Regulation of Arcuate Neurons Coexpressing Kisspeptin, Neurokinin B, and Dynorphin by Modulators of Neurokinin 3 and κ-Opioid Receptors in Adult Male Mice

Ruka, Kristen A.; Burger, Laura L.; Moenter, Suzanne M.

doi:10.1210/en.2013-1268

Cited by 150Hypothalamic control of reproductive hormonesNeuropeptides and Animal PhysiologyRegulation of Appetite and Obesity

Regulation of Arcuate Neurons Coexpressing Kisspeptin, Neurokinin B, and Dynorphin by Modulators of Neurokinin 3 and κ-Opioid Receptors in Adult Male Mice

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Ruka, Kristen A., Burger, Laura L., Moenter, Suzanne M.·2013·Endocrinology

DOI 10.1210/en.2013-1268PMC PMC3713217

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Abstract

Pulsatile GnRH release is essential to fertility and is modulated by gonadal steroids, most likely via steroid-sensitive afferents. Arcuate neurons coexpressing kisspeptin, neurokinin B (NKB), and dynorphin (KNDy neurons) are steroid-sensitive and have been postulated to both generate GnRH pulses and mediate steroid feedback on pulse frequency. KNDy neurons are proposed to interact with one another via NKB and dynorphin to activate and inhibit the KNDy network, respectively, and thus alter kisspeptin output to GnRH neurons. To test the roles of NKB and dynorphin on KNDy neurons and the steroid sensitivity of these actions, targeted extracellular recordings were made of Tac2(NKB)-GFP-identified neurons from castrate and intact male mice. Single-cell PCR confirmed most of these cells had a KNDy phenotype. The neurokinin 3 receptor (NK3R) agonist senktide increased action potential firing activity of KNDy neurons. Dynorphin reduced spontaneous KNDy neuron activity, but antagonism of κ-opioid receptors (KOR) failed to induce firing activity in quiescent KNDy neurons. Senktide-induced activation was greater in KNDy neurons from castrate mice, whereas dynorphin-induced suppression was greater in KNDy neurons from intact mice. Interactions of dynorphin with senktide-induced activity were more complex; dynorphin treatment after senktide had no consistent inhibitory effect, whereas pretreatment with dynorphin decreased senktide-induced activity only in KNDy neurons from intact but not castrate mice. These data suggest dynorphin-mediated inhibition of senktide-induced activity requires gonadal steroid feedback. Together, these observations support the hypotheses that activation of NK3R and KOR, respectively, excites and inhibits KNDy neurons and that gonadal steroids modulate these effects.

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Complete coexpression of kisspeptin, NKB and dynorphin is not always found.
“Complete coexpression of kisspeptin, NKB and dynorphin is not always found (Hrabovszky et al., 2012; Navarro et al., 2011), but this issue is complicated by limitations in the sensitivity of detection (Ruka et al., 2013) and differential expression depending on developmental stage (Gill et al., 2012) or physiological state of the animal (Foradori et al., 2005; Navarro et al., 2011; Rance and Bruce”
From Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: A novel hypothesis on the mechanism of hot flushes (2013) · cites this paper as Ruka et al., 2013

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Measuring the Firing Rate of High-Resistance Neurons with Cell-Attached Recording
Alcamí, P., Franconville, R., Llano, I., & Marty, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5371-11.2012 · Cited by 72 · see citing works
GnRH-Deficient Phenotypes in Humans and Mice with Heterozygous Variants inKISS1/Kiss1
Chan, Y.-M., Broder-Fingert, S., Paraschos, S., Lapatto, R., Au, M., Hughes, V., Bianco, S. D. C., Min, L., Plummer, L., Cerrato, F., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0518 · Cited by 68 · see citing works
Dose-Dependent Switch in Response of Gonadotropin-Releasing Hormone (GnRH) Neurons to GnRH Mediated through the Type I GnRH Receptor
Xu, C., Xu, X.-Z., Nunemaker, C. S., & Moenter, S. M. (2003) · Endocrinology · doi:10.1210/en.2003-0562 · Cited by 68 · see citing works
Presence of nuclear androgen receptor-like immunoreactivity in neurokinin B-containing neurons of the hypothalamic arcuate nucleus of the adult male rat
Ciofi, P., Krause, J. E., Prins, G. S., & Mazzuca, M. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90795-1 · Cited by 67 · see citing works
Kappa‐Opioid Receptor Involvement in the Regulation of Pulsatile Luteinizing Hormone Release During Early Pregnancy in the Rat
Gallo, R. V. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00465.x · Cited by 39 · see citing works

