Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2017

Open Access 01-12-2017 | Research

Intracerebroventricular injection of RFRP-3 delays puberty onset and stimulates growth hormone secretion in female rats

Authors: Xinghui Han, Yuanyuan He, Gulan Zeng, Yonghong Wang, Wen Sun, Junchao Liu, Yanyan Sun, Jian Yu

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

Login to get access

Abstract

Background

Puberty onset is a complex, organized biological process with multilevel regulation, and its physiopathological mechanisms are yet to be elucidated. RFRP-3, the mammalian ortholog to gonadotropin-inhibitory hormone, is implicated in inhibiting the synthesis and release of gonadotropin in mammals. However, it is unclear whether RFRP-3 participates in regulating pubertal development.

Methods

This study investigated the functional significance and regulatory mechanism of hypothalamic RFRP-3 neuropeptide in the onset of puberty in young female rats. On postnatal day 22, we implanted cannulas into the lateral ventricles of female rat pups. From postnatal day 28 to postnatal day 36, the intracerebroventricular injection of RFRP-3, or vehicle, was conducted twice a day. To investigate whether puberty onset was affected, we examined the body weight, age of vaginal opening, serum hormone levels, uterus and ovary development, and hypothalamic Kiss-1 mRNA expression.

Results

Intracerebroventricular injection of RFRP-3 significantly decreased the serum concentrations of luteinizing hormone and estradiol, delayed uterine maturation, and postponed the time of vaginal opening. This study suggests that RFRP-3 can delay the onset of puberty in young female rats; the expression of Kiss-1 mRNA is potently inhibited in the RFRP-3 group. Moreover, our data show that RFRP-3 elevates serum growth hormone levels.

