Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus

Brain Research

Volumn 1364, Issue , 2010, Pages 103-115

  Maeda, Kei Ichiro ^a   Ohkura, Satoshi ^a   Uenoyama, Yoshihisa ^a   Wakabayashi, Yoshihiro ^b   Oka, Yoshitaka ^c   Tsukamura, Hiroko ^a   Okamura, Hiroaki ^b  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Gonadotropin; GPR54; Kiss1; Kisspeptin; Multiple unit activity

Indexed keywords

ANDROGEN; ESTROGEN; FOLLITROPIN; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE;

ENVIRONMENTAL FACTOR; ESTROGEN RELEASE; FOLLITROPIN RELEASE; HYPOTHALAMUS; LUTEINIZING HORMONE RELEASE; MAMMAL; NEUROBIOLOGY; NONHUMAN; NUTRITION; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; PHOTOPERIODICITY; POSITIVE FEEDBACK; PRIORITY JOURNAL; REGULATORY MECHANISM; REPRODUCTION; REVIEW; SPERMATOGENESIS; STEROIDOGENESIS; STRESS;

ANIMALS; DYNORPHINS; ENVIRONMENT; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMUS; LUTEINIZING HORMONE; NEUROBIOLOGY; NEUROKININ B; NEURONS; STEROIDS; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 78649511376     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.10.026     Document Type: Review

References (149)

1. S. Adachi, S. Yamada, Y. Takatsu, H. Matsui, M. Kinoshita, K. Takase, H. Sugiura, T. Ohtaki, H. Matsumoto, Y. Uenoyama, H. Tsukamura, K. Inoue, and K. Maeda Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats J. Reprod. Dev. 53 2007 367 378 (Pubitemid 46743563)
2. T. Akema, Y. Tadokoro, and F. Kimura Regional specificity in the effect of estrogen implantation within the forebrain on the frequency of pulsatile luteinizing hormone secretion in the ovariectomized rat Neuroendocrinology 39 1984 517 523 (Pubitemid 15215704)
3. M. Amstalden, L.M. Coolen, A.M. Hemmerle, H.J. Billings, J.M. Connors, R.L. Goodman, and M.N. Lehman Neurokinin 3 receptor immunoreactivity in the septal region, preoptic area and hypothalamus of the female sheep: colocalisation in neurokinin B cells of the arcuate nucleus but not in gonadotrophin-releasing hormone neurones J. Neuroendocrinol. 22 2010 1 12
4. H.J. Billings, J.M. Connors, S.N. Altman, S.M. Hileman, I. Holaskova, M.N. Lehman, C.J. McManus, C.C. Nestor, B.H. Jacobs, and R.L. Goodman Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep Endocrinology 151 2010 3836 3846
5. C.A. Blake, and C.H. Sawyer Effects of hypothalamic deafferentation on the pulsatile rhythm in plasma concentrations of luteinizing hormone in ovariectomized rats Endocrinology 94 1974 730 736
6. C.H. Brown, J.A. Russell, and G. Leng Opioid modulation of magnocellular neurosecretory cell activity Neurosci. Res. 36 2000 97 120 (Pubitemid 30072727)
7. M.C. Burke, P.A. Letts, S.J. Krajewski, and N.E. Rance Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus J. Comp. Neurol. 498 2006 712 726
8. W.R. Butler, P.V. Malven, L.B. Willett, and D.J. Bolt Patterns of pituitary release and cranial output of LH and prolactin in ovariectomized ewes Endocrinology 91 1972 793 801
9. F.R. Cagampang, K.I. Maeda, H. Tsukamura, S. Ohkura, and K. Ota Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats J. Endocrinol. 129 1991 321 328
10. R.E. Campbell, G. Gaidamaka, S.K. Han, and A.E. Herbison Dendro-dendritic bundling and shared synapses between gonadotropin-releasing hormone neurons Proc. Natl. Acad. Sci. U. S. A. 106 2009 10835 10840
11. A. Caraty, C. Fabre-Nys, B. Delaleu, A. Locatelli, G. Bruneau, F.J. Karsch, and A. Herbison 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 139 1998 1752 1760 (Pubitemid 28513834)
12. Z. Chu, J. Andrade, M.A. Shupnik, and S.M. Moenter Differential regulation of gonadotropin-releasing hormone neuron activity and membrane properties by acutely applied estradiol: dependence on dose and estrogen receptor subtype J. Neurosci. 29 2009 5616 5627
13. I.J. Clarke, and J.T. Cummins The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes Endocrinology 111 1982 1737 1739
