The role of kisspeptin and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep

Smith, J.T.

doi:10.1016/j.domaniend.2011.11.003

Cited by 55Hypothalamic control of reproductive hormonesReproductive Physiology in LivestockNeuropeptides and Animal Physiology

The role of kisspeptin and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep

Smith, J.T.·2012·Domestic Animal Endocrinology

DOI 10.1016/j.domaniend.2011.11.003

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Abstract

Sheep are seasonal breeders, experiencing an annual period of reproductive quiescence in response to increased photoperiod during the late-winter into spring and renaissance during the late summer. The nonbreeding (anestrous) season is characterized by a reduction in the pulsatile secretion of GnRH from the brain, in part because of an increase in negative feedback activity of estrogen. Neuronal populations in the hypothalamus that produce kisspeptin and gonadotropin-inhibitory hormone (GnIH) appear to be important for the seasonal shift in reproductive activity, and the former are also mandatory for puberty onset. Kisspeptin cells in the arcuate nucleus (ARC) and preoptic area appear to regulate GnRH neurons and transmit sex-steroid feedback signals to these neurons. Moreover, kisspeptin expression in the ARC is markedly up-regulated at the onset of the breeding season, as too are the number of kisspeptin fibers in close apposition to GnRH neurons. The lower levels of kisspeptin seen during the nonbreeding season can be "corrected" by infusion of kisspeptin, which causes ovulation in seasonally acyclic females. The role of GnIH is less clear, but mounting evidence supports a role for this neuropeptide in the inhibitory regulation of both GnRH secretion and gonadotropin release from the pituitary gland. Contrary to kisspeptin, GnIH expression is markedly reduced at the onset of the breeding season. In addition, the number of GnIH fibers in close apposition to GnRH neurons also decreases during this time. Importantly, exogenous GnIH treatment can block both the pulsatile release of LH and the preovulatory LH surge during the breeding season. In summary, it is most likely the integrated function of both these neuropeptide systems that modulate the annual shift in photoperiod to a physiological change in fertility.

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In mammals, the pulsatile secretion of GnRH is reduced in the nonbreeding (anestrous) season, and the reactivation of the hypothalamic-pituitary-gonadal axis is dictated by a seasonal-dependent increase in kisspeptin expression and a concomitant reduction in Gonadotropin-inhibitory hormone (GnIH) production.
“In mammals, the pulsatile secretion of GnRH is reduced in the nonbreeding (anestrous) season, and the reactivation of the hypothalamic–pituitary–gonadal axis is dictated by a seasonal-dependent increase in kisspeptin expression and a concomitant reduction in Gonadotropin-inhibitory hormone (GnIH) production (26–28).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis (2020) · cites this paper as [28]

