Skip to main content
Log in

Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

We recently identified a novel hypothalamic neuropeptide inhibiting gonadotropin release in the quail brain and termed it gonadotropin inhibitory hormone (GnIH). In this study, we investigated the localization and distribution of GnIH in both sexes of adult quails by immunohistochemistry with a specific antiserum against GnIH and in situ hybridization. Quantitative analysis demonstrated that the concentration of GnIH in the diencephalon was greater than that in the mesencephalon without sex difference. GnIH concentrations in the cerebrum and cerebellum were below the level of detectability. Clusters of GnIH-like immunoreactive (GnlH-ir) cell bodies were localized in the paraventricular nucleus (PVN) of the hypothalamus. There was no significant difference in the number of GnlH-ir cells in the PVN between males and females. By double immunostaining with antisera reacting with GnIH or avian posterior pituitary hormones (vasotocin and mesotocin), GnIH-ir cells were found to be parvocellular neurons in the ventral portion of PVN, which showed no immunoreaction with the antisera against vasotocin and mesotocin. In situ hybridization revealed the cellular localization of GnIH mRNA in the PVN. GnIH-ir nerve fibers were however widely distributed in the diencephalic and mesencephalic regions. Dense networks of immunoreactive fibers were found in the ventral paleostriatum, septal area, preoptic area, hypothalamus, and optic tectum. The most prominent fibers were seen in the median eminence of the hypothalamus and the dorsal motor nucleus of the vagus in the medulla oblongata. Thus, GnIH may participate not only in neuroendocrine functions, but also in behavioral and autonomic mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–E.
Fig. 2A–C.
Fig. 3A–C. A
Fig. 4A–D.
Fig. 5A–F.

Similar content being viewed by others

References

  • Chartrel N, Dujardin C, Leprince J, Desrues L, Tonon MC, Cellier E, Cosette P, Jouenne T, Simonnet G, Vaudry H (2002) Isolation, characterization, and distribution of a novel neuropeptide, Rana RFamide (R-RFa), in the brain of the European green frog Rana esculenta. J Comp Neurol 448:111–127

    Article  CAS  PubMed  Google Scholar 

  • D'Aniello B, Fiorentino M, Pinelli C, Meglio M di, Vallarino M, Rastogi RK (1996) Distribution of FMRFamide-like immunoreactivity in the brain and pituitary of Rana esculenta during development. Dev Brain Res 95:194–204

    Article  CAS  Google Scholar 

  • D'Aniello B, Pinelli C, Jadhao AG, Rastogi RK, Meyer DL (1999) Comparative analysis of FMRFamide-like immunoreactivity in caiman (Caiman crocodilus) and turtle (Trachemys scripta elegans) brains. Cell Tissue Res 298:549–559

    CAS  PubMed  Google Scholar 

  • Dockray GJ, Reeve JR Jr, Shively J, Gayton RJ, Barnard CS (1983) A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide. Nature 305:328–330

    CAS  PubMed  Google Scholar 

  • Fujii K, Kobayashi H (1992a) FMRFamide-like immunoreactivity in the brain of the Japanese quail, Coturnix coturnix japonica. Neuroendocrinol Lett 14:97–102

    CAS  Google Scholar 

  • Fujii K, Kobayashi H (1992b) FMRFamide-like immunoreactivity in the brain and pituitary of the goldfish, Carassius auratus. Ann Anat 174:217–222

    CAS  Google Scholar 

  • Fujimoto M, Takeshita K, Wang X, Takabatake I, Fujisawa Y, Teranishi H, Ohtani M, Muneoka Y, Ohta S (1998) Isolation and characterization of a novel bioactive peptide, Carassius RFamide (C-RFa), from the brain of the Japanese crucian carp. Biochem Biophys Res Commun 242:436–440