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Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: A novel hypothesis on the mechanism of hot flushes
Rance, N. E., Dacks, P. A., Mittelman-Smith, M. A., Romanovsky, A. A., & Krajewski-Hall, S. J. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.07.003 · Cited by 380 · see citing works
The Gonadotropin-Releasing Hormone Pulse Generator
Herbison, A. E. (2018) · Endocrinology · doi:10.1210/en.2018-00653 · Cited by 261 · see citing works
High-frequency stimulation-induced peptide release synchronizes arcuate kisspeptin neurons and excites GnRH neurons
Qiu, J., Nestor, C. C., Zhang, C., Padilla, S. L., Palmiter, R. D., Kelly, M. J., & Rønnekleiv, O. K. (2016) · eLife · doi:10.7554/elife.16246 · Cited by 199 · see citing works
“…shown that dynorphin and k-opioid receptor agonist U69,593 inhibit the activity of spontaneously firing Kiss1ARH neurons, although it has not been established whether this was a postsynaptic or presynaptic action on excitatory input to Kiss1ARH neurons (de Croft et al., 2013; Ruka et al., 2013).”
Background
KNDy Cells Revisited
Moore, A. M., Coolen, L. M., Porter, D. T., Goodman, R. L., & Lehman, M. N. (2018) · Endocrinology · doi:10.1210/en.2018-00389 · Cited by 190 · see citing works
Neuroendocrine control of gonadotropin‐releasing hormone: Pulsatile and surge modes of secretion
Goodman, R. L., Herbison, A. E., Lehman, M. N., & Navarro, V. M. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13094 · Cited by 157 · see citing works
Opioid Receptor-Mediated Regulation of Neurotransmission in the Brain
Reeves, K. C., Shah, N., Muñoz, B., & Atwood, B. K. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.919773 · Cited by 156 · see citing works
Polycystic Ovary Syndrome: Pathophysiology and Therapeutic Opportunities
Dong, J., & Rees, D. A. (2023) · BMJ Medicine · doi:10.1136/bmjmed-2023-000548 · Cited by 123 · see citing works
The Role of the Brain in the Pathogenesis and Physiology of Polycystic Ovary Syndrome (PCOS)
Coutinho, E. A., & Kauffman, A. S. (2019) · Medical Sciences · doi:10.3390/medsci7080084 · Cited by 113 · see citing works
“Since kisspeptin stimulates GnRH neurons and NKB stimulates kisspeptin neurons via the NK3 receptor [90], the findings in the PCOS models suggest a role of the ARN KNDy neurons in driving GnRH hyperactivity and downstream elevated LH pulse secretion.”
Role of KNDy Neurons Expressing Kisspeptin, Neurokinin B, and Dynorphin A as a GnRH Pulse Generator Controlling Mammalian Reproduction
Uenoyama, Y., Nagae, M., Tsuchida, H., Inoue, N., & Tsukamura, H. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.724632 · Cited by 112 · see citing works
Characterization of GnRH Pulse Generator Activity in Male Mice Using GCaMP Fiber Photometry
Han, S. Y., Kane, G., Cheong, I., & Herbison, A. E. (2019) · Endocrinology · doi:10.1210/en.2018-01047 · Cited by 94 · see citing works
Genetic dissection of the different roles of hypothalamic kisspeptin neurons in regulating female reproduction
Wang, L., Vanacker, C., Burger, L. L., Barnes, T. M., Shah, Y. M., Myers, M. G., & Moenter, S. M. (2019) · eLife · doi:10.7554/elife.43999 · Cited by 96 · see citing works
κ-Opioid Receptor Is Colocalized in GnRH and KNDy Cells in the Female Ovine and Rat Brain
Weems, P. W., Witty, C. F., Amstalden, M., Coolen, L. M., Goodman, R. L., & Lehman, M. N. (2016) · Endocrinology · doi:10.1210/en.2015-1763 · Cited by 95 · see citing works
Mechanism of kisspeptin neuron synchronization for pulsatile hormone secretion in male mice
Han, S. Y., Morris, P. G., Kim, J.-C., Guru, S., Pardo-Navarro, M., Yeo, S.-H., McQuillan, H. J., & Herbison, A. E. (2023) · Cell Reports · doi:10.1016/j.celrep.2022.111914 · Cited by 91 · see citing works
“Both pre-and post-synaptic mechanisms of dynorphin action have been reported for ARN KISS neurons 14,15,18,31 with the presynaptic inhibition of AMPA transmission 18,31 being compatible with the proposed gating of SE initiation by dynorphin.”
Influential
A review of the pathophysiology of functional hypothalamic amenorrhoea in women subject to psychological stress, disordered eating, excessive exercise or a combination of these factors
Morrison, A., Fleming, S., & Levy, M. J. (2020) · Clinical Endocrinology · doi:10.1111/cen.14399 · Cited by 101 · see citing works
Neuroanatomy of the Human Hypothalamic Kisspeptin System
Hrabovszky, E. (2013) · Neuroendocrinology · doi:10.1159/000356903 · Cited by 88 · see citing works
Molecular and Environmental Mechanisms Regulating Puberty Initiation: An Integrated Approach
Livadas, S., & Chrousos, G. P. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00828 · Cited by 84 · see citing works
“The role of KNDY in humans is highlighted from the observations that lossof-function mutations in the genes encoding for kisspeptin (KISS1), kisspeptin receptor (KISS1R), NKB (TAC3), or NKB receptor (TACR3) are associated with delayed puberty and hypogonadism (10).”
Background
Kisspeptin Neurons and Estrogen–Estrogen Receptor α Signaling: Unraveling the Mystery of Steroid Feedback System Regulating Mammalian Reproduction
Uenoyama, Y., Inoue, N., Nakamura, S., & Tsukamura, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179229 · Cited by 82 · see citing works
Neuroendocrine Determinants of Polycystic Ovary Syndrome
Szeliga, A., Rudnicka, E., Maciejewska-Jeske, M., Kucharski, M., Kostrzak, A., Hajbos, M., Niwczyk, O., Smolarczyk, R., & Męczekalski, B. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19053089 · Cited by 86 · see citing works
“It is unlikely that kisspeptin itself affects KNDy neurons as no GPR54 have been found on their surface [24].”
Background
Highly redundant neuropeptide volume co-transmission underlying episodic activation of the GnRH neuron dendron
Liu, X., Yeo, S., McQuillan, H. J., Herde, M. K., Hessler, S., Cheong, I., Porteous, R. W., & Herbison, A. E. (2021) · eLife · doi:10.7554/elife.62455 · Cited by 86 · see citing works
“, 2013), while the co-released neuropeptides NKB and dynorphin directly excite and inhibit firing, respectively (de Croft et al., 2013; Ruka et al., 2013; Qiu et al., 2016).”
Background
Neuropeptide co-expression in hypothalamic kisspeptin neurons of laboratory animals and the human
Skrapits, K., Borsay, B. Á., Herczeg, L., Ciofi, P., Liposits, Z., & Hrabovszky, E. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00029 · Cited by 77 · see citing works
“Morphological and electrophysiological studies provided evidence that KNDy neurons communicate extensively with each other (Burke et al., 2006; Foradori et al., 2006; Goodman et al., 2007; Navarro et al., 2011a,b; De Croft et al., 2013; Ruka et al., 2013).”
Background
Puberty in Mice and Rats
