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Control Puberty in Rodents

Special Focus on the Female

  • Chapter
When Puberty is Precocious

Part of the book series: Contemporary Endocrinology ((COE))

Abstract

The neuroendocrine control of the onset of puberty in rodents has been extensively reviewed over the years (1–7). In this chapter, we will provide both a brief account of the basic mechanisms underlying the pubertal process in these animals and an update of some recent developments in the field. Because the rat is the animal most extensively studied, we will discuss mainly results obtained in this species, and when available, we will offer the reader a comparison of these results with those obtained in mice.

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References

  1. Donovan BT, van der Werff ten Bosch JJ. Physiology of puberty. In: Barcroft H, Davson H, Paton WDM, editors. Monographs of the Physiological Society, No. 15. Baltimore, MD: Williams & Wilkins, 1965:1–204.

    Google Scholar 

  2. Critchlow V, Bar-Sela M. Control of the onset of puberty. In: Martini L, Ganong WF, editors. Neuroendocrinology, Vol II. New York: Academic Press, 1967:101–162.

    Google Scholar 

  3. Ramirez VD. Endocrinology of puberty. In: Greep RO, Astwood EB, editors. Handbook of Physiology, Vol II, section 7. Washington, D.C.: American Physiological Society, 1973:1–28.

    Google Scholar 

  4. Ojeda SR, Smith(White) SS, Urbanski HF, Aguado LI. The onset of female puberty: underlying neuroendocrine mechanisms. In: Müller EE, MacLeod RM, editors. Neuroendocrine Perspectives, 3 rd edition. New York: Elsevier Science Publishers, 1984:225–278.

    Google Scholar 

  5. Ojeda SR, Urbanski HF. Puberty in the rat. In: Knobil E, Neill JD, editors. The Physiology of Reproduction, 2nd edition, Vol 2. New York: Raven Press, 1994:363–409.

    Google Scholar 

  6. Ojeda SR, Terasawa E. Neuroendocrine regulation of puberty. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R, editors. Hormones, Brain and Behavior, Vol 4. New York: Elsevier, 2002:589–659.

    Google Scholar 

  7. Ojeda SR, Skinner MK. Puberty in the rat. In: Neill JD, editor. The Physiology of Reproduction, 3rd edition. San Diego, CA: Academic Press/Elsevier, 2006:2061–2126.

    Google Scholar 

  8. Plant TM. Puberty in primates. In: Knobil E, Neill J, editors. The Physiology of Reproduction, 2nd edition, Vol 2. New York: Raven Press, 1994:453–485.

    Google Scholar 

  9. Urbanski HF, Ojeda SR. The juvenile-peripubertal transition period in the female rat: establishment of a diurnal pattern of pulsatile luteinizing hormone secretion. Endocrinology 1985;117:644–649.

    Article  PubMed  CAS  Google Scholar 

  10. Tanner JM. Sequence and tempo in the somatic changes in puberty. In: Grumbach MM, Grave GD, Mayer FE, editors. The Control of the Onset of Puberty. New York: John Wiley & Sons, 1974:448–470.

    Google Scholar 

  11. Nelson JF, Karelus K, Felicio LS, Johnson TE. Genetic influences on the timing of puberty in mice. Biol Reprod 1990;42:649–655.

    Article  PubMed  CAS  Google Scholar 

  12. Stiff ME, Bronson FH, Stetson MH. Plasma gonadotropins in prenatal and prepubertal female mice: disorganization of pubertal cycles in the absence of a male. Endocrinology 1974;94:492–496.

    Article  PubMed  CAS  Google Scholar 

  13. Ojeda SR, Wheaton JE, Jameson HE, McCann SM. The onset of puberty in the female rat. I. Changes in plasma prolactin, gonadotropins, LHRH levels and hypothalamic LHRH content. Endocrinology 1976;98:630–638.

    Article  PubMed  CAS  Google Scholar 

  14. Meijs-Roelofs HMA, Uilenbroek JThJ, de Greef WJ, de Jong FH, Kramer D. Gonadotropin and steroid levels around the time of first ovulation in the rat. J Endocrinol 1975;67:275–282.

    Article  PubMed  CAS  Google Scholar 

  15. Ojeda SR, Andrews WW, Advis JP, Smith-White S. Recent advances in the endocrinology of puberty. Endocr Rev 1980;1:228–257.

    Article  PubMed  CAS  Google Scholar 

  16. Ojeda SR, Ramirez VD. Plasma levels of LH and FSH in maturing rats: response to hemigonadectomy. Endocrinology 1972;90:466–472.

    Article  PubMed  CAS  Google Scholar 

  17. Kragt CL, Dahlgren J. Development of neural regulation of follicle-stimulating hormone (FSH) secretion. Neuroendocrinology 1972;9:30–40.

    Article  PubMed  CAS  Google Scholar 

  18. Döhler KD, Wuttke W. Serum LH, FSH, prolactin and progesterone from birth to puberty in female and male rats. Endocrinology 1974;94:1003–1008.

    Article  PubMed  Google Scholar 

  19. McKinnon PCB, Mattock JM, ter Haar MB. Serum gonadotrophin levels during development in male, female and androgenized female rats and the effect of general disturbance on high luteinizing hormone levels. J Endocrinol 1976;70:361–371.

    Article  Google Scholar 

  20. Hompes PGA, Vermes I, Tilders FJH, Schoemaker J. In vitro release of LHRH from the hypothalamus of female rats during prepubertal development. Neuroendocrinology 1982;35:8–12.

    Article  PubMed  CAS  Google Scholar 

  21. Matagne V, Rasier G, Lebrethon M-C, Gérard A, Bourguignon J-P. Estradiol stimulation of pulsatile gonadotropin-releasing hormone secretion in vitro: correlation with prenatal exposure to sex steroids and induction of sexual precocity in vivo. Endocrinology 2004;145:2775–2783.

    Article  PubMed  CAS  Google Scholar 

  22. Ojeda SR, Ramirez VD. Short-term steroid treatment on plasma LH and FSH in castrated rats from birth to puberty. Neuroendocrinology 1973;13:100–114.

    Article  PubMed  CAS  Google Scholar 

  23. Ojeda SR, Kalra SP, McCann SM. Further studies on the maturation of the estrogen negative feedback on gonadotropin release in the prepubertal female rat. Neuroendocrinology 1975;18:242–255.

    Article  PubMed  CAS  Google Scholar 

  24. Meijs-Roelofs HMA, Kramer P. Maturation of the inhibitory feedback action of oestrogen on folliclestimulating hormone secretion in the immature female rat: a role for alphafoetoprotein. J Endocrinol 1979;81:199–208.

    Article  PubMed  CAS  Google Scholar 

  25. Andrews WW, Ojeda SR. On the feedback actions of estrogen on gonadotropins and prolactin release in infantile female rats. Endocrinology 1977;101:1517–1523.

