Artículo

Di Yorio, M.P.; Pérez Sirkin, D.I.; Muñoz-Cueto, J.A.; Delgadin, T.H.; Tsutsui, K.; Somoza, G.M.; Vissio, P.G. "Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus" (2019) General and Comparative Endocrinology. 273:144-151
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:

Reproduction is regulated by the hypothalamic-pituitary-gonadal axis. The first neuropeptide identified that regulates this function was the decapeptide gonadotropin-releasing hormone (GnRH). Nowadays, in gnatostomates, a number of GnRH variants have been identified and classified into three different types: GnRH1, GnRH2, and GnRH3. Almost 30 years later, a new peptide that inhibits gonadotropin synthesis and secretion was discovered and thus named as gonadotropin-inhibitory hormone (GnIH). In avians and mammals, the interaction and regulation between GnRH and GnIH neurons has been widely studied; however, in other vertebrate groups there is little information about the relationship between these neurons. In previous works, three GnRH variants and a GnIH propeptide were characterized in Cichlasoma dimerus, and it was demonstrated that GnIH inhibited gonadotropins release in this species. Because no innervation was detected at the pituitary level, we speculate that GnIH would inhibit gonadotropins via GnRH. Thus, the aim of the present study was to evaluate the anatomical relationship between neurons expressing GnIH and the three GnRH variants by double labelling confocal immunofluorescence in adults of C. dimerus. Our results showed no apparent contacts between GnIH and GnRH1, fiber to fiber interactions between GnIH and GnRH2, and co-localization of GnIH and GnRH3 variant in neurons of the nucleus olfacto-retinalis. In conclusion, whether GnIH regulates the expression or secretion of GnRH1 in this species, an indirect modulation seems more plausible. Moreover, the present results suggest an interaction between GnIH and GnRH2 systems. Finally, new clues were provided to investigate the role of nucleus olfacto-retinalis cells and putative GnIH and GnRH3 interactions in the modulation of the reproductive network in teleost fish. © 2018 Elsevier Inc.

Registro:

Documento: Artículo
Título:Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus
Autor:Di Yorio, M.P.; Pérez Sirkin, D.I.; Muñoz-Cueto, J.A.; Delgadin, T.H.; Tsutsui, K.; Somoza, G.M.; Vissio, P.G.
Filiación:Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Intituto de Biodiversidad y Biología Experimental y Aplicada (IBBEA), CONICET-Universidad de Buenos Aires, Buenos Aires, Argentina
Department of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Marine Campus of International Excellence (CEIMAR) and Agrifood Campus of International Excellence (ceiA3), INMAR-CACYTMAR Research Institutes, Puerto Real University Campus, Puerto Real, Spain
Department of Biology and Center for Medical Life Science, Waseda UniversityTokyo 162-8480, Japan
Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús, CONICET-UNSAM, Chascomús, Argentina
Palabras clave:Brain; Fish; GnIH; GnRH variants; Neurons; Pituitary
Año:2019
Volumen:273
Página de inicio:144
Página de fin:151
DOI: http://dx.doi.org/10.1016/j.ygcen.2018.06.010
Título revista:General and Comparative Endocrinology
Título revista abreviado:Gen. Comp. Endocrinol.
