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Developmental expression of LPXRFa, kisspeptin, and their receptor mRNAs in the half-smooth tongue sole Cynoglossus semilaevis

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Abstract

Both gonadotropin-inhibitory hormone (GnIH) and kisspeptin play a critical role in the control of reproduction in vertebrates. However, the spatial–temporal expression patterns and possible roles of these two peptides during development are poorly understood. To this end, we evaluated dynamic expression profiles of lpxrfa, the piscine ortholog of gnih, kisspeptin (kiss2) and their receptor mRNAs during embryogenesis and early larval development in a flatfish, Cynoglossus semilaevis. Quantitative RT-PCR analysis indicated that both ligand (lpxrfa and kiss2) and receptor (lpxrfa-r and kiss2r) mRNAs were detected in unfertilized eggs and during embryogenesis, but with different expression profiles. In addition, lpxrfa-r, kiss2 and kiss2r transcripts increased significantly at 6 days post-hatching (dph), while lpxrfa mRNAs did not vary significantly during all larval development. Taken together, these results of the present study suggest that both LPXRFa and kisspeptin systems could be functional and play differential roles during embryogenesis and early larval development in tongue sole.

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References

  • Biswas S, Jadhao AG, Pinelli C, Palande NV, Tsutsui K (2015) GnIH and GnRH expressions in the central nervous system and pituitary of Indian major carp, Labeo rohita during ontogeny: an immunocytochemical study. Gen Comp Endocrinol 220:88–92

    Article  CAS  PubMed  Google Scholar 

  • Di Yorio MP, Perez Sirkin DI, Delgadin TH, Shimizu A, Tsutsui K, Somoza GM, Vissio PG (2016) Gonadotropin-inhibitory hormone in the cichlid fish Cichlasoma dimerus: structure, brain distribution and differential effects on the secretion of gonadotropins and growth hormone. J Neuroendocrinol. https://doi.org/10.1111/jne.12377

    Article  PubMed  Google Scholar 

  • Di Yorio MP, Sallemi JE, Toledo Solis FJ, Perez Sirkin DI, Delgadin TH, Tsutsui K, Vissio PG (2018) Ontogeny of gonadotropin-inhibitory hormone (GnIH) in the cichlid fish Cichlasoma dimerus. J Neuroendocrinol 30:e12608

    Article  CAS  Google Scholar 

  • Hodne K, Weltzien FA, Oka Y, Okubo K (2013) Expression and putative function of kisspeptins and their receptors during early development in medaka. Endocrinology 154:3437–3446

    Article  CAS  PubMed  Google Scholar 

  • Kitahashi T, Ogawa S, Parhar IS (2009) Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150:821–831

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhuang Z, Ma A, Chen S, Sun Z, Liang Y, Xu Y (2005) Reproductive biology and breeding technology of Cynoglossus semilaevis. Mar Fish Res 26:7–14

    CAS  Google Scholar 

  • Liu C, Xin N, Zhai Y, Jiang L, Zhai J, Zhang Q, Qi J (2014) Reference gene selection for quantitative real-time RT-PCR normalization in the half-smooth tongue sole (Cynoglossus semilaevis) at different developmental stages, in various tissue types and on exposure to chemicals. PLoS One 9:e91715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Wang B, Liu X, Xu Y, Shi B, Liu Z (2017) Effects of gonadotropin-inhibitory hormone peptides on the reproduction-related gene expression in the hypothalamus of half-smooth tongue sole (Cynoglossus semilaevis). Prog Fish Sci 38:56–62

    Google Scholar 

  • Ma X, Liu X, Wen H, Xu Y, Zhang L (2006) Histological observation on gonadal sex differentiation in Cynoglossus semilaevis. Mar Fish Res 27:55–61

    Google Scholar 

  • Mechaly AS, Vinas J, Piferrer F (2013) The kisspeptin system genes in teleost fish, their structure and regulation, with particular attention to the situation in Pleuronectiformes. Gen Comp Endocrinol 188:258–268

    Article  CAS  PubMed  Google Scholar 

  • Mechaly AS, Tovar Bohorquez MO, Mechaly AE, Suku E, Perez MR, Giorgetti A, Orti G, Vinas J, Somoza GM (2018) Evidence of alternative splicing as a regulatory mechanism for Kissr2 in pejerrey fish. Front Endocrinol (Lausanne) 9:604

    Article  Google Scholar 

  • Mohamed JS, Benninghoff AD, Holt GJ, Khan IA (2007) Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia. J Mol Endocrinol 38:235–244

    Article  CAS  PubMed  Google Scholar 

  • Munoz-Cueto JA, Paullada-Salmeron JA, Aliaga-Guerrero M, Cowan ME, Parhar IS, Ubuka T (2017) A journey through the gonadotropin-inhibitory hormone system of fish. Front Endocrinol (Lausanne) 8:285

