Effect of taurine intervention on oleic acid-induced primary hepatocyte steatosis in orange-spotted grouper (Epinephelus coioides)
DOI:
https://doi.org/10.2298/ABS210916043XKeywords:
Epinephelus coioides, taurine, hepatocyte steatosis, differential expression gene, RNA-SeqAbstract
Paper description:
- Control of metabolic syndrome in cultured fish is needed to counteract the increase in fatty liver.
- An oleic acid-induced primary hepatocyte steatosis model in grouper was established to investigate effects of taurine intervention in liver lipid metabolism. Transcriptome hepatocyte analysis was used to identify differentially expressed genes and construct a metabolic network of taurine in lipid metabolism.
- Differentially expressed genes are involved in primary bile acid biosynthesis, glycerophospholipid metabolism, glycerolipid metabolism, fatty acid elongation.
- Taurine intervention affected the expression of identified genes. Taurine plays a regulatory role in lipid metabolism improving the functioning of steatosis hepatocytes.
Abstract: Examination of the molecular mechanism of taurine regulation of lipid metabolism in fish is limited. In this study, an oleic acid (OA)-induced hepatocyte steatosis model of orange-spotted grouper (Epinephelus coioides) was established for the first time. The model was used to test the effect of taurine on steatosis hepatocytes in Control, High-fat (0.4 mM OA) and Taurine (0.4 mM OA + 2 mM taurine) experimental groups of fish. Hepatocyte samples were subjected to transcriptome analysis. A total of 99634 unigenes was assembled, 69982 unigenes were annotated and 1831 differentially expressed genes (DEGs) in Control vs High-fat group, and 526 DEGs in the High-fat vs Taurine group were identified, of which 824 DEGs (Control vs High-fat) and 237 DEGs (High-fat vs Taurine) were observed to be upregulated, and 1007 DEGs (Control vs High-fat) and 289 DEGs (High-fat vs Taurine) were downregulated after taurine intervention. These genes are involved in peroxisome proliferator-activated receptor (PPAR) and 5' AMP-activated protein kinase (AMPK) signaling pathways, fatty acid elongation, primary bile acid biosynthesis, glycerophospholipid and glycerolipid metabolism. The findings provide new clues in understanding the regulatory role of taurine in lipid and fatty acid metabolism of fish. It is hoped that the obtained results will help in the design of feed formulations to improve grouper growth from the perspective of aquaculture nutrition.
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References
Turchini GM, Torstensen BE, Ng WK. Fish oil replacement in finfish nutrition. Rev Aquac. 2009;1(1):10-57.
https://doi.org/10.1111/j.1753-5131.2008.01001.x
Li X, Zheng S, Ma X, Cheng K, Wu G. Effects of dietary starch and lipid levels on the protein retention and growth of largemouth bass (Micropterus salmoides). Amino Acids. 2020;52:999-1016.
https://doi.org/10.1007/s00726-020-02869-6
Welengane E, Sado RY, de Almeida Bicudo AJ. Protein‐sparing effect by dietary lipid increase in juveniles of the hybrid fish tambatinga (♀ Colossoma macropomum × ♂ Piaractus brachypomus). Aquac Nutr. 2019;25(6):1272-80.
https://doi.org/10.1111/anu.12941
Boujard T, Gelineau A, Coves D, Corraze G, Dutto G, Gasset E, Kaushik S. Regulation of feed intake, growth, nutrient and energy utilisation in European sea bass (Dicentrarchus labrax) fed high fat diets. Aquaculture. 2003;231(1):529-45.
https://doi.org/10.1016/j.aquaculture.2003.11.010
Zhou Y, Guo J, Tang R, Ma H, Chen Y, Lin S. High dietary lipid level alters the growth, hepatic metabolism enzyme, and anti-oxidative capacity in juvenile largemouth bass Micropterus salmoides. Fish Physiol Biochem. 2020;46(1):125-34.
