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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Figure 1 Colocalization of kisspeptin, NKB, and Dyn in the caudal ARC and ME of the goat. Photomicrographs of sections of the ARC stained by immunocytochemistry for kisspeptin ( A ) and NKB ( B ), or kisspeptin ( D ) and Dyn ( E ), are shown. C and F are computer-aid merged images of A and B , or D and E , respectively. An arrow in A or C indicates a cell body containing immunoreactivity (ir) for kisspeptin but not NKB-ir. The large arrows in D or F , or small arrows in E or F , show some cell bodies containing exclusively kisspeptin-ir or Dyn-ir, respectively. Note that numerous kisspeptin/NKB- or kisspeptin/Dyn-positive fibers surround immunopositivecellbodies. G and H are mergedimagesofsectionsoftheMEdoublestainedforkisspeptin/NKBorkisspeptin/Dyn, respectively. The arrowhead in G indicates a fiber with only NKB-ir. The arrowheads in H show fibers with exclusively Dyn-ir. I-K show kisspeptin-ir and positive signals for NKB and PDYN in triple-label histochemistry, respectively. L is a merged image of I-K . MEe, External layer of median eminence; pt, pars tuberalis. Scale bars: A-C , I-L , 50 𝛍 m; D-F , 100 𝛍 m; G , H , 25 𝛍 m.CC-BY-NC-SA · From the PDF

Figure 2 Photomicrographs showing the placement of MUA recording electrodes in three goats [no. Y69 ( A ), no. 709 ( B ), and no. 713 ( C )] from which MUA was successfully recorded. Sections were immunostained for kisspeptin. A pair of brackets indicates the area where a trace of a bundle of electrodes is observed, and a magnification of the indicated area is shown on the right side of each panel. Some kisspeptin-immunopositive cell bodies are shown by arrowheads. Note that because it was not possible to perfuse goats Y69 and 709, immunostaining of their sections was poor. 3V, Third ventricle. Scale bars: left panels, 500 𝛍 m; right panels, 100 𝛍 m.CC-BY-NC-SA · From the PDF

Figure3 Effect of NKB on the MUA andplasmaLHintheOVXgoat.Representativeprofilesofthe MUAandplasmaLHconcentrationsinOVXanimalsthatreceivedanintracerebroventricularinjection of vehicle ( A ) or 0.2 ( B ) or 2 nmol ( C ) of NKB are shown. The arrow indicates timing of injection.CC-BY-NC-SA · From the PDF

Figure 5 Effects of Dyn and nor-BNI on the MUA and plasma LH in the OVX goat. A , Representative profiles of MUA and plasma LHconcentrations in one animal that received an intracerebroventricular injection of 2 nmol of Dyn are shown. The arrow indicates timing of injection. B , Representative profiles of MUA and plasma LH concentrations in one animal that received an intracerebroventricular infusion of nor-BNI at a rate of 60 nmol H18528 600 𝛍 l -1 H18528 h -1 for 2 h are shown. The bar indicates the period of infusion.CC-BY-NC-SA · From the PDF

Figure 6 Schematic representation of the role of ARC kisspeptin/NKB/Dyn neurons in the generation of the pulsatile GnRH release. According to this model, kisspeptin/NKB/Dyn neurons in the ARC form a neural circuit by their collaterals and dendrites. Within the neural circuit, NKB/NK3 signaling plays the role of accelerator, whereas Dyn/KOR signaling serves as a brake on activation of kisspeptin/NKB/Dyn neurons. Through the reciprocal actions of NKB/NK3 and Dyn/KOR signaling, rhythmic oscillation of neural activity is generated in kisspeptin/NKB/Dyn neurons, which in turn induces pulsatile kisspeptin release at the ME and hence pulsatile GnRH release into the portal circulation. Thus, ARC kisspeptin/NKB/Dyn neurons would act as the GnRH pulse generator through the coordinated interaction between three peptides. See text for details.CC-BY-NC-SA · From the PDF

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Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone
Belchetz, P. E., Plant, T. M., Nakai, Y., Keogh, E. J., & Knobil, E. (1978) · Science · doi:10.1126/science.100883 · Cited by 1,385
The Neuroendocrine Control of the Menstrual Cycle
Knobil, E. (1980) · Elsevier eBooks · doi:10.1016/b978-0-12-571136-4.50008-5 · Cited by 1,285 · cited 1×
“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
Algorithms for the study of episodic hormone secretion
Merriam, G. R., & Wachter, K. W. (1982) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1982.243.4.e310 · Cited by 1,221 · cited 1×
“LH pulses were identified by the PULSAR computer program (Merriam and Wachter, 1982).”