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Seasonal Changes in Pulsatile Luteinizing Hormone (LH) Secretion in the Ewe: Relationship of Frequency of LH Pulses to Day Length and Response to Estradiol Negative Feedback1
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Distribution of novel RFamide-related peptide-like immunoreactivity in the mouse central nervous system
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Redefining the Limits of Day Length Responsiveness in a Seasonal Mammal
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Role of the Thyroid Gland in Seasonal Reproduction. III. Thyroidectomy Blocks Seasonal Suppression of Gonadotropin-Releasing Hormone Secretion in Sheep*
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GnRH pulse frequency determines LH pulse amplitude by altering the amount of releasable LH in the pituitary glands of ewes
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Expression of Fos and in Vivo Median Eminence Release of LHRH Identifies an Active Role for Preoptic Area Kisspeptin Neurons in Synchronized Surges of LH and LHRH in the Ewe
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Administration of Kisspeptin‐54 into Discrete Regions of the Hypothalamus Potently Increases Plasma Luteinising Hormone and Testosterone in Male Adult Rats
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Neural Systems Mediating Seasonal Breeding in the Ewe
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Projections from the arcuate/ventromedial region of the hypothalamus to the preoptic area and bed nucleus of stria terminalis in the brain of the ewe; lack of direct input to gonadotropin-releasing hormone neurons
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Kisspeptin Cells in the Ovine Arcuate Nucleus Express Prolactin Receptor but not Melatonin Receptor
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Thyroxine is Permissive to Seasonal Transitions in Reproductive Neuroendocrine Activity in the Ewe1
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Hypothalamic Sites of Catecholamine Inhibition of Luteinizing Hormone in the Anestrous Ewe1
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Rat RFRP-3 Alters Hypothalamic GHRH Expression and Growth Hormone Secretion but Does Not Affect KiSS-1 Gene Expression or the Onset of Puberty in Male Rats
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Photic and Nonphotic Seasonal Cues Differentially Engage Hypothalamic Kisspeptin and RFamide‐Related Peptide mRNA Expression in Siberian Hamsters
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Evidence That the Mediobasal Hypothalamus Is the Primary Site of Action of Estradiol in Inducing the Preovulatory Gonadotropin Releasing Hormone Surge in the Ewe
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Effects of Photoperiod on Kisspeptin Neuronal Populations of the Ewe Diencephalon in Connection with Reproductive Function
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Morphological Plasticity in the Neural Circuitry Responsible for Seasonal Breeding in the Ewe
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Gonadotrophin-releasing hormone secretion (GnRH) in anoestrous ewes and the induction of GnRH surges by oestrogen
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Seasonal breeding as a neuroendocrine model for puberty in sheep
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Seasonal Variation in GnRH Response to Kisspeptin in Sheep: Possible Kisspeptin Regulation of the Kisspeptin Receptor
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Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals
Kriegsfeld, L. J., Ubuka, T., Bentley, G. E., & Tsutsui, K. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.12.001 · Cited by 117 · see citing works
The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks
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Seasonal regulation of structural plasticity and neurogenesis in the adult mammalian brain: Focus on the sheep hypothalamus
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Cellular mechanisms and integrative timing of neuroendocrine control of GnRH secretion by kisspeptin
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Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis
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Structural and Functional Divergence of Gonadotropin-Inhibitory Hormone from Jawless Fish to Mammals
Ogawa, S., & Parhar, I. S. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00177 · Cited by 61 · see citing works
Immunohistochemical characterization of the arcuate kisspeptin/neurokinin B/dynorphin (KNDy) and preoptic kisspeptin neuronal populations in the hypothalamus during the estrous cycle in heifers
Hassaneen, A. S. A., Naniwa, Y., Suetomi, Y., Matsuyama, S., Kimura, K., Ieda, N., Inoue, N., Uenoyama, Y., Tsukamura, H., Maeda, K.-I., et al. (2016) · Journal of Reproduction and Development · doi:10.1262/jrd.2016-075 · Cited by 60 · see citing works
Kisspeptin as a master player in the central control of reproduction in mammals: An overview of kisspeptin research in domestic animals
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The involvement of gonadotropin inhibitory hormone and kisspeptin in the metabolic regulation of reproduction
Wahab, F., Shahab, M., & Behr, R. (2015) · Journal of Endocrinology · doi:10.1530/joe-14-0688 · Cited by 55 · see citing works
