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Two isoforms of hormone-sensitive lipase b are generated by alternative exons usage and transcriptional regulation by insulin in grass carp (Ctenopharyngodon idella)

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Abstract

The aim of this study was to investigate the gene structure of two hormone-sensitive lipase b (HSLb) isoforms and their transcriptional regulation by insulin in grass carp (Ctenopharyngodon idella). HSL is an important lipolytic enzyme responsible for the hydrolysis of triacylglycerols (TAGs). Two isoforms (HSLa and HSLb) have been cloned in fish, but information about their gene structure and function is very few. In this study, a novel grass carp HSLb isoform (HSLb2) were firstly isolated and characterized from grass carp, encoding peptides of 848 amino acid residues. HSLb2 comprises 13 coding exons and contains a different exon encoding six amino acids in the 5′-region compared to previous reported HSLb (HSLb1), revealing that alternative multiple exons usage (Exon b1 and Exon b2) results in a significant variation in the 5′-region of HSLb transcripts. Exon b2 is located close to the 3′ end of exon b1. Both HSLb2 and HSLb1 mRNAs were expressed in a wide range of tissues, but the abundance of each HSLb messenger RNA (mRNA) showed the tissue-dependent expression patterns. Incubation of hepatocytes with insulin in vitro reduced the mRNA levels of HSLb2 rather than HSLb1, suggesting two HSLb forms may serve somewhat different roles in the regulation of lipogenesis by insulin. To our knowledge, for the first time, the present study provides evidence that HSLb1 and HSLb2 are differentially expressed among tissues and also differentially regulated by insulin in vitro, which provide the groundwork to elucidate the gene structure and physiological function of HSL in fish.

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References

  • Blaise R, Grober J, Rouet P, Tavernier G, Daegelen D, Langin D (1999) Testis expression of hormone-sensitive lipase is conferred by a specific promoter that contains four regions binding testicular nuclear proteins. J Biol Chem 274:9327–9334

    Article  CAS  PubMed  Google Scholar 

  • Blaise R, Guillaudeux T, Tavernier G, Daegelen D, Evrard B, Mairal A, Holm C, Jégou B, Langin D (2001) Testis hormone-sensitive lipase expression in spermatids is governed by a short promoter in transgenic mice. J Biol Chem 276:5109–5115

    Article  CAS  PubMed  Google Scholar 

  • Burland TG (2000) Dnastar’s lasergene sequence analysis software. Methods Mol Biol 132:71–91

    CAS  PubMed  Google Scholar 

  • Chen QL, Luo Z, Song YF, Wu K, Huang C, Pan YX, Zhu QL (2014) Hormone-sensitive lipase in yellow catfish Pelteobagrus fulvidraco: molecular characterization, mRNA tissue expression and transcriptional regulation by leptin in vivo and in vitro. Gen Comp Endocr 206:130–138

    Article  CAS  PubMed  Google Scholar 

  • Cowley DJ, Sheridan MA (1993) Insulin stimulates hepatic lipogenesis in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 11:421–428

    Article  CAS  PubMed  Google Scholar 

  • Ellesat KS, Yazdani M, Holth TF, Hylland K (2011) Species-dependent sensitivity to contaminants: an approach using primary hepatocyte cultures with three marine fish species. Mar Environ Res 72:216–224

    Article  CAS  PubMed  Google Scholar 

  • Grober J, Laurell H, Blaise R, Fabry B, Schaak S, Holm C, Langin D (1997) Characterization of the promoter of human adipocyte hormone-sensitive lipase. Biochem J 328:453–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harmon JS, Sheridan MA (1992) Effects of nutritional state, insulin, and glucagon on lipid mobilization in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 87:214–221

    Article  CAS  PubMed  Google Scholar 

  • Harmon JS, Rieniets LM, Sheridan MA (1993) Glucagon and insulin regulate lipolysis in trout liver by altering phosphorylation of triacylglycerol lipase. Am J Phys 256:255–260

    Google Scholar 

  • Holm C, Kirchgessner TG, Svenson KL, Fredrikson G, Nilsson S, Miller CG et al (1988) Hormone-sensitive lipase: sequence, expression, and chromosomal localization to 19 cent-q13.3. Science 241:1503–1506

    Article  CAS  PubMed  Google Scholar 

  • Holm C, Østerlund T, Laurell H, Contreras JA (2000) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu Rev Nutr 20:365–393

    Article  CAS  PubMed  Google Scholar 

  • Holm C (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31:1120–1124

    Article  CAS  PubMed  Google Scholar 

  • Kittilson JD, Reindl KM, Sheridan MA (2011) Rainbow trout (Oncorhynchus mykiss) possess two hormone-sensitive lipase-encoding mRNAs that are differentially expressed and independently regulated by nutritional state. Comp Biochem Physiol A 158:52–60