Prévot, V. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00030-2 · Cited by 78 · see citing works
Glutamatergic Transmission to Hypothalamic Kisspeptin Neurons Is Differentially Regulated by Estradiol through Estrogen Receptor α in Adult Female Mice
Wang, L.-H., Burger, L. L., Greenwald-Yarnell, M., Myers, M. G., & Moenter, S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2428-17.2017 · Cited by 71 · see citing works
“Dynorphin can inhibit firing activity of arcuate kisspeptin neurons (Ruka et al., 2013); we thus tested the effect of dynorphin on sEPSCs and mEPSCs of arcuate kisspeptin neurons.”
BackgroundMethodResultInfluential
The Role of Kiss1 Neurons As Integrators of Endocrine, Metabolic, and Environmental Factors in the Hypothalamic–Pituitary–Gonadal Axis
Yeo, S.-H., & Colledge, W. H. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00188 · Cited by 76 · see citing works
“More than 90% of Kiss1ARC neurons in the ewe express kappa opioid receptor (KOR) (73); whereas a lower percentage of KOR was revealed by in situ hybridization (39, 74) and single-cell reverse transcription-PCR studies (59).”
Background
Estrogen-Negative Feedback and Estrous Cyclicity Are Critically Dependent Upon Estrogen Receptor-α Expression in the Arcuate Nucleus of Adult Female Mice
Yeo, S., & Herbison, A. E. (2014) · Endocrinology · doi:10.1210/en.2014-1128 · Cited by 72 · see citing works
“As yet, definitive evidence supporting a role for ARN kisspeptin neurons in the adult estrogen negative feedback mechanism has not been forthcoming (22, 53, 54) and is complicated, experimentally, by a putative role for these cells in GnRH pulse generation (4, 55).”
Background
Development of Gonadotropin-Releasing Hormone Secretion and Pituitary Response
Glanowska, K. M., Burger, L. L., & Moenter, S. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2200-14.2014 · Cited by 70 · see citing works
“Linearity and parallelism of the preamplification step was confirmed as described previously (Ruka et al., 2013).”
MethodResultInfluential
Oestrogen‐Induced Activation of Preoptic Kisspeptin Neurones May be Involved in the Luteinising Hormone Surge in Male and Female Japanese Monkeys
Watanabe, Y., Uenoyama, Y., Suzuki, J., Takase, K., Suetomi, Y., Ohkura, S., Inoue, N., Maeda, K., & Tsukamura, H. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12227 · Cited by 70 · see citing works
Electrical properties of kisspeptin neurons and their regulation of GnRH neurons
Piet, R., de Croft, S., Liu, X., & Herbison, A. E. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.05.006 · Cited by 65 · see citing works
A review on critical appraisal and pathogenesis of polycystic ovarian syndrome
Hajam, Y. A., Rather, H., Neelam, Kumar, R., Basheer, M., & Reshi, M. S. (2024) · Endocrine and Metabolic Science · doi:10.1016/j.endmts.2024.100162 · Cited by 72 · see citing works
Activation of Neurokinin 3 Receptors Stimulates GnRH Release in a Location-Dependent but Kisspeptin-Independent Manner in Adult Mice
Gaskins, G. T., Glanowska, K. M., & Moenter, S. M. (2013) · Endocrinology · doi:10.1210/en.2013-1479 · Cited by 64 · see citing works
KNDy Neurons Modulate the Magnitude of the Steroid-Induced Luteinizing Hormone Surges in Ovariectomized Rats
Helena, C. V. V., Toporikova, N., Kalil, B., Stathopoulos, A. M., Pogrebna, V. V., Carolino, R. O. G., Anselmo-Franci, J. A., & Bertram, R. (2015) · Endocrinology · doi:10.1210/en.2015-1070 · Cited by 65 · see citing works
The Role of Neurokinin B Signalling in Reproductive Neuroendocrinology
Grachev, P., Millar, R. P., & O'Byrne, K. T. (2013) · Neuroendocrinology · doi:10.1159/000357734 · Cited by 64 · see citing works
“Indeed, KOR is expressed by mouse KNDy neurones [35], and application of KOR agonists to ex vivo murine hypothalamic slices strongly suppresses the firing rate of GFP-labelled ARC kisspeptin neurones [40,41].”
Background
Differential Roles of Hypothalamic AVPV and Arcuate Kisspeptin Neurons in Estradiol Feedback Regulation of Female Reproduction
Wang, L., & Moenter, S. M. (2020) · Neuroendocrinology · doi:10.1159/000503006 · Cited by 63 · see citing works
Excitability and Burst Generation of AVPV Kisspeptin Neurons Are Regulated by the Estrous Cycle Via Multiple Conductances Modulated by Estradiol Action
Wang, L., DeFazio, R. A., & Moenter, S. M. (2016) · eneuro · doi:10.1523/eneuro.0094-16.2016 · Cited by 79 · see citing works
GABAergic Transmission to Kisspeptin Neurons Is Differentially Regulated by Time of Day and Estradiol in Female Mice
DeFazio, R. A., Elias, C. F., & Moenter, S. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3057-14.2014 · Cited by 59 · see citing works
KNDy Neurons of the Hypothalamus and Their Role in GnRH Pulse Generation: an Update
Moore, A. M., Novak, A. G., & Lehman, M. N. (2023) · Endocrinology · doi:10.1210/endocr/bqad194 · Cited by 62 · see citing works
Effects and Interactions of Tachykinins and Dynorphin on FSH and LH Secretion in Developing and Adult Rats
Ruíz-Pino, F., García-Galiano, D., Manfredi-Lozano, M., León, S., Sanchez-Garrido, M. A., Roa, J., Pinilla, L., Navarro, V. M., & Tena‐Sempere, M. (2014) · Endocrinology · doi:10.1210/en.2014-1026 · Cited by 58 · see citing works
Cyanidin-3-O-glucoside protects against cadmium-induced dysfunction of sex hormone secretion via the regulation of hypothalamus-pituitary-gonadal axis in male pubertal mice
Li, X., Guo, J., Jiang, X., Sun, J., Tian, L., Jiao, R., Tang, Y., & Bai, W. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.04.033 · Cited by 56 · see citing works
Both Estrogen and Androgen Modify the Response to Activation of Neurokinin-3 and κ-Opioid Receptors in Arcuate Kisspeptin Neurons From Male Mice
Ruka, K. A., Burger, L. L., & Moenter, S. M. (2015) · Endocrinology · doi:10.1210/en.2015-1688 · Cited by 52 · see citing works
Endogenous opiates and behavior: 2013
Bodnar, R. J. (2014) · Peptides · doi:10.1016/j.peptides.2014.09.013 · Cited by 52 · see citing works
Evidence that Neurokinin B Controls Basal Gonadotropin-Releasing Hormone Secretion but Is Not Critical for Estrogen-Positive Feedback in Sheep
Li, Q., Millar, R. P., Clarke, I. J., & Smith, J. T. (2015) · Neuroendocrinology · doi:10.1159/000377702 · Cited by 49 · see citing works
Immunoelectron microscopic observation of the subcellular localization of kisspeptin, neurokinin B and dynorphin A in KNDy neurons in the arcuate nucleus of the female rat
Murakawa, H., Iwata, K., Takeshita, T., & Ozawa, H. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.12.008 · Cited by 50 · see citing works
Kisspeptin-neuron control of LH pulsatility and ovulation
Stevenson, H., Bartram, S., Charalambides, M. M., Murthy, S., Petitt, T., Pradeep, A., Vineall, O., Abaraonye, I., Lancaster, A., Koysombat, K., et al. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.951938 · Cited by 48 · see citing works
