Activation of Gonadotropin-Releasing Hormone Neurons by Kisspeptin as a Neuroendocrine Switch for the Onset of Puberty

Han, Seong-Kyu; Gottsch, Michelle L.; Lee, Kathy J.; Popa, Simina M.; Smith, Jeremy T.; Jakawich, Sonya K.; Clifton, Donald K.; Steiner, Robert A.; Herbison, Allan E.

doi:10.1523/jneurosci.3328-05.2005

Cited by 1,036Hypothalamic control of reproductive hormonesNeuropeptides and Animal PhysiologyRegulation of Appetite and Obesity

Activation of Gonadotropin-Releasing Hormone Neurons by Kisspeptin as a Neuroendocrine Switch for the Onset of Puberty

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Han, Seong-Kyu, Gottsch, Michelle L., Lee, Kathy J., Popa, Simina M., Smith, Jeremy T., Jakawich, Sonya K., Clifton, Donald K., Steiner, Robert A. +1 more·2005·The Journal of Neuroscience

DOI 10.1523/jneurosci.3328-05.2005PMC PMC6725899

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Abstract

We examined the role of kisspeptin and its receptor, the G-protein-coupled receptor GPR54, in governing the onset of puberty in the mouse. In the adult male and female mouse, kisspeptin (10–100 n m ) evoked a remarkably potent, long-lasting depolarization of >90% of gonadotropin-releasing hormone (GnRH)–green fluorescent protein neurons in situ . In contrast, in juvenile [postnatal day 8 (P8) to P19] and prepubertal (P26–P33) male mice, kisspeptin activated only 27 and 44% of GnRH neurons, respectively. This developmental recruitment of GnRH neurons into a kisspeptin-responsive pool was paralleled by an increase in the ability of centrally administered kisspeptin to evoke luteinizing hormone secretion in vivo . To learn more about the mechanisms through which kisspeptin–GPR54 signaling at the GnRH neuron may change over postnatal development, we performed quantitative in situ hybridization for kisspeptin and GPR54 transcripts. Approximately 90% of GnRH neurons were found to express GPR54 mRNA in both juvenile and adult mice, without a detectable difference in the mRNA content between the age groups. In contrast, the expression of KiSS-1 mRNA increased dramatically across the transition from juvenile to adult life in the anteroventral periventricular nucleus (AVPV; p < 0.001). These results demonstrate that kisspeptin exerts a potent depolarizing effect on the excitability of almost all adult GnRH neurons and that the responsiveness of GnRH neurons to kisspeptin increases over postnatal development. Together, these observations suggest that activation of GnRH neurons by kisspeptin at puberty reflects a dual process involving an increase in kisspeptin input from the AVPV and a post-transcriptional change in GPR54 signaling within the GnRH neuron.

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Activation of arcuate nucleus kisspeptin neurons directly influences pulsatile GnRH release.
“In contrast, activation of kisspeptin neurons in the arcuate nucleus has been shown to directly influence the regulation of pulsatile GnRH release (Han et al., 2005; Millar et al., 2010).”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as Han et al., 2005
The Introduction mentions kisspeptin neurons in the arcuate nucleus, and the section on adult GnRH neurons reports that applied kisspeptin directly depolarized GnRH neurons. But the experiments did not activate arcuate kisspeptin neurons or show an effect on pulsatile GnRH release; the discussion instead focuses on possible input from the AVPV. Page numbers are unavailable in our copy. (LLM, conf=0.88)
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The GPR54 Gene as a Regulator of Puberty
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“Mutations in GPR54 are associated with sexual immaturity and infertility in humans (de Roux et al., 2003; Seminara et al., 2003; Semple et al., 2005), and this phenotype is mirrored in mice having genetically targeted deletions of GPR54 (Funes et al., 2003; Seminara et al., 2003).”
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Herbison AE (2005) Physiology of the GnRH neuronal network. In: Knobil and Neill's physiology of reproduction, Ed 3 (Neill JD, ed). San Diego: Elsevier.

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Authors: Han, S.-K., Gottsch, M. L., Lee, K. J., Popa, S. M., Smith, J. T., Jakawich, S. K., Clifton, D. K., Steiner, R. A., & Herbison, A. E.
Affiliations: University of Otago (NZ)
University of Washington (US)
Corresponding author: Herbison, Allan E.
ORCID: Steiner, Robert A.
Herbison, Allan E.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2005-12-07
Volume: 25
Issue: 49
Pages: 11349-11356
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.3328-05.2005
PMC: PMC6725899
OpenAlex: W2158795213
Cited by: 1,036
References: 5
Citations by year: 2026: 18 · 2025: 28 · 2024: 28 · 2023: 34 · 2022: 41 · 2021: 68 · 2020: 35 · 2019: 42 · 2018: 55 · 2017: 49 · 2016: 57 · 2015: 53 · 2014: 70 · 2013: 91 · 2012: 81
FWCI: 40.44
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
National Institutes of Health (5u54hd012629-31)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK061517, R01 DK61517)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01 HD 27142, U54-HD-12629, U54HD-012629, R01HD027142)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: kisspeptin, GPR54, GnRH neurons, puberty onset, neuronal excitability, postnatal development, anteroventral periventricular nucleus, luteinizing hormone secretion
MeSH terms: Action Potentials, Age Factors, Animals, Animals, Newborn, Female, Gonadotropin-Releasing Hormone, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Mice, Mutant Strains, Neurons, Neurosecretory Systems, Proteins, Sexual Maturation, Anterior Thalamic Nuclei, Tumor Suppressor Proteins, Mice, Kisspeptins

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Activation of Gonadotropin-Releasing Hormone Neurons by Kisspeptin as a Neuroendocrine Switch for the Onset of Puberty

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