Intra-Ovarian Actions of Steroids in Regulation of Follicular Steroid Biosynthesis

  • D. T. Armstrong
  • S. A. J. Daniel
  • R. E. Gore-Langton


The follicle is the principal functional unit of the mammalian ovary, the primary function of which is the production and release of a mature oocyte at the culmination of each ovarian cycle. A secondary role of the follicle is the biosynthesis and secretion of a group of steroid hormones which serve many important functions in regulation of peripheral (i. e extra-ovarian) cells and tissues.


Granulosa Cell Follicular Fluid Aromatase Activity Theca Cell Progesterone Production 
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  1. Adashi, E. Y., and Hsueh, A. J. W., 1982, Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells, J. Biol. Chem., 257:6077.PubMedGoogle Scholar
  2. Armstrong, D. T., 1979, Alterations of progesterone metabolism in immature rat ovaries by luteinizing hormone, Biol. Reprod., 21:1025.PubMedCrossRefGoogle Scholar
  3. Armstrong, D. T., and Dorrington, J. H., 1976, Androgens augment FSH-induced progesterone secretion by cultured rat granulosa cells, Endocrinology, 99:1411.PubMedCrossRefGoogle Scholar
  4. Armstrong, D. T., and Dorrington, J. H., 1977, Estrogen biosynthesis in the ovaries and testes, in: “Regulatory Mechanisms Affecting Gonadal Hormone Action; Advances in Sex Hormone Research,” J. A. Thomas, R. L. Singhal, eds., Vol. III, p. 217, University Park Press, Baltimore.Google Scholar
  5. Armstrong, D. T., Daniel, S. A. J., Salhanick, A. R., and Sheela Rani, C. S., 1980, Hormonal interactions in regulation of steroid biosynthesis by the ovarian follicle, in: “Functional Correlates of Hormone Receptors in Reproduction,” V. B. Makesh, T. G. Muldoon, B. B. Saxena, W. A. Sadler, eds., p. 245, Elsevier North Holland Inc., New York.Google Scholar
  6. Armstrong, D. T., Dorrington, J. H., and Robinson, J., 1976, Effects of indomethacin and aminoglutethimide phosphate in vivo on luteinizing-hormone-induced alterations of cyclic adenosine monophosphate, prosta-glandin F, and steroid levels in preovulatory rat ovaries, Can. J. Biochem., 54:796.PubMedCrossRefGoogle Scholar
  7. Bagnell, C. A., Mills, T. M., Costoff, A., and Mahesh, V. B., 1982, A model for the study of androgen effects of follicular atresia and ovulation, Biol. Reprod., 2.7:903.CrossRefGoogle Scholar
  8. Bahr, J. M., 1978, Simultaneous measurement of steroids in follicular fluid and ovarian venous blood in the rabbit, Biol. Reprod. 18:193.PubMedCrossRefGoogle Scholar
  9. Batta, S. K., Wentz, A. C., and Channing, C. P., 1980, Steroidogenesis by human ovarian cell types in culture: influence of mixing of cell types and effect of added testosterone, J. Clin. Endocrinol. Metab., 50:274.PubMedCrossRefGoogle Scholar
  10. Beattie, C. W., and Corbin, A., 1975, The differential effects of diestrous progesterone administration on proestrous gonadotrophin levels, Endocrinology, 97:885.PubMedCrossRefGoogle Scholar
  11. Bernard, J., 1975, Effect of follicular fluid and estradiol on the luteinization of rat granulosa cells in vitro, J. Reprod. Fertil., 45:453.Google Scholar
  12. Bieszczad, R. R., McClintock, J. S., Pepe, G. J., and Dimino, M. J., 1982, Progesterone secretion by granulosa cells from different sized follicles of human ovaries after short term incubation, J. Clin. Endocrinol. Metab., 55:181.PubMedCrossRefGoogle Scholar
  13. Bogovich, K., Richards, J. S., and Reichert, L. E. Jr., 1981, Obligatory role of LH in the initiation of preovulatory follicular growth in the pregnant rat: specific effects of human chorionic gonadotropin and follicle-stimulating hormone on LH receptors and steroidogenesis in theca, granulosa and luteal cells, Endocrinology, 109:860.PubMedCrossRefGoogle Scholar
  14. Bradbury, J. T., 1961, Direct action of estrogen on the ovary of the immature rat, Endocrinology, 68:112.CrossRefGoogle Scholar
