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Article| Volume 79, ISSUE 5, P813-821, May 1996

Interaction Among Bovine Somatotropin, Insulin, and Gonadotropins on Steroid Production by Bovine Granulosa and Thecal Cells1

  • Author Footnotes
    2 To whom reprint requests should be sent.
    L.J. Spicer
    Footnotes
    2 To whom reprint requests should be sent.
    Affiliations
    Department of Animal Science, Oklahoma State University, Stillwater 74078
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  • R.E. Stewart
    Affiliations
    Department of Animal Science, Oklahoma State University, Stillwater 74078
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  • Author Footnotes
    1 Approved for publication by the director of the Oklahoma Agricultural Experiment Station. This research was supported under Project H-2088 and Project Number HR4-032 from the Oklahoma Center for the Advancement of Science and Technology.
    2 To whom reprint requests should be sent.
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      Abstract

      The objective of the present study was to determine the interactions among bST, insulin, and gonadotropins on steroid production by granulosa and thecal cells from bovine follicles. Basal production of estradiol by granulosa cells from small (1 to 5 mm) and large (≥8 mm) follicles (expressed as picograms of estradiol per 105 cells per 24 h) was not affected by 50 or 300 ng/ml of bST, but 300 ng/ml of bST inhibited estradiol production that was induced by FSH plus insulin in cells from small and large follicles. Progesterone production and proliferation by granulosa cells from large follicles were not affected by 3 to 100 ng/ml of bST. In cultures of thecal cells that exhibited a >3-fold increase in androstenedione production induced by LH, 3 to 30 ng/ml of bST further increased androstenedione production by 29 to 42%) but cell proliferation and progesterone production were unaffected by bST. In cultures of thecal cells that exhibited a <2-fold increase in androstenedione production induced by LH, 3 to 30 ng/ml of bST inhibited androstenedione production by 32 to 33% and inhibited cell proliferation by 9 to 13%, but progesterone was unaffected by bST. In summary, only pharmacologic doses of bST inhibited estradiol production by granulosa cells, but physiologic doses of bST altered androstenedione production by thecal cells, which indicated that bST might not have an important role in granulosa cell function but might play a role in thecal cell function in cattle.

      Key words

      Abbreviation key:

      FCS (fetal calf serum)