    Article  Google Scholar 

  • Ogawa S, Parhar IS (2014) Structural and functional divergence of gonadotropin-inhibitory hormone from jawless fish to mammals. Front Endocrinol (Lausanne) 5:177

    Article  Google Scholar 

  • Ogawa S, Ng KW, Xue X, Ramadasan PN, Sivalingam M, Li S, Levavi-Sivan B, Lin H, Liu X, Parhar IS (2013) Thyroid hormone upregulates hypothalamic kiss2 gene in the male Nile tilapia, Oreochromis niloticus. Front Endocrinol (Lausanne) 4:184

    Article  Google Scholar 

  • Ohga H, Selvaraj S, Matsuyama M (2018) The roles of kisspeptin system in the reproductive physiology of fish with special reference to chub mackerel studies as main axis. Front Endocrinol (Lausanne) 9:147

    Article  Google Scholar 

  • Pasquier J, Kamech N, Lafont AG, Vaudry H, Rousseau K, Dufour S (2014) Molecular evolution of GPCRs: kisspeptin/kisspeptin receptors. J Mol Endocrinol 52:T101–T117

    Article  CAS  PubMed  Google Scholar 

  • Pasquier J, Lafont AG, Denis F, Lefranc B, Dubessy C, Moreno-Herrera A, Vaudry H, Leprince J, Dufour S, Rousseau K (2018) Eel kisspeptins: identification, functional activity, and inhibition on both pituitary LH and GnRH receptor expression. Front Endocrinol (Lausanne) 8:353

    Article  Google Scholar 

  • Paullada-Salmeron JA, Loentgen GH, Cowan M, Aliaga-Guerrero M, Rendon-Unceta MD, Munoz-Cueto JA (2017) Developmental changes and day-night expression of the gonadotropin-inhibitory hormone system in the European sea bass: effects of rearing temperature. Comp Biochem Physiol A Mol Integr Physiol 206:54–62

    Article  CAS  PubMed  Google Scholar 

  • Power DM, Llewellyn L, Faustino M, Nowell MA, Bjornsson BT, Einarsdottir IE, Canario AV, Sweeney GE (2001) Thyroid hormones in growth and development of fish. Comp Biochem Physiol C Toxicol Pharmacol 130:447–459

    Article  CAS  PubMed  Google Scholar 

  • Sandvik GK, Hodne K, Haug TM, Okubo K, Weltzien FA (2014) RFamide peptides in early vertebrate development. Front Endocrinol (Lausanne) 5:203

    Article  Google Scholar 

  • Schreiber AM (2013) Flatfish: an asymmetric perspective on metamorphosis. Curr Top Dev Biol 103:167–194

    Article  CAS  PubMed  Google Scholar 

  • Selvaraj S, Kitano H, Ohga H, Yamaguchi A, Matsuyama M (2015) Expression changes of mRNAs encoding kisspeptins and their receptors and gonadotropin-releasing hormones during early development and gonadal sex differentiation periods in the brain of chub mackerel (Scomber japonicus). Gen Comp Endocrinol 222:20–32

    Article  CAS  PubMed  Google Scholar 

  • Shao C, Bao B, Xie Z, Chen X, Li B, Jia X, Yao Q, Orti G, Li W, Li X, Hamre K, Xu J, Wang L, Chen F, Tian Y, Schreiber AM, Wang N, Wei F, Zhang J, Dong Z, Gao L, Gai J, Sakamoto T, Mo S, Chen W, Shi Q, Li H, Xiu Y, Li Y, Xu W, Shi Z, Zhang G, Power DM, Wang Q, Schartl M, Chen S (2017) The genome and transcriptome of Japanese flounder provide insights into flatfish asymmetry. Nat Genet 49:119–124

    Article  CAS  PubMed  Google Scholar 

  • Tena-Sempere M, Felip A, Gomez A, Zanuy S, Carrillo M (2012) Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen Comp Endocrinol 175:234–243

    Article  CAS  PubMed  Google Scholar 

  • Tovar Bohorquez MO, Mechaly AS, Hughes LC, Campanella D, Orti G, Canosa LF, Somoza GM (2017) Kisspeptin system in pejerrey fish (Odontesthes bonariensis). Characterization and gene expression pattern during early developmental stages. Comp Biochem Physiol A Mol Integr Physiol 204:146–156

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661–667

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui K, Osugi T, Lee Son Y, Ubuka T (2018) Review: structure, function and evolution of GnIH. Gen Comp Endocrinol 264:48–57

    Article  CAS  PubMed  Google Scholar 

  • Ubuka T, Parhar I (2018) Dual actions of mammalian and piscine gonadotropin-inhibitory hormones, RFamide-related peptides and LPXRFamide peptides, in the hypothalamic-pituitary-gonadal axis. Front Endocrinol (Lausanne) 8:377

