Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women

Journal of Clinical Endocrinology and Metabolism

Volumn 92, Issue 10, 2007, Pages 3958-3966

  Dhillo, Waljit S ^a   Chaudhri, Owais B ^a   Thompson, Emily L ^a   Murphy, Kevin G ^a   Patterson, Michael ^a   Ramachandran, Radha ^a,b   Nijher, Gurjinder K ^a,b   Amber, Vian ^a,b   Kokkinos, Alexander ^a   Donaldson, Mandy ^b   Ghatei, Mohammad A ^a   Bloom, Stephen R ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GONADOTROPIN; LUTEINIZING HORMONE; METASTIN; PLACEBO; SODIUM CHLORIDE;

ABSENCE OF SIDE EFFECTS; ADULT; ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG POTENCY; FEMALE; FOLLICULAR PHASE; GONADOTROPIN BLOOD LEVEL; GONADOTROPIN RELEASE; HEALTH CARE FACILITY; HUMAN; HUMAN EXPERIMENT; LUTEAL PHASE; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; MENSTRUAL CYCLE; NAUSEA; NORMAL HUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; STIMULATION;

MUS; PRIMATES; RODENTIA;

EID: 35349022556     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2007-1116     Document Type: Article

References (53)

1. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M 2001 The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G proteincoupled receptor GPR54. J Biol Chem 276:34631-34636
2. 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
3. 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 WH 2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627
4. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL 2003 The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312:1357-1363
5. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M 2004 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 145:4565-4574
6. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T 2004 Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 320:383-388
7. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M 2005 Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146:156-163
8. 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
9. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Barreiro ML, Casanueva FF, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M 2005 Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146:1689-1697
10. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA 2004 Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80:264-272
11. Tovar S, Vazquez MJ, Navarro VM, Fernandez-Fernandez R, Castellano JM, Vigo E, Roa J, Casanueva FF, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M 2006 Effects of single or repeated intravenous administration of kisspeptin upon dynamic LH secretion in conscious male rats. Endocrinology 147:2696-2704
12. Patterson M, Murphy KG, Thompson EL, Patel S, Ghatei MA, Bloom SR 2006 Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats. J Neuroendocrinol 18:349-354
13. Castellano JM, Navarro VM, Fernandez-Fernandez R, Roa J, Vigo E, Pineda R, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M 2006 Expression of hypothalamic KiSS-1 system and rescue of defective gonadotropic responses by kisspeptin in streptozotocin-induced diabetic male rats. Diabetes 55:2602-2610
14. 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
15. 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
16. Arreguin-Arevalo JA, Lents CA, Farmerie TA, Nett TM, Clay CM, KiSS-1 peptide induces release of LH by a direct effect on the hypothalamus of ovariectomized ewes. Anim Reprod Sci 101:265-275
17. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM 2005 Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 102:2129-2134
18. Plant TM, Ramaswamy S, Dipietro MJ 2006 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 147:1007-1013
19. 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
20. 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
21. 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
22. Pompolo S, Pereira A, Estrada KM, Clarke IJ 2006 Colocalization of kisspeptin and gonadotropin-releasing hormone in the ovine brain. Endocrinology 147:804-810
23. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA 2005 Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146:2976-2984
24. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA 2005 Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146:3686-3692
25. Smith JT, Clay CM, Caraty A, Clarke IJ 2006 KiSS-1 mRNA expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148:1150-1157
26. Rometo AM, Krajewski SJ, Voytko ML, Rance NE 2007 Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab 92:2744-2750
27. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K 2005 Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146:4431-4436
28. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M 2007 Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148:1774-1783
29. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K 2007 Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 53:367-378
30. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ 2006 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 18:806-809
31. Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez-Fernandez 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
32. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M 2004 Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 561:379-386
33. 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
34. Clarkson J, Herbison AE 2006 Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147:5817-5825
35. Thompson EL, Murphy KG, Patterson M, Bewick GA, Stamp GW, Curtis AE, Cooke JH, Jethwa PH, Todd JF, Ghatei MA, Bloom SR 2006 Chronic subcutaneous administration of kisspeptin-54 causes testicular degeneration in adult male rats. Am J Physiol Endocrinol Metab 291:E1074-E1082
36. Hashimoto T, Miyai K, Izumi K, Kumahara Y 1973 Gonadotropin response to synthetic LH-RH in normal subjects: correlation between LH and FSH. J Clin Endocrinol Metab 37:910-916
37. Neill JD 2006 Knobil and Neill's physiology of reproduction. St. Louis: Academic Press
38. de Gomez MS, Frei A, Vitins P, Cekan SZ 1981 Influence of antisera, purification procedures, and tracers on validity of a testosterone radioimmunoassay. Ann Clin Biochem 18:281-286
39. Belgorosky A, Escobar ME, Rivarola MA 1987 Validity of the calculation of non-sex hormone-binding globulin-bound estradiol from total testosterone, total estradiol and sex hormone-binding globulin concentrations in human serum. J Steroid Biochem 28:429-432
40. Dhillo WS, Savage P, Murphy KG, Chaudhri OB, Patterson M, Nijher GM, Foggo VM, Dancey GS, Mitchell H, Seckl MJ, Ghatei MA, Bloom SR 2006 Plasma kisspeptin is raised in patients with gestational trophoblastic neoplasia and falls during treatment. Am J Physiol Endocrinol Metab 291:E878-E884
41. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M 2001 Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411:613-617
42. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CG, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC 2001 AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276:28969-28975
43. Bilban M, Ghaffari-Tabrizi N, Hintermann E, Bauer S, Molzer S, Zoratti C, Malli R, Sharabi A, Hiden U, Graier W, Knofler M, Andreae F, Wagner O, Quaranta V, Desoye G 2004 Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 117:1319-1328
44. Mead EJ, Maguire JJ, Kuc RE, Davenport AP 2007 Kisspeptins are novel potent vasoconstrictors in humans, with a discrete localization of their receptor GPR54, to atherosclerosis prone vessels. Endocrinology 148:140-147
45. Yen SS, Rebar R, Vandenberg G, Ehara Y, Siler T 1973 Pituitary gonadotrophin responsiveness to synthetic LRF in subjects with normal and abnormal hypothalamic-pituitary-gonadal axis. J Reprod Fertil Suppl 20:137-161
46. 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
47. Shaw RW, Butt WR, London DR, Marshall JC 1974 Variation in response to synthetic luteinizing hormone-releasing hormone (LH-RH) at different phases of the same menstrual cycle in normal women. J Obstet Gynaecol Br Commonw 81:632-639
48. Nakano R, Kotsuji F, Tojo S 1975 Pituitary responsiveness to synthetic luteinizing hormone releasing hormone (LH-RH) during the menstrual cycle and in female hypogonadism. Br J Obstet Gynaecol 82:805-811
49. de Kretser DM, Burger HG, Dumpys R 1978 Patterns of serum LH and FSH in response to 4-hour infusions of luteinizing hormone releasing hormone in normal women during menstrual cycle, on oral contraceptives, and in postmenopausal state. J Clin Endocrinol Metab 46:227-235
50. Jewelewicz R, Dyrenfurth I, Ferin M, Bogumil J, Vande Wiele RL 1977 Gonadotropin, estrogen and progesterone response to long term gonadotropin-releasing hormone infusion at various stages of the menstrual cycle. J Clin Endocrinol Metab 45:662-667
51. Loucopoulos A, Ferin M 1987 The treatment of luteal phase defects with pulsatile infusion of gonadotropin-releasing hormone. Fertil Steril 48:933-936
52. McLachlan RI, Cohen NL, Vale WW, Rivier JE, Burger HG, Bremner WJ, Soules MR 1989 The importance of luteinizing hormone in the control of inhibin and progesterone secretion by the human corpus luteum. J Clin Endocrinol Metab 68:1078-1085
53. Castellano JM, Gaytan M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E, Sanchez-Criado JE, Pellicer A, Pinilla L, Gaytan F, Tena-Sempere M 2006 Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology 147:4852-4862