      References

        • Ando M.
        • Yoshimura Y.
        • Iwashita M.
        • Oda T.
        • Karube M.
        • Ubukata Y.
        • Jinno M.
        • Nakamura Y.
        Direct ovarian effect of growth hormone in the rabbit.
        Am. J. Reprod. Immunol. 1994; 31: 123
        • Apa R.
        • Lanzone A.
        • Miceli F.
        • Caruso A.
        • Mancuso S.
        • Canipari R.
        Growth hormone induction of rat granulosa cell tissue-plasminogen activator expression and progesterone synthesis.
        Mol. Cell Endocrinol. 1994; 99: 153
        • Barreca A.
        • Artini P.G.
        • Del Monte P.
        • Ponzani P.
        • Pasquini P.
        • Cariola G.
        • Volpe A.
        • Genazzani A.R.
        • Giordano G.
        • Minuto F.
        In vivo and in vitro effect of growth hormone on estradiol secretion by human granulosa cells.
        J. Clin. Endocrinol. Metab. 1993; 77: 61
        • CarIsson B.
        • Bergh C.
        • Bentham J.
        • Olsson J.-H.
        • Norman M.R.
        • Billig H.
        • Roos P.
        • Hillensjo T.
        Expression of functional growth hormone receptors in human granulosa cells.
        Human Reprod. 1992; 7: 1205
        • Cole W.J.
        • Madsen K.S.
        • Hintz R.L.
        • Collier R.J.
        Effect of recombinantly-derived bovine somatotropin on reproductive performance of dairy cattle.
        Theriogenology. 1991; 36: 573
        • Crooker B.A.
        • McGuire M.A.
        • Cohick W.S.
        • Harkins M.
        • Bauman D.E.
        • Sejrsen K.
        Effect of dose of bovine somatotropin on nutrient utilization in growing dairy heifers.
        J. Nutr. 1990; 120: 1256
        • De La Sota R.L.
        • Lucy M.C.
        • Staples C.R.
        • Thatcher W.W.
        Effects of recombinant bovine somatotropin (Sometribove) on ovarian function in lactating and nonlactating dairy cows.
        J. Dairy Sci. 1993; 76: 1002
        • Enright W.J.
        • Spicer L.J.
        • Prendiville D.J.
        • Murphy M.G.
        • Campbell R.M.
        Interaction between dietary intake and ovariectomy on concentrations of insulin-like growth factor-I. GH and LH in plasma of heifers.
        Theriogenology. 1994; 41: 1231
        • Enright W.J.
        • Zinn S.A.
        • Chapin L.T.
        • Tucker H.A.
        Growth hormone response of bull calves to growth hormone-releasing factor.
        Proc. Soc. Exp. Biol. Med. 1987; 194: 483
        • Esteban E.
        • Kass P.H.
        • Weaver L.D.
        • Rowe J.D.
        • Holmberg C.A.
        • Franti C.E.
        • Troutt H.F.
        Reproductive performance in high producing dairy cows treated with recombinant bovine somatotropin.
        J. Dairy Sci. 1994; 77: 3371
        • Gong J.G.
        • Bramley T.
        • Webb R.
        The effects of recombinant bovine somatotropin on ovarian function in heifers: follicular populations and peripheral hormones.
        Biol. Reprod. 1991; 45: 941
        • Gong J.G.
        • Bramley T.A.
        • Wilmut I.
        • Webb R.
        Effect of recombinant bovine somatotropin on the superovulatory response to pregnant mare serum gonadotropin in heifers.
        Biol. Reprod. 1993; 48: 1141
        • Gong J.G.
        • McBride D.
        • Bramley T.A.
        • Webb R.
        Effect of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on the proliferation of bovine granulosa cells in vitro.
        J. Endocrinol. 1993; 139: 67
        • Gong J.G.
        • McBride D.
        • Bramley T.A.
        • Webb R.
        Effects of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on bovine granulosa cell steroidogenesis in vitro.
        J. Endocrinol. 1994; 143: 157
        • Hall J.B.
        • Schillo K.K.
        • Fitzgerald B.P.
        • Bradley N.W.
        Effects of recombinant bovine somatotropin and dietary energy intake on growth, secretion of luteinizing hormone, follicular development, and onset of puberty in beef heifers.
        J Anim. Sci. 1994; 72: 709
        • Hemken R.W.
        • Harmon R.J.
        • Silvia W.J.
        • Tucker W.B.
        • Heersche G.
        • Eggert R.G.
        Effect of dietary energy and previous bovine somatotropin on milk yield, mastitis, and reproduction in dairy cows.
        J. Dairy Sci. 1991; 74: 4265
        • Herbein J.J.
        • Aiello R.J.
        • Eckler L.I.
        • Pearson R.E.
        • Akers R.M.
        Glucagon, insulin, growth hormone, and glucose concentrations in blood plasma of lactating dairy cows.
        J. Dairy Sci. 1985; 68: 320
        • Hsu C.-J.
        • Hammond J.M.
        Concomitant effects of growth hormone on secretion of insulin-like growth factor-I and progesterone in cultured porcine granulosa cells.
        Endocrinology. 1987; 121: 1343
        • Hutchinson L.A.
        • Findlay J.K.
        • Herington A.C.
        Growth hormone and insulin-like growth factor-I accelerate PMSG-induced differentiation of granulosa cells.
        Mol. Cell. Endocrinol. 1988; 55: 61
        • Ireland J.J.
        • Roche J.F.
        Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins.
        Endocrinology. 1983; 112: 150
        • Jia X.-C.
        • Kalmijn J.
        • Hsueh A.J.W.
        Growth hormone enhances follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells.
        Endocrinology. 1986; 118: 1401
        • Kirkwood R.N.
        • Thacker P.A.
        • Rajkumar K.
        Effects of growth hormone and triiodothyronine on insulin-induced progesterone production by granulosa cells from prepubertal gilts.
        Can. J. Anim. Sci. 1992; 72: 589
        • Kuehner L.F.
        • Rieger D.
        • Walton J.S.
        • Zhao X.
        • Johnson W.H.
        The effect of depot injection of recombinant bovine somatotropin on follicular development and embryo yield in superovulated Holstein heifers.
        Theriogenology. 1993; 40: 1003
        • Langhout D.J.
        • Spicer L.J.
        • Geisert R.D.
        Development of a culture system for bovine granulosa cells: effects of growth hormone, estradiol, and gonadotropins on cell proliferation, steroidogenesis, and protein synthesis.
        J. Anim. Sci. 1991; 69: 3321
        • Lapierre H.
        • Pelletier G.
        • Petitclerc D.
        • Dubreuil P.
        • Morisset J.
        • Gaudreau P.
        • Couture Y.
        • Brazeau P.
        Effect of human growth hormone-releasing factor (1-29)NH2 on growth hormone release and milk production in dairy cows.
        J. Dairy Sci. 1988; 71: 92
        • Lucy M.C.
        • Byatt J.C.
        • Curran T.L.
        • Curran D.F.
        • Collier R.J.
        Placental lactogen and somatotropin: hormone binding to the corpus luteum and effects on the growth and functions of the ovary in heifers.
        Biol. Reprod. 1994; 50: 1136
        • Lucy M.C.
        • De La Sota R.L.
        • Staples C.R.
        • Thatcher W.W.
        Ovarian follicular populations in lactating dairy cows treated with recombinant bovine somatotropin (Sometribove) or saline and fed diets differing in fat content and energy.
        J. Dairy Sci. 1993; 76: 1014
        • Nitray J.
        • Sirotkin A.V.
        • Poltarsky J.
        • Bulla J.
        The effect of recombinant somatotropic hormone on secretion of ovarian hormones of sexually mature gilts in vivo and in vitro.
        Vet. Med. (Prague). 1993; 38: 53
        • Ott L.
        Multiple comparisons.
        An Introduction to Statistical Methods and Data Analysis. Duxbury Press, North Scituate, MA1977 (Page 384)
        • Plouzek C.A.
        • Vale W.
        • Rivier J.
        • Anderson L.L.
        • Trenkle A.
        Growth hormone-releasing factor on growth hormone secretion in prepubertal calves.
        Proc. Soc. Exp. Biol. Med. 1988; 188: 198
        • Roberts A.J.
        • Skinner M.K.
        Hormonal regulation of thecal cell function during antral follicle development in bovine ovaries.
        Endocrinology. 1990; 127: 2907
      1. SAS® User's Guide: Statistics. Version 6 Edition. 1988. SAS Inst., Inc., Cary, NC.