Method
Advances in Male Contraception
Page, S. T., Amory, J. K., & Bremner, W. J. (2008) · Endocrine Reviews · doi:10.1210/er.2007-0041 · Cited by 1,138
Regulation of Kiss1 gene expression in the brain of the female mouse
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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.”
Background
Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology
Watson, R. E., Wiegand, S. J., Clough, R. W., & Hoffman, G. E. (1986) · Peptides · doi:10.1016/0196-9781(86)90076-8 · Cited by 933
Kisspeptin Signaling in the Brain
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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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“[41] Wakabayashi Y, Nakada T, Murata K, et al.”
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Navarro, V. M. (2010) · Frontiers in Bioscience-Scholar · doi:10.2741/s150 · Cited by 42
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“Multiunit activity (MUA) volleys near KNDy neurons in the ARC closely correspond with LH pulses (8).”
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Background
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“A quarter century later, another group reported that GnRH pulse-generating activity by MUA is readily recorded when electrodes are located in or near the arcuate nucleus (ARC), in close proximity to kisspeptin neurons in goats (Wakabayashi et al., 2010).”
Background
Does the KNDy Model for the Control of Gonadotropin-Releasing Hormone Pulses Apply to Monkeys and Humans?
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BackgroundInfluential
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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 32
Kisspeptin and neurokinin B: roles in reproductive health
Koysombat, K., Tsoutsouki, J., Patel, A., Comninos, A. N., Dhillo, W. S., & Abbara, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00015.2024 · Cited by 39
Indirect Suppression of Pulsatile LH Secretion by CRH Neurons in the Female Mouse
Yip, S. H., Liu, X., Hessler, S., Cheong, I., Porteous, R. W., & Herbison, A. E. (2020) · Endocrinology · doi:10.1210/endocr/bqaa237 · Cited by 31
The Decline in Pulsatile GnRH Release, as Reflected by Circulating LH Concentrations, During the Infant-Juvenile Transition in the Agonadal Male Rhesus Monkey (Macaca mulatta) Is Associated With a Reduction in Kisspeptin Content of KNDy Neurons of the Arcuate Nucleus in the Hypothalamus
Ramaswamy, S., Dwarki, K., Ali, B. F., Gibbs, R. B., & Plant, T. M. (2013) · Endocrinology · doi:10.1210/en.2012-2154 · Cited by 30
Neurokinin‐3 Receptor Activation in the Retrochiasmatic Area is Essential for the Full Pre‐Ovulatory Luteinising Hormone Surge in Ewes
Porter, K. L., Hileman, S. M., Hardy, S. L., Nestor, C. C., Lehman, M. N., & Goodman, R. L. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12180 · Cited by 30
Control of the Menstrual Cycle
Zeleznik, A. J., & Plant, T. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00028-4 · Cited by 30
Neurokinin B regulates reproduction via inhibition of kisspeptin in a teleost, the striped bass
Zmora, N., Wong, T.-T., Stubblefield, J., Levavi‐Sivan, B., & Zohar, Y. (2017) · Journal of Endocrinology · doi:10.1530/joe-16-0575 · Cited by 30
KNDy neuron as a gatekeeper of puberty onset
Uenoyama, Y., Tsukamura, H., & Maeda, K. (2014) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.12398 · Cited by 29
“examined the effect of neurokinin B and dynorphin A on GnRH pulse generation and demonstrated that neurokinin B facilitated and dynorphin A inhibited the MUA volley in goats.(69) These findings suggest that KNDy neurons are an intrinsic source of GnRH pulse generator, in which neurokinin B and dynorphin A function as…”
Background
Differential response patterns of kisspeptin and RFamide‐related peptide to photoperiod and sex steroid feedback in the Djungarian hamster (Phodopus sungorus)
Rasri-Klosen, K., Simonneaux, V., & Klosen, P. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12529 · Cited by 29
Characterization of Kisspeptin Neurons in the Human Rostral Hypothalamus
Rumpler, É., Skrapits, K., Takács, S., Göcz, B., Trinh, S. H., Rácz, G. A., Matolcsy, A., Kozma, Z., Ciofi, P., Dhillo, W. S., et al. (2020) · Neuroendocrinology · doi:10.1159/000507891 · Cited by 29
Opioidergic pathways and kisspeptin in the regulation of female reproduction in mammals
Uenoyama, Y., Tsuchida, H., Nagae, M., Inoue, N., & Tsukamura, H. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.958377 · Cited by 30
“Using immunohistochemistry, Goodman and colleagues first demonstrated that dynorphin and NKB are largely coexpressed in a single population of ARC neurons in ewes (Foradori et al., 2006) and then revealed that kisspeptin is also expressed in the majority of the same neuronal population (Goodman et al., 2007).”
