A "Timed" Kiss Is Essential for Reproduction: Lessons from Mammalian Studies

Putteeraj, Manish; Soga, Tomoko; Ubuka, Takayoshi; Parhar, Ishwar S.

doi:10.3389/fendo.2016.00121

Cited by 28Hypothalamic control of reproductive hormonesCircadian rhythm and melatoninNeuroendocrine regulation and behavior

A "Timed" Kiss Is Essential for Reproduction: Lessons from Mammalian Studies

Open access

Putteeraj, Manish, Soga, Tomoko, Ubuka, Takayoshi, Parhar, Ishwar S.·2016·Frontiers in Endocrinology

DOI 10.3389/fendo.2016.00121PMC PMC5005330

Open this paper in CoChat — free account Open PDF

Abstract

Reproduction is associated with the circadian system, primarily as a result of the connectivity between the biological clock in the suprachiasmatic nucleus (SCN) and reproduction-regulating brain regions, such as preoptic area (POA), anteroventral periventricular nucleus (AVPV), and arcuate nucleus (ARC). Networking of the central pacemaker to these hypothalamic brain regions is partly represented by close fiber appositions to specialized neurons, such as kisspeptin and gonadotropin-releasing hormone (GnRH) neurons; accounting for rhythmic release of gonadotropins and sex steroids. Numerous studies have attempted to dissect the neurochemical properties of GnRH neurons, which possess intrinsic oscillatory features through the presence of clock genes to regulate the pulsatile and circadian secretion. However, less attention has been given to kisspeptin, the upstream regulator of GnRH and a potent mediator of reproductive functions including puberty. Kisspeptin exerts its stimulatory effects on GnRH secretion via its cognate Kiss-1R receptor that is co-expressed on GnRH neurons. Emerging studies have found that kisspeptin neurons oscillate on a circadian basis and that these neurons also express clock genes that are thought to regulate its rhythmic activities. Based on the fiber networks between the SCN and reproductive nuclei such as the POA, AVPV, and ARC, it is suggested that interactions among the central biological clock and reproductive neurons ensure optimal reproductive functionality. Within this neuronal circuitry, kisspeptin neuronal system is likely to "time" reproduction in a long term during development and aging, in a medium term to regulate circadian or estrus cycle, and in a short term to regulate pulsatile GnRH secretion.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.3389/fendo.2016.00121