  15. Brophy, P. J., and Gower, D. B., 1974, Studies on the inhibition by 5-pregnane-3,20-dione of the biosynthesis of 16-androstenes and dehydro-epiandrosterone in boar testis preparations, Biochim. Biophys. Acta, 360:252.PubMedCrossRefGoogle Scholar
  16. Buffler, G., and Roser, S., 1974, New data concerning the role played by progesterone in the control of follicular growth in the rat, Acta Endocrinol., 75:569.PubMedGoogle Scholar
  17. Campo, S. M., Carson, R. S., and Findlay, K. K., 1984, Distribution and characterization of specific androgen-binding sites within the ovine follicle, 15th Annual Conference of the Australian Society for Reproductive Biology, Canberra, Abstract, p. 27.Google Scholar
  18. Carson, R. S., Findlay, J. K., Clarke, I. J., and Burger, H. G., 1981, Estradiol, testosterone, and androstenedione in ovine follicular fluid during growth and atresia of ovarian follicles, Biol. Reprod., 24:105.PubMedCrossRefGoogle Scholar
  19. Corredor, A., and Flickinger, G. L., 1983, Hormonal regulation of progesterone secretion by cultured mouse granulosa cells, Biol. Reprod., 29:1142.PubMedCrossRefGoogle Scholar
  20. Daniel, S. A. J., and Armstrong, D. T., 1980, Enhancement of follicle-stimulating hormone-induced aromatase by androgens in cultured rat granulosa cells, Endocrinology, 107:1027.PubMedCrossRefGoogle Scholar
  21. Daniel, S. A. J., and Armstrong, D. T., 1983, Involvement of estrogens in the regulation of granulosa cell aromatase activity, Can. J. Physiol. Pharmacol., 61:507.PubMedCrossRefGoogle Scholar
  22. Daniel, S. A. J., and Armstrong, D. T., 1984, Site of action of androgens on follicle-stimulating hormone-induced aromatase activity in cultured rat granulosa cells, Endocrinology, 114:1975.PubMedCrossRefGoogle Scholar
  23. Dorrington, J. H., and Armstrong, D. T., 1979, Effect of FSH on gonadal functions, Rec. Prog. Horn. Res., 35:301.Google Scholar
  24. Duleba, A. J., Takahashi, H., and Moon, Y. S., 1983, Androgenic modulation of progesterone metabolism by rat granulosa cells in culture, Steroids, 42:321.PubMedCrossRefGoogle Scholar
  25. Eckstein, B., and Nimrod, A., 1977, Properties of microsomal 3-ketosteroid 5α-reductase in immature rat ovary, Biochim. Biophys. Acta, 499:1.PubMedCrossRefGoogle Scholar
  26. Engels, J. A., Friedlander, R. L., and Eik-Nes, K. B., 1968, An effect in vivo of clomiphene on the rate of conversion of androstenedione-14C to estrone-14C and estradiol-14C by the canine ovary, Metabolism, 17:189.PubMedCrossRefGoogle Scholar
  27. Evans, G., Leung, P. C. K., Brodie, A. M. H., and Armstrong, D. T., 1981, Effect of an aromatase inhibitor (4-acetoxy-4-androstene-3,17-dione) on the stimulatory action of luteinizing hormone on estradiol-17β synthesis by rat preovulatory follicles in vitro, Biol. Reprod., 25:290.PubMedCrossRefGoogle Scholar
  28. Evans, G., Lischinsky, A., Daniel, S. A. J., and Armstrong, D. T., 1984, Androgen inhibition of FSH-stimulated progesterone production by granulosa cells of prepubertal pig, Can. J. Physiol. Pharmacol., 62:840.PubMedCrossRefGoogle Scholar
  29. Fanjul, L. F., de Galarreta, R., and Hsueh, A. J. W., 1983, Progestin augmentation of gonadotrophin-stimulated progesterone production by cultured rat granulosa cells, Endocrinology, 112:405.PubMedCrossRefGoogle Scholar
  30. Fortune, J. E., and Hansel, W., 1979, The effects of 17 β-estradiol on progesterone secretion by bovine theca and granulosa cells, Endocrinology, 104:1834.PubMedCrossRefGoogle Scholar
  31. Fortune, J. E., and Vincent, S. E., 1983, Progesterone inhibits the induction of aromatase activity in rat granulosa cells in vitro, Biol. Reprod., 28:1078.PubMedCrossRefGoogle Scholar
  32. Goff, A. K., and Henderson, K. M., 1979, Changes in follicular fluid and serum concentrations of steroids in PMS-treated immature rats following LH administration, Biol. Reprod., 20:1153.PubMedCrossRefGoogle Scholar
