Hormonal programming across the lifespan

Hormone and Metabolic Research

Volumn 44, Issue 8, 2012, Pages 577-586

  Nugent, B M ^a   Tobet, S A ^b   Lara, H E ^c   Lucion, A B ^d   Wilson, M E ^e   Recabarren, S E ^f   Paredes, A H ^c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c UNIVERSITY OF CHILE   (Chile)

^d Departamento de Fisiologia   (Brazil)

^e UNIVERSITY OF KENTUCKY   (United States)

^f UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

aging; brain; development; gonadal hormones; ovary; stress

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; ANDROSTANOLONE; DNA METHYLTRANSFERASE 3A; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FOLLITROPIN; GONADORELIN; HISTONE ACETYLTRANSFERASE; LUTEINIZING HORMONE RECEPTOR; METHYL CPG BINDING PROTEIN 2; NERVE GROWTH FACTOR; PROGESTERONE; PROTIRELIN; SEX HORMONE; TESTOSTERONE; TRANSCRIPTION FACTOR;

ADULTHOOD; AGING; BODY MASS; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN NUCLEUS; CONGENITAL ADRENAL HYPERPLASIA; DNA METHYLATION; EPIGENETICS; FEMALE INFERTILITY; FETUS DEVELOPMENT; GENE EXPRESSION; GENOMICS; GLIA; GONAD DEVELOPMENT; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; LIFESPAN; MALE GENITAL SYSTEM; NERVE CELL; NERVE CONDUCTION; NONHUMAN; OVARY; OVARY FUNCTION; OVARY POLYCYSTIC DISEASE; PARAVENTRICULAR THALAMIC NUCLEUS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; REVIEW; SERTOLI CELL; SEX DIFFERENCE; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; SPERMATOGONIUM; STRESS; SYMPATHETIC NERVE; SYNAPTOGENESIS; TRANSPORT AT THE CELLULAR LEVEL; VASCULARIZATION;

AGING; ANIMALS; BRAIN; EPIGENESIS, GENETIC; GROWTH AND DEVELOPMENT; HORMONES; HUMANS; REPRODUCTION;

ANIMALIA;

EID: 84863779694     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0032-1312593     Document Type: Review

References (125)