https://doi.org/10.1007/s10695-019-00705-7
Li A, Yuan X, Liang X, Liu L, Li J, Li B, Fang J, Li J, He S, Xue M, Wang J, Tao Y. Adaptations of lipid metabolism and food intake in response to low and high fat diets in juvenile grass carp (Ctenopharyngodon idellus). Aquaculture. 2016;457:43-9.
https://doi.org/10.1016/j.aquaculture.2016.01.014
Cao X, Dai Y, Liu M, Yuan X, Wang C, Huang Y, Liu W, Jiang G. High-fat diet induces aberrant hepatic lipid secretion in blunt snout bream by activating endoplasmic reticulum stress-associated IRE1/XBP1 pathway. BBA-Mol Cell Biol L. 2019;1864(3):213-23.
https://doi.org/10.1016/j.bbalip.2018.12.005
Tang T, Hu Y, Peng M, Chu W, Hu Y, Zhong L. Effects of high-fat diet on growth performance, lipid accumulation and lipid metabolism-related MicroRNA/gene expression in the liver of grass carp (Ctenopharyngodon idella). Comp. Biochem Physiol B Biochem Mol Biol. 2019;234:34-40.
https://doi.org/10.1016/j.cbpb.2019.04.006
Jia R, Cao L, Du J, He Q, Gu Z, Jeney G, Xu P, Yin G. Effects of high-fat diet on antioxidative status, apoptosis and inflammation in liver of tilapia (Oreochromis niloticus) via Nrf2, TLRs and JNK pathways. Fish Shellfish Immun. 2020;104:391-401.
https://doi.org/10.1016/j.fsi.2020.06.025
Zhong Y, Pan Y, Liu L, Li H, Li Y, Jiang J, Xiang J, Zhang J, Chu W. Effects of high fat diet on lipid accumulation, oxidative stress and autophagy in the liver of Chinese softshell turtle (Pelodiscus sinensis). Comp Biochem Physiol B Biochem Mol Biol. 2020;240:110331.
https://doi.org/10.1016/j.cbpb.2019.110331
Abdel FMES. Is dietary taurine supplementation beneficial for farmed fish and shrimp? a comprehensive review. Rev Aquac. 2014;6(4):241-55.
https://doi.org/10.1111/raq.12042
Salze GP, Davis DA. Taurine: a critical nutrient for future fish feeds. Aquaculture. 2015;437:215-29.
https://doi.org/10.1016/j.aquaculture.2014.12.006
Yang H, Tian L, Huang J, Liang G, Liu Y. Dietary taurine can improve the hypoxia-tolerance but not the growth performance in juvenile grass carp Ctenopharyngodon idellus. Fish Physiol Biochem. 2013;39(5):1071-8.
https://doi.org/10.1007/s10695-012-9763-5
Caine JJ, Geracioti TD. Taurine, energy drinks, and neuroendocrine effects. Cleve Clin J Med. 2016;83(12):895-904.
https://doi.org/10.3949/ccjm.83a.15050
Wang X, He G, Mai K, Xu W, Zhou H. Differential regulation of taurine biosynthesis in rainbow trout and Japanese flounder. Sci Rep. 2016;6(2):21231.
https://doi.org/10.1038/srep21231
Espe M, Ruohonen K, El-Mowafi A. Effect of taurine supplementation on the metabolism and body lipid-to-protein ratio in juvenile Atlantic salmon (Salmo salar). Aquac Res. 2012;43(3):349-60.
https://doi.org/10.1111/j.1365-2109.2011.02837.x
Chen W, Guo JX, Chang P. The effect of taurine on cholesterol metabolism. Mol Nutr Food Res. 2012;56(5):681-90.
https://doi.org/10.1002/mnfr.201100799
Carina SS, Daniel F, Letícia MI, Talita R, Erika AR, Ana PA, Joseane M, Adriana ST, Everardo MC, Licio AV. Taurine enhances the anorexigenic effects of insulin in the hypothalamus of rats. Amino Acids. 2012;42(6):2403-10.