    Article  CAS  PubMed  Google Scholar 

  • Goossens N, Blähser S, Oksche A, Vandesande F, Dierickx K (1977) Immunocytochemical investigation of the hypothalamo-neurohypophysial system in birds. Cell Tissue Res 184:1–13

    CAS  PubMed  Google Scholar 

  • Haruta K, Yamashita T, Kawashima S (1991) Changes in arginine vasotocin content in the pituitary of the Medaka (Oryzias latipes) during osmotic stress. Gen Comp Endocrinol 83:327–336

    PubMed  Google Scholar 

  • Hinuma S, Habata Y, Fujii R, Kawamata Y, Hosoya M, Fukusumi S, Kitada C, Masuo Y, Asano T, Matsumoto H, Sekiguchi M, Kurokawa T, Nishimura O, Onda H, Fujino M (1998) A prolactin-releasing peptide in the brain. Nature 393:272–276

    Article  CAS  PubMed  Google Scholar 

  • Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, Yano T, Yamamoto T, Kawamata Y, Habata Y, Asada M, Kitada C, Kurokawa T, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M (2000) New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2:703–708

    Article  CAS  PubMed  Google Scholar 

  • Józsa R, Korf HW, Csernus V, Mess B (1988) Thyrotropin-releasing hormone (TRH)-immunoreactive structures in the brain of the domestic mallard. Cell Tissue Res 251:441–449

    PubMed  Google Scholar 

  • Katz DM, Karten HJ (1985) Topographic representation of visceral target organs within the dorsal motor nucleus of the vagus nerve of the pigeon Columba livia. J Comp Neurol 242:397–414

    CAS  PubMed  Google Scholar 

  • Kawamoto K (1985) Immunohistochemical study of vasopressin and oxytocin in the neurosecretory system during reorganization of the neural lobe in mice. Zool Sci 2:371–380

    CAS  Google Scholar 

  • Koda A, Ukena K, Teranishi H, Ohta S, Yamamoto K, Kikuyama S, Tsutsui K (2002) A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology 143:411–419

    CAS  PubMed  Google Scholar 

  • Lawrence CB, Celsi F, Brennand J, Luckman SM (2000) Alternative role for prolactin-releasing peptide in the regulation of food intake. Nat Neurosci 3:645–646

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, Zeng Z, Jacobson M, Williams DL Jr, Yu H, Bomford D, Figueroa D, Mallee J, Wang R, Evans J, Gould R, Austin CP (2001) Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276:36961–36969

    Article  CAS  PubMed  Google Scholar 

  • Maruyama M, Matsumoto H, Fujiwara K, Noguchi J, Kitada C, Hinuma S, Onda H, Nishimura O, Fujino M, Higuchi T, Inoue K (1999) Central administration of prolactin-releasing peptide stimulates oxytocin release in rats. Neurosci Lett 276:193–196

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H, Maruyama M, Noguchi J, Horikoshi Y, Fujiwara K, Kitada C, Hinuma S, Onda H, Nishimura O, Inoue K, Fujino M (2000) Stimulation of corticotropin-releasing hormone-mediated adrenocorticotropin secretion by central administration of prolactin-releasing peptide in rats. Neurosci Lett 285:234–238

    Article  CAS  PubMed  Google Scholar 

  • Mey J, Thanos S (1992) Development of the visual system of the chick—a review. J Hirnforsch 33:673–702

    CAS  PubMed  Google Scholar 

  • Panula P, Aarnisalo AA, Wasowicz K (1996) Neuropeptide FF, a mammalian neuropeptide with multiple functions. Prog Neurobiol 48:461–487

    Article  CAS  PubMed  Google Scholar 

  • Panula P, Kalso E, Nieminen M, Kontinen VK, Brandt A, Pertovaara A (1999) Neuropeptide FF and modulation of pain. Brain Res 848:191–196

    Article  CAS  PubMed  Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Balthazart J (1996) The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior (Review). Front Neuroendocrinol 17:51–125