  33. Goff, A. K., Leung, P. C. K., and Armstrong, D. T., 1979, Stimulatory action of follicle-stimulating hormone and androgens on the responsiveness of rat granulosa cells to gonadotropins in vitro, Endocrinology, 104:1124.PubMedCrossRefGoogle Scholar
  34. Goldenberg, R. L., Bidson, W. E., and Kohler, P. O., 1972, Estrogen stimulation of progesterone synthesis by porcine granulosa cells in culture, Biochem. Biophys. Res. Comm., 48:101.PubMedCrossRefGoogle Scholar
  35. Goodman, A. L., and Hodgen, G. D., 1977, Systemic versus intra-ovarian progesterone replacement after lutiectomy in rhesus monkeys: differential patterns of gonadotropins and follicle growth, J. Clin. Endocrinol. Metab., 45:837.PubMedCrossRefGoogle Scholar
  36. Gore-Langton, R. E., and Armstrong, D. T., 1987, Follicular steroidogenesis and its control, in: “The Physiology of Reproduction,” E. Knobil, J. D. Neill, eds., Raven Press, New York, in press.Google Scholar
  37. Greenwald, G. S., 1974, Gonadotropin regulation of follicular development, in: “Gonadotropins and Gonadal Function,” N. R. Moudgal, ed., p. 205, Academic Press, New York.Google Scholar
  38. Greep, R. O., Fevold, H. L., and Hisaw, F. L., 1936, Effect of two hypophy-seal gonadotrophic hormones on the reproductive system of the male rat, Anat. Rec, 65:261.CrossRefGoogle Scholar
  39. Greep, R. O., van Dyke, H. B., and Chow, B. F., 1942, Gonadotropins of the swine pituitary. I. Various biological effects of purified thylakentrin (FSH) and pure metakentrin (ICSH), Endocrinology, 30:635.CrossRefGoogle Scholar
  40. Hammond, J. M., Hershey, R. M., Walega, M. A., and Weisz, J., 1986, Cate-cholestrogen production by porcine ovarian cells, Endocrinology, 118:2292.PubMedCrossRefGoogle Scholar
  41. Haney, A. F., and Schomberg, D. W., 1978, Steroidal modulation of progesterone secretion by granulosa cells from large porcine follicles: a role for androgens and estrogens in controlling steroidogenesis, Biol. Reprod., 19:242.PubMedCrossRefGoogle Scholar
  42. Harman, S. M., Louvet, J. P., and Ross, G. T., 1975, Interaction of estrogen and gonadotrophins on follicular atresia, Endocrinology, 96:1145.PubMedCrossRefGoogle Scholar
  43. Hillier, S. G., and DeZwart, F. A., 1981, Evidence that granulosa cell induction/activation by follicle-stimulating hormone is an androgen receptor regulated process in vitro, Endocrinology, 109:1303.PubMedCrossRefGoogle Scholar
  44. Hillier, S. G., and DeZwart, F. A., 1982, Androgen/antiandrogen modulation of cyclic AMP-induced steroidogenesis during granulosa cell differentiation in tissue culture, Mol. Cell. Endocrinol., 28:347.PubMedCrossRefGoogle Scholar
  45. Hillier, S. G., and Ross, G. T., 1979, Effects of exogenous testosterone on ovarian weight, follicular morphology and intra-ovarian progesterone concentration in estrogen-primed hypophysectomized immature female rats, Biol. Reprod., 20:261.PubMedCrossRefGoogle Scholar
  46. Hillier, S. G., Knazek, R. A., and Ross, G. T., 1977, Androgenic stimulation of progesterone production by granulosa cells from preantral ovarian follicles: further in vitro studies using replicate cell cultures, Endocrinology, 100:1539.PubMedCrossRefGoogle Scholar
  47. Hillier, S. G., van den Boogaard, A. M. J., Reichert, L. E. Jr., and van Hall, E. V., 1980a, Alterations in granulosa cell aromatase activity accompanying preovulatory follicular development in the rat ovary with evidence that 5α-reduced C19 steroids inhibit the aromatase reaction in vitro, J. Endocrinol., 84:409.PubMedCrossRefGoogle Scholar
  48. Hillier, S. G., van den Boogaard, A. M. J., Reichert, L. E. Jr., and van Hall, E. V., 1980b, Intra-ovarian sex steroid hormone interactions and the regulation of follicular maturation: aromatization of androgens by human granulosa cells in vitro, J. Clin. Endocrinol. Metab., 50:640.PubMedCrossRefGoogle Scholar