“In particular, KPneurons in the ARC (ARC KP-neurons) co-express Neurokinin B (NKB) and Dynorphin, and hence are termed Kisspeptin-Neurokinin B-Dynorphin (KNDy) neurons (7).”
Background
Novel Pituitary Actions of TAC3 Gene Products in Fish Model: Receptor Specificity and Signal Transduction for Prolactin and Somatolactin α Regulation by Neurokinin B (NKB) and NKB-Related Peptide in Carp Pituitary Cells
Hu, G., He, M., Ko, W. K. W., Lin, C., & Wong, A. (2014) · Endocrinology · doi:10.1210/en.2014-1105 · Cited by 47 · see citing works
“In grass carp, high level of TAC3 signal could be identified in the hypothalamus, which corroborates with the recent findings of NKB-containing neurons in the hypothalamus of zebrafish (26) and NKB modulation of hypothalamic kisspeptin/GnRH system in mammalian models (18, 19).”
BackgroundInfluential
Neurokinin B and reproductive functions: “KNDy neuron” model in mammals and the emerging story in fish
Hu, G., Lin, C., He, M., & Wong, A. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.08.009 · Cited by 45 · see citing works
Does Dynorphin Play a Role in the Onset of Puberty in Female Sheep?
Lopez, J. A., Bedenbaugh, M. N., McCosh, R. B., Weems, P. W., Meadows, L. J., Wisman, B. A., Coolen, L. M., Goodman, R. L., & Hileman, S. M. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12445 · Cited by 41 · see citing works
Effects of intravenous administration of neurokinin receptor subtype-selective agonists on gonadotropin-releasing hormone pulse generator activity and luteinizing hormone secretion in goats
Yamamura, T., Wakabayashi, Y., Ohkura, S., Navarro, V. M., & OKAMURA, H. (2014) · Journal of Reproduction and Development · doi:10.1262/jrd.2014-109 · Cited by 41 · see citing works
“Moreover, senktide activated KNDy neurons in vitro [19, 21, 22].”
Background
Estradiol Membrane‐Initiated Signaling and Female Reproduction
Micevych, P. E., Wong, A., & Mittelman‐Smith, M. A. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140056 · Cited by 45 · see citing works
Hypothalamic Kisspeptin Neurons: Integral Elements of the GnRH System
Prashar, V., Arora, T., Singh, R., Sharma, A., & Parkash, J. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-01027-5 · Cited by 41 · see citing works
“Approximately 41% and 90% of KNDy express KOR in male mice [163] and sheep [183].”
BackgroundInfluential
Identification of Genes Enriched in GnRH Neurons by Translating Ribosome Affinity Purification and RNAseq in Mice
Burger, L. L., Vanacker, C., Phumsatitpong, C., Wagenmaker, E. R., Wang, L., Olson, D. P., & Moenter, S. M. (2018) · Endocrinology · doi:10.1210/en.2018-00001 · Cited by 41 · see citing works
Nitric oxide-heat shock protein axis in menopausal hot flushes: neglected metabolic issues of chronic inflammatory diseases associated with deranged heat shock response
Miragem, A. A., & de Bittencourt, P. I. H. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx020 · Cited by 39 · see citing works
Estradiol alters body temperature regulation in the female mouse
Krajewski, S. J., Blackmore, E. M., McMinn, J. R., & Rance, N. E. (2017) · Temperature · doi:10.1080/23328940.2017.1384090 · Cited by 39 · see citing works
“In mice, E2 treatment decreases NKB (Tac2) and NK3 receptor (Tacr3) gene expression in KNDy neurons,(16) reduces KNDy neuron excitability(33) and inhibits senktide-induced KNDy neuron firing in hypothalamic tissue slices.(64) Thus, the E2 blunting of the thermoregulatory effect of senktide could be mediated by a direc…”
Background
Sex‐ and sub region‐dependent modulation of arcuate kisspeptin neurones by vasopressin and vasoactive intestinal peptide
Schafer, D. M., Kane, G., Colledge, W. H., Piet, R., & Herbison, A. E. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12660 · Cited by 38 · see citing works
The interaction of fasting, caloric restriction, and diet-induced obesity with 17β-estradiol on the expression of KNDy neuropeptides and their receptors in the female mouse
Yang, J., Yasrebi, A., Snyder, M., & Roepke, T. A. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.008 · Cited by 36 · see citing works
Long-Term Recordings of Arcuate Nucleus Kisspeptin Neurons Reveal Patterned Activity That Is Modulated by Gonadal Steroids in Male Mice
Vanacker, C., Moya, M. R., DeFazio, R. A., Johnson, M. L., & Moenter, S. M. (2017) · Endocrinology · doi:10.1210/en.2017-00382 · Cited by 36 · see citing works
The role of kisspeptin/neurokinin B/dynorphin neurons in pathomechanism of vasomotor symptoms in postmenopausal women: from physiology to potential therapeutic applications
Szeliga, A., Czyzyk, A., Podfigurna, A., Genazzani, A. R., Genazzani, A. D., & Męczekalski, B. (2018) · Gynecological Endocrinology · doi:10.1080/09513590.2018.1480711 · Cited by 35 · see citing works
“Taking into consideration fact, that dynorphin, also synthesized in hypothalamus by KNDy neurons, plays inhibitory role on GnRH secretion, previously demonstrated increase in gonadotropins secretion after menopause may be related to decreased amount of neurons expressing prodynorphin in infundibular nucleus, thus decr…”
Background
Episodic hormone secretion: a comparison of the basis of pulsatile secretion of insulin and GnRH
Nunemaker, C. S., & Satin, L. (2014) · Endocrine · doi:10.1007/s12020-014-0212-3 · Cited by 34 · see citing works
Does the KNDy Model for the Control of Gonadotropin-Releasing Hormone Pulses Apply to Monkeys and Humans?
Lehman, M. N., He, W., Coolen, L. M., Levine, J. E., & Goodman, R. L. (2019) · Seminars in Reproductive Medicine · doi:10.1055/s-0039-3400254 · Cited by 33 · see citing works
Deletion of Stim1 in Hypothalamic Arcuate Nucleus Kiss1 Neurons Potentiates Synchronous GCaMP Activity and Protects against Diet-Induced Obesity
Qiu, J., Stincic, T. L., Bosch, M. A., Connors, A. M., Petrie, S. K., Rønnekleiv, O. K., & Kelly, M. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0622-21.2021 · Cited by 35 · see citing works
Neurokinin B Signaling in the Female Rat: a Novel Link Between Stress and Reproduction
Grachev, P., Li, X. F., Hu, M., Li, S. Y., Millar, R. P., Lightman, S. L., & O’Byrne, K. T. (2014) · Endocrinology · doi:10.1210/en.2013-2038 · Cited by 32 · see citing works
Hypothalamic kisspeptin neurons as potential mediators of estradiol negative and positive feedback
Starrett, J. R., & Moenter, S. M. (2023) · Peptides · doi:10.1016/j.peptides.2023.170963 · Cited by 29 · see citing works
KNDy neurones and GnRH / LH pulse generation: Current understanding and future aspects
Uenoyama, Y., & Tsukamura, H. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13285 · Cited by 29 · see citing works
Effects of menopause on temperature regulation
