Neuroendocrine consequences of androgen excess in female rodents

Hormones and Behavior

Volumn 53, Issue 5, 2008, Pages 673-692

  Foecking, Eileen M ^a   McDevitt, Melissa A ^a   Acosta Martínez, Maricedes ^a   Horton, Teresa H ^a   Levine, Jon E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Androgens; Epigenetic programming; Female; GnRH; LH; PCOS; Progesterone receptor; Rat

Indexed keywords

ANDROGEN; ESTROGEN; FETUIN A; FOLLITROPIN BETA SUBUNIT; GLUTATHIONE; GONADORELIN; GONADOTROPIN; LUTEINIZING HORMONE; LUTEINIZING HORMONE BETA SUBUNIT; SMAD2 PROTEIN;

DEVELOPMENTAL STAGE; EPIGENETICS; FOLLITROPIN RELEASE; GENE TARGETING; GONADORELIN RELEASE; LUTEINIZING HORMONE RELEASE; MAMMAL; NERVOUS SYSTEM; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; RODENT; SEX DIFFERENTIATION;

AGING; ANDROGENS; ANIMALS; ANIMALS, NEWBORN; FEMALE; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; MICE; NEUROSECRETORY SYSTEMS; OVULATION; RATS;

EID: 42749090715     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.12.013     Document Type: Review

References (194)

1. Abbott D., et al. Insights into the development of PCOS from studies of prenatally androgenized female rhesus monkeys. Trends Endocrinol. Metab. 9 (1998) 62l-667
2. Abbott D.H., et al. Developmental origin of polycystic ovary syndrome - a hypothesis. J. Endocrinol. 174 (2002) 1-5
3. Abbott D.H., et al. Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome?. Hum. Reprod. Update 11 (2005) 357-374
4. Abbott D.H., et al. Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod. Biol. Endocrinol. 4 (2006) 17
5. Amateau S.K., and McCarthy M.M. A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J. Neurosci. 22 (2002) 8586-8596
6. Amateau S.K., and McCarthy M.M. Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat. Neurosci. 7 (2004) 643-650
7. Attardi B., and Happe H.K. Modulation of the estradiol-induced luteinizing hormone surge by progesterone or antiestrogens: effects on pituitary gonadotropin-releasing hormone receptors. Endocrinology 119 (1986) 274-283
8. Auger A.P., et al. Expression of the nuclear receptor coactivator, cAMP response element-binding protein, is sexually dimorphic and modulates sexual differentiation of neonatal rat brain. Endocrinology 143 (2002) 3009-3016
9. Barraclough C.A. Production of anovulatory, sterile rats by single injections of testosterone propionate. Endocrinology 68 (1961) 62-67
10. Barraclough C.A., and Gorski R.A. Evidence that the hypothalamus is responsible for androgen-induced sterility in the female rat. Endocrinology 68 (1961) 68-79
11. Barraclough C.A., and Haller E.W. Positive and negative feedback effects of estrogen on pituitary LH synthesis and release in normal and androgen-sterilized rats. Endocrinology 86 (1970) 542-551
12. Bauer-Dantoin A.C., et al. Roles of estrogen, progesterone, and gonadotropin-releasing hormone (GnRH) in the control of pituitary GnRH receptor gene expression at the time of the preovulatory gonadotropin surges. Endocrinology 136 (1995) 1014-1019
13. Baum M.J., et al. Immediate postnatal rise in whole body androgen content in male rats: correlation with increased testicular content and reduced body clearance of testosterone. Biol. Reprod. 38 (1988) 980-986
14. Baum M.J., et al. Sex difference in whole-body androgen content in rats on fetal days 18 and 19 without evidence that androgen passes from males to females. Biol. Reprod. 44 (1991) 747-751
15. Becker J.B., et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146 (2005) 1650-1673
16. Becu-Villalobos D., et al. Brain sexual differentiation and gonadotropins secretion in the rat. Cell Mol. Neurobiol. 17 (1997) 699-715
17. Belsham D.D., et al. Regulation of gonadotropin-releasing hormone (GnRH) gene expression by 5alpha-dihydrotestosterone in GnRH-secreting GT1-7 hypothalamic neurons. Endocrinology 139 (1998) 1108-1114
18. Birch R.A., et al. Prenatal programming of reproductive neuroendocrine function: fetal androgen exposure produces progressive disruption of reproductive cycles in sheep. Endocrinology 144 (2003) 1426-1434
19. Blackwell R.E., and Amoss Jr. M.S. A sex difference in the rate of rise of plasma LH in rats following gonadectomy. Proc. Soc. Exp. Biol. Med. 136 (1971) 11-14
