Kisspeptin expression in the brain: Catalyst for the initiation of puberty

Reviews in Endocrine and Metabolic Disorders

Volumn 8, Issue 1, 2007, Pages 1-9

  Smith, J T ^a   Clarke, I J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Hypogonadotropic hypogonadism; Kisspeptin; Neuroendocrine

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; GONADOTROPIN; KISSPEPTIN; METASTIN; SEX HORMONE;

ARCUATE NUCLEUS; BREEDING; ESTRUS CYCLE; FEEDBACK SYSTEM; GENE EXPRESSION; GENE MUTATION; GONADOTROPIN RELEASE; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; HYPOTHALAMUS; NEUROENDOCRINE SYSTEM; NONHUMAN; OVULATION; PHOTOPERIODICITY; PROESTRUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PUBERTY; REPRODUCTION; REVIEW; SEASONAL VARIATION;

ANIMALS; BRAIN; ESTROUS CYCLE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADAL STEROID HORMONES; GONADOTROPINS; HUMANS; MODELS, BIOLOGICAL; PUBERTY; REPRODUCTION; SEASONS; SEXUAL MATURATION; TUMOR SUPPRESSOR PROTEINS;

EID: 34047226334     PISSN: 13899155     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11154-007-9026-4     Document Type: Review

References (82)

1. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, et al. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 1996;88(23):1731-7.
2. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, et al. 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.
3. Lee DK, Nguyen T, O'Neill GP, Cheng R, Liu Y, Howard AD, et al. Discovery of a receptor related to the galanin receptors. FEBS Lett 1999;446(1):103-7.
4. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, et al. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001;276(31):28969-75.
5. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001;411(6837):613-7.
6. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 2003;100(19):10972-6.
7. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Jr, Shagoury JK, et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003;349(17):1614-27.
8. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003;312(4):1357-63.
9. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004;145(9):4073-7.
10. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 2004;320(2):383-8.
11. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, et al. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004;145(10):4565-74.
12. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005;146(1):156-63.
13. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, et al. 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.
14. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. 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.
15. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, et al. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005;90(12):6609-15.
16. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004;80(4):264-72.
17. Clarke IJ, Cummins JT, de Kretser DM. Pituitary gland function after disconnection from direct hypothalamic influences in the sheep. Neuroendocrinology 1983;36(5):376-84.
18. Fraser HM, Clarke IJ, McNeilly AS. Effect of oestrogen and an LH-RH agonist on the release of gonadotrophins in ovariectomized ewes deprived of LH-RH. J Reprod Fertil 1981;62(1):131-40.
19. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, et al. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005;146(4):1689-97.
20. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, et al. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004;16(10):850-58.
21. Smith JT, Pereira A, Roa A, Morgan K, R. M, Clarke IJ. Evidence that pituitary gonadotropes are not major targets of kisspeptin. In: Proc 89th Annual Meeting of the Endocrine Society; 2007; Toronto, Ontario, Canada.
22. Parhar IS, 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.
23. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, et al. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005;25(49):11349-56.
24. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006;147(12):5817-25.
25. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, et al. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005;146(10):4431-6.
26. Skinner DC, Caraty A, Malpaux B, Evans NP. Simultaneous measurement of gonadotropin-releasing hormone in the third ventricular cerebrospinal fluid and hypophyseal portal blood of the ewe. Endocrinology 1997;138(11):4699-704.
27. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005;146(9):3686-92.
28. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005;146(7):2976-84.
29. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 2006;26(25):6687-94.
30. Brailoiu GC, Dun SL, Ohsawa M, Yin D, Yang J, Chang JK, et al. KiSS-1 expression and metastin-like immunoreactivity in the rat brain. J Comp Neurol 2005;481(3):314-29.
31. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ. Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogen-positive feedback. J Neuroendocrinol 2006;18(10):806-9.
32. Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 mRNA expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 2007;148:1150-1157.
33. Pompolo S, Pereira A, Estrada KM, Clarke IJ. Colocalization of kisspeptin and gonadotropin-releasing hormone in the ovine brain. Endocrinology 2006;147(2):804-10.
34. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006;401(3):225-30.
35. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, et al. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A 2006;103(7):2410-15.
36. Clarke IJ. The hypothalamo-pituitary axis. In: Hillier SG, Kitchener HC, Neilsen JP editors. Scientific essentials of reproductive medicine. UK: Saunders; 1996. p. 120-132.
37. Herbison AE, Theodosis DT. Localization of oestrogen receptors in preoptic neurons containing neurotensin but not tyrosine hydroxylase, cholecystokinin or luteinizing hormone-releasing hormone in the male and female rat. Neuroscience 1992;50(2):283-98.
38. Shivers BD, Harlan RE, Morrell JI, Pfaff DW. Absence of oestradiol concentration in cell nuclei of LHRH-immunoreactive neurones. Nature 1983;304(5924):345-7.
39. Skinner DC, Caraty A, Allingham R. Unmasking the progesterone receptor in the preoptic area and hypothalamus of the ewe: no colocalization with gonadotropin-releasing neurons. Endocrinology 2001;142(2):573-9.
40. Hrabovszky E, Shughrue PJ, Merchenthaler I, Hajszan T, Carpenter CD, Liposits Z, et al. Detection of estrogen receptorbeta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2000;141(9):3506-9.
41. Dorling AA, Todman MG, Korach KS, Herbison AE. Critical role for estrogen receptor alpha in negative feedback regulation of gonadotropin-releasing hormone mRNA expression in the female mouse. Neuroendocrinology 2003;78(4):204-9.
42. Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 1998;19(3):302-30.
43. Hagihara K, Hirata S, Osada T, Hirai M, Kato J. Distribution of cells containing progesterone receptor mRNA in the female rat diand telencephalon: an in situ hybridization study. Brain Res Mol Brain Res 1992;14(3):239-49.
44. Scott CJ, Pereira AM, Rawson JA, Simmons DM, Rossmanith WG, Ing NH, et al. The distribution of progesterone receptor immunoreactivity and mRNA in the preoptic area and hypothalamus of the ewe: upregulation of progesterone receptor mRNA in the mediobasal hypothalamus by oestrogen. J Neuroendocrinol 2000;12(6):565-75.