    Article  PubMed  CAS  Google Scholar 

  26. Ojeda SR, Jameson HE, McCann SM. Developmental changes in pituitary responsiveness to luteinizing hormone-releasing hormone (LHRH) in the female rat: ovarian-adrenal influence during the infantile period. Endocrinology 1977;100:440–451.

    Article  PubMed  CAS  Google Scholar 

  27. Andrews WW, Ojeda SR. A detailed analysis of the serum LH secretory profiles of conscious free-moving female rats during the time of puberty. Endocrinology 1981;109:2032–2039.

    Article  PubMed  CAS  Google Scholar 

  28. Kimura F, Kawakami M. Episodic LH secretion in the immature male and female rat as assessed by sequential blood sampling. Neuroendocrinology 1982;35:128–132.

    Article  PubMed  CAS  Google Scholar 

  29. Faiman C, Winter JSD. Gonadotropins and sex hormone patterns in puberty: clinical data. In: Grumbach MM, Grave GD, Mayer FE, editors. Control of the Onset of Puberty. New York: John Wiley & Sons, 1974:32–55.

    Google Scholar 

  30. Frawley LS, Henricks DM. Mode of gonadotropin secretion in infantile female rats and the role of estrogen in feedback regulation. Endocrinology 1979;105:1064–1072.

    Article  PubMed  CAS  Google Scholar 

  31. Raymond JP, Mercier-Bodard C, Baulieu EE. Rat estradiol binding plasma protein (EBP). Steroids 1971;18:767–788.

    Article  Google Scholar 

  32. Nunez E, Engelmann F, Bennassayag C, Joyle MF. Identification et purification préliminaire de la foeto protéine liant les oestrogènes dans le sérum de rats nouveaunes.CRAcad Sci (Paris) 1971;273:834–841.

    Google Scholar 

  33. Andrews WW, Ojeda SR. A quantitative analysis of the maturation of steroid negative feedbacks controlling gonadotropin release in the female rat: transition from an androgenic to a predominantly estrogenic control. Endocrinology 1981;108:1313–1320.

    Article  PubMed  CAS  Google Scholar 

  34. Andrews WW, Mizejewski GJ, Ojeda SR. Development of estradiol-positive feedback on luteinizing hormone release in the female rat: a quantitative study. Endocrinology 1981;109:1404–1413.

    Article  PubMed  CAS  Google Scholar 

  35. Puig-Duran E, MacKinnon PCB. Patterns of LH and prolactin release following steroid manipulations in the rat during development. Ann Biol Anim Biochem Biophys 1976;16:373–375.

    Article  CAS  Google Scholar 

  36. Bronson FH. The regulation of luteinizing hormone secretion by estrogen: relationships among negative feedback, surge potential, and male stimulation in juvenile, peripubertal, and adult female mice. Endocrinology 1981;108:506–516.

    Article  PubMed  CAS  Google Scholar 

  37. Shivers BD, Harlan RE, Morrell JI, Pfaff DW. Absence of oestradiol concentration in cell nuclei of LHRH-immunoreactive neurones. Nature 1983;304:345–347.

    Article  PubMed  CAS  Google Scholar 

  38. Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 1998;19:302–330.

    Article  PubMed  CAS  Google Scholar 

  39. Hrabovszky E, Shughrue PJ, Merchenthaler I et al. Detection of estrogen receptor-β messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2000;141:3506–3509.

    Article  PubMed  CAS  Google Scholar 

  40. Skynner MJ, Sim JA, Herbison AE. Detection of estrogen receptor α and β messenger ribonucleic acids in adult gonadotropin-releasing hormone neurons. Endocrinology 1999;140:5195–5201.

    Article  PubMed  CAS  Google Scholar 

  41. Petersen SL, Ottem EN, Carpenter CD. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 2003;69:1771–1778.

    Article  PubMed  CAS  Google Scholar 

  42. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005;146:3686–3692.

    Article  PubMed  CAS  Google Scholar 

  43. Dungan HM, Clifton DK, Steiner RA. Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 2006;147:1154–1158.

    Article  PubMed  CAS  Google Scholar 

  44. Han SK, Gottsch ML, Lee KJ et al. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005;25: 11349–11356.

    Article  PubMed  CAS  Google Scholar 

  45. Jakubowski M, Blum M, Roberts JL. Postnatal development of gonadotropin-releasing hormone and cyclophilin gene expression in the female and male rat brain. Endocrinology 1991;128:2702–2708.

    Article  PubMed  CAS  Google Scholar 

  46. Bourguignon J-P, Gerard A, Mathieu J, Mathieu A, Franchimont P. Maturation of the hypothalamic control of pulsatile gonadotropin-releasing hormone secretion at onset of puberty. I. Increased activation of N-methyl-D-aspartate receptors. Endocrinology 1990;127:873–881.

    Article  PubMed  CAS  Google Scholar 

  47. Andrews WW, Ojeda SR. The control of LH release in prepubertal female rats: indirect evidence for an enhanced ability of the hypothalamus to release LHRH as the pituitary responsiveness to LHRH declines. J Endocrinol 1978;78:281–282.

    Article  PubMed  CAS  Google Scholar 

  48. Ojeda SR, Lomniczi A, Mastronardi C et al. Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology 2006;147:1166–1174.

    Article  PubMed  CAS  Google Scholar 

  49. Bourguignon J-P, Lebrethon MC, Gérard A et al. Amino acid neurotransmission and early ontogeny of pulsatile GnRH secretion from the rat hypothalamus. In: Bourguignon J-P, Plant TM, editors. The Onset of Puberty in Perspective. Amsterdam: Elsevier Science B.V., 2000:119–129.

    Google Scholar 

  50. van den Pol AN, Trombley PQ. Glutamate neurons in hypothalamus regulate excitatory transmission. J Neurosci 1993;13:2829–2836.

    PubMed  Google Scholar 

  51. Claypool LE, Kasuya E, Saitoh Y, Marzban F, Terasawa E. N-methyl D,L-aspartate induces the release of luteinizing hormone-releasing hormone in the prepubertal and pubertal female rhesus monkey as measured by in vivo push-pull perfusion in the stalk-median eminence. Endocrinology 2000;141:219–228.

    Article  PubMed  CAS  Google Scholar 

  52. Donoso AO, López FJ, Negro-Vilar A. Glutamate receptors of the non-N-methyl-D-aspartic acid type mediate the increase in luteinizing hormone releasing hormone release by excitatory amino acid in vitro. Endocrinology 1990;126:414–420.

    Article  PubMed  CAS  Google Scholar 

  53. Plant TM, Gay VL, Marshall GR, Arslan M. Puberty in monkeys is triggered by chemical stimulation of the hypothalamus. Proc Natl Acad Sci USA 1989;86:2506–2510.

    Article  PubMed  CAS  Google Scholar 

  54. Urbanski HF, Ojeda SR. A role for N-methyl-D-aspartate (NMDA) receptors in the control of LH secretion and initiation of female puberty. Endocrinology 1990;126:1774–1776.