1. Tsai H W, Grant P A, Rissman E F. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics: 2009; 4 47 53
2. Rhees R W, Shryne J E, Gorski R A. Onset of the hormone-sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats. J Neurobiol: 1990; 21 781 786 (Pubitemid 20241547)
3. Arnold A P, Gorski R A. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci: 1984; 7 413 442 (Pubitemid 14155304)
4. Bakker J, De Mees C, Douhard Q, Balthazart J, Gabant P, Szpirer J, Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat Neurosci: 2006; 9 220 226 (Pubitemid 43164545)
5. McEwen B S, Lieberburg I, Chaptal C, Krey L C. Aromatization: important for sexual differentiation of the neonatal rat brain. Horm Behav: 1977; 9 249 263 (Pubitemid 8292758)
6. McCarthy M M. Estradiol and the developing brain. Physiol Rev: 2008; 88 91 134
7. Thornton J, Zehr J L, Loose M D. Effects of prenatal androgens on rhesus monkeys: A model system to explore the organizational hypothesis in primates. Horm Behav: 2009; 55 633 644
8. Bonthuis P, Cox K, Searcy B, Kumar P, Tobet S, Rissman E. Of mice and rats: key species variations in the sexual differentiation of brain and behavior. Front Neuroendocrinol: 2010; 31 341 358
9. Green S, Walter P, Kumar V, Krust A, Bornert J M, Argos P, Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature: 1986; 320 134 135
10. Shughrue P J, Lane M V, Merchenthaler I. Comparative distribution of estrogen receptor α and β mRNA in the rat central nervous system. J Comp Neurol: 1997; 388 507 525 (Pubitemid 27481288)
11. Österlund M K, Grandien K, Keller E, Hurd Y L. The human brain has distinct regional expression patterns of estrogen receptor α mRNA isoforms derived from alternative promoters. J Neurochem: 2000; 75 1390 1397
12. Prewitt A K, Wilson M E. Changes in estrogen receptor-alpha mRNA in the mouse cortex during development. Brain Res: 2007; 1134 62 69 (Pubitemid 46135541)
13. Simerly R, Swanson L, Chang C, Muramatsu M. Distribution of androgen and estrogen receptor mRNA containing cells in the rat brain: an in situ hybridization study. J Comp Neurol: 1990; 294 76 95 (Pubitemid 20104631)
14. Sheridan P J. Estrogen binding in the neonatal neocortex. Brain Res: 1979; 178 201 206 (Pubitemid 10249928)
15. Shughrue P J, Stumpf W E, Maclusky N J, Zielinski J, Hochberg R B. Developmental changes in estrogen receptors in mouse cerebral cortex between birth and postweaning: Studied by autoradiography with 11β-methoxy- 16α-(125I)iodoestradiol. Endocrinology: 1990; 126 1112 1124 (Pubitemid 20079531)
16. O'Keefe J A, Li Y, Burgess L H, Handa R J. Estrogen receptor mRNA alterations in the developing rat hippocampus. Mol Brain Res: 1995; 30 115 124
17. Overman W H. Sex differences in early childhood, adolescence, and adulthood on cognitive tasks that rely on orbital prefrontal cortex. Brain Cogn: 2004; 55 134 147 (Pubitemid 38591435)
18. Galea LA M, Uban K A, Epp J R, Brummelte S, Barha C K, Wilson W L, Lieblich S E, Pawluski J L. Endocrine regulation of cognition and neuroplasticity: Our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Exp Psychol. 2008; 62 247 260
19. Welborn B L, Papademetris X, Reis D L, Rajeevan N, Bloise S M, Gray J R. Variation in orbitofrontal cortex volume: relation to sex, emotion regulation and affect. Soc Cog Affec Neurosci: 2009; 4 328 339
20. Westberry J M, Trout A L, Wilson M E. Epigenetic regulation of estrogen receptor {alpha} gene expression in the mouse cortex during early postnatal development. Endocrinology: 2010; 151 731 740
21. Kurian J R, Bychowski M E, Forbes-Lorman R M, Auger C J, Auger A P. Mecp2 organizes juvenile social behavior in a sex-specific manner. J Neurosci: 2008; 28 7137 7142
22. Champagne F A, Weaver ICG, Diorio J, Dymov S, Szyf M, Meaney M J. Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology: 2006; 147 2909 2915 (Pubitemid 43764626)
23. Emery D L, Royo N C, Fischer I, Saatman K E, McIntosh T K. Plasticity following injury to the adult central nervous system: is recapitulation of a developmental state worth promoting? J Neurotrauma: 2003; 20 1271 1292 (Pubitemid 38018365)
