Dual Phenotype Kisspeptin-Dopamine Neurones of the Rostral Periventricular Area of the Third Ventricle Project to Gonadotrophin-Releasing Hormone Neurones

Journal of Neuroendocrinology

Volumn 23, Issue 4, 2011, Pages 293-301

  Clarkson, J ^a   Herbison, A E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

GnRH; Kisspeptin; POA; RP3V; TH

Indexed keywords

DOPAMINE; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; DIESTRUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; MALE; MOUSE; NERVE FIBER; NONHUMAN; OVULATION; PREOPTIC AREA; PRIORITY JOURNAL; PROESTRUS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; DOPAMINE; ESTROUS CYCLE; FEMALE; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEURONS; PHENOTYPE; SEX CHARACTERISTICS; THIRD VENTRICLE; TUMOR SUPPRESSOR PROTEINS; TYROSINE 3-MONOOXYGENASE;

EID: 79952715059     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02107.x     Document Type: Article

References (47)

1. 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.
2. 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.
3. 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.
4. 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.
5. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004; 561: 379-386.
6. 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.
7. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005; 102: 2129-2134.
8. 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.
9. 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.
10. 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.
11. 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.
12. Clarkson J, d'Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE. Distribution of kisspeptin neurons in the adult female mouse brain. J Neuroendocrinol 2009; 21: 673-682.
13. 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.
14. Gonzalez-Martinez D, De Mees C, Douhard Q, Szpirer C, Bakker J. Absence of gonadotropin-releasing hormone 1 and Kiss1 activation in alpha-fetoprotein knockout mice: prenatal estrogens defeminize the potential to show preovulatory luteinizing hormone surges. Endocrinology 2008; 149: 2333-2340.
15. 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.
16. Liu X, Petersen SL, d'Anglemont de Tassigny X, Colledge WH, Herbison AE. Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neurons excitability. J Neurosci 2010; In Press.
17. Clarkson J, Herbison AE. Oestrogen, kisspeptin, GPR54 and the pre-ovulatory luteinising hormone surge. J Neuroendocrinol 2009; 21: 305-311.
18. 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.
19. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci USA 1997; 94: 14077-14082.
20. Horvath TL, Naftolin F, Leranth C. Luteinizing hormone-releasing hormone and gamma-aminobutyric acid neurons in the medial preoptic area are synaptic targets of dopamine axons originating in anterior periventricular areas. J Neuroendocrinol 1993; 5: 71-79.
21. Szawka RE, Ribeiro AB, Leite CM, Helena CV, Franci CR, Anderson GM, Hoffman GE, Anselmo-Franci JA. Kisspeptin regulates prolactin release through hypothalamic dopaminergic neurons. Endocrinology 2010; 151: 3247-3257.
22. 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.
23. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005; 146: 2976-2984.
24. Spergel DJ, Kruth U, Hanley DF, Sprengel R, Seeburg PH. GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 1999; 19: 2037-2050.
25. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 206; 401: 225-230.
26. Palkovits M, Jacobowitz DM. Topographic atlas of catecholamine and acetylcholinesterase-containing neurons in the rat brain. II. Hindbrain (mesencephalon, rhombencephalon). J Comp Neurol 1974; 157: 29-42.
27. Simerly RB, Swanson LW, Gorski RA. The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res 1985; 330: 55-64.
28. Clarkson J, Boon WC, Simpson ER, Herbison AE. Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 2009; 150: 3214-3220.
29. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 2004.
30. Semaan SJ, Murray EK, Poling MC, Dhamija S, Forger NG, Kauffman AS. BAX-dependent and BAX-independent regulation of Kiss1 neuron development in mice. Endocrinology 2010; 151: 5807-5817.
31. Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 2010; 151: 3479-3489.
32. 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.
33. 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.
34. Herbison AE, de Tassigny X, Doran J, Colledge WH. Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons. Endocrinology 2010; 151: 312-321.
35. Roberts CB, Campbell RE, Herbison AE, Suter KJ. Dendritic action potential initiation in hypothalamic gonadotropin releasing hormone (GnRH) neurons. Endocrinology 2008; 149: 3355-3360.
36. Leranth C, MacLusky NJ, Shanabrough M, Naftolin F. Catecholaminergic innervation of luteinizing hormone-releasing hormone and glutamic acid decarboxylase immunopositive neurons in the rat medial preoptic area. An electron-microscopic double immunostaining and degeneration study. Neuroendocrinology 1988; 48: 591-602.
37. Chen WP, Witkin JW, Silverman AJ. Gonadotropin releasing hormone (GnRH) neurons are directly innervated by catecholamine terminals. Synapse 1989; 3: 288-290.
38. Campbell RE, Herbison AE. Definition of brainstem afferents to gonadotropin-releasing hormone neurons in the mouse using conditional viral tract tracing. Endocrinology 2007; 148: 5884-5890.
39. Han SK, Herbison AE. Norepinephrine suppresses gonadotropin-releasing hormone neuron excitability in the adult mouse. Endocrinology 2008; 149: 1129-1135.
40. Turi GF, Liposits Z, Moenter SM, Fekete C, Hrabovszky E. Origin of neuropeptide Y-containing afferents to gonadotropin-releasing hormone neurons in male mice. Endocrinology 2003; 144: 4967-4974.
41. Goodman RL, Jansen HT, Billings HJ, Coolen LM, Lehman MN. Neural systems mediating seasonal breeding in the ewe. J Neuroendocrinol 2010; 22: 674-681.
42. 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.
43. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 2004; 320: 383-388.
44. 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.
45. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Characterization of the potent LH releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005; 146: 156-163.
46. Ottem EN, Godwin JG, Krishnan S, Petersen SL. Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function. J Neurosci 2004; 24: 8097-8105.
47. Verhage M, McMahon HT, Ghijsen WE, Boomsma F, Scholten G, Wiegant VM, Nicholls DG. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 1991; 6: 517-524.