    Article  PubMed  CAS  Google Scholar 

  55. Ottem EN, Godwin JG, Petersen SL. Glutamatergic signaling through the N-methyl-D-aspartate receptor directly activates medial subpopulations of luteinizing hormone-releasing hormone (LHRH) neurons, but does not appear to mediate the effects of estradiol on LHRH gene expression. Endocrinology 2002;143:4837–4845.

    Article  PubMed  CAS  Google Scholar 

  56. Gore AC. Gonadotropin-releasing hormone neurons. NMDA receptors, and their regulation by steroid hormones across the reproductive life cycle. Brain Res Rev 2001;37:235–248.

    Article  PubMed  CAS  Google Scholar 

  57. Eyigor O, Jennes L. Expression of glutamate receptor subunit mRNAs in gonadotropin-releasing hormone neurons during the sexual maturation of the female rat. Neuroendocrinology 1997;66: 122–129.

    Article  PubMed  CAS  Google Scholar 

  58. Eyigor O, Jennes L. Kainate receptor subunit-positive gonadotropin-releasing hormone neurons express c-Fos during the steroid-induced luteinizing hormone surge in the female rat. Endocrinology 2000;141:779–786.

    Article  PubMed  CAS  Google Scholar 

  59. van den Pol AN, Wuarin J-P, Dudek FE. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 1990;250:1276–1278.

    Article  PubMed  Google Scholar 

  60. Witkin JW, Silverman A-J. Synaptology of luteinizing hormone-releasing hormone neurons in rat preoptic area. Peptides 1985;6:263–271.

    Article  PubMed  CAS  Google Scholar 

  61. Campbell RE, Han SK, Herbison AE. Biocytin filling of adult gonadotropin-releasing hormone neurons in situ reveals extensive, spiny, dendritic processes. Endocrinology 2005;146:1163–1169.

    Article  PubMed  CAS  Google Scholar 

  62. Spergel DJ, Krüth U, Hanley DF, Sprengel R, Seeburg PH. GABA-and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 1999;19:2037–2050.

    PubMed  CAS  Google Scholar 

  63. Suter KJ. Control of firing by small (S)-alpha-amino-3-hydroxy-5-methyl-isoxazolepropionic acidlike inputs in hypothalamic gonadotropin releasing-hormone (GnRH) neurons. Neuroscience 2004;128:443–450.

    Article  PubMed  CAS  Google Scholar 

  64. Kuehl-Kovarik MC, Pouliot WA, Halterman GL, Handa RJ, Dudek FE, Partin KM. Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J Neurosci 2002;22:2313–2322.

    PubMed  CAS  Google Scholar 

  65. Boehm U, Zou Z, Buck LB. Feedback loops link odor and pheromone signaling with reproduction. Cell 2005;123:683–695.

    Article  PubMed  CAS  Google Scholar 

  66. Ohtaki T, Shintani Y, Honda S et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001;411:613–617.

    Article  PubMed  CAS  Google Scholar 

  67. Kotani M, Detheux M, Vandenbogaerde A et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001;276:34631–34636.

    Article  PubMed  CAS  Google Scholar 

  68. Muir AI, Chamberlain L, Elshourbagy NA et al. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001;276:28969–28975.

    Article  PubMed  CAS  Google Scholar 

  69. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005;102:2129–2134.

    Article  PubMed  CAS  Google Scholar 

  70. Gottsch ML, Cunningham MJ, Smith JT et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004;145:4073–4077.

    Article  PubMed  CAS  Google Scholar 

  71. Navarro VM, Fernandez-Fernandez R, Castellano JM et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004;561:379–386.

    Article  PubMed  CAS  Google Scholar 

  72. de Roux N, Genin E, Carel J-C, Matsuda F, Chaussain J-L, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003;100:10972–10976.

    Article  PubMed  CAS  Google Scholar 

  73. Seminara SB, Messager S, Chatzidaki EE et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003;349:1614–1627.

    Article  PubMed  CAS  Google Scholar 

  74. Semple RK, Achermann JC, Ellery J et al. Two novel missense mutations in g protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. J Clin Endocrinol Metab 2005;90:1849–1855.

    Article  PubMed  CAS  Google Scholar 

  75. Funes S, Hedrick JA, Vassileva G et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003;312:1357–1363.

    Article  PubMed  CAS  Google Scholar 

  76. Brailoiu GC, Dun SL, Ohsawa M et al. KiSS-1 expression and metastin-like immunoreactivity in the rat brain. J Comp Neurol 2005;481:314–329.

    Article  PubMed  CAS  Google Scholar 

  77. Irwig MS, Fraley GS, Smith JT et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2005;80:264–272.

    Article  CAS  Google Scholar 

  78. Navarro VM, Castellano JM, Fernández-Fernández R et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005;146:156–163.

    Article  PubMed  CAS  Google Scholar 

  79. Parhar IS, Ogawa S, Sakuma Y. Laser captured single digoxigenin-labeled neurons of gonadotropinreleasing hormone types reveal a novel G protein-coupled receptor (GPR54) during maturation in cichlid fish. Endocrinology 2004;145:3613–3618.

    Article  PubMed  CAS  Google Scholar 

  80. Messager S, Chatzidaki EE, Ma D et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005;102:1761–1766.

    Article  PubMed  CAS  Google Scholar 

  81. Goroll D, Arias P, Wuttke W. Preoptic release of amino acid neuro-transmitters evaluated in peripubertal and young adult female rats by push-pull perfusion. Neuroendocrinology 1993;58:11–15.

    Article  PubMed  CAS  Google Scholar 

  82. Terasawa E, Fernandez DL. Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 2001;22:111–151.

    Article  PubMed  CAS  Google Scholar 

  83. Lagrange AH, Ronnekleiv OK, Kelly MJ. Estradiol-17β and μ-opioid peptides rapidly hyperpolarize GnRH neurons: a cellular mechanism of negative feedback? Endocrinology 1995;136:2341–2344.

    Article  PubMed  CAS  Google Scholar 

  84. DeFazio RA, Heger S, Ojeda SR, Moenter SM. Activation of A-type γ-aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 2002;16:2872–2891.

    Article  PubMed  CAS  Google Scholar 

  85. Moenter SM, DeFazio RA. Endogenous gamma-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 2005;146:5374–5379.

    Article  PubMed  CAS  Google Scholar 

  86. Ferin M, Wehrenberg WB, Lam NY, Alston EJ, Vande Wiele RL. Effects and site action of morphine on gonadotropin secretion in the female rhesus monkey. Endocrinology 1982;111:1652–1656.

    CAS  Google Scholar 

  87. Mallory DS, Bona-Gallo A, Gallo RV. Neurotransmitter involvement in naloxone-induced stimulation of pulsatile LH release on day 8 of pregnancy in the rat. Brain Res Bull 1989;22:1015–1021.

