Cited by 599Hypothalamic control of reproductive hormonesNeuropeptides and Animal PhysiologyNeuroendocrine regulation and behavior

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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

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Wakabayashi, Yoshihiro, Nakada, Tomoaki, Murata, Ken, Ohkura, Satoshi, Mogi, Kazutaka, Navarro, Victor M., Clifton, Donald K., Mori, Yuji, Tsukamura, Hiroko, Maeda, Kei-Ichiro, Steiner, Robert A., Okamura, Hiroaki·2010·The Journal of Neuroscience

DOI 10.1523/jneurosci.5848-09.2010PMC PMC6633939

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Abstract

Gonadotropin-releasing hormone (GnRH) neurons in the basal forebrain are the final common pathway through which the brain regulates reproduction. GnRH secretion occurs in a pulsatile manner, and indirect evidence suggests the kisspeptin neurons in the arcuate nucleus (ARC) serve as the central pacemaker that drives pulsatile GnRH secretion. The purpose of this study was to investigate the possible coexpression of kisspeptin, neurokinin B (NKB), and dynorphin A (Dyn) in neurons of the ARC of the goat and evaluate their potential roles in generating GnRH pulses. Using double and triple labeling, we confirmed that all three neuropeptides are coexpressed in the same population of neurons. Using electrophysiological techniques to record multiple-unit activity (MUA) in the medial basal hypothalamus, we found that bursts of MUA occurred at regular intervals in ovariectomized animals and that these repetitive bursts (volleys) were invariably associated with discrete pulses of luteinizing hormone (LH) (and by inference GnRH). Moreover, the frequency of MUA volleys was reduced by gonadal steroids, suggesting that the volleys reflect the rhythmic discharge of steroid-sensitive neurons that regulate GnRH secretion. Finally, we observed that central administration of Dyn-inhibit MUA volleys and pulsatile LH secretion, whereas NKB induced MUA volleys. These observations are consistent with the hypothesis that kisspeptin neurons in the ARC drive pulsatile GnRH and LH secretion, and suggest that NKB and Dyn expressed in those neurons are involved in the process of generating the rhythmic discharge of kisspeptin.

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Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone
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“The pulsatile release of gonadotropin-releasing hormone (GnRH) is a prerequisite for sustaining normal gonadotropin secretion in mammals (Knobil, 1980; Karsch, 1984); however, the cellular and molecular mechanisms that generate the rhythmic discharge of GnRH are unknown.”
Background
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“Finally, kisspeptin/ NKB/Dyn neurons in the ARC have been proposed to be a primary site of negative feedback action of E2 and P (Smith et al., 2005a,b, 2007; Burke et al., 2006; Foradori et al., 2006; Goodman et al., 2007), and we demonstrated here that E2 and P suppress the occurrence of MUA…”
BackgroundSelf-citation
Activation of Gonadotropin-Releasing Hormone Neurons by Kisspeptin as a Neuroendocrine Switch for the Onset of Puberty
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. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3328-05.2005 · Cited by 1,036 · cited 2×
“duces a prolonged activation of GnRH neurons in the mouse (Han et al., 2005; Pielecka-Fortuna et al., 2008).”
BackgroundResult
TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction
Topaloglu, A. K., Reimann, F., Guclu, M., Yalin, A. S., Kotan, L. D., Porter, K. M., Serin, A., Mungan, N. O., Cook, J. R., Ozbek, M. N., et al. (2009) · Nature Genetics · doi:10.1038/ng.306 · Cited by 961 · cited 2×
“Indeed, Topaloglu et al. (2009) have recently shown that mutations of either Trc3 or Tacr3, which encode NKB and NK3, respectively, produce gonadotropin deficiency and pubertal failure in humans.”
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“Kisspeptin neurons in the hypothalamus play a key role in the regulation of GnRH neurons (Oakley et al., 2009), but the precise nature of the interaction between kisspeptin and GnRH neurons is just emerging.”
Background
Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse
Navarro, V. M., Gottsch, M. L., Chavkin, C., Okamura, H., Clifton, D. K., & Steiner, R. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1569-09.2009 · Cited by 779 · cited 19×
“Finally, we tested the hypothesis that NKB and Dyn play crucial roles in driving GnRH pulse generator activity by analyzing the effects of centrally administered NKB, Dyn, and a KOR antagonist on pulsatile MUA and LH secretion.”
BackgroundResultInfluential

