Ultrastructural Evidence of Kisspeptin-Gonadotrophin-Releasing Hormone (GnRH) Interaction in the Median Eminence of Female Rats: Implication of Axo-Axonal Regulation of GnRH Release

Journal of Neuroendocrinology

Volumn 23, Issue 10, 2011, Pages 863-870

  Uenoyama, Y ^a   Inoue, N ^a   Pheng, V ^a   Homma, T ^b   Takase, K ^a   Yamada, S ^a   Ajiki, K ^c   Ichikawa, M ^c   Okamura, H ^b   Maeda, K I ^a   Tsukamura, H ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Gonadotrophin; GPR54; Kiss1r; Metastin

Indexed keywords

ESTRADIOL; GONADORELIN; GONADOTROPIN; KISSPEPTIN; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; HORMONE RELEASE; IMMUNOHISTOCHEMISTRY; LUTEINIZING HORMONE RELEASE; MEDIAN EMINENCE; NERVE CELL; NONHUMAN; OVARIECTOMY; PREOPTIC AREA; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REPRODUCTION;

ANIMALS; AXONS; FEMALE; GONADOTROPIN-RELEASING HORMONE; IMMUNOHISTOCHEMISTRY; KISSPEPTINS; MEDIAN EMINENCE; RADIOIMMUNOASSAY; RATS; RATS, WISTAR;

EID: 80053141024     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02199.x     Document Type: Article

References (48)

1. Bouligand J, Ghervan C, Trabado S, Brailly-Tabard S, Guiochon-Mantel A, Young J. Genetics defects in GNRH1: a paradigm of hypothalamic congenital gonadotropin deficiency. Brain Res 2010; 1364: 3-9.
2. Moenter SM. Identified GnRH neuron electrophysiology: a decade of study. Brain Res 2010; 1364: 10-24.
3. Maeda K, Ohkura S, Uenoyama Y, Wakabayashi Y, Oka Y, Tsukamura H, Okamura H. Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brain Res 2010; 1364: 103-115.
4. Ojeda SR, Lomniczi A, Sandau US. Glial-gonadotrophin hormone (GnRH) neurone interactions in the median eminence and the control of GnRH secretion. J Neuroendocrinol 2008; 20: 732-742.
5. Crown A, Clifton DK, Steiner RA. Neuropeptide signaling in the integration of metabolism and reproduction. Neuroendocrinology 2007; 86: 175-182.
6. Terasawa E, Kurian JR, Guerriero KA, Kenealy BP, Hutz ED, Keen KL. Recent discoveries on the control of gonadotrophin-releasing hormone neurones in nonhuman primates. J Neuroendocrinol 2010; 22: 630-638.
7. 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.
8. 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.
9. 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.
10. Greives TJ, Mason AO, Scotti MA, Levine J, Ketterson ED, Kriegsfeld LJ, Demas GE. Environmental control of kisspeptin: implications for seasonal reproduction. Endocrinology 2007; 148: 1158-1166.
11. Clarke IJ, Smith JT, Caraty A, Goodman RL, Lehman MN. Kisspeptin and seasonality in sheep. Peptides 2008; 30: 154-163.
12. 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.
13. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004; 16: 850-858.
14. 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.
15. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. 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 2004; 145: 4565-4574.
16. 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.
17. 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.
18. Parhar IS, Ogawa S, Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology 2004; 145: 3613-3618.
19. 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.
20. Pielecka-Fortuna J, Chu Z, Moenter SM. Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 2008; 1949: 1979-186.
21. 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.
22. Patterson M, Murphy KG, Thompson EL, Patel S, Ghatei MA, Bloom SR. Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats. J Neuroendocrinol 2006; 18: 349-354.
23. 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.
24. 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 KI. 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.
25. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. 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 2008; 149: 4387-4395.
26. Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, Wakabayashi Y, Uenoyama Y, Mori Y, Steiner RA, Tsukamura H, Maeda KI, Okamura H. Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 2009; 21: 813-821.
27. Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res 2010; 1364: 90-102.
28. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 2008; 149: 3926-3932.
29. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S, Ota K. Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol 1991; 129: 321-328.
30. Park MK, Wakabayashi K. Preparation of a monoclonal antibody to common amino acid sequence of LHRH and its application. Endocrinol Jpn 1986; 33: 257-272.
31. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 2007.
32. Hasegawa Y, Miyamoto K, Yazaki C, Igarashi M. Regulation of the second surge of follicle-stimulating hormone; effects of antiluteinizing hormone-releasing hormone serum and pentobarbital. Endocrinology 1981; 109: 130-135.
33. Silverman AJ, Jhamandas J, Renaud LP. Localization of luteinizing hormone-releasing hormone (LHRH) neurons that project to the median eminence. J Neurosci 1987; 7: 2312-2319.
34. 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.
35. Wiegand SJ, Price JL. Cells of origin of the afferent fibers to the median eminence in the rat. J Comp Neurol 1980; 192: 1-19.
36. Kawakami S, Ichikawa M, Murahashi K, Hirunagi K, Tsukamura H, Maeda K. Excitatory amino acids act on the median eminence nerve terminals to induce gonadotropin-releasing hormone release in female rats. Gen Comp Endocrinol 1998; 112: 372-382.
37. Kawakami SI, Hirunagi K, Ichikawa M, Tsukamura H, Maeda KI. Evidence for terminal regulation of GnRH release by excitatory amino acids in the median eminence in female rats: a dual immunoelectron microscopic study. Endocrinology 1998; 139: 1458-1461.
38. Li C, Chen P, Smith MS. Morphological evidence for direct interaction between arcuate nucleus neuropeptide Y (NPY) neurons and gonadotropin-releasing hormone neurons and the possible involvement of NPY Y1 receptors. Endocrinology 1999; 140: 5382-5390.
39. Kirilov MJ, Porteous R, Chai M, Parkitna J, Wintermantel A, Herbison A, Schütz G. Complete rescue of gonadal steroid-dependent fertility by GnRH neuron-selective expression of the kisspeptin receptor GPR54. Annual Meeting of the Society for Neuroscience, Chicago, IL, USA (Abstract # 66517/DD69), 2009.
40. Agnati LF, Zoli M, Stromberg I, Fuxe K. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 1995; 69: 711-726.
41. Fuxe K, Dahlstrom AB, Jonsson G, Marcellino D, Guescini M, Dam M, Manger P, Agnati L. The discovery of central monoamine neurons gave volume transmission to the wired brain. Prog Neurobiol 2010; 90: 82-100.
42. Yeo SH, Herbison AE. Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology 2011; 152: 2387-2399.
43. True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J Neuroendocrinol 2010; 23: 52-64.
44. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007; 148: 5752-5760.
45. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 2009; 29: 11859-11866.
46. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H. 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 2010; 30: 3124-3132.
47. Krajewski SJ, Anderson MJ, Iles-Shih L, Chen KJ, Urbanski HF, Rance NE. Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. J Comp Neurol 2005; 489: 372-386.
48. 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.