    Article  PubMed  CAS  Google Scholar 

  88. Kesner JS, Kaufman JM, Wilson RC, Kuroda G, Knobil E. The effect of morphine on the electrophysiological activity of the hypothalamic luteinizing hormone-releasing hormone pulse generator in the rhesus monkey. Neuroendocrinology 1986;43:686–688.

    Article  PubMed  CAS  Google Scholar 

  89. Medhamurthy R, Gay VL, Plant TM. The prepubertal hiatus in gonadotropin secretion in the male rhesus monkey (Macaca mulatta) does not appear to involve endogenous opioid peptide restraint of hypothalamic gonadotropin-releasing hormone release. Endocrinology 1990;126:1036–1042.

    Article  PubMed  CAS  Google Scholar 

  90. Mastronardi C, Smiley G, Kuswakabe T et al. Deletion of the Ttfl gene in differentiated neurons disrupts female reproduction without impairing basal ganglia function. J Neurosci 2006;26:13167–13179.

    Article  PubMed  CAS  Google Scholar 

  91. Nedergaard M, Ransom B, Goldman SA. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 2003;26:523–530.

    Article  PubMed  CAS  Google Scholar 

  92. Galbiati M, Zanisi M, Messi E, Cavarretta I, Martini L, Melcangi RC. Transforming growth factor-β and astrocytic conditioned medium influence luteinizing hormone-releasing hormone gene expression in the hypothalamic cell line GT1. Endocrinology 1996;137:5605–5609.

    Article  PubMed  CAS  Google Scholar 

  93. Buchanan CD, Mahesh VB, Brann DW. Estrogen-astrocyte-luteinizing hormone-releasing hormone signaling: a role for transforming growth factor-β. Biol Reprod 2000;62:1710–1721.

    Article  PubMed  CAS  Google Scholar 

  94. Prevot V, Cornea A, Mungenast A, Smiley G, Ojeda SR. Activation of erbB-1 signaling in tanycytes of the median eminence stimulates transforming growth factor β1 release via prostaglandin E2 production and induces cell plasticity. J Neurosci 2003;23:10622–10632.

    PubMed  CAS  Google Scholar 

  95. Kozlowski GP, Coates PW. Ependymoneuronal specializations between LHRH fibers and cells of the cerebroventricular system. Cell Tissue Res 1985;242:301–311.

    Article  PubMed  CAS  Google Scholar 

  96. Prevot V. Glial-neuronal-endothelial interactions are involved in the control of GnRH secretion. J Neuroendocrinol 2002;14:247–255.

    Article  PubMed  CAS  Google Scholar 

  97. Gill JC, Moenter SM, Tsai P-S. Developmental regulation of gonadotropin-releasing hormone neurons by fibroblast growth factor signaling. Endocrinology 2004;145:3830–3839.

    Article  PubMed  CAS  Google Scholar 

  98. Tsai PS, Moenter SM, Postigo HR et al. Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in gonadotropin-releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol Endocrinol 2005;19:225–236.

    Article  PubMed  CAS  Google Scholar 

  99. Voigt P, Ma YJ, Gonzalez D et al. Neural and glial-mediated effects of growth factors acting via tyrosine kinase receptors on LHRH neurons. Endocrinology 1996;137:2593–2605.

    Article  PubMed  CAS  Google Scholar 

  100. Tsai P-S, Werner S, Weiner RI. Basic fibroblast growth factor is a neurotropic factor in GT1 gonadotropin-releasing hormone neuronal cell lines. Endocrinology 1995;136:3831–3838.

    Article  PubMed  CAS  Google Scholar 

  101. Galbiati M, Magnaghi V, Martini L, Melcangi RC. Hypothalamic transforming growth factor β1 and basic fibroblast growth factor mRNA expression is modified during the rat oestrous cycle. J Neuroendocrinol 2001;13:483–489.

    Article  PubMed  CAS  Google Scholar 

  102. Galbiati M, Martini L, Melcangi RC. Oestrogens, via transforming growth factor _, modulate basic fibroblast growth factor synthesis in hypothalamic astrocytes: in vitro observations. J Neuroendocrinol 2002;14:829–835.

    Article  PubMed  CAS  Google Scholar 

  103. Handelsman DJ, Spaliviero JA, Scott CD, Baxter RC. Hormonal regulation of the peripubertal surge of insulin-like growth factor-I in the rat. Endocrinology 1987;120:491–496.

    Article  PubMed  CAS  Google Scholar 

  104. Copeland KC, Eichberg JW, Parker CR Jr, Bartke A. Puberty in the chimpanzee: somatomedin-C and its relationship to somatic growth and steroid hormone concentrations. J Clin Endocrinol Metab 1985;60:1154–1160.

    Article  PubMed  CAS  Google Scholar 

  105. Grumbach MM, Styne DM. Puberty: ontogeny, neuroendocrinology, physiology, and disorders. In: Williams RH, Foster DW, Kroenenberg H, Larsen PR, Zorab R, editors. Williams Textbook of Endocrinology, 9th edition. Philadelphia, PA: W.B. Saunders, 1998:1509–1625.

    Google Scholar 

  106. Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 1996;137:3717–3728.

    Article  PubMed  CAS  Google Scholar 

  107. Garcia-Segura LM, Naftolin F, Hutchison JB, Azcoitia I, Chowen JA. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J Neurobiol 1999;40:574–584.

    Article  PubMed  CAS  Google Scholar 

  108. Dueñas M, Luquin S, Chowen JA, Torres-Aleman I, Naftolin F, Garcia-Segura LM. Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats. Neuroendocrinology 1994;59:528–538.

    Article  PubMed  Google Scholar 

  109. Wilson ME. Premature elevation in serum insulin-like growth factor-I advances first ovulation in rhesus monkeys. J Endocrinol 1998;158:247–257.

    Article  PubMed  CAS  Google Scholar 

  110. Danilovich N, Wernsing D, Coschigano KT, Kopchick JJ, Bartke A. Deficits in female reproductive function in GH-R-KO mice; role of IGF-I. Endocrinology 1999;140:2637–2640.

    Article  PubMed  CAS  Google Scholar 

  111. Ojeda SR, Ma YJ, Lee BJ, Prevot V. Glia-to-neuron signaling and the neuroendocrine control of female puberty. Recent Prog Horm Res 2000;55:197–224.

    PubMed  CAS  Google Scholar 

  112. Ma YJ, Hill DF, Junier M-P, Costa ME, Felder SE, Ojeda SR. Expression of epidermal growth factor receptor changes in the hypothalamus during the onset of female puberty. Mol Cell Neurosci 1994;5:246–262.

    Article  PubMed  CAS  Google Scholar 

  113. Ma YJ, Hill DF, Creswick KE, Costa ME, Ojeda SR. Neuregulins signaling via a glial erbB2/erbB4 receptor complex contribute to the neuroendocrine control of mammalian sexual development. J Neurosci 1999;19:9913–9927.

