Prenatal exposure to low levels of androgen accelerates female puberty onset and reproductive senescence in mice

Endocrinology

Volumn 153, Issue 9, 2012, Pages 4522-4532

  Witham, Emily A ^a   Meadows, Jason D ^a   Shojaei, Shadi ^a   Kauffman, Alexander S ^a   Mellon, Pamela L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROSTANOLONE; G PROTEIN COUPLED RECEPTOR 54; TESTOSTERONE;

ANDROGEN THERAPY; ANIMAL EXPERIMENT; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FEMALE FERTILITY; MORPHOLOGY; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PUBERTY; REPRODUCTION; SENESCENCE; SIGNAL TRANSDUCTION;

AGING; ANDROGENS; ANIMALS; DIHYDROTESTOSTERONE; ESTROUS CYCLE; FEMALE; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PUBERTY; REPRODUCTION;

EID: 84865438211     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1283     Document Type: Article

References (36)

1. Smith JT 2008 Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Res Rev 57:288-298 (Pubitemid 351381755)
2. Thackray VG, Mellon PL, Coss D 2010 Hormones in synergy: regulation of the pituitary gonadotropin genes. Mol Cell Endocrinol 314:192-203
3. Kauffman AS 2010 Coming of age in the kisspeptin era: sex differences, development, and puberty. Mol Cell Endocrinol 324:51-63
4. Romero CJ, Pine-Twaddell E, Radovick S 2011 Novel mutations associated with combined pituitary hormone deficiency. J Mol Endocrinol 46:R93-R102
5. Kauffman AS, Clifton DK, Steiner RA 2007 Emerging ideas about kisspeptin-GPR54 signaling in the neuroendocrine regulation of reproduction. Trends Neurosci 30:504-511 (Pubitemid 47513238)
6. Topaloglu AK, Tello JA, Kotan LD, Ozbek MN, Yilmaz MB, Erdogan S, Gurbuz F, Temiz F, Millar RP, Yuksel B 2012 Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med 366:629-635
7. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno Jr JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley Jr WF, Aparicio SA, Colledge WH 2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627 (Pubitemid 37303886)
8. Kermath BA, Gore AC 2012 Neuroendocrine control of the transition to reproductive senescence: lessons learned from the female rodent model. Neuroendocrinology 95:1-12
9. Hu YC, Wang PH, Yeh S, Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY, Chang C 2004 Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci USA 101:11209-11214 (Pubitemid 39038327)
10. Franks S, McCarthy MI, Hardy K 2006 Development of polycystic ovary syndrome: involvement of genetic and environmental factors. Int J Androl 29:278-285; discussion 286-290
11. Gore AC, Patisaul HB 2010 Neuroendocrine disruption: historical roots, current progress, questions for the future. Front Neuroendocrinol 31:395-399
12. Ibáñez L, Ferrer A, Ong K, Amin R, Dunger D, de Zegher F 2004 Insulin sensitization early after menarche prevents progression from precocious pubarche to polycystic ovary syndrome. J Pediatr 144:23-29 (Pubitemid 38091417)
13. Abbott DH, Barnett DK, Levine JE, Padmanabhan V, Dumesic DA, Jacoris S, Tarantal AF 2008 Endocrine antecedents of polycystic ovary syndrome in fetal and infant prenatally androgenized female rhesus monkeys. Biol Reprod 79:154-163 (Pubitemid 351931028)
14. Foecking EM, McDevitt MA, Acosta-Martínez M, Horton TH, Levine JE 2008 Neuroendocrine consequences of androgen excess in female rodents. Horm Behav 53:673-692
15. Manikkam M, Thompson RC, Herkimer C, Welch KB, Flak J, Karsch FJ, Padmanabhan V 2008 Developmental programming: impact of prenatal testosterone excess on pre- and postnatal gonadotropin regulation in sheep. Biol Reprod 78:648-660 (Pubitemid 351469344)
16. Simerly RB 2002 Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536 (Pubitemid 34748027)
17. Foecking EM, Szabo M, Schwartz NB, Levine JE 2005 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 72:1475-1483 (Pubitemid 40696090)
18. Sullivan SD, Moenter SM 2004 Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: implications for a common fertility disorder. Proc Natl Acad Sci USA 101:7129-7134 (Pubitemid 38596454)
19. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA, Rissman EF 2007 The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci 27:8826-8835 (Pubitemid 47292767)
20. Poling MC, Kauffman AS 2012 Sexually dimorphic testosterone secretion in prenatal and neonatal mice is independent of kisspeptin-Kiss1r and GnRH signaling. Endocrinology 153:782-793
21. Yeh S, Tsai MY, Xu Q, Mu XM, Lardy H, Huang KE, Lin H, Yeh SD, Altuwaijri S, Zhou X, Xing L, Boyce BF, Hung MC, Zhang S, Gan L, Chang C, Hung MC 2002 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 USA 99:13498-13503 (Pubitemid 35215410)
22. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF 2001 Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15:859-876 (Pubitemid 32295067)
23. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M 2007 Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148:1774-1783 (Pubitemid 46457121)
24. Ibáñez L, de Zegher F, Potau N 1998 Premature pubarche, ovarian hyperandrogenism, hyperinsulinism and the polycystic ovary syndrome: from a complex constellation to a simple sequence of prenatal onset. J Endocrinol Invest 21:558-566 (Pubitemid 28532463)
25. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972-10976 (Pubitemid 37140137)
26. Gill JC, Wang O, Kakar S, Martinelli E, Carroll RS, Kaiser UB 2010 Reproductive hormone-dependent and -independent contributions to developmental changes in kisspeptin in GnRH-deficient hypogonadal mice. PLoS One 5:e11911
27. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G 1977 Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 269:338-340 (Pubitemid 8178658)
28. Abbott DH, Barnett DK, Bruns CM, Dumesic DA 2005 Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum Reprod Update 11:357-374 (Pubitemid 40895465)
29. Nelson JF, Felicio LS, Osterburg HH, Finch CE 1981 Altered profiles of estradiol and progesterone associated with prolonged estrous cycles and persistent vaginal cornification in aging C57BL/6J mice. Biol Reprod 24:784-794 (Pubitemid 11043205)
30. Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L 2008 An alternate pathway for androgen regulation of brain function: activation of estrogen receptor β by the metabolite of dihydrotestosterone, 5α-androstane-3β, 17β-diol. Horm Behav 53:741-752
31. Casanova M, You L, Gaido KW, Archibeque-Engle S, Janszen DB, Heck HA 1999 Developmental effects of dietary phytoestrogens in Sprague-Dawley rats and interactions of genistein and daidzein with rat estrogen receptors α and β in vitro. Toxicol Sci 51:236-244 (Pubitemid 29496230)
32. Roland AV, Nunemaker CS, Keller SR, Moenter SM 2010 Prenatal androgen exposure programs metabolic dysfunction in female mice. J Endocrinol 207:213-223
33. Garcia-Segura LM, Lorenz B, DonCarlos LL 2008 The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction 135:419-429 (Pubitemid 351578148)
34. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK 2009 TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 41:354-358
35. Kimura T, Basu SL, Nandi S 1967 Nature of induced persistent vaginal cornification in mice. 3. Effects of estradiol and testosterone on vaginal epithelium in vitro. J Exp Zool 165:497-503
36. Kaku K, Fiedorek Jr FT, Province M, Permutt MA 1988 Genetic analysis of glucose tolerance in inbred mouse strains. Evidence for polygenic control. Diabetes 37:707-713 (Pubitemid 19043176)