The role of kisspeptin and RFamide-related peptide-3 neurones in the circadian-timed preovulatory luteinising hormone surge

Journal of Neuroendocrinology

Volumn 24, Issue 1, 2012, Pages 131-143

  Khan, A R ^a   Kauffman, A S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Clock; GnIH; GnRH; Kiss1; Kisspeptin; Ovulation; RFRP 3; SCN

Indexed keywords

ESTRADIOL; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE LIKE PEPTIDE; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE LIKE PEPTIDE 3; UNCLASSIFIED DRUG;

CIRCADIAN RHYTHM; GONADORELIN RELEASE; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; LUTEINIZING HORMONE RELEASE; NERVE CELL; NEUROANATOMY; NONHUMAN; OVULATION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CIRCADIAN RHYTHM; FEMALE; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; KISSPEPTINS; LUTEINIZING HORMONE; NEURONS; NEUROPEPTIDES; PITUITARY GLAND;

EID: 84055188823     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02162.x     Document Type: Review

References (169)

1. Moenter SM, Brand RC, Karsch FJ. Dynamics of gonadotropin-releasing hormone (GnRH) secretion during the GnRH surge: insights into the mechanism of GnRH surge induction. Endocrinology 1992; 130: 2978-2984.
2. Moenter SM, Caraty A, Karsch FJ. The estradiol-induced surge of gonadotropin-releasing hormone in the ewe. Endocrinology 1990; 127: 1375-1384.
3. Sarkar DK, Chiappa SA, Fink G, Sherwood NM. Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature 1976; 264: 461-463.
4. Freeman ME. The neuroendocrine control of the ovarian cycle of the rat. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. New York, NY: Raven Press Ltd, 1994: 613-658.
5. Goodman RL, Inskeep EK. Neuroendocrine control of the ovarian cycle of the sheep. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. New York, NY: Raven Press Ltd, 2006: 2389-2447.
6. Kauffman AS. Mammalian female sexual behavior and hormones. In: Breed MD, Moore J, eds. Encyclopedia of Animal Behavior. Oxford: Academic Press, 2010: 355-369.
7. Caligaris L, Astrada JJ, Taleisnik S. Release of luteinizing hormone induced by estrogen injection into ovariectomized rats. Endocrinology 1971; 88: 810-815.
8. Norman RL, Spies HG. Neural control of the estrogen-dependent twenty-four-hour periodicity of LH release in the golden hamster. Endocrinology 1974; 95: 1367-1372.
9. Legan SJ, Coon GA, Karsch FJ. Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 1975; 96: 50-56.
10. Klein DC, Moore RY, Reppert SM. Suprachiasmatic Nucleus: The Mind's Clock. New York, NY: Oxford University Press, 1991.
11. Schwartz WJ, Gainer H. Suprachiasmatic nucleus: use of 14C-labeled deoxyglucose uptake as a functional marker. Science 1977; 197: 1089-1091.
12. Shibata S, Oomura Y, Kita H, Hattori K. Circadian rhythmic changes of neuronal activity in the suprachiasmatic nucleus of the rat hypothalamic slice. Brain Res 1982; 247: 154-158.
13. Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, Sangoram AM, King DP, Pinto LH, Takahashi JS. Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 1997; 89: 655-667.
14. Rosewell KL, Siwicki KK, Wise PM. A period (per)-like protein exhibits daily rhythmicity in the suprachiasmatic nuclei of the rat. Brain Res 1994; 659: 231-236.
15. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ. Role of the CLOCK protein in the mammalian circadian mechanism. Science 1998; 280: 1564-1569.
16. Tei H, Okamura H, Shigeyoshi Y, Fukuhara C, Ozawa R, Hirose M, Sakaki Y. Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 1997; 389: 512-516.
17. Inouye ST, Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 1979; 76: 5962-5966.
18. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 1972; 42: 201-206.
19. Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 1972; 69: 1583-1586.
20. Rusak B, Zucker I. Neural regulation of circadian rhythms. Physiol Rev 1979; 59: 449-526.
21. Sawaki Y, Nihonmatsu I, Kawamura H. Transplantation of the neonatal suprachiasmatic nuclei into rats with complete bilateral suprachiasmatic lesions. Neurosci Res 1984; 1: 67-72.
