Research Advances in the Source, Evolution and Function of Gonadotropin Releasing Hormone 3 (GnRH3) in Fish
SUN Jing1, 3, SUN Ai2, 3, WU Li-Xin1, HU Hong-Xia2, 3, *
1 College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China; 2 Beijing Fisheries Research Institute, Beijing 100068, China; 3 Beijing Key Laboratory of Fishery Biotechnology, Beijing 100068, China
Abstract：Gonadotropin releasing hormone 3 (GnRH3) is a member of the gonadotropin releasing hormone family. GnRH3 has been derived from an earlier genome duplication in an ancestral vertebrate, followed by its loss in the tetrapod lineage,so it has been a unique GnRH type in fish. GnRH3 of fish has a classical decapeptide structure, which plays a crucial regulatory role in maturation of gonads and sensory regulation of fish by binding to gonadotropin releasing hormone receptors. This paper discusses from the following four parts. 1. Structure of GnRH3: It is composed of 3 introns and 4 exons. Non-coding regions and introns are different from vertebrates, but the coding regions are highly conserved; 2. Source of GnRH3: It was generated in two rounds of genome replication events and ultimately reserved in fish; 3. Production and migration of GnRH3: GnRH3 neurons in the olfactory area and the ectoderm of the embryo eventually migrated to the preoptic area and the ventral brain; 4. Research progress of GnRH3. In this paper, the research progress of GnRH3 was reviewed, and the future development prospect was prospected, so as to provide a theoretical basis for the regulation of fish reproduction.
孙静, 孙爱, 吴立新, 胡红霞. 鱼类促性腺激素释放激素3 (GnRH3)来源、进化及功能研究进展[J]. 农业生物技术学报, 2019, 27(4): 735-742.
SUN Jing, SUN Ai, WU Li-Xin, HU Hong-Xia. Research Advances in the Source, Evolution and Function of Gonadotropin Releasing Hormone 3 (GnRH3) in Fish. 农业生物技术学报, 2019, 27(4): 735-742.
1 林浩然. 2004. 促性腺激素释放激素(GnRH)结构与功能及其受体的进化发展[J]. 中山大学学报: 自然科学版,43(6): 1-5. (Lin H R.2004. The structure and function of gonadotropin releasing hormone (GnRH) and the evolutionary development of its receptors[J]. Journal of Sun Yat-sen University: Natural Science Edition, 43(6): 1-5.) 2 Abraham E, Palevitch O, Ijiri S, et al.2008. Early development of forebrain gonadotrophin-releasing hormone (GnRH) neurones and the role of GnRH as an autocrine migration factor[J]. Journal of Neuroendocrinology, 20(3): 394-405. 3 Abraham E, Palevitch O, Gothilf Y, et al.2009. The zebrafish as a model system for forebrain GnRH neuronal development[J]. General & Comparative Endocrinology, 164(2-3): 151-160. 4 Abraham E, Palevitch O, Gothilf Y, et al.2010. Targeted gonadotropin-releasing hormone-3 neuron ablation in zebrafish: effects on neurogenesis, neuronal migration, and reproduction[J]. Endocrinology, 151(1): 332-340. 5 Adams B A, Tello J A, Erchegyi J, et al.2003. Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis[J]. Endocrinology, 144(5): 1907-1919. 6 Aguillon R, Blader P, Madelaine R, et al.2018. Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm[J]. eLife,7: e32041. 7 Ando H, Swanson P, Kitani T, et al.2004. Synergistic effects of salmon gonadotropin-releasing hormone and estradiol-17β on gonadotropin subunit gene expression and release in masu salmon pituitary cells in vitro[J]. General and Comparative Endocrinology, 137(1): 109-121. 8 Breton B, Jalabert B, Billard R, et al.1971. In vitro stimulation of the release of pituitary gonadotropic hormone by a hypothalamic factor in the carp Cyprinus carpio L[J]. Comptes Rendus Hebdomadaires des Seances de L'Academie des Sciences. Serie D: Sciences Naturelles, 273(25): 2591-2594. 9 Carolsfeld J, Powell J F F, Park M, et al.2000. Primary structure and function of three gonadotropin-releasing hormones, including a novel form, from an ancient teleost, herring[J]. Endocrinology, 141(2): 505-512. 10 Das K, Ogawa S, Kitahashi T, Parhar I S.2019. Expression of neuropeptide Y and gonadotropin-releasing hormone gene types in the brain of female Nile tilapia (Oreochromis niloticus) during mouthbrooding and food restriction[J]. Peptides, 112: 67-77. 11 Decatur W A, Hall J A, Smith J J, et al.2013. Insight from the lamprey genome: glimpsing early vertebrate development via neuroendocrine-associated genes and shared synteny of gonadotropin-releasing hormone (GnRH)[J] General and Comparative Endocrinology, 192: 237-245. 12 Fernald R D, White R B.1999. Gonadotropin-releasing hormone genes: Phylogeny, structure, and functions[J]. Frontiers in Neuroendocrinology, 20(3): 224-240. 13 Gaillard A L, Tay B H, Pérez Sirkin D I, et al.2018. Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives[J]. Frontiers in Neuroscience, 12: 607. 14 González-Martínez D, Zmora N, Mañanos E, et al.2002. 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]. Journal of Comparative Neurology, 446(2): 95-113. 15 Hu W, Li S, Tang B, et al.2007. Antisense for gonadotropin-releasing hormone reduces gonadotropin synthesis and gonadal development in transgenic common carp (Cyprinus carpio)[J]. Aquaculture, 271(1-4): 498-506. 16 Jimenez-Liñan M, Rubin B S, King J C.1997. Examination of guinea pig luteinizing hormone-releasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain[J]. Endocrinology, 138(10): 4123-4130. 17 Kavanaugh S I, Nozaki M, Sower S A .2008. Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: Identification of a novel GnRH in a basal vertebrate, the sea lamprey[J]. Endocrinology, 149(8): 3860-3869. 18 Kawai T, Abe H, Oka Y .2013. Burst generation mediated by cholinergic input in terminal nerve-gonadotrophin releasing hormone neurones of the goldfish[J]. The Journal of Physiology, 591(22): 5509-5523. 19 Kawai T, Abe H, Akazome Y, et al.2010. Neuromodulatory effect of GnRH on the synaptic transmission of the olfactory bulbar neural circuit in goldfish, Carassius auratus[J]. Journal of Neurophysiology, 104(6): 3540-3550. 20 Kim D K, Cho E B, Moon M J, et al.2011. Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: Secrets hidden in genomes[J]. General & Comparative Endocrinology, 170(1): 68-78. 21 King J A, Millar R P.1982. Structure of chicken hypothalamic luteinizing hormone-releasing hormone. II. Isolation and characterization[J]. Journal of Biological Chemistry, 257(18): 10729-10732. 22 Kinoshita M, Kobayashi S, Urano A, et al.2010. Neuromodulatory effects of gonadotropin-releasing hormone on retinotectal synaptic transmission in the optic tectum of rainbow trout[J]. European Journal of Neuroscience, 25(2): 480-484. 23 Koide T, Yabuki Y, Yoshihara Y.2018. Terminal nerve GnRH3 neurons mediate slow avoidance of carbon dioxide in larval zebrafish[J]. Cell Reports, 22(5): 1115-1123. 24 Lepretre E, Anglade I, Williot P, et al.1993. Comparative distribution of mammalian GnRH (gonadotrophin-releasing hormone) and chicken GnRH-II in the brain of the immature Siberian sturgeon (Acipenser baeri)[J].Journal of Comparative Neurology,337(4) : 568-583. 25 Li L, Wojtowicz J L, Malin J H, et al.2017. GnRH-mediated olfactory and visual inputs promote mating-like behaviors in male zebrafish[J]. PLoS One, 12(3): e0174143. 26 Lien S, Koop B F, Sandve S R, et al.2016. The Atlantic salmon genome provides insights into rediploidization[J]. Nature, 22(5): 200-205. 27 Liu Y, Tang H, Xie R, et al.2017. Genetic evidence for multifactorial control of the reproductive axis in zebrafish[J]. Endocrinology, 158(3): 604-611. 28 Lovejoy D A, Fischer W H, Ngamvongchon S, et al.1992. Distinct sequence of gonadotropin-releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution.[J]. Proceedings of the National Academy of Sciences of the USA, 1992, 89(14): 6373-6377. 29 Maruska K P, Tricas T C, 2011. Gonadotropin-releasing hormone (GnRH) modulates auditory processing in the fish brain[J]. Hormones and Behavior, 59(4): 451-464. 30 Miyamoto K, Hasegawa Y, Nomura M, et al.1984. 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.[J]. Proceedings of the National Academy of Sciences of the USA, 81(12): 3874-3878. 31 Montaner A D, Park M K, Fischer W H, et al.2001. Primary structure of a novel gonadotropin-releasing hormone in the brain of a teleost, pejerrey[J]. Endocrinology, 142(4): 1453-1460. 32 Narita Y, Tsutiya A, Nakano Y, et al.2018. Androgen induced cellular proliferation, neurogenesis, and generation of GnRH3 neurons in the brain of mature female Mozambique tilapia[J]. Science Reports, 8(1): 16855. 33 Ngamvongchon S, Lovejoy D A, Fischer W H, et al.1992. Primary structures of two forms of gonadotropin-releasing hormone, one distinct and one conserved, from catfish brain[J]. Molecular and Cellular Neuroscience, 3(1): 17-22. 34 Nock T G, Chand D, Lovejoy D A.2011. Identification of members of the gonadotropin-releasing hormone (GnRH), corticotropin-releasing factor (CRF) families in the genome of the holocephalan, Callorhinchus milii (elephant shark)[J]. General & Comparative Endocrinology, 171(2): 237-244. 35 O'Neill D F, Powell J F, Standen E M, et al.1998. Gonadotropin-releasing hormone (GnRH) in ancient teleosts, the bonytongue fishes: putative origin of salmon GnRH[J]. General & Comparative Endocrinology, 112(3): 415-425. 36 Ogawa S, Akiyama G, Kato S, et al.2006. Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids[J]. Neuroscience Letters, 403(3): 201-205. 37 Okubo K, Nagahama Y, 2008. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates[J]. Acta Physiologica, 193(1): 3-15. 38 Okubo K, Sakai F, Lau E L, et al.2006. Forebrain gonadotropin-releasing hormone neuronal development: Insights from transgenic medaka and the relevance to X-linked Kallmann syndrome[J]. Endocrinology, 147(3): 1076-1084. 39 Okuyama T, Yokoi S, Abe H, et al.2014. A neural mechanism underlying mating preferences for familiar individuals in medaka fish[J]. Science, 343(6166): 91-94. 40 Parhar I S, Soga T, Ishikawa Y, et al.1998. Neurons synthesizing gonadotropin‐releasing hormone mRNA subtypes have multiple developmental origins in the medaka[J]. Journal of Comparative Neurology, 401(2): 217-226. 41 Powell J F, Zohar Y, Elizur A, et al.1994. Three forms of gonadotropin-releasing hormone characterized from brains of one species[J]. Proceedings of the National Academy of Sciences of the USA, 91(25): 12081-12085. 42 Read T D, Petit R A, Joseph S J, et al.2017. Draft sequencing and assembly of the genome of the world's largest fish, the whale shark: Rhincodon typus Smith 1828[J]. BMC Genomics, 18(1): 532. 43 Roch G J, Busby E R, Sherwood N M.2014. GnRH receptors and peptides: Skating backward[J]. General and Comparative Endocrinology, 209: 118-134. 44 Roch G J, Busby E R, Sherwood N M.2011. Evolution of GnRH: Diving deeper[J]. General and Comparative Endocrinology, 171(1): 1-16. 45 Sherwood N, Eiden L, Brownstein M, et al.1983. Characterization of a teleost gonadotropin-releasing hormone[J]. Proceedings of the National Academy of Sciences of the USA, 80(9): 2794-2798. 46 Sower S A, Chiang Y C, Lovas S, et al.1993. Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain[J]. Endocrinology, 1993, 132(3): 1125-1131. 47 Spicer O S, Wong T T, Zmora N, et al.2016. Targeted mutagenesis of the hypophysiotropic Gnrh3 in zebrafish (Danio rerio) reveals no effects on reproductive performance[J]. PLoS One, 11(6): e0158141. 48 Sukhan Z P, Kitano H, Selvaraj S, et al.2013. Identification and distribution of three gonadotropin-releasing hormone (GnRH) isoforms in the brain of a clupeiform fish, Engraulis japonicas[J]. Zoological science, 30(12): 1081-1091. 49 Takahashi A, Islam M S, Abe H, et al.2016. Morphological analysis of the early development of telencephalic and diencephalic gonadotropin‐releasing hormone neuronal systems in enhanced green fluorescent protein‐expressing transgenic medaka lines[J]. Journal of Comparative Neurology, 524(4): 896-913. 50 Tostivint H, 2011. Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations[J]. General & Comparative Endocrinology, 170(3): 575-581. 51 Tsai P S, 2017. Gonadotropin-releasing hormone by any other name would smell as sweet[J]. General and Comparative Endocrinology, 264(1): 58-63. 52 Tuziak S M, Volkoff, Hélène.2013. Gonadotrophin-releasing hormone in winter flounder (Pseudopleuronectes americanus): Molecular characterization, distribution and effects of fasting[J]. General and Comparative Endocrinology, 184: 9-21. 53 Umatani C, Misu R, Oishi S, et al.2015. GnRH suppresses excitability of visual-processing neurons in the optic tectum[J]. Journal of Neurophysiology, 114(5): 2775-2784. 54 Umatani C, Oka Y.2018. Juvenile-specific burst firing of terminal nerve GnRH3 neurons suggests novel functions in addition to neuromodulation[J]. Endocrinology, 159(4): 1678-1689. 55 Whitlock K E, Wolf C D, Boyce M L, 2003. Gonadotropin-releasing hormone (gnrh) cells arise from cranial neural crest and adenohypophyseal regions of the neural plate in the zebrafish, Danio rerio[J]. Developmental Biology, 257(1): 140-152. 56 Xu J, Huang W, Zhong C R, et al.2011. Defining global gene expression changes of the hypothalamic-pituitary-gonadal axis in female sGnRH-antisense transgenic common carp (Cyprinus carpio)[J]. PLoS One, 6: e21057. 57 Yoo M S, Kang H M, Choi H S, et al.2000. Molecular cloning, distribution and pharmacological characterization of a novel gonadotropin-releasing hormone ([Trp8] GnRH) in frog brain[J]. Molecular & Cellular Endocrinology, 164(1): 197-204. 58 Zhao Y, Lin M C A, Farajzadeh M, et al.2013. Early development of the gonadotropin-releasing hormone neuronal network in transgenic zebrafish[J]. Frontiers in Endocrinology, 4: 107. 59 Zhou X, Yi Q, Zhong Q, et al.2012. Molecular cloning, tissue distribution, and ontogeny of gonadotropin-releasing hormone III gene (GnRH-III) in half-smooth tongue sole (Cynoglossus semilaevis)[J]. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 163(1): 59-64.
