Anatomy of the kisspeptin neural network in mammals

Brain Research

Volumn 1364, Issue , 2010, Pages 90-102

  Lehman, Michael N ^a   Merkley, Christina M ^a   Coolen, Lique M ^a   Goodman, Robert L ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GnRH; Hypothalamus; Kisspeptin; Neuroanatomy; Steroid receptor

Indexed keywords

GONADORELIN; HORMONE RECEPTOR; KISSPEPTIN; SEX HORMONE; STEROID RECEPTOR;

ADULTHOOD; CELL POPULATION; GONADORELIN RELEASE; HUMAN; HYPOTHALAMUS; MAMMAL; MOLECULAR INTERACTION; NERVE CELL NETWORK; NEUROANATOMY; NEUROCHEMISTRY; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUBERTY; REVIEW;

ANIMALS; BRAIN; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMUS; NERVE FIBERS; NERVE NET; NEURONS; RECEPTORS, STEROID; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 78649510651     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.09.020     Document Type: Review

References (93)

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.-I. Maeda Involvement of anteroventricular periventricular matastin/kisspeptin neurons in estrogen positive feedback action on leutentizing hormone release in female rats J. Reprod. Dev. 53 2007 367 378 (Pubitemid 46743563)
2. V.L. Adams, R.L. Goodman, A.K. Salm, L.M. Coolen, F.J. Karsch, and M.N. Lehman Morphological plasticity in the neural circuitry responsible for seasonal breeding in the ewe Endocrinology 147 2006 4843 4851
3. L.F. Agnati, M. Zoli, I. Strömberg, and K. Fuxe Intercellular communication in the brain: wiring versus volume transmission Neuroscience 69 1995 711 726
4. L. Ansel, M. Bolborea, A.H. Bentsen, P. Klosen, J.D. Mikkelsen, and V. Simonneaux Differential regulation of Kiss1 expression by melatonin and gonadal hormones in male and female Syrian hamsters J. Biol. Rhythms 25 2010 81 91
5. U. Boehm, Z. Zou, and L.B. Buck Feedback loops link odor and pheromone signaling with reproduction Cell 123 2005 683 695 (Pubitemid 41608469)
6. G.C. Brailoiu, L.D. Siok, O. Masahiro, Y. Deling, Y. Jun, C. Jaw Kang, B. Eugen, and J.D. Nae KiSS-1 expression and metastin-like immunoreactivity in the rat brain J. Comp. Neurol. 481 2005 314 329 (Pubitemid 40023540)
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. 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. 106 2009 10835 10840
9. 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)
10. G. Cheng, L.M. Coolen, V. Padmanabhan, R.L. Goodman, and M.N. Lehman The Kisspeptin/Neurokinin B/Dynorphin (KNDy) cell population of the arcuate nucleus: sex differences and effects of prenatal testosterone in sheep Endocrinology 151 2010 301 311
11. 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)
12. J. Clarkson, X. d'Anglemont de Tassigny, A.S. Moreno, W.H. Colledge, and A.E. Herbison Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge J. Neurosci. 28 2008 8691 8697
13. J. Clarkson, X.d.a.d. Tassigny, W.H. Colledge, A. Caraty, and A.E. Herbison Distribution of kisspeptin neurones in the adult female mouse brain J. Neuroendocrinol. 21 2009 673 682
14. X. d'Anglemont de Tassigny, L.A. Fagg, M.B.L. Carlton, and W.H. Colledge Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals Endocrinology 149 2008 3926 3932
15. E.C. Davis, P. Popper, and R.A. Gorski The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area Brain Res. 734 1996 10 18 (Pubitemid 26334024)
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. C. Decourt, Y. Tillet, A. Caraty, I. Franceschini, and C. Briant Kisspeptin immunoreactive neurons in the equine hypothalamus: interactions with GnRH neuronal system J. Chem. Neuroanat. 36 2008 131 137
18. Desroziers, E., Mikkelsen, J., Simonneaux, V., Keller, M., Tillet, Y., Caraty, A., Franceschini, I., 2010. Mapping of kisspeptin fibres in the brain of the pro-oestrus rat. J. Neuroendocrinol. Accepted Article; 10.1111/j.1365-2826. 2010.02053.x.
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. H.M. Dungan Lemko, R. Naderi, V. Adjan, L.H. Jennes, V.M. Navarro, D.K. Clifton, and R.A. Steiner Interactions between neurotensin and GnRH neurons in the positive feedback control of GnRH/LH secretion in the mouse Am. J. Physiol. Endocrinol. Metab. 298 2010 E80 E88