Gombert, M., Vesterdorf, K., Fuller, A., Maloney, S. K., & Baker, F. C. (2025) · Temperature · doi:10.1080/23328940.2025.2484499 · Cited by 37 · see citing works
Effects and Therapeutic Potentials of Kisspeptin Analogs: Regulation of the Hypothalamic-Pituitary-Gonadal Axis
Matsui, H., & Asami, T. (2014) · Neuroendocrinology · doi:10.1159/000357809 · Cited by 31 · see citing works
Cellular and molecular mechanisms regulating the KNDy neuronal activities to generate and modulate GnRH pulse in mammals
Ikegami, K., Watanabe, Y., Nakamura, S., Goto, T., Inoue, N., Uenoyama, Y., & Tsukamura, H. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100968 · Cited by 31 · see citing works
Do Substance P and Neurokinin A Play Important Roles in the Control of LH Secretion in Ewes?
Fergani, C., Mazzella, L. K., Coolen, L. M., McCosh, R. B., Hardy, S. L., Newcomb, N., Grachev, P., Lehman, M. N., & Goodman, R. L. (2016) · Endocrinology · doi:10.1210/en.2016-1565 · Cited by 28 · see citing works
Neurokinin B Receptor Antagonism Decreases Luteinising Hormone Pulse Frequency and Amplitude and Delays Puberty Onset in the Female Rat
Li, S. Y., Li, X. F., Hu, M., Shao, B., Poston, L., Lightman, S. L., & O'Byrne, K. T. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12167 · Cited by 28 · see citing works
Electrophysiology of Arcuate Neurokinin B Neurons in Female Tac2-EGFP Transgenic Mice
Cholanian, M., Krajewski, S. J., Levine, R. B., McMullen, N. T., & Rance, N. E. (2014) · Endocrinology · doi:10.1210/en.2014-1065 · Cited by 23 · see citing works
“Notably, a recent study of arcuate Tac2-EGFP neurons showed a reduced excitatory response to senktide (an NK3R agonist) in intact male mice, compared with orchidectomized mice (34).”
BackgroundResultInfluential
Kisspeptin-Gpr54 Signaling at the GnRH Neuron Is Necessary for Negative Feedback Regulation of Luteinizing Hormone Secretion in Female Mice
Yeo, S., Clarkson, J., & Herbison, A. E. (2014) · Neuroendocrinology · doi:10.1159/000368608 · Cited by 25 · see citing works
Colocalization of Cocaine- and Amphetamine-Regulated Transcript with Kisspeptin and Neurokinin B in the Human Infundibular Region
Skrapits, K., Borsay, B. Á., Herczeg, L., Ciofi, P., Bloom, S. R., Ghatei, M. A., Dhillo, W. S., Liposits, Z., & Hrabovszky, E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103977 · Cited by 24 · see citing works
“Such autoreceptors include the NK3 [2,9,10], NK1 [11] and NK2 [11] tachykinin receptors through which NKB can excite [11–13], and the k-opioid autoreceptor through which dynorphin and selective kappa-opioid receptor agonists can inhibit [11,13] KNDy neuronal activity.”
Background
Role of Kisspeptin and Neurokinin B in Puberty in Female Non-Human Primates
Terasawa, E., Garcia, J. P., Seminara, S. B., & Keen, K. L. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00148 · Cited by 24 · see citing works
“While direct application of the NK3R agonist senktide on sliced brain preparation stimulates GnRH neuronal activity in mice (36) and the NK3R is described in close proximity to GnRH neuroterminals in rats and sheep (37, 38), only a small number or no GnRH neuronal cell bodies express NK3R in rat and mice (37, 39, 40).”
Background
The role of non-neuronal cells in hypogonadotropic hypogonadism
Smedlund, K., & Hill, J. W. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110996 · Cited by 25 · see citing works
“This population acts as a “pulse generator” that stimulates GnRH pulses under the control of negative feedback by male or female sex steroids (Herbison, 1998; Ciofi et al., 1994; Smith et al., 2005; Navarro et al., 2009a; Ruka et al., 2013).”
Background
Impose of KNDy/GnRH neural circuit in PCOS, ageing, cancer and Alzheimer’s disease: StAR actions in prevention of neuroendocrine dysfunction
Panda, S. P., Kesharwani, A., Singh, G. D., Prasanth, D., Vatchavai, B. R., Kumari, P. V. K., Panda, S. K., & Mallick, S. P. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102086 · Cited by 24 · see citing works
Deficiency of arcuate nucleus kisspeptin results in postpubertal central hypogonadism
Nandankar, N., Negrón, A. L., Wolfe, A., Levine, J. E., & Radovick, S. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00088.2021 · Cited by 24 · see citing works
A role for glial fibrillary acidic protein (GFAP)-expressing cells in the regulation of gonadotropin-releasing hormone (GnRH) but not arcuate kisspeptin neuron output in male mice
Vanacker, C., DeFazio, R. A., Sykes, C. M., & Moenter, S. M. (2021) · eLife · doi:10.7554/elife.68205 · Cited by 22 · see citing works
Chronic Oestradiol Reduces the Dendritic Spine Density of KND y (Kisspeptin/Neurokinin B/Dynorphin) Neurones in the Arcuate Nucleus of Ovariectomised Tac2‐Enhanced Green Fluorescent Protein Transgenic Mice
Cholanian, M., Krajewski, S. J., McMullen, N. T., & Rance, N. E. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12263 · Cited by 23 · see citing works
17β-Estradiol Increases Arcuate KNDy Neuronal Sensitivity to Ghrelin Inhibition of the M-Current in Female Mice
Conde, K., & Roepke, T. A. (2019) · Neuroendocrinology · doi:10.1159/000503146 · Cited by 23 · see citing works
A neurokinin 3 receptor-selective agonist accelerates pulsatile luteinizing hormone secretion in lactating cattle†
Nakamura, S., Wakabayashi, Y., Yamamura, T., Ohkura, S., & Matsuyama, S. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox068 · Cited by 23 · see citing works
Kisspeptin Variations in Patients with Polycystic Ovary Syndrome—A Prospective Case Control Study
Akad, M., Socolov, R. V., Furnică, C., Covali, R. A., Stan, C. D., Crauciuc, E., & Păvăleanu, I. (2022) · Medicina · doi:10.3390/medicina58060776 · Cited by 22 · see citing works
“in 2013 showed that the amount of KISS1 and kisspeptin cells in the arcuate nucleus positively correlates with LH levels in rodent subjects with PCOS [34].”
Background
Kisspeptin neuron electrophysiology: Intrinsic properties, hormonal modulation, and regulation of homeostatic circuits
Jamieson, B. B., & Piet, R. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101006 · Cited by 23 · see citing works
Gonadal steroid neuromodulation of developing and mature hypothalamic neuronal networks
Campbell, R. E., & Herbison, A. E. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.003 · Cited by 21 · see citing works
Prenatal Androgen Treatment Does Not Alter the Firing Activity of Hypothalamic Arcuate Kisspeptin Neurons in Female Mice
Gibson, A. G., Jaime, J., Burger, L. L., & Moenter, S. M. (2021) · eNeuro · doi:10.1523/eneuro.0306-21.2021 · Cited by 20 · see citing works
“9 quality check, this test is also biologically relevant as senktide activates firing activity of Tac2224 GFP neurons (Ruka et al., 2013), and it is possible that age and treatment alter this.”
