Kisspeptin administration to women: A window into endogenous kisspeptin secretion and GnRH responsiveness across the menstrual cycle

Journal of Clinical Endocrinology and Metabolism

Volumn 97, Issue 8, 2012, Pages

  Chan, Yee Ming ^a,b   Butler, James P ^b   Sidhoum, Valerie F ^a   Pinnell, Nancy E ^a   Seminara, Stephanie B ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; KISSPEPTIN; KISSPEPTIN[112-121]; LUTEINIZING HORMONE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; FOLLICULAR PHASE; HORMONE RELEASE; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; LUTEAL PHASE; MENSTRUAL CYCLE; NORMAL HUMAN; PRIORITY JOURNAL; PULSE GENERATOR; SEX DIFFERENCE;

ADULT; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; KISSPEPTINS; LUTEINIZING HORMONE; MENSTRUAL CYCLE; YOUNG ADULT;

MAMMALIA;

EID: 84864802249     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2012-1282     Document Type: Article

References (45)

1. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972-10976 (Pubitemid 37140137)
2. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno Jr JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley Jr WF, Aparicio SA, Colledge WH2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627 (Pubitemid 37303886)
3. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077 (Pubitemid 39120554)
4. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA 2005 Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 102:1761-1766 (Pubitemid 40209241)
5. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR 2005 Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 90:6609-6615 (Pubitemid 41759323)
6. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M, Ghatei MA, Bloom SR 2007 Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 92:3958-3966 (Pubitemid 47607647)
7. Jayasena CN, Nijher GM, Chaudhri OB, Murphy KG, Ranger A, Lim A, Patel D, Mehta A, Todd C, Ramachandran R, Salem V, Stamp GW, Donaldson M, Ghatei MA, Bloom SR, Dhillo WS 2009 Subcutaneous injection of kisspeptin-54 acutely stimulates gonadotropin secretion in women with hypothalamic amenorrhea, but chronic administration causes tachyphylaxis. J Clin Endocrinol Metab 94:4315-4323
8. Jayasena CN, Nijher GM, Abbara A, Murphy KG, Lim A, Patel D, Mehta A, Todd C, Donaldson M, Trew GH, Ghatei MA, Bloom SR, Dhillo WS 2010 Twice-weekly administration of kisspeptin-54 for 8 weeks stimulates release of reproductive hormones in women with hypothalamic amenorrhea. Clin Pharmacol Ther 88:840-847
9. Chan YM, Butler JP, Pinnell NE, Pralong FP, Crowley Jr WF, Ren C, Chan KK, Seminara SB 2011 Kisspeptin resets the hypothalamic GnRH clock in men. J Clin Endocrinol Metab 96:E908-E915
10. George JT, Veldhuis JD, Roseweir AK, Newton CL, Faccenda E, Millar RP, Anderson RA 2011 Kisspeptin-10 is a potent stimulator of LH and increases pulse frequency in men. J Clin Endocrinol Metab 96:E1228-E1236
11. Jayasena CN, Nijher GM, Comninos AN, Abbara A, Januszewki A, Vaal ML, Sriskandarajah L, Murphy KG, Farzad Z, Ghatei MA, Bloom SR, Dhillo WS 2011 The effects of kisspeptin-10 on reproductive hormone release show sexual dimorphism in humans. J Clin Endocrinol Metab 96:E1963-E1972
12. Young J, George JT, Tello JA, Francou B, Bouligand J, Guiochon-Mantel A, Brailly-Tabard S, Anderson RA, Millar RP 24 February 2012 Kisspeptin restores pulsatile LH secretion in patients with neurokinin B signaling deficiencies: physiological, pathophysiological and therapeutic implications. Neuroendocrinology 10.1159/000336376
13. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE 2005 Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349-11356 (Pubitemid 43083709)
14. Pielecka-Fortuna J, Chu Z, Moenter SM 2008 Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 149:1979-1986 (Pubitemid 351468349)
15. Zhang C, Roepke TA, Kelly MJ, Rønnekleiv OK 2008 Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28:4423-4434
16. Dumalska I, Wu M, Morozova E, Liu R, van den Pol A, Alreja M 2008 Excitatory effects of the puberty-initiating peptide kisspeptin and group I metabotropic glutamate receptor agonists differentiate two distinct subpopulations of gonadotropin-releasing hormone neurons. J Neurosci 28:8003-8013
17. Constantin S, Caligioni CS, Stojilkovic S, Wray S 2009 Kisspeptin-10 facilitates a plasma membrane-driven calcium oscillator in gonadotropin- releasing hormone-1 neurons. Endocrinology 150:1400-1412
18. Santen RJ, BardinCW1973 Episodic luteinizing hormone secretion in man. Pulse analysis, clinical interpretation, physiologic mechanisms. J Clin Invest 52:2617-2628
19. Spratt DI, Carr DB, Merriam GR, Scully RE, Rao PN, Crowley Jr WF 1987 The spectrum of abnormal patterns of gonadotropin-releasing hormone secretion in men with idiopathic hypogonadotropic hypogonadism: clinical and laboratory correlations. J Clin Endocrinol Metab 64:283-291 (Pubitemid 17001060)
20. Pralong FP, Boepple PA, Conn PM, Whitcomb RW, Butler JP, Schoenfeld D, Crowley Jr WF 1996 Contour of the GnRH pulse independently modulates gonadotropin secretion in the human male. Neuroendocrinology 64:247-256 (Pubitemid 26280818)
21. Roa J, Vigo E, Castellano JM, Navarro VM, Fernández- Fernández R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M 2006 Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 147:2864-2878 (Pubitemid 43764622)
