Summary
We have previously demonstrated that estrogen can exert inhibitory or atretogenic effects on the ovaries of both rats and rhesus monkeys in vivo. This study was designed to test whether the hamster (Mesocricetus auratus) is an appropriate model in which to test the effects of estrogens (diethylstilbestrol and estradiol-17β) on steroid accumulation by ovarian granulosa cells in vitro, and whether the effects are similar to those demonstrated for other species in vivo. Immature female hamsters were injected with pregnant mare's serum gonadotropin at 28 to 30 days of age. Animals were sacrificed and follicular contents aspirated three days later. Granulosa cells were either left untreated or treated with diethylstilbestrol or estradiol (1×10-7 M) in vitro for 72 h in the presence of androstenedione (1×10-7 M), and in the presence or absence of serum (10%) or human follicle-stimulating hormone (20 ng/ml), and long-term accumulation of estrogen and progesterone was determined. Diethylstilbestrol inhibited accumulation of estrogen regardless of the presence or absence of follicle-stimulating hormone. In contrast, only estradiol plus follicle-stimulating hormone augmented accumulation of progesterone by granulosa cells. These findings that estrogen can be non-stimulatory or inhibitory to function of granulosa cells in vitro parallel those shown in vivo. Our experimental approach may therefore represent an appropriate model for study of the direct effects of estradiol on the function of granulosa cells.
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References
Adashi EY, Hsueh AJW (1982) Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells. J Biol Chem 257:6077–6083
Burghardt RC, Anderson E (1981) Hormonal modulation of gap junctions in rat ovarian follicles. Cell Tissue Res 214:181–193
Channing CP, Reichert LE Jr (1984) Effect of follicle-stimulating hormone upon estrogen and progesterone secretion by cultures of monkey granulosa cells recovered during the periovulatory period. Fertil Steril 43:446–452
Chiras DD, Greenwald GS (1978) Effects of steroids and gonadotropins on follicular development in the hypophysectomized hamster. Am J Anat 152:307–319
Clark JR, Dierschke DJ, Wolf RC (1978) Hormonal regulation of ovarian folliculogenesis in rhesus monkeys. I. Concentrations of serum luteinizing hormone and progesterone during laparoscopy and patterns of follicular development during successive menstrual cycles. Biol Reprod 18:779–783
Clark JR, Dierschke DJ, Meller PA, Wolf RC (1979) Hormonal regulation of ovarian folliculogenesis in rhesus monkeys. II. Serum concentrations of estradiol-17β and follicle stimulating hormone associated with growth and identification of the preovulatory follicle. Biol Reprod 21:497–503
Clark JR, Dierschke DJ, Wolf RC (1981) Hormonal regulation of ovarian folliculogenesis in rhesus monkeys: III. Atresia of the preovulatory follicle induced by exogenous steroids and subsequent follicular development. Biol Reprod 25:332–341
Daniel SAJ, Armstrong DT (1983) Involvement of estrogens in the regulation of granulosa cell aromatase activity. J Physiol Pharmacol 61:507–511
Dierschke DJ, Braw RH, Tsafriri A (1983) Estradiol-17β reduces number of ovulations in adult rats: direct action on the ovary. Biol Reprod 29:1147–1154
Dierschke DJ, Hutz RJ, Wolf RC (1985) Strength-duration relationships of the estrogen simulus. Endocrinology 117:1397–1403
Goldenberg RL, Vaitukaitis JL, Ross GT (1972) Estrogen and follicle stimulating hormone interactions on follicle growth in rats. Endocrinology 90:1492–1498
Gorski J, Toft D, Shyamala G, Smith D, Notides A (1968) Hormone receptors: Studies on the interaction of estrogen with the uterus. Recent Prog Horm Res 24:45–80
Greenwald GS, Peppler RD (1968) Prepubertal and pubertal changes in the hamster ovary. Anat Rec 161:447–458
Greenwald GS (1975) Proestrous hormone surges dissociated from ovulation in the estrogen-treated hamster. Endocrinology 97:878–884
Hammond JM, Hersey RM, Walega M, Weisz J (1984) Synthesis of catechol estrogens in the porcine ovary. Proceedings of the International Congress of Endocrinology, Quebec City, Canada
Harman SM, Louvet JP, Ross GT (1975) Interaction of estrogen and gonadotropins on follicular atresia. Endocrinology 96:1145–1152
Hillier SG, Ross GT (1979) Effects of exogenous testosterone on ovarian weight, follicular morphology and intraovarian progesterone concentration in estrogen-primed hypophysectomized immature female rats. Endocrinology 96:1145–1152
Hutz RJ, Ghosh M, Dukelow WR (1984) Steroid uptake and 3-Huridine incorporation by early hamster and squirrel monkey (in vitro fertilized) embryos: Effects of ovulatory regimen. Zool Sci 1:771–776
