Chronic peripheral administration of kappa-opioid receptor antagonist advances puberty onset associated with acceleration of pulsatile luteinizing hormone secretion in female rats

Journal of Reproduction and Development

Volumn 59, Issue 5, 2013, Pages 479-484

  Nakahara, Tatsuo ^a   Uenoyama, Yoshihisa ^b   Iwase, Akira ^a   Oishi, Shinya ^c   Nakamura, Sho ^d   Minabe, Shiori ^b   Watanabe, Youki ^b   Deura, Chikaya ^b   Noguchi, Taro ^c   Fujii, Nobutaka ^c   Kikkawa, Fumitaka ^a   Maeda, Kei Ichiro ^d   Tsukamura, Hiroko ^b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

GPR54; Metastin; Sexual maturation

Indexed keywords

DRUG DERIVATIVE; DYNORPHIN; KAPPA OPIATE RECEPTOR; LUTEINIZING HORMONE; NALTREXONE; NARCOTIC ANTAGONIST; NERVE PROTEIN; NEUROKININ 3 RECEPTOR; NEUROKININ B; NORBINALTORPHIMINE; PEPTIDE FRAGMENT; SENKTIDE; SUBSTANCE P;

ANIMAL; ARTICLE; BLOOD; CHEMICALLY INDUCED DISORDER; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; DRUG IMPLANT; DRUG POTENTIATION; FEMALE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; OVARY; PRECOCIOUS PUBERTY; RANDOMIZATION; RAT; SECRETION (PROCESS); SEXUAL MATURATION; SIGNAL TRANSDUCTION; WEANING; WISTAR RAT;

ANIMALS; DRUG IMPLANTS; DYNORPHINS; FEMALE; LUTEINIZING HORMONE; NALTREXONE; NARCOTIC ANTAGONISTS; NERVE TISSUE PROTEINS; NEUROKININ B; NEURONS; OVARY; PEPTIDE FRAGMENTS; PUBERTY, PRECOCIOUS; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, NEUROKININ-3; RECEPTORS, OPIOID, KAPPA; SEXUAL MATURATION; SIGNAL TRANSDUCTION; SUBSTANCE P; WEANING;

EID: 84886681693     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.2013-046     Document Type: Article

References (36)

