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Hypophyseal corticosteroids stimulate somatotrope differentiation in the embryonic chicken pituitary gland

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Abstract

Although it is known that glucocorticoids induce differentiation of growth hormone (GH)-producing cells in rodents and birds, the effect of mineralocorticoids on GH mRNA expression and the origin of corticosteroids affecting somatotrope differentiation have not been elucidated. In this study, we therefore carried out experiments to determine the effect of mineralocorticoids on GH mRNA expression in the chicken anterior pituitary gland in vitro and to determine whether corticosteroids are synthesized in the chicken embryonic pituitary gland. In a pituitary culture experiment with E11 embryos, both corticosterone and aldosterone stimulated GH mRNA expression and increased the number of GH cells in both lobes of the pituitary gland in a dose-dependent manner. These effects of the corticosteroids were significantly reversed by pretreatment with mifepristone, a glucocorticoid receptor (GR) antagonist, or spironolactone, a mineralocorticoid receptor (MR) antagonist. Interestingly, an in vitro serum-free culture experiment with an E11 pituitary gland showed that the GH mRNA level spontaneously increased during cultivation for 2 days without any extra stimulation, and this increase in GH mRNA level was completely suppressed by metyrapone, a corticosterone-producing enzyme P450C11 inhibitor. Moreover, progesterone, the corticosterone precursor, also stimulated GH mRNA expression in the cultured chicken pituitary gland, and this effect was blocked by pretreatment with metyrapone. We also detected mRNA expression of enzymes of cytochrome P450 cholesterol side chain cleavage (P450scc) and 3β-hydroxysteroid dehydrogenase1 (3β-HSD1) in the developmental chicken pituitary gland from E14 and E18, respectively. These results suggest that mineralocorticoids as well as glucocorticoids can stimulate GH mRNA expression and that corticosteroids generated in the embryonic pituitary gland by intrinsic steroidogenic enzymes stimulate somatotrope differentiation.

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Reference

  • Adkins-RE, Ottinger MA, Park J (1995) Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J Exp Zool 271:466–470

    Article  Google Scholar 

  • Ashwell JD, Lu FW, Vacchio MS (2000) Glucocorticoids in T cell development and function*. Annu Rev Immunol 18:309–345

    Article  PubMed  CAS  Google Scholar 

  • Bahr JM, Wang SC, Huang MY, Calvo FO (1983) Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol Reprod 29:326–334

    Article  PubMed  CAS  Google Scholar 

  • Barabanov VM (1991) Determination of adenohypophysis cytodifferentiation during embryonic development. Ontogenez 22:175–181

    PubMed  CAS  Google Scholar 

  • Beato M, Herrlich P, Schutz G (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83:851–857

    Article  PubMed  CAS  Google Scholar 

  • Berghman LR, van Beeumen J, Decuypere E, Kuhn ER, Vandesande F (1988) One-step purification of chicken growth hormone from a crude pituitary extract by use of a monoclonal immunoadsorbent. Comp Biochem Physiol B Biochem Mol Biol 113:773–780

    Article  Google Scholar 

  • Bossis I, Porter TE (2000) Ontogeny of corticosterone-inducible growth hormone secreting cells during chick embryonic development. Endocrinology 141:2683–2690

    Article  PubMed  CAS  Google Scholar 

  • Bossis I, Nishimura S, Muchow M, Porter TE (2004) Pituitary expression of type I and type II glucocorticoid receptors during chicken embryonic development and their involvement in growth hormone cell differentiation. Endocrinology 145:3523–3531

    Article  PubMed  CAS  Google Scholar 

  • Cima I, Corazza N, Dick B, Fuhrer A, Herren S, Jakob S, Ayuni E, Mueller C, Brunner T (2004) Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation. J Exp Med 20:1635–1646

    Article  CAS  Google Scholar 

  • Dean CE, Morpurgo B, Porter TE (1999) Induction of somatotroph differentiation in vivo by corticosterone administration during chicken embryonic development. Endocrine 11:151–156