14. J. Clarkson, and A.E. Herbison Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons Endocrinology 147 2006 5817 5825 (Pubitemid 44833498)
15. J.A. Colombo, D.I. Whitmoyer, and C.H. Sawyer Local changes in multiple unit activity induced by electrochemical means in preoptic and hypothalamic areas in the female rat Brain Res. 71 1974 35 45
16. N. de Roux, E. Genin, J.C. Carel, F. Matsuda, J.L. Chaussain, and E. Milgrom Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54 Proc. Natl. Acad. Sci. U. S. A. 100 2003 10972 10976 (Pubitemid 37140137)
17. D.J. Dierschke, A.N. Bhattacharya, L.E. Atkinson, and E. Knobil Circhoral oscillations of plasma LH levels in the ovariectomized rhesus monkey Endocrinology 87 1970 850 853
18. B.T. Donovan, M.B. Haar, and N. Parvizi Gonadotrophin secretion in the ovariectomized guinea-pig: effects of electrical stimulation of the hypothalamus and of LH-RH J. Physiol. 265 1977 597 613 (Pubitemid 8056773)
19. E. Ducret, G. Gaidamaka, and A.E. Herbison Electrical and morphological characteristics of anteroventral periventricular nucleus kisspeptin and other neurons in the female mouse Endocrinology 151 2010 2223 2232
20. A.H. Duittoz, and M. Batailler Pulsatile GnRH secretion from primary cultures of sheep olfactory placode explants J. Reprod. Fertil. 120 2000 391 396
21. H.M. Dungan, M.L. Gottsch, H. Zeng, A. Gragerov, J.E. Bergmann, D.K. Vassilatis, D.K. Clifton, and R.A. Steiner The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone J. Neurosci. 27 2007 12088 12095 (Pubitemid 350072118)
22. G. Emons, O. Ortmann, S. Thiessen, and R. Knuppen Effects of estradiol and some antiestrogens (clomiphene, tamoxifen, and hydroxytamoxifen) on luteinizing hormone secretion by rat pituitary cells in culture Arch. Gynecol. 237 1986 199 211 (Pubitemid 16162280)
23. B.P. Fitzgerald, H. I'Anson, R.G. Loy, and S.J. Legan Evidence that changes in LH pulse frequency may regulate the seasonal modulation of LH secretion in ovariectomized mares J. Reprod. Fertil. 69 1983 685 692 (Pubitemid 13021976)
24. C.D. Foradori, R.L. Goodman, V.L. Adams, M. Valent, and M.N. Lehman Progesterone increases dynorphin A concentrations in cerebrospinal fluid and preprodynorphin messenger ribonucleic acid levels in a subset of dynorphin neurons in the sheep Endocrinology 146 2005 1835 1842 (Pubitemid 40396893)
25. C.D. Foradori, M. Amstalden, R.L. Goodman, and M.N. Lehman Colocalisation of dynorphin A and neurokinin B immunoreactivity in the arcuate nucleus and median eminence of the sheep J. Neuroendocrinol. 18 2006 534 541 (Pubitemid 43821725)
26. D.L. Foster, and L.M. Jackson Puberty in the sheep J.D. Neill, Knobil and Neill's Physiology of Reproduction Vol. 2 2005 Academic Press St. Louis, MO 2127 2176
27. I. Franceschini, D. Lomet, M. Cateau, G. Delsol, Y. Tillet, and A. Caraty Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha Neurosci. Lett. 401 2006 225 230 (Pubitemid 43729526)
28. T. Funabashi, K. Jinnai, and F. Kimura Fos expression by naloxone in LHRH neurons of the mediobasal hypothalamus and effects of pentobarbital sodium in the proestrous rat J. Neuroendocrinol. 9 1997 87 92 (Pubitemid 27060113)
29. R.V. Gallo Pulsatile LH release during periods of low level LH secretion in the rat estrous cycle Biol. Reprod. 24 1981 771 777
30. R.V. Gallo Pulsatile LH release during the ovulatory LH surge on proestrus in the rat Biol. Reprod. 24 1981 100 104 (Pubitemid 11144786)
31. R.V. Gallo Kappa-opioid receptor involvement in the regulation of pulsatile luteinizing hormone release during early pregnancy in the rat J. Neuroendocrinol. 2 1990 685 691
32. V.L. Gay, and N.A. Sheth Evidence for a periodic release of LH in castrated male and female rats Endocrinology 90 1972 158 162
33. M. Giri, and J.M. Kaufman In vitro GnRH release from the isolated medial basal hypothalamus of the male guinea pig: evidence for the existence of two pools of releasable GnRH Brain Res. 648 1994 270 280 (Pubitemid 24186926)