    PubMed  CAS  Google Scholar 

  114. Ma YJ, Berg-von der Emde K, Rage F, Wetsel WC, Ojeda SR. Hypothalamic astrocytes respond to transforming growth factor alpha with secretion of neuroactive substances that stimulate the release of luteinizing hormone-releasing hormone. Endocrinology 1997;138:19–25.

    Article  PubMed  CAS  Google Scholar 

  115. Rage F, Lee BJ, Ma YJ, Ojeda SR. Estradiol enhances prostaglandin E2 receptor gene expression in luteinizing hormone-releasing hormone (LHRH) neurons and facilitates the LHRH response to PGE2 by activating a glia-to-neuron signaling pathway. J Neurosci 1997;17:9145–9156.

    PubMed  CAS  Google Scholar 

  116. Ojeda SR, Prevot V, Heger S, Lomniczi A, Dziedzic B, Mungenast A. Glia-to neuron signaling and the neuroendocrine control of female puberty. Ann Med 2003;35:244–255.

    Article  PubMed  Google Scholar 

  117. Ma YJ, Junier M-P, Costa ME, Ojeda SR. Transforming growth factor alpha (TGFα) gene expression in the hypothalamus is developmentally regulated and linked to sexual maturation. Neuron 1992;9:657–670.

    Article  PubMed  CAS  Google Scholar 

  118. Apostolakis EM, Garai J, Lohmann JE, Clark JH, O’Malley BW. Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents. Mol Endocrinol 2000;14:1086–1098.

    Article  PubMed  CAS  Google Scholar 

  119. Ma YJ, Dissen GA, Merlino G, Coquelin A, Ojeda SR. Overexpression of a human transforming growth factor alpha (TGFα) transgene reveals a dual antagonistic role of TGFα in female sexual development. Endocrinology 1994;135:1392–1400.

    Article  PubMed  CAS  Google Scholar 

  120. Rage F, Hill DF, Sena-Esteves M et al. Targeting transforming growth factor α expression to discrete loci of the neuroendocrine brain induces female sexual precocity. Proc Natl Acad Sci USA 1997;94:2735–2740.

    Article  PubMed  CAS  Google Scholar 

  121. Prevot V, Rio C, Cho GJ et al. Normal female sexual development requires neuregulin-erbB receptor signaling in hypothalamic astrocytes. J Neurosci 2003;23:230–239.

    PubMed  CAS  Google Scholar 

  122. Prevot V, Lomniczi A, Corfas G, Ojeda SR. ErbB-1 and erbB-4 receptors act in concert to facilitate both female sexual development and mature reproductive function. Endocrinology 2005;146:1465–1472.

    Article  PubMed  CAS  Google Scholar 

  123. Meijs-Roelofs HMA, Kramer P, Sander HJ. Changes in serum concentrations of luteinizing hormone in the female rat approaching puberty. J Endocrinol 1983;98:241–249.

    Article  PubMed  CAS  Google Scholar 

  124. Urbanski HF, Ojeda SR. Gonadal-independent activation of enhanced afternoon luteinizing hormone release during pubertal development in the female rat. Endocrinology 1987;121:907–913.

    Article  PubMed  CAS  Google Scholar 

  125. Urbanski HF, Ojeda SR. Development of afternoon minisurges of luteinizing hormone secretion in prepubertal female rats is ovary dependent. Endocrinology 1986;118:1187–1193.

    Article  PubMed  CAS  Google Scholar 

  126. Urbanski HF, Ojeda SR. In vitro simulation of prepubertal changes in pulsatile luteinizing hormone release enhances progesterone and 17β-estradiol secretion from immature ovaries. Endocrinology 1985;117:638–643.

    Article  PubMed  CAS  Google Scholar 

  127. Urbanski HF, Ojeda SR. The juvenile-peripubertal transition period in the female rat: establishment of a diurnal pattern of pulsatile luteinizing hormone secretion. Endocrinology 1985;117:644–649.

    Article  PubMed  CAS  Google Scholar 

  128. Sisk CL, Richardson HN, Chappell PE, Levine JE. In vivo gonadotropin-releasing hormone secretion in female rats during peripubertal development and on proestrus. Endocrinology 2001;142:2929–2936.

    Article  PubMed  CAS  Google Scholar 

  129. Sarkar DK, Fink G. Mechanism of the first spontaneous gonadotrophin surge and that induced by pregnant mare serum and effects of neonatal androgen in the rat. J Endocrinol 1979;83:339–354.

    Article  PubMed  CAS  Google Scholar 

  130. Aiyer MS, Fink G. The role of sex steroid hormones in modulating the responsiveness of the anterior pituitary gland to luteinizing hormone releasing factor in the female rat. J Endocrinol 1974;62:553–572.

    Article  PubMed  CAS  Google Scholar 

  131. Advis JP, Andrews WW, Ojeda SR. Changes in ovarian steroidal and prostaglandin E responsiveness to gonadotropins during the onset of puberty in the female rat. Endocrinology 1979;104:653–658.

    Article  PubMed  CAS  Google Scholar 

  132. Parker CR Jr, Mahesh VB. Hormonal events surrounding the natural onset of puberty in female rats. Biol Reprod 1976;14:347–353.

    Article  PubMed  CAS  Google Scholar 

  133. Andrews WW, Advis JP, Ojeda SR. The first proestrus in the female rat: circulating steroid levels preceding and accompanying the preovulatory LH surge. Proc Soc Exp Biol Med 1980;163: 305–309.

    PubMed  CAS  Google Scholar 

  134. Kim K, Ramirez VD. In vitro progesterone stimulates the release of luteinizing hormone-releasing hormone from superfused hypothalamic tissue from ovariectomized estradiol-primed prepubertal rats. Endocrinology 1982;111:750–757.

    Article  PubMed  CAS  Google Scholar 

  135. Kinoshita M, Tsukamura H, Adachi S et al. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005;146:4431–4436.

    Article  PubMed  CAS  Google Scholar 

  136. Ma YJ, Berg-von der Emde K, Moholt-Siebert M, Hill DF, Ojeda SR. Region-specific regulation of transforming growth factor α (TGFα) gene expression in astrocytes of the neuroendocrine brain. J Neurosci 1994;14:5644–5651.

    Google Scholar 

  137. Terasawa E. Hypothalamic control of the onset of puberty. Curr Opin Endocrinol Diabetes 1999;6:44–49

    Article  Google Scholar 

  138. Ojeda SR, Bilger M. In: Conn PM, Freeman ME, editors. Neuroendocrinology in Physiology and Medicine. Totowa, NJ: Humana Press, 1999;197–224.

    Google Scholar 

  139. Bourguignon J-P, Gérard A, Alvarez-Gonzalez M-L, Fawe L, Franchimont P. Gonadal-independent developmental changes in activation of N-methyl-D-aspartate receptors involved in gonadotropinreleasing hormone secretion. Neuroendocrinology 1992;55:634–641.

    Article  PubMed  CAS  Google Scholar 

  140. Gore AC, Wu TJ, Rosenberg JJ, Roberts JL. Gonadotropin-releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats. J Neurosci 1996;16:5281–5289.