22. Smith JT, Saleh SN, Clarke IJ 2009 Seasonal and cyclical change in the luteinizing hormone response to kisspeptin in the ewe. Neuroendocrinology 90:283-291
23. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H 2010 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. J Neurosci 30:3124-3132
24. Guerriero KA, Keen KL, Millar RP, Terasawa E 2012 Developmental changes in GnRH release in response to kisspeptin agonist and antagonist in female rhesus monkeys (Macaca mulatta): implication for the mechanism of puberty. Endocrinology 153:825-836
25. Novaira HJ, Ng Y, Wolfe A, Radovick S 2009 Kisspeptin increases GnRH mRNA expression and secretion in GnRH secreting neuronal cell lines. Mol Cell Endocrinol 311:126-134
26. Tonsfeldt KJ, Goodall CP, Latham KL, Chappell PE 2011 Oestrogen induces rhythmic expression of the Kisspeptin-1 receptor GPR54 in hypothalamic gonadotrophin-releasing hormone-secreting GT1-7 cells. J Neuroendocrinol 23:823-830
27. Seminara SB, Dipietro MJ, Ramaswamy S, Crowley Jr WF, Plant TM 2006 Continuous human metastin 45-54 infusion desensitizes G protein-coupled receptor 54-induced gonadotropin-releasing hormone release monitored indirectly in the juvenile male Rhesus monkey (Macaca mulatta): a finding with therapeutic implications. Endocrinology 147:2122-2126
28. Ramaswamy S, Seminara SB, Pohl CR, DiPietro MJ, Crowley Jr WF, Plant TM 2007 Effect of continuous intravenous administration of human metastin 45-54 on the neuroendocrine activity of the hypothalamic-pituitary-testicular axis in the adult male rhesus monkey (Macaca mulatta). Endocrinology 148:3364-3370 (Pubitemid 46996993)
29. Roa J, Vigo E, García-Galiano D, Castellano JM, Navarro VM, Pineda R, Diéguez C, Aguilar E, Pinilla L, Tena-Sempere M 2008 Desensitization of gonadotropin responses to kisspeptin in the female rat: analyses of LH and FSH secretion at different developmental and metabolic states. Am J Physiol Endocrinol Metab 294:E1088-E1096
30. Roseweir AK, Kauffman AS, Smith JT, Guerriero KA, Morgan K, Pielecka-Fortuna J, Pineda R, Gottsch ML, Tena-Sempere M, Moenter SM, Terasawa E, Clarke IJ, Steiner RA, Millar RP 2009 Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci 29:3920-3929
31. Santoro N, Wierman ME, Filicori M, Waldstreicher J, Crowley Jr WF 1986 Intravenous administration of pulsatile gonadotropin-releasing hormone in hypothalamic amenorrhea: effects of dosage. J Clin Endocrinol Metab 62:109-116 (Pubitemid 16186851)
32. Hall JE 2009 Neuroendocrine control of the menstrual cycle. In: Strauss III JF and Barbieri RL, ed. Yen and Jaffe's reproductive endocrinology. 6th ed. Philadelphia, PA: Elsevier Saunders; 139-154
33. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR 2004 Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 16:850-858 (Pubitemid 39489998)
34. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA 2005 Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 102:1761-1766 (Pubitemid 40209241)
35. Caraty A, Smith JT, Lomet D, Ben Saïd S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ 2007 Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 148:5258-5267 (Pubitemid 350017445)
36. Nillius SJ, Wide L 1972 Variation in LH and FSH response to LH-releasing hormone during the menstrual cycle. J Obstet Gynaecol Br Commonw 79:865-873
37. Thomas K, Donnez J, Ferin J 1972 LH and FSH releasing potency of the synthetic decapeptide p-Glu-His-Trp-Ser-Tyr-Gly-Leu-Arg-Pro-Gly-NH 2 in human beings. Contraception 6:55-64
38. Yen SS, VandenBerg G, Rebar R, Ehara Y 1972 Variation of pituitary responsiveness to synthetic LRF during different phases of the menstrual cycle. J Clin Endocrinol Metab 35:931-934
39. Aono T, Minagawa J, Kinugasa T, Tanizawa O, Kurachi K 1973 Response of pituitary LH and FSH to synthetic LH-releasing hormone in normal subjects and patients with Sheehan's syndrome. Am J Obstet Gynecol 117:1046-1052
40. Franchimont P, Becker H, Ernould C, Thys C, Demoulin A, Bourguignon JP, Legros JJ, Valcke JC 1974 The effect of hypothalamic luteinizing hormone releasing hormone (LH-RH) on plasma gonadotrophin levels in normal subjects. Clin Endocrinol (Oxf) 3:27-39
41. Wang CF, Yen SS 1975 Direct evidence of estrogen modulation of pituitary sensitivity to luteinizing hormone-releasing factor during the menstrual cycle. J Clin Invest 55:201-204
42. Thompson IE, Arfania J, Taymor ML 1973 Effects of estrogen and progesterone on pituitary response to stimulation by luteinizing hormone-releasing factor. J Clin Endocrinol Metab 37:152-155
43. Hall JE, Taylor AE, Martin KA, Rivier J, Schoenfeld DA, Crowley Jr WF 1994 Decreased release of gonadotropin-releasing hormone during the preovulatory midcycle luteinizing hormone surge in normal women. Proc Natl Acad Sci USA 91:6894-6898 (Pubitemid 24226768)
44. Butler JP, Spratt DI, O'Dea LS, Crowley Jr WF 1986 Interpulse interval sequence of LH in normal men essentially constitutes a renewal process. Am J Physiol 250:E338-E340
45. Santoro N, Butler JP, Filicori M, Crowley Jr WF 1988 Alterations of the hypothalamic GnRH interpulse interval sequence over the normal menstrual cycle. Am J Physiol 255:E696-E701