34. R.L. Goodman, E.L. Bittman, D.L. Foster, and F.J. Karsch The endocrine basis of the synergistic suppression of luteinizing hormone by estradiol and progesterone Endocrinology 109 1981 1414 1417
35. R.L. Goodman, L.M. Coolen, G.M. Anderson, S.L. Hardy, M. Valent, J.M. Connors, M.E. Fitzgerald, and M.N. Lehman Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin-releasing hormone neurons in sheep Endocrinology 145 2004 2959 2967 (Pubitemid 38686245)
36. R.L. Goodman, M.N. Lehman, J.T. Smith, L.M. Coolen, C.V. de Oliveira, M.R. Jafarzadehshirazi, A. Pereira, J. Iqbal, A. Caraty, P. Ciofi, and I.J. Clarke Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B Endocrinology 148 2007 5752 5760 (Pubitemid 350146171)
37. A. Gorbman, and S.A. Sower Evolution of the role of GnRH in animal (Metazoan) biology Gen. Comp. Endocrinol. 134 2003 207 213 (Pubitemid 37443475)
38. B. Halasz, and L. Pupp Hormone secretion of the anterior pituitary gland after physical interruption of all nervous pathways to the hypophysiotrophic area Endocrinology 77 1965 553 562
39. J.E. Hall, A.E. Taylor, K.A. Martin, J. Rivier, D.A. Schoenfeld, and W.F. Crowley Jr. Decreased release of gonadotropin-releasing hormone during the preovulatory midcycle luteinizing hormone surge in normal women Proc. Natl. Acad. Sci. U. S. A. 91 1994 6894 6898 (Pubitemid 24226768)
40. T. Hamada, T. Shimizu, M. Ichikawa, and Y. Mori Immunohistochemical study on gonadotropin-releasing hormone neurons in the Shiba goat brain J. Reprod. Dev. 38 1992 133 142
41. G.W. Harris Neural control of the pituitary gland Physiol. Rev. 28 1948 139 179
42. A.E. Herbison Multimodal influence of estrogen upon gonadotropin- releasing hormone neurons Endocr. Rev. 19 1998 302 330
43. A.E. Herbison, X. de Tassigny, J. Doran, and W.H. Colledge Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons Endocrinology 151 2010 312 321
44. E. Hrabovszky, A. Steinhauser, K. Barabas, P.J. Shughrue, S.L. Petersen, I. Merchenthaler, and Z. Liposits Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain Endocrinology 142 2001 3261 3264 (Pubitemid 32575565)
45. K.J. Iremonger, and J.S. Bains Retrograde opioid signaling regulates glutamatergic transmission in the hypothalamus J. Neurosci. 29 2009 7349 7358
46. M. Jung, J.C. Michaud, R. Steinberg, M.C. Barnouin, A. Hayar, G. Mons, J. Souilhac, X. Emonds-Alt, P. Soubrie, and G. Le Fur Electrophysiological, behavioural and biochemical evidence for activation of brain noradrenergic systems following neurokinin NK3 receptor stimulation Neuroscience 74 1996 403 414 (Pubitemid 26274211)
47. F.J. Karsch, E.L. Bittman, D.L. Foster, R.L. Goodman, S.J. Legan, and J.E. Robinson Neuroendocrine basis of seasonal reproduction Recent Prog. Horm. Res. 40 1984 185 232
48. M. Kawakami, E. Terasawa, and T. Ibuki Changes in multiple unit activity of the brain during the estrous cycle Neuroendocrinology 6 1970 30 48
49. M. Kawakami, T. Uemura, and R. Hayashi Electrophysiological correlates of pulsatile gonadotropin release in rats Neuroendocrinology 35 1982 63 67 (Pubitemid 12125937)
50. H. Kawano, and S. Daikoku Immunohistochemical demonstration of LHRH neurons and their pathways in the rat hypothalamus Neuroendocrinology 32 1981 179 186 (Pubitemid 11141938)
51. K.L. Keen, F.H. Wegner, S.R. Bloom, M.A. Ghatei, and E. Terasawa An increase in kisspeptin-54 release occurs with the pubertal increase in luteinizing hormone-releasing hormone-1 release in the stalk-median eminence of female rhesus monkeys in vivo Endocrinology 149 2008 4151 4157
52. M.J. Kelly, J. Qiu, and O.K. Ronnekleiv Estrogen modulation of G-protein-coupled receptor activation of potassium channels in the central nervous system Ann. N. Y. Acad. Sci. 1007 2003 6 16 (Pubitemid 38253650)
53. M. Kinoshita, H. Tsukamura, S. Adachi, H. Matsui, Y. Uenoyama, K. Iwata, S. Yamada, K. Inoue, T. Ohtaki, H. Matsumoto, and K. Maeda Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats Endocrinology 146 2005 4431 4436 (Pubitemid 41324041)
