Skip to main content
Log in

Leptin and its receptor in turbot Scophthalmus maximus: cloning, characterization and expression response to ratios of dietary carbohydrate–lipid

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

In the present study, the full-length cDNA sequences of leptin (LEP) and its receptor (LEPR) from turbot Scophthalmus maximus were cloned. The cDNA of tLEP was 1126 bp in length encoding 157 amino acids. The amino acid sequence shared low identity with human LEP (18.8 %), but the three-dimensional structures of these two LEPs were strongly conserved. The deduced 1173-amino acid sequence of tLEPR was 28 % identical to human LEPR, and 82 % too range-spotted grouper LEPR, containing all functionally important domains conserved in vertebrate LEPR. Tissue distribution analysis showed that tLEP was abundantly expressed in brain, eyes and liver. The highest level of tLEPR mRNA was found in liver and kidney. After a 9-week feeding trial using diets with different ratios of carbohydrate–lipid (1:6, 1:2, 2:1 and 14:1), it was found that the increase in dietary carbohydrate-to-lipid ratios from 1:6 to 2:1 did not significantly influence tLEP and tLEPR expression in turbot liver (P > 0.05). The hepatic tLEP expression was significantly elevated in treatment with 14:1 dietary carbohydrate-to-lipid ratio (P < 0.05). The hepatic tLEPR mRNA level in group with 14:1 dietary carbohydrate-to-lipid ratio was significantly lower than that in 1:6 group (P < 0.05), but had no significant difference with the other two groups (P > 0.05). These results revealed the important relationship between dietary carbohydrate-to-lipid ratio and LEP expression in turbot.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguilar AJ, Conde-Sieira M, Polakof S, Miguez JM, Soengas JL (2010) Central leptin treatment modulates brain glucosensing function and peripheral energy metabolism of rainbow trout. Peptides 31:1044–1054

    Article  CAS  PubMed  Google Scholar 

  • Ahima RS, Flier JS (2000) Leptin. Annu Rev Physiol 62:413–437

    Article  CAS  PubMed  Google Scholar 

  • Baltzegar DA, Reading BJ, Douros JD, Borski RJ (2014) Role for leptin in promoting glucose mobilization during acute hyperosmotic stress in teleost fishes. J Endocrinol 220:61–72

    Article  CAS  PubMed  Google Scholar 

  • Bjorbaek C, Kahn BB (2004) Leptin signaling in the central nervous system and the periphery. Recent Prog Horm Res 59:305–332

    Article  CAS  PubMed  Google Scholar 

  • Cao YB, Xue JL, Wu LY, Jiang W, Hu PN, Zhu J (2011) The detection of 3 leptin receptor isoforms in crucian carp gill and the influence of fasting and hypoxia on their expression. Domest Anim Endocrinol 41:74–80

    Article  CAS  PubMed  Google Scholar 

  • Chua SC Jr, Koutras IK, Han L, Liu S-M, Kay J, Young SJ, Chung WK, Leibel RL (1997) Fine structure of the murine leptin receptor gene: splice site suppression is required to form two alternatively spliced transcripts. Genomics 45:264–270

    Article  CAS  PubMed  Google Scholar 

  • Copeland DL, Duff RJ, Liu Q, Prokop J, Londraville RL (2011) Leptin in teleost fishes: an argument for comparative study. Front Physiol 2:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Crespi EJ, Denver RJ (2006) Leptin (ob gene) of the South African clawed frog Xenopus laevis. Proc Natl Acad Sci USA 103:10092–10097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Pedro N, Martinez-Alvarez R, Delgado MJ (2006) Acute and chronic leptin reduces food intake and body weight in goldfish (Carassius auratus). J Endocrinol 188:513–520

    Article  PubMed  Google Scholar 

  • De Vos P, Guerre-Millot M, Leturque A, Girard J, Staels B, Auwerx J (1995) Transient increase in obese gene expression after food intake or insulin administration. Nature 377:527–528

    Article  PubMed  Google Scholar 

  • Denver RJ, Bonett RM, Boorse GC (2011) Evolution of leptin structure and function. Neuroendocrinology 94:21–38

    Article  CAS  PubMed  Google Scholar 

  • Frühbeck G, Salvador J (2000) Relation between leptin and the regulation of glucose metabolism. Diabetologia 43:3–12

    Article  PubMed  Google Scholar 

  • Gong N, Björnsson BT (2014) Leptin signaling in the rainbow trout central nervous system is modulated by a truncated leptin receptor isoform. Endocrinology 155(7):2445–2455