Cites

139 of 140 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The LH surge is inhibited by GABA.
“Different data converge to indicate that the LH surge is stimulated by glutamate [102,103] and inhibited by GABA [104,105]”
From Fibromyalgia pathogenesis explained by a neuroendocrine multistable model (2024) · cites this paper as [105]
The Introduction’s Figure 1 caption identifies GABA as inhibitory to AVPV kisspeptin neurons, which the same section links to positive feedback on the GnRH/LH surge. It does not state that GABA inhibits the LH surge itself; the claim presents an indirect pathway as a direct effect. (LLM, conf=0.82)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The GPR54 Gene as a Regulator of Puberty
Seminara, S. B., Messager, S., Chatzidaki, E. E., Thresher, R. R., Acierno, J. S., Shagoury, J. K., Bo-Abbas, Y., Kuohung, W., Schwinof, K. M., Hendrick, A. G., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa035322 · Cited by 2,557 · see citing works
Coordinated Transcription of Key Pathways in the Mouse by the Circadian Clock
Panda, S., Antoch, M. P., Miller, B. H., Su, A. I., Schook, A. C., Straume, M., Schultz, P. G., Kay, S. A., Takahashi, J. S., & Hogenesch, J. B. (2002) · Cell · doi:10.1016/s0092-8674(02)00722-5 · Cited by 2,272 · see citing works
A Serum Shock Induces Circadian Gene Expression in Mammalian Tissue Culture Cells
Balsalobre, A., Damiola, F., & Schibler, U. (1998) · Cell · doi:10.1016/s0092-8674(00)81199-x · Cited by 2,001 · see citing works
The Metastasis Suppressor Gene KiSS-1 Encodes Kisspeptins, the Natural Ligands of the Orphan G Protein-coupled Receptor GPR54
Kotani, M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden, J.-M., Le Poul, E., Brézillon, S., Tyldesley, R., Suarez-Huerta, N., Vandeput, F., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104847200 · Cited by 1,546 · see citing works
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 · see citing works
Dynamics of gonadotropin-releasing hormone release during a pulse.
Moenter, S. M., Brand, R. M., MIDGLEY, A. R., & Karsch, F. J. (1992) · Endocrinology · doi:10.1210/endo.130.1.1727719 · Cited by 1,257 · see citing works
Suprachiasmatic Nucleus: Cell Autonomy and Network Properties
Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135919 · Cited by 1,216 · see citing works
Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54
Messager, S., Chatzidaki, E. E., Ma, D., Hendrick, A. G., Zahn, D., Dixon, J., Thresher, R. R., Malinge, I., Lomet, D., Carlton, M. B. L., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409330102 · Cited by 1,215 · see citing works
Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock
Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., & Antoch, M. P. (2006) · Genes & Development · doi:10.1101/gad.1432206 · Cited by 1,188 · see citing works
A role for kisspeptins in the regulation of gonadotropin secretion in the mouse
Gottsch, M. L., Cunningham, M. J., Smith, J. T., Popa, S. M., Acohido, B. V., Crowley, W. F., Seminara, S., Clifton, D. K., & Steiner, R. A. (2004) · Endocrinology · doi:10.1210/en.2004-0431 · Cited by 1,161 · see citing works
Physiology of Circadian Entrainment
Golombek, D. A., & Rosenstein, R. E. (2010) · Physiological Reviews · doi:10.1152/physrev.00009.2009 · Cited by 1,103 · see citing works
Regulation of Kiss1 gene expression in the brain of the female mouse
Smith, J. T., Cunningham, M. J., Rissman, E. F., Clifton, D. K., & Steiner, R. A. (2005) · Endocrinology · doi:10.1210/en.2005-0488 · Cited by 1,102 · see citing works
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 · see citing works
Kisspeptin Activation of Gonadotropin Releasing Hormone Neurons and Regulation of KiSS-1 mRNA in the Male Rat
Irwig, M. S., Fraley, G. S., Smith, J. T., Acohido, B. V., Popa, S. M., Cunningham, M. J., Gottsch, M. L., Clifton, D. K., & Steiner, R. A. (2004) · Neuroendocrinology · doi:10.1159/000083140 · Cited by 913 · see citing works
Postnatal Development of Kisspeptin Neurons in Mouse Hypothalamus; Sexual Dimorphism and Projections to Gonadotropin-Releasing Hormone Neurons
Clarkson, J., & Herbison, A. E. (2006) · Endocrinology · doi:10.1210/en.2006-0787 · Cited by 875 · see citing works
Kisspeptin Signaling in the Brain
Oakley, A. E., Clifton, D. K., & Steiner, R. A. (2009) · Endocrine Reviews · doi:10.1210/er.2009-0005 · Cited by 842 · see citing works
Loss of Circadian Rhythmicity in Blood Testosterone Levels with Aging in Normal Men*
Bremner, W. J., Vitiello, M. V., & Prinz, P. N. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1278 · Cited by 785 · see citing works
Wired for Reproduction: Organization and Development of Sexually Dimorphic Circuits in the Mammalian Forebrain
Simerly, R. B. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142745 · Cited by 723 · see citing works
Differential Regulation of KiSS-1 mRNA Expression by Sex Steroids in the Brain of the Male Mouse
Smith, J. T., Lemko, H. M. D., Stoll, E. A., Gottsch, M. L., Braun, R. E., Eacker, S. M., Clifton, D. K., & Steiner, R. A. (2005) · Endocrinology · doi:10.1210/en.2005-0323 · Cited by 694 · see citing works
Multimodal Influence of Estrogen upon Gonadotropin-Releasing Hormone Neurons
Herbison, A. E. (1998) · Endocrine Reviews · doi:10.1210/edrv.19.3.0332 · Cited by 618 · see citing works
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
Wakabayashi, Y., Nakada, T., Murata, K., Ohkura, S., Mogi, K., Navarro, V. M., Clifton, D. K., Mori, Y., Tsukamura, H., Maeda, K.-I., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5848-09.2010 · Cited by 597 · cited 1× · see citing works
“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
Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene
de Tassigny, X. D., Fagg, L. A., Dixon, J. P. C., Day, K. A., Leitch, H. G., Hendrick, A. G., Zahn, D., Franceschini, I., Caraty, A., Carlton, M. B. L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704114104 · Cited by 597 · see citing works
Kiss1 Neurons in the Forebrain as Central Processors for Generating the Preovulatory Luteinizing Hormone Surge
Smith, J. T., Popa, S. M., Clifton, D. K., Hoffman, G. E., & Steiner, R. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1618-06.2006 · Cited by 588 · see citing works
Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals
Kriegsfeld, L. J., Mei, D. F., Bentley, G. E., Ubuka, T., Mason, A. O., Inoue, K., Ukena, K., Tsutsui, K., & Silver, R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511003103 · Cited by 552 · see citing works
Self-citation
Metabolism and cancer: the circadian clock connection
Sahar, S., & Sassone-Corsi, P. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2747 · Cited by 551 · see citing works
Suprachiasmatic nucleus organization
Moore, R. Y., Speh, J. C., & Leak, R. K. (2002) · Cell and Tissue Research · doi:10.1007/s00441-002-0575-2 · Cited by 547 · see citing works
Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity
Bendová, Z., Cermakian, N., Reppert, S. M., & Sassone‐Corsi, P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.102075599 · Cited by 543 · see citing works
Kiss1 −/− Mice Exhibit More Variable Hypogonadism than Gpr54−/− Mice
Lapatto, R., Pallais, J. C., Zhang, D., Chan, Y.-M., Mahan, A., Cerrato, F. E., Le, W. W., Hoffman, G. E., & Seminara, S. B. (2007) · Endocrinology · doi:10.1210/en.2007-0078 · Cited by 533 · see citing works
Discovery of a receptor related to the galanin receptors
Lee, D. K., Nguyen, T., O’Neill, G. P., Cheng, R., Liu, Y., Howard, A. D., Coulombe, N., Tan, C. P., Tang-Nguyen, A.-T., George, S. R., et al. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00009-5 · Cited by 502 · see citing works
Sexual Differentiation of Kiss1 Gene Expression in the Brain of the Rat
Kauffman, A. S., Gottsch, M. L., Roa, J., Byquist, A. C., Crown, A., Clifton, D. K., Hoffman, G. E., Steiner, R. A., & Tena‐Sempere, M. (2007) · Endocrinology · doi:10.1210/en.2006-1540 · Cited by 493 · see citing works
Pituitary stalk portal blood collection in rhesus monkeys: evidence for pulsatile release of gonadotropin-releasing hormone (GnRH)
CARMEL, P. W., ARAKI, S., & FERIN, M. (1976) · Endocrinology · doi:10.1210/endo-99-1-243 · Cited by 482 · see citing works
Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats
Kirby, E. D., Geraghty, A. C., Ubuka, T., Bentley, G. E., & Kaufer, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901176106 · Cited by 379 · see citing works
Self-citation
Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts
Bilban, M., Ghaffari‐Tabrizi‐Wizsy, N., Hintermann, E., Bauer, S., Molzer, S., Zoratti, C., Malli, R., Sharabi, A. B., Hiden, U., Graier, W. F., et al. (2004) · Journal of Cell Science · doi:10.1242/jcs.00971 · Cited by 379 · see citing works
Circadian Clock Mutation Disrupts Estrous Cyclicity and Maintenance of Pregnancy
Miller, B. H., Olson, S. L., Turek, F. W., Levine, J. E., Horton, T. H., & Takahashi, J. S. (2004) · Current Biology · doi:10.1016/j.cub.2004.07.055 · Cited by 377 · see citing works
The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors
Schmutz, I., Ripperger, J. A., Baeriswyl-Aebischer, S., & Albrecht, U. (2010) · Genes & Development · doi:10.1101/gad.564110 · Cited by 361 · see citing works
Laser-Captured Single Digoxigenin-Labeled Neurons of Gonadotropin-Releasing Hormone Types Reveal a Novel G Protein-Coupled Receptor (Gpr54) during Maturation in Cichlid Fish
Parhar, I. S., Ogawa, S., & Sakuma, Y. (2004) · Endocrinology · doi:10.1210/en.2004-0395 · Cited by 321 · see citing works
Self-citation
Distribution and Postnatal Development of Gpr54 Gene Expression in Mouse Brain and Gonadotropin-Releasing Hormone Neurons
Herbison, A. E., de Tassigny, X. D., Doran, J., & Colledge, W. H. (2009) · Endocrinology · doi:10.1210/en.2009-0552 · Cited by 316 · see citing works
The Kisspeptin/Neurokinin B/Dynorphin (KNDy) Cell Population of the Arcuate Nucleus: Sex Differences and Effects of Prenatal Testosterone in Sheep
Cheng, G., Coolen, L. M., Padmanabhan, V., Goodman, R. L., & Lehman, M. N. (2009) · Endocrinology · doi:10.1210/en.2009-0541 · Cited by 304 · see citing works
The suprachiasmatic nucleus and the circadian time-keeping system revisited
van Esseveldt, L. E., Lehman, M. N., & Boer, G. J. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00025-4 · Cited by 296 · see citing works
RFamide-Related Peptide-3, a Mammalian Gonadotropin-Inhibitory Hormone Ortholog, Regulates Gonadotropin-Releasing Hormone Neuron Firing in the Mouse
Ducret, E., Anderson, G. M., & Herbison, A. E. (2009) · Endocrinology · doi:10.1210/en.2008-1623 · Cited by 295 · see citing works
Regulation of BMAL1 Protein Stability and Circadian Function by GSK3β-Mediated Phosphorylation
Sahar, S., Zocchi, L., Kinoshita, C., Borrelli, E., & Sassone‐Corsi, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008561 · Cited by 291 · see citing works
The Circadian Clock Protein BMAL1 Is Necessary for Fertility and Proper Testosterone Production in Mice
Alvarez, J. D., Hansen, A. G., Ord, T. S., Bębas, P., Chappell, P. E., Giebultowicz, J. M., Williams, C. J., Moss, S., & Sehgal, A. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730407311254 · Cited by 285 · see citing works
Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus
Burke, M. C., Letts, P. A., Krajewski, S. J., & Rance, N. E. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.21086 · Cited by 280 · see citing works
Identification, Expression, and Physiological Functions of Siberian Hamster Gonadotropin-Inhibitory Hormone
Ubuka, T., Inoue, K., Fukuda, Y., Mizuno, T., Ukena, K., Kriegsfeld, L. J., & Tsutsui, K. (2011) · Endocrinology · doi:10.1210/en.2011-1110 · Cited by 279 · see citing works
Self-citation
Nucleocytoplasmic shuttling and mCRY‐dependent inhibition of ubiquitylation of the mPER2 clock protein
Yagita, K., Tamanini, F., Yasuda, M., Hoeijmakers, J. H. J., van der Horst, G. T. J., & Okamura, H. (2002) · The EMBO Journal · doi:10.1093/emboj/21.6.1301 · Cited by 271 · 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
Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling
Smith, J. T., Clifton, D. K., & Steiner, R. A. (2006) · Reproduction · doi:10.1530/rep.1.00368 · Cited by 254 · see citing works
Postnatal Development of an Estradiol-Kisspeptin Positive Feedback Mechanism Implicated in Puberty Onset
Clarkson, J., Boon, W. C., Simpson, E. R., & Herbison, A. E. (2009) · Endocrinology · doi:10.1210/en.2008-1733 · Cited by 232 · see citing works
The Role of Kisspeptin–GPR54 Signaling in the Tonic Regulation and Surge Release of Gonadotropin-Releasing Hormone/Luteinizing Hormone
Lemko, H. M. D., Gottsch, M. L., Zeng, H., Gragerov, A., Bergmann, J. E., Vassilatis, D. K., Clifton, D. K., & Steiner, R. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2748-07.2007 · Cited by 220 · see citing works
Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity
Christian, C. A., Mobley, J. L., & Moenter, S. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504270102 · Cited by 218 · see citing works
Progress in Brain Research
(1976) · Progress in brain research · doi:10.1016/s0079-6123(08)60974-7 · Cited by 213 · see citing works
Alterations in RFamide-Related Peptide Expression Are Coordinated with the Preovulatory Luteinizing Hormone Surge
Gibson, E. M., Humber, S. A., Jain, S., Williams, W. P., Zhao, S., Bentley, G. E., Tsutsui, K., & Kriegsfeld, L. J. (2008) · Endocrinology · doi:10.1210/en.2008-0316 · Cited by 212 · see citing works
Abnormalities in reproductive function associated with the destruction of the suprachiasmatic nuclei in female rats
Brown-Grant, K., & Raisman, G. (1977) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1977.0098 · Cited by 208 · see citing works
Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function
Ottem, E. N., Godwin, J. G., Krishnan, S., & Petersen, S. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2267-04.2004 · Cited by 201 · see citing works
