Abstract
To clarify the possible roles of gonadotropin-releasing hormone (GnRH) in the reproduction of Japanese flounder Paralichthys olivaceus, localization of salmon GnRH (sGnRH), chicken GnRH-II (cGnRH-II), and sea bream GnRH (sbGnRH) immunoreactive (ir) cell bodies and fibers in the brain and pituitary were examined together with follicle stimulating hormone (FSH) and luteinizing hormone (LH)-ir cells in the pituitary by immunohistochemistry. sGnRH-ir cell bodies were localized in the ventromedial part of the rostral olfactory bulb and cGnRH-II-ir cell bodies were restricted to the midbrain tegmentum, while sbGnRH-ir cell bodies were evident in the preoptic area. sGnRH-ir fibers were distributed throughout the brain, especially abundant in the forebrain. cGnRH-II-ir fibers were also scattered in many areas of the brain with abundance in the midbrain, but sbGnRH-ir fibers were observed in the preoptic-hypothalamic area and innervated the pituitary. In the pituitary, neither sGnRH-ir fibers nor cGnRH-II-ir fibers were found, but sbGnRH-ir fibers were profuse in the neurohypophysis and invaded the proximal pars distalis, targeting FSH and LH cells. These results suggest that three GnRH systems can play different physiological roles in the brain of Japanese flounder. Among them, sbGnRH is considered to be involved in reproduction by stimulating gonadotropin secretion, while sGnRH and cGnRH-II can function as a neurotransmitter and/or neuromodulator within the brain in this species.
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References
Amano M, Urano A, Aida K. Distribution and function of gonadotropin-releasing hormone (GnRH) in the teleost brain. Zool. Sci. 1997; 14: 1–11.
Okuzawa K, Kobayashi M. Gonadotropin-releasing hormone neuronal systems in the teleostean brain and functional significance. In: Prasada Rao PD, Peter RE (eds). Neural Regulation in the Vertebrate Endocrine System. Kluwer Academic/Plenum Publishers, New York, NY. 1999; 85–100.
Lethimonier C, Madigou T, Muñoz-Cueto JA, Lareyre JJ, Kah O. Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen. Comp. Endocrinol. 2004; 135: 1–16.
Amano M, Oka Y, Aida K, Okumoto N, Kawashima S, Hasegawa Y. Immunocytochemical demonstration of salmon GnRH and chicken GnRH-II in the brain of masu salmon, Oncorhynchus masou. J. Comp. Neurol. 1991; 314: 587–597.
Kim MH, Oka Y, Amano M, Kobayashi M, Okuzawa K, Hasegawa Y, Kawashima S, Suzuki Y, Aida K. Immunocytochemical localization of sGnRH and cGnRH-II in the brain of goldfish, Carassius auratus. J. Comp. Neurol. 1995; 356: 72–82.
Stefano AV, Aldana-Marcos HJ, Affani JM, Somoza GM. Gonadotropin-releasing hormone (GnRH) neuronal systems in the pejerrey, Odontesthes bonariensis (Atheriniformes). Fish. Physiol. Biochem. 2000; 23: 215–223.
Amano M, Oka Y, Yamanome T, Okuzawa K, Yamamori K. Three GnRH systems in the brain and pituitary of a pléuronectiform fish, the barfin flounder, Verasper moseri. Cell Tissue Res. 2002; 309: 323–329.
Vickers ED, Laberge F, Adams BA, Hara TJ, Sherwood NM. Cloning and localization of three forms of gonadotropin-releasing hormone, including the novel whitefish form, in a salmonid, Coregonus clupeaformis. Biol. Reprod. 2004; 70: 1136–1146.
González-Martínez D, Zmora N, Mananos E, Saligaut D, Zanuy S, Zohar Y, Elizur A, Kah O, Muñoz-Cueto JA. 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. J. Comp. Neurol. 2002; 446: 95–113.
Mohamed JS, Thomas P, Khan IA. Isolation, cloning, and expression of three prepro-GnRH mRNAs. in Atlantic croaker brain and pituitary. J. Comp. Neurol. 2005; 488: 384–395.
Pandolfi M, Muñoz-Cueto JA, Lo Nostro FL, Downs JL, Paz DA, Maggese MC, Urbanski HF. GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides. Cell Tissue Res. 2005; 321: 219–232.