Hypothalamic Distribution, Adenohypophyseal Receptor Expression, and Ligand Functionality of RFamide-Related Peptide 3 in the Mare During the Breeding and Nonbreeding Seasons1
Thorson, J. F., Prezotto, L. D., Cardoso, R. C., Sharpton, S. M., Edwards, J. F., Welsh, T. H., Riggs, P. K., Caraty, A., Amstalden, M., & Williams, G. L. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.112185 · Cited by 37 · see citing works
Physiology of Seasonal Breeding: A Review
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New concepts of the central control of reproduction, integrating influence of stress, metabolic state, and season
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Melatonin deprival modifies follicular and corpus luteal growth dynamics in a sheep model
Manca, M. E., Manunta, M. L., Spezzigu, A., Torres-Rovira, L., Gonzalez‐Bulnes, A., Pasciu, V., Piu, P., Leoni, G. G., Succu, S., Chesneau, D., et al. (2014) · Reproduction · doi:10.1530/rep-13-0405 · Cited by 26 · see citing works
Discontinuity in the molecular neuroendocrine response to increasing daylengths in Ile‐de‐France ewes: Is transient Dio2 induction a key feature of circannual timing?
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Transcriptomic Changes of Photoperiodic Response in the Hypothalamus Were Identified in Ovariectomized and Estradiol-Treated Sheep
He, X., Di, R., Guo, X., Cao, X., Zhou, M., Li, X., Xia, Q., Wang, X., Zhang, J., Zhang, X., et al. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.848144 · Cited by 21 · see citing works
Seasonal Changes in the Distinct Taxonomy and Function of the Gut Microbiota in the Wild Ground Squirrel (Spermophilus dauricus)
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Physiology of reproductive seasonality in sheep – an update
Pampori, Z. A., Sheikh, A. A., Aarif, O., Hasin, D., & Bhat, I. A. (2018) · Biological Rhythm Research · doi:10.1080/09291016.2018.1548112 · Cited by 20 · see citing works
Immunization against Kisspeptin-54 perturb hypothalamic–pituitary–testicular signaling pathway in ram lambs
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Leptin actions through the nitrergic system to modulate the hypothalamic expression of the kiss1 mRNA in the female rat
Petrine, J. C. P., Franci, C. R., & Borges, B. D. B. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146574 · Cited by 15 · see citing works
Melatonin treatment and male replacement every week on the reproductive performance in Sarda sheep breed
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Impact of Food Restriction on Ovarian Development, RF amide‐Related Peptide‐3 and the Hypothalamic–Pituitary–Ovarian Axis in Pre‐Pubertal Ewes
Li, H., Song, H., Huang, M., Nie, H., Wang, Z., & Wang, F. (2014) · Reproduction in Domestic Animals · doi:10.1111/rda.12375 · Cited by 13 · see citing works
Seasonal reproductive performance of crossbred ewes in intensive lamb-production systems
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Molecular cloning and epigenetic change detection of Kiss1 during seasonal reproduction in Chinese indigenous sheep
He, X., Liu, Q., Li, X., Guo, X., Wang, X., Hu, W., Di, R., & Chu, M. (2017) · Reproduction Fertility and Development · doi:10.1071/rd17028 · Cited by 11 · see citing works
Screening of Differentially Expressed Genes and miRNAs in Hypothalamus and Pituitary Gland of Sheep under Different Photoperiods
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Seasonal Changes in the Structure and Function of Gut Microbiota in the Muskrat (Ondatra zibethicus)
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Initiation of active immunization against testosterone during early puberty alters negative feedback regulation of the hypothalamic-pituitary-testicular axis in rabbits
Han, X., Cheng, W., Chen, Z. Y., Du, X., Cao, X., & Zeng, X. Y. (2014) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2014.04.001 · Cited by 10 · see citing works
Spexin mRNA profile and its response to different photoperiods in Chinese Yangzhou geese (Anas cygnoides)
Liu, J., Dai, S., Shao, X., Wei, C., Dai, Z., Yang, P., Lei, M., Chen, R., & Zhu, H. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.961431 · Cited by 8 · see citing works
Analysis on DNA sequence of goat RFRP gene and its possible association with average daily sunshine duration
Huang, D., Di, R., Wang, J., Chu, M., He, J., Cao, G., Li, F., Feng, T., & Li, N. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1789-3 · Cited by 8 · see citing works
Effect of season and frequency of embryo collections on superovulatory response and embryo recovery in Santa Inês hair sheep
Lagares, M. D. A., Varago, F. C., Moustacas, V. S., Gheller, V. A., Nicolino, R. R., Borges, I. D., & Henry, M. (2021) · Small Ruminant Research · doi:10.1016/j.smallrumres.2021.106441 · Cited by 8 · see citing works
A single intravenous injection of Kisspeptin evokes an increase in luteinising hormone in 15- and 18-week-old gilts
Ralph, C. R., Kirkwood, R. N., & Tilbrook, A. J. (2017) · Animal Production Science · doi:10.1071/anv57n12ab067 · Cited by 7 · see citing works
Effects of Sulpiride on the Reproductive System of Male Rats after Puberty
Abd, A. A., Al-Juhaishi, O. A., & Jumma, Q. S. (2025) · World s Veterinary Journal · doi:10.54203/scil.2025.wvj5 · Cited by 5 · see citing works