Regulation of Kiss1 and Dynorphin Gene Expression in the Murine Brain by Classical and Nonclassical Estrogen Receptor Pathways
Gottsch, M. L., Navarro, V. M., Zhao, Z., Glidewell-Kenney, C., Weiss, J., Jameson, J. L., Clifton, D. K., Levine, J. E., & Steiner, R. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0763-09.2009 · Cited by 195 · see citing works
Kisspeptin Signalling in the Hypothalamic Arcuate Nucleus Regulates GnRH Pulse Generator Frequency in the Rat
Li, X., Kinsey‐Jones, J. S., Cheng, Y., Knox, A. M. I., Lin, Y., Petrou, N. A., Roseweir, A. K., Lightman, S. L., Milligan, S. R., Millar, R. P., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008334 · Cited by 194 · see citing works
Circadian Regulation of Kiss1 Neurons: Implications for Timing the Preovulatory Gonadotropin-Releasing Hormone/Luteinizing Hormone Surge
Robertson, J. L., Clifton, D. K., de la Iglesia, H. O., Steiner, R. A., & Kauffman, A. S. (2009) · Endocrinology · doi:10.1210/en.2009-0247 · Cited by 189 · see citing works
Stimulatory Effect of RFRP-3 on the Gonadotrophic Axis in the Male Syrian Hamster: The Exception Proves the Rule
Ancel, C., Overgaard, A., Sébert, M., Tena‐Sempere, M., Mikkelsen, J. D., & Simonneaux, V. (2012) · Endocrinology · doi:10.1210/en.2011-1622 · Cited by 181 · see citing works
Circadian Control of Kisspeptin and a Gated GnRH Response Mediate the Preovulatory Luteinizing Hormone Surge
Williams, W. P., Jarjisian, S. G., Mikkelsen, J. D., & Kriegsfeld, L. J. (2011) · Endocrinology · doi:10.1210/en.2010-0943 · Cited by 181 · see citing works
Developmental and reproductive performance in circadian mutant mice
Dolatshad, H., Campbell, E. A., O’Hara, L., Maywood, E. S., Hastings, M. H., & Johnson, M. H. (2005) · Human Reproduction · doi:10.1093/humrep/dei313 · Cited by 176 · see citing works
RFamide-Related Peptide-3 Receptor Gene Expression in GnRH and Kisspeptin Neurons and GnRH-Dependent Mechanism of Action
Rizwan, M. Z., Poling, M. C., Corr, M., Cornes, P. A., Augustine, R. A., Quennell, J. H., Kauffman, A. S., & Anderson, G. M. (2012) · Endocrinology · doi:10.1210/en.2012-1133 · Cited by 172 · see citing works
Lesions of the Suprachiasmatic Nucleus Indicate the Presence of a Direct Vasoactive Intestinal Polypeptide‐Containing Projection to Gonadotrophin‐Releasing Hormone Neurons in the Female Rat
van der Beek, E. M., Wiegant, V. M., van der Donk, H. A., van den Hurk, R., & Buijs, R. M. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00373.x · Cited by 172 · see citing works
Circadian Gene Expression Regulates Pulsatile Gonadotropin-Releasing Hormone (GnRH) Secretory Patterns in the Hypothalamic GnRH-Secreting GT1-7 Cell Line
Chappell, P. E., White, R. S., & Mellon, P. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11202.2003 · Cited by 168 · see citing works
The Mammalian GnRH Gene and Its Pivotal Role in Reproduction
Seeburg, P. H., Mason, A. J., Stewart, T. A., & Nikolics, K. (1987) · Elsevier eBooks · doi:10.1016/b978-0-12-571143-2.50008-3 · Cited by 167 · see citing works
Positive, But Not Negative Feedback Actions of Estradiol in Adult Female Mice Require Estrogen Receptor α in Kisspeptin Neurons
Dubois, S. L., Acosta‐Martínez, M., DeJoseph, M. R., Wolfe, A., Radovick, S., Boehm, U., Urban, J. H., & Levine, J. E. (2014) · Endocrinology · doi:10.1210/en.2014-1851 · Cited by 167 · see citing works
Impaired Steroidogenesis and Implantation Failure in Bmal1−/− Mice
Ratajczak, C. K., Boehle, K. L., & Muglia, L. J. (2008) · Endocrinology · doi:10.1210/en.2008-1021 · Cited by 162 · see citing works
Diurnal Testosterone Levels in Peripheral Plasma of Human Male Subjects
Resko, J. A., & Eik‐Nes, K. B. (1966) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-26-5-573 · Cited by 160 · see citing works
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 · see citing works
Vasopressin induces a luteinizing hormone surge in ovariectomized, estradiol-treated rats with lesions of the suprachiasmatic nucleus
Palm, I. F., van der Beek, E. M., Wiegant, V. M., Buijs, R. M., & Kalsbeek, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00106-2 · Cited by 159 · see citing works
The association of testosterone, sleep, and sexual function in men and women
Andersen, M. L., Alvarenga, T. A., Mazaro‐Costa, R., Hachul, H., & Tufik, S. (2011) · Brain Research · doi:10.1016/j.brainres.2011.07.060 · Cited by 156 · see citing works
Gonadal- and Sex-Chromosome-Dependent Sex Differences in the Circadian System
Kuljis, D. A., Loh, D. H., Truong, D. A., Vosko, A. M., Ong, M. L., McClusky, R., Arnold, A. P., & Colwell, C. S. (2013) · Endocrinology · doi:10.1210/en.2012-1921 · Cited by 151 · see citing works
Central Circadian Control of Female Reproductive Function
Miller, B. H., & Takahashi, J. S. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00195 · Cited by 151 · see citing works
Epigenetic regulation of Kiss1 gene expression mediating estrogen-positive feedback action in the mouse brain
Tomikawa, J., Uenoyama, Y., Ozawa, M., Fukanuma, T., Takase, K., Goto, T., Abe, H., Ieda, N., Minabe, S., Deura, C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114245109 · Cited by 150 · see citing works
Interactivating Feedback Loops within the Mammalian Clock: BMAL1 Is Negatively Autoregulated and Upregulated by CRY1, CRY2, and PER2
Yu, W., Nomura, M., & Ikeda, M. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.6300 · Cited by 149 · see citing works
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 139 · see citing works
Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): An anterograde and retrograde analysis
Kriegsfeld, L. J., Leak, R. K., Yackulic, C. B., LeSauter, J., & Silver, R. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10995 · Cited by 137 · see citing works
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 · see citing works
The role of circadian rhythmicity in reproduction
Kennaway, D. J. (2005) · Human Reproduction Update · doi:10.1093/humupd/dmh054 · Cited by 120 · see citing works
Changes in sleep-wakefulness in female rats during circadian and estrous cycles
Colvin, G. B., Whitmoyer, D. I., Lisk, R. D., Walter, D. O., & Sawyer, C. H. (1968) · Brain Research · doi:10.1016/0006-8993(68)90095-4 · Cited by 119 · see citing works
Vasopressin Regulation of the Proestrous Luteinizing Hormone Surge in Wild-Type and Clock Mutant Mice1
Miller, B. H., Olson, S. L., Levine, J. E., Turek, F. W., Horton, T. H., & Takahashi, J. S. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.106.052845 · Cited by 117 · see citing works
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 · see citing works
Disrupted Kisspeptin Signaling in GnRH Neurons Leads to Hypogonadotrophic Hypogonadism
Novaira, H. J., Sonko, M. L., Hoffman, G. E., Koo, Y., Ko, C. J., Wolfe, A., & Radovick, S. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1319 · Cited by 113 · see citing works