    PubMed  CAS  Google Scholar 

  141. Price MT, Olney JW, Cicero TJ. Acute elevations of serum luteinizing hormone induced by kainic acid, N-methyl aspartic acid or homocystic acid. Neuroendocrinology 1978;26:352–358.

    Article  PubMed  CAS  Google Scholar 

  142. Seeburg PH. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 1993;16:359–365.

    Article  PubMed  CAS  Google Scholar 

  143. Bourguignon J-P, Gerard A, Alvarez Gonzalez M-L, Purnelle G, Franchimont P. Endogenous glutamate involvement in pulsatile secretion of gonadotropin-releasing hormone: evidence from effect of glutamine and developmental changes. Endocrinology 1995;136:911–916.

    Article  PubMed  CAS  Google Scholar 

  144. Shimshek DR, Bus T, Grinevich V et al. Impaired reproductive behavior by lack of GluR-B containing AMPA receptors but not of NMDA receptors in hypothalamic and septal neurons. Mol Endocrinol 2006;20:219–231.

    Article  PubMed  CAS  Google Scholar 

  145. Navarro VM, Castellano JM, Fernández-Fernández R et al. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004;145:4565–4574.

    Article  PubMed  CAS  Google Scholar 

  146. Castellano JM, Navarro VM, Fernandez-Fernandez R et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005;146:3917–3925.

    Article  PubMed  CAS  Google Scholar 

  147. Jarry H, Perschl A, Wuttke W. Further evidence that preoptic anterior hypothalamic GABAergic neurons are part of the GnRH pulse and surge generator. Acta Endocrinol 1988; 118:573–579.

    PubMed  CAS  Google Scholar 

  148. Akema T, Kimura F. Modulation of pulsatile LH secretion by baclofen, a selective GABAB receptor agonist, in ovariectomized rats. Neuroendocrinology 1992;56:141–147.

    Article  PubMed  CAS  Google Scholar 

  149. Wilkinson M, Bhanot R. A puberty-related attenuation of opiate peptide-induced inhibition of LH secretion. Endocrinology 1982;110:1046–1048.

    Article  PubMed  CAS  Google Scholar 

  150. Blank MS, Mann DR. Diurnal influences on serum luteinizing hormone responses to opiate receptor blockade with naloxone or to luteinizing hormone-releasing hormone in the immature female rat. Proc Soc Exp Biol Med 1981;168:338–343.

    PubMed  CAS  Google Scholar 

  151. van den Pol AN, Gao X-B, Patrylo PR, Ghosh PK, Obrietan K. Glutamate inhibits GABA excitatory activity in developing neurons. J Neurosci 1998;18:10749–10761.

    PubMed  Google Scholar 

  152. Min M-Y, Melyan Z, Kullmann DM. Synaptically released glutamate reduces γ-aminobutyric acid (GABA)ergic inhibition in the hippocampus via kainate receptors. Proc Natl Acad Sci USA 1999;96:9932–9937.

    Article  PubMed  CAS  Google Scholar 

  153. Rodriguez-Moreno A, Herreras O, Lerma J. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 1997;19:893–901.

    Article  PubMed  CAS  Google Scholar 

  154. Rodriguez-Moreno A, Lerma J. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 1998;20:1211–1218.

    Article  PubMed  CAS  Google Scholar 

  155. Satake S, Saitow F, Yamada J, Konishi S. Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 2000;3:551–558.

    Article  PubMed  CAS  Google Scholar 

  156. Clarke VRJ, Ballyk BA, Hoo KH et al. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 1997;389:599–603.

    Article  PubMed  CAS  Google Scholar 

  157. Memo M, Bovolin P, Costa E, Grayson DR. Regulation of γ-aminobutyric acidA receptor subunit expression by activation of N-methyl-D-aspartate-selective glutamate receptors. Mol Pharmacol 1991;39:599–603.

    PubMed  CAS  Google Scholar 

  158. Cherubini E, Gaiarsa JL, Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 1991;14:515–519.

    Article  PubMed  CAS  Google Scholar 

  159. Obrietan K, van den Pol AN. GABA neurotransmission in the hypothalamus: developmental reversal from Ca2+ elevating to depressing. J Neurosci 1995;15:5065–5077.

    PubMed  CAS  Google Scholar 

  160. Chen G, Trombley PQ, van den Pol AN. GABA receptors precede glutamate receptors in hypothalamic development: differential regulation by astrocytes. J Neurophysiol 1995;74:1473–1483.

    PubMed  CAS  Google Scholar 

  161. Insel TR, Miller LP, Gelhard RE. The ontogeny of excitatory amino acid receptors in rat forebrain–I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 1990;35:31–43.

    CAS  Google Scholar 

  162. Heger S, Seney M, Bless E et al. Overexpression of glutamic acid decarboxylase-67 (GAD-67) in GnRH neurons disrupts migratory fate and female reproductive function in mice. Endocrinology 2003;144:2566–2579.

    Article  PubMed  CAS  Google Scholar 

  163. Han SK, Abraham IM, Herbison AE. Effect of GABA on GnRH neurons switches from depolzarization to hyperpolarizationat puberty in the female mouse. Endocrinology 2002;143:1459–1466.

    Article  PubMed  CAS  Google Scholar 

  164. Han SK, Todman MG, Herbison AE. Endogenous GABA release inhibits the firing of adult gonadotropin-releasing neurons. Endocrinology 2004;145:495–499.

    Article  PubMed  CAS  Google Scholar 

  165. Fields RD, Stevens-Graham B. New insights into neuron-glia communication. Science 2002;298:556–562.

    Article  PubMed  CAS  Google Scholar 

  166. Dziedzic B, Prevot V, Lomniczi A, Jung H, Cornea A, Ojeda SR. Neuron-to-glia signaling mediated by excitatory amino acid receptors regulates erbB receptor function in astroglial cells of the neuroendocrine brain. J Neurosci 2003;23:915–926.

    PubMed  CAS  Google Scholar 

  167. Lomniczi A, Cornea A, Costa ME, Ojeda SR. Hypothalamic tumor necrosis factor-α converting enzyme (TACE) mediates excitatory amino acid-dependent neuron-to-glia signaling in the neuroendocrine brain. J Neurosci 2006;26:51–62.

    Article  PubMed  CAS  Google Scholar 

  168. Kang J, Jiang L, Goldman SA, Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1998;1:683–692.

    Article  PubMed  CAS  Google Scholar 

  169. Fraser DD, Mudrick-Donnon LA, MacVicer BA. Astrocytic GABA receptors. Glia 1994;11:83–93.

    Article  PubMed  CAS  Google Scholar 

  170. Verkhratsky A, Steinhauser C. Ion channels in glial cells. Brain Res Rev 2000;32:380–412.

    Article  PubMed  CAS  Google Scholar 

  171. Treacy MN, Rosenfeld MG. Expression of a family of POU-domain protein regulatory genes during development of the central nervous system. Annu Rev Neurosci 1992;15:139–165.