    Article  PubMed  CAS  Google Scholar 

  • Frawley LS, Boockfor FR, Hoeffler JP (1985) Identification by plaque assays of a pituitary cell type that secretes both growth hormone and prolactin. Endocrinology 116:734–737

    Article  PubMed  CAS  Google Scholar 

  • Frawley LS, Boockfor FR (1991) Mammosomatotropes: presence and functions in normal and neoplastic pituitary tissue. Endocr Rev 12:337–355

    Article  PubMed  CAS  Google Scholar 

  • Funder JW (1997) Glucocorticoid and mineralocorticoid receptors: biology and clinical relevance. Annu Rev Med 48:231–240

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Sánchez CE, Zhou MY, Cozza EN, Morita H, Eddleman FC, Gómez-Sánchez EP (1996) Corticosteroid synthesis in the central nervous system. Endocr Res 22:463–470

    PubMed  Google Scholar 

  • Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371

    Article  PubMed  CAS  Google Scholar 

  • Hayward LS, Satterlee DG, Wingfield JC (2005) Japanese quail selected for high plasma corticosterone response deposit high levels of corticosterone in their eggs. Physiol Biochem Zool 78:1026–1031

    Article  PubMed  CAS  Google Scholar 

  • Hemming FJ, Aubert ML, Dubois PM (1988) Differentiation of fetal rat somatotropes in vitro: effects of cortisol, 3,5,3′-triiodothyronine, and glucagon, a light microscopic and radioimmunological study. Endocrinology 123:1230–1236

    PubMed  CAS  Google Scholar 

  • Jenkins SA, Porter TE (2004) Ontogeny of the hypothalamo-pituitary-adrenocortical axis in the chicken embryo: a review. Domest Anim Endocrinol 26:267–275

    Article  PubMed  CAS  Google Scholar 

  • Jozsa R, Scanes CG, Vigh S, Mess B (1979) Functional differentiation of the embryonic chicken pituitary gland studied by immunohistological approach. Gen Comp Endocrinol 39:158–163

    Article  PubMed  CAS  Google Scholar 

  • Kalliecharan R, Hall BK (1974) A developmental study of the levels of progesterone, corticosterone, cortisol, and cortisone circulating in plasma of chick embryos. Gen Comp Endocrinol 24:364–372

    Article  PubMed  CAS  Google Scholar 

  • Kanda I, Akazome Y, Ogasawara O, Mori T (2000) Expression of cytochrome P450 cholesterol side chain cleavage and 3beta-hydroxysteroid dehydrogenase during embryogenesis in chicken adrenal glands and gonads. Gen Comp Endocrinol 118:96–104

    Article  PubMed  CAS  Google Scholar 

  • Lipar JL, Ketterson ED, Nolan V Jr (1999a) Intra-clutch variation in testosterone content of red-winged blackbird eggs. Auk 116:231–235

    Google Scholar 

  • Lipar JL, Ketterson ED, Nolan V Jr, Casto JM (1999b) Egg yolk layers vary in the concentration of steroid hormones in two avian species. Gen Comp Endocrinol 115:220–227

    Article  PubMed  CAS  Google Scholar 

  • MacKenzie SM, Clark CJ, Fraser R, Gómez-Sánchez CE, Connell JM, Davies E (2000) Expression of 11beta-hydroxylase and aldosterone synthase genes in the rat brain. J Mol Endocrinol 24:321–328

    Article  PubMed  CAS  Google Scholar 

  • Morpurgo B, Dean CE, Porter TE (1997) Identification of the blood-borne somatotroph-differentiating factor during chicken embryonic development. Endocrinology 138:4530–4535

    Article  PubMed  CAS  Google Scholar 

  • Nogami H, Inoue K, Kawamura K (1997) Involvement of glucocorticoid-induced factor(s) in the stimulation of growth hormone expression in the fetal rat pituitary gland in vitro. Endocrinology 138:1810–1815

    Article  PubMed  CAS  Google Scholar 

  • Porter TE, Couger GS, Dean CE, Hargis BM (1995) Ontogeny of growth hormone (GH)-secreting cells during chicken embryonic development: initial somatotrophs are responsive to GH-releasing hormone. Endocrinology 136:1850–1856