Low reproductive success in Per1 and Per2 mutant mouse females due to accelerated ageing?
Pilorz, V., & Steinlechner, S. (2008) · Reproduction · doi:10.1530/rep-07-0434 · Cited by 113 · see citing works
Kisspeptin Neurones do not Directly Signal to RFRP ‐3 Neurones but RFRP ‐3 may Directly Modulate a Subset of Hypothalamic Kisspeptin Cells in Mice
Poling, M. C., Quennell, J. H., Anderson, G. M., & Kauffman, A. S. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12084 · Cited by 112 · see citing works
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 · see citing works
Age-related changes in dopamine, LHRH and somatostatin in the rat hypothalamus☆
HOFFMAN, G., & SLADEKJR, J. (1980) · Neurobiology of Aging · doi:10.1016/0197-4580(80)90021-4 · Cited by 102 · see citing works
Vasoactive Intestinal Polypeptide Can Excite Gonadotropin-Releasing Hormone Neurons in a Manner Dependent on Estradiol and Gated by Time of Day
Christian, C. A., & Moenter, S. M. (2008) · Endocrinology · doi:10.1210/en.2007-1098 · Cited by 101 · see citing works
Molecular Basis for the Activation of Gonadotropin-Inhibitory Hormone Gene Transcription by Corticosterone
Son, Y. L., Ubuka, T., Narihiro, M., Fukuda, Y., Hasunuma, I., Yamamoto, K., Belsham, D. D., & Tsutsui, K. (2014) · Endocrinology · doi:10.1210/en.2013-2076 · Cited by 99 · see citing works
Self-citation
The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent
Palm, I. F., van der Beek, E. M., Wiegant, V. M., Buijs, R. M., & Kalsbeek, A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02309-5 · Cited by 97 · see citing works
Structural and Functional Analyses of PAS Domain Interactions of the Clock Proteins Drosophila PERIOD and Mouse PERIOD2
Hennig, S., Strauss, H. M., Vanselow, K., Yıldız, Ö., Schulze, S., Arens, J., Kramer, A., & Wolf, E. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000094 · Cited by 97 · see citing works
Kisspeptins and RFRP-3 Act in Concert to Synchronize Rodent Reproduction with Seasons
Simonneaux, V., Ancel, C., Poirel, V., & Gauer, F. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00022 · Cited by 96 · see citing works
PUBERTY-RELATED INCREASE IN EPISODIC LHRH RELEASE FROM RAT HYPOTHALAMUSIN VITRO1
Bourguignon, J.-P., & Franchimont, P. (1984) · Endocrinology · doi:10.1210/endo-114-5-1941 · Cited by 95 · see citing works
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 · see citing works
Localization of the VIP2Receptor Protein on GnRH Neurons in the Female Rat
Smith, M. J., Jennes, L., & Wise, P. M. (2000) · Endocrinology · doi:10.1210/endo.141.11.7876 · Cited by 90 · see citing works
Gonadotropin-releasing hormone and the control of gonadotrope function
Counis, R., Laverrière, J., Garrel, G., Bleux, C., Cohen-Tannoudji, J., Lerrant, Y., Kottler, M., & Magre, S. (2005) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:2005017 · Cited by 90 · see citing works
Molecular, cellular, morphological, physiological and behavioral aspects of gonadotropin-inhibitory hormone
Ubuka, T., Son, Y. L., & Tsutsui, K. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.009 · Cited by 87 · see citing works
Self-citation
Shift in Kiss1 cell activity requires estrogen receptor α
Frazão, R., Cravo, R. M., Donato, J., Ratra, D. V., Clegg, D., Elmquist, J., Zigman, J., Williams, K. W., & Elias, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1610-12.2013 · Cited by 84 · see citing works
Expression of Circadian Rhythm Genes in Gonadotropin-Releasing Hormone-Secreting GT1-7 Neurons
Gillespie, J. M. A., Chan, B. P. K., Roy, D., Cai, F., & Belsham, D. D. (2003) · Endocrinology · doi:10.1210/en.2003-0802 · Cited by 80 · see citing works
Estradiol Down-Regulates RF-Amide-Related Peptide (RFRP) Expression in the Mouse Hypothalamus
Molnár, C. S., Kalló, I., Liposits, Z., & Hrabovszky, E. (2011) · Endocrinology · doi:10.1210/en.2010-1418 · Cited by 80 · see citing works
Reproductive Hormone-Dependent and -Independent Contributions to Developmental Changes in Kisspeptin in GnRH-Deficient Hypogonadal Mice
Gill, J. C., Wang, O., Kakar, S., Martinelli, E., Carroll, R. S., & Kaiser, U. B. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011911 · Cited by 79 · see citing works
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
The Dorsomedial Suprachiasmatic Nucleus Times Circadian Expression of Kiss1 and the Luteinizing Hormone Surge
Smarr, B. L., Morris, E. L., & de la Iglesia, H. O. (2012) · Endocrinology · doi:10.1210/en.2011-1857 · Cited by 75 · see citing works
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 · see citing works
Unwinding the differences of the mammalian PERIOD clock proteins from crystal structure to cellular function
Kucera, N., Schmalen, I., Hennig, S., Öllinger, R., Strauss, H. M., Grudziecki, A., Wieczorek, C. M., Kramer, A., & Wolf, E. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113280109 · Cited by 74 · see citing works
Gonadotropin‐Releasing Hormone Exhibits Circadian Rhythm in Phase with Arginine‐Vasopressin in Co‐Cultures of the Female Rat Preoptic Area and Suprachiasmatic Nucleus
Funabashi, T., Shinohara, K., Mitsushima, D., & Kimura, F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00481.x · Cited by 72 · see citing works
Developmental aspect of the gonadotropin-releasing hormone system
Tobet, S. A., Bless, E. P., & Schwarting, G. A. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00616-5 · Cited by 72 · see citing works
KiSS-1 and GPR54 at the pituitary level: Overview and recent insights
Richard, N., Corvaisier, S., Camacho, E., & Kottler, M. (2008) · Peptides · doi:10.1016/j.peptides.2008.09.015 · Cited by 72 · see citing works
Electrical and Morphological Characteristics of Anteroventral Periventricular Nucleus Kisspeptin and Other Neurons in the Female Mouse
Ducret, E., Gaidamaka, G., & Herbison, A. E. (2010) · Endocrinology · doi:10.1210/en.2009-1480 · Cited by 70 · see citing works
Circadian Control of the Female Reproductive Axis Through Gated Responsiveness of the RFRP-3 System to VIP Signaling
Russo, K. A., La, J. L., Stephens, S. B. Z., Poling, M. C., Padgaonkar, N. A., Jennings, K. J., Piekarski, D. J., Kauffman, A. S., & Kriegsfeld, L. J. (2015) · Endocrinology · doi:10.1210/en.2014-1762 · Cited by 70 · see citing works
Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats
Lederman, M. A., Lebesgue, D., Gonzalez, V. V., Shu, J., Merhi, Z. O., Etgen, A. M., & Neal-Perry, G. S. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.015 · Cited by 69 · see citing works
Vasoactive Intestinal Polypeptide Contacts on Gonadotropin‐Releasing Hormone Neurones Increase Following Puberty in Female Rats
Kriegsfeld, L. J., Silver, R., Gore, A. C., & Crews, D. P. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00818.x · Cited by 67 · see citing works
Changes in Ovarian Luteinizing Hormone and Follicle-Stimulating Hormone Receptor Content and in Gonadotropin-Induced Ornithine Decarboxylase Activity during Prepubertal and Pubertal Development of the Female Rat*