    Article  PubMed  CAS  Google Scholar 

  172. Alvarez-Bolado G, Rosenfeld MG, Swanson LW. Model of forebrain regionalization based on spatiotemporal patterns of POU-III homeobox gene expression, birthdates, and morphological features. J Comp Neurol 1995;355:237–295.

    Article  PubMed  CAS  Google Scholar 

  173. Hatzopoulos AK, Stoykova AS, Erselius JR, Goulding M, Neuman T, Gruss P. Structure and expression of the mouse Oct2a and Oct2b, two differentially spliced products of the same gene. Development 1990;109:349–362.

    PubMed  CAS  Google Scholar 

  174. Ojeda SR, Hill J, Hill DF et al. The Oct-2 POU-domain gene in the neuroendocrine brain: a transcriptional regulator of mammalian puberty. Endocrinology 1999;140:3774–3789.

    Article  PubMed  CAS  Google Scholar 

  175. Kimura S, Hara Y, Pineau T et al. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 1996;10:60–69.

    Article  PubMed  CAS  Google Scholar 

  176. Lee BJ, Cho GJ, Norgren R et al. TTF-1, a homeodomain gene required for diencephalic morphogenesis, is postnatally expressed in the neuroendocrine brain in a developmentally regulated and cell-specific fashion. Mol Cell Neurosci 2001;17:107–126.

    Article  PubMed  CAS  Google Scholar 

  177. Ojeda SR, Lomniczi A, Mungenast A et al. Towards understanding the neurobiology of mammalian puberty: genetic, genomic and proteomic approaches. In: Kordon C, Gaillard R, Christen Y, editors. Hormones and the Brain. Berlin: Springer Verlag, 2005:47–60.

    Google Scholar 

  178. Rampazzo A, Pivotto F, Occhi G et al. Characterization of C14orf4, a novel intronless human gene containing a polyglutamine repeat, mapped to the ARVD1 critical region. Biochem Biophys Res Commun 2000;278:766–774.

    Article  PubMed  CAS  Google Scholar 

  179. Heger S, Mastronardi C, Lomniczi A et al. Role of a novel gene (enhanced at puberty, EAP-1) in the regulation of female puberty. Horm Res 2005;64(Suppl 1):22.

    Google Scholar 

  180. Barraclough CA, Wise PM. The role of catecholamines in the regulation of pituitary luteinizing hormone and follicle-stimulating hormone secretion. Endocr Rev 1982;3:91–119.

    Article  Google Scholar 

  181. Kalra SP, Crowley WR. Neuropeptide Y: a novel neuroendocrine peptide in the control of pituitary hormone secretion, and its relation to luteinizing hormone. In: Ganong WF, Martini L, editors. Frontiers in Neuroendocrinology, Vol 13. New York: Raven Press, 1992:1–46.

    Google Scholar 

  182. Turek FW, Van Cauter E. Rhythms in reproduction. In: Knobil E, Neill JD, editors. The Physiology of Reproduction, 2nd edition. New York: Raven Press, 1994:487–540.

    Google Scholar 

  183. VanderBeekEM.Circadiancontrolofreproductioninthefemalerat.ProgBrainRes1996;111:295–320.

    CAS  Google Scholar 

  184. Van der Beek EM, Wiegant VM, Vander Donk HA, van den HR, Buijs RM. Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotropin-releasing hormone neurons in the female rat. J Neuroendocrinol 1993;5:137–144.

    Article  PubMed  Google Scholar 

  185. Funabashi T, Shinohara K, Mitsushima D, Kimura F. Gonadotropin-releasing hormone exhibits circadian rhythm in phase with arginine-vasopressin in co-cultures of the female rat preoptic area and suprachiasmatic nucleus. J Neuroendocrinol 2000;12:521–528.

    Article  PubMed  CAS  Google Scholar 

  186. van den Pol AN, Finkbeiner SM, Cornell-Bell AH. Calcium excitability and oscillations in suprachiasmatic nucleus neurons and glia in vitro. J Neurosci 1992;12:2648–2664.

    PubMed  Google Scholar 

  187. Cagampang FRA, Rattray M, Powell JF, Campbell IC, Coen CW. Circadian changes of glutamate decarboxylase 65 and 67 mRNA in the rat suprachiasmatic nuclei. Neuroreport 1996;7:1925–1928.

    Article  PubMed  CAS  Google Scholar 

  188. Shibata S, Liou SY, Ueki S. Influence of excitatory amino acid receptor antagonists and of baclofen on synaptic transmission in the optic nerve to the suprachiasmatic nucleus in slices of rat hypothalamus. Neuropharmacology 1986;25:403–409.

    Article  PubMed  CAS  Google Scholar 

  189. van der Horst GTJ, Muijtjens M, Kobayashi K et al. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 1999;398:627–630.

    Article  PubMed  Google Scholar 

  190. Krewson TD, Supelak PJ, Hill AE et al. Chromosomes 6 and 13 harbor genes that regulate pubertal timing in mouse chromosome substitution strains. Endocrinology 2004;145:4447–4451.

    Article  PubMed  CAS  Google Scholar 

  191. Yoon H, Enquist LW, Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 2005;123:669–682.

    Article  PubMed  CAS  Google Scholar 

  192. Vandenbergh JG. Pheromones and mammalian reproduction. In: Neill JD, editor. The Physiology of Reproduction, 3 rd edition. San Diego, CA: Academic Press/Elsevier, 2006:2041–2058.

    Google Scholar 

  193. Cheung CC, Thornton JE, Nurani SD, Clifton DK, Steiner RA. A reassessment of leptin’s role in triggering the onset of puberty in the rat and mouse. Neuroendocrinology 2001;74:12–21.

    Article  PubMed  CAS  Google Scholar 

  194. Stoker TE, Parks LG, Gray LE, Cooper RL. Endocrine-disrupting chemicals: prepubertal exposures and effects on sexual maturation and thyroid function in the male rat. A focus on the EDSTAC recommendations. Endocrine Disrupter Screening and Testing Advisory Committee. Crit Rev Toxicol 2000;30:197–252.

    Article  PubMed  CAS  Google Scholar 

  195. Parent AS, Rasier G, Gerard A et al. Early onset of puberty: tracking genetic and environmental factors. Horm Res 2005;64(Suppl 2):41–47.

    Article  PubMed  CAS  Google Scholar 

  196. Atanassova N, McKinnell C, Turner KJ et al. Comparative effects of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and the relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology 2000;141:3898–3907.

    Article  PubMed  CAS  Google Scholar 

  197. Kuwada M, Kawashima R, Nakamura K et al. Neonatal exposure to endocrine disruptors suppresses juvenile testis weight and steroidogenesis but spermatogenesis is considerably restored during puberty. Biochem Biophys Res Commun 2002;295:193–197.

