Abstract
The hormone-sensitive lipase (HSL) gene plays an important role in mammals’ lipid metabolism. Therefore, its function in fish is capturing increasing attention. In this study, two distinct cDNAs, designated HSL1 and HSL2, are firstly identified from common carp Cyprinus carpio. The full-length cDNA of HSL1 and HSL2 consists of 3379 bp and 2732 bp, encoding polypeptide of 693 and 847 amino acids, respectively, and shares 60.6% amino acid identity. Phylogenetic analysis suggests that HSL1 and HSL2 are derived from paralogous genes, which might have arisen during a teleost-specific genome duplication event. The two HSL mRNAs are differentially expressed, both in terms of distribution among tissues and in terms of abundance during embryogenesis. Moreover, both HSL mRNAs are expressed in various tissues, the highest in abdominal fat. Meanwhile, the two HSLs are detected at all stages of embryonic development, suggesting that they could be functional and involved in embryogenesis. In addition, the results show that the mRNA expression level of HSL2 in the high group of intramuscular fat content is significantly higher than that in the low group (P < 0.01). The research provides basic data for developing a further understanding of the function of HSL as well as molecular regulation mechanism in fat metabolism of common carp.
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References
Anthonsen MW, Ronnstrand L, Wernstedt C, Degerman E, Holm C (1998) Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproterenol and govern activation properties in vitro. J Biol Chem 273(1):215–221
Chen J, Yang XJ, Tong H, Chen J, Zhao RQ (2004) Expressions of FAS and HSL mRNA in longissimus dorsi muscle and their relation to intramuscular fat contents in pig. J Agric Biotechnol 12:422–426
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 Endocrinol 206:130–138
Desvilettes C, Bourdier G, Breton JC (1997) Changes in lipid class and fatty acid composition during development in pike (Esox lucius L) eggs and larvae. Fish Physiol Biochem 16(5):381–393
Doherty MK, Owen MA, Davies SJ, Young IS, Whitfield PD (2013) Assessment of global proteome dynamics in carp: a model for investigating environmental stress. J Proteome Res 12(11):5246–5252
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791
Fraher D, Sanigorski A, Mellett N, Meikle P, Sinclair A, Gibert Y (2016) Zebrafish embryonic lipidomic analysis reveals that the yolk cell is metabolically active in processing lipid. Cell Rep 14(6):1317–1329
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of phyml 3.0. Syst Biol 59(3):307–321
Haemmerle G, Zimmermann R, Hayn M, Theussl C, Waeg G, Wagner E, Sattler W, Magin TM, Wagner EF, Zechner R (2002) Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J Biol Chem 277(7):4806–4815
Haemmerle G, Zimmermann R, Zechner R (2003) Letting lipids go: hormone-sensitive lipase. Curr Opin Lipidol 14(3):289–297
Han CY, Wen XB, Zheng QM, Li HB (2011) Effect of starvation on activities and mRNA expression of lipoprotein lipase and hormone-sensitive lipase in tilapia (Oreochromis niloticus × O. areus). Fish Physiol Biochem 37:113–122
Harbitz I, Langset M, Ege AG, Høyheim B, Davies W (1999) The porcine hormone-sensitive lipase gene: sequence, structure, polymorphisms and linkage mapping. Anim Genet 30(1):10–16
Holm C (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31(6):1120–1124
Holm C, Kirchgessner TG, Svenson KL, Fredrikson G, Nilsson S, Miller CG, Shively JE, Heinzmann C, Sparkes RS, Mohandas T, Lusis AJ, Belfrage P, Schotz MC (1988) Hormone-sensitive lipase: sequence, expression, and chromosomal localization to 19 cent-q13.3. Science 241(4872):1503–1506
Huang HL, Zhang Y, Cao MY, Xue LY, Shen WL (2018) Effects of fasting on the activities and mRNA expression levels of lipoprotein lipase (LPL), hormone-sensitive lipase (HSL) and fatty acid synthetase (FAS) in spotted seabass lateolabrax maculatus. Fish Physiol Biochem 44(1):387–400
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8(3): 275–282
Kazala EC, Petrak JL, Lozeman FJ, Mir PS, Laroche A, Deng JT, Weselake RJ (2003) Hormone-sensitive lipase activity in relation to fat content of muscle in Wagyu hybrid cattle. Livest Prod Sci 79(1):87–96
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(2):341–351
Khieokhajonkhet A, Kaneko G, Hirano Y, Wang L, Ushio H (2016) Different effects of growth hormone and fasting on the induction patterns of two hormone-sensitive lipase genes in red seabream Pagrus major. Gen Comp Endocrinol 236:121–130
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 Mol Integr Physiol 158:52–60
