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Dietary taurine stimulates the hepatic biosynthesis of both bile acids and cholesterol in the marine teleost, tiger puffer (Takifugu rubripes)

  • Houguo Xu (a1) (a2), Qinggong Zhang (a1), Shin-Kwon Kim (a3), Zhangbin Liao (a1), Yuliang Wei (a1) (a2), Bo Sun (a1), Linlin Jia (a1), Shuyan Chi (a4) and Mengqing Liang (a1) (a2)...


Taurine (TAU) plays important roles in the metabolism of bile acids, cholesterol and lipids. However, little relevant information has been available in fish where TAU has been identified as a conditionally essential nutrient. The present study aimed to investigate the effects of dietary TAU on the metabolism of bile acids, cholesterol and lipids in tiger puffer, which is both an important aquaculture species and a good research model, having a unique lipid storage pattern. An 8-week feeding trial was conducted in a flow-through seawater system. Three experimental diets differed only in TAU level, that is, 1·7, 8·2 and 14·0 mg/kg. TAU supplementation increased the total bile acid content in liver but decreased the content in serum. TAU supplementation also increased the contents of total cholesterol and HDL-cholesterol in both liver and serum. The hepatic bile acid profile mainly includes taurocholic acid (94·48 %), taurochenodeoxycholic acid (4·17 %) and taurodeoxycholic acid (1·35 %), and the contents of all these conjugated bile acids were increased by dietary TAU. The hepatic lipidomics analysis showed that TAU tended to decrease the abundance of individual phospholipids and increase those of some individual TAG and ceramides. The hepatic mRNA expression study showed that TAU stimulated the biosynthesis of both bile acids and cholesterol, possibly via regulation of farnesoid X receptor and HDL metabolism. TAU also stimulated the hepatic expression of lipogenic genes. In conclusion, dietary TAU stimulated the hepatic biosynthesis of both bile acids and cholesterol and tended to regulate lipid metabolism in multiple ways.


Corresponding author

*Corresponding author: Mengqing Liang, fax +86-532-85822914, email liangmq@ysfri.accn