ISSN:00166480
CODEN:GCENA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00166480_v273_n_p144_DiYorio

Referencias:

  • Amano, M., Moriyama, S., Iigo, M., Kitamura, S., Amiya, N., Yamamori, K., Ukena, K., Tsutsui, K., Novel fish hypothalamic neuropeptides stimulate the reléase of gonadotrophins and growth hormone from the pituitary of sockeye salmon (2006) J. Endocrinol., 188, pp. 417-423
  • Aliaga-Guerrero, M., Paullada-Salmerón, J.A., Piquer, V., Mañanós, E.L., Muñoz-Cueto, J.A., Gonadotropin-inhibitory hormone in the flatfish, Solea senegalensis: molecular cloning, brain localization and physiological effects (2018) J. Comp. Neurol., 526, pp. 349-370
  • Bentley, G.E., Kriegsfeld, L.J., Osugi, T., Ukena, K., O'Brien, S., Perfito, N., Moore, I.T., Wingfield, J.C., Interactions of gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH) in birds and mammals (2006) J. Exp. Zool., 305A, pp. 807-814
  • 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 (2015) Gen. Comp. Endocrinol., 220, pp. 88-92
  • Burgus, R., Butcher, M., Ling, N., Monahan, M., Rivier, J., Fellows, R., Amoss, M., Guillemin, R., Molecular structure of the hypothalamic factor (LRF) of ovine origin monitoring the secretion of pituitary gonadotropic hormone of luteinization (LH) (1971) CR Acad. Sci. Hebd. Seances. Acad. Sci., D273, pp. 1611-1613
  • Clarke, I.J., Smith, J.T., Henry, B.A., Oldfield, B.J., Stefanidis, A., Millar, R.P., Sari, I.P., Fraley, G.S., Gonadotropin-inhibitory hormone is a hypothalamic peptide that provides a molecular switch between reproduction and feeding (2012) Neuroendocrinology, 9, pp. 305-316
  • Chowdhury, V.S., Yamamoto, K., Ubuka, T., Bentley, G.E., Hattori, A., Tsutsui, K., Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus (2010) Endocrinology, 151, pp. 271-280
  • Decatur, W.A., Hall, J.A., Smith, J.J., Li, W., Sower, S.A., Insight from the lamprey genome: glimpsing early vertebrate development via neuroendocrine-associated genes and shared synteny of gonadotropin-releasing hormone (GnRH) (2013) Gen. Comp. Endocrinol., 192, pp. 237-245
  • Di Yorio, M.P., Pérez Sirkin, D.I., Delgadin, T.H., Shimizu, A., Tsutsui, K., Somoza, G.M., Vissio, P.G., Gonadotrophin-inhibitory hormone in the cichlid fish Cichlasoma dimerus: structure, brain distribution and differential effects on the secretion of gonadotrophins and growth hormone (2016) J. Neuroendocrinol., 28
  • Di Yorio, M.P., Sallemi, J.E., Toledo Solís, F.J., Pérez Sirkin, D.I., Delgadin, T.H., Tsutsui, K., Vissio, P.G., Ontogeny of gonadotropin-inhibitory hormone (GnIH) in the cichlid fish Cichlasoma dimerus (2018) J. Neuroendocrinol., 13, p. e12608
  • Golan, M., Zelinger, E., Zohar, Y., Levavi-Sivan, B., Architecture of GnRH-gonadotrope-vasculature reveals a dual mode of gonadotropin regulation in fish (2015) Endocrinology, 156, pp. 4163-4173
  • González-Martínez, D., Zmora, N., Mañanos, E., Saligaut, D., Zanuy, S., Zohar, Y., Elizur, A., Muñoz-Cueto, J.A., Immunohistochemical localization of three different prepro-GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides (2002) J. Comp. Neurol., 446, pp. 95-113
  • González-Martínez, D., Zmora, N., Saligaut, D., Zanuy, S., Elizur, A., Kah, O., Muñoz-Cueto, J.A., New insights in developmental origins of different GnRH (gonadotrophin-releasing hormone) systems in perciform fish: an immunohistochemical study in the European sea bass (Dicentrarchus labrax) (2004) J. Chem. Neuroanat., 28, pp. 1-15
