Immunofluorescent histochemical and ultrastructural studies on the innervation of kisspeptin/neurokinin B neurons to tuberoinfundibular dopaminergic neurons in the arcuate nucleus of rats

Neuroscience Research

Volumn 74, Issue 1, 2012, Pages 10-16

  Sawai, Nobuhiko ^a,b   Iijima, Norio ^a   Takumi, Ken ^a   Matsumoto, Keisuke ^a   Ozawa, Hitoshi ^a  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b GUNMA UNIVERSITY   (Japan)

Author keywords

Arcuate nucleus; Kisspeptin; Neurokinin B; Prolactin; Sexual difference; Synaptic contact; Tuberoinfundibular dopaminergic neurons

Indexed keywords

ESTRADIOL; KISSPEPTIN; NEUROKININ B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; ARCUATE NUCLEUS; DOPAMINERGIC NEURONS; ESTRADIOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; KISSPEPTINS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; NEURAL PATHWAYS; NEUROKININ B; OVARIECTOMY; PROLACTIN; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

EID: 84865977697     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2012.05.011     Document Type: Article

References (37)

1. 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.
2. Arbogast L.A., Voogt J.L. Progesterone reverses the estradiol-induced decrease in tyrosine hydroxylase mRNA levels in the arcuate nucleus. Neuroendocrinology 1993, 58:501-510.
3. Ben-Jonathan N. Dopamine: a prolactin-inhibiting hormone. Endocr. Rev. 1985, 6:564-589.
4. Burke M.C., Letts P.A., Krajewski S.J., Rance N.E. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J. Comp. Neurol. 2006, 498:712-726.
5. Ciofi P., Leroy D., Tramu G. Sexual dimorphism in the organization of the rat hypothalamic infundibular area. Neuroscience 2006, 141:1731-1745.
6. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J. Neurosci. 2008, 28:8691-8697.
7. DeMaria J.E., Livingstone J.D., Freeman M.E. Ovarian steroids influence the activity of neuroendocrine dopaminergic neurons. Brain Res. 2000, 879:139-147.
8. Dhillo W.S., Chaudhri O.B., Patterson M., Thompson E.L., Murphy K.G., Badman M.K., McGowan B.M., Amber V., Patel S., Ghatei M.A., Bloom S.R. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J. Clin. Endocrinol. Metab. 2005, 90:6609-6615.
9. Goodman R.L., Lehman M.N., Smith J.T., Coolen L.M., de Oliveira C.V., Jafarzadehshirazi M.R., Pereira A., Iqbal J., Caraty A., Ciofi P., Clarke I.J. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007, 148:5752-5760.
10. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., Seminara S., Clifton D.K., Steiner R.A. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004, 145:4073-4077.
11. Iijima N., Takumi K., Sawai N., Ozawa H. An immunohistochemical study on the expressional dynamics of kisspeptin neurons relevant to GnRH neurons using a newly developed anti-kisspeptin antibody. J. Mol. Neurosci. 2011, 43:146-154.
12. Irwig M.S., Fraley G.S., Smith J.T., Acohido B.V., Popa S.M., Cunningham M.J., Gottsch M.L., Clifton D.K., Steiner R.A. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004, 80:264-272.
13. Jones E.E., Naftolin F. Estrogen effects on the tuberoinfundibular dopaminergic system in the female rat brain. Brain Res. 1990, 510:84-91.
14. Koga M., Nakao H., Arao M., Sato B., Noma K., Morimoto Y., Kishimoto S., Mori S., Uozumi T. Demonstration of specific dopamine receptors on human pituitary adenomas. Acta Endocrinol. 1987, 114:595-602.
15. Kokay I.C., Petersen S.L., Grattan D.R. Identification of prolactin-sensitive GABA and kisspeptin neurons in regions of the rat hypothalamus involved in the control of fertility. Endocrinology 2011, 152:526-535.
16. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brézillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., Vassart G., Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol. Chem. 2001, 276:34631-34636.
17. Lee D.K., Nguyen T., O'Neill G.P., Cheng R., Liu Y., Howard A.D., Coulombe N., Tan C.P., Tang-Nguyen A.T., George S.R., O'Dowd B.F. Discovery of a receptor related to the galanin receptors. FEBS Lett. 1999, 446:103-107.