24. Dubal D B, Rau S W, Shughrue P J, Zhu H, Yu J, Cashion A B, Suzuki S, Gerhold L M, Bottner M B, Dubal S B. Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERα in estradiol-mediated protection against delayed cell death. Endocrinology: 2006; 147 3076 3084 (Pubitemid 43764643)
25. Westberry J M, Prewitt A K, Wilson M E. Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats. Neuroscience: 2008; 152 982 989
26. DeFraja C, Conti L, Magrassi L, Govoni S, Cattaneo E. Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J Neurosci Res: 1998; 54 320 330 (Pubitemid 28493942)
27. Kudwa A, Michopoulos V, Gatewood J, Rissman E. Roles of estrogen receptors α and β in differentiation of mouse sexual behavior. Neuroscience: 2006; 138 921 928
28. Kudwa A E, Bodo C, Gustafsson JÅ, Rissman E. A previously uncharacterized role for estrogen receptor β: Defeminization of male brain and behavior. Proc Natl Acad Sci USA: 2005; 102 4608 4612 (Pubitemid 40397159)
29. Arnold A P, Chen X. What does the "four core genotypeso" mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol: 2009; 30 1 9
30. Majdic G, Tobet S. Cooperation of sex chromosomal genes and endocrine influences for hypothalamic sexual differentiation. Front Neuroendocrinol: 2011; 32 137 145
31. McClellan K M, Stratton M S, Tobet S A. Roles for γ-aminobutyric acid in the development of the paraventricular nucleus of the hypothalamus. J Comp Neurol: 2010; 518 2710 2728
32. Stratton M S, Searcy B T, Tobet S A. GABA regulates corticotropin releasing hormone levels in the paraventricular nucleus of the hypothalamus in newborn mice. Physiol Behav: 2011; 104 327 333
33. Tobet S, Fox T. Sex-and hormone-dependent antigen immunoreactivity in developing rat hypothalamus. Proc Natl Acad Sci USA: 1989; 86 382 386 (Pubitemid 19036390)
34. Tobet S A, Chickering T W, Hanna I, Crandall J E, Schwarting G A. Can gonadal steroids influence cell position in the developing brain? Horm Behav: 1994; 28 320 327
35. Henderson R G, Brown A E, Tobet S A. Sex differences in cell migration in the preoptic area/anterior hypothalamus of mice. J Neurobiol: 1999; 41 252 266 (Pubitemid 29494151)
36. Knoll J G, Wolfe C A, Tobet S A. Estrogen modulates neuronal movements within the developing preoptic area-anterior hypothalamus. Eur J Neurosci: 2007; 26 1091 1099 (Pubitemid 47346767)
37. Scordalakes E M, Shetty S J, Rissman E F. Roles of estrogen receptor α and androgen receptor in the regulation of neuronal nitric oxide synthase. J Comp Neurol: 2002; 453 336 344 (Pubitemid 35231186)
38. Orikasa C, Kondo Y, Hayashi S, McEwen B S, Sakuma Y. Sexually dimorphic expression of estrogen receptor β in the anteroventral periventricular nucleus of the rat preoptic area: implication in luteinizing hormone surge. Proc Natl Acad Sci: 2002; 99 3306 3311 (Pubitemid 34240627)
39. Wolfe C A, Van Doren M, Walker H J, Seney M L, McClellan K M, Tobet S A. Sex differences in the location of immunochemically defined cell populations in the mouse preoptic area/anterior hypothalamus. Dev Brain Res: 2005; 157 34 41 (Pubitemid 40812942)
40. Büdefeld T, Grgurevic N, Tobet S A, Majdic G. Sex differences in brain developing in the presence or absence of gonads. Dev Neurobiol: 2008; 68 981 995 (Pubitemid 351794117)
41. Stratton M, Budefeld T, Majdic G, Tobet S. Embryonic GABA-B receptor blockade alters adult hypothalamic structure, and anxiety- and depression-like behaviors in mice. Society for Neuroscience Abstract. 2011; Washington, DC, USA
42. Finley K H. The capillary bed of the paraventricular and supraoptic nuclei of the hypothalamus. Res Publ Assoc Res Nerv Ment Dis: 1938; 18 94 109
43. Frahm K A, Schow M J, Okland T S, Eitel C M, Tobet S A. The vasculature within the paraventricular nucleus of the hypothalamus in mice varies as a function of development, sub-nuclear location, and GABA signaling. Horm Metab Res. 2012; 44 advance online publication 5 April 2012. 10.1055/S-0032-1304624
44. Dellovade T L, Davis A M, Ferguson C, Sieghart W, Homanics G E, Tobet S A. GABA influences the development of the ventromedial nucleus of the hypothalamus. J Neurobiol: 2001; 49 264 276 (Pubitemid 33104872)