BackgroundMethodResultInfluential
Mechanism of Arcuate Kisspeptin Neuron Synchronization in Acute Brain Slices From Female Mice
Morris, P. G., & Herbison, A. E. (2023) · Endocrinology · doi:10.1210/endocr/bqad167 · Cited by 21 · see citing works
“…glutamate, ARN KISS neurons co-express neurokinin B (NKB) and dynorphin in almost all mammals (8, 9), and experiments in mice have shown that essentially all ARN KISS neurons synthesize functional tachykinin and kappa opioid receptors that activate and suppress their firing, respectively (10, 11 ).”
Background
The human hypothalamic kisspeptin system: Functional neuroanatomy and clinical perspectives
Hrabovszky, E., Takács, S., Rumpler, É., & Skrapits, K. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820107-7.00017-3 · Cited by 19 · see citing works
The 3rd World Conference on Kisspeptin, “Kisspeptin 2017: Brain and Beyond”: Unresolved questions, challenges and future directions for the field
Lehman, M. N., Coolen, L. M., Steiner, R. A., Neal-Perry, G. S., Wang, L., Moenter, S. M., Moore, A. M., Goodman, R. L., Yeo, S. ‐., Padilla, S. L., et al. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12600 · Cited by 17 · see citing works
A CRH receptor type 1 agonist increases GABA transmission to GnRH neurons in a circulating-estradiol-dependent manner.
Phumsatitpong, C., Guzman, R. D. D., Zuloaga, D., & Moenter, S. (2020) · Endocrinology · doi:10.1210/endocr/bqaa140 · Cited by 12 · see citing works
Estradiol Enhances the Depolarizing Response to GABA and AMPA Synaptic Conductances in Arcuate Kisspeptin Neurons by Diminishing Voltage-Gated Potassium Currents
DeFazio, R. A., Navarro, M. A., Adams, C. E., Milescu, L. S., & Moenter, S. M. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-19.2019 · Cited by 14 · see citing works
“Arcuate kisspeptin neurons were visualized in brain slices from Tac2-enhanced green fluorescent protein (GFP) BAC transgenic mice [015495-UCD/ STOCK Tg (Tac2-EGFP)381Gsat, Mouse Mutant Regional Resource Center; Ruka et al., 2013] and kisspeptin-hrGFP transgenic mice (Cravo et al., 2013).”
BackgroundMethod
Heterogeneity in GnRH and kisspeptin neurons and their significance in vertebrate reproductive biology
Ogawa, S., & Parhar, I. S. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100963 · Cited by 15 · see citing works
Quercetin-loaded PEGylated liposomes alleviate testicular dysfunction in alloxan-induced diabetic rats: The role of Kisspeptin/Neurokinin B/Dynorphin pathway
Mansour, M. F., Behairy, A., Mostafa, M., Khamis, T., Alsemeh, A. E., Ahmed, N. M. Q., & El-Emam, M. M. A. (2025) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2025.117337 · Cited by 14 · see citing works
Glutamate neurotransmission from leptin receptor cells is required for typical puberty and reproductive function in female mice
de Miera, C. S., Bellefontaine, N., Allen, S. J., Myers, M. G., & Elias, C. F. (2024) · eLife · doi:10.7554/elife.93204 · Cited by 15 · see citing works
“These findings indicate that blockade of glutamatergic neurotransmission in LepRb neurons disrupts key components of the GnRH pulse generator ( Han et al., 2023 ; Ruka et al., 2013 ; Uenoyama and Tsukamura, 2023 ), leading ultimately to reproductive deficits.”
Background
Conditional Deletion of KOR (Oprk1) in Kisspeptin Cells Does Not Alter LH Pulses, Puberty, or Fertility in Mice
Coutinho, E. A., Esparza, L. A., Hudson, A. D., Rizo, N., Steffen, P., & Kauffman, A. S. (2022) · Endocrinology · doi:10.1210/endocr/bqac175 · Cited by 14 · see citing works
Growth variations with opposite clinical outcomes and the emerging role of IGF-1
Papadimitriou, A., Marakaki, C., & Papadimitriou, D. T. (2022) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2022.02.004 · Cited by 14 · see citing works
Social isolation and aggression training lead to escalated aggression and hypothalamus-pituitary-gonad axis hyperfunction in mice
Oliveira, V. E. D. M., Evrard, F., Faure, M., & Bakker, J. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01808-3 · Cited by 14 · see citing works
Importance of neuroanatomical data from domestic animals to the development and testing of the KNDy hypothesis for GnRH pulse generation
Lehman, M. N., Coolen, L. M., & Goodman, R. L. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106441 · Cited by 13 · see citing works
Development and Modulation of Female Reproductive Function by Circadian Signals
Gotlieb, N., Moeller, J., & Kriegsfeld, L. J. (2020) · Masterclass in neuroendocrinology · doi:10.1007/978-3-030-40002-6_16 · Cited by 13 · see citing works
“In contrast to NKB, dynorphin inhibits Arc kisspeptin secretion and is thought to participate in the termination of each pulse (Goodman et al. 2013; Ruka et al. 2013).”
Background
Tachykinin signaling defines distinct populations of glia in the enteric nervous system
Muppirala, A. N., Mitchell, P. E., Courtney, E., Debnath, S., D’Alessandro, L. R., Mani, N., Dadabhoy, M., Robinson, A. F., Díaz-Muñoz, C., Paraskevopoulou, M. D., et al. (2026) · Neuron · doi:10.1016/j.neuron.2025.11.030 · Cited by 11 · see citing works
“39 In the intestine, Tacr3 was expressed in the MP in juveniles (3 weeks) and adults (8–12 weeks), exclusively within tdTomato + cells (Figure S2D).”
Kisspeptin in functional hypothalamic amenorrhea: Pathophysiology and therapeutic potential
Patel, A., Koysombat, K., Pierret, A. C. S., Young, M., Comninos, A. N., Dhillo, W. S., & Abbara, A. (2024) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15220 · Cited by 16 · see citing works
Investigation of irisin's role in pubertal onset physiology in female rats
Kutlu, E., Özgen, İ. T., Bulut, H., Koçyiğit, A., Üstünova, S., Hüseyinbaş, Ö., Torun, E., & Cesur, Y. (2023) · Peptides · doi:10.1016/j.peptides.2023.170976 · Cited by 11 · see citing works
The Roles of Neurokinins and Endogenous Opioid Peptides in Control of Pulsatile LH Secretion
Weems, P. W., Lehman, M. N., Coolen, L. M., & Goodman, R. L. (2018) · Vitamins and hormones · doi:10.1016/bs.vh.2018.01.011 · Cited by 11 · see citing works
GnRH Neurons on LSD: A Year of Rejecting Hypotheses That May Have Made Karl Popper Proud
Moenter, S. M. (2017) · Endocrinology · doi:10.1210/en.2017-03040 · Cited by 11 · see citing works
“Treatment of brain slices from intact mice with the KOR antagonist norbinaltorphimine had no effect on long-term firing pattern, consistent with observation of its lack of effect on shortterm firing rate (22).”
Background
Estrogen promotes gonadotropin-releasing hormone expression by regulating tachykinin 3 and prodynorphin systems in chicken
Wu, X., Zhang, Z., Li, Y., Zhao, Y., Ren, Y., Tian, Y., Hou, M., Guo, Y., Li, Q., Tian, W., et al. (2024) · Poultry Science · doi:10.1016/j.psj.2024.103820 · Cited by 10 · see citing works

