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Repetitive Activation of Hypothalamic G Protein-Coupled Receptor 54 with Intravenous Pulses of Kisspeptin in the Juvenile Monkey (Macaca mulatta) Elicits a Sustained Train of Gonadotropin-Releasing Hormone Discharges
Abstract
The purpose of the present study was to further examine the hypothesis that activation of G protein-coupled receptor 54 (GPR54) signaling at the end of the juvenile phase of primate development is responsible for initiation of gonadarche and the onset of puberty. Accordingly, we determined whether repetitive iv administration of the GPR54 receptor agonist kisspeptin-10 (2 μg as a brief 1-min infusion once every hour for 48 h) to the juvenile male rhesus monkey would prematurely elicit sustained, pulsatile release of hypothalamic GnRH, the neuroendocrine trigger for gonadarche. GnRH release was monitored indirectly by measuring LH secretion from the in situ pituitary, the GnRH responsiveness of which had been heightened before the experiment with an intermittent iv infusion of synthetic GnRH. Agonadal animals (n = 4) were employed to eliminate any confounding and secondary effects of changing feedback signals from the testis. The first brief infusion of kisspeptin-10 evoked an LH discharge that mimicked those produced by GnRH priming, and this was followed by a train of similar LH discharges in response to hourly activation of GPR54 by repetitive kisspeptin-10 administration. Concomitant treatment with a GnRH receptor antagonist, acyline, abolished kisspeptin-10-induced LH release. Repetitive kisspeptin-10 administration also provided a GnRH-dependent signal to FSH secretion. These findings are consistent with the notion that, in primates, the transition from the juvenile (attenuated GnRH release) to pubertal (robust GnRH release) state is controlled by activation of GPR54 resulting from increased expression of hypothalamic KiSS-1 and release of kisspeptin in this region of the brain.
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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
Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54
de Roux, N., Genin, E., Carel, J.-C., Matsuda, F., Chaussain, J.-L., & Milgrom, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834399100 · Cited by 2,431
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The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system
Funes, S., Hedrick, J. A., Vassileva, G., Markowitz, L., Abbondanzo, S., Golovko, A., Yang, S., Monsma, F. J., & Gustafson, E. L. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.11.066 · Cited by 675
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Cited by
Clarkson, J., & Herbison, A. E. (2006) · Endocrinology · doi:10.1210/en.2006-0787 · Cited by 875
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
Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B
Goodman, R. L., Lehman, M. N., Smith, J. T., Coolen, L. M., de Oliveira, C. V. R., Jafarzadehshirazi, M. R., Pereira, A., Iqbal, J., Caraty, A., Ciofi, P., et al. (2007) · Endocrinology · doi:10.1210/en.2007-0961 · Cited by 692
A GPR54 -Activating Mutation in a Patient with Central Precocious Puberty
Teles, M. G., Bianco, S. D. C., Brito, V. N., Trarbach, E. B., Kuohung, W., Xu, S., Seminara, S. B., Mendonca, B. B., Kaiser, U. B., & Latronico, A. C. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa073443 · Cited by 572
Control of puberty onset and fertility by gonadotropin-releasing hormone neurons
Herbison, A. E. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.70 · Cited by 515
Characterization of Kiss1 neurons using transgenic mouse models
Cravo, R. M., Margatho, L. O., Osborne-Lawrence, S., Donato, J., Atkin, S., Bookout, A. L., Rovinsky, S., Frazão, R., Lee, C. E., Gautron, L., et al. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.11.022 · Cited by 353
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Ramaswamy, S., Seminara, S. B., Ali, B., Ciofi, P., Amin, N. A., & Plant, T. M. (2010) · Endocrinology · doi:10.1210/en.2010-0223 · Cited by 267
Self-citationThe Gonadotropin-Releasing Hormone Pulse Generator
Herbison, A. E. (2018) · Endocrinology · doi:10.1210/en.2018-00653 · Cited by 261
Han, S. Y., McLennan, T., Czieselsky, K., & Herbison, A. E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512243112 · Cited by 189
Kisspeptin-10 is a potent stimulator of LH and increases pulse frequency in men
George, J. T., Veldhuis, J. D., Roseweir, A. K., Newton, C. L., Faccenda, E., Millar, R. P., & Anderson, R. A. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0089 · Cited by 186
Neuroanatomy of the kisspeptin signaling system in mammals: comparative and developmental aspects
Lehman, M. N., Hileman, S. M., & Goodman, R. L. (2013) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-6199-9_3 · Cited by 180
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
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
Estrogen Regulates KiSS1 Gene Expression through Estrogen Receptor α and SP Protein Complexes
Li, D., Mitchell, D., Luo, J., Yi, Z., Cho, S.-G., Guo, J., Li, X., Ning, G., Wu, X., & Liu, M. (2007) · Endocrinology · doi:10.1210/en.2007-0154 · Cited by 90
Kisspeptin antagonists: Unraveling the role of kisspeptin in reproductive physiology
Millar, R. P., Roseweir, A. K., Tello, J. A., Anderson, R. A., George, J. T., Morgan, K., & Pawson, A. J. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.044 · Cited by 69
Increased plasma metastin levels in adolescent women with polycystic ovary syndrome
Chen, X., Mo, Y., Li, L., Chen, Y., Li, Y., & Yang, D. (2010) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2009.11.018 · Cited by 60
Jayasena, C. N., Abbara, A., Narayanaswamy, S., Comninos, A. N., Ratnasabapathy, R., Bassett, P., Mogford, J. T., Malik, Z., Calley, J., Ghatei, M. A., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev143 · Cited by 52
Neurokinin B signalling in the human reproductive axis
Topaloglu, A. K., & Semple, R. K. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.014 · Cited by 41
Potential clinical use of kisspeptin
Prague, J. K., & Dhillo, W. S. (2015) · Neuroendocrinology · doi:10.1159/000439133 · Cited by 26
Metadata
- Authors
- Plant, T. M., Ramaswamy, S., & DiPietro, M. J.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2006-02-01
- Volume
- 147
- Issue
- 2
- Pages
- 1007-1013
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2048872158
- Cited by
- 296
- References
- 6
- FWCI
- 21.60
- Type
- journal article
- Language
- en
- Open access
- closed
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