20. Blank S.K., et al. Neuroendocrine effects of androgens in adult polycystic ovary syndrome and female puberty. Semin. Reprod. Med. 25 (2007) 352-359
21. Blank S.K., et al. The origins and sequelae of abnormal neuroendocrine function in polycystic ovary syndrome. Hum. Reprod. Update. 12 (2006) 351-361
22. Bloch G.J., and Gorski R.A. Estrogen/progesterone treatment in adulthood affects the size of several components of the medial preoptic area in the male rat. J. Comp. Neurol. 275 (1988) 613-622
23. Bousios S., et al. Effects of gender and stress on the regulation of steroid receptor coactivator-1 expression in the rat brain and pituitary. J. Steroid Biochem. Mol. Biol. 78 (2001) 401-407
24. Brann D.W., et al. gamma-Aminobutyric acid-opioid interactions in the regulation of gonadotropin secretion in the immature female rat. Neuroendocrinology 56 (1992) 445-452
25. Brown T.J., et al. Regional sex differences in progestin receptor induction in the rat hypothalamus: effects of various doses of estradiol benzoate. J. Neurosci. 7 (1987) 2529-2536
26. Brown W.M., et al. Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Horm. Behav. 42 (2002) 380-386
27. Bruns C.M., et al. Prenatal androgen excess negatively impacts body fat distribution in a nonhuman primate model of polycystic ovary syndrome. Int. J. Obes. (Lond). 31 (2007) 1579-1585
28. Burger L.L., et al. The regulation of FSHbeta transcription by gonadal steroids: testosterone and estradiol modulation of the activin intracellular signaling pathway. Am. J. Physiol. Endocrinol. Metab. 293 (2007) E277-E285
29. Caraty A., and Locatelli A. Effect of time after castration on secretion of LHRH and LH in the ram. J. Reprod. Fertil. 82 (1988) 263-269
30. Cardona-Gomez G.P., et al. Estrogen receptors and insulin-like growth factor-I receptors mediate estrogen-dependent synaptic plasticity. Neuroreport 11 (2000) 1735-1738
31. Carruth L.L., et al. Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5 (2002) 933-934
32. Cattrall F.R., et al. Anatomical evidence for in utero androgen exposure in women with polycystic ovary syndrome. Fertil. Steril. 84 (2005) 1689-1692
33. Chappel S.C., and Barraclough C.A. Plasma concentration changes in LH and FSH following electrochemical stimulation of the medial preoptic are or dorsal anterior hypothalamic area of estrogen- or androgen-sterilized rats. Biol. Reprod. 15 (1976) 661-669
34. Chappell P.E., et al. Stimulation of gonadotropin-releasing hormone surges by estrogen. II. Role of cyclic adenosine 3′5′-monophosphate. Endocrinology 141 (2000) 1486-1492
35. Chappell P.E., and Levine J.E. Stimulation of gonadotropin-releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 141 (2000) 1477-1485
36. Chappell P.E., et al. Endocrine defects in mice carrying a null mutation for the progesterone receptor gene. Endocrinology 138 (1997) 4147-4152
37. Chappell P.E., et al. Absence of gonadotropin surges and gonadotropin-releasing hormone self-priming in ovariectomized (OVX), estrogen (E2)-treated, progesterone receptor knockout (PRKO) mice. Endocrinology 140 (1999) 3653-3658
38. Chung W.C., et al. Apoptosis during sexual differentiation of the bed nucleus of the stria terminalis in the rat brain. J. Neurobiol. 43 (2000) 234-243
39. Clay C.M., et al. Transcriptional repression of the glycoprotein hormone alpha subunit gene by androgen may involve direct binding of androgen receptor to the proximal promoter. J. Biol. Chem. 268 (1993) 13556-13564
40. Colciago A., et al. Dimorphic expression of testosterone metabolizing enzymes in the hypothalamic area of developing rats. Brain Res. Dev. Brain Res. 155 (2005) 107-116
41. Corbier P. Sexual differentiation of positive feedback: effect of hour of castration at birth on estradiol-induced luteinizing hormone secretion in immature male rats. Endocrinology 116 (1985) 142-147
42. Cui Y., et al. Phosphorylation of estrogen receptor alpha blocks its acetylation and regulates estrogen sensitivity. Cancer Res. 64 (2004) 9199-9208
43. Dohler K.D., and Wuttke W. Changes with age in levels of serum gonadotropins, prolactin and gonadal steroids in prepubertal male and female rats. Endocrinology 97 (1975) 898-907