22. Drucker-Colin R, Aguilar-Roblero R, Garcia-Hernandez F, Fernandez-Cancino F, Bermudez Rattoni F. Fetal suprachiasmatic nucleus transplants: diurnal rhythm recovery of lesioned rats. Brain Res 1984; 311: 353-357.
23. Lehman MN, Silver R, Gladstone WR, Kahn RM, Gibson M, Bittman EL. Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J Neurosci 1987; 7: 1626-1638.
24. Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990; 247: 975-978.
25. Green DJ, Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 1982; 245: 198-200.
26. Groos G, Hendriks J. Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neurosci Lett 1982; 34: 283-288.
27. Earnest DJ, Sladek CD. Circadian rhythms of vasopressin release from individual rat suprachiasmatic explants in vitro. Brain Res 1986; 382: 129-133.
28. Moore RY. The retinohypothalamic tract, suprachiasmatic hypothalamic nucleus and central neural mechanisms of circadian rhythm regulation. In: Suda M, Hayaishi O, Hakagawa H, eds. Biological Rhythms and their Central Mechanism. Amsterdam: Elsevier/North Holland, 1979: 343-354.
29. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 2006; 497: 326-349.
30. Abrahamson EE, Moore RY. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 2001; 916: 172-191.
31. Leak RK, Card JP, Moore RY. Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res 1999; 819: 23-32.
32. Welsh DK, Logothetis DE, Meister M, Reppert SM. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995; 14: 697-706.
33. Welsh DK, Takahashi JS, Kay SA. Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 2010; 72: 551-577.
34. Deurveilher S, Semba K. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 2005; 130: 165-183.
35. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002; 417: 405-410.
36. Antle MC, Silver R. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci 2005; 28: 145-151.
37. Card JP, Fitzpatrick-McElligott S, Gozes I, Baldino F Jr. Localization of vasopressin-, vasoactive intestinal polypeptide-, peptide histidine isoleucine- and somatostatin-mRNA in rat suprachiasmatic nucleus. Cell Tissue Res 1988; 252: 307-315.
38. Besson J, Sarrieau A, Vial M, Marie JC, Rosselin G, Rostene W. Characterization and autoradiographic distribution of vasoactive intestinal peptide binding sites in the rat central nervous system. Brain Res 1986; 398: 329-336.
39. Vertongen P, Schiffmann SN, Gourlet P, Robberecht P. Autoradiographic visualization of the receptor subclasses for vasoactive intestinal polypeptide (VIP) in rat brain. Ann NY Acad Sci 1998; 865: 412-415.
40. Shinohara K, Honma S, Katsuno Y, Honma K. Circadian release of excitatory amino acids in the suprachiasmatic nucleus culture is Ca(2+)-independent. Neurosci Res 2000; 36: 245-250.
41. Dardente H, Menet JS, Challet E, Tournier BB, Pevet P, Masson-Pevet M. Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res Mol Brain Res 2004; 124: 143-151.
42. Shinohara K, Funabashi T, Kimura F. Temporal profiles of vasoactive intestinal polypeptide precursor mRNA and its receptor mRNA in the rat suprachiasmatic nucleus. Brain Res Mol Brain Res 1999; 63: 262-267.
43. Vosko AM, Schroeder A, Loh DH, Colwell CS. Vasoactive intestinal peptide and the mammalian circadian system. Gen Comp Endocrinol 2007; 152: 165-175.
44. Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, Morrison CF, Dorin JR, Piggins HD, Reubi JC, Kelly JS, Maywood ES, Hastings MH. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 2002; 109: 497-508.
45. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, Hu Z, Liu X, Waschek JA. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol 2003; 285: R939-R949.
46. Reppert SM, Artman HG, Swaminathan S, Fisher DA. Vasopressin exhibits a rhythmic daily pattern in cerebrospinal fluid but not in blood. Science 1981; 213: 1256-1257.
47. Peterson GM, Watkins WB, Moore RY. The suprachiasmatic hypothalamic nuclei of the rat. VI. Vasopressin neurons and circadian rhythmicity. Behav Neural Biol 1980; 29: 236-245.
