nitric oxide synthase. Biol Reprod 1994; 51: 310–318.PubMedGoogle Scholar
  76. 76.
    Gospodarowicz G, Plouët J, Fujii DK. Ovarian germinal epithelial cells respond to basic fibroblast growth factor and express its gene: Implications for early folliculogenesis. Endocrinology 1989; 125: 1266–1276.PubMedGoogle Scholar
  77. 77.
    Ueno S, Manganaro TF, Donahoe PK. Human recombinant mullerian inhibiting substance inhibition of rat oocyte meiosis is reversed by epidermal growth factor in vitro. Endocrinology 1988; 123: 1652–1659.PubMedGoogle Scholar
  78. 78.
    Fox MD, Hyde JF, Muse KN, Keeble SC, Howard G, London SN, Curry TE. Galanin: A novel intraovarian regulatory peptide. Endocrinol 1994; 135: 636–641.Google Scholar
  79. 79.
    Terranova PF, Sancho-Tello M, Hunter VF. Tumor necrosis factor-α and ovarian function. In: Adashi EY, Leung PCK, eds. The ovary. Raven Press, Ltd., New York, NY 1993:395–410.Google Scholar
  80. 80.
    Koos RD, Olson CE, Ma C. Vascular endothelial growth factor expression in rat granulosa cells: Effect of gonadotropin stimulation of follicular development. [Abstract] Biol Reprod 1992; 46 (Suppl):505.Google Scholar
  81. 81.
    Facchinetti F, Ruspa M, Turci A, Petraglia F, Segre A, Forabosco A, Genazzani AR. Met-enkephalin enhances follicle-stimulating hormone-dependent progesterone production from cultured granulosa cells. J Clin Endocrinol Metab 1986; 63: 1222–1224.PubMedGoogle Scholar
  82. 82.
    Grasso G, Muscettola M. Possible role of interferon-gamma in ovarian function. Ann NY Acad Sci 1992; 650: 191–196.PubMedGoogle Scholar
  83. 83.
    Usuki S, Saitoh T, Masahiro S, Tanaka J, Kawakura Y, Usuki Y, Shinjo M, Kim S-J. Endothelin-renin-angiotensin-atrial natriuretic peptide system in ovaries: An intraovarian ERAANP system. J Cardiovasc Pharmacol 1993; 22(Suppl):S207–S210.PubMedGoogle Scholar
  84. 84.
    Barad DH, Ryan KJ, Elkind-Hirsch K, Makris A. Immunoreactive substance P in the human ovary. Am J Obstet Gynecol 1988; 159: 242–246.).PubMedGoogle Scholar
  85. 85.
    Hillier SG, Saunders PTK, White R, Parker MG. Oestrogen receptor mRNA and a related RNA transcript in mouse ovaries. J Molec Endocrinol 1989; 2: 39–45.Google Scholar
  86. 86.
    Richards JS. Maturation of Ovarian Follicles: Actions and Interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiological Rev 1980; 60: 51–83.Google Scholar
  87. 87.
    Hsueh AJW, Adashi EY, Jones PBC, Welsh TH. Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocrine Rev 1984; 5: 76–99.Google Scholar
  88. 88.
    Hild-Petito S, Stouffer RL, Brenner RM. Immunocytochemical localization of estradiol and progesterone receptors in the monkey ovary throughout the menstrual cycle. Endocrinology 1988; 123: 2896–2905.PubMedGoogle Scholar
  89. 89.
    Goldenberg RL, Vaitukaitis JL, Ross GT. Estrogen and follicle stimulating hormone interactions on follicle growth in rats. Endocrinology 1972; 90: 1492–1498.PubMedGoogle Scholar
  90. 90.
    Koering MJ, Danforth DR, Hodgen GD. Early folliculogenesis in primate ovaries: Testing the role of estrogen. Biol Reprod 1991; 45: 890–897.PubMedGoogle Scholar
  91. 91.