1. Watanabe G, Terasawa E. In vivo release of luteinizing hormone releasing hormone increases with puberty in the female rhesus monkey. Endocrinology 1989; 125: 92-99. [Medline]
2. 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. [Medline]
3. Sisk CL, Foster DL. The neural basis of puberty and adolescence. Nat Neurosci 2004; 7: 1040-1047. [Medline]
4. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley WF Jr, Aparicio SA, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627. [Medline]
5. 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. [Medline]
6. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 2009; 41: 354-358. [Medline]
7. Gianetti E, Tusset C, Noel SD, Au MG, Dwyer AA, Hughes VA, Abreu AP, Carroll J, Trarbach E, Silveira LF, Costa EM, de Mendonca BB, de Castro M, Lofrano A, Hall JE, Bolu E, Ozata M, Quinton R, Amory JK, Stewart SE, Arlt W, Cole TR, Crowley WF, Kaiser UB, Latronico AC, Seminara SB. TAC3/TACR3 mutations reveal preferential activation of gonadotropin-releasing hormone release by neurokinin B in neonatal life followed by reversal in adulthood. J Clin Endocrinol Metab 2010; 95: 2857-2867. [Medline]
8. Young J, Bouligand J, Francou B, Raffin-Sanson ML, Gaillez S, Jeanpierre M, Grynberg M, Kamenicky P, Chanson P, Brailly-Tabard S, Guiochon-Mantel A. TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab 2010; 95: 2287-2295. [Medline]
9. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. 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. [Medline]
10. Takase K, Uenoyama Y, Inoue N, Matsui H, Yamada S, Shimizu M, Homma T, Tomikawa J, Kanda S, Matsumoto H, Oka Y, Tsukamura H, Maeda KI. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 2009; 21: 527-537. [Medline]
11. Gill JC, Navarro VM, Kwong C, Noel SD, Martin C, Xu S, Clifton DK, Carroll RS, Steiner RA, Kaiser UB. Increased neurokinin B (Tac2) expression in the mouse arcuate nucleus is an early marker of pubertal onset with differential sensitivity to sex steroidnegative feedback than Kiss1. Endocrinology 2012; 153: 4883-4893. [Medline]
12. Navarro VM, Ruiz-Pino F, Sanchez-Garrido MA, Garcia-Galiano D, Hobbs SJ, Manfredi- Lozano M, Leon S, Sangiao-Alvarellos S, Castellano JM, Clifton DK, Pinilla L, Steiner RA, Tena-Sempere M. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci 2012; 32: 2388-2397. [Medline]
13. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. 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. [Medline]
14. Civelli O, Douglass J, Goldstein A, Herbert E. Sequence and expression of the rat prodynorphin gene. Proc Natl Acad Sci USA 1985; 82: 4291-4295. [Medline]
15. Goodman RL, Coolen LM, Anderson GM, Hardy SL, Valent M, Connors JM, Fitzgerald ME, Lehman MN. Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin-releasing hormone neurons in sheep. Endocrinology 2004; 145: 2959-2967. [Medline]
16. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H. Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 2010; 30: 3124-3132. [Medline]
17. Maeda K, Ohkura S, Uenoyama Y, Wakabayashi Y, Oka Y, Tsukamura H, Okamura H. Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brain Res 2010; 1364: 103-115. [Medline]
18. Mostari MP, Ieda N, Deura C, Minabe S, Yamada S, Uenoyama Y, Maeda KI, Tsukamura H. Dynorphin-kappa opioid receptor signaling partly mediates estrogen negative feedback effect on LH pulses in female rats. J Reprod Dev 2013; 59: 266-272. [Medline]
19. Simerly RB, McCall LD, Watson SJ. Distribution of opioid peptides in the preoptic region: immunohistochemical evidence for a steroid-sensitive enkephalin sexual dimorphism. J Comp Neurol 1988; 276: 442-459. [Medline]
20. Burke MC, Letts PA, Krajewski SJ, Rance NE. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: Morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol 2006; 498: 712-726. [Medline]
21. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 2009; 29: 11859-11866. [Medline]
22. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, Lai J, Ciofi P, McMullen NT, Rance NE. Arcuate kisspeptin/neurokinin B/dynorphin (KNDy) neurons mediate the estrogen suppression of gonadotropin secretion and body weight. Endocrinology 2012; 153: 2800-2812. [Medline]
23. Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropinreleasing hormone secretion. Endocrinology 2010; 151: 3479-3489. [Medline]
24. Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, Wakabayashi Y, Uenoyama Y, Mori Y, Steiner RA, Tsukamura H, Maeda KI, Okamura H. Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 2009; 21: 813-821. [Medline]
25. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80: 264-272. [Medline]
26. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 2004; 320: 383-388. [Medline]
27. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005; 146: 4431-4436. [Medline]
28. 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. [Medline]
29. Pheng V, Uenoyama Y, Homma T, Inamoto Y, Takase K, Yoshizawa-Kumagaye K, Isaka S, Watanabe TX, Ohkura S, Tomikawa J, Maeda KI, Tsukamura H. Potencies of centrally- or peripherally-injected full-length kisspeptin or its C-terminal decapeptide on LH release in intact male rats. J Reprod Dev 2009; 55: 378-382. [Medline]
30. Grachev P, Li XF, Lin YS, Hu MH, Elsamani L, Paterson SJ, Millar RP, Lightman SL, O'Byrne KT. GPR54-dependent stimulation of luteinizing hormone secretion by neurokinin B in prepubertal rats. PLoS One 2012; 7: e44344. [Medline]
31. Wakabayashi Y, Yamamura T, Ohkura S, Homma T, Sakamoto K, Mori Y, Okamura H. Senktide, a neurokinin B receptor agonist, stimulates pulsatile LH secretion through a mechanism mediated by the GnRH pulse generator in goats. In: Program of 42nd Society for Neuroscience Annual Meeting; 2012; New Orleans, USA. Abstract 90.07.
32. Merriam GR, Wachter KW. Algorithms for the study of episodic hormone secretion. Am J Physiol 1982; 243: E310-E318. [Medline]
33. Mitchell V, Prevot V, Jennes L, Aubert JP, Croix D, Beauvillain JC. Presence of mu and kappa opioid receptor mRNAs in galanin but not in GnRH neurons in the female rat. Neuroreport 1997; 8: 3167-3172. [Medline]
34. Sannella MI, Petersen SL. Dual label in situ hybridization studies provide evidence that luteinizing hormone-releasing hormone neurons do not synthesize messenger ribonucleic acid for mu, kappa, or delta opiate receptors. Endocrinology 1997; 138: 1667-1672. [Medline]
35. Navarro VM, Gottsch ML, Wu M, Garcia-Galiano D, Hobbs SJ, Bosch MA, Pinilla L, Clifton DK, Dearth A, Ronnekleiv OK, Braun RE, Palmiter RD, Tena-Sempere M, Alreja M, Steiner RA. Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology 2011; 152: 4265-4275. [Medline]
36. Amstalden M, Coolen LM, Hemmerle AM, Billings HJ, Connors JM, Goodman RL, Lehman MN. Neurokinin 3 receptor immunoreactivity in the septal region, preoptic area and hypothalamus of the female sheep: colocalisation in neurokinin B cells of the arcuate nucleus but not in gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2010; 22: 1-12. [Medline]