    Article  PubMed  CAS  Google Scholar 

  198. Masutomi N, Shibutani M, Takagi H, Uneyama C, Takahashi N, Hirose M. Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life. Toxicology 2003;192:149–170.

    Article  PubMed  CAS  Google Scholar 

  199. Nagao T, Yoshimura S, Saito Y, Nakagomi M, Usumi K, Ono H. Reproductive effects in male and female rats of neonatal exposure to genistein. Reprod Toxicol 2001;15:399–411.

    Article  PubMed  CAS  Google Scholar 

  200. Tan BL, Kassim NM, Mohd MA. Assessment of pubertal development in juvenile male rats after sub-acute exposure to bisphenol A and nonylphenol. Toxicol Lett 2003;143:261–270.

    Article  PubMed  CAS  Google Scholar 

  201. Kwon S, Stedman DB, Elswick BA, Cattley RC, Welsch F. Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol Sci 2000;55:399–406.

    Article  PubMed  CAS  Google Scholar 

  202. Stoker TE, Laws SC, Guidici DL, Cooper RL. The effect of atrazine on puberty in male wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol Sci 2000;58:50–59.

    Article  PubMed  CAS  Google Scholar 

  203. Stoker TE, Guidici DL, Laws SC, Cooper RL. The effects of atrazine metabolites on puberty and thyroid function in the male Wistar rat. Toxicol Sci 2002;67:198–206.

    Article  PubMed  CAS  Google Scholar 

  204. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005;308:1466–1469.

    Article  PubMed  CAS  Google Scholar 

  205. Lutz W, O’Neill BC, Scherbov S. Demographics. Europe’s population at a turning point. Science 2003;299:1991–1992.

    CAS  Google Scholar 

  206. Jensen TK, Carlsen E, Jorgensen N et al. Poor semen quality may contribute to recent decline in fertility rates. Hum Reprod 2002;17:1437–1440.

    Article  PubMed  Google Scholar 

  207. Krstevska-Konstantinova M, Charlier C, Craen M et al. Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod 2001;16:1020–1026.

    Article  PubMed  CAS  Google Scholar 

  208. Parent AS, Krstevska-Konstantinova M, Matagne V et al. Endocrine disrupter contribution to sexual precocity: suggestive detection of pesticide derivatives in patients immigrant to Belgium and stimulation of GnRH pulsatility in rat hypothalamus. Pediatr Res 2001;49:139A.

    Article  Google Scholar 

  209. Rasier G, Matagne V, Parent AS, Gerard A, Lebrethon M-C, Bourguignon J-P. Estradiol (E2) and dichlorodiphenyltrichloroethane (DTT) administration in infantile female rats: similar stimulation of gonadotropin-releasing hormone (GnRH) secretion in vitro and sexual maturation in vivo through different receptor mechanisms. Programs and Abstracts of the 87th Annual Meeting of the Endocrine Society; June 4–7, San Diego, CA, 2005:190.

    Google Scholar 

  210. Ojeda SR, Heger S. New thoughts on female precocious puberty. J Pediatr Endocrinol Metab 2001;14:245–256.

    Article  PubMed  CAS  Google Scholar 

  211. Jiang Y-H, Lev-Lehman E, Bressler J, Tsai T-F, Beaudet AL. Genetics of Angelman syndrome. Am J Hum Genet 1999;65:1–6.

    Article  PubMed  CAS  Google Scholar 

  212. Bourguignon J-P, Jaeken J, Gerard A, de Zegher F. Amino acid neurotransmission and initiation of puberty: evidence from nonketotic hyperglycinemia in a female infant and gonadotropin-releasing hormone secretion by rat hypothalamic explants. J Clin Endocrinol Metab 1997;82:1899–1903.

    Article  PubMed  CAS  Google Scholar 

  213. Teles MG, Bianco SC, Brito VN et al. An activating mutation in GPR54 gene causes gonadotropindependent precocious puberty. Programs and Abstracts of the 88th Annual Meeting of the Endocrine Society; June 24–27, Boston, MA, 2006.

    Google Scholar 

  214. Nicholls RD. The impact of genomic imprinting for neurobehavioral and developmental disorders. J Clin Invest 2000;105:413–418.

    Article  PubMed  CAS  Google Scholar 

  215. Knoll JHM, Nicholls RD, Magenis RE, Graham JM Jr, Lalande M, Latt SA. Angelman and Prader- Willi syndromes share a common chromosome 15 deletion but differ in parental origin of the deletion. Am J Med Genet 1989;32:285–290.

    Article  PubMed  CAS  Google Scholar 

  216. Nicholls RD, Gottlieb W, Russell LB, Davda M, Horsthemke B, Rinchik EM. Evaluation of potential models for imprinted and nonimprinted components of human chromosome 15q11-q13 syndromes by fine-structure homology mapping in the mouse. Proc Natl Acad Sci USA 1993;90:2050–2054.

    Article  PubMed  CAS  Google Scholar 

  217. Ebert MH, Schmidt DE, Thompson T, Butler MG. Elevated plasma gamma-aminobutyric acid (GABA) levels in individuals with either Prader-Willi syndrome or Agelman syndrome. J Neuropsychiatry Clin Neurosci 1997;9:75–80.

    PubMed  CAS  Google Scholar 

  218. Culiat CT, Stubbs LJ, Montgomery CS, Russell LB, Rinchik EM. Phenotypic consequences of deletion of the γ3, α5, or β3 subunit of the type A γ-aminobutyric acid receptor in mice. Proc Natl Acad Sci USA 1994;91:2815–2818.

    Article  PubMed  CAS  Google Scholar 

  219. Homanics GE, DeLorey TM, Firestone LL et al. Mice devoid of γ-aminobutyrate type A receptor β3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci USA 1997;94:4143–4148.

    Article  PubMed  CAS  Google Scholar 

  220. Jung H, Carmel P, Schwartz MS et al. Some hypothalamic hamartomas contain transforming growth factor alpha, a puberty-inducing growth factor, but not luteinizing hormone-releasing hormone neurons. J Clin Endocrinol Metab 1999;84:4695–4701.

    Article  PubMed  CAS  Google Scholar 

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Authors
  1. Sabine Heger MD
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  2. Sergio R. Ojeda DVM
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Editors and Affiliations

  1. Departments of Pediatrics and Cellular and Integrative Physiology, Riley Hospital for Children, Indiana University School of Medicine, Indianapolis, IN

    Ora H. Pescovitz MD

  2. Section of Pediatric Endocrinology and Diabetology, Department of Pediatrics, Riley Hospital for Children, Indiana University School of Medicine, Indianapolis, IN, USA

    Emily C. Walvoord MD

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Heger, S., Ojeda, S.R. (2007). Control Puberty in Rodents. In: Pescovitz, O.H., Walvoord, E.C. (eds) When Puberty is Precocious. Contemporary Endocrinology. Humana Press. https://doi.org/10.1007/978-1-59745-499-5_1

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  • DOI: https://doi.org/10.1007/978-1-59745-499-5_1

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-58829-742-6

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