Neuropeptide and Gonadal Steroid Action on Arcuate Kisspeptin Neurons: Implications for Central Regulation of Fertility.
Ruka, K. A. (2015) · Deep Blue (University of Michigan)
Both Estrogen and Androgen Modify the Response to Activation of Neurokinin-3 and κ-Opioid Receptors in Arcuate Kisspeptin Neurons From Male Mice
Ruka, K. A., Burger, L. L., & Moenter, S. M. (2015) · Endocrinology · doi:10.1210/en.2015-1688 · Cited by 52 · see citing works
Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse
Navarro, V. M., Gottsch, M. L., Wu, M., García-Galiano, D., Hobbs, S. J., Bosch, M. A., Pinilla, L., Clifton, D. K., Dearth, A., Ronnekleiv, O. K., et al. (2011) · Endocrinology · doi:10.1210/en.2011-1143 · Cited by 254 · see citing works
Neurokinin B Activates Arcuate Kisspeptin Neurons Through Multiple Tachykinin Receptors in the Male Mouse
de Croft, S., Boehm, U., & Herbison, A. E. (2013) · Endocrinology · doi:10.1210/en.2013-1231 · Cited by 150 · see citing works
Long-Term Recordings of Arcuate Nucleus Kisspeptin Neurons Reveal Patterned Activity That Is Modulated by Gonadal Steroids in Male Mice
Vanacker, C., Moya, M. R., DeFazio, R. A., Johnson, M. L., & Moenter, S. M. (2017) · Endocrinology · doi:10.1210/en.2017-00382 · Cited by 36 · see citing works