A novel mechanism of kisspeptin regulating ovarian granulosa cell function via down-regulating let-7b to activate ERK/PI3K-Akt pathway in Tan sheep
Dai, T., Wei, S., Li, X., Yang, D., Gui, L., Xiang, H., Ma, Y., & Dan, X. (2025) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2025.106947 · Cited by 5 · see citing works
Programmed for sex: Nutrition–reproduction relationships from an inter-generational perspective
Sharpe, R. M. (2017) · Reproduction · doi:10.1530/rep-17-0537 · Cited by 4 · see citing works
Reproductive Physiology, Genetic Architecture, and Management of Duolang Sheep Under Arid-Zone Production Systems: A Review
Shahbaz, G., Sajid, M., Sun, H., He, C., Zhu, L.-L., Li, W., Gu, R., Wang, C., 陈树鑫, & Xing, F. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27104554 · Cited by 2 · see citing works
O neuropeptídeo kisspeptina e a reprodução animal: uma revisão
Dias, J. C. O., Veloso, C. M., Donzele, R. F. M. D. O., & de Carvalho, G. R. (2018) · Multi-Science Journal · doi:10.33837/msj.v1i2.76 · Cited by 2 · see citing works
Nasal immunization with AMH-INH-RFRP DNA vaccine for improving follicle development and fertility in buffaloes
Chen, C., Zhao, X., An, Z., Ahmad, M. J., Niu, K., Zhang, X., Nie, P., Tang, J., Liang, A., & Yang, L. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1076404 · Cited by 2 · see citing works
Seasonal Breeding Alters Fecal Microbiota and Metabolome in the Male Captive Yangtze Finless Porpoise ( Neophocaena asiaeorientalis asiaeorientalis )
Shah, S. A. U. R., Tang, B., He, D., Ahmad, M., Nabi, G., Wang, C., Kou, Z., Wang, K., & Hao, Y. (2025) · Ecology and Evolution · doi:10.1002/ece3.71611 · Cited by 2 · see citing works
A influência do fotoperíodo na reprodução do macho caprino e ovino
Dias, J. C. O., & Veloso, C. M. (2020) · Research Society and Development · doi:10.33448/rsd-v9i10.8243 · Cited by 2 · see citing works
Effects of Age Category and eCG Dose on Reproductive Performance in Ile-de-France Ewe Lambs and Adult Ewes Under Seasonal-Transition Field Conditions
Çiftçi, M. F., & Satılmış, F. (2026) · Veterinary Sciences · doi:10.3390/vetsci13090992 · Cited by 1 · see citing works
Hypothalamic-pituitary-gonadal axis response to photoperiod changes in female guanacos (Lama guanicoe)
Correa, L. M., Moreno, R. D., & Riveros, J. L. (2023) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2023.114427 · Cited by 1 · see citing works
A sazonalidade na reprodução dos mamíferos: uma revisão
Dias, J. C. O., & Veloso, C. M. (2020) · Research Society and Development · doi:10.33448/rsd-v9i10.8236 · Cited by 1 · see citing works
Characterizing the relationship between gonadotropin releasing hormone (GnRH), kisspeptin, and RFamide related peptide 3 (RFRP-3) neurons in the equine hypothalamus across the estrous cycle and in the anovulatory seasons
McGrath, B. M., Norman, S. T., Gaspardis, C., Rose, J. L., & Scott, C. (2024) · Theriogenology · doi:10.1016/j.theriogenology.2024.02.027 · Cited by 1 · see citing works
Avaliação reprodutiva de ovelhas da raça Texel submetidas a diferentes protocolos de indução de estro na contraestação reprodutiva
Rocha, M. S. (2014) · doi:10.11606/d.10.2014.tde-11042014-114526
Effects of gestational heat stress on the lactational performance of gilts and growth performance and carcass characteristics of second-generation offspring
Wiegert, J. (2016) · VTechWorks (Virginia Tech)
The Affect of Breeding Season of Iraqi Sheep in Relation to Number, Quality and Maturity Index of abattoir Ovarian Oocytes
Saleh, W. M., & Hatif, S. A. (2019) · doi:10.24897/acn.64.68.6014
Resposta folicular e taxa de prenhez de novilhas Nelore pré-púberes tratadas com Kisspeptina ou GnRH no momento da IATF
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Abstracts from the 16th Biennial Conference of APSA
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ФОТОПЕРИОДИЧЕСКАЯ РЕГУЛЯЦИЯ РЕПРОДУКТИВНОГО СТАТУСА: НЕЙРОЭНДОКРИННЫЙ КОНТРОЛЬ СЕЗОННОГО РАЗМНОЖЕНИЯ И ФИЗИОЛОГИЧЕСКИЕ ФУНКЦИИ МЕЛАТОНИНА (обзор)
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The role of kisspeptin and gonadotropin inhibitory hormone (GnIH) in the seasonality of reproduction in sheep
Clarke, I. J., & Smith, J. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.7.012
Self-citation
Kisspeptin and seasonality in sheep
Clarke, I. J., Smith, J. T., Caraty, A., Goodman, R. L., & Lehman, M. N. (2009) · Peptides · doi:10.1016/j.peptides.2008.08.022 · Cited by 96 · see citing works
Self-citation
Kisspeptin-10 stimulates luteinising hormone release from the ovine pituitary gland in vitro
Smith, J. T., Pereira, A., Rao, A., & Clarke, I. J. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.03.162 · Cited by 2 · see citing works
Self-citation
The role of kisspeptin in reproductive function in the ewe
Smith, J. T., Hawken, P. A., Lehman, M. N., & Martin, G. B. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.8.008 · Cited by 8 · see citing works
Self-citation
Variation in Kisspeptin and RFamide-Related Peptide (RFRP) Expression and Terminal Connections to Gonadotropin-Releasing Hormone Neurons in the Brain: A Novel Medium for Seasonal Breeding in the Sheep
Smith, J. T., Coolen, L. M., Kriegsfeld, L. J., Sari, I. P., Jaafarzadehshirazi, M. R., Maltby, M., Bateman, K., Goodman, R. L., Tilbrook, A. J., Ubuka, T., et al. (2008) · Endocrinology · doi:10.1210/en.2008-0581 · Cited by 387 · see citing works
Self-citation

