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The Discovery of GnRH-GtH Paracrine System in Common Carp (Cyprinus carpio) Gonad and Its Roles in Growth and Reproduction Regulation |
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Abstract Abstract Growth and reproduction are closely related in fish. Herely, the hormone cross-talk between the two systems in the gonad has been analyzed with Common carp (Cyprinus carpio) and growth hormone (gh) transgenic common carp by using real qRT-PCR, immunofluorescence, in situ hybridization, and in vitro incubation. The expression of gonadotropin hormone alpha (gthα), follicle-stimulating hormone beta (fshβ), luteinizing-stimulating hormone beta (lhβ), gonadotropin-releasing hormone 3 (gnrh3), growth hormone receptor (ghr) and 4 GnRH receptor mRNA were detected in testis and ovary of common carp. Immunofluorescence showed that GTHα and LHβ were localized mainly in the somatic cells and primary sperm cells of the gonads. In vitro incubation of ovary fractions with GnRH confirmed the existence of gonadal GnRH-GtH paracrine system, which was independent of the hypothalamus-pituitary-gonad axis. The expression levels of gnrh3, gthα, fshβ and lhβ mRNA were significantly different in the gonad of GH-transgenic carp when compared with non-transgenic carp. Further analysis in vitro showed that GH up-regulated the expression of gnrh3, gthα, fshβ and lhβ in the ovarian GnRH-GtH system at primary growth stages. But the signals were inhibited in the ovarian at the secondary growth stages. Our results confirmed the GnRH-GtH paracrine system in gonad and uncovered its important role in the interaction between growth and reproduction in common carp, which provides scientific data to reveal the regulation mechanism between growth and reproduction in fish.
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Received: 20 March 2017
Published: 06 August 2017
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Bessey C. 2003. Reproductive performance of growth-enhanced transgenic coho salmon (Oncorhynchus kisutch)[J]. Transactions of the American Fisheries Society, 133(5):1205-1220.Cailleau J, Vermeire S, Verhoeven G. 1990. Independent control of the production of insulin-like growth factor I and its binding protein by cultured testicular cells[J]. Molecular & Cellular Endocrinology, 69(1):79-89.Cao M, Chen J, Peng W, et al. 2014. Effects of growth hormone over-expression on reproduction in the common carp Cyprinus carpio L[J]. General & Comparative Endocrinology, 195(1):47-57.Chi M L, Meng N, Li J F, et al. 2015. Molecular cloning and characterization of gonadotropin subunits (GTHα, FSHβ and LHβ) and their regulation by hCG and GnRHa in Japanese sea bass (Lateolabrax japonicas) in vivo[J]. Fish Physiology and Biochemistry, 41(3):1-15.Devlin R H, Biagi C A, Yesaki T Y. 2004. Growth, viability and genetic characteristics of GH transgenic coho salmon strains[J]. Aquaculture, 236(1):607-632.Franks S. 1998. Growth hormone and ovarian function[J]. Baillière’s Clinical Endocrinology & Metabolism, 12(2):331-340.Gac F L, Blaise O, Fostier A, et al. 1993. Growth hormone (GH) and reproduction: a review[J]. Fish Physiology and Biochemistry, 11(1):219.Grober M S, Myers T R, Marchaterre M A, et al. 1995. Structure, localization, and molecular phylogeny of a GnRH cDNA from a paracanthopterygian fish, the plainfin midshipman (Porichthys notatus)[J]. General & Comparative Endocrinology, 99(1):85-99.Hill J W, Elmquist J K, Elias C F. 2008. Hypothalamic pathways linking energy balance and reproduction[J]. American Journal of Physiology, 294(1):827-832.Huang H, Zhang Y, Huang W R, et al. 2009. Molecular characterization of marbled eel (Anguilla marmorata) gonadotropin subunits and their mRNA expression profiles during artificially induced gonadal development[J]. General & Comparative Endocrinology, 162(2):192-202.Hull K L, Harvey S. 2000. Growth hormone: a reproductive endocrine-paracrine regulator?