Conclusions

These data suggest that intracerebroventricular injection of RFRP-3 significantly delays the onset of puberty in female rats. Additionally, RFRP-3 may be associated with prepubertal rise in the secretion of growth hormone.
Literature
1.
go back to reference Grumbach MM. The neuroendocrinology of human puberty revisited. Horm Res. 2002;57 Suppl 2:2–14.PubMed Grumbach MM. The neuroendocrinology of human puberty revisited. Horm Res. 2002;57 Suppl 2:2–14.PubMed
2.
go back to reference Ojeda SR, Lomniczi A, Mastronardi C, Heger S, Roth C, Parent AS, Matagne V, Mungenast AE. Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology. 2006;147:1166–74.CrossRefPubMed Ojeda SR, Lomniczi A, Mastronardi C, Heger S, Roth C, Parent AS, Matagne V, Mungenast AE. Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology. 2006;147:1166–74.CrossRefPubMed
5.
go back to reference Tena-Sempere M. Deciphering puberty: novel partners, novel mechanisms. Eur J Endocrinol. 2012;167:733–47.CrossRefPubMed Tena-Sempere M. Deciphering puberty: novel partners, novel mechanisms. Eur J Endocrinol. 2012;167:733–47.CrossRefPubMed
7.
go back to reference Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25:11349–56.CrossRefPubMed Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25:11349–56.CrossRefPubMed
8.
go back to reference Rhie YJ. Kisspeptin/G protein-coupled receptor-54 system as an essential gatekeeper of pubertal development. Ann Pediatr Endocrinol Metab. 2013;18:55–9.CrossRefPubMedPubMedCentral Rhie YJ. Kisspeptin/G protein-coupled receptor-54 system as an essential gatekeeper of pubertal development. Ann Pediatr Endocrinol Metab. 2013;18:55–9.CrossRefPubMedPubMedCentral
9.
go back to reference Pralong FP. Insulin and NPY pathways and the control of GnRH function and puberty onset. Mol Cell Endocrinol. 2010;324:82–6.CrossRefPubMed Pralong FP. Insulin and NPY pathways and the control of GnRH function and puberty onset. Mol Cell Endocrinol. 2010;324:82–6.CrossRefPubMed
10.
go back to reference Sheffer-Babila S, Sun Y, Israel DD, Liu SM, Neal-Perry G, Chua SJ. Agouti-related peptide plays a critical role in leptin’s effects on female puberty and reproduction. Am J Physiol Endocrinol Metab. 2013;305:E1512–20.CrossRefPubMedPubMedCentral Sheffer-Babila S, Sun Y, Israel DD, Liu SM, Neal-Perry G, Chua SJ. Agouti-related peptide plays a critical role in leptin’s effects on female puberty and reproduction. Am J Physiol Endocrinol Metab. 2013;305:E1512–20.CrossRefPubMedPubMedCentral
11.
go back to reference Simavli S, Thompson IR, Maguire CA, Gill JC, Carroll RS, Wolfe A, Kaiser UB, Navarro VM. Substance p regulates puberty onset and fertility in the female mouse. Endocrinology. 2015;156:2313–22.CrossRefPubMedPubMedCentral Simavli S, Thompson IR, Maguire CA, Gill JC, Carroll RS, Wolfe A, Kaiser UB, Navarro VM. Substance p regulates puberty onset and fertility in the female mouse. Endocrinology. 2015;156:2313–22.CrossRefPubMedPubMedCentral
12.
go back to reference Li SY, Li XF, Hu MH, Shao B, Poston L, Lightman SL, O’Byrne KT. Neurokinin B receptor antagonism decreases luteinising hormone pulse frequency and amplitude and delays puberty onset in the female rat. J Neuroendocrinol. 2014;26:521–7.CrossRefPubMed Li SY, Li XF, Hu MH, Shao B, Poston L, Lightman SL, O’Byrne KT. Neurokinin B receptor antagonism decreases luteinising hormone pulse frequency and amplitude and delays puberty onset in the female rat. J Neuroendocrinol. 2014;26:521–7.CrossRefPubMed
13.
go back to reference Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, et al. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet. 2009;41:354–8.CrossRefPubMed Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, et al. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet. 2009;41:354–8.CrossRefPubMed
14.
go back to reference Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman MN, McManus CJ, Nestor CC, Jacobs BH, Goodman RL. Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology. 2010;151:3836–46.CrossRefPubMedPubMedCentral Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman MN, McManus CJ, Nestor CC, Jacobs BH, Goodman RL. Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology. 2010;151:3836–46.CrossRefPubMedPubMedCentral
15.
go back to reference Poling MC, Kauffman AS. Regulation and Function of RFRP-3 (GnIH) Neurons during Postnatal Development. Front Endocrinol (Lausanne). 2015;6:150. Poling MC, Kauffman AS. Regulation and Function of RFRP-3 (GnIH) Neurons during Postnatal Development. Front Endocrinol (Lausanne). 2015;6:150.