Lafontan M, Langin D (2009) Lipolysis and lipid mobilization in human adipose tissue. Prog Lipid Res 48(5):275–297
Lampidonis AD, Argyrokastritis A, Stravopodis DJ, Voutsinas GE, Ntouroupi TG, Margaritis LH, Bizelis I, Rogdakis E (2008) Cloning and functional characterization of the ovine hormone sensitive lipase (hsl) full-length cDNAs: an integrated approach. Gene 416:30–43
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(11):4897–4901
Li Z, Sumida M, Birchbauer A, Schotz MC, Reue K (1994) Isolation and characterization of the gene for mouse hormone-sensitive lipase. Genomics 24(2):259–265
Li SL, Mai KS, Xu W, Yuan YH, Zhang YJ, Zhou HH, Ai QH (2016) Effects of dietary lipid level on growth, fatty acid composition, digestive enzymes and expression of some lipid metabolism related genes of orange-spotted grouper larvae (Epinephelus coioides H.). Aquac Res 47(8):2481–2495
Liao K, Meng R, Ran ZS, Cheng GQ, Wang YJ, Xu JL, Xu SL, Yan XJ (2017) Short-term starvation in silver pomfret (Pampus argenteus): molecular effects on lipid mobilization and utilization. Aquac Res 48(9):4874–4885
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–△△CT method. Methods 25(4):402–408
Luan ZJ, Liu KD, He JN, Cheng M, Qu XX, Liu N (2016) The FAM134B, PPARγ, HSL and FAS gene expresion paterns and their asociation with intramuscular fat content in sheep. Acta Vet Et Zotech Sin 47(12):2379–2389
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 Biophys Res Commun 291(2):286–290
Meyer A, Van d PY (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945
Qiao Y, Huang ZG, Li QF, Liu ZS, Hao CL, Shi GQ, Dai R, Xie Z (2007) Developmental changes of the FAS and HSL mRNA expression and their effects on the content of intramuscular fat in Kazak and Xinjiang sheep. J Genet Genomics 34(10):909–917
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Sun J, Ji H, Li XX, Shi XC, Du ZY, Chen LQ (2016) Lipolytic enzymes involving lipolysis in teleost: synteny, structure, tissue distribution, and expression in grass carp (Ctenopharyngodon idella). Comp Biochem Physiol B Biochem Mol Biol 198:110–118
Sun ZP, Lv WH, Kuang YY, Cao DC, Tong GX, Sun XW, Zheng XH (2017) Cloning and expression of fatty acid synthase gene in common carp Cyprinus carpio. Chin J Fish 30(4):1–6
Takahara T, Minamoto T, Yamanaka H, Doi H, Kawabata Z (2012) Estimation of fish biomass using environmental DNA. PLoS One 7(4):e35868
Wang YP, Xu CC, Luo HL (2017) Research progress in relevant candidate genes of animal intramuscular fat deposition. Chin J Anim Nutr 29(5):1475–1480
Watt MJ, Holmes AG, Pinnamaneni SK, Garnham AP, Steinberg GR, Kemp BE, Febbraio MA (2006) Regulation of HSL serine phosphorylation in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab 290(3):E500–E508
Wu J, Zheng XH, Kuang YY, Lv WH, Cao DC, Dong F, Sun XW (2015a) Cloning and characteristic analysis of fatty acid elongase 5 in mirror carp (Cyprinus carpio). J Fish Sci Chin 22(1):9–16
Wu J, Zheng XH, Kuang YY, Lv WH, Cao DC, Dong F, He LC, Sun XW (2015b) Molecular cloning and analyzing of △6 fatty acid desaturase in mirror common carp. Chin J Fish 28(1):11–17
Yang G, Forrest R, Zhou H, Hickford J (2014) Variation in the ovine hormone-sensitive lipase gene (HSL) and its association with growth and carcass traits in New Zealand Suffolk sheep. Mol Biol Rep 41(4):2463–2469
Yeaman SJ (1990) Hormone-sensitive lipase-A multipurpose enzyme in lipid metabolism. Biochim Biophys Acta 1052(1):128–132
Zheng XH, Kuang YY, Lv WH, Cao DC, Sun ZP, Sun XW (2016) Genome-wide association study for muscle fat content and abdominal fat traits in common carp (Cyprinus carpio). PLoS One 11:e0169127
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This work was supported by the Central Public-interest Scientific Institution Basal Research Fund, HRFRI (HSY201805M), the National Natural Science Foundation of China (31302174), and the National Infrastructure of Fishery Germplasm Resources.
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All procedures were performed in accordance with the Guide for Care and Use of Laboratory Animals and approved by the Animal Care and Use Committee of Heilongjiang River Fisheries Research Institute.
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Zheng, X., Dang, H., Lv, W. et al. Molecular characterization and expression patterns of two hormone-sensitive lipase genes in common carp Cyprinus carpio. Fish Physiol Biochem 46, 439–450 (2020). https://doi.org/10.1007/s10695-019-00738-y
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DOI: https://doi.org/10.1007/s10695-019-00738-y