44. Dohler K.D., et al. Pre- and postnatal influence of testosterone propionate and diethylstilbestrol on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res. 302 (1984) 291-295
45. Drouin J., and Labrie F. Selective effect of androgens on LH and FSH release in anterior pituitary cells in culture. Endocrinology 98 (1976) 1528-1534
46. Drouva S.V., et al. Effects of ovarian steroids on in vitro release of LHRH from mediobasal hypothalamus. Neuroendocrinology 37 (1983) 336-341
47. Dumesic D.A., et al. Prenatal exposure of female rhesus monkeys to testosterone propionate increases serum luteinizing hormone levels in adulthood. Fertil. Steril. 67 (1997) 155-163
48. Dumesic D.A., et al. Impaired developmental competence of oocytes in adult prenatally androgenized female rhesus monkeys undergoing gonadotropin stimulation for in vitro fertilization. J. Clin. Endocrinol. Metab. 87 (2002) 1111-1119
49. Dunaif A., and Thomas A. Current concepts in the polycystic ovary syndrome. Annu. Rev. Med. 52 (2001) 401-419
50. Dunlap K.D., and Sridaran R. Plasma levels of dihydrotestosterone in the cycling rat: implications for the regulation of lordosis behavior. Physiol. Behav. 42 (1988) 199-202
51. Eagleson C.A., et al. Polycystic ovarian syndrome: evidence that flutamide restores sensitivity of the gonadotropin-releasing hormone pulse generator to inhibition by estradiol and progesterone. J. Clin. Endocrinol. Metab. 85 (2000) 4047-4052
52. Eldridge J.C., et al. Effects of castration of immature rats on serum FSH and LH, and of various steroid treatments after castration. Biol. Reprod. 10 (1974) 438-446
53. Ellis G.B., et al. Control of pulsatile LH release in male rats. Neuroendocrinology 37 (1983) 177-183
54. Emons G., et al. Effects of progesterone on gonadotropin-releasing hormone receptor concentration in cultured estrogen-primed female rat pituitary cells. J. Steroid Biochem. Mol. Biol. 42 (1992) 831-839
55. Fels E., and Bosch L. Effect of prenatal administration of testosterone on ovarian function in rats. Am. J. Obstet. Gynecol. 111 (1971) 964-969
56. Fink G. The self-priming effect of LHRH: a unique servomechanism and possible cellular model for memory. Front Neuroendocrinol. 16 (1995) 183-190
57. Foecking E. The pathophysiological effects of androgens on female reproduction and metabolism in the rat. Neurobiology and Physiology (2006), Northwestern University, Evanston 230 Vol. PhD
58. Foecking E.M., and Levine J.E. Effects of experimental hyperandrogenemia on the female rat reproductive axis: suppression of progesterone-receptor messenger RNA expression in the brain and blockade of luteinizing hormone surges. Gend. Med. 2 (2005) 155-165
59. Foecking E.M., et al. Neuroendocrine consequences of prenatal androgen exposure in the female rat: absence of luteinizing hormone surges, suppression of progesterone receptor gene expression, and acceleration of the gonadotropin-releasing hormone pulse generator. Biol. Reprod. 72 (2005) 1475-1483 (2005 Mar 2, Electronic publication ahead of print)
60. Forger N.G., et al. Deletion of Bax eliminates sex differences in the mouse forebrain. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13666-13671
61. Garcia-Segura L.M., et al. Neuroprotection by estradiol. Prog. Neurobiol. 63 (2001) 29-60
62. Gaveriaux-Ruff C., and Kieffer B.L. Conditional gene targeting in the mouse nervous system: Insights into brain function and diseases. Pharmacol. Ther. 113 (2007) 619-634
63. Giguere V., et al. Androgens decrease LHRH binding sites in rat anterior pituitary cells in culture. Endocrinology 108 (1981) 350-352
64. Glidewell-Kenney C., et al. Nonclassical estrogen receptor alpha signaling mediates negative feedback in the female mouse reproductive axis. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 8173-8177
65. Gogan F., et al. Effect of neonatal administration of steroids or gonadectomy upon oestradiol-induced luteinizing hormone release in rats of both sexes. J. Endocrinol 85 (1980) 69-74
66. Goomer N., et al. Effect of neonatal testosterone and oestradiol treatment on the development of the hypothalamo-hypophysial axis in the female rat. J. Reprod. Fertil. 50 (1977) 239-243