16.
17.
go back to reference 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;145:4565–74.CrossRefPubMed 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;145:4565–74.CrossRefPubMed
18.
go back to reference Kuohung W, Kaiser UB. GPR54 and KiSS-1: role in the regulation of puberty and reproduction. Rev Endocr Metab Disord. 2006;7:257–63.CrossRefPubMed Kuohung W, Kaiser UB. GPR54 and KiSS-1: role in the regulation of puberty and reproduction. Rev Endocr Metab Disord. 2006;7:257–63.CrossRefPubMed
19.
go back to reference Kaiser UB, Kuohung W. KiSS-1 and GPR54 as new players in gonadotropin regulation and puberty. Endocrine. 2005;26:277–84.CrossRefPubMed Kaiser UB, Kuohung W. KiSS-1 and GPR54 as new players in gonadotropin regulation and puberty. Endocrine. 2005;26:277–84.CrossRefPubMed
20.
go back to reference 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 U S A. 2005;102:2129–34.CrossRefPubMedPubMedCentral 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 U S A. 2005;102:2129–34.CrossRefPubMedPubMedCentral
21.
go back to reference Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JJ, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614–27.CrossRefPubMed Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JJ, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614–27.CrossRefPubMed
22.
go back to reference Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp JP. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Bioph Res Co. 2000;275:661–7.CrossRef Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp JP. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Bioph Res Co. 2000;275:661–7.CrossRef
23.
go back to reference Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, et al. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol. 2000;2:703–8.CrossRefPubMed Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, et al. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol. 2000;2:703–8.CrossRefPubMed
24.
go back to reference Anderson GM, Relf HL, Rizwan MZ, Evans JJ. Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology. 2009;150:1834–40.CrossRefPubMed Anderson GM, Relf HL, Rizwan MZ, Evans JJ. Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology. 2009;150:1834–40.CrossRefPubMed
25.
go back to reference Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A. 2006;103:2410–5.CrossRefPubMedPubMedCentral Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A. 2006;103:2410–5.CrossRefPubMedPubMedCentral
26.
go back to reference Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One. 2009;4:e8400.CrossRefPubMedPubMedCentral Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One. 2009;4:e8400.CrossRefPubMedPubMedCentral
27.
go back to reference Johnson MA, Tsutsui K, Fraley GS. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav. 2007;51:171–80.CrossRefPubMed Johnson MA, Tsutsui K, Fraley GS. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav. 2007;51:171–80.CrossRefPubMed
28.
go back to reference Rizwan MZ, Poling MC, Corr M, Cornes PA, Augustine RA, Quennell JH, Kauffman AS, Anderson GM. RFamide-Related Peptide-3 Receptor Gene Expression in GnRH and Kisspeptin Neurons and GnRH-Dependent Mechanism of Action. Endocrinology. 2012;153:3770–9.CrossRefPubMed Rizwan MZ, Poling MC, Corr M, Cornes PA, Augustine RA, Quennell JH, Kauffman AS, Anderson GM. RFamide-Related Peptide-3 Receptor Gene Expression in GnRH and Kisspeptin Neurons and GnRH-Dependent Mechanism of Action. Endocrinology. 2012;153:3770–9.CrossRefPubMed
29.
go back to reference Losa-Ward SM, Todd KL, McCaffrey KA, Tsutsui K, Patisaul HB. Disrupted organization of RFamide pathways in the hypothalamus is associated with advanced puberty in female rats neonatally exposed to bisphenol A. Biol Reprod. 2012;87:28.CrossRefPubMedPubMedCentral Losa-Ward SM, Todd KL, McCaffrey KA, Tsutsui K, Patisaul HB. Disrupted organization of RFamide pathways in the hypothalamus is associated with advanced puberty in female rats neonatally exposed to bisphenol A. Biol Reprod. 2012;87:28.CrossRefPubMedPubMedCentral
30.
go back to reference Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology. 2012;153:373–85.CrossRefPubMed Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology. 2012;153:373–85.CrossRefPubMed
31.