  • Guilgur, L.G., Moncaut, N.P., Canário, A.V., Somoza, G.M., Evolution of GnRH ligands and receptors in gnathostomata (2006) Comp. Biochem. Physiol., 144A, pp. 272-283
  • 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
  • Kah, O., Lethimonier, C., Somoza, G., Guilgur, L.G., Vaillant, C., Lareyre, J.J., GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective (2007) Gen. Comp. Endocrinol., 153, pp. 346-364
  • Kavanaugh, S.I., Nozaki, M., Sower, S.A., Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey (2008) Endocrinology, 149, pp. 3860-3869
  • Kawai, T., Abe, H., Akazome, Y., Oka, Y., Neuromodulatory effect of GnRH on the synaptic transmission of the olfactory bulbar neural circuit in goldfish, Carassius auratus (2010) J. Neurophysiol., 104, pp. 3540-3550
  • Kim, D.K., Cho, E.B., Moon, M.J., Park, S., Hwang, J.I., Kah, O., Sower, S.A., Seong, J.Y., Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes (2011) Gen. Comp. Endocrinol., 170, pp. 68-78
  • Klingerman, C.M., Williams, W.P., 3rd, Simberlund, J., Brahme, N., Prasad, A., Schneider, J.E., Kriegsfeld, L.J., Food restriction-induced changes in gonadotropin-inhibiting hormone cells are associated with changes in sexual motivation and food hoarding, but not sexual performance and food intake (2011) Front. Endocrinol. (Lausanne), 2, p. 101
  • 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
  • Kriegsfeld, L.J., Mei, D.F., Bentley, G.E., Ubuka, T., Mason, A.O., Inoue, K., Ukena, K., Silver, R., Identifcation and characterization of a gonadotropin-inhibitory system in the brains of mammals (2006) Proc. Natl. Acad. Sci. U.S.A., 103, pp. 2410-2415
  • Matsuo, H., Baba, Y., Nair, R.G., Arimura, A., Schally, A.V., Structure of the porcine LH-and FSH-releasing hormone. I. The proposed amino acid sequence (1971) Biochem. Biophys. Res. Commun., 43, pp. 1334-1339
  • Matsuda, K., Nakamura, K., Shimakura, S., Miura, T., Kageyama, H., Uchiyama, M., Shioda, S., Ando, H., Inhibitory effect of chicken gonadotropin-releasing hormone II on foodintake in the goldfish, Carassius auratus (2008) Horm. Behav., 54, pp. 83-89
  • Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kangawa, K., Matsuo, H., Identification of the second gonadotropin-releasing hormone in chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species (1984) Proc. Natl. Acad. Sci. U.S.A., 81, pp. 3874-3878
  • Mohamed, J.S., Thomas, P., Khan, I.A., Isolation, cloning, and expression of three prepro-GnRH mRNAs in Atlantic croaker brain and pituitary (2005) J. Comp. Neurol., 488, pp. 384-395
  • Morgan, K., Millar, R.P., Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species (2004) Gen. Comp. Endocrinol., 139, pp. 191-197
  • Muñoz-Cueto, J.A., Paullada-Salmerón, J.A., Aliaga-Guerrero, M., Cowan, M.E., Parhar, I.S., Ubuka, T., A journey through the gonadotropin-inhibitory hormone system of fish (2017) Front. Endocrinol., 8, p. 285
  • Ogawa, S., Akiyama, G., Kato, S., Soga, T., Sakuma, Y., Parhar, I.S., Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids (2006) Neurosci. Lett., 403, pp. 201-205
  • Ogawa, S., Sivalingam, M., Biran, J., Golan, M., Anthonysamy, R.S., Levavi-Sivan, B., Parhar, I.S., Distribution of LPXRFa, a gonadotropin-inhibitory hormone ortholog peptide, and LPXRFa receptor in the brain and pituitary of the tilapia (2016) J. Comp. Neurol., 524, pp. 2753-2775
  • Osugi, T., Ubuka, T., Tsutsui, K., An evolutionary scenario for gonadotrophin-inhibitory hormone in chordates (2015) J. Neuroendocrinol., 27, pp. 556-566