    Article  CAS  PubMed  Google Scholar 

  • Peeters K, Gerets HH, Arckens L, Vandesande F (2000) Distribution of pituitary adenylate cyclase-activating polypeptide and pituitary adenylate cyclase-activating polypeptide type I receptor mRNA in the chicken brain. J Comp Neurol 423:66–82

    CAS  PubMed  Google Scholar 

  • Pinelli C, D'Aniello B, Fiorentino M, Calace P, Meglio M di, Iela L, Meyer DL, Bagnara JT, Rastogi RK (1999) Distribution of FMRFamide-like immunoreactivity in the amphibian brain: comparative analysis. J Comp Neurol 414:275–305

    Article  CAS  PubMed  Google Scholar 

  • Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671

    CAS  PubMed  Google Scholar 

  • Samson WK, Resch ZT, Murphy TC (2000) A novel action of the newly described prolactin-releasing peptides: cardiovascular regulation. Brain Res 858:19–25

    Article  CAS  PubMed  Google Scholar 

  • Satake H, Hisada M, Kawada T, Minakata H, Ukena K, Tsutsui K (2001)Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem J 354:379–385

    Article  CAS  PubMed  Google Scholar 

  • Sawada K, Ukena K, Kikuyama S, Tsutsui K (2002a) Identification of a cDNA encoding a novel amphibian growth hormone-reseasing peptide and localization of its transcript. J Endocrinol 174:395–402

    CAS  PubMed  Google Scholar 

  • Sawada K, Ukena K, Satake H, Iwakoshi E, Minakata H, Tsutsui K (2002b) Novel fish hypothalamic neuropeptide: cloning of a cDNA encoding the precursor polypeptide and identification and localization of the mature peptide. Eur J Biochem 269:6000–6008

    CAS  PubMed  Google Scholar 

  • Seal LJ, Small CJ, Kim MS, Stanley SA, Taheri S, Ghatei MA, Bloom SR (2000) Prolactin releasing peptide (PrRP) stimulates luteinizing hormone (LH) and follicle stimulating hormone (FSH) via a hypothalamic mechanism in male rats. Endocrinology 141:1909–1912

    PubMed  Google Scholar 

  • Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661–667

    Article  CAS  PubMed  Google Scholar 

  • Ukena K, Tsutsui K (2001) Distribution of novel RFamide-related peptide-like immunoreactivity in the mouse central nervous system. Neurosci Lett 300:153–156

    Article  CAS  PubMed  Google Scholar 

  • Ukena K, Kohchi C, Tsutsui K (1999) Expression and activity of 3β-hydroxysteroid dehydrogenase/∆5-∆4-isomerase in the rat Purkinje neuron during neonatal life. Endocrinology 140:805–813

    CAS  PubMed  Google Scholar 

  • Ukena K, Iwakoshi E, Minakata H, Tsutsui K (2002) A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett 512:255–258

    Article  CAS  PubMed  Google Scholar 

  • Yamada S, Mikami S (1985) Immunohistochemical localization of corticotropin-releasing factor (CRF)-containing neurons in the hypothalamus of the Japanese quail, Coturnix coturnix. Cell Tissue Res 239:299–304

    CAS  PubMed  Google Scholar 

  • Yang HY, Fratta W, Majane EA, Costa E (1985) Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci USA 82:7757–7761

    PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. S. Kawashima (Zenyaku Kogyo Ltd., Japan) for the supply of the antiserum cross-reacting with avian vasotocin or mesotocin and his valuable discussion.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazuyoshi Tsutsui.

Additional information

This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan (12440233, 12894021, 13210101) to K.T., the SUNBOR Grant from the Suntory Institute for Bioorganic Research, Osaka, Japan to K.U., and the Narishige Zoological Science Award to K.U.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ukena, K., Ubuka, T. & Tsutsui, K. Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res 312, 73–79 (2003). https://doi.org/10.1007/s00441-003-0700-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-003-0700-x

Keywords

Navigation