  49. Hori, T., Kato, G., and Miyake, T., 1973, Acute effects of ovarian steroids upon follicular growth in the cycling rat, Endocrinol. Jpn., 20:475.PubMedCrossRefGoogle Scholar
  50. Hsueh, A. J. W., Adashi, E. Y., Jones, P. B. C., and Welsh, T. H., 1984, Hormonal regulation of the differentiation of cultured ovarian granulosa cells, Endocrine Rev., 5:76.CrossRefGoogle Scholar
  51. Hudson, K. E., and Hillier, S. G., 1985, Catechol estradiol control of FSH-stimulated granulosa cell steroidogenesis, J. Endocrinol., 106:R1.PubMedCrossRefGoogle Scholar
  52. Hunter, M. G., and Armstrong, D. T., 1986, Estrogens inhibit steroid production by dispersed porcine thecal cells, Biol. Reprod., 34 (Suppl. 1), Abstract No. 293, p. 196.Google Scholar
  53. Inaba, T., Imori, T., and Matsumoto, K., 1978, Formation of 5α-reduced C19-steroids from progesterone in vivo by 5α-reduced pathway in immature rat ovaries, J. Steroid Biochem., 9:1105.PubMedCrossRefGoogle Scholar
  54. Jacobs, B. R., and Smith, R. G., 1980, Evidence for a receptor-like protein for progesterone in bovine ovarian cytosol, Endocrinology, 106:1276.PubMedGoogle Scholar
  55. Jacobs, B. R., Suchocki, S., and Smith, R. G., 1980, Evidence for human ovarian progesterone receptor, Am. J. Obstet. Gynecol., 138:332.PubMedGoogle Scholar
  56. Jesel, L., 1970, Données nouvelles sur le contrôle eneece par le corps jaune sur la croissance folliculaire au debut du cycle oestral chez le Cobaye, C.R. Acad. Sci. [D] (Paris), 271:1693.Google Scholar
  57. Jones, P. B. C., and Hsueh, A. J. W., 1982, Pregnenolone biosynthesis by cultured granulosa cells: modulation by follicle-stimulating hormone and gonadotropin-releasing hormone, Endocrinology, 111:713.PubMedCrossRefGoogle Scholar
  58. Kalra, S. P., and Kalra, P. S., 1974, Temporal interrelationships among circulating levels of estradiol, progesterone and LH during the rat estrous cycle: effects of exogenous progesterone, Endocrinology, 95:1711.PubMedCrossRefGoogle Scholar
  59. Katz, Y., and Armstrong, D. T., 1976, Inhibition of ovarian estradiol-17 secretion by luteinizing hormone in prepubertal, pregnant mare serum-treated rats, Endocrinology, 99:1442.PubMedCrossRefGoogle Scholar
  60. Khan, M. I., and Gibori, G., 1984, Catechol estrogens and their role in luteal steroidogenesis, Biol. Reprod., 30 (Suppl. 1), Abstract No. 194, p. 127.Google Scholar
  61. Knecht, M., Darbon, J. M., Ranta, T., Baukal, A. J., and Catt, K. J., 1984, Estrogens enhance the adenosine 3′,5′-monophosphate-mediated induction of follicle-stimulating hormone and luteinizing hormone receptors in rat granulosa cells, Endocrinology, 115:41.PubMedCrossRefGoogle Scholar
  62. Kumari, G. L., Datta, J. K., Das, R. P., and Roy, S., 1978, Evidence for a role of androgens in the growth and maturation ovarian follicles in rats, Horn. Res., 9:112.CrossRefGoogle Scholar
  63. Leung, P. C. K., and Armstrong, D. T., 1979a, Estrogen treatment of immature rats inhibits ovarian androgen production in vitro, Endocrinology, 104:1411.PubMedCrossRefGoogle Scholar
  64. Leung, P. C. K., and Armstrong, D. T., 1979b, A mechanism for the intra-ovarian inhibitory action of estrogen on androgen production, Biol. Reprod., 21:1035.PubMedCrossRefGoogle Scholar
  65. Leung, P. C. K., and Armstrong, D. T., 1980, Further evidence in support of a short-loop feedback action of estrogen on ovarian androgen production, Life Sci., 27:415.PubMedCrossRefGoogle Scholar
  66. Leung, P. C. K., Goff, A. K., and Armstrong, D. T., 1979, Stimulatory action of androgen administration in vivo on ovarian responsiveness to gonado-tropins, Endocrinology, 104:1119.PubMedCrossRefGoogle Scholar
  67. Leung, P. C. K., Goff, A. K., Kennedy, T. G., and Armstrong, D. T., 1978, An intra-ovarian inhibitory action of estrogen and androgen production in vivo, Biol. Reprod., 19:641.PubMedCrossRefGoogle Scholar