48. Groblewski TA, Nunez AA, Gold RM. Circadian rhythms in vasopressin deficient rats. Brain Res Bull 1981; 6: 125-130.
49. Shibata S, Moore RY. Electrical and metabolic activity of suprachiasmatic nucleus neurons in hamster hypothalamic slices. Brain Res 1988; 438: 374-378.
50. Liou SY, Albers HE. Single unit response of suprachiasmatic neurons to arginine vasopressin (AVP) is mediated by a V1-like receptor in the hamster. Brain Res 1989; 477: 336-343.
51. Mihai R, Coculescu M, Wakerley JB, Ingram CD. The effects of [Arg8]vasopressin and [Arg8]vasotocin on the firing rate of suprachiasmatic neurons in vitro. Neuroscience 1994; 62: 783-792.
52. Kalsbeek A, Buijs RM, van Heerikhuize JJ, Arts M, van der Woude TP. Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 1992; 580: 62-67.
53. Kalsbeek A, van Heerikhuize JJ, Wortel J, Buijs RM. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V1 antagonist. J Neurosci 1996; 16: 5555-5565.
54. Kalsbeek A, van der Vliet J, Buijs RM. Decrease of endogenous vasopressin release necessary for expression of the circadian rise in plasma corticosterone: a reverse microdialysis study. J Neuroendocrinol 1996; 8: 299-307.
55. Kalsbeek A, Verhagen LA, Schalij I, Foppen E, Saboureau M, Bothorel B, Buijs RM, Pevet P. Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur J Neurosci 2008; 27: 818-827.
56. Dai J, Swaab DF, Van der Vliet J, Buijs RM. Postmortem tracing reveals the organization of hypothalamic projections of the suprachiasmatic nucleus in the human brain. J Comp Neurol 1998; 400: 87-102.
57. Everett JW, Sawyer CH. A 24-hour periodicity in the 'LH-release apparatus' of female rats, disclosed by barbiturate sedation. Endocrinology 1950; 47: 198-218.
58. Everett JW, Sawyer CH, Markee JE. A neurogenic timing factor in control of the ovulatory discharge of luteinizing hormone in the cyclic rat. Endocrinology 1949; 44: 234-250.
59. Sawyer CH, Everett JW, Markee JE. A neural factor in the mechanism by which estrogen induces the release of luteinizing hormone in the rat. Endocrinology 1949; 44: 218-233.
60. Siegel HI, Bast JD, Greenwald GS. The effects of phenobarbital and gonadal steroids on periovulatory serum levels of luteinizing hormone and follicle-stimulating hormone in the hamster. Endocrinology 1976; 98: 48-55.
61. Stetson MH, Watson-Whitmyre M. The neural clock regulating estrous cyclicity in hamsters: gonadotropin release following barbiturate blockade. Biol Reprod 1977; 16: 536-542.
62. Legan SJ, Karsch FJ. A daily signal for the LH surge in the rat. Endocrinology 1975; 96: 57-62.
63. Norman RL, Blake CA, Sawyer CH. Estrogen-dependent 24-hour periodicity in pituitary LH release in the female hamster. Endocrinology 1973; 93: 965-970.
64. Tsukahara S. Increased Fos immunoreactivity in suprachiasmatic nucleus before luteinizing hormone surge in estrogen-treated ovariectomized female rats. Neuroendocrinology 2006; 83: 303-312.
65. Silver R, LeSauter J, Tresco PA, Lehman MN. A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 1996; 382: 810-813.
66. Stetson MH, Anderson PJ. Circadian pacemaker times gonadotropin release in free-running female hamsters. Am J Physiol 1980; 238: R23-R27.
67. Stetson MH, Gibson JT. The estrous cycle in golden hamsters: a circadian pacemaker times preovulatory gonadotropin release. J Exp Zool 1977; 201: 289-294.
68. Alleva JJ, Waleski MV, Alleva FR. A biological clock controlling the estrous cycle of the hamster. Endocrinology 1971; 88: 1368-1379.
69. Fitzgerald K, Zucker I. Circadian organization of the estrous cycle of the golden hamster. Proc Natl Acad Sci USA 1976; 73: 2923-2927.