67. Gorski R.A. Sexual dimorphisms of the brain. J. Anim. Sci. 61 (1985) 38-61
68. Gorski R.A., et al. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 148 (1978) 333-346
69. Goy R.W., et al. Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm. Behav. 22 (1988) 552-571
70. Gu G., et al. Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J. Comp. Neurol. 460 (2003) 542-562
71. Gu G.B., and Simerly R.B. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J. Comp. Neurol. 384 (1997) 142-164
72. Haisenleder D.J., et al. Gonadotropin subunit and gonadotropin-releasing hormone receptor gene expression are regulated by alterations in the frequency of calcium pulsatile signals. Endocrinology 138 (1997) 5227-5230
73. Handa R.J., et al. Gonadotropin secretion following intraventricular norepinephrine infusion into neonatally androgenized female rats. Neuroendocrinology 43 (1986) 269-272
74. Hart B.L. Neonatal castration: influence on neural organization of sexual reflexes in male rats. Science 160 (1968) 1135-1136
75. Hassani M., et al. Action of testosterone propionate on the gonadotropic function of the pituitary gland in the cyclic female rat. Acta. Endocrinol. (Copenh). 89 (1978) 551-556
76. Henderson R.G., et al. Sex differences in cell migration in the preoptic area/anterior hypothalamus of mice. J. Neurobiol. 41 (1999) 252-266
77. Henderson S.R., et al. Proceedings: effect of precise oestradiol-17 beta exposure on the gonadotrophin response to luteinizing hormone releasing factor and the spontaneous secretion of luteinizing hormone in acutely and chronically ovariectomized rats. J. Endocrinol. 69 (1976) 1P-2P
78. Herbison A.E. Neurochemical identity of neurones expressing oestrogen and androgen receptors in sheep hypothalamus. J. Reprod. Fertil. Suppl. 49 (1995) 271-283
79. Hiatt E.S., et al. Sex differences following gonadectomy in basal gonadotropin secretion rate of rat pituitary fragments in vitro. Biol. Reprod. 37 (1987) 1114-1120
80. Hrabovszky E., et al. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 141 (2000) 3506-3509
81. Huffman L., and Hendricks S.E. Prenatally injected testosterone propionate and sexual behavior of female rats. Physiol. Behav. 26 (1981) 773-778
82. Jackson G.L., et al. Testosterone inhibits gonadotropin-releasing hormone pulse frequency in the male sheep. Biol. Reprod. 45 (1991) 188-194
83. Jakacka M., et al. An estrogen receptor (ER)alpha deoxyribonucleic acid-binding domain knock-in mutation provides evidence for nonclassical ER pathway signaling in vivo. Mol. Endocrinol. 16 (2002) 2188-2201
84. Kamel F., and Krey L.C. Gonadal steroid modulation of LH secretion stimulated by LHRH, Ca2+ and cAMP. Mol. Cell Endocrinol. 32 (1983) 285-300
85. Kamel F., and Kubajak C.L. Modulation of gonadotropin secretion by corticosterone: interaction with gonadal steroids and mechanism of action. Endocrinology 121 (1987) 561-568
86. Kamel F., and Kubajak C.L. Gonadal steroid effects on LH response to arachidonic acid and protein kinase C. Am. J. Physiol. 255 (1988) E314-E321
87. Kamel F., et al. Gonadal steroids modulate pulsatile luteinizing hormone secretion by perifused rat anterior pituitary cells. Endocrinology 120 (1987) 1651-1657
88. Kauffman A.S., et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148 (2007) 1774-1783
89. King J.C.T., S.A., Snavely F.L., and Arimura A.A. The LHRH system in normal and neonatally androgenized female rats. Peptides 1 (1985) 85-100
90. Knobil E. Patterns of hypophysiotropic signals and gonadotropin secretion in the rhesus monkey. Biol. Reprod. 24 (1981) 44-49
91. Korenbrot C.C., et al. Effects of testosterone propionate or dihydrotestosterone propionate on plasma FSH and LH levels in neonatal rats and on sexual differentiation of the brain. Endocrinology 97 (1975) 709-717
92. Kubo K., et al. Similarity of plasma LH release in androgenized and normal rats following electrochemical stimulation of the basal forebrain. Endocrinology 96 (1975) 492-500
93. Kudwa A.E., et al. Roles of estrogen receptors alpha and beta in differentiation of mouse sexual behavior. Neuroscience 138 (2006) 921-928
94. Landys M.M., et al. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol. 148 (2006) 132-149
