Endogenously elevated androgens alter the developmental programming of the hypothalamic-pituitary axis in male mice

Molecular and Cellular Endocrinology

Volumn 332, Issue 1-2, 2011, Pages 78-87

  Gonzalez, Betina ^a   Ratner, Laura D ^a   Di Giorgio, Noelia P ^a   Poutanen, Matti ^b   Huhtaniemi, Ilpo T ^b,c   Calandra, Ricardo S ^a   Lux Lantos, Victoria A R ^a   Rulli, Susana B ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSITY OF TURKU   (Finland)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Androgen; Follicle stimulating hormone; Human chorionic gonadotrophin; Hypothalamic pituitary axis; Transgenic model

Indexed keywords

ANDROGEN; ANTIANDROGEN; AROMATASE; CHORIONIC GONADOTROPIN ALPHA SUBUNIT; CHORIONIC GONADOTROPIN BETA SUBUNIT; FLUTAMIDE; FOLLITROPIN; GLUTAMATE DECARBOXYLASE 67; GONADORELIN; GONADOTROPIN; MESSENGER RNA; METASTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DEVELOPMENT; EX VIVO STUDY; FOLLITROPIN BLOOD LEVEL; GENE EXPRESSION; GESTATION PERIOD; HORMONAL REGULATION; HORMONE RELEASE; HYPOPHYSIS; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULSATILE HORMONE RELEASE; TRANSGENIC MOUSE;

ANDROGEN ANTAGONISTS; ANDROGENS; ANIMALS; AROMATASE; CASTRATION; CHORIONIC GONADOTROPIN, BETA SUBUNIT, HUMAN; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GLUTAMATE DECARBOXYLASE; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; HYPOTHALAMUS; LUTEINIZING HORMONE; MALE; MICE; MICE, TRANSGENIC; PITUITARY GLAND; PROTEINS; PUBERTY;

EID: 78650518059     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.09.016     Document Type: Article

References (59)

