Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: Regulation by oestrogen

Journal of Neuroendocrinology

Volumn 22, Issue 9, 2010, Pages 1032-1039

  Vida, B ^a   Deli, L ^a   Hrabovszky, E ^a   Kalamatianos, T ^b   Caraty, A ^c   Coen, C W ^b   Liposits, Z ^a,d   Kallo I ^a,d  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^d PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

GnRH; Kisspeptin; Oestrogen; Suprachiasmatic nucleus; Vasopressin

Indexed keywords

ESTROGEN; GALANIN; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOPRESSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; FEMALE; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUPRACHIASMATIC NUCLEUS;

ANIMALS; BRAIN; ESTRADIOL; FEMALE; INTRALAMINAR THALAMIC NUCLEI; MALE; MICE; NEURONS; PHYTOHEMAGGLUTININS; SUPRACHIASMATIC NUCLEUS; SYNAPSES; TUMOR SUPPRESSOR PROTEINS; VASOPRESSINS;

EID: 77956002457     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02045.x     Document Type: Article

References (49)

1. 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.
2. Coen CW, MacKinnon PC. Lesions of the suprachiasmatic nuclei and the serotonin-dependent phasic release of luteinizing hormone in the rat: effects on drinking rhythmicity and on the consequences of preoptic area stimulation. J Endocrinol 1980, 84:231-236.
3. 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.
4. 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.
5. 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.
6. Van der Beek EM, Wiegant VM, van der Donk HA, van den Hurk R, Buijs RM. Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotrophin-releasing hormone neurons in the female rat. J Neuroendocrinol 1993, 5:137-144.
7. 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.
8. Gu GB, Simerly RB. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J Comp Neurol 1997, 384:142-164.
9. Hahn JD, Coen CW. 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 2006, 494:190-214.
10. 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.
11. Le WW, Attardi B, Berghorn KA, Blaustein J, Hoffman GE. Progesterone blockade of a luteinizing hormone surge blocks luteinizing hormone-releasing hormone Fos activation and activation of its preoptic area afferents. Brain Res 1997, 778:272-280.
12. Watson RE, Langub MC, 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.
13. 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.
14. Kallo I, Kalamatianos T, Wiltshire N, Shen S, Sheward WJ, Harmar AJ, Coen CW. Transgenic approach reveals expression of the VPAC2 receptor in phenotypically defined neurons in the mouse suprachiasmatic nucleus and in its efferent target sites. Eur J Neurosci 2004, 19:2201-2211.
15. Kalamatianos T, Kallo I, Piggins HD, Coen CW. Expression of VIP and/or PACAP receptor mRNA in peptide synthesizing cells within the suprachiasmatic nucleus of the rat and in its efferent target sites. J Comp Neurol 2004, 475:19-35.
16. 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.
17. 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.
18. Abrahamson EE, Moore RY. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 2001, 2:172-191.
19. Miller MA, Kolb PE, Raskind MA. Extra-hypothalamic vasopressin neurons coexpress galanin messenger RNA as shown by double in situ hybridization histochemistry. J Comp Neurol 1993, 329:378-384.
20. Rokaeus A, Young WS, Mezey E. Galanin coexists with vasopressin in the normal rat hypothalamus and galanin's synthesis is increased in the Brattleboro (diabetes insipidus) rat. Neurosci Lett 1988, 2:45-50.
21. Planas B, Kolb PE, Raskind MA, Miller MA. Vasopressin and galanin mRNAs coexist in the nucleus of the horizontal diagonal band: a novel site of vasopressin gene expression. J Comp Neurol 1995, 361:48-56.
22. Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 1998, 19:302-330.
23. Vida B, Hrabovszky E, Kalamatianos T, Coen CW, Liposits Z, Kallo I. Oestrogen receptor alpha and beta immunoreactive cells in the suprachiasmatic nucleus of mice: distribution, sex differences and regulation by gonadal hormones. J Neuroendocrinol 2008, 20:1270-1277.
24. Crowley WR, Kalra SP. Neonatal exposure to estradiol prevents the expression of ovarian hormone-induced luteinizing hormone and prolactin surges in adulthood but not antecedent changes in neuropeptide Y or adrenergic transmitter activity: implications for sexual differentiation of gonadotropin secretion. Brain Res 1994, 663:257-265.
25. Liu X, Lee K, Herbison AE. Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 2008, 149:4605-4614.
26. 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.
27. Zarnani AH, Moazzeni SM, Shokri F, Salehnia M, Jeddi Tehrani M. Analysis of endometrial myeloid and lymphoid dendritic cells during mouse estrous cycle. J Reprod Immunol 2006, 71:28-40.
28. Maguire JL, Stell BM, Rafizadeh M, Mody I. Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 2005, 8:797-804.
29. Cohen PE, Milligan SR. Silastic implants for delivery of oestradiol to mice. J Reprod Fertil 1993, 99:219-223.
30. Gerfen CR, Sawchenko PE. An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 1984, 290:219-238.
31. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates 2001, San Diego, CA, Academic Press
32. 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.
33. 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 2006, 401:225-230.
34. Kallo I, Butler JA, Barkovics-Kallo M, Goubillon ML, Coen CW. Oestrogen receptor beta-immunoreactivity in gonadotropin releasing hormone-expressing neurones: regulation by oestrogen. J Neuroendocrinol 2001, 13:741-748.
35. Ben-Barak Y, Russell JT, Whitnall MH, Ozato K, Gainer H. Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies. J Neurosci 1985, 5:81-97.
36. Ichikawa H, Sugimoto T. Pituitary adenylate cyclase-activating polypeptide-immunoreactive nerve fibers in rat and human tooth pulps. Brain Res 2003, 980:288-292.
37. Lopez FJ, Meade EH, Negro-Vilar A. Endogenous galanin modulates the gonadotropin and prolactin proestrous surges in the rat. Endocrinology 1993, 132:795-800.
38. 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.
39. 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.
40. 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.
41. Meyer-Bernstein EL, Jetton AE, Matsumoto SI, Markuns JF, Lehman MN, Bittman EL. Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 1999, 140:207-218.
42. Kalsbeek A, Buijs RM. Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting. Cell Tissue Res 2002, 309:109-118.
43. Dennison-Cavanagh ME, Papadopoulos G, Parnavelas JG. The emergence of the cortical GABAergic neuron: with particular reference to some peptidergic subpopulations. J Neurocytol 1993, 22:805-814.
44. Moore RY, Speh JC. GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 1993, 150:112-116.
45. Gore AC. Diurnal rhythmicity of gonadotropin-releasing hormone gene expression in the rat. Neuroendocrinology 1998, 68:257-263.
46. Hannibal J. Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study. J Comp Neurol 2002, 453:389-417.
47. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS. Circadian regulation of Kiss1 neurons: implications for timing the preovulatory GnRH/LH surge. Endocrinology 2009, 150:3664-3671.
48. Kurunczi A, Hoyk Z, Csakvari E, Gyenes A, Parducz A. 17beta-Estradiol-induced remodeling of GABAergic axo-somatic synapses on estrogen receptor expressing neurons in the anteroventral periventricular nucleus of adult female rats. Neuroscience 2009, 158:553-557.
49. Gerrits PO, Kortekaas R, Veening JG, de Weerd H, Algra A, Mouton LJ, van der Want JJ. Estrous cycle-dependent neural plasticity in the caudal brainstem in the female golden hamster: ultrastructural and immunocytochemical studies of axo-dendritic relationships and dynamic remodeling. Horm Behav 2008, 54:627-639.