Maturation of kisspeptinergic neurons coincides with puberty onset in male rats

Peptides

Volumn 31, Issue 2, 2010, Pages 275-283

  Bentsen, Agnete H ^a,b   Ansel, Laura ^c   Simonneaux, Valerie ^c   Tena Sempere, Manuel ^d,e   Juul, Anders ^a   Mikkelsen, Jens D ^a,b  

^a University of Copenhagen   (Denmark)

^b NEUROSEARCH A S   (Denmark)

^c Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

^d UNIVERSITY OF CÓRDOBA   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Arcuate nucleus; Development; Hypothalamus; In situ hybridization; Kiss1; Kisspeptin; Luteinizing hormone; Ontogeny; Puberty

Indexed keywords

KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA; METASTIN; PEPTIDE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NUCLEUS; CELL MATURATION; CONTROLLED STUDY; EVOKED RESPONSE; GENE EXPRESSION; IMMUNOREACTIVITY; LUTEINIZING HORMONE RELEASE; MALE; NERVE CELL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; PUBERTY; RAT; TESTOSTERONE RELEASE;

ANIMALS; ARCUATE NUCLEUS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LUTEINIZING HORMONE; MALE; NERVOUS SYSTEM; NEURONS; PITUITARY GLAND, ANTERIOR; PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; PUBERTY; RATS; RATS, WISTAR; TESTOSTERONE; THALAMIC NUCLEI;

RATTUS;

EID: 73949110561     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2009.11.017     Document Type: Article

References (52)