1. Abdelgadir S.E., Resko J.A., Ojeda S.R., Lephart E.D., McPhaul M.J., Roselli C.E. Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain. Endocrinology 1994, 135:395-401.
2. Achermann J.C., Jameson J.L. Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol. Endocrinol. 1999, 13:812-818.
3. Ahtiainen P., Rulli S.B., Shariatmadari R., Pelliniemi L.J., Toppari J., Poutanen M., Huhtaniemi I.T. Fetal but not adult Leydig cells are susceptible to adenoma formation in response to persistently high hCG level: a study on hCG overexpressing transgenic mice. Oncogene 2005, 24:7301-7309.
4. Ascoli M., Fanelli F., Segaloff D.L. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 2002, 23:141-174.
5. Bilezikjian L.M., Blount A.L., Donaldson C.J., Vale W.W. Pituitary actions of ligands of the TGF-beta family: activins and inhibins. Reproduction 2006, 132:207-215.
6. Celotti F., Negri-Cesi P., Poletti A. Steroid metabolism in the mammalian brain: 5alpha-reduction and aromatization. Brain Res. Bull. 1997, 44:365-375.
7. Cheng K.W., Ngan E.S., Kang S.K., Chow B.K., Leung P.C. Transcriptional down-regulation of human gonadotropin-releasing hormone (GnRH) receptor gene by GnRH: role of protein kinase C and activating protein 1. Endocrinology 2000, 141:3611-3622.
8. Childs G.V., Unabia G. Epidermal growth factor and gonadotropin releasing hormone stimulate proliferation of enriched population of gonadotropes. Endocrinology 2001, 142:847-853.
9. Chu Z., Andrade J., Shupnik M.A., Moenter S.M. Differential regulation of gonadotropin-releasing hormone neuron activity and membrane properties by acutely applied estradiol: dependence on dose and estrogen receptor subtype. J. Neurosci. 2009, 29:5616-5627.
10. 2+ levels. Mol. Pharmacol. 1984, 25:51-55.
11. Corbier P., Kerdelhue B., Picon R., Roffi J. Changes in testicular weight and serum gonadotropin and testosterone levels before, during, and after birth in the perinatal rat. Endocrinology 1978, 103:1985-1991.
12. Davis A.M., Grattan D.R., Selmanoff M., McCarthy M.M. Sex differences in glutamic acid decarboxylase mRNA in neonatal rat brain: implications for sexual differentiation. Horm. Behav. 1996, 30:538-552.
13. De Mees C., Laes J.F., Bakker J., Smitz J., Hennuy B., Van Vooren P., Gabant P., Szpirer J., Szpirer C. Alpha-fetoprotein controls female fertility and prenatal development of the gonadotropin-releasing hormone pathway through an antiestrogenic action. Mol. Cell. Biol. 2006, 26:2012-2018.
14. Dhar J.D., Setty B.S. Effect of flutamide, a nonsteroidal antiandrogen on testis and accessory genital organs of male rats: a reevaluation in prepubertal and adult rat. Indian J. Exp. Biol. 1987, 25:81-85.
15. Garcia-Segura L.M., Lorenz B., DonCarlos L.L. The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction 2008, 135:419-429.
16. Gore A.C. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front. Neuroendocrinol. 2008, 29:358-374.
17. Gray L.E., Wilson V.S., Stoker T., Lambright C., Furr J., Noriega N., Howdeshell K., Ankley G.T., Guillette L. Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. Int. J. Androl. 2006, 29:96-108.
18. Foster D.L., Jackson L.M., Padmanabhan V. Programming of GnRH feedback controls timing puberty and adult reproductive activity. Mol. Cell. Endocrinol. 2006, 254-255:109-119.
19. Han S.K., Gottsch M.L., Lee K.J., Popa S.M., Smith J.T., Jakawich S.K., Clifton D.K., Steiner R.A., Herbison A.E. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J. Neurosci. 2005, 25:11349-11356.
20. Heger S., Seney M., Bless E., Schwarting G.A., Bilger M., Mungenast A., Ojeda S.R., Tobet S.A. Overexpression of glutamic acid decarboxylase-67 (GAD-67) in gonadotropin-releasing hormone neurons disrupts migratory fate and female reproductive function in mice. Endocrinology 2003, 144:2566-2579.
21. Herbison A.E. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res. Rev. 2008, 57:277-287.
22. Hutchison J.B. Gender-specific steroid metabolism in neural differentiation. Cell Mol. Neurobiol. 1997, 17:603-626.
23. Kauffman A.S. Sexual differentiation and the Kiss1 system: hormonal and developmental considerations. Peptides 2009, 30:83-93.
24. Kirk S.E., Dalkin A.C., Yasin M., Haisenleder D.J., Marshall J.C. Gonadotropin-releasing hormone pulse frequency regulates expression of pituitary follistatin messenger ribonucleic acid: a mechanism for differential gonadotrope function. Endocrinology 1994, 135:876-880.
25. Kudo A., Park M.K., Kawashima S. Effects of gonadotropin-releasing hormone (GnRH) on the cytodifferentiation of gonadotropes in rat adenohypophysial primordia in organ culture. Cell Tissue Res. 1994, 276:35-43.
26. Kumar T.R., Fairchild-Huntress V., Low M.J. Gonadotrope-specific expression of the human follicle-stimulating hormone beta-subunit gene in pituitaries of transgenic mice. Mol. Endocrinol. 1992, 6:81-90.
27. Lindzey J., Wetsel W.C., Couse J.F., Stoker T., Cooper R., Korach K.S. Effects of castration and chronic steroid treatments on hypothalamic gonadotropin-releasing hormone content and pituitary gonadotropins in male wild-type and estrogen receptor-alpha knockout mice. Endocrinology 1998, 139:4092-4101.
28. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
29. McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