Authors: Smith, J. T.
Affiliations: Monash University (AU)
Corresponding author: Smith, J.T.
Venue: Domestic Animal Endocrinology
Publisher: Elsevier BV
Published: 2012-08
Volume: 43
Issue: 2
Pages: 75-84
ISSN: 0739-7240 (ISSN-L)
DOI: 10.1016/j.domaniend.2011.11.003
OpenAlex: W2026247947
Cited by: 55
References: 94
Citations by year: 2026: 3 · 2025: 4 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 2 · 2020: 5 · 2019: 5 · 2018: 3 · 2017: 6 · 2016: 3 · 2015: 2 · 2014: 8 · 2013: 3 · 2012: 1
FWCI: 0.61
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Domestic Animal Endocrinology (publishedVersion)
PubMed (publishedVersion)
UWA Profiles and Research Repository (UWA) (submittedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: kisspeptin, gonadotropin-inhibitory hormone, seasonal reproduction, sheep, anestrus, photoperiod, GnRH neurons, hypothalamus, arcuate nucleus, preoptic area, puberty onset, estrogen negative feedback, luteinizing hormone surge, ovulation, reproductive quiescence
MeSH terms: Animals, Breeding, Female, Gonadotropins, Pituitary, Hormone Antagonists, Hypothalamus, Luteinizing Hormone, Gonadotropin-Releasing Hormone, Neuropeptides, Pituitary Gland, Reproduction, Seasons, Sheep, Photoperiod, Feedback, Physiological, Kisspeptins

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The role of kisspeptin and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep

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