  68. Lischinsky, A., Evans, G., and Armstrong, D. T., 1983, Site of androgen inhibition of FSH-stimulated progesterone production in porcine granulosa cells, Endocrinology, 113:1999.PubMedCrossRefGoogle Scholar
  69. Louvet, J. P., Harman, S. M., Schreiber, J. R., and Ross, G. T., 1975, Evidence for a role of androgens in follicular maturation, Endocrinology, 97:366.PubMedCrossRefGoogle Scholar
  70. Lucky, A. W., Schreiber, J. R., Hillier, S. G., Schulman, J. D., and Ross, G. T., 1977, Progesterone production by cultured preantral rat granulosa cells: stimulation by androgens, Endocrinology, 100:128.PubMedCrossRefGoogle Scholar
  71. Lyon, M. F., and Glenister, P. H., 1974, Evidence from Tfm/O that androgen is essential for reproduction in female mice, Nature (London), 247:366.CrossRefGoogle Scholar
  72. Magoffin, D.A., and Erickson, G. F., 1982, Direct inhibitory effects of estrogen on LH-stimulated androgen synthesis by ovarian cells cultured in defined medium, Mol. Cell. Endocrinol., 28:81.PubMedCrossRefGoogle Scholar
  73. Mahajan, D. K., and Samuels, L. T., 1975, Inhibition of 17, 20(17-hydroxy-progesterone)-lyase by progesterone, Steroids, 25:217.PubMedCrossRefGoogle Scholar
  74. McNatty, K. P., Makris, A., Reinhold, V. N., DeGrazia, C., Osathanondoh, R., and Ryan, K. J., 1979, Metabolism of androstenedione by human ovarian tissues in vitro with particular references to reductase and aromatase activity, Steroids, 34:429.PubMedCrossRefGoogle Scholar
  75. McNatty, K. P., Moore Smith, D., Makris, A., Osathanondh, R., and Ryan, K. J., 1979, The microenvironment of the human antral follicle: interrelationships among the steroid levels in antral fluid, the population of granulosa cells, and the status of the oocyte in vivo and in vitro, J. Clin. Endocrinol. Metab., 49:851.PubMedCrossRefGoogle Scholar
  76. Milwidsky, A., Younes, M. A., Besch, N. F., Besch, P. K., and Kaufman, R. H., 1980, Receptor-like binding proteins for testosterone and progesterone in the human ovary, Am. J. Obstet. Gynecol., 138:93.PubMedGoogle Scholar
  77. Moon, Y. S., Duleba, A. J., Kim, K. S., and Ho Yuen, B., 1985, Alterations of 20α-hydroxysteroid dehydrogenase activity in cultured rat granulosa cells by follicle-stimulating hormone and testosterone, Biol. Reprod., 32:998.PubMedCrossRefGoogle Scholar
  78. Moon, Y. S., Duleba, A. J., and Takahashi, H., 1984, Differential actions of LH and androgens on progesterone catabolism by rat granulosa cells, Biochem. Biophys. Res. Comm., 119:694.PubMedCrossRefGoogle Scholar
  79. Moor, R. M., Hay, M. F., and Seamark, R. F., 1975, The sheep ovary: regulation of steroidogenic, haemodynamic and structural changes in the largest follicle and adjacent tissue before ovulation, J. Reprod. Fertil., 45:595.PubMedCrossRefGoogle Scholar
  80. Mori, T., Suzuki, A., Nishimura, T., and Kambegawa, A., 1977, Evidence for androgen participation in induced ovulation in immature rats, Endocrinology, 101:623.PubMedCrossRefGoogle Scholar
  81. Naess, O., 1981, Characterization of cytoplasmic progesterone receptors in rat granulosa cells: evidence of nuclear translocation, Acta Endocrinol., 98:288.PubMedGoogle Scholar
  82. Neumann, F., von Berswordt-Wallrabe, R., Elger, W., Steinbeck, K., Hann, J. D., and Kramer, M., 1970, Aspects of androgen-dependent events as studied by antiandrogens, Rec. Prog. Horm. Res., 26:337.PubMedGoogle Scholar
  83. Nimrod, A., 1977, Studies on the synergistic effect of androgen on the stimulation of progestin secretion by FSH in cultured rat granulosa cells: a search for the mechanism of action, Mol. Cell. Endocrinol., 8:201.PubMedCrossRefGoogle Scholar
  84. Nimrod, A., 1981, On the synergistic action of androgen and FSH on progestin secretion by cultured rat granulosa cells: cellular and mitochondrial cholesterol metabolism, Mol. Cell. Endocrinol., 21:51.PubMedCrossRefGoogle Scholar