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1.Chen, W, Guo, JX & Chang, P (2012) The effect of taurine on cholesterol metabolism. Mol Nutr Food Res 56, 681690.
2.Militante, JD & Lombardini, JB (2004) Dietary taurine supplementation, hypolipidemic and antiatherogenic effects. Nutr Res 24, 787801.
3.Kishida, T, Miyazato, S, Ogawa, H, et al. (2003) Taurine prevents hypercholesterolemia in ovariectomized rats fed corn oil but not in those fed coconut oil. J Nutr 133, 26162621.
4.Ebihara, K, Miyazato, S, Ogawa, H & Kishida, T (2006) Taurine increases cholesterol 7α-hydroxylase activity and fecal bile acids excretion but does not reduce the plasma cholesterol concentration in ovariectomized rats fed with coconut oil. Nutr Res 26, 167172.
5.Salze, GP & Davis, DA (2015) Taurine: a critical nutrient for future fish feeds. Aquaculture 437, 215229.
6.National Research Council (2011) Nutrient Requirements of Fish. Washington, DC: National Academies Press.
7.Kim, S-K, Matsunari, H, Takeuchi, T, et al. (2007) Effect of different dietary taurine levels on the conjugated bile acid composition and growth performance of juvenile and fingerling Japanese flounder Paralichthys olivaceus. Aquaculture 273, 595601.
8.Takagi, S, Murata, H, Goto, T, et al. (2011) Role of taurine deficiency in inducing green liver symptom and effect of dietary taurine supplementation in improving growth in juvenile red sea bream Pagrus major fed non-fishmeal diets based on soy protein concentrate. Fish Sci 77, 235244.
9.Yun, B, Ai, Q, Mai, K, et al. (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 324–325, 8591.
10.Han, Y, Koshio, S, Jiang, Z, et al. (2014) Interactive effects of dietary taurine and glutamine on growth performance, blood parameters and oxidative status of Japanese flounder Paralichthys olivaceus. Aquaculture 434, 348354.
11.Koven, W, Peduel, A, Gada, M, et al. (2016) Taurine improves the performance of white grouper juveniles (Epinephelus aeneus) fed a reduced fish meal diet. Aquaculture 460, 814.
12.Li, M, Lai, H, Li, Q, et al. (2016) Effects of dietary taurine on growth, immunity and hyperammonemia in juvenile yellow catfish Pelteobagrus fulvidraco fed all-plant protein diets. Aquaculture 450, 349355.
13.Satriyo, TB, Galaviz, MA, Salze, G, et al. (2017) Assessment of dietary taurine essentiality on the physiological state of juvenile, Totoaba macdonaldi. Aquac Res 48, 56775689.
14.Magalhães, R, Martins, N, Martins, S, et al. (2019) Is dietary taurine required for white seabream (Diplodus sargus) juveniles? Aquaculture 502, 296302.
15.Nishimura, N, Umeda, C, Oda, H, et al. (2003) The effect of taurine on the cholesterol metabolism in rats fed diets supplemented with cholestyramine or high amounts of bile acid. J Nutr Sci Vitaminol 49, 2126.
16.Lam, NV, Chen, W, Suruga, K, et al. (2006) Enhancing effect of taurine on CYP7A1 mRNA expression in Hep G2 cells. Amino Acids 30, 4348.
17.Yang, SF, Tzang, BS, Yang, KT, et al. (2010) Taurine alleviates dyslipidemia and liver damage induced by a high-fat/cholesterol-dietary habit. Food Chem 120, 156162.
18.Murakami, S, Fujita, M, Nakamura, M, et al. (2016) Taurine ameliorates cholesterol metabolism by stimulating bile acid production in high-cholesterol-fed rats. Clin Exp Pharmacol Physiol 43, 372378.
19.Parks, DJ, Blanchard, SG, Bledsoe, RK, et al. (1999) Bile acids: natural ligands for an orphan nuclear receptor. Science 284, 13651368.
20.Murakami, S, Kondo, Y, Toda, Y, et al. (2002) Effect of taurine on cholesterol metabolism in hamsters: up-regulation of LDL receptor by taurine. Life Sci 70, 23552366.
21.Wang, Y, Mei, X, Yuan, J, et al. (2016) Taurine zinc solid dispersions enhance bile-incubated L02 cell viability and improve liver function by inhibiting ERK2 and JNK phosphorylation during cholestasis. Toxicology 366–367, 1019.
22.Guo, J, Gao, Y, Cao, X, et al. (2017) Cholesterol-lowing effect of taurine in HepG2 cell. Lipids Health Dis 16, 56.
23.Fernandes, JMO, Mackenzie, MG, Elgar, G, et al. (2005) A genomic approach to reveal novel genes associated with myotube formation in the model teleost, Takifugu rubripes. Physiol Genomics 22, 327338.
24.Kai, W, Kikuchi, K, Fujita, M, et al. (2005) A genetic linkage map for the tiger pufferfish Takifugu rubripes. Genetics 171, 227238.
25.Imai, S, Sasaki, T, Shimizu, A, et al. (2007) The genome size evolution of medaka (Oryzias latipes) and fugu (Takifugu rubripes). Genes Genet Syst 82, 135144.
26.Wongwarangkana, C, Fujimori, KE, Akiba, M, et al. (2015) Deep sequencing, profiling and detailed annotation of microRNAs in Takifugu rubripes. BMC Genomics 16, 457.