  • Pandolfi, M., Cueto, J.A.M., Nostro, F.L.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
  • Parhar, I.S., Ogawa, S., Ubuka, T., Reproductive neuroendocrine pathways of social behavior (2016) Front. Endocrinol. (Lausanne), 7, p. 28
  • Park, M.K., Wakabayashi, K., Preparation of a monoclonal antibody to common aminoacid sequence of LHRH and its application (1986) Endocrinol. Japn., 33, pp. 257-272
  • Paullada-Salmerón, J.A., Cowan, M., Aliaga-Guerrero, M., Gómez, A., Zanuy, S., Mañanos, E., Muñoz-Cueto, J.A., LPXRFapeptidesystem in the European sea bass: a molecular and immunohistochemical approach (2016) J. Comp. Neurol., 524, pp. 176-198
  • Paullada-Salmerón, J.A., Cowan, M., Aliaga-Guerrero, M., Morano, F., Zanuy, S., Muñoz-Cueto, J.A., Gonadotropin inhibitory hormone down-regulates the brain-pituitary reproductive axis of male European sea bass (Dicentrarchus labrax) (2016) Biol. Reprod., 94, pp. 1-11
  • Paullada-Salmerón, J.A., Cowan, M., Aliaga-Guerrero, M., López-Olmeda, J.F., Mañanós, E.L., Zanuy, S., Muñoz-Cueto, J.A., Testicular steroidogenesis and locomotor activity are regulated by gonadotropin-inhibitory hormone in male European sea bass (2016) PLoS One, 11, p. e0165494
  • Pawson, A.J., Morgan, K., Maudsley, S.R., Millar, R.P., Type II gonadotrophin-releasing hormone (GnRH-II) in reproductive biology (2003) Reproduction, 126, pp. 271-278
  • Peragine, D.E., Pokarowski, M., Mendoza-Viveros, L., Swift-Gallant, A., Cheng, H.M., Bentley, G.E., Holmes, M.M., RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal (2017) Proc. Natl. Acad. Sci. U.S.A., 114, pp. 1207-1212
  • 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
  • Piekarski, D.J., Zhao, S., Jennings, K.J., Iwasa, T., Legan, S.J., Mikkelsen, J.D., Tsutsui, K., Kriegsfeld, L.J., Gonadotropin-inhibitory hormone reduces sexual motivation but not lordosis behavior in female Syrian hamsters (Mesocricetus auratus) (2013) Horm. Behav., 64, pp. 501-510
  • Plachetzki, D.C., Tsai, P.S., Kavanaugh, S.I., Sower, S.A., Ancient origins of metazoan gonadotropin-releasing hormone and their receptors revealed by phylogenomic analyses (2016) Gen. Comp. Endocrinol., 234, pp. 10-19
  • Roch, G.J., Busby, E.R., Sherwood, N.M., GnRH receptors and peptides: skating backward (2014) Gen. Comp. Endocrinol., 209, pp. 118-134
  • Sawada, K., Ukena, K., Satake, H., Iwakoshi, E., Minakata, H., Tsutsui, K., Novel fish hypothalamic neuropeptide (2002) Eur. J. Biochem., 269, pp. 6000-6008
  • Seeburg, P.H., Adelman, J.P., Characterization of cDNA for precursor of human luteinizing hormone releasing hormone (1984) Nature, 311, pp. 666-668
  • Servili, A., Lethimonier, C., Lareyre, J.J., López-Olmeda, J.F., Sánchez-Vázquez, F.J., Kah, O., Muñoz-Cueto, J.A., The highly conserved gonadotropin-releasing hormone-2 form acts as a melatonin-releasing factor in the pineal of a teleost fish, the european sea bass Dicentrarchus labrax (2010) Endocrinology, 151, pp. 2265-2275
  • Servili, A., Herrera-Pérez, P., Yáñez, J., Muñoz-Cueto, J.A., Afferent and efferent connections of the pineal organ in the European sea bass Dicentrarchus labrax: a carbocyanine dye tract-tracing study (2011) Brain Behav. Evol., 78, pp. 272-285
  • Sherwood, N., Eiden, L., Brownstein, M., Spiess, J., Rivier, J., Vale, W., Characterization of ateleost gonadotropin-releasing hormone (1983) Proc. Natl. Acad. Sci. U.S.A., 80, pp. 2794-2798
  • Somoza, G.M., Miranda, L.A., Strobl-Mazzulla, P.H., Guilgur, L.G., Gonadotropin-releasing hormone (GnRH): from fish to mammalian brains (2002) Cell. Mol. Neurobiology, 22, pp. 589-609