45. Tobet S, Hanna I, Schwarting G. Migration of neurons containing gonadotropin releasing hormone (GnRH) in slices from embryonic nasal compartment and forebrain. Dev Brain Res: 1996; 97 287 292 (Pubitemid 27008279)
46. Navratil A M, Knoll J G, Whitesell J D, Tobet S A, Clay C M. Neuroendocrine plasticity in the anterior pituitary: gonadotropin-releasing hormone-mediated movement in vitro and in vivo. Endocrinology: 2007; 148 1736 1744 (Pubitemid 46457134)
47. Frahm K A, Clay C M, Tobet S A. Characterization of an ovarian slice model in vitro to view ovulation. Soc Study Reproduction Abstract. 2010; Milwaukee, WI, USA
48. Pettine W, Jibson M, Chen T, Tobet S, Henry C. Characterization of novel microelectrode geometries for detection of neurotransmitters. Sensors J, IEEE: 2011; PP (99) 1 1
49. Lynn N S, Tobet S, Henry C S, Dandy D S. Mapping spatio-temporal molecular distributions using a microfluidic array. Anal Chem: 2011; 84 1360 1366
50. McCarthy M M, Auger A P, Bale T L, De Vries G J, Dunn G A, Forger N G, Murray E K, Nugent B M, Schwarz J M, Wilson M E. The epigenetics of sex differences in the brain. J Neurosci: 2009; 29 12815 12823
51. Klose R J, Bird A P. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci: 2006; 31 89 97 (Pubitemid 43221841)
52. Cooper D N, Krawczak M. Cytosine methylation and the fate of CpG dinucleotides in vertebrate genomes. Hum Genet: 1989; 83 181 188 (Pubitemid 19234570)
53. Bird A P, Wolffe A P. Methylation-induced repression - belts, braces, and chromatin. Cell: 1999; 99 451 454 (Pubitemid 129746827)
54. Weaver IC G, Cervoni N, Champagne F A, D'Alessio A C, Sharma S, Seckl J R, Dymov S, Szyf M, Meaney M J. Epigenetic programming by maternal behavior. Nat Neurosci: 2004; 7 847 854 (Pubitemid 38989508)
55. Renthal W, Nestler E J. Epigenetic mechanisms in drug addiction. Trends Mol Med: 2008; 14 341 350
56. Miller C A, Campbell S L, Sweatt J D. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem: 2008; 89 599 603 (Pubitemid 351484241)
57. Day J J, Sweatt J D. Epigenetic mechanisms in cognition. Neuron: 2011; 70 813 829
58. Guo J U, Ma D K, Mo H, Ball M P, Jang M H, Bonaguidi M A, Balazer J A, Eaves H L, Xie B, Ford E. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci: 2011; 14 1345 1351
59. Tate P H, Bird A P. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr Opin Genet Dev: 1993; 3 226 231 (Pubitemid 23108662)
60. He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci: 2005; 8 616 625 (Pubitemid 40594203)
61. Wilson M E. Methylation of the ER promoter as a regulator of brain region specific hormone sensitivity. Society for Neuroscience Abstract. 2009; Chicago, IL, USA
62. Schwarz J M, Nugent B M, McCarthy M M. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology: 2010; 151 4871 4881
63. Konkle A, McCarthy M M. Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology: 2011; 152 223 235
64. Ahmed E I, Zehr J L, Schulz K M, Lorenz B H, DonCarlos L L, Sisk C L. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci: 2008; 11 995 997
65. Métivier R, Gallais R, Tiffoche C, Le Péron C, Jurkowska R Z, Carmouche R P, Ibberson D, Barath P, Demay F, Reid G. Cyclical DNA methylation of a transcriptionally active promoter. Nature: 2008; 452 45 50 (Pubitemid 351355084)
66. Kim M S, Kondo T, Takada I, Youn M Y, Yamamoto Y, Takahashi S, Matsumoto T, Fujiyama S, Shirode Y, Yamaoka I. DNA demethylation in hormone-induced transcriptional derepression. Nature: 2009; 461 1007 1012
67. Kurian J R, Forbes-Lorman R M, Auger A P. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics: 2007; 2 173 178 (Pubitemid 350200395)
68. Jessen H M, Kolodkin M H, Bychowski M E, Auger C J, Auger A P. The nuclear receptor corepressor has organizational effects within the developing amygdala on juvenile social play and anxiety-like behavior. Endocrinology: 2010; 151 1212 1220
69. Kornberg R D, Lorch Y. Twenty-five years of the nucleosome, review fundamental particle of the eukaryote chromosome. Cell: 1999; 98 285 294 (Pubitemid 29380564)