[J]. Reviews of Reproduction, 5(3):175-182.Hull K L, Harvey S. 2014. Growth Hormone and Reproduction: A Review of Endocrine and Autocrine/Paracrine Interactions[J]. International Journal of Endocrinology, 2014(4):234014.Jing Xu, Wei Huang, Chengrong Zhong, 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(6):e21057.Klausen C, Chang J P, Habibi H R. 2002. Time- and dose-related effects of gonadotropin-releasing hormone on growth hormone and gonadotropin subunit gene expression in the goldfish pituitary[J]. Canadian Journal of Physiology & Pharmacology, 80(9):915-924.Kuo M W, Lou S W, Postlethwait J, et al. 2005. Chromosomal organization, evolutionary relationship, and expression of zebrafish GnRH family members[J]. Journal of Biomedical Science online, 12(4):629-639.Lin X W, Lin H R, Peter R E. 1993. Growth hormone and gonadotropin secretion in the common carp (Cyprinus carpio L.): in vitro interactions of gonadotropin-releasing hormone, somatostatin, and the dopamine agonist apomorphine[J]. General & Comparative Endocrinology, 89(1):62.Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method[J]. Methods, 25(4):402-408.Moreau D T R, Corinne C, Fleming I A. 2011. Reproductive performance of alternative male phenotypes of growth hormone transgenic Atlantic salmon (Salmo salar)[J]. Evolutionary Applications, 4(6):736–748.Pati D, Habibi H R. 1998. Presence of salmon gonadotropin-releasing hormone (GnRH) and compounds with GnRH-like activity in the ovary of goldfish[J]. Endocrinology, 139(4):2015-2024.Schneider J E. 2004. Energy balance and reproduction[J]. Physiology & Behavior, 81(2):289-317.Servili A, Le P Y, Leprince J, et al. 2011. Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish[J]. Endocrinology, 152(4):1527-40.So W K, Kwok H F, Ge W. 2005. Zebrafish gonadotropins and their receptors: II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits--their spatial-temporal expression patterns and receptor specificity[J]. Biology of Reproduction, 72(6):1382.Sun C, He M, Ko W K, et al. 2014. Mechanisms for luteinizing hormone induction of growth hormone gene transcription in fish model: crosstalk of the cAMP/PKA pathway with MAPK-and PI3K-dependent cascades[J]. Molecular & Cellular Endocrinology, 382(2):835.Tello J A, Wu S, Rivier J E, et al. 2008. Four functional GnRH receptors in zebrafish: analysis of structure, signaling, synteny and phylogeny[J]. Integrative & Comparative Biology, 48(5):570-587.Thisse C, Thisse B. 2008. High-resolution in situ hybridization to whole-mount zebrafish embryos[J]. Nature Protocol, 3(1):59-69.Trudeau V L. 1997. Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus[J]. Reviews of Reproduction, 2(1):55-68.von Schalburg K R, Warby C M, Sherwood N M. 1999. Evidence for gonadotropin-releasing hormone peptides in the ovary and testis of rainbow trout[J]. 60(6):1338-1344.Wong A O L, Zhou H, Jiang Y, et al. 2006. Feedback regulation of growth hormone synthesis and secretion in fish and the emerging concept of intrapituitary feedback loop[J]. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology, 144(3):284-305.Wong T T, Zohar Y. 2004. Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata)[J]. Endocrinology, 145(11):5210.Wu G, Chen L H, Zhong S, et al. 2008. Enzyme-linked immunosorbent assay of changes in serum levels of growth hormone (cGH) in common carps (Cyprinus carpio)[J]. Science China Life Sciences, 51(2):157-163.Xu Z, Qi L, Yun W, et al. 2009. Production, characterization, and applications of mouse monoclonal antibodies against gonadotropin, somatolactin, and prolactin from common carp (Cyprinus carpio)[J]. General & Comparative Endocrinology, 167(3):373-378.Zachmann M. 1992. Interrelations between growth hormone and sex hormones: physiology and therapeutic consequences[J]. Hormone Research, 38 Suppl 1(Suppl. 1):1-8.Zhong C, Song Y, Wang Y, et al. 2012. Growth hormone transgene effects on growth performance are inconsistent among offspring derived from different homozygous transgenic common carp ( Cyprinus carpio L.)[J]. Aquaculture, s 356–357(4):404–411.Zhou H, Ko W K, Ho W K, et al. 2004. Novel aspects of growth hormone (GH) autoregulation: GH-induced GH gene expression in grass carp pituitary cells through autocrine/paracrine mechanisms[J]. Endocrinology, 145(10):4615-4628.Zhou H, Wang X, Ko W K, et al. 2005. Evidence for a novel intrapituitary autocrine/paracrine feedback loop regulating growth hormone synthesis and secretion in grass carp pituitary cells by functional interactions between gonadotrophs and somatotrophs[J]. Endocrinology, 145(12):5548-5559. |
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