95. Lapidus R.G., et al. Methylation of estrogen and progesterone receptor gene 5′ CpG islands correlates with lack of estrogen and progesterone receptor gene expression in breast tumors. Clin. Cancer Res. 2 (1996) 805-810
96. Larsson K. Effects of neonatal castration upon the development of the mating behavior of the male rat. Z. Tierpsychol. 23 (1966) 867-873
97. Lauber A.H., et al. Sex difference in estradiol regulation of progestin receptor mRNA in rat mediobasal hypothalamus as demonstrated by in situ hybridization. Neuroendocrinology 53 (1991) 608-613
98. Leader J.E., et al. Epigenetic regulation of nuclear steroid receptors. Biochem. Pharmacol. 72 (2006) 1589-1596
99. Legan S.J., and Karsch F.J. A daily signal for the LH surge in the rat. Endocrinology 96 (1975) 57-62
100. Legan S.J., et al. Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 96 (1975) 50-56
101. Legro R.S., et al. Prevalence and predictors of risk for type 2 diabetes mellitus and impaired glucose tolerance in polycystic ovary syndrome: a prospective, controlled study in 254 affected women. J. Clin. Endocrinol. Metab. 84 (1999) 165-169
102. Leipheimer R.E., and Gallo R.V. Acute and long-term changes in central and pituitary mechanisms regulating pulsatile luteinizing hormone secretion after ovariectomy in the rat. Neuroendocrinology 37 (1983) 421-426
103. Levine J.E. New concepts of the neuroendocrine regulation of gonadotropin surges in rats. Biol. Reprod. 56 (1997) 293-302
104. Levine J.E., and Duffy M.T. Simultaneous measurement of luteinizing hormone (LH)-releasing hormone, LH, and follicle-stimulating hormone release in intact and short-term castrate rats. Endocrinology 122 (1988) 2211-2221
105. Levine J.E., and Ramirez V.D. Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology 111 (1982) 1439-1448
106. Liaw J.J., and Barraclough C.A. N-methyl-d, l-aspartic acid differentially affects Lh-release and Lhrh messenger-Rna levels in estrogen-treated ovariectomized control and androgen-sterilized rats. Molecular Brain Research 17 (1993) 112-118
107. Liaw J.J., and Barraclough C.A. Pituitary gland responsiveness to LHRH and LHRH neuronal responsiveness to excitatory stimuli are severely impaired in female rats treated neonatally with high doses of androgen. Brain Res. 607 (1993) 233-240
108. Lindzey J., et al. 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 139 (1998) 4092-4101
109. Lund T.D., et al. Dihydrotestosterone may inhibit hypothalamo-pituitary-adrenal activity by acting through estrogen receptor in the male mouse. Neurosci. Lett. 365 (2004) 43-47
110. Lund T.D., et al. Pre- or postnatal testosterone and flutamide effects on sexually dimorphic nuclei of the rat hypothalamus. Brain Res. Dev. Brain Res. 120 (2000) 261-266
111. Mani S.K. Signaling mechanisms in progesterone-neurotransmitter interactions. Neuroscience 138 (2006) 773-781
112. Manneras L., et al. A new rat model exhibiting both ovarian and metabolic characteristics of polycystic ovary syndrome. Endocrinology 148 (2007) 3781-3791
113. Masek K.S., et al. Prenatal dihydrotestosterone differentially masculinizes tonic and surge modes of luteinizing hormone secretion in sheep. Endocrinology 140 (1999) 3459-3466
114. McAbee M.D., and DonCarlos L.L. Ontogeny of region-specific sex differences in androgen receptor messenger ribonucleic acid expression in the rat forebrain. Endocrinology 139 (1998) 1738-1745
115. McEwen B.S., and Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 43 (2003) 2-15
116. McGinnis M.Y., et al. In vitro measurement of cytosol and cell nuclear androgen receptors in male rat brain and pituitary. Brain Res. 275 (1983) 75-82
117. Meredith J.M., and Levine J.E. Effects of castration on LH-RH patterns in intrahypophysial microdialysates. Brain Res. 571 (1992) 181-188
118. Moguilevsky J.A., et al. Effect of castration on serum gonadotropin levels in androgenized male and female rats. Neuroendocrinology 29 (1979) 323-328
119. Mong J.A., et al. Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J. Neurosci. 19 (1999) 1464-1472
120. Naik S.I., et al. Pituitary gonadotropin-releasing hormone receptor regulation in mice. I: Males. Endocrinology 115 (1984) 106-113