70. Hansen J C, Tse C, Wolffes A P. Structure and Function of the Core Histone N-Termini: More Than Meets the Eye. Biochemistry: 1998; 37 17637 17641 (Pubitemid 29023917)
71. Strahl B D, Allis C D. The language of covalent histone modifications. Nature: 2000; 40 41 45 (Pubitemid 30038513)
72. Kuo M H, Allis CD. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays: 1998; 20 615 626 (Pubitemid 28422221)
73. Matsuda K I, Mori H, Nugent B M, Pfaff D W, McCarthy M M, Kawata M. Histone Deacetylation during Brain Development Is Essential for Permanent Masculinization of Sexual Behavior. Endocrinology: 2011; 152 2760 2767
74. Hernandez E R, Jimenez J L, Payne D W, Adashi E Y. Adrenergic regulation of ovarian androgen biosynthesis is mediated via β2-adrenergic theca-interstitial cell recognition sites. Endocrinology: 1988; 122 1592 1602 (Pubitemid 18091994)
75. Ricu M, Paredes A, Greiner M, Ojeda S R, Lara H E. Functional development of the ovarian noradrenergic innervation. Endocrinology: 2008; 149 50 56
76. Lara H E, Porcile A, Espinoza J, Romero C, Luza S M, Fuhrer J, Miranda C, Roblero L. Release of norepinephrine from human ovary. Endocrine: 2001; 15 187 192 (Pubitemid 32977328)
77. Heider U, Pedal I, Spanel-Borowski K. Increase in nerve fibers and loss of mast cells in polycystic and postmenopausal ovaries. Fertil Steril: 2001; 75 1141 1147 (Pubitemid 32522611)
78. Greiner M, Paredes A, Araya V, Lara H E. Role of stress and sympathetic innervation in the development of polycystic ovary syndrome. Endocrine: 2005; 28 319 324 (Pubitemid 43042731)
79. Lara H, Dorfman M, Venegas M, Luza S, Luna S, Mayerhofer A, Guimaraes M, Rosa e Silva A, Ramirez V. Changes in sympathetic nerve activity of the mammalian ovary during a normal estrous cycle and in polycystic ovary syndrome: studies on norepinephrine release. Microsc Res Tech: 2002; 59 495 502 (Pubitemid 35470964)
80. Jedel E, Waern M, Gustafson D, Landén M, Eriksson E, Holm G, Nilsson L, Lind A K, Janson P O, Stener-Victorin E. Anxiety and depression symptoms in women with polycystic ovary syndrome compared with controls matched for body mass index. Human Reprod: 2010; 25 450 456
81. Stener-Victorin E, Ploj K, Larsson B M, Holmäng A. Rats with steroid-induced polycystic ovaries develop hypertension and increased sympathetic nervous system activity. Reprod Biol Endo: 2005; 3 44
82. Barria A, Leyton V, Ojeda S, Lara H E. Ovarian steroidal response to gonadotropins and β-adrenergic stimulation is enhanced in polycystic ovary syndrome: Role of Sympathetic Innervation. Endocrinology: 1993; 133 2696 2703 (Pubitemid 24000722)
83. Lara H, Ferruz J, Luza S, Bustamante D, Borges Y, Ojeda S. Activation of ovarian sympathetic nerves in polycystic ovary syndrome. Endocrinology: 1993; 133 2690 2695 (Pubitemid 24000721)
84. Goldstein D S, Kopin IJ. Adrenomedullary, adrenocortical, and sympathoneural responses to stressors: a meta-analysis. Endocr Regul: 2008; 42 111 119
85. Bernuci M P, Szawka R E, Helena CV V, Leite C M, Lara H E, Anselmo-Franci J A. Locus coeruleus mediates cold stress-induced polycystic ovary in rats. Endocrinology: 2008; 149 2907 2916 (Pubitemid 351724516)
86. Dorfman M, Arancibia S, Fiedler J, Lara H. Chronic intermittent cold stress activates ovarian sympathetic nerves and modifies ovarian follicular development in the rat. Biol Reprod: 2003; 68 2038 2043 (Pubitemid 36686994)
87. Fiedler J, Jara P, Luza S, Dorfman M, Grouselle D, Rage F, Lara H E, Arancibia S. Cold stress induces metabolic activation of thyrotrophin-releasing hormone-synthesising neurones in the magnocellular division of the hypothalamic paraventricular nucleus and concomitantly changes ovarian sympathetic activity parameters. J Neuroendocrinol: 2006; 18 367 376
88. Jara P, Rage F, Dorfman M, Grouselle D, Barra R, Arancibia S, Lara H. Cold-induced glutamate release in vivo from the magnocellular region of the paraventricular nucleus is involved in ovarian sympathetic activation. J Neuroendocrinol: 2010; 22 979 986