WHITE, S. S., & Ojeda, S. R. (1981) · Endocrinology · doi:10.1210/endo-109-1-152 · Cited by 67 · see citing works
Daily Changes in GT1–7 Cell Sensitivity to GnRH Secretagogues That Trigger Ovulation
Zhao, S., & Kriegsfeld, L. J. (2009) · Neuroendocrinology · doi:10.1159/000192370 · Cited by 65 · see citing works
Lesions of the Suprachiasmatic Nuclei Abolish the Cervically Stimulated Prolactin Surges in the Rat*
Bethea, C. L., & Neill, J. D. (1980) · Endocrinology · doi:10.1210/endo-107-1-1 · Cited by 62 · see citing works
CircadianClockMutation in Dams Disrupts Nursing Behavior and Growth of Pups
Hoshino, K., Wakatsuki, Y., Iigo, M., & Shibata, S. (2006) · Endocrinology · doi:10.1210/en.2005-1343 · Cited by 60 · see citing works
Effects of Single and Multiple Injections of Synthetic GnRH on Serum LH, FSH and Testosterone in Young and Old Male Rats
Bruni, J. F., Huang, H.-H., Marshall, S., & Meites, J. (1977) · Biology of Reproduction · doi:10.1095/biolreprod17.3.309 · Cited by 59 · see citing works
Oestrogen Induces Rhythmic Expression of the Kisspeptin-1 Receptor GPR54 in Hypothalamic Gonadotrophin-Releasing Hormone-Secreting GT1-7 Cells
Tonsfeldt, K. J., Goodall, C. P., Latham, K. L., & Chappell, P. E. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02188.x · Cited by 54 · see citing works
Endocrine regulation of testicular function in men: implications for contraceptive development
Amory, J. K., & Bremner, W. J. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00562-7 · Cited by 53 · see citing works
Evidence for a Putative Circadian Kiss-Clock in the Hypothalamic AVPV in Female Mice
Chassard, D., Bur, I. M., Poirel, V., Mendoza, J., & Simonneaux, V. (2015) · Endocrinology · doi:10.1210/en.2014-1769 · Cited by 51 · see citing works
Inhibitory action of gonadotropin‐inhibitory hormone on the signaling pathways induced by kisspeptin and vasoactive intestinal polypeptide in GnRH neuronal cell line, GT1–7
Son, Y. L., Ubuka, T., Soga, T., Yamamoto, K., Bentley, G. E., & Tsutsui, K. (2016) · The FASEB Journal · doi:10.1096/fj.201500055 · Cited by 51 · see citing works
Self-citation
Estradiol Stimulation of Pulsatile Gonadotropin-Releasing Hormone Secretionin Vitro: Correlation with Perinatal Exposure to Sex Steroids and Induction of Sexual Precocityin Vivo
Matagne, V., Rasier, G., Lebrethon, M. C., Gérard, A., & Bourguignon, J.-P. (2004) · Endocrinology · doi:10.1210/en.2003-1259 · Cited by 46 · see citing works
Localization of the VIP2 Receptor Protein on GnRH Neurons in the Female Rat
Smith, M. J. (2000) · Endocrinology · doi:10.1210/en.141.11.4317 · Cited by 38 · see citing works
Aging-related changes in RP3V kisspeptin neurons predate the reduced activation of GnRH neurons during the early reproductive decline in female mice
Zhang, J., Yang, L., Lin, N., Pan, X., Zhu, Y., & Chen, X. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.08.038 · Cited by 36 · see citing works
Gonadotropin-releasing hormone (GnRH) neurons: gene expression and neuroanatomical studies
Gore, A. C. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)41094-1 · Cited by 33 · see citing works
Development of the light sensitivity of the clock genes Period1 and Period2, and immediate‐early gene c‐fos within the rat suprachiasmatic nucleus
Matějů, K., Bendová, Z., El‐Hennamy, R. E., Sládek, M., Sosniyenko, S., & Sumová, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06609.x · Cited by 30 · see citing works
Effects of Aging and Melatonin Administration on Gonadotropin-Releasing Hormones (GnRH) Gene Expression in the Male and Female Rat
Li, S., Givalois, L., & Pelletier, G. (1997) · Peptides · doi:10.1016/s0196-9781(97)00076-4 · Cited by 28 · see citing works
Circadian variation of serum testosterone in the adult male rat with a late morning acrophase
Wilson, M., McMillin, J. M., Seal, U. S., & Ahmed, K. (1976) · Cellular and Molecular Life Sciences · doi:10.1007/bf02003784 · Cited by 28 · see citing works
Compensation for intracellular environment in expression levels of mammalian circadian clock genes
Matsumura, R., Okamoto, A., Node, K., & Akashi, M. (2014) · Scientific Reports · doi:10.1038/srep04032 · Cited by 24 · see citing works
Twenty-Four Hour Pattern of Prolactin Levels in Female Rats Subjected to Transection of the Mesencephalic Raphe or Ablation of the Suprachiasmatic Nuclei
Dunn, J. D., Johnson, D. C., Castro, A. J., & Swenson, R. M. (2008) · Neuroendocrinology · doi:10.1159/000123055 · Cited by 24 · see citing works
Furin Is the Major Proprotein Convertase Required for KISS1-to-Kisspeptin Processing
Harihar, S., Pounds, K. M., Iwakuma, T., Seidah, N. G., & Welch, D. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084958 · Cited by 23 · see citing works
Hormones and rhythms in man and animals.
Cp, R. (1957) · PubMed · Cited by 22 · see citing works
The Increase in Signaling by Kisspeptin Neurons in the Preoptic Area and Associated Changes in Clock Gene Expression That Trigger the LH Surge in Female Rats Are Dependent on the Facilitatory Action of a Noradrenaline Input
Kalil, B., Ribeiro, A. B., Leite, C. M., Uchôa, E. T., Carolino, R. O. G., Cardoso, T. S. R., Elias, L. L. K., Rodrigues, J. A., Plant, T. M., Poletini, M. O., et al. (2015) · Endocrinology · doi:10.1210/en.2015-1323 · Cited by 21 · see citing works
The Exception Proves the Rule
Holton, R. (2009) · Journal of Political Philosophy · doi:10.1111/j.1467-9760.2009.00358.x · Cited by 21 · see citing works
Reduced responsiveness of kisspeptin neurons to estrogenic positive feedback associated with age-related disappearance of LH surge in middle-age female rats
Ishii, M. N., Matsumoto, K., Matsui, H., Seki, N., Matsumoto, H., Ishikawa, K., Chatani, F., Watanabe, G., & Taya, K. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.06.024 · Cited by 20 · see citing works
PERsuading nuclear receptors to dance the circadian rhythm
Ripperger, J. A., Schmutz, I., & Albrecht, U. (2010) · Cell Cycle · doi:10.4161/cc.9.13.12075 · Cited by 19 · see citing works
Gonadotropin Hormones
Kaiser, U. B. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-380926-1.10007-0 · Cited by 19 · see citing works
Gonadotropin-releasing hormone (GnRH) surge generator in female rats
Funabashi, T., Mitsushima, D., Nakamura, T. J., Uemura, T., Hirahara, F., Shinohara, K., Suyama, K., & Kimura, F. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)41091-6 · Cited by 15 · see citing works
297. Reproduction in the arrhythmic Bmal1 knockout mouse
Boden, M. J., & Kennaway, D. J. (2005) · Reproduction Fertility and Development · doi:10.1071/srb05abs297 · Cited by 13 · see citing works
Anatomy of the Mammalian Circadian System
Gooley, J. J., & Saper, C. B. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00033-5 · Cited by 9 · see citing works
Circadian rhythms: A fine c(l)ocktail!
Albrecht, U. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00308-6 · Cited by 7 · see citing works