70. Moline ML, Albers HE. Response of circadian locomotor activity and the proestrous luteinizing hormone surge to phase shifts of the light-dark cycle in the hamster. Physiol Behav 1988; 43: 435-440.
71. Lucas RJ, Stirland JA, Darrow JM, Menaker M, Loudon AS. Free running circadian rhythms of melatonin, luteinizing hormone, and cortisol in Syrian hamsters bearing the circadian tau mutation. Endocrinology 1999; 140: 758-764.
72. Brown-Grant K, Raisman G. Abnormalities in reproductive function associated with the destruction of the suprachiasmatic nuclei in female rats. Proc R Soc Lond B Biol Sci 1977; 198: 279-296.
73. Stetson MH, Watson-Whitmyre M. Nucleus suprachiasmaticus: the biological clock in the hamster? Science 1976; 191: 197-199.
74. Wiegand SJ, Terasawa E, Bridson WE, Goy RW. Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion. Neuroendocrinology 1980; 31: 147-157.
75. Miller BH, Olson SL, Turek FW, Levine JE, Horton TH, Takahashi JS. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol 2004; 14: 1367-1373.
76. de la Iglesia HO, Blaustein JD, Bittman EL. The suprachiasmatic area in the female hamster projects to neurons containing estrogen receptors and GnRH. Neuroreport 1995; 6: 1715-1722.
77. Kriegsfeld LJ, Leak RK, Yackulic CB, LeSauter J, Silver R. Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 2004; 468: 361-379.
78. Leak RK, Moore RY. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 2001; 433: 312-334.
79. Van der Beek EM, Horvath TL, Wiegant VM, Van den Hurk R, Buijs RM. Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol 1997; 384: 569-579.
80. Watson RE Jr, Langub MC Jr, Engle MG, Maley BE. Estrogen-receptive neurons in the anteroventral periventricular nucleus are synaptic targets of the suprachiasmatic nucleus and peri-suprachiasmatic region. Brain Res 1995; 689: 254-264.
81. Smith MJ, Jiennes L, Wise PM. Localization of the VIP2 receptor protein on GnRH neurons in the female rat. Endocrinology 2000; 141: 4317-4320.
82. Lee WS, Smith MS, Hoffman GE. Luteinizing hormone-releasing hormone neurons express Fos protein during the proestrous surge of luteinizing hormone. Proc Natl Acad Sci USA 1990; 87: 5163-5167.
83. van der Beek EM, van Oudheusden HJ, Buijs RM, van der Donk HA, van den Hurk R, Wiegant VM. Preferential induction of c-fos immunoreactivity in vasoactive intestinal polypeptide-innervated gonadotropin-releasing hormone neurons during a steroid-induced luteinizing hormone surge in the female rat. Endocrinology 1994; 134: 2636-2644.
84. Harney JP, Scarbrough K, Rosewell KL, Wise PM. In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology 1996; 137: 3696-3701.
85. Christian CA, Moenter SM. Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 2008; 149: 3130-3136.
86. Stack CM, Lim MA, Cuasay K, Stone MM, Seibert KM, Spivak-Pohis I, Crawley JN, Waschek JA, Hill JM. Deficits in social behavior and reversal learning are more prevalent in male offspring of VIP deficient female mice. Exp Neurol 2008; 211: 67-84.
87. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008; 57: 277-287.
88. Kalamatianos T, Kallo I, Goubillon ML, Coen CW. Cellular expression of V1a vasopressin receptor mRNA in the female rat preoptic area: effects of oestrogen. J Neuroendocrinol 2004; 16: 525-533.
89. Funabashi T, Shinohara K, Mitsushima D, Kimura F. Estrogen increases arginine-vasopressin V1a receptor mRNA in the preoptic area of young but not of middle-aged female rats. Neurosci Lett 2000; 285: 205-208.
90. Krajnak K, Kashon ML, Rosewell KL, Wise PM. Sex differences in the daily rhythm of vasoactive intestinal polypeptide but not arginine vasopressin messenger ribonucleic acid in the suprachiasmatic nuclei. Endocrinology 1998; 139: 4189-4196.