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Background
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Background
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Background
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BackgroundInfluential
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TACkling NKB’s Role in Puberty
Angell, A. E., & Steiner, R. A. (2015) · Endocrinology · doi:10.1210/en.2015-1158 · Cited by 4
Clinical Symptoms and Quality of Life: Hot Flashes and Mood
Llaneza, P. (2017) · Springer eBooks · doi:10.1007/978-3-319-59318-0_4 · Cited by 4
Estradiol elicits distinct firing patterns in arcuate nucleus kisspeptin neurons of females through altering ion channel conductancesPreprint
Qiu, J., Voliotis, M., Bosch, M. A., Li, X. F., Zweifel, L. S., Tsaneva-Atanasova, K. T., O'Byrne, K. T., Rønnekleiv, O. K., & Kelly, M. J. (2024) · eLife · doi:10.7554/elife.96691 · Cited by 4
Advent of NK3R Antagonists for the Treatment of Menopausal Hot Flushes: A Narrative Review
Patel, A., Pierret, A. C. S., Mills, E., Comninos, A. N., Dhillo, W. S., & Abbara, A. (2025) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.18338 · Cited by 4
Neurokinin 3 receptor–selective agonist, senktide, decreases core temperature in Japanese Black cattle
Nakamura, S., Masafumi, M. I. W. A., Morita, Y., Ohkura, S., Yamamura, T., Wakabayashi, Y., & Matsuyama, S. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106522 · Cited by 3
Kisspeptin system–physiology and clinical perspectives
Stoynev, N., & Kumanov, P. (2025) · Annales d Endocrinologie · doi:10.1016/j.ando.2025.101793 · Cited by 4
Effect of intermittent administration of neurokinin 3 receptor agonist on luteinizing hormone secretion, estrus, and ovulation in feed-restricted goats
Natsumi, E. N. D. O., & TANAKA, T. (2015) · Small Ruminant Research · doi:10.1016/j.smallrumres.2015.04.011 · Cited by 3
Morphological and functional evidence for sexual dimorphism in neurokinin B signalling in the retrochiasmatic area of sheep
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How alcohol affects insulin‐like growth factor‐1's influences on the onset of puberty: A critical review
Dees, W. L., Hiney, J. K., & Srivastava, V. K. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14711 · Cited by 3
Impact of One-Week Administration of Dihydrotestosterone in Rat Anterior Pituitary Gland
Kanasaki, H., Tumurbaatar, T., Cairang, Z., Tumurgan, Z., Oride, A., Okada, H., & Kyo, S. (2022) · International Journal of Endocrinology · doi:10.1155/2022/9525227 · Cited by 3
“In addition, kisspeptin secretion is stimulated and inhibited by NKB and Dyn A, respectively [37].”
Background
Interactions between β‐endorphin and kisspeptin neurons of the ewe arcuate nucleus are modulated by photoperiod
Hellier, V., Dardente, H., Lomet, D., Cognié, J., & Dufourny, L. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13242 · Cited by 3
“Moreover, KNDy neurons establish reciprocal connections (KNDy-KNDy) that account for GnRH/ LH pulsatile release(29) and are considered as the “pulse generator” in several mammalian species including mouse(30) and goat.(31) The question remains whether other peptidergic neuronal populations involved in the”
Background
Molecular species of prostaglandins involved in modulating luteinising hormone pulses of female rats under infectious stress conditions
Matsuwaki, T., Komatsuda, M., Fujisawa, A., Doke, M., Yamanouchi, K., & Nishihara, M. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12490 · Cited by 3
Hypothalamic concentrations of kisspeptin and gonadotropin‐releasing hormone during the breeding season and non‐breeding season in ewes
Urías-Castro, C., Arreguin-Arevalo, J. A., Magee, C., Weber, E., & Nett, T. M. (2019) · American Journal of Reproductive Immunology · doi:10.1111/aji.13146 · Cited by 3
The effects of supraphysiological levels of testosterone on neural networks upstream of gonadotropin-releasing hormone neurons.
Salehi, M. S., Khazali, H., Mahmoudi, F., & Janahmadi, M. (2019) · PubMed Central · doi:10.22038/ijbms.2019.36127.8605 · Cited by 3