54. J.S. Kinsey-Jones, X.F. Li, S.M. Luckman, and K.T. O'Byrne Effects of kisspeptin-10 on the electrophysiological manifestation of gonadotropin- releasing hormone pulse generator activity in the female rat Endocrinology 149 2008 1004 1008
55. J.S. Kinsey-Jones, X.F. Li, A.M. Knox, E.S. Wilkinson, X.L. Zhu, A.A. Chaudhary, S.R. Milligan, S.L. Lightman, and K.T. O'Byrne Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinising hormone secretion in the female rat J. Neuroendocrinol. 21 2009 20 29
56. E. Knobil The neuroendocrine control of the menstrual cycle Recent Prog. Horm. Res. 36 1980 53 88
57. E. Knobil Patterns of hypophysiotropic signals and gonadotropin secretion in the rhesus monkey Biol. Reprod. 24 1981 44 49 (Pubitemid 11144783)
58. E. Knobil, T.M. Plant, L. Wildt, P.E. Belchetz, and G. Marshall Control of the rhesus monkey menstrual cycle: permissive role of hypothalamic gonadotropin-releasing hormone Science 207 1980 1371 1373 (Pubitemid 10111130)
59. M. Kotani, M. Detheux, A. Vandenbogaerde, D. Communi, J.M. Vanderwinden, E. Le Poul, S. Brezillon, R. Tyldesley, N. Suarez-Huerta, F. Vandeput, C. Blanpain, S.N. Schiffmann, G. Vassart, and M. Parmentier The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54 J. Biol. Chem. 276 2001 34631 34636 (Pubitemid 37384458)
60. S.J. Krajewski, M.C. Burke, M.J. Anderson, N.T. McMullen, and N.E. Rance Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat Neuroscience 166 2010 680 697
61. J.H. Krege, J.B. Hodgin, J.F. Couse, E. Enmark, M. Warner, J.F. Mahler, M. Sar, K.S. Korach, J.A. Gustafsson, and O. Smithies Generation and reproductive phenotypes of mice lacking estrogen receptor beta Proc. Natl. Acad. Sci. U. S. A. 95 1998 15677 15682 (Pubitemid 29018759)
62. L.C. Krey, W.R. Butler, and E. Knobil Surgical disconnection of the medial basal hypothalamus and pituitary function in the rhesus monkey. I. Gonadotropin secretion Endocrinology 96 1975 1073 1087
63. L.Z. Krsmanovic, S.S. Stojilkovic, F. Merelli, S.M. Dufour, M.A. Virmani, and K.J. Catt Calcium signaling and episodic secretion of gonadotropin- releasing hormone in hypothalamic neurons Proc. Natl. Acad. Sci. U. S. A. 89 1992 8462 8466
64. T.T. Kung, Y. Crawley, H. Jones, B. Luo, H. Gilchrest, S. Greenfeder, J.C. Anthes, S. Lira, M. Wiekowski, D.N. Cook, J.A. Hey, R.W. Egan, and R.W. Chapman Tachykinin NK3-receptor deficiency does not inhibit pulmonary eosinophilia in allergic mice Pharmacol. Res. 50 2004 611 615 (Pubitemid 39388972)
65. J.H. Lee, M.E. Miele, D.J. Hicks, K.K. Phillips, J.M. Trent, B.E. Weissman, and D.R. Welch KiSS-1, a novel human malignant melanoma metastasis-suppressor gene J. Natl. Cancer Inst. 88 1996 1731 1737
66. M.N. Lehman, J.E. Robinson, F.J. Karsch, and A.J. Silverman Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) pathways in the sheep brain during anestrus and the mid-luteal phase of the estrous cycle J. Comp. Neurol. 244 1986 19 35
67. M.N. Lehman, L.M. Coolen, and R.L. Goodman Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion Endocrinology 151 2010 3479 3489
68. J.E. Levine Pulsatility in primates-a perspective from the placode Endocrinology 140 1999 1033 1035
69. X.F. Li, J.S. Kinsey-Jones, Y. Cheng, A.M. Knox, Y. Lin, N.A. Petrou, A. Roseweir, S.L. Lightman, S.R. Milligan, R.P. Millar, and K.T. O'Byrne Kisspeptin signalling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat PLoS One 4 2009 e8334
70. G.A. Lincoln, and R.V. Short Seasonal breeding: nature's contraceptive Recent Prog. Horm. Res. 36 1980 1 52
71. D.B. Lubahn, J.S. Moyer, T.S. Golding, J.F. Couse, K.S. Korach, and O. Smithies Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene Proc. Natl. Acad. Sci. U. S. A. 90 1993 11162 11166 (Pubitemid 23354389)
72. K. Maeda, S. Adachi, K. Inoue, S. Ohkura, and H. Tsukamura Metastin/kisspeptin and control of estrous cycle in rats Rev. Endocr. Metab. Disord. 8 2007 21 29 (Pubitemid 46536849)
73. K.A. Martin, C.K. Welt, A.E. Taylor, J.A. Smith, W.F. Crowley Jr., and J.E. Hall Is GnRH reduced at the midcycle surge in the human? Evidence from a GnRH-deficient model Neuroendocrinology 67 1998 363 369