Flagged first, then by citations

Sorted by citations

Kisspeptin modulates sexual and emotional brain processing in humans
Comninos, A. N., Wall, M. B., Demetriou, L., Shah, A., Clarke, S. A., Narayanaswamy, S., Nesbitt, A., Izzi‐Engbeaya, C. N., Prague, J., Abbara, A., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89519 · Cited by 121 · see citing works
GnIH Control of Feeding and Reproductive Behaviors
Tsutsui, K., & Ubuka, T. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00170 · Cited by 55 · see citing works
Self-citation
Brain circuits that regulate social behavior
Li, H., Zhao, Z., Jiang, S., & Wu, H. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03037-6 · Cited by 57 · see citing works
Integration of Circadian and Metabolic Control of Reproductive Function
Evans, M. C., & Anderson, G. M. (2018) · Endocrinology · doi:10.1210/en.2018-00691 · Cited by 41 · see citing works
Special features of neuroendocrine interactions between stress and reproduction in teleosts
Rousseau, K., Prunet, P., & Dufour, S. (2020) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2020.113634 · Cited by 38 · see citing works
Chronic Stress and Ovulatory Dysfunction: Implications in Times of COVID-19
Pilar Vigil, P., Meléndez, J., Soto, H., Petkovic, G., Bernal, Y. A., & Molina, S. (2022) · Frontiers in Global Women s Health · doi:10.3389/fgwh.2022.866104 · Cited by 37 · see citing works
Kisspeptin-8 Induces Anxiety-Like Behavior and Hypolocomotion by Activating the HPA Axis and Increasing GABA Release in the Nucleus Accumbens in Rats
Ibos, K. E., Bodnár, É., Bagosi, Z., Bozsó, Z., Tóth, G., Szabó, G., & Csabafi, K. (2021) · Biomedicines · doi:10.3390/biomedicines9020112 · Cited by 34 · see citing works
The Circadian Clock, Nutritional Signals and Reproduction: A Close Relationship
Ono, M., Ando, H., Daikoku, T., Fujiwara, T., Mieda, M., Mizumoto, Y., Iizuka, T., Kagami, K., Hosono, T., Nomura, S., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021545 · Cited by 33 · see citing works
Eel Kisspeptins: Identification, Functional Activity, and Inhibition on both Pituitary LH and GnRH Receptor Expression
Pasquier, J., Lafont, A.-G., Denis, F., Lefranc, B., Dubessy, C., Moreno-Herrera, A., Vaudry, H., Leprince, J., Dufour, S., & Rousseau, K. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00353 · Cited by 25 · see citing works
Central and peripheral neuropeptide RFRP-3: A bridge linking reproduction, nutrition, and stress response
Singh, P., Anjum, S., Srivastava, R. K., Tsutsui, K., & Krishna, A. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100979 · Cited by 26 · see citing works
Reproductive status‐dependent kisspeptin and RF amide‐related peptide (Rfrp) gene expression in female Damaraland mole‐rats
Voigt, C., & Bennett, N. C. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12571 · Cited by 18 · see citing works
The effects of chronic testosterone administration on hypothalamic gonadotropin-releasing hormone regulatory factors (Kiss1, NKB, pDyn and RFRP) and their receptors in female rats
Iwasa, T., Matsuzaki, T., Yano, K., Yanagihara, R., Mayila, Y., & Irahara, M. (2017) · Gynecological Endocrinology · doi:10.1080/09513590.2017.1409709 · Cited by 16 · see citing works
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
Self-citation
Neonatal exposure to 17α-ethynyl estradiol (EE) disrupts follicle development and reproductive hormone profiles in female rats
Zhang, H., Taya, K., Nagaoka, K., Yoshida, M., & Watanabe, G. (2017) · Toxicology Letters · doi:10.1016/j.toxlet.2017.05.014 · Cited by 15 · see citing works
Fibromyalgia pathogenesis explained by a neuroendocrine multistable model
Demori, I., Losacco, S., Giordano, G., Mucci, V., Blanchini, F., & Burlando, B. (2024) · PLOS ONE · doi:10.1371/journal.pone.0303573 · Cited by 14 · see citing works
The content of gonadotropin-releasing hormone (GnRH), kisspeptin, and estrogen receptors (ERα/ERβ) in the anteromedial hypothalamus displays daily variations throughout the rat estrous cycle
Olvera, E., Silva, C., Flores, A., Arrieta‐Cruz, I., Mendoza‐Garcés, L., Martínez‐Coria, H., López-Valdés, H. E., Cárdenas, M., Domı́nguez, R., Juárez, R. G., et al. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03258-x · Cited by 14 · see citing works
Kisspeptin Neuron-Specific and Self-Sustained Calcium Oscillation in the Hypothalamic Arcuate Nucleus of Neonatal Mice: Regulatory Factors of its Synchronization
Kim, D., Jang, S., Kim, J., Park, I., Ku, K., Choi, M., Lee, S., Heo, W. D., Son, G. H., Choe, H. K., et al. (2020) · Neuroendocrinology · doi:10.1159/000505922 · Cited by 12 · see citing works
Development-related changes in the expression of the ovarian Kiss1 and Kiss1r genes and their sensitivity to human chorionic gonadotropin in prepubertal female rats
YAMASAKI, M., Kuwahara, A., Iwasa, T., Yamamoto, Y., Taniguchi, Y., Yano, Y., Matsui, S., Matsuzaki, T., & Irahara, M. (2017) · Journal of Reproduction and Development · doi:10.1262/jrd.2016-179 · Cited by 6 · see citing works
Effects of dihydrotestosterone administration on the expression of reproductive and body weight regulatory factors in ovariectomized and estradiol-treated female rats
Iwasa, T., Matsuzaki, T., Yano, K., Mayila, Y., & Irahara, M. (2017) · Gynecological Endocrinology · doi:10.1080/09513590.2017.1337096 · Cited by 6 · see citing works
Alpha-synuclein expression in GnRH neurons of young and old bovine hypothalami
Niyonzima, Y. B., Asato, Y., Murakami, T., & Kadokawa, H. (2024) · Reproduction Fertility and Development · doi:10.1071/rd24033 · Cited by 3 · see citing works
Loop Modeling of the Reciprocal Inhibition Between HPA and HPG Endocrine Axes Reveals Transitions to Bistability and Critical Bifurcation Parameters
Demori, I., Siriya, S., & Burlando, B. (2025) · Applied Sciences · doi:10.3390/app151910483 · Cited by 2 · see citing works
What is the protective effect of preischemic kisspeptin-10 administration against ischemia/reperfusion injury of striatum on mice?
Akkaya, H., Sümer, E., Kutlu, S., Solak, H., & Yılmaz, B. (2022) · TURKISH JOURNAL OF MEDICAL SCIENCES · doi:10.55730/1300-0144.5493 · Cited by 2 · see citing works
Pharmacologic blockade of nicotinic receptors in the suprachiasmatic nucleus increases ovarian atresia and inhibits follicular growth
Vieyra, E., Calderón, R., Linares, R., Rosas, G., Ramírez, D. A., Espinoza, J. A., Chaparro, A., Silva, C., Domı́nguez, R., & Morales‐Ledesma, L. (2024) · Journal of Neuroendocrinology · doi:10.1111/jne.13421 · Cited by 2 · see citing works
Third Level: The Hypothalamus
Cardinali, D. P. (2017) · Springer eBooks · doi:10.1007/978-3-319-57571-1_5 · Cited by 2 · see citing works
Análise morfológica de neurônios que expressam o receptor de leptina durante as diferentes fases da maturação sexual de camundongos.
de Moraes, L. C. L. (2019) · doi:10.11606/d.42.2019.tde-31072019-074925
Participación de los receptores muscarínicos M2 presentes en el núcleo supraquiasmático sobre la regulación de la ovulación a lo largo del ciclo estral de la rata adulta
Estrada, M. I. G. (2020) · doi:10.24275/uami.gx41mh98g
Ontogénèse de l’axe gonadotrope chez le bar européen (Dicentrarchus labrax) et effets des xénoestrogènes sur sa mise en place
Nihoul, F. (2019) · doi:10.70675/a818d9fbz4c49z4812za420zde74dd5035e7
Differential hypothalamic expression of Musashi protein 2 in Mongolian sheep with single and double ovulation
Fan, J., Li, P., Teng, B., Liu, H., Hao, Q., He, Y., Mingyang, Y., Zhang, Z., Li, X., Yin, J., et al. (2026) · Frontiers in Veterinary Science · doi:10.3389/fvets.2026.1822626

