The two kisspeptin neuronal populations are differentially organized and activated by estradiol in mice

Endocrinology

Volumn 154, Issue 8, 2013, Pages 2739-2749

  Brock, Olivier ^a   Bakker, Julie ^a,b,c  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTANOLONE; AROMATASE; ESTRADIOL; KISSPEPTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; GENE SILENCING; GENOTYPE; GONADECTOMY; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; WILD TYPE;

ANDROGENS; ANIMALS; ARCUATE NUCLEUS; AROMATASE; CASTRATION; CELL COUNT; DIHYDROTESTOSTERONE; ESTRADIOL; ESTROGENS; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; KISSPEPTINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; SEX FACTORS; TIME FACTORS;

EID: 84880649633     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1120     Document Type: Article

References (57)

1. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology. 2006; 147:5817-5825.
2. Kauffman AS, Gottsch ML, Roa J, et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology. 2007; 148:1774-1783.
3. Clarkson J, Boon WC, Simpson ER, Herbison AE. Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology. 2009;150:3214-3220.
4. Smith JT, Clifton DK, Steiner RA. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction. 2006;131:623-630.
5. Roa J, Tena-Sempere M. KiSS-1 system and reproduction: Comparative aspects and roles in the control of female gonadotropic axis in mammals. Gen Comp Endocrinol. 2007;153:132-140.
6. Castellano JM, Roa J, Luque RM, et al. KiSS-1/kisspeptins and the metabolic control of reproduction: Physiologic roles and putative physiopathological implications. Peptides. 2009;30:139-145.
7. Simonneaux V, Ansel L, Revel FG, Klosen P, Pévet P, Mikkelsen JD. Kisspeptin and the seasonal control of reproduction in hamsters. Peptides. 2009;30:146-153.
8. Kauffman AS, Park JH, McPhie-Lalmansingh AA, et al. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci. 2007;27:8826-8835.
9. Gottsch ML, Cunningham MJ, Smith JT, et al.Arole for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology. 2004;145:4073-4077.
10. 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.
11. Smith JT, Dungan HM, Stoll EA, et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology. 2005;146:2976-2984.
12. Bellingham M, Fowler PA, Amezaga MR, et al. Exposure to a complex cocktail of environmental endocrine-disrupting compounds disturbs the kisspeptin/GPR54 system in ovine hypothalamus and pituitary gland. Environ Health Perspect. 2009;117:1556-1562.
13. Homma T, Sakakibara M, Yamada S, et al. Significance of neonatal testicular sex steroids to defeminize anteroventral periventricular kisspeptin neurons and theGnRH/LHsurge system in male rats. Biol Reprod. 2009;81:1216-1225.
14. Takase K, Uenoyama Y, Inoue N, et al. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol. 2009;21:527-537.
15. Adachi S, Yamada S, Takatsu Y, et al. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev. 2007;53:367-378.
16. PolingMC,Kauffman AS. Organizational and activational effects of sex steroids on kisspeptin neuron development. Front Neuroendocrinol. 2013;34:3-17.
17. Bakker J, Pierman S, González-Martinez D. Effects of aromatase mutation (ArKO) on the sexual differentiation of kisspeptin neuronal numbers and their activation by same versus opposite sex urinary pheromones. Horm Behav. 2010;57:390-395.
18. Gonzalez-Martinez D, De Mees C, Douhard Q, Szpirer C, Bakker J. Absence of gonadotropin-releasing hormone 1 and Kiss1 activation in ?-fetoprotein knockout mice: Prenatal estrogens defeminize the potential to show preovulatory luteinizing hormone surges. Endocrinology. 2008;149:2333-2340.
19. Tsukamura H, Homma T, Tomikawa J, Uenoyama Y, Maeda K. Sexual differentiation of kisspeptin neurons responsible for sex difference in gonadotropin release in rats. Ann N Y Acad Sci. 2010; 1200:95-103.
20. XuZ, Kaga S, Mochiduki A, et al. Immunocytochemical localization of kisspeptin neurons in the rat forebrain with special reference to sexual dimorphism and interaction with GnRH neurons. Endocr J. 2012;59:161-171.
21. Desroziers E, Droguerre M, Bentsen AH, et al. Embryonic development of kisspeptin neurones in rat. J Neuroendocrinol. 2012;24: 1284-1295.
22. Cao J, Mickens JA, McCaffrey KA, Leyrer SM, Patisaul HB. Neonatal bisphenol A exposure alters sexually dimorphic gene expression in the postnatal rat hypothalamus. Neurotoxicology. 2012;33: 23-36.
23. Desroziers E, Mikkelsen JD, Duittoz A, Franceschini I. Kisspeptinimmunoreactivity changes in a sex-and hypothalamic-region-specific manner across rat postnatal development. J Neuroendocrinol. 2012;24:1154-1165.
24. Takumi K, Iijima N, Ozawa H. Developmental changes in the expression of kisspeptin mRNA in rat hypothalamus. J Mol Neurosci. 2011;43:138-145.
25. Bentsen AH, Ansel L, Simonneaux V, Tena-Sempere M, Juul A, Mikkelsen JD. Maturation of kisspeptinergic neurons coincides with puberty onset in male rats. Peptides. 2010;31:275-283.
26. 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.
27. True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokininBneuronal projections and regulation during lactation in the rat. J Neuroendocrinol. 2011;23: 52-64.