21. H.M. Dungan, D.K. Clifton, and R.A. Steiner Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion Endocrinology 147 2006 1154 1158
22. K.M. Estrada, C.M. Clay, S. Pompolo, J.T. Smith, and I.J. Clarke 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 2006 806 809 (Pubitemid 44340517)
23. C.D. Foradori, L.M. Coolen, M.E. Fitzgerald, D.C. Skinner, R.L. Goodman, and M.N. Lehman Colocalization of progesterone receptors in parvicellular dynorphin neurons of the ovine preoptic area and hypothalamus Endocrinology 143 2002 4366 4374
24. 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)
25. 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)
26. R. Goodman, D.B. Parfitt, N.P. Evands, G.E. Dahl, and F.J. Karsch Endogenous opioid peptides control the amplitude and shape of gonadotropin-releasing hormone pulses in the ewe Endocrinology 136 1995 2412 2420
27. 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)
28. R.L. Goodman, M.N. Lehman, J.T. Smith, L.M. Coolen, C.V.R. 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)
29. Goodman, R.L., Nestor, C.C., Connors, J.M., Holaskova, I., Lehman, M.N., 2010. The actions of neurokinin B in the arcuate nucleus are important for episodic LH secretion in ewes. In Annual Meeting of the Society for Neuroscience. Vol., ed. eds., San Diego, CA.
30. M.L. Gottsch, M.J. Cunningham, J.T. Smith, S.M. Popa, B.V. Acohido, W.F. Crowley, S. Seminara, D.K. Clifton, and R.A. Steiner A role for kisspeptins in the regulation of gonadotropin secretion in the mouse Endocrinology 145 2004 4073 4077 (Pubitemid 39120554)
31. T.J. Greives, A.O. Mason, M.-A.L. Scotti, J. Levine, E.D. Ketterson, L.J. Kriegsfeld, and G.E. Demas Environmental control of kisspeptin: implications for seasonal reproduction Endocrinology 148 2007 1158 1166 (Pubitemid 46272807)
32. G.B. Gu, and R.B. Simerly Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat J. Comp. Neurol. 384 1997 142 164 (Pubitemid 27280229)
33. J.D. Hahn, and C.W. Coen Comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats J. Comp. Neurol. 494 2006 190 214
34. S.-K. Han, M.L. Gottsch, K.J. Lee, S.M. Popa, J.T. Smith, S.K. Jakawich, D.K. Clifton, R.A. Steiner, and A.E. Herbison Activation of gonadotropin- releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty J. Neurosci. 25 2005 11349 11356
35. A.E. Herbison 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. 57 2008 277 287
36. A.E. Herbison, X. d'Anglemont 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
37. D.L. Hess, R.H. Wilkins, J. Moossy, J.L. Chang, T.M. Plant, J.T. McCormack, Y. Nakai, and E. Knobil Estrogen-induced gonadotropin surges in decerebrated female rhesus monkeys with medial basal hypothalamic peninsulae Endocrinology 101 1977 1264 1271 (Pubitemid 8188346)
38. E. Hrabovszky, P. Ciofi, B. Vida, M.C. Horvath, E. Keller, A. Caraty, S.R. Bloom, M.A. Ghatei, W.S. Dhillo, Z. Liposits, and I. Kallo The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons Eur. J. Neurosci. 31 2010 1984 1998
39. M.S. Irwig, G.S. Fraley, J.T. Smith, B.V. Acohido, S.M. Popa, M.J. Cunningham, M.L. Gottsch, D.K. Clifton, and R.A. Steiner Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat Neuroendocrinology 80 2004 264 272
40. C.N. Jayasena, W.S. Dhillo, and S.R. Bloom Kisspeptins and the control of gonadotropin secretion in humans Peptides 30 2009 76 82
41. A.S. Kauffman Sexual differentiation and the Kiss1 system: hormonal and developmental considerations Peptides 30 2009 83 93
42. A.S. Kauffman, D.K. Clifton, and R.A. Steiner Emerging ideas about kisspeptin-GPR54 signaling in the neuroendocrine regulation of reproduction Trends Neurosci. 30 2007 504 511
43. A.S. Kauffman, M.L. Gottsch, J. Roa, A.C. Byquist, A. Crown, D.K. Clifton, G.E. Hoffman, R.A. Steiner, and M. Tena-Sempere Sexual differentiation of Kiss1 gene expression in the brain of the rat Endocrinology 148 2007 1774 1783 (Pubitemid 46457121)
44. A.S. Kauffman, J. Kim, D.K. Clifton, and R.A. Steiner Regulation of Kiss1 gene expression by sex steroids in the medial amygdala of mice Society for Neuroscience 37th Annual Meeting, San Diego, CA Society for Neuroscience 2007