The role of kisspeptin and RFRP in the circadian control of female reproduction
Beymer, M., Henningsen, J. B., Bahougne, T., & Simonneaux, V. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.06.026 · Cited by 21 · see citing works
A kiss for daily and seasonal reproduction
Simonneaux, V., Bur, I. M., Ancel, C., Ansel-Bollepalli, L., & Klosen, P. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59427-3.00024-1 · Cited by 27 · see citing works
Kisspeptins in Reproductive Biology: Consensus Knowledge and Recent Developments1
Roa, J., Navarro, V. M., & Tena‐Sempere, M. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.091538 · Cited by 142 · see citing works
The Role of Kisspeptins and GPR54 in the Neuroendocrine Regulation of Reproduction
Popa, S. M., Clifton, D. K., & Steiner, R. A. (2007) · Annual Review of Physiology · doi:10.1146/annurev.physiol.70.113006.100540 · Cited by 245 · see citing works
Kisspeptin: Past, Present, and Prologue
Steiner, R. A. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-6199-9_1 · Cited by 14 · see citing works

Authors: Putteeraj, M., Soga, T., Ubuka, T., & Parhar, I. S.
Affiliations: Monash University Malaysia (MY)
Corresponding author: Parhar, Ishwar S.
ORCID: Putteeraj, Manish
Soga, Tomoko
Ubuka, Takayoshi
Parhar, Ishwar S.
Venue: Frontiers in Endocrinology
Publisher: Frontiers Media SA
Published: 2016-08-31
Volume: 7
Pages: 121-121
ISSN: 1664-2392 (ISSN-L)
DOI: 10.3389/fendo.2016.00121
PMC: PMC5005330
OpenAlex: W2515748643
Cited by: 28
References: 139
Citations by year: 2026: 1 · 2025: 2 · 2024: 3 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 4 · 2019: 2 · 2018: 3 · 2017: 6 · 2016: 1
FWCI: 0.58
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Endocrinology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Monash University Research Portal (Monash University) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: kisspeptin, kisspeptin neurons, kisspeptin receptor, GnRH neurons, circadian clock, suprachiasmatic nucleus, clock genes, pulsatile GnRH secretion, hypothalamic-pituitary-gonadal axis, preoptic area, anteroventral periventricular nucleus, arcuate nucleus, estrous cycle, puberty, breeding phenology

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

A "Timed" Kiss Is Essential for Reproduction: Lessons from Mammalian Studies

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks