Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The role of gonadotrophin-inhibitory hormone (GnIH) in the inhibition of the reproductive axis has been well-established in birds and mammals. However, its role in other vertebrates, such as the teleost fish, remains controversial. In this context, the present study aimed to evaluate whether GnIH modulates the release of gonadotrophins and growth hormone (GH) in the cichlid fish Cichlasoma dimerus. First, we partially sequenced the precursor polypeptide for GnIH and identified three putative GnIH peptides. Next, we analysed the expression of this precursor polypeptide via a polymerase chain reaction in the reproductive axis of both sexes. We found a high expression of the polypeptide in the hypothalamus and gonads of males. Immunocytochemistry allowed the observation of GnIH-immunoreactive somata in the nucleus posterioris periventricularis and the nucleus olfacto-retinalis, with no differences between the sexes. GnIH-immunoreactive fibres were present in all brain regions, with a high density in the nucleus lateralis tuberis and at both sides of the third ventricle. Finally, we performed in vitro studies on intact pituitary cultures to evaluate the effect of two doses (10−6 m and 10−8 m) of synthetic C. dimerus (cd-) LPQRFa-1 and LPQRFa-2 on the release of gonadotrophins and GH. We observed that cd-LPQRFa-1 decreased β-luteinising hormone (LH) and β-follicle-stimulating hormone (FSH) and also increased GH release to the culture medium. The release of β-FSH was increased only when it was stimulated with the higher cd-LPQRFa-2 dose. The results of the present study indicate that cd-LPQRFa-1, the cichlid fish GnIH, inhibits β-LH and β-FSH release and stimulates GH release in intact pituitary cultures of C. dimerus. The results also show that cd-LPQRF-2 could act as an β-FSH-releasing factor in this fish species. © 2016 British Society for Neuroendocrinology

Registro:

Documento: Artículo
Título:Gonadotrophin-Inhibitory Hormone in the Cichlid Fish Cichlasoma dimerus: Structure, Brain Distribution and Differential Effects on the Secretion of Gonadotrophins and Growth Hormone
Autor:Di Yorio, M.P.; Pérez Sirkin, D.I.; Delgadin, T.H.; Shimizu, A.; Tsutsui, K.; Somoza, G.M.; Vissio, P.G.
Filiación:Laboratorio de Neuroendocrinología del Crecimiento y la Reproducción, DBBE, FCEN-UBA/IBBEA-CONICET-UBA, Ciudad Universitaria, (C1428EHA), Buenos Aires, Argentina
National Research Institute of Fisheries Science, Fisheries Research Agency, Yokohama, Kanagawa, Japan
Department of Biology and Center for Medical Life Science, Waseda University, Tokyo, Japan
Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús (IIB-INTECH), CONICET-UNSAM, Chascomús, Buenos Aires, Argentina
Palabras clave:fish; follicle-stimulating hormone; gonadotrophin-inhibitory hormone; growth hormone; luteinising hormone; follitropin; follitropin releasing factor; gonadotrophin inhibitory hormone; gonadotropin; growth hormone; luteinizing hormone; neuropeptide; peptide derivative; polypeptide; synthetic LPQRFa 1 peptide; synthetic LPQRFa 2 peptide; synthetic peptide; unclassified drug; fish protein; follitropin beta subunit; gonadotropin; growth hormone; hypothalamus hormone; messenger RNA; peptide hormone; adult; animal cell; animal experiment; Article; brain; brain region; brain third ventricle; cell density; cell nucleus; Cichlasoma dimerus; cichlid; controlled study; culture medium; female; follitropin release; gonad; gonadotropin release; growth hormone release; hypophysis; hypothalamus; immunocytochemistry; immunoreactivity; in vitro study; in vivo study; male; nerve fiber; neuromodulation; nonhuman; olfactory nerve; peptide synthesis; polymerase chain reaction; priority journal; protein expression; reproduction; retina; somatic cell; animal; cichlid; drug effects; genetics; metabolism; secretion (process); Animals; Cichlids; Female; Fish Proteins; Follicle Stimulating Hormone, beta Subunit; Gonadotropins; Growth Hormone; Hypothalamic Hormones; Male; Peptide Hormones; Pituitary Gland; RNA, Messenger
Año:2016
Volumen:28
Número:5
DOI: http://dx.doi.org/10.1111/jne.12377
Título revista:Journal of Neuroendocrinology
Título revista abreviado:J. Neuroendocrinol.
ISSN:09538194
CODEN:JOUNE
CAS:follitropin, 9002-68-0; follitropin releasing factor, 9034-38-2; gonadotropin, 63231-54-9; growth hormone, 36992-73-1, 37267-05-3, 66419-50-9, 9002-72-6; luteinizing hormone, 39341-83-8, 9002-67-9; Fish Proteins; Follicle Stimulating Hormone, beta Subunit; Gonadotropins; Growth Hormone; Hypothalamic Hormones; Peptide Hormones; RNA, Messenger
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09538194_v28_n5_p_DiYorio

Referencias:

  • Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., Ishii, S., Sharp, P.J., A novel avian hypothalamic peptide inhibiting gonadotropin release (2000) Biochem Biophys Res Commun, 275, pp. 661-667
  • Satake, H., Hisada, M., Kawada, T., Minakata, H., Ukena, K., Tsutsui, K., Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release (2001) Biochem J, 354, pp. 379-385
  • Ubuka, T., Kim, S., Huang, Y.C., Reid, J., Jiang, J., Osugi, T., Chowdhury, V.S., Bentley, G.E., Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain (2008) Endocrinology, 149, pp. 268-278
  • Tobari, Y., Iijima, N., Tsunekawa, K., Osugi, T., Okanoya, K., Tsutsui, K., Ozawa, H., Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): peptide isolation, cDNA cloning and brain distribution (2010) Peptides, 31, pp. 816-826
  • Ukena, K., Tsutsui, K., A new member of the hypothalamic RF-amide peptide family, LPXRF-amide peptides: structure, localization, and function (2005) Mass Spectrom Rev, 24, pp. 469-486
  • Tsutsui, K., Ukena, K., Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity (2006) Peptides, 27, pp. 1121-1129
  • Tsutsui, K., A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): biosynthesis, mode of action and functional significance (2009) Prog Neurobiol, 88, pp. 76-88
  • Tsutsui, K., How to contribute to the progress of neuroendocrinology: new insights from discovering novel neuropeptides and neurosteroids regulating pituitary and brain functions (2016) Gen Comp Endocrinol, 227, pp. 3-15
  • Tsutsui, K., Bentley, G.E., Bedecarrats, G.T., Osugi, T., Ubuka, T., Kriegsfeld, L.J., Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function (2010) Front Neuroendocrinol, 31, pp. 284-295
  • Tsutsui, K., Bentley, G.E., Kriegsfeld, L.J., Osugi, T., Seong, J.Y., Vaudry, H., Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction (2010) J Neuroendocrinol, 22, pp. 716-727
  • Ogawa, S., Parhar, I.S., Structural and functional divergence of gonadotropin-inhibitory hormone from jawless fish to mammals (2014) Front Endocrinol (Lausanne), 5, p. 177
  • Moussavi, M., Wlasichuk, M., Chang, J.P., Habibi, H.R., Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish (2012) Mol Cell Endocrinol, 350, pp. 53-60
  • Biran, J., Golan, M., Mizrahi, N., Ogawa, S., Parhar, I.S., Levavi-Sivan, B., LPXRFa, the piscine ortholog of GnIH, and LPXRF receptor positively regulate gonadotropin secretion in Tilapia (Oreochromis niloticus) (2014) Endocrinology, 155, pp. 4391-4401
  • Zhang, Y., Li, S., Liu, Y., Lu, D., Chen, H., Huang, X., Liu, X., Cheng, C.H., Structural diversity of the GnIH/GnIH receptor system in teleost: its involvement in early development and the negative control of LH release (2010) Peptides, 31, pp. 1034-1043
  • Qi, X., Zhou, W., Li, S., Lu, D., Yi, S., Xie, R., Liu, X., Lin, H., Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus (2013) Mol Cell Endocrinol, 366, pp. 9-20
  • Wang, Q., Qi, X., Guo, Y., Li, S., Zhang, Y., Liu, X., Lin, H., Molecular identification of GnIH/GnIHR signal and its reproductive function in protogynous hermaphroditic orange-spotted grouper (Epinephelus coioides) (2015) Gen Comp Endocrinol, 216, pp. 9-23
  • Amano, M., Moriyama, S., Iigo, M., Kitamura, S., Amiya, N., Yamamori, K., Ukena, K., Tsutsui, K., Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon (2006) J Endocrinol, 188, pp. 417-423
  • Shahjahan, M., Ikegami, T., Osugi, T., Ukena, K., Doi, H., Hattori, A., Tsutsui, K., Ando, H., Synchronised expressions of LPXRFamide peptide and its receptor genes: seasonal, diurnal and circadian changes during spawning period in grass puffer (2011) J Neuroendocrinol, 23, pp. 39-51
  • Moussavi, M., Wlasichuk, M., Chang, J.P., Habibi, H.R., Seasonal effects of GnIH on basal and GnRH-induced goldfish somatotrope functions (2014) J Endocrinol, 223, pp. 191-202
  • Yin, H., Ukena, K., Ubuka, T., Tsutsui, K., A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity (2005) J Endocrinol, 184, pp. 257-266
  • Hinuma, S., Shintani, Y., Fukusumi, S., Iijima, N., Matsumoto, Y., Hosoya, M., Fujii, R., Fujino, M., New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals (2000) Nat Cell Biol, 2, pp. 703-708
  • Ikemoto, T., Park, M.K., Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations (2005) J Reprod Develop, 51, pp. 359-377
  • Alonso, F., Cánepa, M.M., Guimarães, M.R., Pandolfi, M., Social and reproductive physiology and behavior of the Neotropical cichlid fish Cichlasoma dimerus under laboratory conditions (2011) Neotrop Ichthyol, 9, pp. 559-570
  • Pérez Sirkin, D.I., Cánepa, M.M., Fossati, M., Fernandino, J.I., Delgadin, T., Canosa, L.F., Somoza, G.M., Vissio, P.G., Melanin concentrating hormone (MCH) is involved in the regulation of growth hormone in Cichlasoma dimerus (Cichlidae, Teleostei) (2012) Gen Comp Endocrinol, 176, pp. 102-111
  • Ramallo, M.R., Grober, M., Cánepa, M.M., Morandini, L., Pandolfi, M., Arginine-vasotocin expression and participation in reproduction and social behavior in male of the cichlid fish Cichlasoma dimerus (2012) Gen Comp Endocrinol, 179, pp. 221-231
  • Delgadin, T.H., Pérez Sirkin, D.I., Di Yorio, M.P., Arranz, S.E., Vissio, P.G., GH, IGF-I and GH receptors mRNA expression in response to growth impairment following a food deprivation period in individually housed cichlid fish Cichlasoma dimerus (2015) Fish Physiol Biochem, 41, pp. 51-60
  • Di Yorio, M.P., Delgadin, T.H., Pérez Sirkin, D.I., Vissio, P.G., Growth hormone, luteinizing hormone, and follicle-stimulating hormone regulation by neuropeptide Y in both sexes of the cichlid fish, Cichlasoma dimerus (2015) Fish Physiol Biochem, 41, pp. 843-852
  • Pandolfi, M., Cánepa, M.M., Meijide, F.J., Alonso, F., Vázquez, G.R., Maggese, M.C., Vissio, P.G., Studies on the reproductive and developmental biology of Cichlasoma dimerus (Percifomes, Cichlidae) (2009) Biocell, 33, pp. 1-18
  • Pandolfi, M., Paz, D.A., Maggese, C., Meijide, F.J., Vissio, P.G., Immunocytochemical localization of different cell types in the adenohypophysis of the cichlid fish Cichlasoma dimerus (Heckel, 1840) (2001) Biocell, 25, pp. 35-42
  • Pandolfi, M., Cánepa, M.M., Ravaglia, M.A., Maggese, M.C., Paz, D.A., Vissio, P.G., Melanin-concentrating hormone system in the brain and skin of the cichlid fish Cichlasoma dimerus: anatomical localization, ontogeny and distribution in comparison to alpha-melanocyte-stimulating hormone-expressing cells (2003) Cell Tissue Res, 311, pp. 61-69
  • Pandolfi, M., Muñoz Cueto, J.A., Lo Nostro, F.L., Downs, J.L., Paz, D.A., Maggese, M.C., Urbanski, H.F., GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides (2005) Cell Tissue Res, 321, pp. 219-232
  • Cánepa, M., Pozzi, A., Astola, A., Maggese, M.C., Vissio, P., Effect of salmon melanin-concentrating hormone and mammalian gonadotrophin-releasing hormone on somatolactin release in pituitary culture of Cichlasoma dimerus (2008) Cell Tissue Res, 333, pp. 49-59
  • Pérez, S.D., Suzuki, H., Cánepa, M.M., Vissio, P.G., Orexin and neuropeptide Y: tissue specific expression and immunoreactivity in the hypothalamus and preoptic area of the cichlid fish Cichlasoma dimerus (2013) Tissue Cell, 45, pp. 452-459
  • Paullada-Salmerón, J.A., Cowan, M., Aliaga-Guerrero, M., Gómez, A., Zanuy, S., Mañanos, E., Muñoz-Cueto, J.A., LPXRFa peptide system in the European sea bass: a molecular and immunohistochemical approach (2016) J Comp Neurol, 524, pp. 176-198
  • Southey, B.R., Amare, A., Zimmerman, T.A., Rodriguez-Zas, S.L., Sweedler, J.V., NeuroPred: a tool to predict cleavage sites in neuropeptide precursors and provide the masses of the resulting peptides (2006) Nucleic Acids Res, 34, pp. W267-W272
  • Cerdá-Reverter, J.M., Zanuy, S., Muñoz-Cueto, J.A., Cytoarchitectonic study of the brain of a perciform species. The sea bass (Dicentrarchus labrax). II. The diencephalon (2001) J Morphol, 247, pp. 229-251
  • Sawada, K., Ukena, K., Satake, H., Iwakoshi, E., Minakata, H., Tsutsui, K., Novel fish hypothalamic neuropeptide (2002) Eur J Biochem, 269, pp. 6000-6008
  • Biswas, S., Jadhao, A.G., Pinelli, C., Palande, N.V., Tsutsui, K., GnIH and GnRH expressions in the central nervous system and pituitary of Indian major carp, Labeo rohita during ontogeny: an immunocytochemical study (2014) Gen Comp Endocrinol, 220, pp. 88-92
  • Volkoff, H., Xu, M., MacDonald, E., Hoskins, L., Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes (2009) Comp Biochem Physiol A Mol Integr Physiol, 153, pp. 8-12
  • Kalra, S.P., Dube, M.G., Pu, S., Xu, B., Horvath, T.L., Kalra, P.S., Interacting appetite-regulating pathways in the hypothalamic regulation of body weight (1999) Endocr Rev, 20, pp. 68-100
  • Johnson, M.A., Tsutsui, K., Fraley, G.S., Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat (2007) Horm Behav, 51, pp. 171-180
  • Murakami, M., Matsuzaki, T., Iwasa, T., Yasui, T., Irahara, M., Osugi, T., Tsutsui, K., Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats (2008) J Endocrinol, 199, pp. 105-112
  • Tachibana, T., Sato, M., Takahashi, H., Ukena, K., Tsutsui, K., Furuse, M., Gonadotropin-inhibiting hormone stimulates feeding behavior in chicks (2005) Brain Res, 1050, pp. 94-100