121. Nansel D.D., and Trent D.F. Frequency modulation of pulsatile luteinizing hormone-releasing hormone stimulation can alter the effectiveness of direct androgen feedback on luteinizing hormone-releasing hormone-induced luteinizing hormone release. Endocrinology 104 (1979) 532-535
122. Navarro C.E., et al. Regulation of cyclic adenosine 3′,5′-monophosphate signaling and pulsatile neurosecretion by Gi-coupled plasma membrane estrogen receptors in immortalized gonadotropin-releasing hormone neurons. Mol. Endocrinol. 17 (2003) 1792-1804 (2003 Jun 20, Electronic publication ahead of print)
123. Pang S.F., et al. Serum concentrations of testosterone, oestrogens, luteinizing hormone and follicle-stimulating hormone in male and female rats during the critical period of neural sexual differentiation. J. Endocrinol. 80 (1979) 103-110
124. Pastor C.L., et al. Polycystic ovary syndrome: evidence for reduced sensitivity of the gonadotropin-releasing hormone pulse generator to inhibition by estradiol and progesterone. J. Clin. Endocrinol. Metab. 83 (1998) 582-590
125. Pelletier G., et al. Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J. Endocrinol. 165 (2000) 359-370
126. Petersen S.L., and Barraclough C.A. Effect of naloxone and morphine on LH and prolactin release in androgen-sterilized rats. Neuroendocrinology 44 (1986) 84-88
127. Petersen S.L., and Barraclough C.A. Suppression of spontaneous LH surges in estrogen-treated ovariectomized rats by microimplants of antiestrogens into the preoptic brain. Brain Res. 484 (1989) 279-289
128. Petersen S.L., et al. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol. Reprod. 69 (2003) 1771-1778
129. Pielecka J., and Moenter S.M. Effect of steroid milieu on gonadotropin-releasing hormone-1 neuron firing pattern and luteinizing hormone levels in male mice. Biol. Reprod. 74 (2006) 931-937
130. Poletti A., et al. Steroid binding and metabolism in the luteinizing hormone-releasing hormone-producing neuronal cell line GT1-1. Endocrinology 135 (1994) 2623-2628
131. Rainbow T.C., et al. Sex differences in rat brain oestrogen and progestin receptors. Nature 300 (1982) 648-649
132. Recabarren S.E., et al. Postnatal developmental consequences of altered insulin sensitivity in female sheep treated prenatally with testosterone. Am. J. Physiol. Endocrinol. Metab. 289 (2005) E801-E806
133. Resko J.A., and Roselli C.E. Prenatal hormones organize sex differences of the neuroendocrine reproductive system: observations on guinea pigs and nonhuman primates. Cell Mol. Neurobiol. 17 (1997) 627-648
134. Rhees R.W., et al. Effects of prenatal testosterone on sexual behavior, reproductive morphology and LH secretion in the female rat. Dev. Neurosci. 19 (1997) 430-437
135. Rhoda J., et al. Gonadal steroid concentrations in serum and hypothalamus of the rat at birth: aromatization of testosterone to 17 beta-estradiol. Endocrinology 114 (1984) 1754-1760
136. Robinson J. Prenatal programming of the female reproductive neuroendocrine system by androgens. Reproduction 132 (2006) 539-547
137. Robinson J.E., et al. In utero exposure of female lambs to testosterone reduces the sensitivity of the gonadotropin-releasing hormone neuronal network to inhibition by progesterone. Endocrinology 140 (1999) 5797-5805
138. Ronnekleiv O.K., and Kelly M.J. Diversity of ovarian steroid signaling in the hypothalamus. Front Neuroendocrinol 26 (2005) 65-84
139. Roos J., et al. Mechanisms of action of testosterone propionate on LH and FSH release by the pituitary gland in cyclic female rats. Acta. Endocrinol. (Copenh). 95 (1980) 158-165
140. Roselli C.E., et al. Quantitative distribution of nuclear androgen receptors in microdissected areas of the rat brain. Neuroendocrinology 49 (1989) 449-453
141. Rosenfield R.L. Current concepts of polycystic ovary syndrome. Baillieres Clin. Obstet. Gynaecol. 11 (1997) 307-333
142. Roy D., et al. Estrogen directly represses gonadotropin-releasing hormone (GnRH) gene expression in estrogen receptor-alpha (ERalpha)- and ERbeta-expressing GT1-7 GnRH neurons. Endocrinology 140 (1999) 5045-5053
143. Rudick C.N., and Woolley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J. Neurosci. 21 (2001) 6532-6543
144. Rush M.E., and Blake C.A. Serum testosterone concentrations during the 4-day estrous cycle in normal and adrenalectomized rats. Proc. Soc. Exp. Biol. Med. 169 (1982) 216-221
145. Ryan B.C., and Vandenbergh J.G. Intrauterine position effects. Neurosci. Biobehav. Rev. 26 (2002) 665-678
146. Sam S., and Dunaif A. Polycystic ovary syndrome: syndrome XX?. Trends Endocrinol Metab. 14 (2003) 365-370
147. Sarma H.N., et al. Fetal programming: excess prenatal testosterone reduces postnatal luteinizing hormone, but not follicle-stimulating hormone responsiveness, to estradiol negative feedback in the female. Endocrinology 146 (2005) 4281-4291 (2005 Jun 23, Electronic publication ahead of print)
148. Shakil T., et al. Differential regulation of gonadotropin-releasing hormone secretion and gene expression by androgen: membrane versus nuclear receptor activation. Mol. Endocrinol. 16 (2002) 2592-2602
149. Shiina H., et al. Premature ovarian failure in androgen receptor-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 224-229
150. Shupnik M.A. Gonadotropin gene modulation by steroids and gonadotropin-releasing hormone. Biol. Reprod. 54 (1996) 279-286
151. Siddiqui A., and Shah B.H. Neonatal androgen manipulation differentially affects the development of monoamine systems in rat cerebral cortex, amygdala and hypothalamus. Brain Res. Dev. Brain Res. 98 (1997) 247-252
152. Simerly R.B. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav. Brain Res. 92 (1998) 195-203
153. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25 (2002) 507-536
154. Simerly R.B. Wired on hormones: endocrine regulation of hypothalamic development. Curr. Opin. Neurobiol. 15 (2005) 81-85
155. Simerly R.B., et al. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 294 (1990) 76-95
156. Simerly R.B., et al. The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res. 330 (1985) 55-64
157. Skynner M.J., et al. Detection of estrogen receptor alpha and beta messenger ribonucleic acids in adult gonadotropin-releasing hormone neurons. Endocrinology 140 (1999) 5195-5201
158. Slob A.K., et al. Prenatal testosterone propionate and postnatal ovarian activity in the rat. Acta. Endocrinol. (Copenh). 103 (1983) 420-427
159. Slob A.K., et al. Prenatal and early postnatal sex differences in plasma and gonadal testosterone and plasma luteinizing hormone in female and male rats. J. Endocrinol. 87 (1980) 81-87
160. Smith J.T., et al. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146 (2005) 3686-3692
161. Smith J.T., et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146 (2005) 2976-2984
162. Smith J.T., et al. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J. Neurosci. 26 (2006) 6687-6694
163. Smith M.J., and Jennes L. Neural signals that regulate GnRH neurones directly during the oestrous cycle. Reproduction 122 (2001) 1-10
164. Steiner R.A., et al. Sexual differentiation and feedback control of luteinizing hormone secretion in the rhesus monkey. Biol. Reprod. 15 (1976) 206-212
165. Sullivan S.D., and Moenter S.M. Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: implications for a common fertility disorder. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 7129-7134 (2004 Apr 19, Electronic publication ahead of print)
166. Swanson H., and van der Werff ten Bosch J. The "early-androgen" syndrome; differences in response to pre-natal and postnatal administration of various doses of testosterone propionate in female and male rats. Acta. Endocrinol. (Copenh). 47 (1964) 37-50
167. Swanson H., and van der Werff ten Bosch J. The "early-androgen" syndrome: effects of pre-natal testosterone propionate. Acta. Endocrinol. (Copenh) 50 (1965) 379-390
168. Taga M., et al. Effects of sex steroid hormones on rat anterior pituitary LH-RH receptor. Nippon Sanka Fujinka Gakkai Zasshi 34 (1982) 627-633
169. Tarttelin M.F., and Gorski R.A. Postnatal influence of diethylstilbestrol on the differentiation of the sexually dimorphic nucleus in the rat is as effective as perinatal treatment. Brain Res. 456 (1988) 271-274
170. Temple J.L., et al. Direct action of estradiol on gonadotropin-releasing hormone-1 neuronal activity via a transcription-dependent mechanism. J. Neurosci. 24 (2004) 6326-6333