        • Schams D.
        • Winkler U.
        • Theyerl-Abele M.
        • Prokopp A.
        Variation of BST and IGF-I concentrations in blood plasma of cattle.
        in: Sejrsen K. Vestergaard M. Neimann-Sorensen A. Use of Somatotropin in Livestock Production. Elsevier Appl. Sci., New York, NY1989: 18
        • Schemm S.R.
        • Deaver D.R.
        • Griel Jr., L.C.
        • Muller L.D.
        Effects of recombinant bovine somatotropin on luteinizing hormone and ovarian function in lactating dairy cows.
        Biol. Reprod. 1990; 42: 815
        • Spicer L.J.
        • Alpizar E.
        • Echternkamp S.E.
        Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and(or) insulin-like growth factor I production in vitro.
        J. Anim. Sci. 1993; 71: 1232
        • Spicer L.J.
        • Enright W.J.
        Concentrations of insulin-like growth factor I and steroids in follicular fluid of preovulatory bovine ovarian follicles: effect of daily injections of a growth hormone-releasing factor analog and(or) thyrotropin-releasing hormone.
        J. Anim. Sci. 1991; 69: 1133
        • Spicer L.J.
        • Tucker W.B.
        • Adams G.D.
        Insulin-like growth factor-I in dairy cows: relationships among energy balance, body condition, ovarian activity, and estrous behavior.
        J. Dairy. Sci. 1990; 73: 929
        • Stelwagen K.
        • Grieve D.G.
        • McBride B.W.
        • Rehman J.D.
        Growth and subsequent lactation in primigravid Holstein heifers after prepartum bovine somatotropin treatment.
        J. Dairy Sci. 1992; 75: 463
        • Villa-Godoy A.
        • Hughes T.L.
        • Emery R.S.
        • Enright W.J.
        • Ealy A.D.
        • Zinn S.A.
        • Fogwell R.L.
        Energy balance and body condition influence luteal function in Holstein heifers.
        Domest. Anim. Endocrinol. 1990; 7: 135
        • Webb R.
        • Gong J.G.
        • Law A.S.
        • Rusbridge S.M.
        Control of ovarian function in cattle.
        J. Reprod. Fertil. 1992; 45: 141
        • Yoshimura Y.
        • Nakamura Y.
        • Koyama N.
        • Iwashita M.
        • Adachi T.
        • Takeda Y.
        Effects of growth hormone on follicle growth, oocyte maturation, and ovarian steroidogenesis.
        Fertil. Steril. 1993; 59: 917
        • Zhao X.
        • Burton J.H.
        • McBride B.W.
        Lactation, health, and reproduction of dairy cows receiving daily injectable or sustained-release somatotropin.
        J. Dairy Sci. 1992; 75: 3122