“In addition, several lines of evidence have suggested that ARC kisspeptin neurons regulate pulsatile GnRH secretion via the autosynaptic activity of the neurokinin B (NKB) and dynorphin (DYN), involved in generating the rhythmic discharge of kisspeptin (8, 9).”
Background
Different pituitary action of NK3Ra and NK3Rb in grass carp
Xu, S., Zhou, L., Guo, S., Hu, Q., Shi, X., Xia, C., Zhang, H., Ye, C., Jia, Y., & Hu, G. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113829 · Cited by 3
Epigenetic and transcriptional regulation of GnRH gene under altered metabolism and ageing
Chandra, K., Banerjee, A., & Das, M. (2021) · The Nucleus · doi:10.1007/s13237-021-00374-z · Cited by 3
Gene Networks, Epigenetics and the Control of Female Puberty
Lomniczi, A., Castellano, J. M., Wright, H., Selcuk, B., Sönmez, K., & Ojeda, S. R. (2014) · Research and perspectives in endocrine interactions · doi:10.1007/978-3-319-09168-6_8 · Cited by 3
“KNDy neurons release NKB, which acts on other KNDy neurons via specific receptors to stimulate kisspeptin release (Wakabayashi et al. 2010; Navarro et al. 2011).”
BackgroundInfluential
Establishment of immortalised cell lines derived from female Shiba goat KNDy and GnRH neurones
Suetomi, Y., Tatebayashi, R., Sonoda, S., Munetomo, A., Matsuyama, S., Inoue, N., Uenoyama, Y., Takeuchi, Y., Tsukamura, H., Ohkura, S., et al. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12857 · Cited by 3
Control of GnRH Secretion
Bonomi, M., Vezzoli, V., & Cariboni, A. M. (2017) · Endocrinology · doi:10.1007/978-3-319-44441-3_1 · Cited by 4
Continuous acceleration of neural activity of the GnRH pulse generator during chronic peripheral infusion of neurokinin 3 receptor agonist in goats
Yamamura, T., OKAMURA, H., & Wakabayashi, Y. (2023) · Journal of Reproduction and Development · doi:10.1262/jrd.2023-025 · Cited by 3
The Effects of the Novel Reproductive Peptide Phoenixin-20 Amide on GnRH and Kisspeptin Hypothalamic Cell Models
Treen, A. K. (2014) · TSpace (University of Toronto) · Cited by 3
Kisspeptin control of hypothalamus-pituitary-ovarian functions
Joy, K. P., & Chaube, R. (2024) · Vitamins and hormones · doi:10.1016/bs.vh.2024.06.005 · Cited by 3
KNDy Neurons and the Control of the Gonadotropic Axis in the Midgestation Fetal Sheep
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Chronic periadolescent leuprolide exposure affects the expression of multiple genes in the hypothalamus and pituitary gland with a different pattern of expression in female and male Long-Evans rats
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KNDy neurons as an indirect target of insulin‐like growth factor‐1
Silva, J. D. N., de Sousa, L. M. M., de Sousa, M. E., Vieira, H. R., Alves, G. A., Neifert, N. T., Moore, A. M., Donato, J., & Frazão, R. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70130 · Cited by 3
Kisspeptin made in the preoptic area is required for normal estradiol-induced LH surges and optimal fertility in females
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Socio-Sexual Stimuli and Reproductive Function: Emerging Perspectives of the Male Effect in Sheep and Goats
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O neuropeptídeo kisspeptina e a reprodução animal: uma revisão
Dias, J. C. O., Veloso, C. M., Donzele, R. F. M. D. O., & de Carvalho, G. R. (2018) · Multi-Science Journal · doi:10.33837/msj.v1i2.76 · Cited by 2
Characteristics of Neurokinin-3 Receptor and Its Binding Sites by Mutational Analysis
Atre, I., Mizrahi, N., & Levavi‐Sivan, B. (2021) · Biology · doi:10.3390/biology10100968 · Cited by 2
Male‐induced early puberty correlates with the maturation of arcuate nucleus kisspeptin neurons in does
Meunier, M. A., Porte, C., Poissenot, K., Vacher, H., Brachet, M., Chamero, P., Beltramo, M., Abecia, J. A., Delgadillo, J. A., Chemineau, P., et al. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13284 · Cited by 3
“Yet, immunohistochemical approaches show a particular abundance of kisspeptin protein in the caudal part of the ARC.(31,38,50) The approach used in this study could explain why the results obtained in the ARCc are not found in the ARCm.”