    Article  PubMed  Google Scholar 

  • Gong Y, Luo Z, Zhu QL, Zheng JL, Tan XY, Chen QL, Lin YC, Lu RH (2013a) Characterization and tissue distribution of leptin, leptin receptor and leptin receptor overlapping transcript genes in yellow catfish Pelteobagrus fulvidraco. Gen Comp Endocrinol 182:1–6

    Article  CAS  PubMed  Google Scholar 

  • Gong N, Einarsdottir IE, Johansson M, Björnsson BT (2013b) Alternative splice variants of the rainbow trout leptin receptor encode multiple circulating leptin-binding proteins. Endocrinology 154(7):2331–2340

    Article  CAS  PubMed  Google Scholar 

  • Gong N, Jönsson E, Bjornsson BT (2015) Acute anorexigenic action of leptin in rainbow trout is mediated by the hypothalamic Pi3 k pathway. J Mol Endocrinol. doi:10.1530/JME-15-0279

    Google Scholar 

  • Gorissen M, Bernier NJ, Nabuurs SB, Flik G, Huising MO (2009) Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution. J Endocrinol 201:329–339

    Article  CAS  PubMed  Google Scholar 

  • Huising MO, Geven EJ, Kruiswijk CP, Nabuurs SB, Stolte EH, Spanings FA, Verburg-van Kemenade BM, Flik G (2006) Increased leptin expression in common Carp (Cyprinus carpio) after food intake but not after fasting or feeding to satiation. Endocrinology 147:5786–5797

    Article  CAS  PubMed  Google Scholar 

  • Kling P, Rønnestad I, Stefansson SO, Murashita K, Kurokawa T, Björnsson BT (2009) A homologous salmonid leptin radioimmunoassay indicates elevated plasma leptin levels during fasting of rainbow trout. Gen Comp Endocrinol 162:307–312

    Article  CAS  PubMed  Google Scholar 

  • Kolaczynski JW, Considine RV, Ohannesian J, Marco C, Opentanova I, Nyce MR, Myint M, Caro JF (1996a) Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves. Diabetes 45:1511–1515

    Article  CAS  PubMed  Google Scholar 

  • Kolaczynski JW, Nyce MR, Considine RV, Boden G, Nolan JJ, Henry R, Mudaliar SR, Olefsky J, Caro JF (1996b) Acute and chronic effect of insulin on leptin production in humans: studies in vivo and in vitro. Diabetes 45:699–701

    Article  CAS  PubMed  Google Scholar 

  • Kurokawa T, Murashita K (2009) Genomic characterization of multiple leptin genes and a leptin receptor gene in the Japanese medaka, Oryzias latipes. Gen Comp Endocrinol 161:229–237

    Article  CAS  PubMed  Google Scholar 

  • Kurokawa T, Murashita K, Suzuki T, Uji S (2008) Genomic characterization and tissue distribution of leptin receptor and leptin receptor overlapping transcript genes in the pufferfish, Takifugu rubripes. Gen Comp Endocrinol 158:108–114

    Article  CAS  PubMed  Google Scholar 

  • Li GG, Liang XF, Xie Q, Li G, Yu Y, Lai K (2010) Gene structure, recombinant expression and functional characterization of grass carp leptin. Gen Comp Endocrinol 166:117–127

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - {\Delta \Delta }C_{\text{t}} }}\) method. Methods 25:402–408

  • Lu RH, Liang XF, Wang M, Zhou Y, Bai XL, He Y (2012) The role of leptin in lipid metabolism in fatty degenerated hepatocytes of the grass carp Ctenopharyngodon idellus. Fish Physiol Biochem 38:1759–1774

    Article  CAS  PubMed  Google Scholar 

  • Muoio DM, Dohn GL, Fiedorek FT, Tapscott EB, Coleman RA (1997) Leptin directly alters lipid partitioning in skeletal muscle. Diabetes 46:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Murashita K, Uji S, Yamamoto T, Ronnestad I, Kurokawa T (2008) Production of recombinant leptin and its effects on food intake in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part B Biochem Mol Biol 150:377–384

    Article  Google Scholar 

  • Nemecz M, Preininger K, Englisch R, Fürnsinn C, Schneider B, Waldhäusl W, Roden M (1999) Acute effect of leptin on hepatic glycogenolysis and gluconeogenesis in perfused rat liver. Hepatology 29:166–172

    Article  CAS  PubMed  Google Scholar 

  • Nie Q, Miao H, Miao S, Chen C, Li J, Zhang W, Mai K (2013) Effects of dietary carbohydrate sources and levels on the activities of carbohydrate metabolic enzymes in turbot (Scophthalmus maximus L.). Acta Hydrobiol Sin 37:425–433 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Pallett AL, Morton NM, Cawthorne MA, Emilsson V (1997) Leptin inhibits insulin secretion and reduces insulin mRNA levels in rat isolated pancreatic islets. Biochem Biophys Res Commun 238:267–270