89. Gomes C M, Donadio MV F, Anselmo-Franci J, Franci C R, Lucion A B, Sanvitto G L. Neonatal handling induces alteration in progesterone secretion after sexual behavior but not in angiotensin II receptor density in the medial amygdala: implications for reproductive success. Life Sci: 2006; 78 2867 2871
90. Gomes C, Raineki C, de Paula P R, Severino G, Helena C, Anselmo-Franci J, Franci C, Sanvitto G, Lucion A. Neonatal handling and reproductive function in female rats. J Endocrinol: 2005; 184 435 445 (Pubitemid 40340177)
91. Raineki C, De Souza M, Szawka R, Lutz M, De Vasconcellos L, Sanvitto G, Izquierdo I, Bevilaqua L, Cammarota M, Lucion A. Neonatal handling and the maternal odor preference in rat pups: involvement of monoamines and cyclic AMP response element-binding protein pathway in the olfactory bulb. Neuroscience: 2009; 159 31 38
92. Raineki C, Szawka R E, Gomes C M, Lucion M K, Barp J, Belló-Klein A, Franci C R, Anselmo-Franci J A, Sanvitto G L, Lucion A B. Effects of neonatal handling on central noradrenergic and nitric oxidergic systems and reproductive parameters in female rats. Neuroendocrinology: 2008; 87 151 159 (Pubitemid 351563809)
93. Anderson H, Fogel N, Grebe S K, Singh R J, Taylor R L, Dunaif A. Infants of women with polycystic ovary syndrome have lower cord blood androstenedione and estradiol levels. J Clin Endo Metab: 2010; 95 2180 2186
94. Bzoskie L, Blount L, Kashiwai K, Humme J, Padbury J. The contribution of transporter-dependent uptake to fetal catecholamine clearance. Neonatology: 1997; 71 102 110 (Pubitemid 27086940)
95. Gu W, Jones C T. The effect of elevation of maternal plasma catecholamines on the fetus and placenta of the pregnant sheep. J Dev Physiol: 1986; 8 173 186 (Pubitemid 16007509)
96. Broekmans F J, Knauff EA H, te Velde E R, Macklon N S, Fauser B C. Female reproductive ageing: current knowledge and future trends. Trend Endo Metab: 2007; 18 58 65 (Pubitemid 46275460)
97. Faddy M, Gosden R, Gougeon A, Richardson S J, Nelson J. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Human Reproduction: 1992; 7 1342 1346 (Pubitemid 23042150)
98. Acua E, Fornes R, Fernandois D, Garrido M P, Greiner M, Lara H E, Paredes A H. Increases in norepinephrine release and ovarian cyst formation during ageing in the rat. Reprod Biol Endo: 2009; 7 64
99. Lara H, McDonald J, Ahmed C, Ojeda S. Guanethidine-mediated destruction of ovarian sympathetic nerves disrupts ovarian development and function in rats. Endocrinology: 1990; 127 2199 2209 (Pubitemid 20381748)
100. Ferruz J, Barria A, Galleguillos X, Lara H. Release of norepinephrine from the rat ovary: local modulation of gonadotropins. Biol Reprod: 1991; 45 592 597
101. Aguado L, Petrovic S, Ojeda S. Ovarian β-adrenergic receptors during the onset of puberty: characterization, distribution, and coupling to steroidogenic responses. Endocrinology: 1982; 110 1124 1132
102. Menken J, Trussell J, Larsen U. Age and infertility. Science: 1986; 233 1389 1394 (Pubitemid 17169372)
103. Lenton E A, DeKretser D M, Woodward A J, Robertson M D. Inhibin concentrations throughout the menstrual cycles of normal, infertile, and older women compared with those during spontaneous conception cycles. J Clin Endo Metab: 1991; 73 1180 1190 (Pubitemid 121000690)
104. Margolin E, Zhornitzki T, Kopernik G, Kogan S, Schattner A, Knobler H. Polycystic ovary syndrome in post-menopausal women - marker of the metabolic syndrome. Maturitas: 2005; 50 331 336 (Pubitemid 40365038)
105. Dissen G, Parrott J, Skinner M, Hill D, Costa M, Ojeda S. Direct effects of nerve growth factor on thecal cells from antral ovarian follicles. Endocrinology: 2000; 141 4736 4750 (Pubitemid 32055154)
106. Bai Y H, Lim S C, Song C H, Bae C S, Jin C S, Choi B C, Jang C H, Lee S H, Pak S C. Electro-acupuncture reverses nerve growth factor abundance in experimental polycystic ovaries in the rat. Gynecol Obstet Invest: 2004; 57 80 85 (Pubitemid 38209799)
107. Lara H, Dissen G, Leyton V, Paredes A, Fuenzalida H, Fiedler J, Ojeda S. An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat. Endocrinology: 2000; 141 1059 1072 (Pubitemid 32260449)