  • McConn, B., Wang, G., Yi, J., Gilbert, E.R., Osugi, T., Ubuka, T., Tsutsui, K., Cline, M.A., Gonadotropin-inhibitory hormone-stimulation of food intake is mediated by hypothalamic effects in chicks (2014) Neuropeptides, 48, pp. 327-334
  • Kriegsfeld, L.J., Ubuka, T., Bentley, G.E., Tsutsui, K., Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals (2015) Front Neuroendocrinol, 37, pp. 65-75
  • Fryer, J.N., Boudreault-Chateauvert, C., Kirby, R.P., Pituitary afferents originating in the paraventricular organ (PVO) of the goldfish hypothalamus (1985) J Comp Neurol, 242, pp. 475-484
  • Moussavi, M., Wlasichuk, M., Chang, J.P., Habibi, H.R., Seasonal effect of gonadotrophin inhibitory hormone on gonadotrophin-releasing hormone-induced gonadotroph functions in the goldfish pituitary (2013) J Neuroendocrinol, 25, pp. 506-516
  • Clarke, I.J., Parkington, H.C., Gonadotropin inhibitory hormone (GnIH) as a regulator of gonadotropes (2014) Mol Cell Endocrinol, 385, pp. 36-44
  • Koda, A., Ukena, K., Teranishi, H., Ohta, S., Yamamoto, K., Kikuyama, S., Tsutsui, K., A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity (2002) Endocrinology, 143, pp. 411-419
  • Clarke, I.J., Sari, I.P., Qi, Y., Smith, J.T., Parkington, H.C., Ubuka, T., Iqbal, J., Bentley, G.E., Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion (2008) Endocrinology, 149, pp. 5811-5821
  • Canosa, L.F., Chang, J.P., Peter, R.E., Neuroendocrine control of growth hormone in fish (2007) Gen Comp Endocrinol, 151, pp. 1-26

Citas:

---------- APA ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Delgadin, T.H., Shimizu, A., Tsutsui, K., Somoza, G.M. & Vissio, P.G. (2016) . Gonadotrophin-Inhibitory Hormone in the Cichlid Fish Cichlasoma dimerus: Structure, Brain Distribution and Differential Effects on the Secretion of Gonadotrophins and Growth Hormone. Journal of Neuroendocrinology, 28(5).
http://dx.doi.org/10.1111/jne.12377
---------- CHICAGO ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Delgadin, T.H., Shimizu, A., Tsutsui, K., Somoza, G.M., et al. "Gonadotrophin-Inhibitory Hormone in the Cichlid Fish Cichlasoma dimerus: Structure, Brain Distribution and Differential Effects on the Secretion of Gonadotrophins and Growth Hormone" . Journal of Neuroendocrinology 28, no. 5 (2016).
http://dx.doi.org/10.1111/jne.12377
---------- MLA ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Delgadin, T.H., Shimizu, A., Tsutsui, K., Somoza, G.M., et al. "Gonadotrophin-Inhibitory Hormone in the Cichlid Fish Cichlasoma dimerus: Structure, Brain Distribution and Differential Effects on the Secretion of Gonadotrophins and Growth Hormone" . Journal of Neuroendocrinology, vol. 28, no. 5, 2016.
http://dx.doi.org/10.1111/jne.12377
---------- VANCOUVER ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Delgadin, T.H., Shimizu, A., Tsutsui, K., Somoza, G.M., et al. Gonadotrophin-Inhibitory Hormone in the Cichlid Fish Cichlasoma dimerus: Structure, Brain Distribution and Differential Effects on the Secretion of Gonadotrophins and Growth Hormone. J. Neuroendocrinol. 2016;28(5).
http://dx.doi.org/10.1111/jne.12377