30. McCarthy M.M., Auger A.P., Perrit-Sinal T.S. Getting excited about GABA and sex differences in the brain. Trends Neurosc. 2002, 25:307-312.
31. Meidan R., Aroya N.B., Koch Y. Variations in the number of pituitary LHRH receptors correlated with altered responsiveness to LHRH. Life Sci. 1982, 30:535-541.
32. Mongiat L.A., Fernández M.O., Lux-Lantos V.A., Guilgur L.G., Somoza G.M., Libertun C. Experimental data supporting the expression of the highly conserved GnRH-II in the brain and pituitary gland of rats. Regul. Pept. 2006, 136:50-57.
33. Mores N., Krsmanovic L.Z., Catt K.J. Activation of LH receptors expressed in GnRH neurons stimulates cyclic AMP production and inhibits pulsatile neuropeptide release. Endocrinology 1996, 137:5731-5734.
34. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Barreiro M.L., Gaytan F., Aguilar E., Pinilla L., Dieguez C., Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KISS-1 peptide, the natural ligand of GPR54. Endocrinology 2005, 146:156-163.
35. Navarro V.M., Sánchez-Garrido M.A., Castellano J.M., Roa J., García-Galiano D., Pineda R., Aguilar E., Pinilla L., Tena-Sempere M. Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology 2009, 150:2359-2367.
36. Negri-Cesi P., Colciago A., Pravettoni A., Casati L., Conti L., Celotti F. Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences. J. Steroid. Biochem. Mol. Biol. 2008, 109:294-299.
37. Ojeda S.R., Prevot V., Heger S., Lomniczi A., Dziedzic B., Mungenast A. Glia-to-neuron signalling and the neuroendocrine control of female puberty. Ann. Med. 2003, 35:244-255.
38. Ojeda S.R., Skinner M.K. Puberty in the rat. The Physiology of Reproduction 2006, 2061-2126. Academic Press/Elsevier, San Diego, CA. 3rd ed. J.D. Neill (Ed.).
39. O'Shaughnessy P.J., Baker P., Sohnius U., Haavisto A.M., Charlton H.M., Huhtaniemi I. Fetal development of Leydig cell activity in the mouse is independent of pituitary gonadotroph function. Endocrinology 1998, 139:1141-1146.
40. O'Shaughnessy P.J., McLelland D., McBride M.W. Regulation of luteinizing hormone-receptor and follicle-stimulating hormone-receptor messenger ribonucleic acid levels during development in the neonatal mouse ovary. Biol. Reprod. 1997, 57:602-608.
41. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
42. Pielecka J., Moenter S.M. Effect of steroid milieu on gonadotropin-releasing hormone-1 neuron firing pattern and luteinizing hormone levels in male mice. Biol. Reprod. 2006, 74:931-937.
43. Purvis K., Calandra R., Haug E., Hansson V. 5alpha-reduced androgens and testicular function in the immature rat: effects of 5alpha-androstan-17beta-ol-3one (DHT) propionate and 5alpha-androstan-3alpha, 17beta-diol. Mol. Cell. Endocrinol. 1977, 7:203-219.
44. Roa J., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front. Neuroendocrinol. 2008, 29:48-69.
45. Robinson J. Prenatal programming of the female reproductive neuroendocrine system by androgens. Reproduction 2006, 132:539-547.
46. Roselli C.E. Synergistic induction of aromatase activity in the rat brain by estradiol and 5 alpha-dihydrotestosterone. Neuroendocrinology 1991, 53:79-84.
47. Rulli S.B., Gonzalez-Calvar S.I., Campo S., Calandra R.S. Effects of two non-steroidal antiandrogens on testicular function in prepubertal rats. J. Androl. 1995, 16:225-232.
48. Rulli S.B., Creus S., Pellizzari E., Cigorraga S.B., Calandra R.S., Campo S. Immunological and biological activities of pituitary FSH isoforms in prepubertal male rats: effect of antiandrogens. Neuroendocrinology 1996, 63:514-521.
49. Rulli S.B., Kuorelahti A., Karaer O., Pelliniemi L.J., Poutanen M., Huhtaniemi I. Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin. Endocrinology 2002, 143:4084-4095.
50. Rulli S.B., Ahtiainen P., Mäkelä S., Toppari J., Poutanen M., Huhtaniemi I. Elevated steroidogenesis, defective reproductive organs, and infertility in transgenic male mice overexpressing human chorionic gonadotropin. Endocrinology 2003, 144:4980-4990.
51. Sakuma Y. Gonadal steroid action and brain sex differentiation in the rat. J. Neuroendocrinol. 2009, 21:410-414.
52. Sisk L., Foster D.L. The neural basis of puberty and adolescence. Nat. Neurosci. 2004, 7:1040-1047.
53. Smith J.T., Dungan H.M., Stoll E.A., Gottsch M.L., Braun R.E., Eacker S.M., Clifton D.K., Steiner R.A. Differential regulation of Kiss-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005, 146:2976-2984.
54. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
55. Szarek E., Farrand K., McMillen I.C., Young I.R., Houghton D., Schwartz J. Hypothalamic input is required for development of normal numbers of thyrotrophs and gonadotrophs, but not other anterior pituitary cells in late gestation sheep. J. Physiol. 2008, 586:1185-1194.
56. Tena-Sempere M. Kisspeptin signaling in the brain: recent developments and future challenges. Mol. Cell. Endocrinol. 2010, 314:164-169.
57. Themmen A.P.N., Huhtaniemi I.T. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 2000, 21:551-583.
58. Veldhuis J.D., Johnson M.L. Cluster analysis: a simple versatile, and robust algorithm for endocrine pulse detection. Am. J. Physiol. 1986, 250:E486-E493.
59. Weisz J., Ward I.L. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 1980, 106:306-316.