BackgroundInfluential
Oestrogen‐Dependent Suppression of Pulsatile Luteinising Hormone Secretion andKiss1mRNA Expression in the Arcuate Nucleus During Late Lactation in Rats
Yamada, S., Uenoyama, Y., Deura, C., Minabe, S., Naniwa, Y., Iwata, K., Kawata, M., Maeda, K., & Tsukamura, H. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02330.x · Cited by 29
Prenatal testosterone exposure decreases colocalization of insulin receptors in kisspeptin/neurokinin B/dynorphin and agouti‐related peptide neurons of the adult ewe
Cernea, M., Phillips, R., Padmanabhan, V., Coolen, L. M., & Lehman, M. N. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13373 · Cited by 28
“secretion (Wakabayashi et al., 2010; Okamura et al., 2013) and, in sheep, also appear to be activated during the preovulatory GnRH surge (Merkley et al.”
Background
A "Timed" Kiss Is Essential for Reproduction: Lessons from Mammalian Studies
Putteeraj, M., Soga, T., Ubuka, T., & Parhar, I. S. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00121 · Cited by 28
“Central administration of Dyn inhibited multiple-unit activity (MUA) in the medial basal hypothalamus and pulsatile LH secretion, whereas NKB induced MUA and pulsatile LH secretion (135).”
Background
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
“bursts of multiunit electrical activity in goats (44), but this”
Background
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
Evaluation of Immortalized AVPV- and Arcuate-Specific Neuronal Kisspeptin Cell Lines to Elucidate Potential Mechanisms of Estrogen Responsiveness and Temporal Gene Expression in Females
Jacobs, D. C., Veitch, R. E., & Chappell, P. E. (2016) · Endocrinology · doi:10.1210/en.2016-1294 · Cited by 28
Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
Campo, A., Lafont, A.-G., Lefranc, B., Leprince, J., Tostivint, H., Kamech, N., Dufour, S., & Rousseau, K. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00304 · Cited by 28
“However, evidence for stimulatory [mouse (17, 18); monkey (20, 26, 65); sheep (19, 26, 66–68); and human (21, 22)] or inhibitory [rat (69); mouse (70); and goat (71)] effects of NKB on LH have also been documented.”
Background
Regulation of kisspeptin and gonadotropin-releasing hormone expression in rat placenta: study using primary cultures of rat placental cells
Oride, A., Kanasaki, H., Mijiddorj, T., Sukhbaatar, U., Ishihara, T., & Kyo, S. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0083-3 · Cited by 27
“In this series of experiment, we also examined NKB expression, which is coexpressed in kisspeptin-producing neurons in the arcuate nucleus (ARC) of the rat hypothalamus and positively regulates their activity [18, 19].”
Background
Pacemaking kisspeptin neurons
Kelly, M. J., Zhang, C., Qiu, J., & Rønnekleiv, O. K. (2013) · Experimental Physiology · doi:10.1113/expphysiol.2013.074559 · Cited by 25
“As such, Kiss1 neurons may themselves be an endogenous source of GABA, whose action could be autoinhibitory and perhaps be responsible for hyperpolarizing Kiss1 neurons via GABAB receptors in addition to the actions of dynorphin via κ-opioid receptors (Navarro et al. 2009; Wakabayashi et al. 2010).”