74. G. Martinez de la Escalera, A.L. Choi, and R.I. Weiner Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: intrinsic properties of the GT1-1 GnRH neuronal cell line Proc. Natl. Acad. Sci. U. S. A. 89 1992 1852 1855
75. E.L. Marut, R.F. Williams, B.D. Cowan, A. Lynch, S.P. Lerner, and G.D. Hodgen Pulsatile pituitary gonadotropin secretion during maturation of the dominant follicle in monkeys: estrogen positive feedback enhances the biological activity of LH Endocrinology 109 1981 2270 2272
76. A. Matsumoto, S. Murakami, Y. Arai, and I. Nagatsu Ultrastructural and immunohistochemical analysis of fetal mediobasal hypothalamic tissue transplanted into the aged rat brain Ann. N. Y. Acad. Sci. 495 1987 404 414
77. M.A. McDevitt, C. Glidewell-Kenney, M.A. Jimenez, P.C. Ahearn, J. Weiss, J.L. Jameson, and J.E. Levine New insights into the classical and non-classical actions of estrogen: evidence from estrogen receptor knock-out and knock-in mice Mol. Cell. Endocrinol. 290 2008 24 30
78. P.L. Mellon, J.J. Windle, P.C. Goldsmith, C.A. Padula, J.L. Roberts, and R.I. Weiner Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis Neuron 5 1990 1 10
79. S.M. Moenter, R.C. Brand, and F.J. Karsch Dynamics of gonadotropin-releasing hormone (GnRH) secretion during the GnRH surge: insights into the mechanism of GnRH surge induction Endocrinology 130 1992 2978 2984
80. S.M. Moenter, R.M. Brand, A.R. Midgley, and F.J. Karsch Dynamics of gonadotropin-releasing hormone release during a pulse Endocrinology 130 1992 503 510
81. S.M. Moenter, A.R. DeFazio, G.R. Pitts, and C.S. Nunemaker Mechanisms underlying episodic gonadotropin-releasing hormone secretion Front. Neuroendocrinol. 24 2003 79 93
82. K. Morgan, and R.P. Millar Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species Gen. Comp. Endocrinol. 139 2004 191 197 (Pubitemid 39550345)
83. Y. Mori, M. Nishihara, T. Tanaka, T. Shimizu, M. Yamaguchi, Y. Takeuchi, and K. Hoshino Chronic recording of electrophysiological manifestation of the hypothalamic gonadotropin-releasing hormone pulse generator activity in the goat Neuroendocrinology 53 1991 392 395
84. Y. Nakai, T.M. Plant, D.L. Hess, E.J. Keogh, and E. Knobil On the sites of the negative and positive feedback actions of estradiol in the control of gonadotropin secretion in the rhesus monkey Endocrinology 102 1978 1008 1014 (Pubitemid 8317832)
85. E. Nalivaiko, J.C. Michaud, P. Soubrie, G. Le Fur, and P. Feltz Tachykinin neurokinin-1 and neurokinin-3 receptor-mediated responses in guinea-pig substantia nigra: an in vitro electrophysiological study Neuroscience 78 1997 745 757 (Pubitemid 27179656)
86. V.M. Navarro, J.M. Castellano, R. Fernandez-Fernandez, M.L. Barreiro, J. Roa, J.E. Sanchez-Criado, E. Aguilar, C. Dieguez, L. Pinilla, and M. Tena-Sempere 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 2004 4565 4574 (Pubitemid 39281449)
87. V.M. Navarro, M.L. Gottsch, C. Chavkin, H. Okamura, D.K. Clifton, and R.A. Steiner Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse J. Neurosci. 29 2009 11859 11866
88. M. Nishihara, H. Hiruma, and F. Kimura Interactions between the noradrenergic and opioid peptidergic systems in controlling the electrical activity of luteinizing hormone-releasing hormone pulse generator in ovariectomized rats Neuroendocrinology 54 1991 321 326
89. M. Nishihara, Y. Takeuchi, T. Tanaka, and Y. Mori Electrophysiological correlates of pulsatile and surge gonadotrophin secretion Rev. Reprod. 4 1999 110 116 (Pubitemid 29245935)
90. S.D. Noel, K.L. Keen, D.I. Baumann, E.J. Filardo, and E. Terasawa Involvement of G protein-coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons Mol. Endocrinol. 23 2009 349 359
91. R.L. Norman, S.A. Lindstrom, D. Bangsberg, W.E. Ellinwood, P. Gliessman, and H.G. Spies Pulsatile secretion of luteinizing hormone during the menstrual cycle of rhesus macaques Endocrinology 115 1984 261 266 (Pubitemid 14086820)