28. Brock O, Baum MJ, Bakker J. The development of female sexual behavior requires prepubertal estradiol. J Neurosci. 2011;31:5574-5578.
29. Honda S, Harada N, Ito S, Takagi Y, Maeda S. Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene. Biochem Biophys Res Commun. 1998;252:445-449.
30. Brock O, Bakker J. Potential contribution of prenatal estrogens to the sexual differentiation of mate preferences in mice. Horm Behav. 2011;59:83-89.
31. Bakker J, Honda S, Harada N, Balthazart J. The aromatase knockout mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J Neurosci. 2002;22:9104-9112.
32. Singh J, O'Neill C, Handelsman DJ. Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology. 1995;136:5311-5321.
33. Szymanski L, Bakker J. Aromatase knockout mice show normal steroid-induced activation of gonadotrophin-releasing hormone neurones and luteinising hormone surges with a reduced population of kisspeptin neurones in the rostral hypothalamus. J Neuroendocrinol. 2012;24:1222-1233.
34. Paxinos G, Franklin KB. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press; 2001.
35. Brock O, Douhard Q, Baum MJ, Bakker J. Reduced prepubertal expression of progesterone receptor in the hypothalamus of female aromatase knockout mice. Endocrinology. 2010;151:1814-1821.
36. Kauffman AS. Gonadal and nongonadal regulation of sex differences in hypothalamic Kiss1 neurones. J Neuroendocrinol. 2010; 22:682-691.
37. Iijima N, Takumi K, Sawai N, Ozawa H. An immunohistochemical study on the expressional dynamics of kisspeptin neurons relevant toGnRHneurons using a newly developed anti-kisspeptin antibody. J Mol Neurosci. 2011;43:146-154.
38. Gill JC, Wang O, Kakar S, Martinelli E, Carroll RS, Kaiser UB. Reproductive hormone-dependent and-independent contributions to developmental changes in kisspeptin in GnRH-deficient hypogonadal mice. PLoS ONE. 2010;5:e11911.
39. Mannan MA, O'Shaughnessy PJ. Steroidogenesis during postnatal development in the mouse ovary. J Endocrinol. 1991;130:101-106.
40. Andrews WW, Advis JP, Ojeda SR. The maturation of estradiolnegative feedback in female rats: Evidence that the resetting of the hypothalamic "gonadostat" does not precede the first preovulatory surge of gonadotropins. Endocrinology. 1981;109:2022-2031.
41. Conte FA, Grumbach MM, Kaplan SL. A diphasic pattern of gonadotropin secretion in patients with the syndrome of gonadal dysgenesis. J Clin Endocrinol Metab. 1975;40:670-674.
42. Plant TM, Barker-Gibb ML. Neurobiological mechanisms of puberty in higher primates. Hum Reprod Update. 2004;10:67-77.
43. Fiorini Z, Jasoni CL.Anovel developmental role for kisspeptin in the growth of gonadotrophin-releasing hormone neurites to the median eminence in the mouse. J Neuroendocrinol. 2010;22:1113-1125.
44. Knoll J, Clay C, Henion T, Schwarting GA, Tobet S. Sex difference in kisspeptin mRNA during murine development. Program of the 90th Annual Meeting of The Endocrine Society, 2008; San Francisco, CA. Abstract P1-680.
45. Han SK, Gottsch ML, Lee KJ, et al. Activation of gonadotropinreleasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25:11349-11356.
46. Kauffman AS, Navarro VM, Kim J, Clifton DK, Steiner RA. Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: Implications for the timing of puberty. Am J Physiol Endocrinol Metab. 2009;297:E1212-E1221.
47. Polston EK, Simerly RB. Ontogeny of the projections from the anteroventral periventricular nucleus of the hypothalamus in the female rat. J Comp Neurol. 2006;495:122-132.
48. Bouret SG, Draper SJ, Simerly RB. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci. 2004;24:2797-2805.
49. Caron E, Ciofi P, Prevot V, Bouret SG. Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J Neurosci. 2012;32:11486-11494.
50. Yeo SH, Herbison AE. Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology. 2011;152:2387-2399.
51. KimJ, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, Kauffman AS. Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology. 2011;152:2020-2030.
52. Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L. An alternate pathway for androgen regulation of brain function: Activation of estrogen receptor α by the metabolite of dihydrotestosterone, 5'-androstane-3β,17β-diol. Horm Behav. 2008;53:741-752.
53. Lund TD, Hinds LR, Handa RJ. The androgen 5'-dihydrotestosterone and its metabolite 5'-androstan-3',17?-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus. J Neurosci. 2006;26:1448-1456.
54. Lederman MA, Lebesgue D, Gonzalez VV, et al. Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats. Neuropharmacology. 2010;58:314-320.
55. Bateman HL, Patisaul HB. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology. 2008; 29:988-997.
56. Patisaul HB, Todd KL, Mickens JA, Adewale HB. Impact of neonatal exposure to the ERα agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology. 2009;30:350-357.
57. PatisaulHB,Losa-WardSM,ToddKL, McCaffreyKA,Mickens JA. Influence ofERα selective agonism during the neonatal period on the sexual differentiation of the rat hypothalamic-pituitary-gonadal (HPG) axis. Biol Sex Differ. 2012;3:2.