Kisspeptin Directly Excites Anorexigenic Proopiomelanocortin Neurons but Inhibits Orexigenic Neuropeptide Y Cells by an Indirect Synaptic Mechanism
Open accessAbstract
The neuropeptide kisspeptin is necessary for reproduction, fertility, and puberty. Here, we show strong kisspeptin innervation of hypothalamic anorexigenic proopiomelanocortin (POMC) cells, coupled with a robust direct excitatory response by POMC neurons ( n > 200) to kisspeptin, mediated by mechanisms based on activation of a sodium/calcium exchanger and possibly opening of nonselective cation channels. The excitatory actions of kisspeptin on POMC cells were corroborated with quantitative PCR data showing kisspeptin receptor GPR54 expression in the arcuate nucleus, and the attenuation of excitation by the selective kisspeptin receptor antagonist, peptide 234. In contrast, kisspeptin inhibits orexigenic neuropeptide Y (NPY) neurons through an indirect mechanism based on enhancing GABA-mediated inhibitory synaptic tone. In striking contrast, gonadotropin-inhibiting hormone (GnIH and RFRP-3) and NPY, also found in axons abutting POMC cells, inhibit POMC cells and attenuate the kisspeptin excitation by a mechanism based on opening potassium channels. Together, these data suggest that the two central peptides that regulate reproduction, kisspeptin and GnIH, exert a strong direct action on POMC neurons. POMC cells may hypothetically serve as a conditional relay station downstream of kisspeptin and GnIH to signal the availability of energy resources relevant to reproduction.
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RFRP-3 inhibits firing of some GnRH and ARC kisspeptin neurons, suggesting it may inhibit reproduction partly by signaling to these populations.
“RFRP-3 has been functionally shown to inhibit the electrical firing of some GnRH and ARC kisspeptin neurons11–13 suggesting that RFRP-3 may inhibit the reproductive axis, in part, by signaling to kisspeptin and/or GnRH populations.”
From Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling (2018) · cites this paper as [11]
The Introduction reports that GnIH hyperpolarizes GnRH neurons, and the Results identify RFRP-3 as its mammalian analog. The Results show RFRP-3 reducing firing in arcuate POMC neurons, not ARC kisspeptin neurons; the paper does not report RFRP-3 inhibiting kisspeptin-neuron firing or signaling to that population. Page numbers were not available in our copy. (LLM, conf=0.84)
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Matsuyama, S., Ohkura, S., Sakurai, K., et al. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.04.026 · Cited by 14 · see citing works
Our Evolving Understanding of Peptides and the Control of Food Intake
Seeley, R. J. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-48643-1_6 · Cited by 1 · see citing works
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Sex differences in the physiology of eating
Asarian, L., & Geary, N. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00446.2012 · Cited by 513 · see citing works
Definition of the hypothalamic GnRH pulse generator in mice
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Female reproduction and type 1 diabetes: From mechanisms to clinical findings
Codner, E., Merino, P. M., & Tena-Sempere, M. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms024 · Cited by 182 · see citing works
Neuroanatomy of the kisspeptin signaling system in mammals: comparative and developmental aspects
Lehman, M. N., Hileman, S. M., & Goodman, R. L. (2013) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-6199-9_3 · Cited by 180 · see citing works
The physiological control of eating: signals, neurons, and networks
Watts, A. G., Kanoski, S. E., Sanchez-Watts, G., & Langhans, W. (2022) · Physiological Reviews · doi:10.1152/physrev.00028.2020 · Cited by 168 · see citing works
Impact of dietary fats on brain functions
Chianese, R., Coccurello, R., Viggiano, A., Scafuro, M., Fiore, M., Coppola, G., Operto, F. F., Fasano, S., Laye, S., Pierantoni, R., et al. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666171017102547 · Cited by 159 · see citing works
Padilla, S. L., Perez, J. G., Ben-Hamo, M., Johnson, C. W., Sanchez, R. E. A., Bussi, I. L., Palmiter, R. D., & de la Iglesia, H. O. (2019) · Current Biology · doi:10.1016/j.cub.2019.01.022 · Cited by 113 · see citing works
Yeo, S.-H., & Colledge, W. H. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00188 · Cited by 76 · see citing works
Metabolic Regulation of Kisspeptin
Castellano, J. M., & Tena-Sempere, M. (2013) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-6199-9_17 · Cited by 42 · see citing works
Ullah, R., Shen, Y., Zhou, Y.-D., Huang, K., Fu, J.-F., Wahab, F., & Shahab, M. (2016) · Neuropeptides · doi:10.1016/j.npep.2016.05.004 · Cited by 30 · see citing works
- Authors
- Fu, L.-Y., & van den Pol, A. N.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-07-28
- Volume
- 30
- Issue
- 30
- Pages
- 10205-10219
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2933146
- OpenAlex
- W2005121205
- Cited by
- 243
- References
- 92
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 5 · 2023: 11 · 2022: 16 · 2021: 22 · 2020: 18 · 2019: 17 · 2018: 21 · 2017: 14 · 2016: 22 · 2015: 17 · 2014: 14 · 2013: 22 · 2012: 12
- FWCI
- 19.73
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK084052)
- National Institute of Neurological Disorders and Stroke (R01NS048476, NS 41454, R01NS041454, NS48476, NS 34887, R01NS034887)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- kisspeptin, proopiomelanocortin neurons, neuropeptide Y neurons, hypothalamus, arcuate nucleus, Na+/Ca2+ exchanger, GABAergic inhibition, gonadotropin-inhibiting hormone, RFRP-3, potassium channels, appetite regulation, reproduction, energy homeostasis
- MeSH terms
- Receptors, Kisspeptin-1, Animals, Arcuate Nucleus of Hypothalamus, Axons, Calcium Channel Blockers, Chelating Agents, Dose-Response Relationship, Drug, Egtazic Acid, Female, Gene Expression Regulation, Imidazoles, Male, Membrane Potentials, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Neuropeptide Y, Pro-Opiomelanocortin, RNA, Messenger, Thiourea, Patch-Clamp Techniques, Excitatory Amino Acid Agonists, Excitatory Amino Acid Antagonists, 6-Cyano-7-nitroquinoxaline-2,3-dione, Excitatory Postsynaptic Potentials, Sodium-Calcium Exchanger, Tumor Suppressor Proteins, Receptors, G-Protein-Coupled, Renilla, Green Fluorescent Proteins, Mice, Kisspeptins, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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