18. Lyons D.J., Horjales-Araujo E., Broberger C. Synchronized network oscillations in rat tuberoinfundibular dopamine neurons: switch to tonic discharge by thyrotropin-releasing hormone. Neuron 2010, 65:217-229.
19. Mansour A., Meador-Woodruff J.H., Bunzow J.R., Civelli O., Akil H., Watson S.J. Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J. Neurosci. 1990, 10:2587-2600.
20. 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.
21. Matsuyama S., Ohkura S., Mogi K., Wakabayashi Y., Mori Y., Tsukamura H., Maeda K., Ichikawa M., Okamura H. Morphological evidence for direct interaction between kisspeptin and gonadotropin-releasing hormone neurons at the median eminence of the male goat: an immunoelectron microscopic study. Neuroendocrinology 2011, 94:323-332.
22. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B., Colledge W.H., Caraty A., Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1761-1766.
23. Muir A.I., Chamberlain L., Elshourbagy N.A., Michalovich D., Moore D.J., Calamari A., Szekeres P.G., Sarau H.M., Chambers J.K., Murdock P., Steplewski K., Shabon U., Miller J.E., Middleton S.E., Darker J.G., Larminie C.G., Wilson S., Bergsma D.J., Emson P., Faull R., Philpott K.L., Harrison D.C. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J. Biol. Chem. 2001, 276:28969-28975.
24. Navarro V.M., Castellano J.M., Fernández-Fernández R., Barreiro M.L., Roa J., Sanchez-Criado J.E., 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.
25. Navarro V.M., Gottsch M.L., Chavkin C., Okamura H., Clifton D.K., Steiner R.A. 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.
26. Ohtaki T., Shintani Y., Honda S., Matsumoto H., Hori A., Kanehashi K., Terao Y., Kumano S., Takatsu Y., Masuda Y., Ishibashi Y., Watanabe T., Asada M., Yamada T., Suenaga M., Kitada C., Usuki S., Kurokawa T., Onda H., Nishimura O., Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001, 411:613-617.
27. Rance N.E. Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 2009, 30:111-122.
28. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R., Plant T.M. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:2129-2134.
29. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
30. Smith J.T., Popa S.M., Clifton D.K., Hoffman G.E., Steiner R.A. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J. Neurosci. 2006, 26:6687-6694.
31. Szabo F.K., Snyder N., Usdin T.B., Hoffman G.E. A direct neuronal connection between the subparafascicular and ventrolateral arcuate nuclei in non-lactating female rats. Could this pathway play a role in the suckling-induced prolactin release?. Endocrine 2010, 37:62-70.
32. Szawka R.E., Ribeiro A.B., Leite C.M., Helena C.V., Franci C.R., Anderson G.M., Hoffman G.E., Anselmo-Franci J.A. Kisspeptin regulates prolactin release through hypothalamic dopaminergic neurons. Endocrinology 2010, 151:3247-3257.
33. Topaloglu A.K., Reimann F., Guclu M., Yalin A.S., Kotan L.D., Porter K.M., Serin A., Mungan N.O., Cook J.R., Ozbek M.N., Imamoglu S., Akalin N.S., Yuksel B., O'Rahilly S., Semple R.K. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat. Genet. 2009, 41:354-358.
34. True C., Kirigiti M., Ciofi P., Grove K.L., Smith M.S. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J. Neuroendocrinol. 2011, 23:52-64.
35. Wang Q.P., Nakai Y. Enkephalinergic innervation of GABAergic neurons in the dorsal raphe nucleus of the rat. Brain Res. Bull. 1993, 32:315-320.
36. Xu J., Kirigiti M.A., Grove K.L., Smith M.S. Regulation of food intake and gonadotropin-releasing hormone/luteinizing hormone during lactation: role of insulin and leptin. Endocrinology 2009, 150:4231-4240.
37. Yamada S., Uenoyama Y., Kinoshita M., Iwata K., Takase K., Matsui H., Adachi S., Inoue K., Maeda K.I., Tsukamura H. Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats. Endocrinology 2007, 148:2226-2232.