Authors: Ruka, K. A., Burger, L. L., & Moenter, S. M.
Affiliations: University of Michigan (US)
Corresponding author: Moenter, Suzanne M.
ORCID: Burger, Laura L.
Moenter, Suzanne M.
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2013-08-01
Volume: 154
Issue: 8
Pages: 2761-2771
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2013-1268
PMC: PMC3713217
OpenAlex: W2001560124
Cited by: 150
References: 72
Citations by year: 2026: 5 · 2025: 10 · 2024: 12 · 2023: 12 · 2022: 13 · 2021: 15 · 2020: 8 · 2019: 12 · 2018: 13 · 2017: 7 · 2016: 8 · 2015: 9 · 2014: 21 · 2013: 5
FWCI: 17.37
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Endocrinology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01 HD34860, R01HD034860)
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, neurokinin B, dynorphin, KNDy neurons, arcuate nucleus, neurokinin-3 receptor, kappa opioid receptor, senktide, gonadal steroid feedback, pulsatile GnRH release, neuronal firing, castration
MeSH terms: Animals, Arcuate Nucleus of Hypothalamus, Dynorphins, Gonadotropin-Releasing Hormone, Male, Membrane Potentials, Mice, Transgenic, Neurons, Orchiectomy, Peptide Fragments, Pyrrolidines, Substance P, Time Factors, Neurokinin B, Receptors, Opioid, kappa, Receptors, Neurokinin-3, Benzeneacetamides, Green Fluorescent Proteins, Mice, Kisspeptins

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Regulation of Arcuate Neurons Coexpressing Kisspeptin, Neurokinin B, and Dynorphin by Modulators of Neurokinin 3 and κ-Opioid Receptors in Adult Male Mice

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