92. A.E. Oakley, D.K. Clifton, and R.A. Steiner Kisspeptin signaling in the brain Endocr. Rev. 30 2009 713 743
93. K.T. O'Byrne, and E. Knobil Electrophysiological approaches to gonadotrophin releasing hormone pulse generator activity in the rhesus monkey Hum. Reprod. 8 Suppl 2 1993 37 40 (Pubitemid 23337175)
94. K.T. O'Byrne, J.C. Thalabard, P.M. Grosser, R.C. Wilson, C.L. Williams, M.D. Chen, D. Ladendorf, J. Hotchkiss, and E. Knobil Radiotelemetric monitoring of hypothalamic gonadotropin-releasing hormone pulse generator activity throughout the menstrual cycle of the rhesus monkey Endocrinology 129 1991 1207 1214
95. S. Ohkura, H. Tsukamura, and K. Maeda Effects of various types of hypothalamic deafferentation on luteinizing hormone pulses in ovariectomized rats J. Neuroendocrinol. 3 1991 503 508
96. S. Ohkura, H. Tsukamura, and K. Maeda Effects of transplants of fetal mediobasal hypothalamus on luteinizing hormone pulses impaired by hypothalamic deafferentation in adult ovariectomized rats Neuroendocrinology 55 1992 422 426
97. S. Ohkura, K. Takase, S. Matsuyama, K. Mogi, T. Ichimaru, Y. Wakabayashi, Y. Uenoyama, Y. Mori, R.A. Steiner, H. Tsukamura, K.I. Maeda, and H. Okamura Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat J. Neuroendocrinol. 21 2009 813 821
98. S. Ohkura, Y. Uenoyama, S. Yamada, T. Homma, K. Takase, N. Inoue, K. Maeda, and H. Tsukamura Physiological role of metastin/kisspeptin in regulating gonadotropin-releasing hormone (GnRH) secretion in female rats Peptides 30 2009 49 56
99. T. Ohtaki, Y. Shintani, S. Honda, H. Matsumoto, A. Hori, K. Kanehashi, Y. Terao, S. Kumano, Y. Takatsu, Y. Masuda, Y. Ishibashi, T. Watanabe, M. Asada, T. Yamada, M. Suenaga, C. Kitada, S. Usuki, T. Kurokawa, H. Onda, O. Nishimura, and M. Fujino Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor Nature 411 2001 613 617 (Pubitemid 32531412)
100. K. Okubo, and Y. Nagahama Structural and functional evolution of gonadotropin-releasing hormone in vertebrates Acta Physiol. (Oxf.) 193 2008 3 15 (Pubitemid 351490265)
101. D. Pillon, A. Caraty, C. Fabre-Nys, and G. Bruneau Short-term effect of oestradiol on neurokinin B mRNA expression in the infundibular nucleus of ewes J. Neuroendocrinol. 15 2003 749 753 (Pubitemid 36874371)
102. T.M. Plant, L.C. Krey, J. Moossy, J.T. McCormack, D.L. Hess, and E. Knobil The arcuate nucleus and the control of gonadotropin and prolactin secretion in the female rhesus monkey (Macaca mulatta) Endocrinology 102 1978 52 62 (Pubitemid 8277609)
103. C.R. Pohl, D.W. Richardson, J.S. Hutchison, J.A. Germak, and E. Knobil Hypophysiotropic signal frequency and the functioning of the pituitary-ovarian system in the rhesus monkey Endocrinology 112 1983 2076 2080
104. J.C. Porter, R.S. Mical, I.A. Kamberi, and Y.R. Grazia A procedure for the cannulation of a pituitary stalk portal vessel and perfusion of the pars distalis in the rat Endocrinology 87 1970 197 201
105. C.H. Rahe, R.E. Owens, J.L. Fleeger, H.J. Newton, and P.G. Harms Pattern of plasma luteinizing hormone in the cyclic cow: dependence upon the period of the cycle Endocrinology 107 1980 498 503
106. S. Ramaswamy, K.A. Guerriero, R.B. Gibbs, and T.M. Plant Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy Endocrinology 149 2008 4387 4395
107. S. Ramaswamy, S.B. Seminara, B. Ali, P. Ciofi, N.A. Amin, and T.M. Plant Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus Endocrinology 151 2010 4494 4503
108. N.E. Rance Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback Peptides 30 2009 111 122
109. N.E. Rance, and T.R. Bruce Neurokinin B gene expression is increased in the arcuate nucleus of ovariectomized rats Neuroendocrinology 60 1994 337 345 (Pubitemid 24284817)
110. A.K. Roseweir, A.S. Kauffman, J.T. Smith, K.A. Guerriero, K. Morgan, J. Pielecka-Fortuna, R. Pineda, M.L. Gottsch, M. Tena-Sempere, S.M. Moenter, E. Terasawa, I.J. Clarke, R.A. Steiner, and R.P. Millar Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation J. Neurosci. 29 2009 3920 3929