https://doi.org/10.1007/s00726-011-1045-5
Kim S, Kim K, Kim K, Kim K, Son M, Rust M, Johnson R. Effect of dietary taurine levels on the conjugated bile acid composition and growth of juvenile Korean rockfish Sebastes schlegeli (Hilgendorf). Aquac Res. 2015;46(11):2768-75.
https://doi.org/10.1111/are.12431
Murakami S, Ono A, Kawasaki A, Takenaga T, Ito T. Taurine attenuates the development of hepatic steatosis through the inhibition of oxidative stress in a model of nonalcoholic fatty liver disease in vivo and in vitro. Amino Acids. 2018;50(9):1279-88.
https://doi.org/10.1007/s00726-018-2605-8
de Moura LB, Diogenes AF, Vasconcelos Campelo DA, Alves De Almeida FL, Pousao-Ferreira PM, Furuya WM, Peres H, Oliva-Teles A. Nutrient digestibility, digestive enzymes activity, bile drainage alterations and plasma metabolites of meagre (Argyrosomus regius) feed high plant protein diets supplemented with taurine and methionine. Aquaculture. 2019;511:734231.
https://doi.org/10.1016/j.aquaculture.2019.734231
McGettigan PA. Transcriptomics in the RNA-seq era. Curr Opin Chem Biol. 2013;17(1):4-11.
https://doi.org/10.1016/j.cbpa.2012.12.008
Paneru BD, Al-Tobasei R, Kenney B, Leeds TD, Salem M. RNA-Seq reveals MicroRNA expression signature and genetic polymorphism associated with growth and muscle quality traits in rainbow trout. Sci Rep. 2017;7(1):9078.
https://doi.org/10.1038/s41598-017-09515-4
Duan Y, Wang Y, Xiong D, Zhang J. RNA-seq revealed the signatures of immunity and metabolism in the Litopenaeus vannamei intestine in response to dietary succinate. Fish Shellfish Immun. 2019;95:16-24.
https://doi.org/10.1016/j.fsi.2019.09.074
Fernandez I, Fernandes JMO, Roberto VP, Kopp M, Oliveira C, Riesco MF, Dias J, Cox CJ, Cancela ML, Cabrita E, Gavaia P. Circulating small non-coding RNAs provide new insights into vitamin K nutrition and reproductive physiology in teleost fish. Biochim Biophys Acta Gen Subj. 2019;1863(1):39-51.
https://doi.org/10.1016/j.bbagen.2018.09.017
Abernathy J, Overturf K. Toward resolving long noncoding RNAs in fish: identification, mapping and association to disease using strand-specific RNA-seq in rainbow trout fed alternative diets. J Anim Sci. 2016;94(4):S67-8.
https://doi.org/10.2527/jas2016.94supplement467a
He L, Qin Y, Wang Y, Li D, Chen W, Ye J. Effects of dietary replacement of fish oil with soybean oil on the growth performance, plasma components, fatty acid composition, and lipid metabolism of groupers Epinephelus coioides. Aquac Nutr. 2021;27(5):1494-511.
https://doi.org/10.1111/anu.13292
Feng H, Yi K, Qian X, Niu X, Sun Y, Ye J. Growth and metabolic responses of juvenile grouper (Epinephelus coioides) to dietary methionine/cystine ratio at constant sulfur amino acid levels. Aquaculture. 2020;518:734869.
https://doi.org/10.1016/j.aquaculture.2019.734869
Koven W, Peduel A, Gada M, Nixon O, Ucko M. Taurine improves the performance of white grouper juveniles (Epinephelus Aeneus) fed a reduced fish meal diet. Aquaculture. 2016;460:8-14.
https://doi.org/10.1016/j.aquaculture.2016.04.004
Wang X, Zhou M, Huang Yan, Wang K, Ye J. Effects of dietary taurine level on growth performance and body composition of grouper (Epinephelus coioides) at different growth stages. Chinese J Anim Nutr. 2017;29(5):1810-20.