Hutz RJ, Dierschke DJ, Wolf RC (1986a) Markers of atresia in ovarian follicular components from rhesus monkeys treated with estradiol-17β. Biol Reprod 34:65–70
Hutz RJ, Krueger GS, Meller PA, Sholl SA, Dierschke DJ (1986b) FSH-induced aromatase activity in hamster granulosa cells: effect of estradiol-17β in vitro. Proceedings of the Ovarian Workshop, Ithaca, NY
Jonassen JA, Bose K, Richards JS (1982) Enhancement and desensitization of hormone-responsive adenylate cyclase in granulosa cells of preantral and antral ovarian follicles: Effects of estradiol and follicle-stimulating hormone. Endocrinology 111:74–79
Kim I, Shaha C, Greenwald GS (1984) A species difference between hamster and rat in the effect of oestrogens on growth of large preantral follicle. J Reprod Fertil 72:179–185
Leung PCK, Goff AK, Kennedy TG, Armstrong DT (1978) An intraovarian inhibitory action of estrogen on androgen production in vivo. Biol Reprod 19:641–647
Lino J, Baranao S, Hammond JM (1985) Multihormone regulation of steroidogenesis in cultured porcine granulosa cells: studies in serum-free medium. Endocrinology 116:2143–2151
Matson PL, Collins WP (1984) Aromatase activity in ovarian follicles of the golden hamster. J Reprod Fertil 72:101–105
Munabi AK, Cassorla FG, Pfeiffer DG, Albertson BD, Loriaux DL (1983) The effects of estradiol and progesterone on rat ovarian 17-hydroxylase and 3β-hydroxysteroid dehydrogenase activities. Steroids 41:95–98
Na JY, Garza F, Terranova PF (1985) Alterations in follicular fluid steroids and follicular hCG and FSH binding during atresia in hamster. Proc Soc Exp Biol Med 179:123–127
Nordenstrom K, Johanson C (1985) Steroidogenesis in isolated rat granulosa cells —changes during follicular maturation. Acta Endocrinol 108:550–556
Reichert LE Jr (1972) Biological studies on the relatedness of subunits of human follicle-stimulating hormone and chorionic gonadotropin. Endocrinology 90:1119–1122
Richards JS (1975) Content of nuclear estradiol receptor complex in rat granulosa cells during follicular development: modification by estradiol and gonadotropins. Endocrinology 97:1174–1184
Richards JS, Rolfes AI (1980) Hormonal regulation of cyclic AMP binding to specific receptor proteins in rat ovarian follicles. Characterization by photoaffinity labeling. J Biol Chem 255:5481–5489
Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR Jr, Reichert LE Jr (1976) Ovarian follicular development in the rat: hormone receptor regulation by estradiol, follicle-stimulating hormone and luteinizing hormone. Endocrinology 99:1562–1570
Richards JS, Jonassen JR, Rolfes AI, Korsey KA, Reichert LE Jr (1979) Adenosine 3′,5′-monophosphate luteinizing hormone receptor, and progesterone during granulosa cell differentiation: effects of estradiol and follicle stimulating hormone. Endocrinology 104:765–773
Ross GT, Hillier SG (1979) Experimental aspects of follicular maturation. Eur J Obstet Gynecol Reprod Biol 9:169–174
Ross GT, diZerega GS (1983) Regulation of follicle growth. Prog Gynecol 7:21–41
Saidapur SK, Greenwald GS (1978) Peripheral blood and ovarian levels of sex steroids in the cyclic hamster. Biol Reprod 18:401–408
Savion N, Lui G-M, Laherty R, Gospodarowicz D (1981) Factors controlling proliferation and progesterone production by bovine granulosa cells in serum free medium. Endocrinology 109:409–420
Silavin SL, Greenwald GS (1984) Steroid production by isolated theca and granulosa cells after initiation of atresia in the hamster. J Reprod Fertil 71:387–392
Skaf RA, MacDonald GJ, Shelden RM, Moyle WR (1985) Use of antisera to follicle-stimulating hormone (FSH) to detect non-FSH factors in human serum which modulate rat granulosa cell steroidogenesis. Endocrinology 117:106–113
Steel RGD, Torrie JH (1980) In: Principles and procedures of statistics. A biometrical approach. McGraw-Hill, New York
Veldhuis JD, Aziml P, Garmey J, Juchte RD (1985) Bipotential actions of estrogen on progesterone biosynthesis by ovarian cells. II. Relation of estradiol's stimulatory actions to cholesterol and progestin metabolism in cultured swine granulosa cells. Endocrinology 117:1076–1083
Welsh TH Jr, Jones PBC, Ruiz de Galarreta CM, Fanjul LH, Hsueh AJW (1982) Androgen regulation of progestin biosynthetic enzymes in FSH-treated rat granulosa cells in vitro. Steroids 40:691–700
Welsh TJ Jr, Zhuang L-Z, Hsueh AJW (1983) Estrogen augmentation of gonadotropin-stimulated progestin biosynthesis in cultured rat granulosa cells. Endocrinology 112:1916–1924
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Hutz, R.J., Gold, D.A. & Dierschke, D.J. Diminished steroidogenic response of hamster granulosa cells to estrogen in vitro. Cell Tissue Res. 248, 531–534 (1987). https://doi.org/10.1007/BF00216480
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DOI: https://doi.org/10.1007/BF00216480