go back to reference Bentley GE, Ubuka T, McGuire NL, Calisi R, Perfito N, Kriegsfeld LJ, Wingfield JC, Tsutsui K. Gonadotrophin-inhibitory hormone: a multifunctional neuropeptide. J Neuroendocrinol. 2009;21:276–81.CrossRefPubMed Bentley GE, Ubuka T, McGuire NL, Calisi R, Perfito N, Kriegsfeld LJ, Wingfield JC, Tsutsui K. Gonadotrophin-inhibitory hormone: a multifunctional neuropeptide. J Neuroendocrinol. 2009;21:276–81.CrossRefPubMed
32.
go back to reference Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol. 2008;199:105–12.CrossRefPubMed Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol. 2008;199:105–12.CrossRefPubMed
33.
go back to reference Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology. 2009;150:5549–56.CrossRefPubMed Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology. 2009;150:5549–56.CrossRefPubMed
34.
go back to reference Lima C, Cardoso SC, Lemos E, Zingler E, Capanema C, Menezes LD, Vogado G, Dos Santos B, de Moraes OL, Duarte EF, et al. Mutational Analysis of the Genes Encoding RFAmide-Related Peptide-3, the Human Orthologue of Gonadotrophin-Inhibitory Hormone, and its Receptor (GPR147) in Patients with Gonadotrophin-Releasing Hormone-Dependent Pubertal Disorders. J Neuroendocrinol. 2014;26:817–24.CrossRefPubMed Lima C, Cardoso SC, Lemos E, Zingler E, Capanema C, Menezes LD, Vogado G, Dos Santos B, de Moraes OL, Duarte EF, et al. Mutational Analysis of the Genes Encoding RFAmide-Related Peptide-3, the Human Orthologue of Gonadotrophin-Inhibitory Hormone, and its Receptor (GPR147) in Patients with Gonadotrophin-Releasing Hormone-Dependent Pubertal Disorders. J Neuroendocrinol. 2014;26:817–24.CrossRefPubMed
35.
go back to reference Leon S, Garcia-Galiano D, Ruiz-Pino F, Barroso A, Manfredi-Lozano M, Romero-Ruiz A, Roa J, Vazquez MJ, Gaytan F, Blomenrohr M, et al. Physiological Roles of Gonadotropin-Inhibitory Hormone Signaling in the Control of Mammalian Reproductive Axis: Studies in the NPFF1 Receptor Null Mouse. Endocrinology. 2014;155:2953–65.CrossRefPubMed Leon S, Garcia-Galiano D, Ruiz-Pino F, Barroso A, Manfredi-Lozano M, Romero-Ruiz A, Roa J, Vazquez MJ, Gaytan F, Blomenrohr M, et al. Physiological Roles of Gonadotropin-Inhibitory Hormone Signaling in the Control of Mammalian Reproductive Axis: Studies in the NPFF1 Receptor Null Mouse. Endocrinology. 2014;155:2953–65.CrossRefPubMed
36.
go back to reference Xiang W, Zhang B, Lv F, Ma Y, Chen H, Chen L, Yang F, Wang P, Chu M. The Inhibitory Effects of RFamide-Related Peptide 3 on Luteinizing Hormone Release Involves an Estradiol-Dependent Manner in Prepubertal but Not in Adult Female Mice. Biol Reprod. 2015;93:30.CrossRefPubMed Xiang W, Zhang B, Lv F, Ma Y, Chen H, Chen L, Yang F, Wang P, Chu M. The Inhibitory Effects of RFamide-Related Peptide 3 on Luteinizing Hormone Release Involves an Estradiol-Dependent Manner in Prepubertal but Not in Adult Female Mice. Biol Reprod. 2015;93:30.CrossRefPubMed
37.
go back to reference Semaan SJ, Kauffman AS. Daily successive changes in reproductive gene expression and neuronal activation in the brains of pubertal female mice. Mol Cell Endocrinol. 2015;401:84–97.CrossRefPubMed Semaan SJ, Kauffman AS. Daily successive changes in reproductive gene expression and neuronal activation in the brains of pubertal female mice. Mol Cell Endocrinol. 2015;401:84–97.CrossRefPubMed
38.
go back to reference Johnson MA, Fraley GS. Rat RFRP-3 Alters Hypothalamic GHRH Expression and Growth Hormone Secretion but Does Not Affect KiSS-1 Gene Expression or the Onset of Puberty in Male Rats. Neuroendocrinology. 2008;88:305–15.CrossRefPubMed Johnson MA, Fraley GS. Rat RFRP-3 Alters Hypothalamic GHRH Expression and Growth Hormone Secretion but Does Not Affect KiSS-1 Gene Expression or the Onset of Puberty in Male Rats. Neuroendocrinology. 2008;88:305–15.CrossRefPubMed
39.
go back to reference Ancel C, Bentsen AH, Sebert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: the exception proves the rule. Endocrinology. 2012;153:1352–63.CrossRefPubMed Ancel C, Bentsen AH, Sebert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: the exception proves the rule. Endocrinology. 2012;153:1352–63.CrossRefPubMed
40.
go back to reference Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort PI, Tena-Sempere M. Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of GnIH, in the control of gonadotropin secretion in the rat: in vivo and in vitro studies. Am J Physiol Endocrinol Metab. 2010;299:E39–46.CrossRefPubMed Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort PI, Tena-Sempere M. Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of GnIH, in the control of gonadotropin secretion in the rat: in vivo and in vitro studies. Am J Physiol Endocrinol Metab. 2010;299:E39–46.CrossRefPubMed