White SA, Kasten TL, Bond CT, Adelman JP, Fernald RD. Three gonadotropin-releasing hormone genes in one organism suggest novel roles for an ancient peptide. Proc. Natl. Acad. Sci. U.S.A. 1995; 92: 8363–8367.
Yamamoto N, Oka Y, Amano M, Aida K, Hasegawa Y, Kawashima S. Multiple gonadotropin-releasing hormone (GnRH) immunoreactivity system in the brain of the dwarf gourami, Colisa lalia: immunohistochemistry and radioimmunoassay. J. Comp. Neurol. 1995; 355: 354–368.
Dubois EA, Zandbergen NA, Peute J, Bogerd J, Goos HJTh. Development of three distinct GnRH neuron populations expressing two different GnRH forms in the brain of the African catfish (Clarias gariepinus). J. Comp. Neurol. 2001; 437: 308–320.
Yamamoto N. Three gonadotropin-releasing hormone neuronal groups with special reference to teleosts. Anat. Sci. Int. 2003; 78: 139–155.
Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H. Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci. Res. 1998; 31: 31–38.
Honda H, Watanabe Y, Kikuchi K, Iwata N, Takeda S, Uemoto H, Furuta T, Kiyono M. High density rearing of Japanese flounder, Paralichthys olivaceus with a closed seawater recirculation system equipped with a denitrification unit. Suisanzoshoku 1993; 41: 19–26.
Mizuta A, Tabata K, Kanao H. Acceleration of testicular maturation of sex reversed gynogenetic females (Phenotypically males) hirame, Paralichthys olivaceus due to long photoperiod and low water treatments. Suisanzoshoku 1996; 44: 91–98.
Okuzawa K, Amano M, Aida K, Hasegawa Y, Tanaka H, Kagawa H. Chromatographic and immunological identification of gonadotropin-releasing hormone in five marine teleosts. Fish. Physiol. Biochem. 1993; 12: 337–345.
Kajimura S, Yoshiura Y, Suzuki M, Aida K. DNA cloning of two gonadotropin β subunits (GTH-Iβ and GTH-IIβ) and their expression profiles during gametogenesis in the Japanese flounder, Paralichthys olivaceus. Gen. Comp. Endocrinol. 2001; 122: 117–129.
Pham KX, Amano M, Amiya N, Kurita Y, Yamamori K. Distribution of three GnRHs in the brain and pituitary of the wild Japanese flounder Paralichthys olivaceus. Fish. Sci. 2006; 72: 89–94.
Shimizu A, Kagawa H, Tanaka H. Immunocytochemical identification of gonadotrophs (FSH cells and LH cells) in various perciform fishes using antisera raised against synthetic peptides. Fish. Physiol. Biochem. 2003; 28: 109–110.
Shimizu A, Yamashita M. Purification of mummichog (Fundulus heteroclitus) gonad otropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides. Gen. Comp. Endocrinol. 2002; 125: 79–91.
Soga T, Ogawa S, Millar RP, Sakuma Y, Parhar IS. Localization of the three GnRH types and GnRH receptors in the brain of a cichild fish: insights into their neuroendocrine and neuromodulator functions. J. Comp. Neurol. 2005; 487: 28–41.
Gothilf Y, Muñoz-Cueto JA, Sagrillo CA, Selmanoff M, Chen TT, Elizur A, Kah O, Zohar Y. Three forms of gonadotropin-releasing hormone in a perciform fish (Sparus aurata): complementary deoxyribonucleic acid characterization and brain localization. Biol. Reprod. 1996; 55: 636–645.
Oka Y, Matsushima T. Gohadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J. Neurosci. 1993; 13: 2161–2176.
Kobayashi M, Amano M, Kim MH, Furukawa K, Hasegawa Y, Aida K. Gonadotropin-releasing hormones of terminal nerve origin are not essential to ovarian development and ovulation in goldfish. Gen. Comp. Endocrinol. 1994; 95: 192–200.
Yamamoto N, Oka Y, Kawashima S. Lesions of gonadotropin-releasing hormone-im munoreactive terminal nerve cells: effects on the reproductive behavior of male dwarg gouramis. Neuroendocrinology 1997; 65: 403–412.
Nozaki M, Naito N, Swanson P, Miyata K, Nakai Y, Oota Y, Suzuki K, Kawauchi H. Salmonid pituitary gonadotrophs: 1. Distinct cellular distributions of two gonadotropins. GTH-I and GTH-II. Gen. Comp. Endocrinol. 1990; 77: 348–357.