171. Thornton J. Effects of Prenatal Androgens on Adult Ovarian Cyclicity and Female Sexual Behavior in the Rhesus Monkey (1983), University of Wisconsin, Madison Vol. PhD
172. Tsukahara S. Increased Fos immunoreactivity in suprachiasmatic nucleus before luteinizing hormone surge in estrogen-treated ovariectomized female rats. Neuroendocrinology 83 (2006) 303-312
173. Turgeon J.L., and Waring D.W. Androgen modulation of luteinizing hormone secretion by female rat gonadotropes. Endocrinology 140 (1999) 1767-1774
174. Unsworth W.P., et al. Prenatal programming of reproductive neuroendocrine function: the effect of prenatal androgens on the development of estrogen positive feedback and ovarian cycles in the ewe. Biol. Reprod. 72 (2005) 619-627
175. Urban J.H., et al. Steroid modulation of neuropeptide Y-induced luteinizing hormone releasing hormone release from median eminence fragments from male rats. Neuroendocrinology 63 (1996) 112-119
176. Van der Beek E.M., et al. Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: combined tracing and light and electron microscopic immunocytochemical studies. J. Comp. Neurol. 384 (1997) 569-579
177. Watson Jr. R.E., et al. Estrogen-receptive neurons in the anteroventral periventricular nucleus are synaptic targets of the suprachiasmatic nucleus and peri-suprachiasmatic region. Brain Res. 689 (1995) 254-264
178. Watts A.G., and Fink G. Pulsatile luteinizing hormone release, and the inhibitory effect of estradiol-17 beta in gonadectomized male and female rats: effects of neonatal androgen or exposure to constant light. Endocrinology 115 (1984) 2251-2259
179. Weigel R.J., and deConinck E.C. Transcriptional control of estrogen receptor in estrogen receptor-negative breast carcinoma. Cancer Res. 53 (1993) 3472-3474
180. Weiland N.G., and Barraclough C.A. Neonatal castration of male and female rats affects luteinizing hormone responses to estrogen during adulthood. Biol. Reprod. 31 (1984) 942-949
181. Weisz J., and Ward I.L. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology. 106 (1980) 306-316
182. West C., et al. Intra-follicular activin availability is altered in prenatally-androgenized lambs. Mol. Cell Endocrinol. 185 (2001) 51-59
183. Whalen R.E., and Luttge W.G. Perinatal administration of dihydrotestosterone to female rats and the development of reproductive function. Endocrinology 89 (1971) 1320-1322
184. Wiegand S.J., and Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34 (1982) 395-404
185. Wierman M.E., et al. Selective failure of androgens to regulate follicle stimulating hormone beta messenger ribonucleic acid levels in the male rat. Mol. Endocrinol. 2 (1988) 492-498
186. Wierman M.E., et al. Divergent regulation of gonadotropin subunit mRNA levels by androgens in the female rat. Biol. Reprod. 43 (1990) 191-195
187. Winters S.J., et al. Effects of testosterone on gonadotropin subunit messenger ribonucleic acids in the presence or absence of gonadotropin-releasing hormone. Endocrinology 130 (1992) 726-734
188. Wood R.I., and Foster D.L. Sexual differentiation of reproductive neuroendocrine function in sheep. Rev. Reprod. 3 (1998) 130-140
189. Xita N., and Tsatsoulis A. Review: fetal programming of polycystic ovary syndrome by androgen excess: evidence from experimental, clinical, and genetic association studies. J. Clin. Endocrinol. Metab. 91 (2006) 1660-1666
190. Yamane K., et al. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125 (2006) 483-495
191. Yan L., et al. Role of DNA methylation and histone acetylation in steroid receptor expression in breast cancer. J. Mammary Gland Biol. Neoplasia 6 (2001) 183-192
192. Yasin M., et al. Testosterone is required for gonadotropin-releasing hormone stimulation of luteinizing hormone-beta messenger ribonucleic acid expression in female rats. Endocrinology 137 (1996) 1265-1271
193. Yeh S., et al. Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13498-13503 (2002 Oct 7, Electronic publication ahead of print)
194. Zup S.L., et al. Overexpression of bcl-2 reduces sex differences in neuron number in the brain and spinal cord. J. Neurosci. 23 (2003) 2357-2362