41.
go back to reference Fu LY, van den Pol AN. Kisspeptin directly excites anorexigenic proopiomelanocortin neurons but inhibits orexigenic neuropeptide Y cells by an indirect synaptic mechanism. J Neurosci. 2010;30:10205–19.CrossRefPubMedPubMedCentral Fu LY, van den Pol AN. Kisspeptin directly excites anorexigenic proopiomelanocortin neurons but inhibits orexigenic neuropeptide Y cells by an indirect synaptic mechanism. J Neurosci. 2010;30:10205–19.CrossRefPubMedPubMedCentral
42.
go back to reference Poling MC, Quennell JH, Anderson GM, Kauffman AS. Kisspeptin Neurones do not Directly Signal to RFRP-3 Neurones but RFRP-3 may Directly Modulate a Subset of Hypothalamic Kisspeptin Cells in Mice. J Neuroendocrinol. 2013;25:876–86.CrossRefPubMedPubMedCentral Poling MC, Quennell JH, Anderson GM, Kauffman AS. Kisspeptin Neurones do not Directly Signal to RFRP-3 Neurones but RFRP-3 may Directly Modulate a Subset of Hypothalamic Kisspeptin Cells in Mice. J Neuroendocrinol. 2013;25:876–86.CrossRefPubMedPubMedCentral
43.
go back to reference Marshall JC, Dalkin AC, Haisenleder DJ, Griffin ML, Kelch RP. GnRH pulses--the regulators of human reproduction. Trans Am Clin Climatol Assoc. 1993;104:31–46.PubMedPubMedCentral Marshall JC, Dalkin AC, Haisenleder DJ, Griffin ML, Kelch RP. GnRH pulses--the regulators of human reproduction. Trans Am Clin Climatol Assoc. 1993;104:31–46.PubMedPubMedCentral
44.
go back to reference Dai FW, et al. Dynamic Development of Organs and Serum Sex Hormone Levels in Normal Pre-pubertal Female Sprague-Dawley Rats. Chin J Comp Med. 2009;19(07):33–8. In Chinese with English Abstract. Dai FW, et al. Dynamic Development of Organs and Serum Sex Hormone Levels in Normal Pre-pubertal Female Sprague-Dawley Rats. Chin J Comp Med. 2009;19(07):33–8. In Chinese with English Abstract.
45.
go back to reference van der Kaay DC, Rose SR, van Dijk M, Noordam C, van Rheenen E, Hokken-Koelega AC. Reduced levels of GH during GnRH analogue treatment in pubertal short girls born small for gestational age (SGA). Clin Endocrinol (Oxf). 2009;70:914–9.CrossRef van der Kaay DC, Rose SR, van Dijk M, Noordam C, van Rheenen E, Hokken-Koelega AC. Reduced levels of GH during GnRH analogue treatment in pubertal short girls born small for gestational age (SGA). Clin Endocrinol (Oxf). 2009;70:914–9.CrossRef
46.
go back to reference Carel JC, Hay F, Coutant R, Rodrigue D, Chaussain JL. Gonadotropin-releasing hormone agonist treatment of girls with constitutional short stature and normal pubertal development. J Clin Endocrinol Metab. 1996;81:3318–22.PubMed Carel JC, Hay F, Coutant R, Rodrigue D, Chaussain JL. Gonadotropin-releasing hormone agonist treatment of girls with constitutional short stature and normal pubertal development. J Clin Endocrinol Metab. 1996;81:3318–22.PubMed
47.
go back to reference Saggese G, Bertelloni S, Baroncelli GI, Di Nero G, Battini R. Growth velocity and serum aminoterminal propeptide of type III procollagen in precocious puberty during gonadotropin-releasing hormone analogue treatment. Acta Paediatr. 1993;82:261–6.CrossRefPubMed Saggese G, Bertelloni S, Baroncelli GI, Di Nero G, Battini R. Growth velocity and serum aminoterminal propeptide of type III procollagen in precocious puberty during gonadotropin-releasing hormone analogue treatment. Acta Paediatr. 1993;82:261–6.CrossRefPubMed
48.
go back to reference Tato L, Saggese G, Cavallo L, Antoniazzi F, Corrias A, Pasquino AM, Cisternino M. Use of combined Gn-RH agonist and hGH therapy for better attining the goals in precocious puberty treatment. Horm Res. 1995;44 Suppl 3:49–54.PubMed Tato L, Saggese G, Cavallo L, Antoniazzi F, Corrias A, Pasquino AM, Cisternino M. Use of combined Gn-RH agonist and hGH therapy for better attining the goals in precocious puberty treatment. Horm Res. 1995;44 Suppl 3:49–54.PubMed
Metadata
Title
Intracerebroventricular injection of RFRP-3 delays puberty onset and stimulates growth hormone secretion in female rats
Authors
Xinghui Han
Yuanyuan He
Gulan Zeng
Yonghong Wang
Wen Sun
Junchao Liu
Yanyan Sun
Jian Yu
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-017-0254-5

Other articles of this Issue 1/2017

Reproductive Biology and Endocrinology 1/2017 Go to the issue