  85. Nimrod, A., and Lindner, H. R., 1976, A synergistic effect of androgen on the stimulation of progesterone secretion by FSH in cultured rat granulosa cells, Mol. Cell. Endocrinol., 5:315.PubMedCrossRefGoogle Scholar
  86. Nimrod, A., Rosenfield, R. L., and Otto, P., 1980, Relationship of androgen action to androgen metabolism in isolated rat granulosa cells, J. Steroid Biochem., 13:1015.PubMedCrossRefGoogle Scholar
  87. Ohno, S., Christian, L., and Attardi, B., 1973, Role of testosterone in normal female function, Nature (London), 243:119.CrossRefGoogle Scholar
  88. Opavsky, M. A., and Armstrong, D. T., 1985, The effectiveness of FSH in inducing superovulation is influenced by LH, Biol. Reprod., 32 (Suppl. 1), Abstract No. 67, p. 71.Google Scholar
  89. Pasqualini, J. R., and Nguyen, B. J., 1980, Progesterone receptors in fetal uterus and ovary of the guinea pig: evolution during fetal development and induction and stimulation in estradiol-primed animals, Endocrinology, 106:1160.PubMedCrossRefGoogle Scholar
  90. Payne, R. W., and Hellbaum, A. A., 1955, The effect of estrogens on the ovary of the hypophysectomized rat, Endocrinology, 57:193.PubMedCrossRefGoogle Scholar
  91. Payne, R. W., and Runser, R. H., 1958, The influence of estrogen and androgen on the ovarian response of hypophysectomized immature rats to gonado-tropins, Endocrinology, 62:313.PubMedCrossRefGoogle Scholar
  92. Peluso, J. J., Brown, I., and Steger, R. W., 1979, Effects of cyproterone acetate, a potent antiandrogen, on the preovulatory follicle, Biol. Reprod., 21:929.PubMedCrossRefGoogle Scholar
  93. Pencharz, R. I., 1940, Effect of estrogens and androgens alone and in combination with chorionic gonadotropin on the ovary of the hypophysectomized rat, Science, 91:554.PubMedCrossRefGoogle Scholar
  94. Philibert, D., Ojasoo, T., and Raynaud, J. P., 1977, Properties of the cyto-plasmic progestin-binding protein in the rabbit uterus, Endocrinology, 101:1850.PubMedCrossRefGoogle Scholar
  95. Reiter, E. O., Goldenberg, R. L., Vaitukaitis, J. L., and Ross, G. T., 1972, Evidence for a role of estrogen in ovarian augmentation reaction, Endocrinology, 91:1518.PubMedCrossRefGoogle Scholar
  96. Richards, J. S., 1974, Estradiol binding to rat corpora lutea during pregnancy, Endocrinology, 95:1046.PubMedCrossRefGoogle Scholar
  97. Richards, J. S., 1975, Estradiol receptor content of rat granulosa cells during follicular development: modification by estradiol and gonado-tropins, Endocrinology, 97:1174.PubMedCrossRefGoogle Scholar
  98. Richards, J. S., 1980, Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones on follicular cell differentiation, Physiol. Rev., 60:51.PubMedGoogle Scholar
  99. Richards, J. S., and Bogovich, K., 1982, Effect of human chorionic gonado-tropin and progesterone on follicular development in the immature rat, Endocrinology, 111:1429.PubMedCrossRefGoogle Scholar
  100. Saidapur, S. K., and Greenwald, G. S., 1979, Regulation of 17β-estradiol synthesis in the proestrous hamster: role of progesterone and luteinizing hormone, Endocrinology, 105:1432.PubMedCrossRefGoogle Scholar
  101. Saiduddin, S., 1971, 3H-estradiol uptake by the rat ovary, Proc. Soc. Exp. Biol. Med., 138:651.PubMedCrossRefGoogle Scholar
  102. Saiduddin, S., and Milo, G.E. Jr., 1974, Effect of hypophysectomy and pretreatment on uptake and retention of estradiol by the ovary, Proc. Soc. Exp. Biol. Med., 146:513.PubMedCrossRefGoogle Scholar
  103. Saiduddin, S., and Zassenhaus, H. P., 1977, Estradiol-17β receptors in the immature rat ovary, Steroids, 29:197.PubMedCrossRefGoogle Scholar
  104. Saiduddin, S., and Zassenhaus, H. P., 1978, Effect of testosterone and progesterone on the estradiol receptor in the immature rat ovary, Endocrinology, 102:1069.PubMedCrossRefGoogle Scholar