1. Altarejos J.Y., Goebel N., Conkright M.D., Inoue H., Xie J., Arias C.M., et al. The Creb1 coactivator Crtc1 is required for energy balance and fertility. Nat Med 14 (2008) 1112-1117
2. Aparicio S.A. Kisspeptins and GPR54--the new biology of the mammalian GnRH axis. Cell Metab 1 (2005) 293-296
3. Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Castano J.P., Malagon M.M., Aguilar E., et al. Ontogeny and mechanisms of action for the stimulatory effect of kisspeptin on gonadotropin-releasing hormone system of the rat. Mol Cell Endocrinol 257-258 (2006) 75-83
4. Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Nogueiras R., Tovar S., Roa J., et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 146 (2005) 3917-3925
5. Cheung C.C., Thornton J.E., Kuijper J.L., Weigle D.S., Clifton D.K., and Steiner R.A. Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 138 (1997) 855-858
6. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., and Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28 (2008) 8691-8697
7. Clarkson J., and Herbison A.E. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147 (2006) 5817-5825
8. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., and Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100 (2003) 10972-10976
9. de Tassigny X.D., Fagg L.A., Carlton M.B., and Colledge W.H. Kisspeptin can stimulate GnRH release by a direct action at GnRH nerve terminals. Endocrinology 149 (2008) 3926-3932
10. Dhillo W.S., Chaudhri O.B., Thompson E.L., Murphy K.G., Patterson M., Ramachandran R., et al. Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 92 (2007) 3958-3966
11. Dhillo W.S., Savage P., Murphy K.G., Chaudhri O.B., Patterson M., Nijher G.M., et al. Plasma kisspeptin is raised in patients with gestational trophoblastic neoplasia and falls during treatment. Am J Physiol Endocrinol Metab 291 (2006) E878-E884
12. Franceschini I., Lomet D., Cateau M., Delsol G., Tillet Y., and Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neuroscience letters 401 (2006) 225-230
13. Funes S., Hedrick J.A., Vassileva G., Markowitz L., Abbondanzo S., Golovko A., et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312 (2003) 1357-1363
14. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145 (2004) 4073-4077
15. Han S.K., Gottsch M.L., Lee K.J., Popa S.M., Smith J.T., Jakawich S.K., et al. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25 (2005) 11349-11356
16. Kauffman A.S., Gottsch M.L., Roa J., Byquist A.C., Crown A., Clifton D.K., et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148 (2007) 1774-1783
17. Keen K.L., Wegner F.H., Bloom S.R., Ghatei M.A., and Terasawa E. An increase in kisspeptin-54 release occurs with the pubertal increase in luteinizing hormone-releasing hormone-1 release in the stalk-median eminence of female rhesus monkeys in vivo. Endocrinology 149 (2008) 4151-4157
18. Korenbrot C.C., Huhtaniemi I.T., and Weiner R.I. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod 17 (1977) 298-303
19. Larsen P.J., Mikkelsen J.D., Jessop D.S., Lightman S.L., and Chowdrey H.S. Neuropeptide Y mRNA and immunoreactivity in hypothalamic neuroendocrine neurons: effects of adrenalectomy and chronic osmotic stimulation. J Neurosci 13 (1993) 1138-1147
20. Matsui H., Takatsu Y., Kumano S., Matsumoto H., and Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 320 (2004) 383-388
21. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 102 (2005) 1761-1766
22. Mikkelsen J.D., Bentsen A.H., Ansel L., Simonneaux V., and Juul A. Comparison of the effects of peripherally administered kisspeptins. Regul Pept 152 (2009) 95-100
23. Mikkelsen J.D., and Simonneaux V. The neuroanatomy of the kisspeptin system in the mammalian brain. Peptides 30 (2009) 26-33
24. Mikkelsen J.D., Vrang N., and Mrosovsky N. Expression of Fos in the circadian system following nonphotic stimulation. Brain Res Bull 47 (1998) 367-376
25. Miller K.K., Rosner W., Lee H., Hier J., Sesmilo G., Schoenfeld D., et al. Measurement of free testosterone in normal women and women with androgen deficiency: comparison of methods. J Clin Endocrinol Metab 89 (2004) 525-533
26. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Barreiro M.L., Roa J., Sanchez-Criado J.E., 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 145 (2004) 4565-4574
27. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., et al. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146 (2005) 1689-1697
28. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146 (2005) 156-163
29. Oakley A.E., Clifton D.K., and Steiner R.A. Kisspeptin signaling in the brain. Endocr Rev 30 (2009) 713-743
30. Pallais J.C., Bo-Abbas Y., Pitteloud N., Crowley Jr. W.F., and Seminara S.B. Neuroendocrine, gonadal, placental, and obstetric phenotypes in patients with IHH and mutations in the G-protein coupled receptor, GPR54. Mol Cell Endocrinol 254-255 (2006) 70-77
31. Parent A.S., Teilmann G., Juul A., Skakkebaek N.E., Toppari J., and Bourguignon J.P. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24 (2003) 668-693
32. Pielecka-Fortuna J., Chu Z., and Moenter S.M. Kisspeptin acts directly and indirectly to increase GnRH neuron activity and its effects are modulated by estradiol. Endocrinology 149 (2008) 1979-1986
33. Plant T.M., Ramaswamy S., and Dipietro M.J. Repetitive activation of hypothalamic G protein-coupled receptor 54 with intravenous pulses of kisspeptin in the juvenile monkey (Macaca mulatta) elicits a sustained train of gonadotropin-releasing hormone discharges. Endocrinology 147 (2006) 1007-1013
34. Ramaswamy S., Guerriero K.A., Gibbs R.B., and Plant T.M. Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 149 (2008) 4387-4395
35. Ramaswamy S., Seminara S.B., Pohl C.R., DiPietro M.J., Crowley Jr. W.F., and Plant T.M. Effect of continuous intravenous administration of human metastin 45-54 on the neuroendocrine activity of the hypothalamic-pituitary-testicular axis in the adult male rhesus monkey (Macaca mulatta). Endocrinology 148 (2007) 3364-3370
36. Roa J., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front Neuroendocrinol 29 (2008) 48-69
37. Seminara S.B., and Kaiser U.B. New gatekeepers of reproduction: GPR54 and its cognate ligand, KiSS-1. Endocrinology 146 (2005) 1686-1688
38. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno Jr. J.S., Shagoury J.K., et al. The GPR54 gene as a regulator of puberty. N Engl J Med 349 (2003) 1614-1627
39. Semple R.K., Achermann J.C., Ellery J., Farooqi I.S., Karet F.E., Stanhope R.G., et al. Two novel missense mutations in G protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. J Clin Endocrinol Metab 90 (2005) 1849-1855
40. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R., and Plant T.M. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 102 (2005) 2129-2134
41. Smith J.T. Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 30 (2009) 94-102
42. Smith J.T., Clifton D.K., and Steiner R.A. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131 (2006) 623-630
43. Sun Y., Tian Z., Zhao H., Wong S.T., and Chen B. Characteristic of hypothalamic kisspeptin expression in the pubertal development of precocious female rats. Neurosci Lett 420 (2007) 12-17
44. Takase K., Uenoyama Y., Inoue N., Matsui H., Yamada S., Shimizu M., et al. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 21 (2009) 527-537
45. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum Reprod Update 12 (2006) 631-639
46. Tena-Sempere M. The roles of kisspeptins and G protein-coupled receptor-54 in pubertal development. Curr Opin Pediatr 18 (2006) 442-447
47. Thompson E.L., Patterson M., Murphy K.G., Smith K.L., Dhillo W.S., Todd J.F., et al. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 16 (2004) 850-858
48. Vogel G. Reproductive biology. A powerful first KiSS-1. Science 309 (2005) 551-552
49. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Grone H.J., Todman M.G., et al. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52 (2006) 271-280
50. Woldbye D.P., Greisen M.H., Bolwig T.G., Larsen P.J., and Mikkelsen J.D. Prolonged induction of c-fos in neuropeptide Y- and somatostatin-immunoreactive neurons of the rat dentate gyrus after electroconvulsive stimulation. Brain Res 720 (1996) 111-119
51. Zhang C., Roepke T.A., Kelly M.J., and Ronnekleiv O.K. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28 (2008) 4423-4434
52. Zorrilla L.M., Gibson E.K., Jeffay S.C., Crofton K.M., Setzer W.R., Cooper R.L., et al. The effects of triclosan on puberty and thyroid hormones in male Wistar rats. Toxicol Sci 107 (2009) 56-64