Cited by 185Hypothalamic control of reproductive hormonesNeuropeptides and Animal PhysiologyRegulation of Appetite and Obesity

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Neuroanatomy of the Kisspeptin Signaling System in Mammals: Comparative and Developmental Aspects

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Lehman, Michael N., Hileman, Stanley M., Goodman, Robert L.·2013·Advances in Experimental Medicine and Biology

DOI 10.1007/978-1-4614-6199-9_3PMC PMC4059209

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Abstract

Our understanding of kisspeptin and its actions depends, in part, on a detailed knowledge of the neuroanatomy of the kisspeptin signaling system in the brain. In this chapter, we will review our current knowledge of the distribution of kisspeptin cells, fibers, and receptors in the mammalian brain, including the development, phenotype, and projections of different kisspeptin subpopulations. A fairly consistent picture emerges from this analysis. There are two major groups of kisspeptin cell bodies: a large number in the arcuate nucleus (ARC) and a smaller collection in the rostral periventricular area of the third ventricle (RP3V) of rodents and preoptic area (POA) of non-rodents. Both sets of neurons project to GnRH cell bodies, which contain Kiss1r, and the ARC kisspeptin population also projects to GnRH axons in the median eminence. ARC kisspeptin neurons contain neurokinin B and dynorphin, while a variable percentage of those cells in the RP3V of rodents contain galanin and/or dopamine. Neurokinin B and dynorphin have been postulated to contribute to the control of GnRH pulses and sex steroid negative feedback, while the role of galanin and dopamine in rostral kisspeptin neurons is not entirely clear. Kisspeptin neurons, fibers, and Kiss1r are found in other areas, including widespread areas outside the hypothalamus, but their physiological role(s) in these regions remains to be determined.