BackgroundMethodResultInfluential
NK3R signalling in the posterodorsal medial amygdala is involved in stress‐induced suppression of pulsatile LH secretion in female mice
Ivanova, D., Voliotis, M., Tsaneva-Atanasova, K. T., O'Byrne, K. T., & Li, X. (2024) · Journal of Neuroendocrinology · doi:10.1111/jne.13384 · Cited by 3
“In recent years, animal and human studies examining the effect of NK3R signalling on the function of the HPG axis have accumulated largely conflicting evidence.”
Background
Peripheral administration of a κ-opioid receptor agonist nalfurafine inactivates gonadotropin-releasing hormone pulse generator activity in goats
Matsuda, F., Ito, D., Wakabayashi, Y., Yamamura, T., Okamura, H., & Ohkura, S. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.137918 · Cited by 2
“…evidence supports the idea that KNDy neurons, which are cells in the arcuate nucleus (ARC) of the hypothalamus that express kisspeptin, neurokinin B (NKB), and dynorphin A (Dyn) [2,3], are pacemaker cells which drive GnRH/LH pulses, and are thus thought to be the GnRH pulse generator [4 – 6].”
Absence of sex differences in diabetes-induced suppression of KNDy neurons in rats
Otsuka, M., Iwata, K., Otsuka, Y., Uenoyama, Y., Ozawa, H., & Ishii, H. (2024) · Journal of Endocrinology · doi:10.1530/joe-23-0293 · Cited by 2
The Kisspeptin System as Putative Target for Endocrine Disruption of Puberty and Reproductive Health
Tena‐Sempere, M. (2011) · Research and perspectives in endocrine interactions · doi:10.1007/978-3-642-22775-2_2 · Cited by 2
“2010), together with its putative effects on the GnRH pulse generator (Wakabayashi et al. 2010), has led to the contention that NKB participates in the fine tuning of kisspeptin output at the hypothalamus, thereby playing a role in the regulation of pulsatile GnRH secretion.”
Background
Luteal activity of Abadeh ecotype does in summer and winter and the effect of a single dose of kisspeptin-10 injection on luteinizing hormone secretion in the anestrus does
Arjmand, M., Mirzaei, A., Shirazi, M. R. J., Tamadon, A., Salehi, M. S., Saeb, M., Namavar, M. R., Zandi, M., Shahheidari, H., & Moradi, S. (2014) · Cited by 2
Evaluating the potential utility of kisspeptin to treat reproductive disorders
Mogford, J. T., Jayasena, C. N., & Dhillo, W. S. (2014) · Expert Review of Endocrinology & Metabolism · doi:10.1586/17446651.2014.890888 · Cited by 2
Maturation and Physiology of Hypothalamic Regulation of the Gonadal Axis
Uenoyama, Y., Inoue, N., Ieda, N., Pheng, V., Maeda, K., & Tsukamura, H. (2016) · Springer eBooks · doi:10.1007/978-3-319-32122-6_1 · Cited by 2
Studies on the Character of Hypothalamic GnRH Neurons and Kisspeptin Neurons Using Hypothalamic Cell Models
Kanasaki, H., Oride, A., Tumurbaatar, T., & Kyo, S. (2018) · IntechOpen eBooks · doi:10.5772/intechopen.73128 · Cited by 2
“ KNDy neurons generate synchronized oscillatory patterns of neuronal activity by sharing excitatory and inhibitory input from NKB and dynorphin produced within themselves [13, 14].”
Background
Unraveling the Neural Mechanisms Underlying the GnRH Pulse Generator: An Update
Goodman, R. L., Coolen, L. M., & Lehman, M. N. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819801-8.00019-3 · Cited by 2
Multiple‐Unit Activity Recording of the Gonadotropin‐Releasing Hormone Pulse Generator
Okamura, H., & Mori, Y. (2014) · Wiley eBooks · doi:10.1002/9781118606803.ch14 · Cited by 2
Neuroendocrine Regulation of Puberty
Terasawa, E., & Levine, J. E. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00106-1 · Cited by 2
Mathematical modelling elucidates core mechanisms underpinning GnRH pulse generation
Voliotis, M., Li, X. F., De Burgh, R., Lass, G., Lightman, S. L., O’Byrne, K. T., & Tsaneva-Atanasova, K. (2018) · doi:10.1101/245548 · Cited by 2
“Pharmacological modulators of kisspeptin, NKB and 53 Dyn signaling have been extensively used to perturb the system and study the effect on the activity of a 54 hypothalamic neuronal population (using ARC multiunit activity (MUA) volleys, an 55 electrophysiological correlate of GnRH pulse generator activity, as a prox…”
BackgroundMethod