Shen G, Wang S, Dong J, Fen J, Xu J, Xia F, Wang X, Ye J. Metabolic effect of dietary taurine supplementation on grouper (Epinephelus coioides): a 1H-NMR-based metabolomics study. Molecules. 2019;24:2253.
https://doi.org/10.3390/molecules24122253
Zhou W, Rahimnejad S, Tocher DR, Lu K, Zhang C, Sun, Y. Metformin attenuates lipid accumulation in hepatocytes of blunt snout bream (Megalobrama amblycephala) via activation of AMP-activated protein kinase. Aquaculture. 2019;499:90-100.
https://doi.org/10.1016/j.aquaculture.2018.09.028
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511-5.
https://doi.org/10.1038/nbt.1621
Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.
https://doi.org/10.1186/gb-2010-11-10-r106
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006;34:W293-7.
https://doi.org/10.1093/nar/gkl031
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT Method. Methods. 2001;25(4):402-8.
https://doi.org/10.1006/meth.2001.1262
Cao P, Huang G, Yang Q, Guo J, Su Z. The effect of chitooligosaccharides on oleic acid-induced lipid accumulation in HepG(2) cells. Saudi Pharm J. 2016;24(3):292-8.
https://doi.org/10.1016/j.jsps.2016.04.023
Ellesat KS, Yazdani M, Holth TF. Species-dependent sensitivity to contaminants: an approach using primary hepatocyte cultures with three marine fish species. Mar Environ Res. 2011;72(4):216-24.
https://doi.org/10.1016/j.marenvres.2011.09.003
Espe M, Xie S, Chen S, Pedro A, Holen E. Development of a fatty liver model using oleic acid in primary liver cells isolated from Atlantic salmon and the prevention of lipid accumulation using metformin. Aquac Nutr. 2019;25(3):737-46.
https://doi.org/10.1111/anu.12905
Pesonen M, Andersson TB. Fish primary hepatocyte culture; an important model for xenobiotic metabolism and toxicity studies. Aquat Toxicol. 1997;37(2):253-67.
https://doi.org/10.1016/S0166-445X(96)00811-9
Zhao X, Xue J, Xie M. Osthole inhibits oleic acid/lipopolysaccharide-induced lipid accumulation and inflammatory response through activating PPARα signaling pathway in cultured hepatocytes. Exp Gerontol. 2019;119:7-13.
https://doi.org/10.1016/j.exger.2019.01.014
Huang W, Chen Y, Liu H, Wu S, Liou C. Ginkgolide C reduced oleic acid-induced lipid accumulation in HepG2 cells. Saudi Pharm J. 2018;26(8):1178-84.
https://doi.org/10.1016/j.jsps.2018.07.006
Saponaro C, Gaggini M, Carli F, Gastaldelli A. The subtle balance between lipolysis and lipogenesis: a critical point in metabolic homeostasis. Nutrients. 2015;7(11):9453-74.
https://doi.org/10.3390/nu7115475
Fernyhough ME, Okine E, Hausman G, Vierck JL, Dodson MV. PPARγ and GLUT-4 expression as developmental regulators/markers for preadipocyte differentiation into an adipocyte. Domest Anim Endocrinol. 2007;33(4):367-78.
https://doi.org/10.1016/j.domaniend.2007.05.001
Lee HJ, Jang M, Kim H, Kwak W, Park WC, Hwang JY, Lee CK, Jang GW, Park MN, Kim HC, Jeong JY, Seo KS, Kim H, Cho S, Lee BY. Comparative transcriptome analysis of adipose tissues reveals that ECM-receptor interaction is involved in the depot-specific adipogenesis in cattle. PLoS One. 2013;8(6):e66267.
https://doi.org/10.1371/journal.pone.0066267
Reddy JK, Hashimoto T. Peroxisomal β-oxidation and peroxisome proliferator-activated receptor α: an adaptive metabolic system. Annu Rev Nutr. 2001;21:193-230.
https://doi.org/10.1146/annurev.nutr.21.1.193
Kyoung SK, Min JJ, Sungsoon F, Seul GY, Il YK, Je KS, Hyung-In Y, Dae HH. Anti-obesity effect of taurine through inhibition of adipogenesis in white fat tissue but not in brown fat tissue in a high-fat diet-induced obese mouse model. Amino Acids. 2019;51(2):245-54.