    Zelinski-Wooten MB, Hess DL, Baughman WL, Molskness TA, Wolf DP, Stouffer RL. Administration of an aromatase inhibitor during the late follicular phase of gonadotropin-treated cycles in rhesus monkeys: Effects on follicle development, oocyte maturation, and subsequent luteal function. J Clin Endocrinol Metab 1993; 76: 988–995.PubMedGoogle Scholar
  92. 92.
    Zelinski-Wooten MB, Hess DL, Wolf DP, Stouffer RL. Steroid reduction during ovarian stimulation impairs oocyte fertilization, but not folliculogenesis, in rhesus monkeys. Fertil Steril 1994; 61: 1147–1155.PubMedGoogle Scholar
  93. 93.
    Wu T-CJ, Wang L, Wan Y-JY. Detection of estrogen receptor messenger ribonucleic acid in human oocytes and cumulus-oocyte complexes using reverse transcriptase-polymerase chain reaction. Fertil Steril 1993; 59: 54–59.PubMedGoogle Scholar
  94. 94.
    Billiar RB, Loukides JA, Miller MM. Evidence for the presence of estrogen receptor in the ovary of the baboon (papio anubis). J Clin Endocrinol Metab 1992; 75: 1159–1165.PubMedGoogle Scholar
  95. 95.
    Hillier SG, Ross GT. Effects of exogenous testosterone on ovarian weight, follicular morphology and intraovarian progesterone concentration in estrogen-primed hypophysectomized immature female rats. Biol Reprod 1979; 20: 261–268.PubMedGoogle Scholar
  96. 96.
    Erickson GF, Yen SSC. New data on follicle cells in polycystic ovaries: A proposed mechanism for the genesis of cystic follicles. Seminars in Reprod Endocrinol 1984; 2: 231–243.Google Scholar
  97. 97.
    Peluso JJ, Brown I, Steger RW. Effects of cyproterone acetate, a potent antiandrogen, on the preovulatory follicle. Biol Reprod 1979; 21: 929–936.PubMedGoogle Scholar
  98. 98.
    Hild-Petito S, West NB, Brenner RM, Stouffer RL. Localization of androgen receptor in the follicle and corpus luteum of the primate ovary during the menstrual cycle. Biol Reprod 1991; 44: 561–568.PubMedGoogle Scholar
  99. 99.
    Schreiber JR, Nakamura K, Truscello AM, Erickson GF. Progestins inhibit FSH-induced functional LH receptors in cultured rat granulosa cells. Molec Cellular Endocrinol 1982; 25: 113–124.Google Scholar
  100. 100.
    Rothchild I. The regulation of the mammalian corpus luteum. Rec Prog Horm Res 1981; 37: 183–195.PubMedGoogle Scholar
  101. 101.
    Slayden OD, Zelinski-Wooten MB, Stouffer RL, Brenner RM. Radioligand binding assay of progesterone receptors in the primate corpus luteum after in vivo treatment with the 3β-hydroxysteroid dehydrogenase inhibitor, trilostane. J Clin Endocrinol Metab 1994; 79: 620–626.PubMedGoogle Scholar
  102. 102.
    DiMattina M, Albertson B, Seyler DE, Loriaux DL, Falk RJ. Effect of the antiprogestin RU486 on progesterone production by cultured human granulosa cells: Inhibition of the ovarian 3β-hydroxysteroid dehydrogenase. Contraception 1986; 34: 199–206.PubMedGoogle Scholar
  103. 103.
    Lewin B. Genes IV. Oxford University Press, New York, NY and Cell Press, Cambridge, MA. 1990, pp. 805–821.Google Scholar
  104. 104.
    Ron D, Habener J. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes & Dev 1992; 6: 439–453.Google Scholar
  105. 105.
    Waeber G, Meyer T, LeSieur M, Hermann H, Gerard N, Habener J. Developmental stage-specific expression of cyclic adenosine 3′,5′-monophosphate response element-binding protein CREB during spermatogenesis involves alternative exon splicing. Molec Endocrinol 1991; 5: 1418–1430.Google Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Kelle H. Moley
    • 1
  • James R. Schreiber
    • 1
  1. 1.Division of Reproductive Endocrinology, Department of Obstetrics and GynecologyWashington University School of MedicineSt. LouisUSA

Personalised recommendations