  105. Schomberg, D. W., Stouffer, R. L., and Tyrey, L., 1976, Modulation of progestin secretion in ovarian cells by 17β-hydroxy-5-adrostan-3-one (dihydrotestosterone): a direct demonstration in monolayer culture, Biochem. Biophys. Res. Comm., 68:77.PubMedCrossRefGoogle Scholar
  106. Schomberg, D. W., Williams, R. F., Tyrey, L., and Ulberg, L. C., 1978, Reduction of granulosa cell progesterone secretion in vitro by intra-ovarian implants of antiandrogen, Endocrinology, 102:984.PubMedCrossRefGoogle Scholar
  107. Schreiber, J. R., and Erickson, G. F., 1979, Progesterone receptor in the rat ovary: further characterization and localization in the granulosa cell, Steroids, 34:459.PubMedCrossRefGoogle Scholar
  108. Schreiber, J. R., and Ross, G. T., 1976, Further characterization of rat ovarian testosterone receptor with evidence for nuclear translocation, Endocrinology, 99:590.PubMedGoogle Scholar
  109. Schreiber, J. R., Hsueh, A. J. W., and Baulieu, E. E., 1983, Binding of the antiprogestin RU-486 to rat ovary steroid receptors, Contraception, 28:77.PubMedCrossRefGoogle Scholar
  110. Schreiber, J. R., Nakamura, K., and Erickson, G. F., 1980, Progestins inhibit FSH-stimulated steroidogenesis in cultured rat granulosa cells, Mol. Cell. Endocrinol., 19:165.PubMedCrossRefGoogle Scholar
  111. Schreiber, J. R., Nakamura, K., and Erickson, G. F., 1981, Progestins inhibit FSH-stimulated granulosa estrogen production at a post-cAMP site, Mol. Cell. Endocrinol., 21:161.PubMedCrossRefGoogle Scholar
  112. Schreiber, J. R., Reid, R., and Ross, G. T., 1976, A receptor-like testosterone binding protein in ovaries from estrogen-stimulated hypophysectomized immature female rats, Endocrinology, 98:1206.PubMedCrossRefGoogle Scholar
  113. Schreiber, J. R., and Hsueh, A. J. W., 1979, Progesterone “receptor” in rat ovary, Endocrinology, 105:915.PubMedCrossRefGoogle Scholar
  114. Schrieber, J. R., Nakamura, K., and Weinstein, D. B., 1983, Androgen and FSH synergistically stimulate rat ovary granulosa cell utilization of rat and human lipoproteins, in: “Factors Regulating Ovarian Function,” G. Greenwald, P. F. Terranova, eds., p. 311, Raven Press, New York.Google Scholar
  115. Shemesh, M., and Ailenberg, M., 1977, The effect of androstenedione on progesterone accumulation in cultures of bovine ovarian follicles, Biol. Reprod. 17:499.PubMedCrossRefGoogle Scholar
  116. Siiteri, P. K., and Thompson, E. A., 1975, Studies of human placental aroma-tase, J. Steroid Biochem., 6:317.PubMedCrossRefGoogle Scholar
  117. Simpson, M. E., Evans, H. M., Fraenkel-Conrat, H. L., and Li, C. H., 1941, Synergism of estrogens with pituitary gonadotropins in hypophysectomized rats, Endocrinology, 28:37.CrossRefGoogle Scholar
  118. Smith, B. D., 1961, The effect of diethylstilbestrol on the immature rat ovary, Endocrinology, 69:238.CrossRefGoogle Scholar
  119. Smith, B. D., and Bradbury, J. T., 1966, Influence of progestins on ovarian responses to estrogen and gonadotrophins in immature rats, Endocrinology, 78:297.PubMedCrossRefGoogle Scholar
  120. Smith, M. S., Freeman, M. E., and Neill, J. D., 1975, The control of progesterone secretion during the estrous cycle and early pseudopreg-nancy in the rat: prolactin gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy, Endocrinology, 96:219.PubMedCrossRefGoogle Scholar
  121. Smith, O. W., Ofner, P., and Vena, R. L., 1974, In vitro conversion of testosterone-4-14C to androgens of the 5α-androstane series by normal human ovary, Steroids, 24:311.PubMedCrossRefGoogle Scholar
  122. Smith, P. E., 1930, Hypophysectomy and a replacement therapy in the rat, Am. J. Anat., 45:205.CrossRefGoogle Scholar
  123. Stumpf, W. E., 1969, Nuclear concentration of 3H-estradiol in target tissues: dry-mount autoradiography of vagina, oviduct, ovary, testis, mammary tumor, liver and adrenal, Endocrinology, 85:31.PubMedCrossRefGoogle Scholar