111. R. Sadja, N. Alagem, and E. Reuveny Gating of GIRK channels: details of an intricate, membrane-delimited signaling complex Neuron 39 2003 9 12 (Pubitemid 36830944)
112. S. Safe, and K. Kim Non-classical genomic estrogen receptor (ER)/specificity protein and ER/activating protein-1 signaling pathways J. Mol. Endocrinol. 41 2008 263 275
113. T. Sandoval-Guzman, and N.E. Rance Central injection of senktide, an NK3 receptor agonist, or neuropeptide Y inhibits LH secretion and induces different patterns of Fos expression in the rat hypothalamus Brain Res. 1026 2004 307 312 (Pubitemid 39361561)
114. D.K. Sarkar, and G. Fink Effects of gonadal steroids on output of luteinizing hormone releasing factor into pituitary stalk blood in the female rat J. Endocrinol. 80 1979 303 313 (Pubitemid 9142287)
115. D.K. Sarkar, S.A. Chiappa, G. Fink, and N.M. Sherwood Gonadotropin-releasing hormone surge in pro-oestrous rats Nature 264 1976 461 463
116. H.B. Sarnat The discovery, proof and reproof of neurosecretion (Speidel, 1917; Scharrer and Scharrer, 1934) Can. J. Neurol. Sci. 10 1983 208 212
117. C.H. Sawyer, and M. Kawakami Characteristics of behavioral and electroencephalographic after-reactions to copulation and vaginal stimulation in the female rabbit Endocrinology 65 1959 622 630
118. S.B. Seminara, S. Messager, E.E. Chatzidaki, R.R. Thresher, J.S. Acierno Jr., J.K. Shagoury, Y. Bo-Abbas, W. Kuohung, K.M. Schwinof, A.G. Hendrick, D. Zahn, J. Dixon, U.B. Kaiser, S.A. Slaugenhaupt, J.F. Gusella, S. O'Rahilly, M.B. Carlton, W.F. Crowley Jr., S.A. Aparicio, and W.H. Colledge The GPR54 gene as a regulator of puberty N. Engl. J. Med. 349 2003 1614 1627 (Pubitemid 37303886)
119. G. Setalo, S. Vigh, A.V. Schally, A. Arimura, and B. Flerko Immunohistological study of the origin of LH-RH-containing nerve fibers of the rat hypothalamus Brain Res. 103 1976 597 602
120. W.J. Sheward, A.J. Harmar, and G. Fink LH-RH in the rat and mouse hypothalamus and rat hypophysial portal blood: confirmation of identity by high performance liquid chromatography Brain Res. 345 1985 362 365 (Pubitemid 16217090)
121. A.J. Silverman, J.L. Antunes, M. Ferin, and E.A. Zimmerman The distribution of luteinizing hormone-releasing hormone (LHRH) in the hypothalamus of the rhesus monkey. Light microscopic studies using immunoperoxidase technique Endocrinology 101 1977 134 142 (Pubitemid 8141315)
122. A.J. Silverman, J. Jhamandas, and L.P. Renaud Localization of luteinizing hormone-releasing hormone (LHRH) neurons that project to the median eminence J. Neurosci. 7 1987 2312 2319
123. J.T. Smith, M.J. Cunningham, E.F. Rissman, D.K. Clifton, and R.A. Steiner Regulation of Kiss1 gene expression in the brain of the female mouse Endocrinology 146 2005 3686 3692 (Pubitemid 41175732)
124. J.T. Smith, H.M. Dungan, E.A. Stoll, M.L. Gottsch, R.E. Braun, S.M. Eacker, D.K. Clifton, and R.A. Steiner Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse Endocrinology 146 2005 2976 2984
125. J.T. Smith, C.M. Clay, A. Caraty, and I.J. Clarke KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season Endocrinology 148 2007 1150 1157 (Pubitemid 46272806)
126. J.T. Smith, Q. Li, A. Pereira, and I.J. Clarke Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge Endocrinology 150 2009 5530 5538
127. J.T. Smith, M. Shahab, A. Pereira, K.Y. Pau, and I.J. Clarke Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate Biol. Reprod. 83 2010 568 577
128. M.J. Sollenberger, E.C. Carlsen, M.L. Johnson, J.D. Veldhuis, and W.S. Evans Specific physiological regulation of luteinizing hormone secretory events throughout the human menstrual cycle: new insights into the pulsatile mode of gonadotropin release J. Neuroendocrinol. 2 1990 845 852
129. J. Sun, Z. Chu, and S.M. Moenter Diurnal in vivo and rapid in vitro effects of estradiol on voltage-gated calcium channels in gonadotropin-releasing hormone neurons J. Neurosci. 30 2010 3912 3923