Authors: Wakabayashi, Y., Nakada, T., Murata, K., Ohkura, S., Mogi, K., Navarro, V. M., Clifton, D. K., Mori, Y., Tsukamura, H., Maeda, K.-I., Steiner, R. A., & Okamura, H.
Affiliations: Institute of Agrobiological Sciences (JP)
Nagoya University (JP)
University of Washington (US)
The University of Tokyo (JP)
ORCID: Wakabayashi, Yoshihiro
Nakada, Tomoaki
Ohkura, Satoshi
Mogi, Kazutaka
Navarro, Victor M.
Tsukamura, Hiroko
Steiner, Robert A.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2010-02-24
Volume: 30
Issue: 8
Pages: 3124-3132
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.5848-09.2010
PMC: PMC6633939
OpenAlex: W2045555035
Cited by: 597
References: 42
Citations by year: 2026: 12 · 2025: 27 · 2024: 19 · 2023: 24 · 2022: 32 · 2021: 36 · 2020: 38 · 2019: 36 · 2018: 42 · 2017: 39 · 2016: 42 · 2015: 42 · 2014: 54 · 2013: 48 · 2012: 47
FWCI: 58.30
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5u54hd012629-31)
National Institute of Child Health and Human Development
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD049651, U54-HD-12629, U54HD-012629)
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 › Neuroendocrine regulation and behavior
Keywords: kisspeptin neurons, arcuate nucleus, neurokinin B, dynorphin A, pulsatile GnRH secretion, luteinizing hormone, multi-unit activity, goats, neuroendocrine regulation of reproduction
MeSH terms: Action Potentials, Animals, Arcuate Nucleus of Hypothalamus, Biological Clocks, Dynorphins, Electrophysiology, Female, Goats, Luteinizing Hormone, Gonadotropin-Releasing Hormone, Neurons, Neurosecretory Systems, Ovariectomy, Periodicity, Proteins, Reproduction, Gonadal Steroid Hormones, Neurokinin B, Tumor Suppressor Proteins, Estrous Cycle, Kisspeptins

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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

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