45. Scott CJ, Tilbrook AJ, Simmons DM, Rawson JA, Chu S, Fuller PJ, et al. The distribution of cells containing estrogen receptor-alpha (ERalpha) and ERbeta messenger ribonucleic acid in the preoptic area and hypothalamus of the sheep: comparison of males and females. Endocrinology 2000;141(8):2951-62.
46. Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997;388(4):507-25.
47. Simerly RB, Chang C, Muramatsu M, Swanson LW. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 1990;294(1):76-95.
48. Dufourny L, Caraty A, Clarke IJ, Robinson JE, Skinner DC. Progesterone-receptive dopaminergic and neuropeptide Y neurons project from the arcuate nucleus to gonadotropin-releasing hormone-rich regions of the ovine preoptic area. Neuroendocrinology 2005;82(1):21-31.
49. Dufourny L, Caraty A, Clarke IJ, Robinson JE, Skinner DC. Progesterone-receptive beta-endorphin and dynorphin B neurons in the arcuate nucleus project to regions of high gonadotropin-releasing hormone neuron density in the ovine preoptic area. Neuroendocrinology 2005;81(3):139-49.
50. Foradori CD, Coolen LM, Fitzgerald ME, Skinner DC, Goodman RL, Lehman MN. Colocalization of progesterone receptors in parvicellular dynorphin neurons of the ovine preoptic area and hypothalamus. Endocrinology 2002;143(11):4366-74.
51. Pompolo S, Pereira A, Scott CJ, Fujiyma F, Clarke IJ. Evidence for estrogenic regulation of gonadotropin-releasing hormone neurons by glutamatergic neurons in the ewe brain: an immunohistochemical study using an antibody against vesicular glutamate transporter-2. J Comp Neurol 2003;465(1):136-44.
52. Pompolo S, Rawson JA, Clarke IJ. 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. Brain Res 2001;904(1):1-12.
53. Pompolo S, Ischenko O, Pereira A, Iqbal J, Clarke IJ. Evidence that projections from the bed nucleus of the stria terminalis and from the lateral and medial regions of the preoptic area provide input to gonadotropin releasing hormone (GNRH) neurons in the female sheep brain. Neuroscience 2005;132(2):421-36.
54. Gu GB, Simerly RB. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J Comp Neurol 1997;384(1):142-64.
55. Simerly RB. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav Brain Res 1998;92(2):195-203.
56. Gottsch ML, Clifton DK, Steiner RA. Kisspeptin-GPR54 signaling in the neuroendocrine reproductive axis. Mol Cell Endocrinol 2006;254-255:91-96.
57. Blache D, Fabre-Nys CJ, Venier G. Ventromedial hypothalamus as a target for oestradiol action on proceptivity, receptivity and luteinizing hormone surge of the ewe. Brain Res 1991;546(2):241-9.
58. Caraty A, Fabre-Nys C, Delaleu B, Locatelli A, Bruneau G, Karsch FJ, et al. Evidence that the mediobasal hypothalamus is the primary site of action of estradiol in inducing the preovulatory gonadotropin releasing hormone surge in the ewe. Endocrinology 1998;139(4):1752-60.
59. Cumming IA, Brown JM, Goding JR, Bryant GD, Greenwood FC. Secretion of prolactin and luteinizing hormone at oestrus in the ewe. J Endocrinol 1972;54(2):207-13.
60. Ojeda SR, Urbanski HF. Puberty in the rat. In: Knobil E, Neill JD editors. Physiology of reproduction, vol. 2, 2nd ed. New York: Raven; 1994. p. 363-409.
61. Plant TM. Puberty in primates. In: Knobil E, Neill JD editors. Physiology of reproduction, vol. 2, 2nd ed. New York: Raven; 1994. p. 453-485.
62. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004;561(Pt 2):379-86.
63. Cottrell EC, Campbell RE, Han SK, Herbison AE. Postnatal remodeling of dendritic structure and spine density in gonadotropin-releasing hormone neurons. Endocrinology 2006;147(8):3652-61.
64. Ebling FJ, Foster DL. Photoperiod requirements for puberty differ from those for the onset of the adult breeding season in female sheep. J Reprod Fertil 1988;84(1):283-93.
65. Foster DL, Ebling FJ, Claypool LE, Woodfill CJ. Cessation of long day melatonin rhythms time puberty in a short day breeder. Endocrinology 1988;123(3):1636-41.
66. Barker-Gibb ML, Clarke IJ. Effect of season on neuropeptide Y and galanin within the hypothalamus of the ewe in relation to plasma luteinizing hormone concentrations and the breeding season: an immunohistochemical analysis. J Neuroendocrinol 2000;12(7):618-26.
67. Barrell GK, Moenter SM, Caraty A, Karsch FJ. Seasonal changes of gonadotropin-releasing hormone secretion in the ewe. Biol Reprod 1992;46(6):1130-5.
68. Karsch FJ, Dahl GE, Evans NP, Manning JM, Mayfield KP, Moenter SM, et al. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biol Reprod 1993;49(6):1377-83.
69. Robinson JE, Radford HM, Karsch FJ. 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 feedback. Biol Reprod 1985;33(2):324-34.
70. Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 2006;16(17):1730-5.
71. Clarke IJ, Smith JT, Morrissey A, Doughton B, Cameron A, Caraty A. Kisspeptin stimulates ovulation in seasonally acylic ewes. In: Proc 89th Annual Meeting of the Endocrine Society; 2007; Toronto, Ontario, Canada.
72. Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 1998;139(4):1508-16.
73. Lincoln GA. Effects of placing micro-implants of melatonin in the pars tuberalis, pars distalis and the lateral septum of the forebrain on the secretion of FSH and prolactin, and testicular size in rams. J Endocrinol 1994;142(2):267-76.
74. Lincoln GA, Maeda K. Effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area on the secretion of prolactin and beta-endorphin in rams. J Endocrinol 1992;134(3):437-48.
75. Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 1995;269(5223):546-9.
76. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 1995;269(5223):540-3.
77. Clarke IJ, Henry BA. Leptin and reproduction. Rev Reprod 1999;4(1):48-55.
78. Cunningham MJ, Clifton DK, Steiner RA. Leptin's actions on the reproductive axis: perspectives and mechanisms. Biol Reprod 1999;60(2):216-22.
79. Finn PD, Cunningham MJ, Pau KY, Spies HG, Clifton DK, Steiner RA. The stimulatory effect of leptin on the neuroendocrine reproductive axis of the monkey. Endocrinology 1998;139(11):4652-62.
80. Hakansson ML, Brown H, Ghilardi N, Skoda RC, Meister B. Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus. J Neurosci 1998;18(1):559-72.
81. Castellano JM, Navarro VM, Fernandez-Fernandez R, Nogueiras R, Tovar S, Roa J, et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005;146(9):3917-25.
82. Smith JT, Acohido BV, Clifton DK, Steiner RA. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol 2006;18(4):298-303.