108. Chávez-Genaro R, Lombide P, Domínguez R, Rosas P, Vázquez-Cuevas F. Sympathetic pharmacological denervation in ageing rats: effects on ovulatory response and follicular population. Reprod Fertil Dev: 2007; 19 954 960 (Pubitemid 350036663)
109. Sir-Petermann T, Maliqueo M, Angel B, Lara H, Perez-Bravo F, Recabarren S. Maternal serum androgens in pregnant women with polycystic ovarian syndrome: possible implications in prenatal androgenization. Human Reprod: 2002; 17 2573 2579 (Pubitemid 35174106)
110. Sir-Petermann T, Maliqueo M, Codner E, Echiburú B, Crisosto N, Pérez V, Pérez-Bravo F, Cassorla F. Early metabolic derangements in daughters of women with polycystic ovary syndrome. J Clin Endo Metab: 2007; 92 4637 4642 (Pubitemid 350223438)
111. Sir-Petermann T, Codner E, Pérez V, Echiburú B, Maliqueo M, Ladrón de Guevara A, Preisler J, Crisosto N, Sánchez F, Cassorla F. Metabolic and reproductive features before and during puberty in daughters of women with polycystic ovary syndrome. J Clin Endo Metab: 2009; 94 1923 1930
112. Sir-Petermann T, Márquez L, Cárcamo M, Hitschfeld C, Codner E, Maliqueo M, Echiburú B, Aranda P, Crisosto N, Cassorla F. Effects of birth weight on anti-Müllerian hormone serum concentrations in infant girls. J Clin Endo Metab: 2010; 95 903 910
113. Franks S. Do animal models of polycystic ovary syndrome help to understand its pathogenesis and management? Yes, but their limitations should be recognized. Endocrinology: 2009; 150 3983 3985
114. Padmanabhan V, Veiga-Lopez A, Abbott D, Recabarren S, Herkimer C. Developmental programming: impact of prenatal testosterone excess and postnatal weight gain on insulin sensitivity index and transfer of traits to offspring of overweight females. Endocrinology: 2010; 151 595 605
115. Roland A V, Nunemaker C S, Keller S R, Moenter S M. Prenatal androgen exposure programs metabolic dysfunction in female mice. J Endocrinol: 2010; 207 213 223
116. Abbott D H, Tarantal A F, Dumesic D A. Fetal, infant, adolescent and adult phenotypes of polycystic ovary syndrome in prenatally androgenized female rhesus monkeys. Am J Primatol: 2009; 71 776 784
117. Dumesic D A, Abbott D H, Padmanabhan V. Polycystic ovary syndrome and its developmental origins. Rev Endo Metabol Dis: 2007; 8 127 141 (Pubitemid 47434646)
118. New M I. Steroid 21-hydroxylase deficiency (congenital adrenal hyperplasia). Am J Med: 1995; 98 S2 S8
119. Cabrera M S, Vogiatzi M G, New M I. Long term outcome in adult males with classic congenital adrenal hyperplasia. J Clin Endo Metab: 2001; 86 3070 3078 (Pubitemid 32673467)
120. Reisch N, Flade L, Scherr M, Rottenkolber M, Pedrosa Gil F, Bidlingmaier M, Wolff H, Schwarz H P, Quinkler M, Beuschlein F. High prevalence of reduced fecundity in men with congenital adrenal hyperplasia. J Clin Endo Metab: 2009; 94 1665 1670
121. Recabarren S E, Smith R, Rios R, Maliqueo M, Echiburú B, Codner E, Cassorla F, Rojas P, Sir-Petermann T. Metabolic profile in sons of women with polycystic ovary syndrome. J Clin Endo Metab: 2008; 93 1820 1826 (Pubitemid 351656524)
122. Recabarren S E, Sir-Petermann T, Rios R, Maliqueo M, Echiburú B, Smith R, Rojas-García P, Recabarren M, Rey R A. Pituitary and testicular function in sons of women with polycystic ovary syndrome from infancy to adulthood. J Clin Endo Metab: 2008; 93 3318 3324
123. Recabarren S E, Rojas-García P P, Recabarren M P, Alfaro V H, Smith R, Padmanabhan V, Sir-Petermann T. Prenatal testosterone excess reduces sperm count and motility. Endocrinology: 2008; 149 6444 6448
124. Rojas-García P, Recabarren M P, Palmer S, Tovar H, Gabler C, Einspanier R, Maliqueo M, Sir-Petermann T, Recabarren S E. Prenatal testosterone excess alters seminal and cellular characteristics in male sheep via its androgenic actions. Androgen Excess & PCO Society. 2010; Munich, Germany
125. Rojas-García P P, Recabarren M P, Sarabia L, Schön J, Gabler C, Einspanier R, Maliqueo M, Sir-Petermann T, Rey R, Recabarren S E. Prenatal testosterone excess alters Sertoli and germ cell number and testicular FSH receptor expression in rams. Am J Physiol Endo Metab: 2010; 299 E998 E1005