91. Palm IF, Van Der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A. Vasopressin induces a luteinizing hormone surge in ovariectomized, estradiol-treated rats with lesions of the suprachiasmatic nucleus. Neuroscience 1999; 93: 659-666.
92. Miller BH, Olson SL, Levine JE, Turek FW, Horton TH, Takahashi JS. Vasopressin regulation of the proestrous luteinizing hormone surge in wild-type and Clock mutant mice. Biol Reprod 2006; 75: 778-784.
93. Funabashi T, Aiba S, Sano A, Shinohara K, Kimura F. Intracerebroventricular injection of arginine-vasopressin V1 receptor antagonist attenuates the surge of luteinizing hormone and prolactin secretion in proestrous rats. Neurosci Lett 1999; 260: 37-40.
94. Boer K, Boer GJ, Swaab DF. Reproduction in Brattleboro rats with diabetes insipidus. J Reprod Fertil 1981; 61: 273-280.
95. Weick RF, Stobie KM. Vasoactive intestinal peptide inhibits the steroid-induced LH surge in the ovariectomized rat. J Endocrinol 1992; 133: 433-437.
96. Palm IF, van der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A. The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res 2001; 901: 109-116.
97. 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 USA 2003; 100: 10972-10976.
98. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, Day K, Leitch HG, Hendrick AG, Zahn D, Franceschini I, Caraty A, Carlton MB, Aparicio SA, Colledge WH. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci USA 2007; 104: 10714-10719.
99. Lapatto R, Pallais JC, Zhang D, Chan YM, Mahan A, Cerrato F, Le WW, Hoffman GE, Seminara SB. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology 2007; 148: 4927-4936.
100. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, 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 WF Jr, Aparicio SA, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627.
101. 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. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766.
102. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80: 264-272.
103. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
104. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005; 90: 6609-6615.
105. 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. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005; 146: 1689-1697.
106. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA, Rissman EF. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci 2007; 27: 8826-8835.
107. Dumalska I, Wu M, Morozova E, Liu R, van den Pol A, Alreja M. 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 2008; 28: 8003-8013.
108. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25: 11349-11356.
109. Pineda R, Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, Ruiz-Pino F, Morgan K, Pinilla L, Millar RP, Tena-Sempere M. Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 2010; 151: 722-730.
110. Smith JT, Li Q, Yap KS, Shahab M, Roseweir AK, Millar RP, Clarke IJ. Kisspeptin is essential for the full preovulatory LH surge and stimulates GnRH release from the isolated ovine median eminence. Endocrinology 2011; 152: 1001-1012.
111. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005; 146: 4431-4436.
112. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH, Herbison AE. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 2008; 28: 8691-8697.
113. Dungan HM, Gottsch ML, Zeng H, Gragerov A, Bergmann JE, Vassilatis DK, Clifton DK, Steiner RA. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J Neurosci 2007; 27: 12088-12095.
114. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006; 147: 5817-5825.
115. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007; 148: 1774-1783.
116. 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: 3686-3692.
117. Kim J, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, Kauffman AS. Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 2011; 152: 2020-2030.
118. Sim JA, Skynner MJ, Herbison AE. Direct regulation of postnatal GnRH neurons by the progesterone derivative allopregnanolone in the mouse. Endocrinology 2001; 142: 4448-4453.
119. Legan SJ, Tsai HW. Oestrogen receptor-alpha and -beta immunoreactivity in gonadotropin-releasing hormone neurones after ovariectomy and chronic exposure to oestradiol. J Neuroendocrinol 2003; 15: 1164-1170.
120. 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: 283-298.
121. Bloch GJ, Kurth SM, Akesson TR, Micevych PE. Estrogen-concentrating cells within cell groups of the medial preoptic area: sex differences and co-localization with galanin-immunoreactive cells. Brain Res 1992; 595: 301-308.
122. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M. Opposite roles of estrogen receptor (ER)-alpha and ERbeta in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 2008; 149: 1627-1637.
123. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G, Herbison AE. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006; 52: 271-280.
124. Ronnekleiv OK, Kelly MJ. Plasma prolactin and luteinizing hormone profiles during the estrous cycle of the female rat: effects of surgically induced persistent estrus. Neuroendocrinology 1988; 47: 133-141.