Nozaki M, Naito N, Swanson P, Dickhoff WW, Nakai Y, Suzuki K, Kawauchi H. Salmonid pituitary gonadotrophs: 2 Ontogeny of GTH-I and GTH-II cells in the rainbow trout (Salmo gairdneri irideus). Gen. Comp. Endocrinol. 1990; 77: 358–367.
Rendon C, Rodrigues-Gomez FJ, Muñoz-Cueto JA, Pinuela C, Saraquete C. An immunocytochemical study of pituitary cells of the Senegalese sole, Solea senegalensis (Kaup 1858). J. Histochem. 1997; 29: 813–822.
Kagawa H, Kawazoe I, Tanaka H, Okuzawa K. Immunocytochemical identification of two distinct gonadotropic cells (GTH-I and GTH-II) in the pituitary of bluefin tuna, Thunnus thynnus. Gen. Comp. Endocrinol. 1998; 110: 11–18.
Miranda LA, Strussmann CA, Somoza GM. Immunocytochemical identification of GTH-I and GTH-II cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen. Comp. Endocrinol. 2001; 124: 45–52.
Shimizu A, Sakai T, Nashida K, Honda H. Universal antisera for immunocytochemical identification of two different gonadotrophs in acanthopterygian fishes. Fish. Physiol. Biochem. 2003; 29: 275–287.
Shimizu A, Tanaka H, Kagawa H. Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GTH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. Gen. Comp. Endocrinol. 2003; 132: 35–45.
Pham KX, Amano M, Amiya N, Kurita Y, Yamamori K. Changes in brain and pituitary GnRH levels during ovarian maturation in wild female Japanese flounder. Fish. Physiol. Biochem. 2006; 32: 241–248.
Temple JL, Millar RP, Rissman EF. An evolutionarily conserved form of gonadotropin-releasing hormone coordinates energy and reproductive behavior. Endocrinology 2003; 144: 13–19.
Kauffman AS, Wills A, Millar RP, Rissman EF. Evidence that the type-2 gonadotrophin-releasing hormone (GnRH) receptor mediates the behavioural effects of GnRH-II on feeding and reproduction in musk shrews. J. Neuroendocrinol. 2005; 17: 489–497.
Barnett DK, Bunnell TM, Millar RP, Abbott DH. Gonadotropin-releasing hormone II stimulates female sexual behavior in armoset monkeys. Endocrinology 2005; 1: 615–623.
Zohar Y, Elizur A, Sherwood NM, Powell JFF, Rivier JE, Zmora N. Gonadotropin-releasing activities of the three native forms of gonadotropin-releasing hormone present in the brain of gilthead seabream, Sparus aurata. Gen. Comp. Endocrinol. 1995; 97: 289–299.
Goos HJTh, Bosma PT, Bogerd J, Tensen CP, Li KW, Zandbergen MA, Schulz RW. Gonadotropin-releasing hormones in the African catfish: molecular forms, localization, potency and receptors. Fish. Physiol. Biochem. 1997; 17: 45–51.
Forniés MA, Carrillo M, Mañanós E, Sorbera LA, Zohar Y, Zanuy S. Relative potency of the forms of GnRH and their analogs on LH release in sea bass. J. Fish. Biol. 2003; 63: 73–89.
González-Martínez D, Madigou T, Zmora N, Anglade I, Zanuy S, Zohar Y, Elizur A, Muñoz-Cueto JA, Kah O. Differential expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the European sea bass, Dicentrarchus labrax. J. Comp. Neurol. 2001; 429: 144–155.
Montero M, Vidal B, King JA, Tramu G, Vandesande F, Dufour S, Kah O. Immunocytochemical localization of mammalian GnRH (gonadotropin-releasing hormone) and chicken GnRH-II in the brain of the European silver eel (Anguilla anguilla L.). J. Chem. Neuroanat. 1994; 7: 227–241.
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Pham, K.X., Amano, M., Amiya, N. et al. Immunohistochemical localization of three GnRH systems in brain and pituitary of Japanese flounder. Fish Sci 73, 1113–1122 (2007). https://doi.org/10.1111/j.1444-2906.2007.01443.x
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DOI: https://doi.org/10.1111/j.1444-2906.2007.01443.x