Developmental GnRH signaling is not required for sexual differentiation of kisspeptin neurons but is needed for maximal Kiss1 gene expression in adult females

Endocrinology

Volumn 154, Issue 9, 2013, Pages 3273-3283

  Kim, Joshua ^a   Tolson, Kristen P ^a   Dhamija, Sangeeta ^a   Kauffman, Alexander S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; GONADORELIN; KISSPEPTIN;

ADULTHOOD; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEMALE; FEMINIZATION; GENE; GENE EXPRESSION; KISS1 GENE; MOUSE; NERVE CELL; NONHUMAN; OVARY; PRIORITY JOURNAL; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTERIOR THALAMIC NUCLEI; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; GONADOTROPIN-RELEASING HORMONE; HYPOGONADISM; INTRALAMINAR THALAMIC NUCLEI; KISSPEPTINS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NERVE TISSUE PROTEINS; NEURONS; OVARIECTOMY; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; THALAMIC NUCLEI; UP-REGULATION;

EID: 84883200940     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1271     Document Type: Article

References (37)

1. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, 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.
2. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614-1627.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release viaGprotein-coupled receptor 54. Proc Natl Acad Sci USA. 2005;102:1761-1766.
10. WuM, Dumalska I, Morozova E, van den Pol A, Alreja M. Melaninconcentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction. Proc Natl Acad Sci USA. 2009;106:17217-17222.
11. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev. 2008;57:277-287.
12. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci. 2006;26: 6687-6694.
13. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS. Circadian regulation of Kiss1 neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge. Endocrinology. 2009;150:3664-3671.
14. Williams WP 3rd, Jarjisian SG, Mikkelsen JD, Kriegsfeld LJ. Circadian control of kisspeptin and a gatedGnRHresponse mediate the preovulatory luteinizing hormone surge. Endocrinology. 2011;152: 595-606.
15. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, ColledgeWH, Herbison AE. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci. 2008;28:8691-8697.
16. Dror T, Franks J, Kauffman AS. Analysis of multiple positive feedback paradigms demonstrates a complete absence of LH surges and GnRH activation in mice lacking kisspeptin signaling. Biol Reprod. 2013;88:146.
17. 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.
18. Semaan SJ, Murray EK, Poling MC, Dhamija S, Forger NG, Kauffman AS. BAX-dependent and BAX-independent regulation of Kiss1 neuron development in mice. Endocrinology. 2010;151:5807-5817.
19. Takumi K, Iijima N, Ozawa H. Developmental changes in the expression of kisspeptin mRNA in rat hypothalamus. J Mol Neurosci. 2011;43:138-145.
20. Cao J, Patisaul HB. Sexually dimorphic expression of hypothalamic estrogen receptors α and β and Kiss1 in neonatal male and female rats. J Comp Neurol. 2011;519:2954-2977.
21. Poling MC, Kauffman AS. Organizational and activational effects of sex steroids on kisspeptin neuron development. Front Neuroendocrinol. 2013;34:3-17.
22. 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.
23. Semaan SJ, Dhamija S, Kim J, Ku EC, Kauffman AS. Assessment of epigenetic contributions to sexually-dimorphic Kiss1 expression in the anteroventral periventricular nucleus of mice. Endocrinology. 2012;153:1875-1886.
24. Rhees RW, Shryne JE, Gorski RA. Onset of the hormone-sensitiveperinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats. J Neurobiol. 1990;21: 781-786.
25. Rhees RW, Shryne JE, Gorski RA. Termination of the hormonesensitive period for differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res Dev Brain Res. 1990;52:17-23.
26. Schulz KM, Molenda-Figueira HA, Sisk CL. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav. 2009;55:597-604.
27. Sisk CL, Zehr JL. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol. 2005;26:163-174.
28. AhmedEI, Zehr JL, SchulzKM,Lorenz BH, DonCarlos LL, Sisk CL. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci. 2008;11:995-997.
29. Schulz KM, Richardson HN, Zehr JL, Osetek AJ, Menard TA, Sisk CL. Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster. Horm Behav. 2004;45:242-249.
30. 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.
31. 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.
32. Bakker J, Pierman S, González-Martínez 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.
33. Poling MC, Kauffman AS. Sexually dimorphic testosterone secretion in prenatal and neonatal mice is independent of kisspeptin-Kiss1r and GnRH signaling. Endocrinology. 2012;153:782-793.
34. 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.
35. Christian CA, Mobley JL, Moenter SM. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci USA. 2005;102:15682-15687.
36. Chowen JA, Argente J, Vician L, Clifton DK, Steiner RA. Pro-opiomelanocortin messenger RNA in hypothalamic neurons is increased by testosterone through aromatization to estradiol. Neuroendocrinology. 1990;52:581-588.
37. González-Martínez D, De Mees C, Douhard Q, Szpirer C, Bakker J. Absence of gonadotropin-releasing hormone 1 and Kiss1 activation in α-fetoprotein knockout mice: prenatal estrogens defeminize the potential to show preovulatory luteinizing hormone surges. Endocrinology. 2008;149:2333-2340.