125. Wiegand SJ, Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 1982; 34: 395-404.
126. Goodman RL. The site of the positive feedback action of estradiol in the rat. Endocrinology 1978; 102: 151-159.
127. Kalra PS, McCann SM. The stimulatory effect on gonadotropin release of implants of estradiol or progesterone in certain sites in the central nervous system. Neuroendocrinology 1975; 19: 289-302.
128. Petersen SL, Barraclough CA. Suppression of spontaneous LH surges in estrogen-treated ovariectomized rats by microimplants of antiestrogens into the preoptic brain. Brain Res 1989; 484: 279-289.
129. Petersen SL, Cheuk C, Hartman RD, Barraclough CA. Medial preoptic microimplants of the antiestrogen, keoxifene, affect luteinizing hormone-releasing hormone mRNA levels, median eminence luteinizing hormone-releasing hormone concentrations and luteinizing hormone release in ovariectomized, estrogen-treated rats. J Neuroendocrinol 1989; 1: 279-283.
130. Le WW, Berghorn KA, Rassnick S, Hoffman GE. Periventricular preoptic area neurons coactivated with luteinizing hormone (LH)-releasing hormone (LHRH) neurons at the time of the LH surge are LHRH afferents. Endocrinology 1999; 140: 510-519.
131. 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. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007; 53: 367-378.
132. 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: 6687-6694.
133. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS. Circadian regulation of Kiss1 neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge. Endocrinology 2009; 150: 3664-3671.
134. Semaan SJ, Kauffman AS. Sexual differentiation and development of forebrain reproductive circuits. Curr Opin Neurobiol 2010; 20: 424-431.
135. Buhl AE, Norman RL, Resko JA. Sex differences in estrogen-induced gonadotropin release in hamsters. Biol Reprod 1978; 18: 592-597.
136. Homma T, Sakakibara M, Yamada S, Kinoshita M, Iwata K, Tomikawa J, Kanazawa T, Matsui H, Takatsu Y, Ohtaki T, Matsumoto H, Uenoyama Y, Maeda K, Tsukamura H. Significance of neonatal testicular sex steroids to defeminize anteroventral periventricular kisspeptin neurons and the GnRH/LH surge system in male rats. Biol Reprod 2009; 81: 1216-1225.
137. Kauffman AS. Sexual differentiation and the Kiss1 system: hormonal and developmental considerations. Peptides 2009; 30: 83-93.
138. Kauffman AS. Gonadal and nongonadal regulation of sex differences in hypothalamic Kiss1 neurones. J Neuroendocrinol 2010; 22: 682-691.
139. de la Iglesia HO, Blaustein JD, Bittman EL. Oestrogen receptor-alpha-immunoreactive neurones project to the suprachiasmatic nucleus of the female Syrian hamster. J Neuroendocrinol 1999; 11: 481-490.
140. Christian CA, Mobley JL, Moenter SM. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci USA 2005; 102: 15682-15687.
141. Williams WP 3rd, Jarjisian SG, Mikkelsen JD, Kriegsfeld LJ. Circadian control of kisspeptin and a gated GnRH response mediate the preovulatory luteinizing hormone surge. Endocrinology 2011; 152: 595-606.
142. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, Liposits Z, Kallo I. Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol 2010; 22: 1032-1039.
143. Zhao S, Kriegsfeld LJ. Daily changes in GT1-7 cell sensitivity to GnRH secretagogues that trigger ovulation. Neuroendocrinology 2009; 89: 448-457.
144. Hickok JR, Tischkau SA. In vivo circadian rhythms in gonadotropin-releasing hormone neurons. Neuroendocrinology 2010; 91: 110-120.
145. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M, Ghatei MA, Bloom SR. Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 2007; 92: 3958-3966.
146. Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez-Fernandez R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female Rat. Endocrinology 2006; 147: 2864-2878.
147. Ducret E, Gaidamaka G, Herbison AE. Electrical and morphological characteristics of anteroventral periventricular nucleus kisspeptin and other neurons in the female mouse. Endocrinology 2010; 151: 2223-2232.
148. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 2006; 103: 2410-2415.
149. Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC, Ubuka T, Iqbal J, Li Q, Tilbrook A, Morgan K, Pawson AJ, Tsutsui K, Millar RP, Bentley GE. Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 2008; 149: 5811-5821.
150. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N. Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol 2009; 36: 219-224.
151. Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology 2008; 149: 4958-4969.
152. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology 2009; 150: 2799-2804.
153. Wu M, Dumalska I, Morozova E, van den Pol AN, Alreja M. Gonadotropin inhibitory hormone inhibits basal forebrain vGluT2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J Physiol 2009; 587: 1401-1411.
154. Anderson GM, Relf HL, Rizwan MZ, Evans JJ. Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology 2009; 150: 1834-1840.
155. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort PI, Tena-Sempere M. Characterization of the potent gonadotropin-releasing activity of RF9, a selective antagonist of RF-amide-related peptides and neuropeptide FF receptors: physiological and pharmacological implications. Endocrinology 2010; 151: 1902-1913.
156. Molnar CS, Kallo I, Liposits Z, Hrabovszky E. Estradiol down-regulates RF-amide-related peptide (RFRP) expression in the mouse hypothalamus. Endocrinology 2011; 152: 1684-1690.
157. Quennell JH, Rizwan MZ, Relf HL, Anderson GM. Developmental and steroidogenic effects on the gene expression of RFamide related peptides and their receptor in the rat brain and pituitary gland. J Neuroendocrinol 2010; 22: 309-316.
158. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008; 149: 5770-5782.
159. Boulos Z, Morin LP. Entrainment of split circadian activity rhythms in hamsters. J Biol Rhythms 1985; 1: 1-15.
160. Pickard GE, Turek FW. Splitting of the circadian rhythm of activity is abolished by unilateral lesions of the suprachiasmatic nuclei. Science 1982; 215: 1119-1121.
161. Swann JM, Turek FW. Multiple circadian oscillators regulate the timing of behavioral and endocrine rhythms in female golden hamsters. Science 1985; 228: 898-900.
162. de la Iglesia HO, Meyer J, Schwartz WJ. Lateralization of circadian pacemaker output: activation of left- and right-sided luteinizing hormone-releasing hormone neurons involves a neural rather than a humoral pathway. J Neurosci 2003; 23: 7412-7414.
163. Maruyama T, Ohbuchi T, Fujihara H, Shibata M, Mori K, Murphy D, Dayanithi G, Ueta Y. Diurnal changes of arginine vasopressin-enhanced green fluorescent protein fusion transgene expression in the rat suprachiasmatic nucleus. Peptides 2010; 31: 2089-2093.
164. Krajnak K, Kashon ML, Rosewell KL, Wise PM. Aging alters the rhythmic expression of vasoactive intestinal polypeptide mRNA but not arginine vasopressin mRNA in the suprachiasmatic nuclei of female rats. J Neurosci 1998; 18: 4767-4774.
165. Kallo I, Kalamatianos T, Piggins HD, Coen CW. Ageing and the diurnal expression of mRNAs for vasoactive intestinal peptide and for the VPAC2 and PAC1 receptors in the suprachiasmatic nucleus of male rats. J Neuroendocrinol 2004; 16: 758-766.
166. Yambe Y, Arima H, Kakiya S, Murase T, Oiso Y. Diurnal changes in arginine vasopressin gene transcription in the rat suprachiasmatic nucleus. Brain Res Mol Brain Res 2002; 104: 132-136.
167. Gozes I, Werner H, Fawzi M, Abdelatty A, Shani Y, Fridkin M, Koch Y. Estrogen regulation of vasoactive intestinal peptide mRNA in rat hypothalamus. J Mol Neurosci 1989; 1: 55-61.
168. Doan A, Urbanski HF. Diurnal expression of Fos in luteinizing hormone-releasing hormone neurons of Syrian hamsters. Biol Reprod 1994; 50: 301-308.
169. Wu TJ, Segal AZ, Miller GM, Gibson MJ, Silverman AJ. FOS expression in gonadotropin-releasing hormone neurons: enhancement by steroid treatment and mating. Endocrinology 1992; 131: 2045-2050.