45. W. Kim, H.M. Jessen, A.P. Auger, and E. Terasawa Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1) mRNA in the basal hypothalamus of female rhesus monkeys Peptides 30 2009 103 110
46. M. Kinoshita, H. Tsukamura, S. Adachi, H. Matsui, Y. Uenoyama, K. Iwata, S. Yamada, K. Inoue, T. Ohtaki, H. Matsumoto, and K.-I. 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)
47. M.A. Kirigiti, C. True, P. Ciofi, K.L. Grove, and M.S. Smith Kisspeptin and NKB fiber distribution in the adult female rat: relationship to GnRH cell bodies and fibers/terminals in the median eminence Endocr. Soc. Abstr. 2009 2009 P3 P223
48. S.J. Krajewski, M.J. Anderson, L. Iles-Shih, K.J. Chen, H.F. Urbanski, and N.E. Rance Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence J. Comp. Neurol. 489 2005 372 386 (Pubitemid 41026235)
49. 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
50. 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
51. M.N. Lehman, and R. Silver CSF signaling in physiology and behavior L.F. Agnati, K. Fuxe, C. Nicholson, E. Sykov, Progress in Brain Research vol. 125 2000 415 433 (Pubitemid 35460816)
52. 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
53. R.L. Leshan, D.M. Opland, G.W. Louis, G.M. Leinninger, C.M. Patterson, C.J. Rhodes, H. Munzberg, and M.G. Myers Jr. Ventral tegmental area leptin receptor neurons specifically project to and regulate cocaine- and amphetamine-regulated transcript neurons of the extended central amygdala J. Neurosci. 30 2010 5713 5723
54. C. Magee, C.D. Foradori, J.E. Bruemmer, J.A. Arreguin-Arevalo, P.M. McCue, R.J. Handa, E.L. Squires, and C.M. Clay Biological and anatomical evidence for kisspeptin regulation of the hypothalamic-pituitary-gonadal axis of estrous horse mares Endocrinology 150 2009 2813 2821
55. A.O. Mason, T.J. Greives, M.-A.L. Scotti, J. Levine, S. Frommeyer, E.D. Ketterson, G.E. Demas, and L.J. Kriegsfeld Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters Hormones and Behavior 52 2007 492 498 (Pubitemid 47488260)
56. S. Messager, E.E. Chatzidaki, D. Ma, A.G. Hendrick, D. Zahn, J. Dixon, R.R. Thresher, I. Malinge, D. Lomet, M.B.L. Carlton, W.H. Colledge, A. Caraty, and S.A.J.R. Aparicio Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54 Proc. Natl. Acad. Sci. U. S. A. 102 2005 1761 1766 (Pubitemid 40209241)
57. J.D. Mikkelsen, and V. Simonneaux The neuroanatomy of the kisspeptin system in the mammalian brain Peptides 30 2009 26 33
58. 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
59. Nestor, C.C., Seebaugh, A.M., Valent, M., Connors, J.M., Goodman, R.L., Hileman, S.M., 2010. Evaluation of neurokinin B and kisspeptin expression before and after puberty in sheep. In Annual Meeting of the Society for Neuroscience. Vol., ed. eds., San Diego, CA.
60. A.E. Oakley, D.K. Clifton, and R.A. Steiner Kisspeptin signaling in the brain Endocr. Rev. 30 2009 713 743
61. Oakley, A.E., Coolen, L.M., Lehman, M.N., Wagenmaker, E.R., F. J. Karsch, 2009. Are dynorphin neurons in the arcuate nucleus responsive to cortisol and influenced by the combined presence of cortisol and estradiol? In Endocrine Society Meeting. Vol., ed. eds., Washington DC.
62. 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
63. J. Pielecka-Fortuna, Z. Chu, and S.M. Moenter Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol Endocrinology 149 2008 1979 1986 (Pubitemid 351468349)
64. E.K. Polston, and R.B. Simerly Ontogeny of the projections from the anteroventral periventricular nucleus of the hypothalamus in the female rat J. Comp. Neurol. 495 2006 122 132 (Pubitemid 43238056)
65. S. Pompolo, O. Ischenko, A. Pereira, J. Iqbal, and I.J. Clarke Evidence that projections from the bed nucleus of the stria terminalis and from the lateral and medial regions of the preoptic area provide input to gonadotropin releasing hormone (GNRH) neurons in the female sheep brain Neuroscience 132 2005 421 436 (Pubitemid 40417915)
66. 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
67. 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
68. F.G. Revel, M. Saboureau, M. Masson-Pévet, P. Pévet, J.D. Mikkelsen, and V. Simonneaux Kisspeptin mediates the photoperiodic control of reproduction in hamsters Current Biology 16 2006 1730 1735 (Pubitemid 44767530)