130. K. Takase, Y. Uenoyama, N. Inoue, H. Matsui, S. Yamada, M. Shimizu, T. Homma, J. Tomikawa, S. Kanda, H. Matsumoto, Y. Oka, H. Tsukamura, and K.I. Maeda Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats J. Neuroendocrinol. 21 2009 527 537
131. T. Tanaka, Y. Mori, and K. Hoshino Hypothalamic GnRH pulse generator activity during the estradiol-induced LH surge in ovariectomized goats Neuroendocrinology 56 1992 641 645 (Pubitemid 23033824)
132. T. Tanaka, T. Ozawa, K. Hoshino, and Y. Mori Changes in the gonadotropin-releasing hormone pulse generator activity during the estrous cycle in the goat Neuroendocrinology 62 1995 553 561
133. M. Tena-Sempere GPR54 and kisspeptin in reproduction Hum. Reprod. Update 12 2006 631 639 (Pubitemid 44288712)
134. E. Terasawa, K.L. Keen, K. Mogi, and P. Claude Pulsatile release of luteinizing hormone-releasing hormone (LHRH) in cultured LHRH neurons derived from the embryonic olfactory placode of the rhesus monkey Endocrinology 140 1999 1432 1441 (Pubitemid 29104250)
135. 2+ oscillations in luteinizing hormone-releasing hormone neurons derived from the embryonic olfactory placode of the rhesus monkey J. Neurosci. 19 1999 5898 5909 (Pubitemid 29327925)
136. D.T. Theodosis, and D.A. Poulain Evidence for structural plasticity in the supraoptic nucleus of the rat hypothalamus in relation to gestation and lactation Neuroscience 11 1984 183 193
137. D.T. Theodosis, F.B. Wooding, E.L. Sheldrick, and A.P. Flint Ultrastructural localisation of oxytocin and neurophysin in the ovine corpus luteum Cell Tissue Res. 243 1986 129 135 (Pubitemid 16173147)
138. J. Tomikawa, T. Homma, S. Tajima, T. Shibata, Y. Inamoto, K. Takase, N. Inoue, S. Ohkura, Y. Uenoyama, K. Maeda, and H. Tsukamura Molecular characterization and estrogen regulation of hypothalamic KISS1 gene in the pig Biol. Reprod. 82 2010 313 319
139. A.K. Topaloglu, F. Reimann, M. Guclu, A.S. Yalin, L.D. Kotan, K.M. Porter, A. Serin, N.O. Mungan, J.R. Cook, M.N. Ozbek, S. Imamoglu, N.S. Akalin, B. Yuksel, S. O'Rahilly, and R.K. Semple TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction Nat. Genet. 41 2009 354 358
140. S. Tsukahara, F. Maekawa, H. Tsukamura, K. Hirunagi, and K. Maeda Morphological characterization of relationship between gap junctions and gonadotropin releasing hormone nerve terminals in the rat median eminence Neurosci. Lett. 261 1999 105 108 (Pubitemid 29100087)
141. D.F. Van de Wiel, J. Erkens, W. Koops, E. Vos, and A.A. Van Landeghem Periestrous and midluteal time courses of circulating LH, FSH, prolactin, estradiol-17 beta and progesterone in the domestic pig Biol. Reprod. 24 1981 223 233 (Pubitemid 11151386)
142. N. Wade The Nobel Duel 1981 Anchor Press/Doubleday Garden City, NY
143. Y. Wakabayashi, T. Nakada, K. Murata, S. Ohkura, K. Mogi, V.M. Navarro, D.K. Clifton, Y. Mori, H. Tsukamura, K. Maeda, R.A. Steiner, and H. Okamura 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 2010 3124 3132
144. L. Wildt, A. Hausler, G. Marshall, J.S. Hutchison, T.M. Plant, P.E. Belchetz, and E. Knobil Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey Endocrinology 109 1981 376 385 (Pubitemid 11040187)
145. J.W. Witkin, and A.J. Silverman Synaptology of luteinizing hormone-releasing hormone neurons in rat preoptic area Peptides 6 1985 263 271 (Pubitemid 15051828)
146. J.W. Witkin, C.M. Paden, and A.J. Silverman The luteinizing hormone-releasing hormone (LHRH) systems in the rat brain Neuroendocrinology 35 1982 429 438 (Pubitemid 13234390)
147. R.S. Yalow Radioimmunoassay: a probe for the fine structure of biologic systems Science 200 1978 1236 1245 (Pubitemid 8405750)
148. S. Yamada, Y. Uenoyama, M. Kinoshita, K. Iwata, K. Takase, H. Matsui, S. Adachi, K. Inoue, K.I. Maeda, and H. Tsukamura Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats Endocrinology 148 2007 2226 2232 (Pubitemid 46997060)
149. L. Zhang, L.F. Brass, and D.R. Manning The Gq and G12 families of heterotrimeric G proteins report functional selectivity Mol. Pharmacol. 75 2009 235 241