Background
Distribution and regulation of gonadotropin-releasing hormone, kisspeptin, RF-amide related peptide-3, and dynorphin in the bovine hypothalamus
Tanco, V. M., Whitlock, B. K., Jones, M. A., Wilborn, R. R., Brandebourg, T. D., & Foradori, C. D. (2016) · PeerJ · doi:10.7717/peerj.1833 · Cited by 29
“Dynorphin inhibits episodic LH secretion in rats, goats, and sheep (Gallo, 1990; Goodman et al., 2004; Wakabayashi et al., 2010).”
BackgroundInfluential
Photoperiodic Co‐Regulation of Kisspeptin, Neurokinin B and Dynorphin in the Hypothalamus of a Seasonal Rodent
Bartzen-Sprauer, J., Klosen, P., Ciofi, P., Mikkelsen, J. D., & Simonneaux, V. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12171 · Cited by 28
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
“The GnRH pulse generator consists of bursts of multiunit activity in the arcuate nucleus that are timed with pulses of serum LH, and this phenomenon has been demonstrated in the monkey (56), goat (13, 55), and rat (57, 58).”
Background
Ad libitum feeding triggers puberty onset associated with increases in arcuate Kiss1 and Pdyn expression in growth-retarded rats
Majarune, S., Nima, P., Sugimoto, A., Nagae, M., Inoue, N., Tsukamura, H., & Uenoyama, Y. (2019) · Journal of Reproduction and Development · doi:10.1262/jrd.2019-048 · Cited by 26
Molecular causes of hypogonadotropic hypogonadism
Topaloglu, A. K., & Kotan, L. D. (2010) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e32833bb425 · Cited by 27
Prenatal Testosterone Excess Decreases Neurokinin 3 Receptor Immunoreactivity within the Arcuate Nucleus KND y Cell Population
Ahn, T., Fergani, C., Coolen, L. M., Padmanabhan, V., & Lehman, M. N. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12244 · Cited by 27
κ Agonists as a novel therapy for menopausal hot flashes
Oakley, A. E., Steiner, R. A., Chavkin, C., Clifton, D. K., Ferrara, L. K., & Reed, S. D. (2015) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000000476 · Cited by 26
“If kisspeptin neurons trigger hot flashes, it might be possible to inhibit hot flashes pharmacologically with k agonists by inhibiting the neuronal activity of KNDy neurons.(15) Unfortunately, pure k agonists—when administered systemically to humans—cause dysphoria and nausea,(25) making them suboptimal choices for th…”
Background
The role of neuropeptides and neurotransmitters on kisspeptin/kiss1r-signaling in female reproduction
Saedi, S., Khoradmehr, A., Shirazi, M. R. J., & Tamadon, A. (2018) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2018.07.001 · Cited by 26
Photoperiod effects on the expression of kisspeptin and gonadotropin genes in Atlantic cod, Gadus morhua, during first maturation
Cowan, M. E., Davie, A., & Migaud, H. (2012) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2012.05.191 · Cited by 26
Is it time to reconsider the relative weight of sociosexual relationships compared with photoperiod in the control of reproduction of small ruminant females?
Delgadillo, J. A., Hernández, H., Abecia, J. A., Keller, M., & Chemineau, P. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106468 · Cited by 25
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
“The network connectivity and peptidergic communication of KNDy neurons with each other and with GnRH neurons have also been implicated in the regulation of the GnRH/LH pulse generator [2,3,8]; while NKB increases, dynorphin decreases the frequency of LH secretory episodes in gonadectomized goats [3].”
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
GnRH(1-5), a metabolite of gonadotropin-releasing hormone, enhances luteinizing hormone release via activation of kisspeptin neurons in female rats
Ieda, N., Assadullah, Minabe, S., Ikegami, K., Watanabe, Y., Sugimoto, Y., Sugimoto, A., Kawai, N., Ishii, H., Inoue, N., et al. (2020) · Endocrine Journal · doi:10.1507/endocrj.ej19-0444 · Cited by 25
“The coronal forebrain sections (50-μm thickness) including the AVPV and the ARC were made on a cryostat, with one section every 100 and 200 μm, respectively, and were subjected to the ISH as described previously [13].”
BackgroundMethod
Identification of Hypothalamic Arcuate Nucleus-Specific Enhancer Region of Kiss1 Gene in Mice
Goto, T., Tomikawa, J., Ikegami, K., Minabe, S., Abe, H., Fukanuma, T., Imamura, T., Takase, K., Sanbo, M., Tomita, K., et al. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1289 · Cited by 25
“Multiple-unit activities recorded near kisspeptin neurons in the ARC were associated with pulsatile LH secretion in rats (13) and goats (3, 4).”
Background
KNDy Hypothesis for Generation of GnRH Pulses: Evidence from Sheep and Goats
Goodman, R. L., Okhura, S., Okamura, H., Coolen, L. M., & Lehman, M. N. (2018) · Wiley eBooks · doi:10.1002/9781119233275.ch12 · Cited by 24
Conditional kisspeptin neuron-specific Kiss1 knockout with newly generated Kiss1-floxed and Kiss1-Cre mice replicates a hypogonadal phenotype of global Kiss1 knockout mice
Ikegami, K., Goto, T., Nakamura, S., Watanabe, Y., Sugimoto, A., Majarune, S., Horihata, K., Nagae, M., Tomikawa, J., Imamura, T., et al. (2020) · Journal of Reproduction and Development · doi:10.1262/jrd.2020-026 · Cited by 24
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
The impact of inflammatory stress on hypothalamic kisspeptin neurons: Mechanisms underlying inflammation-associated infertility in humans and domestic animals
Magata, F., Tsukamura, H., & Matsuda, F. (2023) · Peptides · doi:10.1016/j.peptides.2023.170958 · Cited by 27
Leap of Faith: Does Serum Luteinizing Hormone Always Accurately Reflect Central Reproductive Neuroendocrine Activity?
Moenter, S. M. (2015) · Neuroendocrinology · doi:10.1159/000438790 · Cited by 24
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
Neurokinin B Causes Acute GnRH Secretion and Repression of GnRH Transcription in GT1–7 GnRH Neurons
Glidewell-Kenney, C., Shao, P., Iyer, A. K., Grove, A., Meadows, J. D., & Mellon, P. L. (2013) · Molecular Endocrinology · doi:10.1210/me.2012-1271 · Cited by 24
Arcuate nucleus neuropeptide coexpression and connections to gonadotrophin‐releasing hormone neurones in the female rhesus macaque
True, C. A., Takahashi, D. L., Kirigiti, M. A., Lindsley, S. R., Moctezuma, C., Arik, A. J., Smith, M. S., Kievit, P., & Grove, K. L. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12491 · Cited by 24
“Coexpression of other neuropeptides with kisspeptin in arcuate neurons is hypothesized to play an important role in the regulation of this critical reproductive output signal [27, 30, 67-70].”
Testing the Critical Window Hypothesis of Timing and Duration of Estradiol Treatment on Hypothalamic Gene Networks in Reproductively Mature and Aging Female Rats
Yin, W., Maguire, S. M., Pham, B., Garcia, A. N., Dang, N.-V., Liang, J., Wolfe, A., Hofmann, H. A., & Gore, A. C. (2015) · Endocrinology · doi:10.1210/en.2015-1032 · Cited by 23
Inducible Kiss1 knockdown in the hypothalamic arcuate nucleus suppressed pulsatile secretion of luteinizing hormone in male mice
Minabe, S., Nakamura, S., Fukushima, E., Sato, M., Ikegami, K., Goto, T., Sanbo, M., Hirabayashi, M., Tomikawa, J., Imamura, T., et al. (2020) · Journal of Reproduction and Development · doi:10.1262/jrd.2019-164 · Cited by 23
Central µ-Opioid Receptor Antagonism Blocks Glucoprivic LH Pulse Suppression and Gluconeogenesis/Feeding in Female Rats
Tsuchida, H., Kawai, N., Yamada, K., Takizawa, M., Inoue, N., Uenoyama, Y., & Tsukamura, H. (2021) · Endocrinology · doi:10.1210/endocr/bqab140 · Cited by 23
Reproductive neuropeptides: Prevalence of GnRH and KNDy neural signalling components in a model avian, gallus gallus
Joseph, N. T., Tello, J. A., Bédécarrats, G. Y., & Millar, R. P. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.05.018 · Cited by 23
“The ARC subpopulation of Kiss neurones co-express neurokinin B (NKB) and dynorphin (Dyn) and have been subsequently termed ‘KNDy neurones’ (Burke et al., 2006; Goodman et al., 2007; Lehman et al., 2010a; Navarro et al., 2009; Wakabayashi et al., 2010).”
Background
Electrophysiology of Kisspeptin Neurons
Alreja, M. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-6199-9_16 · Cited by 21
“Moreover, the recorded burst activity synchronized with discrete pulses of LH and was reduced by gonadal steroid treatments [ 4 ].”
Background
Lights on MsFLASH: a review of contributions
Reed, S. D., LaCroix, A. Z., Anderson, G. L., Ensrud, K. E., Caan, B. J., Carpenter, J. S., Cohen, L. S., Diem, S. J., Freeman, E. W., Joffe, H., et al. (2020) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000001461 · Cited by 24
Dicer ablation in Kiss1 neurons impairs puberty and fertility preferentially in female mice
Roa, J., Ruiz-Cruz, M., Ruiz-Pino, F., Onieva, R., Vazquez, M. J., Sanchez-Tapia, M. J., Ruiz-Rodriguez, J. M., Sobrino, V., Barroso, A., Heras, V., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32347-4 · Cited by 22
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
“Previously, NKB or senktide elicited an obvious increase in LH secretion in seasonally anestrus ewe [19] and juvenile monkeys [20], whose pulsatile GnRH secretions are suppressed, while LH secretions are inhibited by NKB or senktide in the absence or very low levels of sex steroid condition [6, 9, 23, 40].”
BackgroundInfluential
Sex- and brain region-specific patterns of gene expression associated with socially-mediated puberty in a eusocial mammal
Faykoo-Martinez, M., Monks, D. A., Zovkic, I. B., & Holmes, M. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193417 · Cited by 21
Tachykinins, new players in the control of reproduction and food intake: A comparative review in mammals and teleosts
Campo, A., Dufour, S., & Rousseau, K. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1056939 · Cited by 23
Structural insights into neurokinin 3 receptor activation by endogenous and analogue peptide agonists
Sun, W., Yang, F., Zhang, H., Yuan, Q., Ling, S., Wang, Y., Lv, P., Li, Z., Luo, Y., Liu, D., et al. (2023) · Cell Discovery · doi:10.1038/s41421-023-00564-w · Cited by 22
“It was recently demonstrated that the NKB and NK3R systems are involved in the central control of reproduction 15,18,19 .”
Concurrent bullatine A enhances morphine antinociception and inhibits morphine antinociceptive tolerance by indirect activation of spinal κ-opioid receptors
Huang, Q., Sun, M., Chen, Y., Li, X., & Wang, Y. (2016) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2016.12.027 · Cited by 22
“Its specificity was also validated by the antigen absorption test from other laboratories (Wakabayashi et al., 2010; Yamada et al., 2013).”
Background
Development of Novel Neurokinin 3 Receptor (NK3R) Selective Agonists with Resistance to Proteolytic Degradation
Misu, R., Oishi, S., Yamada, A. Y., Yamamura, T., Matsuda, F., Yamamoto, K., Noguchi, T., Ohno, H., Okamura, H., Ohkura, S., et al. (2014) · Journal of Medicinal Chemistry · doi:10.1021/jm500771w · Cited by 22
Surge‐Like Luteinising Hormone Secretion Induced by Retrochiasmatic Area NK 3R Activation is Mediated Primarily by Arcuate Kisspeptin Neurones in the Ewe
Grachev, P., Porter, K. L., Coolen, L. M., McCosh, R. B., Connors, J. M., Hileman, S. M., Lehman, M. N., & Goodman, R. L. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12393 · Cited by 23

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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