    Article  Google Scholar 

  • Khieokhajonkhet A, Kaneko G, Ohara K, Shirakami H, Ushio H (2014) Hormone sensitive lipase in Japanese flounder Paralichthys olivaceus: the potential function of the inclinator muscle of fin as a lipid storage site. Fish Sci 80:341–351

    Article  CAS  Google Scholar 

  • Lampidonis AD, Rogdakis E, Voutsinas GE, Stravopodis DJ (2011) The resurgence of hormone-sensitive lipase (HSL) in mammalian lipolysis. Gene 477:1–11

    Article  CAS  PubMed  Google Scholar 

  • Langin D, Laurell H, Holst LS, Belfrage P, Holm C (1993) Gene organization and primary structure of human hormone-sensitive lipase: possible significance of a sequence homology with a lipase of Moraxella TA144, an antarctic bacterium. Proc Natl Acad Sci U S A 90:4897–4901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Mairal A, Melaine N, Laurell H, Grober J, Holst LS, Guillaudeux T, Holm C, Jégou B, Langin D (2002) Characterization of a novel testicular form of human hormone-sensitive lipase. Biochem Bioph Res Co 291:286–290

    Article  CAS  Google Scholar 

  • Mennigen JA, Plagnes-Juan E, Figueredo-Silva CA, Seiliez I, Panserat S, Skiba-Cassy S (2014) Acute endocrine and nutritional co-regulation of the hepatic omy-miRNA-122b and the lipogenic gene fas in rainbow trout (Oncorhynchus mykiss). Comp Biochem Phyisol B 169:16–24

    Article  CAS  Google Scholar 

  • Plisetskaya EM, Sheridan MA, Mommsen TP (1989) Metabolic changes in coho and Chinook salmon resulting from acute insufficiency in pancreatic hormones. J Exp Zool 249:158–164

    Article  CAS  PubMed  Google Scholar 

  • Plagnes-Juan E, Lansard M, Seiliez I, Medale F, Corraze G, Kaushik S, Panserat S, Skiba-Cassy S (2008) Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J Exp Biol 211:2510–2518

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Zacarias J, Castro-Munozledo F, Kuri-Harcuch W (1992) Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with oil red O. Histochemistry 97:493–497

    Article  CAS  PubMed  Google Scholar 

  • Seth R, Yang S, Choi S, Sabean M, Roberts E (2004) In vitro assessment of copper-induced toxicity in the human hepatoma line, HepG2. Toxicol in Vitro 18:501–509

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Ji H, Li XX, Shi XC, Du Z, Chen LQ (2016) Lipolytic enzymes involving lipolysis in teleost: Synteny, structure, tissue distribution, and expression in grass carp (Ctenopharyngodon idella). Comp Biochem Physiol B 27:110–118

    Article  Google Scholar 

  • Saltiel AR, Kahn CR (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799–806

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Lu Y, Zhang Y, Ning Z, Li Y, Zhao Q, Lu H, Huang R, Xia X, Feng Q et al (2015) The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation. Nat Genet 47:962

    Article  CAS  PubMed  Google Scholar 

  • Watt MJ, Steinberg GR (2008) Regulation and function of triacylglycerol lipases in cellular metabolism. Thorac Cardiovasc Surg 414:313–325

    CAS  Google Scholar 

  • Weil C, Lefèvre F, Bugeon J (2013) Characteristics and metabolism of different adipose tissues in fish. Rev Fish Biol Fisher 23:157–173

    Article  Google Scholar 

  • Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A (2009) Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 50:3–21

    Article  CAS  PubMed  Google Scholar 

  • Zhuo MQ, Luo Z, Wu K, Zhu QL, Zheng JL, Zhang LH, Chen QL (2014) Regulation of insulin on lipid metabolism in freshly isolated hepatocytes from yellow catfish (Pelteobagrus fulvidraco). Comp Biochem Phyisol B 177:21–28

    Article  Google Scholar 

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Acknowledgments

This work was financially supported by the National Basic Research Program of China (2014CB138603).

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Authors and Affiliations

  1. College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China

    Jian Sun, Zhou Yang, PeiZhen Xiao, Yong Liu & Hong Ji

  2. Laboratory of Aquaculture Nutrition and Environmental Health, School of Life Sciences, East China Normal University, Shanghai, China

    ZhenYu Du & LiQiao Chen

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  1. Jian Sun
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  2. Zhou Yang
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  3. PeiZhen Xiao
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  4. Yong Liu
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  5. Hong Ji
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  6. ZhenYu Du
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  7. LiQiao Chen
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Correspondence to Hong Ji.

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Sun, J., Yang, Z., Xiao, P. et al. Two isoforms of hormone-sensitive lipase b are generated by alternative exons usage and transcriptional regulation by insulin in grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 43, 539–547 (2017). https://doi.org/10.1007/s10695-016-0308-1

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  • DOI: https://doi.org/10.1007/s10695-016-0308-1

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