    Article  PubMed  CAS  Google Scholar 

  • Porter TE, Dean CE, Piper MM, Medvedev KL, Ghavam S, Sandor J (2001) Somatotroph recruitment by glucocorticoids involves induction of growth hormone gene expression and secretagogue responsiveness. J Endocrinol 169:499–509

    Article  PubMed  CAS  Google Scholar 

  • Rettenbacher S, Mostl E, Hackl R, Palme R (2005) Corticosterone in chicken eggs. Ann N Y Acad Sci 1046:193–203

    Article  PubMed  CAS  Google Scholar 

  • Sampath-KR, Yu M, Khalil MW, Yang K (1997) Metyrapone is a competitive inhibitor of 11beta-hydroxysteroid dehydrogenase type1 reductase. J Steroid Biochem Mol Biol 62:195–199

    Article  Google Scholar 

  • Savory JG, Prefontaine GG, Lamprecht C, Liao M, Walther RF, Lefebvre YA, Hache RJ (2001) Glucocorticoid receptor homodimers and glucocorticoid–mineralocorticoid receptor heterodimers form in the cytoplasm through alternative dimerization interfaces. Mol Cell Biol 21:781–793

    Article  PubMed  CAS  Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450

    Article  PubMed  CAS  Google Scholar 

  • Scott TR, Johnson WA, Satterlee DG, Gildersleeve RP (1981) Circulating levels of corticosterone in the serum of developing chick embryos and newly hatched chicks. Poult Sci 60:1314–1320

    PubMed  CAS  Google Scholar 

  • Thommes RC, Umporowicz DM, Leung FC, Woods JE (1987) Ontogenesis of immunocytochemically demonstrable somatotrophs in the adenohypophyseal pars distalis of the developing chick embryo. Gen Comp Endocrinol 67:390–398

    Article  PubMed  CAS  Google Scholar 

  • Vacchio MS, Ashwell JD (1997) Thymus-derived glucocorticoids regulate antigen-specific positive selection. J Exp Med 185:2033–2038

    Article  PubMed  CAS  Google Scholar 

  • Vacchio MS, Papadopoulos V, Ashwell JD (1994) Steroid production in the thymus: implications for thymocyte selection. J Exp Med 179:1835–1846

    Article  PubMed  CAS  Google Scholar 

  • Wise PM, Frye BE (1973) Functional development of the hypothalamo-hypophyseal-adrenal cortex axis in the chick embryo, Gallus domesticus. J Exp Zool 185:277–292

    Article  PubMed  CAS  Google Scholar 

  • Zheng J, Nakamura K, Maseki Y, Geelissen SM, Berghman LR, Sakai T (2006) Independent differentiation of mammotropes and somatotropes in the chicken embryonic pituitary gland Analysis by cell distribution and attempt to detect somatomammotropes. Histochem Cell Biol 125:429–439

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Dr Kazuaki Nakamura (Tokyo Metropolitan Institute for Neuroscience) for helpful discussion on the study.

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Authors and Affiliations

  1. Area of Regulatory Biology, Division of Life Science, Graduate School of Science and Engineering, Saitama University, 255 Shimo-Ohkubo, Saitama, Saitama, 338-8570, Japan

    Jun Zheng, Hiroyasu Takagi, Chihiro Tsutsui, Akihito Adachi & Takafumi Sakai

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  1. Jun Zheng
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  2. Hiroyasu Takagi
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  3. Chihiro Tsutsui
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  4. Akihito Adachi
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  5. Takafumi Sakai
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Correspondence to Takafumi Sakai.

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Zheng, J., Takagi, H., Tsutsui, C. et al. Hypophyseal corticosteroids stimulate somatotrope differentiation in the embryonic chicken pituitary gland. Histochem Cell Biol 129, 357–365 (2008). https://doi.org/10.1007/s00418-007-0364-9

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  • DOI: https://doi.org/10.1007/s00418-007-0364-9

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