69. J.L. Robertson, D.K. Clifton, H.O. de la Iglesia, R.A. Steiner, and A.S. Kauffman Circadian regulation of Kiss1 neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge Endocrinology 150 2009 3664 3671
70. A.M. Rometo, S.J. Krajewski, M. Lou Voytko, and N.E. Rance Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys J. Clin. Endocrinol. Metab. 92 2007 2744 2750
71. A.K. Roseweir, and R.P. Millar The role of kisspeptin in the control of gonadotrophin secretion Hum. Reprod. Update 15 2009 203 212
72. 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
73. 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.L. Carlton, W.F. Crowley Jr., S.A.J.R. Aparicio, and W.H. Colledge The GPR54 gene as a regulator of puberty N. Engl. J. Med. 349 2003 1614 1627 (Pubitemid 37303886)
74. M. Shahab, C. Mastronardi, S.B. Seminara, W.F. Crowley, S.R. Ojeda, and T.M. Plant Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates Proc. Natl. Acad. Sci. U. S. A. 102 2005 2129 2134 (Pubitemid 40262023)
75. R.B. Simerly, and L.W. Swanson The organization of the neural inputs to the medial preoptic nucleus of the rat J. Comp. Neurol. 246 1986 312 342
76. R.B. Simerly, B.J. Young, M.A. Capozza, and L.W. Swanson Estrogen differentially regulates neuropeptide gene expression in a sexually dimorphic olfactory pathway Proc. Natl. Acad. Sci. 86 1989 4766 4770
77. J.T. Smith Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe Brain Res. Rev. 57 2008 288
78. 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)
79. J.T. Smith, S.M. Popa, D.K. Clifton, G.E. Hoffman, and R.A. Steiner Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge J. Neurosci. 26 2006 6687 6694
80. 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)
81. J.T. Smith, L.M. Coolen, L.J. Kriegsfeld, I.P. Sari, M.R. Jaafarzadehshirazi, M. Maltby, K. Bateman, R.L. Goodman, A.J. Tilbrook, T. Ubuka, G.E. Bentley, I.J. Clarke, and M.N. Lehman 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 149 2008 5770 5782
82. 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
83. J.T. Smith, M. Shahab, A. Pereira, K.Y.F. 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
84. R.E. Szawka, A.B. Ribeiro, C.M. Leite, C.V. Helena, C.R. Franci, G.M. Anderson, G.E. Hoffman, and J.A. Anselmo-Franci Kisspeptin regulates prolactin release through hypothalamic dopaminergic neurons Endocrinology 151 2010 3247 3257
85. Y. Tillet, M. Batallier, and J. Thibault Neuronal projections to the medial preoptic area of the sheep, with special reference to monoaminergic afferents: immunohistochemical and retrograde tract tracing studies J. Comp. Neurol. 330 1993 195 220 (Pubitemid 23095323)
86. 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
87. Vida, B., Hrabovsky, E., Caraty, A., Ciofi, P., Coen, C.W., Liposits, Z., Kallo Dr., I., 2009. Gender differences in the co-localisation of neuropeptides with kisspeptin in the hypothalamic neurons of the mouse brain. In Annual Meeting of the Society for Neuroscience. Vol., ed. eds., Chicago, I.L., pp. Poster 865.9.
88. B. Vida, L. Deli, E. Hrabovszky, T. Kalamatianos, A. Caraty, C. Coen, Z. Liposits, and I. Kalló Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen J. Neuroendocrinol. 22 2010 1032 1039
89. Y. Wakabayashi, T. Nakada, K. Murata, S. Ohkura, K. Mogi, V.M. Navarro, D.K. Clifton, Y. Mori, H. Tsukamura, K.-I. 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
90. S.J. Wiegand, E. Terasawa, W.E. Bridson, and R.W. Goy Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion Neuroendocrinology 31 1980 147 157 (Pubitemid 10076596)
91. T.M. Wintermantel, R.E. Campbell, R. Porteous, D. Bock, H.-J. Gröne, M.G. Todman, K.S. Korach, E. Greiner, C.A. Pérez, G. Schütz, and A.E. Herbison Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility Neuron 52 2006 271 280 (Pubitemid 44548337)
92. Yeo, S.H., Herbison, A., 2009. Rostral periventricular kisspeptin neurons project to the arcuate nucleus in adult female mice. In Combio, 2009. Vol., ed. eds., Christchurch, New Zealand, pp. 167.
93. H. Yoon, L.W. Enquist, and C. Dulac Olfactory inputs to hypothalamic neurons controlling reproduction and fertility Cell 123 2005 669 682 (Pubitemid 41608468)