  124. Tan, C. H., and Armstrong, D. T., 1984, FSH-stimulated 3β-HSD activity of porcine granulosa cells: inhibition by androgens, Proceedings of the 3rd Joint Meeting of the British Endocrine Societies, Edinburgh, Abstract No. 12.Google Scholar
  125. Thanki, K. H., and Channing, C. P., 1976, Influence of serum, estrogen, and gonadotropins upon growth and progesterone secretion by cultures of granulosa cells from small porcine follicles, Endocr. Res. Commun., 3:319.PubMedCrossRefGoogle Scholar
  126. Thanki, K. H., and Channing, C. P., 1978, Effects of follicle-stimulating hormone and estradiol upon progesterone secretion by porcine granulosa cells in tissue culture, Endocrinology, 103:74.PubMedCrossRefGoogle Scholar
  127. Toaff, M. E., Strauss III, J. F., and Hammond, J. M., 1983, Regulation of cytochrome P-450SCC in immature porcine granulosa cells by FSH and estradiol, Endocrinology, 112:1156.PubMedCrossRefGoogle Scholar
  128. Tsafriri, A., and Braw, R. H., 1984, Experimental approaches to atresia in mammals, in: “Oxford Reviews of Reproductive Biology,” R. E. Clarke, ed., Vol. 6, p. 226, Claredon Press, Oxford.Google Scholar
  129. Veldhuis, J. D., 1985, Bipotential actions of estrogens on progesterone biosynthesis by ovarian cells. II. Relation of estradiol’s stimulatory actions to cholesterol and progestin metabolism in cultured swine granulosa cells, Endocrinology, 117:1076.PubMedCrossRefGoogle Scholar
  130. Veldhuis, J. D., Klase, P. A., Sandon, B. A., and Kolp, L. A., 1983, Progesterone secretion by highly differentiated human granulosa cells isolated from preovulatory Graafian follicles, induced by endogenous gonadotropins and human chorionic gonadotropin, J. Clin. Endocrinol. Metab., 57:287.Google Scholar
  131. Veldhuis, J. D., Klase, P. A., Strauss, J. F., and Hammond, J. M., 1982, Facultative interactions between estradiol and luteinizing hormone in the regulation of progesterone production by cultured swine granulosa cells: relation to cholesterol metabolics, Endocrinology, 111:441.PubMedCrossRefGoogle Scholar
  132. Welsh, T. H. Jr., Jones, P. B. C., Ruiz de Galaretta, C. M., Fanjul, L. F., and Hsueh, A. J. W., 1982, Androgen regulation of progestin biosynthetic enzymes in FSH-treated rat granulosa cells in vitro, Steroids, 40:691.PubMedCrossRefGoogle Scholar
  133. Welsh, T. H. Jr., Jia, X.-C., Jones, P. B. C., Zhuang, L.-Z., and Hsueh, A. J. W., 1984, Disparate effects of triphenylethylene antiestrogens on estrogen and progestin biosyntheses by cultured rat granulosa cells, Endocrinology, 115:1275.PubMedCrossRefGoogle Scholar
  134. Welsh, T. H. Jr., Zhuang, L.-Z., and Hsueh, A. J. W., 1983, Estrogen augmentation of gonadotropin-stimulated progestin biosynthesis in cultured rat granulosa cells, Endocrinology, 112:1916.PubMedCrossRefGoogle Scholar
  135. Williams, P. C., 1940, Effect of stilbestrol on the ovaries of hypophysecto-mized rats, Nature (London), 145:388.CrossRefGoogle Scholar
  136. Williams, P. C., 1944, Ovarian stimulation by oestrogens: effects in immature hypophysectomized rats, Proc. R. Soc. Series B, 132:189.CrossRefGoogle Scholar
  137. Zeleznik, A. J., Hillier, S. G., and Ross, G. T., 1979, Follicle-stimulating hormone-induced follicular development: an examination of the role of androgens, Biol. Reprod., 21:673.PubMedCrossRefGoogle Scholar
  138. Zhuang, L.-Z., Adashi, E. Y., and Hsueh, A. J. W., 1982, Direct enhancement of gonadotropin-stimulated ovarian estrogen biosynthesis by estrogen and clomiphene citrate, Endocrinology, 110:2219.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1987

Authors and Affiliations

  • D. T. Armstrong
    • 1
  • S. A. J. Daniel
    • 1
  • R. E. Gore-Langton
    • 1
  1. 1.Medical Research Council of Canada, Group in Reproductive Biology, Departments of Physiology Obstetrics and GynaecologyUniversity of Western OntarioLondonCanada

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