Kisspeptin and Puberty in Mammals

Overview

Journal Adv Exp Med Biol

Specialties Biology
General Medicine

Date 2013 Apr 4

PMID 23550010

Citations 34

Authors

Ei Terasawa

Kathryn A Guerriero

Tony M Plant

Affiliations

Soon will be listed here.

Abstract

Since the discovery of the G-protein coupled receptor 54 (kisspeptin receptor) and its ligand, kisspeptin, our understanding of the neurobiological mechanisms that govern the pituitary-gonadal axis has evolved dramatically. In this chapter, we have reviewed progress regarding the relationship between kisspeptin and puberty, and have proposed a novel hypothesis for the role of kisspeptin signaling in the onset of this crucial developmental event. According to this hypothesis, although kisspeptin neurons in the arcuate nucleus (ARC) are critical for puberty, this is simply because these cells are an integral component of the hypothalamic GnRH pulse generating mechanism that drives intermittent release of the decapeptide, as an increase in GnRH is obligatory for the onset of puberty. In our model, ARC kisspeptin neurons play no "regulatory" role in controlling the timing of puberty. Rather, as a component of the neural network responsible for GnRH pulse generation, they subserve upstream regulatory mechanisms that are responsible for the timing of puberty.

Citing Articles

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References

Kulin H, Grumbach M, Kaplan S . Changing sensitivity of the pubertal gonadal hypothalamic feedback mechanism in man. Science. 1969; 166(3908):1012-3. DOI: 10.1126/science.166.3908.1012. View

Seminara S, Messager S, Chatzidaki E, Thresher R, Acierno Jr J, Shagoury J . The GPR54 gene as a regulator of puberty. N Engl J Med. 2003; 349(17):1614-27. DOI: 10.1056/NEJMoa035322. View

Frost S, Keen K, Levine J, Terasawa E . Microdialysis methods for in vivo neuropeptide measurement in the stalk-median eminence in the Rhesus monkey. J Neurosci Methods. 2007; 168(1):26-34. PMC: 2386413. DOI: 10.1016/j.jneumeth.2007.09.001. View

Shahab M, Mastronardi C, Seminara S, Crowley W, Ojeda S, Plant T . Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A. 2005; 102(6):2129-34. PMC: 548549. DOI: 10.1073/pnas.0409822102. View

Hrabovszky E, Ciofi P, Vida B, Horvath M, Keller E, Caraty A . The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. Eur J Neurosci. 2010; 31(11):1984-98. DOI: 10.1111/j.1460-9568.2010.07239.x. View

Ross J, Loriaux D, Cutler Jr G . Developmental changes in neuroendocrine regulation of gonadotropin secretion in gonadal dysgenesis. J Clin Endocrinol Metab. 1983; 57(2):288-93. DOI: 10.1210/jcem-57-2-288. View

Takase K, Uenoyama Y, Inoue N, Matsui H, Yamada S, Shimizu M . Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol. 2009; 21(6):527-37. DOI: 10.1111/j.1365-2826.2009.01868.x. View

Mann D, Plant T . The role and potential sites of action of thyroid hormone in timing the onset of puberty in male primates. Brain Res. 2010; 1364:175-85. PMC: 2992600. DOI: 10.1016/j.brainres.2010.09.082. View

Funes S, Hedrick J, Vassileva G, Markowitz L, Abbondanzo S, Golovko A . The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun. 2003; 312(4):1357-63. DOI: 10.1016/j.bbrc.2003.11.066. View

10.

Wilson M, Gordon T, Rudman C, Tanner J . Effects of growth hormone on the tempo of sexual maturation in female rhesus monkeys. J Clin Endocrinol Metab. 1989; 68(1):29-38. DOI: 10.1210/jcem-68-1-29. View

11.

Messager S, Chatzidaki E, Ma D, Hendrick A, Zahn D, Dixon J . Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A. 2005; 102(5):1761-6. PMC: 545088. DOI: 10.1073/pnas.0409330102. View

12.

Plant T, Ramaswamy S, DiPietro M . 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. Endocrinology. 2005; 147(2):1007-13. DOI: 10.1210/en.2005-1261. View

13.

Mayer C, Acosta-Martinez M, Dubois S, Wolfe A, Radovick S, Boehm U . Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A. 2010; 107(52):22693-8. PMC: 3012491. DOI: 10.1073/pnas.1012406108. View

14.

Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden J, Le Poul E . The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem. 2001; 276(37):34631-6. DOI: 10.1074/jbc.M104847200. View

15.

Li X, Kinsey-Jones J, Cheng Y, Knox A, Lin Y, Petrou N . Kisspeptin signalling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat. PLoS One. 2009; 4(12):e8334. PMC: 2789414. DOI: 10.1371/journal.pone.0008334. View

16.

Guerriero K, Keen K, Terasawa E . Developmental increase in kisspeptin-54 release in vivo is independent of the pubertal increase in estradiol in female rhesus monkeys (Macaca mulatta). Endocrinology. 2012; 153(4):1887-97. PMC: 3320265. DOI: 10.1210/en.2011-1701. View

17.

Clarkson J, Herbison A . Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology. 2006; 147(12):5817-25. PMC: 6098691. DOI: 10.1210/en.2006-0787. View

18.

Clarkson J, Han S, Liu X, Lee K, Herbison A . Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty. Mol Cell Endocrinol. 2010; 324(1-2):45-50. DOI: 10.1016/j.mce.2010.01.026. View

19.

Parhar I, Ogawa S, Sakuma Y . Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology. 2004; 145(8):3613-8. DOI: 10.1210/en.2004-0395. View

20.

Loose M, Terasawa E . Pulsatile infusion of luteinizing hormone-releasing hormone induces precocious puberty (vaginal opening and first ovulation) in the immature female guinea pig. Biol Reprod. 1985; 33(5):1084-93. DOI: 10.1095/biolreprod33.5.1084. View