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Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat
Krajewski, S. J., Burke, M. C., Anderson, M. J., McMullen, N. T., & Rance, N. E. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2009.12.053 · Cited by 178
Projections of Arcuate Nucleus and Rostral Periventricular Kisspeptin Neurons in the Adult Female Mouse Brain
Yeo, S., & Herbison, A. E. (2011) · Endocrinology · doi:10.1210/en.2011-0164 · Cited by 174
Anatomy of the kisspeptin neural network in mammals
Lehman, M. N., Merkley, C. M., Coolen, L. M., & Goodman, R. L. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.020 · Cited by 172
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Comparative insights of the kisspeptin/kisspeptin receptor system: Lessons from non-mammalian vertebrates
Tena‐Sempere, M., Felip, A., Gómez, A., Zanuy, S., & Carrillo, M. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.11.015 · Cited by 164
Regulation of Kiss1 Expression by Sex Steroids in the Amygdala of the Rat and Mouse
Kim, J., Semaan, S. J., Clifton, D. K., Steiner, R. A., Dhamija, S., & Kauffman, A. S. (2011) · Endocrinology · doi:10.1210/en.2010-1498 · Cited by 162
Characterisation of Arcuate Nucleus Kisspeptin/Neurokinin B Neuronal Projections and Regulation during Lactation in the Rat
True, C. A., Kirigiti, M. A., Ciofi, P., Grove, K. L., & Smith, M. S. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02076.x · Cited by 159
Significance of Neonatal Testicular Sex Steroids to Defeminize Anteroventral Periventricular Kisspeptin Neurons and the GnRH/LH Surge System in Male Rats1
Homma, T., SAKAKIBARA, M., Yamada, S., Kinoshita, M., Iwata, K., Tomikawa, J., Kanazawa, T., Matsui, H., Takatsu, Y., Ohtaki, T., et al. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.109.078311 · Cited by 157
Inhibition of Metastin (Kisspeptin-54)-GPR54 Signaling in the Arcuate Nucleus-Median Eminence Region during Lactation in Rats
Yamada, S., Uenoyama, Y., Kinoshita, M., Iwata, K., Takase, K., Matsui, H., Adachi, S., Inoue, K., Maeda, K., & Tsukamura, H. (2007) · Endocrinology · doi:10.1210/en.2006-1529 · Cited by 152
Colocalization of Progesterone Receptors in Parvicellular Dynorphin Neurons of the Ovine Preoptic Area and Hypothalamus
Foradori, C. D., Coolen, L. M., Fitzgerald, M. E., Skinner, D. C., Goodman, R. L., & Lehman, M. N. (2002) · Endocrinology · doi:10.1210/en.2002-220586 · Cited by 149
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The neuroanatomy of the kisspeptin system in the mammalian brain
Mikkelsen, J. D., & Simonneaux, V. (2008) · Peptides · doi:10.1016/j.peptides.2008.09.004 · Cited by 148
KiSS‐1 expression and metastin‐like immunoreactivity in the rat brain
Brailoiu, G. C., Dun, S. L., Ohsawa, M., Yin, D., Yang, J., Chang, J. K., Brailoiu, E., & Dun, N. J. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20350 · Cited by 145
KiSS‐1 and GPR54 Genes are Co‐Expressed in Rat Gonadotrophs and Differentially Regulated In Vivo by Oestradiol and Gonadotrophin‐Releasing Hormone
Richard, N., Galmiche, G., Corvaisier, S., Caraty, A., & Kottler, M. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01653.x · Cited by 144
Exposure to a Complex Cocktail of Environmental Endocrine-Disrupting Compounds Disturbs the Kisspeptin/GPR54 System in Ovine Hypothalamus and Pituitary Gland
Bellingham, M., Fowler, P., Amezaga, M. R., Rhind, S. M., Cotinot, C., Mandon‐Pepin, B., Sharpe, R. M., & Evans, N. P. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0900699 · Cited by 144
Kisspeptin signalling in the brain: Steroid regulation in the rodent and ewe
Smith, J. T. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.04.002 · Cited by 138
Development, Sex Steroid Regulation, and Phenotypic Characterization of RFamide-Related Peptide (Rfrp) Gene Expression and RFamide Receptors in the Mouse Hypothalamus
Poling, M. C., Kim, J., Dhamija, S., & Kauffman, A. S. (2012) · Endocrinology · doi:10.1210/en.2011-2049 · Cited by 134
KiSS-1 and Reproduction: Focus on Its Role in the Metabolic Regulation of Fertility
Tena-Sempere, M. (2006) · Neuroendocrinology · doi:10.1159/000095549 · Cited by 132
Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty
Kauffman, A. S., Navarro, V. M., Kim, J. P., Clifton, D. K., & Steiner, R. A. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00461.2009 · Cited by 132
Sexually dimorphic expression of hypothalamic estrogen receptors α and β and kiss1 in neonatal male and female rats
Cao, J., & Patisaul, H. B. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22648 · Cited by 131
Colocalisation of Dynorphin A and Neurokinin B Immunoreactivity in the Arcuate Nucleus and Median Eminence of the Sheep
Foradori, C. D., Amstalden, M., Goodman, R. L., & Lehman, M. N. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01445.x · Cited by 126
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Kisspeptin-GPR54 Signaling in Mouse NO-Synthesizing Neurons Participates in the Hypothalamic Control of Ovulation
Hanchate, N. K., Parkash, J., Bellefontaine, N., Mazur, D., Colledge, W. H., de Tassigny, X. D., & Prévot, V. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4765-11.2012 · Cited by 125
Excitatory Effects of the Puberty-Initiating Peptide Kisspeptin and Group I Metabotropic Glutamate Receptor Agonists Differentiate Two Distinct Subpopulations of Gonadotropin-Releasing Hormone Neurons
Dumalska, I., Wu, M., Morozova, E., Liu, R., van den Pol, A. N., & Alreja, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1225-08.2008 · Cited by 125
Possible Role of Oestrogen in Pubertal Increase of Kiss1/Kisspeptin Expression in Discrete Hypothalamic Areas of Female Rats
Takase, K., Uenoyama, Y., Inoue, N., Matsui, H., Yamada, S., Shimizu, M., Homma, T., Tomikawa, J., Kanda, S., Matsumoto, H., et al. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01868.x · Cited by 125
Direct kisspeptin-10 stimulation on luteinizing hormone secretion from bovine and porcine anterior pituitary cells
Suzuki, S., Kadokawa, H., & HASHIZUME, T. (2007) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2007.05.016 · Cited by 125
Evidence of a Role for Kisspeptin and Neurokinin B in Puberty of Female Sheep
Nestor, C. C., Briscoe, A. M. S., Davis, S. M., Valent, M., Goodman, R. L., & Hileman, S. M. (2012) · Endocrinology · doi:10.1210/en.2011-2009 · Cited by 118
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Mapping of Kisspeptin Fibres in the Brain of the Pro‐Oestrous Rat
Desroziers, E., Mikkelsen, J. D., Simonneaux, V., Keller, M., Tillet, Y., Caraty, A., & Franceschini, I. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02053.x · Cited by 116
Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain
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Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty
Clarkson, J., Han, S., Liu, X., Lee, K., & Herbison, A. E. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.01.026 · Cited by 115
Regulation of Circulating Gonadotropins by the Negative Effects of Ovarian Hormones in Mares1
Ginther, O. J., Gastal, E. L., Gastal, M. O., & Beg, M. A. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.040253 · Cited by 112
Facilitatory and inhibitory effects of electrochemical stimulation of the amygdala on the release of luteinizing hormone
Beltramino, C. A., & Taleisnik, S. (1978) · Brain Research · doi:10.1016/0006-8993(78)90437-7 · Cited by 107
BAX-Dependent and BAX-Independent Regulation of Kiss1 Neuron Development in Mice
Semaan, S. J., Murray, E. K., Poling, M. C., Dhamija, S., Forger, N. G., & Kauffman, A. S. (2010) · Endocrinology · doi:10.1210/en.2010-0783 · Cited by 107
Ultrastructural Evidence of Kisspeptin-Gonadotrophin-Releasing Hormone (GnRH) Interaction in the Median Eminence of Female Rats: Implication of Axo-Axonal Regulation of GnRH Release
Uenoyama, Y., Inoue, N., Pheng, V., Homma, T., Takase, K., Yamada, S., Ajiki, K., Ichikawa, M., Okamura, H., Maeda, K., et al. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02199.x · Cited by 106
Kisspeptin immunoreactive neurons in the equine hypothalamus
Decourt, C., Tillet, Y., Caraty, A., Franceschini, I., & Briant, C. (2008) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2008.07.008 · Cited by 105
Dual Phenotype Kisspeptin-Dopamine Neurones of the Rostral Periventricular Area of the Third Ventricle Project to Gonadotrophin-Releasing Hormone Neurones
Clarkson, J., & Herbison, A. E. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02107.x · Cited by 104
Kisspeptin neurons from mice to men: similarities and differences
Goodman, R. L., & Lehman, M. N. (2012) · Endocrinology · doi:10.1210/en.2012-1550 · Cited by 103
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Evidence That Down Regulation of Hypothalamic KiSS‐1 Expression is Involved in the Negative Feedback Action of Testosterone to Regulate Luteinising Hormone Secretion in the Adult Male Rhesus Monkey (Macaca mulatta)
Shibata, M., Friedman, R. L., Ramaswamy, S., & Plant, T. M. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01549.x · Cited by 102
Differential Regulation of Kiss1 Expression by Melatonin and Gonadal Hormones in Male and Female Syrian Hamsters
Ansel-Bollepalli, L., Bolborea, M., Bentsen, A. H., Klosen, P., Mikkelsen, J. D., & Simonneaux, V. (2010) · Journal of Biological Rhythms · doi:10.1177/0748730410361918 · Cited by 101
Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters
MASON, A., GREIVES, T., Scotti, M. L., LEVINE, J., FROMMEYER, S., Ketterson, E. D., Demas, G. E., & Kriegsfeld, L. J. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.07.004 · Cited by 98
Co‐Localisation of Kisspeptin with Galanin or Neurokinin B in Afferents to Mouse GnRH Neurones
Kalló, I., Vida, B., Deli, L., Molnár, C. S., Hrabovszky, E., Caraty, A., Ciofi, P., Coen, C. W., & Liposits, Z. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02262.x · Cited by 94
Developmental Changes in the Expression of Kisspeptin mRNA in Rat Hypothalamus
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Effects of aromatase mutation (ArKO) on the sexual differentiation of kisspeptin neuronal numbers and their activation by same versus opposite sex urinary pheromones
Bakker, J., Pierman, S., & González-Martı́nez, D. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.11.005 · Cited by 91
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Developmental and Steroidogenic Effects on the Gene Expression of RFamide Related Peptides and their Receptor in the Rat Brain and Pituitary Gland
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Reproductive Hormone-Dependent and -Independent Contributions to Developmental Changes in Kisspeptin in GnRH-Deficient Hypogonadal Mice
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Biological and Anatomical Evidence for Kisspeptin Regulation of the Hypothalamic-Pituitary-Gonadal Axis of Estrous Horse Mares
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Expression of a Functional G Protein-Coupled Receptor 54-Kisspeptin Autoregulatory System in Hypothalamic Gonadotropin-Releasing Hormone Neurons
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Morphological Evidence for Direct Interaction between Kisspeptin and Gonadotropin-Releasing Hormone Neurons at the Median Eminence of the Male Goat: An Immunoelectron Microscopic Study
Matsuyama, S., Ohkura, S., Mogi, K., Wakabayashi, Y., Mori, Y., Tsukamura, H., Maeda, K., Ichikawa, M., & Okamura, H. (2011) · Neuroendocrinology · doi:10.1159/000331576 · Cited by 74
Kisspeptin neurons co‐express met‐enkephalin and galanin in the rostral periventricular region of the female mouse hypothalamus
Porteous, R. W., Petersen, S. L., Yeo, S., Bhattarai, J. P., Ciofi, P., de Tassigny, X. D., Colledge, W. H., Caraty, A., & Herbison, A. E. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22716 · Cited by 74
Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1) mRNA in the basal hypothalamus of female rhesus monkeys.
Kim, W., Jessen, H. M., Auger, A., & Terasawa, E. (2009) · Peptides · doi:10.1016/j.peptides.2008.06.005 · Cited by 70
Electrical and Morphological Characteristics of Anteroventral Periventricular Nucleus Kisspeptin and Other Neurons in the Female Mouse
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Control of Gonadotropin Secretion in the Male during Puberty: A Decrease in Response to Steroid Inhibitory Feedback in the Absence of an Increase in Steroid-Independent Drive in the Sheep*
Olster, D. H., & Foster, D. L. (1986) · Endocrinology · doi:10.1210/endo-118-6-2225 · Cited by 70
Kisspeptin Cells in the Ovine Arcuate Nucleus Express Prolactin Receptor but not Melatonin Receptor
Li, Q., Rao, A., Pereira, A. Z., Clarke, I. J., & Smith, J. T. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02195.x · Cited by 69
Absence of Gonadotropin-Releasing Hormone 1 and Kiss1 Activation in α-Fetoprotein Knockout Mice: Prenatal Estrogens Defeminize the Potential to Show Preovulatory Luteinizing Hormone Surges
González-Martı́nez, D., Mees, C. D., Douhard, Q., Szpirer, C., & Bakker, J. (2008) · Endocrinology · doi:10.1210/en.2007-1422 · Cited by 64
Developmental Changes in Hypothalamic Kiss1 Expression during Activation of the Pulsatile Release of Luteinising Hormone in Maturing Ewe Lambs
Redmond, J. S., Báez-Sandoval, G. M., Spell, K. M., Spencer, T. E., Lents, C. A., Williams, G. L., & Amstalden, M. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02177.x · Cited by 62
Maturation of kisspeptinergic neurons coincides with puberty onset in male rats
Overgaard, A., Ansel-Bollepalli, L., Simonneaux, V., Tena‐Sempere, M., Juul, A., & Mikkelsen, J. D. (2009) · Peptides · doi:10.1016/j.peptides.2009.11.017 · Cited by 62
Ultrastructure and synaptic organization of luteinizing hormone‐releasing hormone (LHRH) neurons in the anestrous ewe
Lehman, M. N., Karsch, F. J., Robinson, J. E., & Silverman, A. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902730402 · Cited by 60
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Tonic Control of Kisspeptin Release in Prepubertal Monkeys: Implications to the Mechanism of Puberty Onset
Kurian, J. R., Keen, K. L., Guerriero, K. A., & Terasawa, E. (2012) · Endocrinology · doi:10.1210/en.2012-1221 · Cited by 57
Studies of the Localisation of Kisspeptin Within the Pituitary of the Rhesus Monkey (Macaca mulatta) and the Effect of Kisspeptin on the Release of Non‐Gonadotropic Pituitary Hormones
Ramaswamy, S., Gibbs, R. B., & Plant, T. M. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01905.x · Cited by 54
Immunocytochemical localization of kisspeptin neurons in the rat forebrain with special reference to sexual dimorphism and interaction with GnRH neurons
Xu, Z., Kaga, S., Mochiduki, A., Tsubomizu, J., Adachi, S., Sakai, T., Inoue, K., & Adachi, A. A. (2012) · Endocrine Journal · doi:10.1507/endocrj.ej11-0193 · Cited by 52
Seasonal Variation in the Gonadotropin-Releasing Hormone Response to Kisspeptin in Sheep: Possible Kisspeptin Regulation of the Kisspeptin Receptor
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Gonadotrophin‐Inhibitory Hormone: A Multifunctional Neuropeptide
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Long-Term Recordings of Networks of Immortalized GnRH Neurons Reveal Episodic Patterns of Electrical Activity
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Kisspeptin‐Immunoreactivity Changes in a Sex‐ and Hypothalamic‐Region‐Specific Manner Across Rat Postnatal Development
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Kisspeptin expression in guinea pig hypothalamus: Effects of 17β‐estradiol
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Cancer Metastasis–Suppressing Peptide Metastin Upregulates Excitatory Synaptic Transmission in Hippocampal Dentate Granule Cells
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Gonadal Steroid Induction of Kisspeptin Peptide Expression in the Rostral Periventricular Area of the Third Ventricle During Postnatal Development in the Male Mouse
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Factors that regulate KiSS1 gene expression in the hippocampus
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GnRH Perikarya in Medial Basal Hypothalamus of Pubertal Female Rhesus Macaque are Ensheathed With Glia
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Characterization of the porcine Kisspeptins receptor gene and evaluation as candidate for timing of puberty in sows
Li, S., Ren, J., Guo-qiang, Y., Guo, Y., & Huang, L. (2008) · Journal of Animal Breeding and Genetics · doi:10.1111/j.1439-0388.2008.00732.x · Cited by 29
Kiss of the Mutant Mouse: How Genetically Altered Mice Advanced Our Understanding of Kisspeptin's Role in Reproductive Physiology
Lemko, H. M. D., & Elias, C. F. (2012) · Endocrinology · doi:10.1210/en.2012-1494 · Cited by 17

Research works printed but not linked: 2

Ohkura S, Wakabayashi Y, Uenoyama Y, Steiner RA, Tsukamura H, Maeda K et al (2010) Gonadotropin-releasing hormone pulse generator activity from the arcuate nucleus kisspeptin neurons in the goat hypothalamus. Endocr J 57:S516
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Background

See all 185

Authors: Lehman, M. N., Hileman, S. M., & Goodman, R. L.
Affiliations: University of Mississippi Medical Center (US)
West Virginia University (US)
Corresponding author: Goodman, Robert L.
ORCID: Lehman, Michael N.
Hileman, Stanley M.
Goodman, Robert L.
Venue: Advances in Experimental Medicine and Biology
Publisher: Springer New York
Published: 2013
Volume: 784
Pages: 27-62
ISSN: 0065-2598 (ISSN-L)
DOI: 10.1007/978-1-4614-6199-9_3
PMC: PMC4059209
OpenAlex: W206317211
Cited by: 180
References: 138
Citations by year: 2026: 5 · 2025: 12 · 2024: 14 · 2023: 11 · 2022: 16 · 2021: 16 · 2020: 16 · 2019: 19 · 2018: 14 · 2017: 10 · 2016: 19 · 2015: 10 · 2014: 9 · 2013: 8
FWCI: 75.82
Type: book chapter
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Advances in experimental medicine and biology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD039916, R01HD033916)
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 neurons, kisspeptin receptor, arcuate nucleus, preoptic area, gonadotropin-releasing hormone, neurokinin B, dynorphin, galanin, dopamine, hypothalamus, comparative neuroanatomy
MeSH terms: Receptors, Kisspeptin-1, Animals, Arcuate Nucleus of Hypothalamus, Axons, Dynorphins, Humans, Gonadotropin-Releasing Hormone, Preoptic Area, Neurokinin B, Signal Transduction, Galanin, Third Ventricle, Receptors, G-Protein-Coupled, Kisspeptins

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Neuroanatomy of the Kisspeptin Signaling System in Mammals: Comparative and Developmental Aspects

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