https://doi.org/10.1007/s00726-018-2659-7
Chiang JYL, Ferrell JM. Up to date on cholesterol 7 alpha-hydroxylase (CYP7A1) in bile acid synthesis. Liver Res. 2020;4(2):47-63.
https://doi.org/10.1016/j.livres.2020.05.001
Russell DW. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem. 2003;72:137-74.
https://doi.org/10.1146/annurev.biochem.72.121801.161712
Tillander V, Alexson SHE, Cohen DE. Deactivating fatty acids: acyl-CoA thioesterase-mediated control of lipid metabolism. Trends Endocrinol Metab. 2017;28(7):473-84.
https://doi.org/10.1016/j.tem.2017.03.001
Hunt MC, Siponen MI, Alexson SEH. The emerging role of acyl-CoA thioesterases and acyltransferases in regulating peroxisomal lipid metabolism. Biochim Biophys Acta. 2012;1822(9):1397-410.
https://doi.org/10.1016/j.bbadis.2012.03.009
Schmitz W, Fingerhut R, Conzelmann E. Purification and properties of an α-methylacyl-CoA racemase from rat liver. Eur J Biochem. 1994;222(2):313-23.
https://doi.org/10.1111/j.1432-1033.1994.tb18870.x
Zong L, Xing J, Liu S, Liu Z, Song F. Cell metabolomics reveals the neurotoxicity mechanism of cadmium in PC12 cells. Ecotoxicol Environ Saf. 2018;147:26-33.
https://doi.org/10.1016/j.ecoenv.2017.08.028
Zufferey R, Pirani K, Cheung-See-Kit M LeeS, Williams TA, Chen DG, Hossain MF. The Trypanosoma brucei dihydroxyacetonephosphate acyltransferase TbDAT is dispensable for normal growth but important for synthesis of ether glycerophospholipids. PLoS One. 2017;12(7):e0181432.
https://doi.org/10.1371/journal.pone.0181432
Shulga YV, Topham MK, Epand RM. Regulation and functions of diacylglycerol kinases. Chem Rev. 2011;111(10):6186-208.
https://doi.org/10.1021/cr1004106
Eichmann TO, Lass A. DAG tales: the multiple faces of diacylglycerol-stereochemistry, metabolism, and signaling. Cell Mol Life Sci. 2015;72(20):3931-52.
https://doi.org/10.1007/s00018-015-1982-3
Mérida I, Torres-Ayuso P, Ávila-Flores A, Arranz-Nicolás J, Andrada E, Tello-Lafoz M, Liébana R, Arcos R. Diacylglycerol kinases in cancer. Adv Biol Regul. 2017;63:22-31.
https://doi.org/10.1016/j.jbior.2016.09.005
Ipsen DH, Lykkesfeldt J, Tveden-Nyborg P. Molecular mechanisms of hepatic lipid accumulation in non-alcoholic fatty liver disease. Cell Mol Life Sci. 2018;75(18):3313-27.
https://doi.org/10.1007/s00018-018-2860-6
Musso G, Gambino R, Cassader M. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Prog Lipid Res. 2009;48(1):1-26.
https://doi.org/10.1016/j.plipres.2008.08.001
Zhang JJ, Zhao JL, Zheng XJ, Cai K, Mao QW, Xia HB. Establishment of a novel hepatic steatosis cell model by Cas9/sgRNA-mediated DGKθ gene knockout. Mol Med Rep. 2018;17(2):2169-76.
https://doi.org/10.3892/mmr.2017.8140
Garcia D, Shaw RJ. AMPK: Mechanisms of cellular energy sensing and restoration of metabolic balance. Mol Cell. 2017;66(6):789-800.
https://doi.org/10.1016/j.molcel.2017.05.032
Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem. 2005;280(32):29060-6.
https://doi.org/10.1074/jbc.M503824200
Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, Muehlbauer MJ, Witters LA, Kemp BE, Means AR. Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metabol. 2008;7(5):377-88.
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