    Article  CAS  PubMed  Google Scholar 

  • Polakof S, Míguez JM, Soengas JL (2007) In vitro evidences for glucosensing capacity and mechanisms in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 293:R1410–R1420

    Article  CAS  PubMed  Google Scholar 

  • Reidy SP, Weber J-M (2000) Leptin: an essential regulator of lipid metabolism. Comp Biochem Physiol A Mol Integr Physiol 125:285–298

    Article  CAS  PubMed  Google Scholar 

  • Rentsch J, Chiesi M (1996) Regulation of ob gene mRNA levels in cultured adipocytes. FEBS Lett 379:55–59

    Article  CAS  PubMed  Google Scholar 

  • Rock F, Altmann S, Van Heek M, Kastelein R, Bazan J (1996) The leptin haemopoietic cytokine fold is stabilized by an intrachain disulfide bond. Horm Metab Res 28:649–652

    Article  CAS  PubMed  Google Scholar 

  • Ronnestad I, Nilsen TO, Murashita K, Angotzi AR, Gamst Moen AG, Stefansson SO, Kling P, Thrandur Bjornsson B, Kurokawa T (2010) Leptin and leptin receptor genes in Atlantic salmon: cloning, phylogeny, tissue distribution and expression correlated to long-term feeding status. Gen Comp Endocrinol 168:55–70

    Article  CAS  PubMed  Google Scholar 

  • Rossetti L, Massillon D, Barzilai N, Vuguin P, Chen W, Hawkins M, Wu J, Wang J (1997) Short term effects of leptin on hepatic gluconeogenesis and in vivo insulin action. J Biol Chem 272:27758–27763

    Article  CAS  PubMed  Google Scholar 

  • Shimabukuro M, Koyama K, Chen G, Wang M-Y, Trieu F, Lee Y, Newgard CB, Unger RH (1997) Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Natl Acad Sci 94:4637–4641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soengas JL (2014) Contribution of glucose—and fatty acid sensing systems to the regulation of food intake in fish. A review. Gen Comp Endocrinol 205:36–48

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Liu R, Hawkins M, Barzilai N, Rossetti L (1998) A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature 393:684–688

    Article  CAS  PubMed  Google Scholar 

  • Weil C, Le Bail P, Sabin N, Le Gac F (2003) In vitro action of leptin on FSH and LH production in rainbow trout (Onchorynchus mykiss) at different stages of the sexual cycle. Gen Comp Endocrinol 130:2–12

    Article  CAS  PubMed  Google Scholar 

  • Won ET, Baltzegar DA, Picha ME, Borski RJ (2012) Cloning and characterization of leptin in a Perciform fish, the striped bass (Morone saxatilis): control of feeding and regulation by nutritional state. Gen Comp Endocrinol 178:98–107

    Article  CAS  PubMed  Google Scholar 

  • Wong MM, Yu RM, Ng PK, Law SH, Tsang AK, Kong RY (2007) Characterization of a hypoxia-responsive leptin receptor [omLepR(L)] cDNA from the marine medaka (Oryzias melastigma). Mar Pollut Bull 54:797–803

    Article  CAS  PubMed  Google Scholar 

  • Yun B, Ai Q, Mai K, Xu W, Qi G, Luo Y (2012) Synergistic effects of dietary cholesterol and taurine on growth performance and cholesterol metabolism in juvenile turbot (Scophthalmus maximus L.) fed high plant protein diets. Aquaculture 324:85–91

    Article  Google Scholar 

  • Zabeau L, Lavens D, Peelman F, Eyckerman S, Vandekerckhove J, Tavernier J (2003) The ins and outs of leptin receptor activation. FEBS Lett 546:45–50

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Chen H, Zhang Y, Li S, Lu D, Zhang H, Meng Z, Liu X, Lin H (2013) Molecular cloning, characterization and expression profiles of multiple leptin genes and a leptin receptor gene in orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol 181:295–305

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the National Basic Research Program (973 Program, No. 2014CB138600), the National Natural Science Foundation of China (No. 31572628) and the Open Fund of the Key Laboratory of Marine Biotech of Guangxi (GLMBT-201401). We thank Xiaojing Dong and Xiaoxue Geng for their assistance during the experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenbing Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, D., Miao, H., Nie, Q. et al. Leptin and its receptor in turbot Scophthalmus maximus: cloning, characterization and expression response to ratios of dietary carbohydrate–lipid. Fish Physiol Biochem 42, 1665–1679 (2016). https://doi.org/10.1007/s10695-016-0248-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0248-9

Keywords

Navigation