    Article  Google Scholar 

  • Ubuka T, Ueno M, Ukena K, Tsutsui K (2003) Developmental changes in gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica) hypothalamo-hypophysial system. J Endocrinol 178:311–318

    Article  CAS  PubMed  Google Scholar 

  • Ubuka T, Son YL, Tsutsui K (2016) Molecular, cellular, morphological, physiological and behavioral aspects of gonadotropin-inhibitory hormone. Gen Comp Endocrinol 227:27–50

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Jia J, Yang G, Qin J, Zhang C, Zhang Q, Sun C, Li W (2016) In vitro effects of somatostatin on the growth hormone-insulin-like growth factor axis in orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol 237:1–9

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Liu Q, Liu X, Xu Y, Shi B (2017a) Molecular characterization of Kiss2 receptor and in vitro effects of Kiss2 on reproduction-related gene expression in the hypothalamus of half-smooth tongue sole (Cynoglossus semilaevis). Gen Comp Endocrinol 249:55–63

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Liu Q, Liu X, Xu Y, Song X, Shi B (2017b) Molecular characterization of kiss2 and differential regulation of reproduction-related genes by sex steroids in the hypothalamus of half-smooth tongue sole (Cynoglossus semilaevis). Comp Biochem Physiol A Mol Integr Physiol 213:46–55

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yang G, Liu Q, Qin J, Xu Y, Li W, Liu X, Shi B (2017c) Inhibitory action of tongue sole LPXRFa, the piscine ortholog of gonadotropin-inhibitory hormone, on the signaling pathway induced by tongue sole kisspeptin in COS-7 cells transfected with their cognate receptors. Peptides 95:62–67

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Liu Q, Liu X, Xu Y, Shi B (2018a) Molecular characterization and expression profiles of LPXRFa at the brain-pituitary-gonad axis of half-smooth tongue sole (Cynoglossus semilaevis) during ovarian maturation. Comp Biochem Physiol B Biochem Mol Biol 216:59–68

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yang G, Liu Q, Qin J, Xu Y, Li W, Liu X, Shi B (2018b) Characterization of LPXRFa receptor in the half-smooth tongue sole (Cynoglossus semilaevis): molecular cloning, expression profiles, and differential activation of signaling pathways by LPXRFa peptides. Comp Biochem Physiol A Mol Integr Physiol 223:23–32

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yang G, Xu Y, Li W, Liu X (2018c) Recent studies of LPXRFa receptor signaling in fish and other vertebrates. Gen Comp Endocrinol. https://doi.org/10.1016/j.ygcen.2018.1011.1011

    Article  PubMed  Google Scholar 

  • White RJ, Collins JE, Sealy IM, Wali N, Dooley CM, Digby Z, Stemple DL, Murphy DN, Billis K, Hourlier T, Fullgrabe A, Davis MP, Enright AJ, Busch-Nentwich EM (2017) A high-resolution mRNA expression time course of embryonic development in zebrafish. Elife. https://doi.org/10.7554/eLife.30860

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Wang B, Liu X, Shi B, Zang K (2017) Evidences for involvement of growth hormone and insulin-like growth factor in ovarian development of starry flounder (Platichthys stellatus). Fish Physiol Biochem 43:527–537

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li S, Liu Y, Lu D, Chen H, Huang X, Liu X, Meng Z, Lin H, Cheng CH (2010) Structural diversity of the GnIH/GnIH receptor system in teleost: its involvement in early development and the negative control of LH release. Peptides 31:1034–1043

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Lin MC, Mock A, Yang M, Wayne NL (2014) Kisspeptins modulate the biology of multiple populations of gonadotropin-releasing hormone neurons during embryogenesis and adulthood in zebrafish (Danio rerio). PLoS One 9:e104330

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31602133), the Natural Science Foundation of Shandong Province (ZR2016CB02), Qingdao Municipal Science and Technology Bureau (17-1-1-61-jch), the Central Public-interest Scientific Institution Basal Research Fund, CAFS (2017HY-XKQ01), and the China Agriculture Research System (CARS-47).

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Authors and Affiliations

  1. Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, No. 106 Nanjing Road, Qingdao, 266071, China

    Bin Wang, Yaxing Zhang, Yongjiang Xu, Xuezhou Liu, Aijun Cui, Bao Shi & Yan Jiang

  2. Laboratory for Marine Fisheries and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Bin Wang, Yongjiang Xu, Xuezhou Liu, Bao Shi & Yan Jiang

  3. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China

    Yaxing Zhang & Aijun Cui

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  1. Bin Wang
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Correspondence to Xuezhou Liu.

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Wang, B., Zhang, Y., Xu, Y. et al. Developmental expression of LPXRFa, kisspeptin, and their receptor mRNAs in the half-smooth tongue sole Cynoglossus semilaevis. Fish Sci 85, 449–455 (2019). https://doi.org/10.1007/s12562-019-01293-4

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