  • Spicer, O.S., Zmora, N., Wong, T.T., Golan, M., Levavi-Sivan, B., Gothilf, Y., Zohar, Y., The gonadotropin-inhibitory hormone (Lpxrfa) system's regulation of reproduction in the brain–pituitary axis of the zebrafish (Danio rerio) (2017) Biol. Reprod., 96, pp. 1031-1042
  • 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
  • Tostivint, H., Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations (2011) Gen. Comp. Endocrinol., 170, pp. 575-581
  • 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
  • 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., Ubuka, T., GnIH control of feeding and reproductive behaviors (2016) Front. Endocrinol. (Lausanne), 7, p. 170
  • Tsutsui, K., Osugi, T., Son, Y.L., Ubuka, T., Review: structure, function and evolution of GnIH (2017) Gen. Comp. Endocrinol., , (in press)
  • Tubert, C., Lo, N.F., Villafañe, V., Pandolfi, M., Aggressive behavior and reproductive physiology in females of the social cichlid fish Cichlasoma dimerus (2012) Physiol. Behav., 106, pp. 193-200
  • Ubuka, T., Bentley, G.E., Ukena, K., Wingfield, J.C., Tsutsui, K., Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain (2005) Proc. Natl. Acad. Sci. U.S.A., 102, pp. 3052-3057
  • Ubuka, T., McGuire, N.L., Calisi, R.M., Perfito, N., Bentley, G.E., The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone (2008) Integr. Comp. Biol., 48, pp. 560-569
  • Ubuka, T., Morgan, K., Pawson, A.J., Osugi, T., Chowdhury, V.S., Minakata, H., Tsutsui, H., Bentley, G.E., Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis (2009) PLoS One, 4, p. e8400
  • Umatani, C., Misu, R., Oishi, S., Yamaguchi, K., Abe, H., Oka, Y., GnRH suppresses excitability of visual processing neurons in the optic tectum (2015) J. Neurophysiol., 114, pp. 2775-2784
  • Yamamoto, N., Oka, Y., Kawashima, S., Lesions of gonadotropin-releasing hormone-immunoreactive terminal nerve cells: effects on the reproductive behavior of male dwarf gouramis (1997) Neuroendocrinology, 65, pp. 403-412
  • Zohar, Y., Muñoz-Cueto, J.A., Elizur, A., Kah, O., Neuroendocrinology of reproduction in teleost fish (2010) Gen. Comp. Endocrinol., 165, pp. 438-455

Citas:

---------- APA ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Muñoz-Cueto, J.A., Delgadin, T.H., Tsutsui, K., Somoza, G.M. & Vissio, P.G. (2019) . Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus. General and Comparative Endocrinology, 273, 144-151.
http://dx.doi.org/10.1016/j.ygcen.2018.06.010
---------- CHICAGO ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Muñoz-Cueto, J.A., Delgadin, T.H., Tsutsui, K., Somoza, G.M., et al. "Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus" . General and Comparative Endocrinology 273 (2019) : 144-151.
http://dx.doi.org/10.1016/j.ygcen.2018.06.010
---------- MLA ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Muñoz-Cueto, J.A., Delgadin, T.H., Tsutsui, K., Somoza, G.M., et al. "Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus" . General and Comparative Endocrinology, vol. 273, 2019, pp. 144-151.
http://dx.doi.org/10.1016/j.ygcen.2018.06.010
---------- VANCOUVER ----------
Di Yorio, M.P., Pérez Sirkin, D.I., Muñoz-Cueto, J.A., Delgadin, T.H., Tsutsui, K., Somoza, G.M., et al. Morphological relationship between GnIH and GnRH neurons in the brain of the neotropical cichlid fish Cichlasoma dimerus. Gen. Comp. Endocrinol. 2019;273:144-151.
http://dx.doi.org/10.1016/j.ygcen.2018.06.010