27.Kaneko, G, Yamada, T, Han, Y, et al. (2013) Differences in lipid distribution and expression of peroxisome proliferator-activated receptor gamma and lipoprotein lipase genes in torafugu and red seabream. Gen Comp Endocrinol 184, 5160.
28.Xu, H, Mu, Y, Zhang, Y, et al. (2016) Graded levels of fish protein hydrolysate in high plant diets for turbot (Scophthalmus maximus): effects on growth performance and lipid accumulation. Aquaculture 454, 140147.
29.Folch, J, Lees, M & Sloane Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497509.
30.Xu, H, Cao, L, Wei, Y, et al. (2018) Lipid contents in farmed fish are influenced by dietary DHA/EPA ratio: a study with the marine flatfish, tongue sole (Cynoglossus semilaevis). Aquaculture 485, 183190.
31.Tu, J, Yin, Y, Xu, M, et al. (2018) Absolute quantitative lipidomics reveals lipidome-wide alterations in aging brain. Metabolomics 14, 5.
32.Han, J, Liu, Y, Wang, R, et al. (2015) Metabolic profiling of bile acids in human and mouse blood by LC-MS/MS in combination with phospholipid-depletion solid-phase extraction. Anal Chem 87, 11271136.
33.Xu, H, Dong, X, Ai, Q, Mai, K, et al. (2014) Regulation of tissue LC-PUFA contents, Δ6 fatty acyl desaturase (FADS2) gene expression and the methylation of the putative FADS2 gene promoter by different dietary fatty acid profiles in Japanese seabass (Lateolabrax japonicus). PLOS ONE 9, e87726.
34.Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.
35.Dunn, WB, Broadhurst, D, Begley, P, et al. (2011) Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 6, 10601083.
36.Chiang, JYL (1998) Regulation of bile acid synthesis: pathways, nuclear receptors, and mechanisms. Front Biosci 3, 176193.
37.Yu, L, Hammer, RE, Li-Hawkins, J, et al. (2002) Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc Natl Acad Sci USA 99, 1623716242.
38.Wang, J, Mitsche, MA, Lütjohann, D, et al. (2015) Relative roles of ABCG5/ABCG8 in liver and intestine. J Lipid Res 56, 319330.
39.Hofmann, AF, Hagey, LR & Krasowski, MD (2010) Bile salts of vertebrates, structural variation and possible evolutionary significance. J Lipid Res 51, 226246.
40.Dawson, PA (2018) Bile formation and the enterohepatic circulation. In Hysiology of the Gastrointestinal Tract, 6th ed., pp. 931956 [Said, HM, editor]. Cambridge MA: Academic Press.
41.Chen, W, Nishimura, N, Oda, H, et al. (2003) Effect of taurine on cholesterol degradation and bile acid pool in rats fed a high-cholesterol diet. Adv Exp Med Biol 526, 261267.
42.Lam, NV, Chen, W, Suruga, K, et al. (2006) Effects of taurine on mRNA levels of nuclear receptors and factors involved in cholesterol and bile acid homeostasis in mice. Adv Exp Med Biol 583, 193202.
43.Nishimura, N, Yamamoto, T & Ota, T (2009) Taurine feeding inhibits bile acid absorption from the ileum in rats fed a high cholesterol and high fat diet. Adv Exp Med Biol 643, 285291.
44.Anderson, JW & Bush, HM (2011) Soy protein effects on serum lipoproteins: a quality assessment and meta-analysis of randomized, controlled studies. J Am Coll Nutr 30, 7991.
45.Nguyen, HP, Khaoian, P, Fukada, H, et al. (2011) Effects of different soybean proteins on lipid digestion and growth of yellowtail Seriola quinqueradiata. Fish Sci 77, 357365.
46.El Khoury, D & Anderson, GH (2013) Recent advances in dietary proteins and lipid metabolism. Curr Opin Lipidol 24, 207213.
47.Kortner, TM, Gu, J, Krogdahl, A, et al. (2013) Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.). Br J Nutr 109, 593604.
48.Murashita, K, Akimoto, A, Iwashita, Y, et al. (2013) Effects of biotechnologically processed soybean meals in a nonfishmeal diet on growth performance, bile acid status, andmorphological condition of the distal intestine and liver of rainbow trout Oncorhynchus mykiss. Fish Sci 79, 447457.
49.Rueda-López, S, Lazo, JP, Reyes, GC, et al. (2011) Effect of dietary protein and energy levels on growth, survival and body composition of juvenile Totoaba macdonaldi. Aquaculture 319, 385390.
50.Bañuelos-Vargas, I, López, LM, Pérez-Jiménez, A, et al. (2014) Effect of fishmeal replacement by soy protein concentrate with taurine supplementation on hepatic intermediary metabolism and antioxidant status of totoaba juveniles (Totoaba macdonaldi). Comp Biochem Physiol 170B, 1825.
51.Fuentes-Quesada, JP, Viana, MT, Rombenso, AN, et al. (2018) Enteritis induction by soybean meal in, Totoaba macdonaldi, diets: effects on growth performance, digestive capacity, immune response and distal intestine integrity. Aquaculture 495, 7889.
52.Barreto-Curiel, F, Focken, U, D’Abramo, LR, et al. (2019) Assessment of amino acid requirements for Totoaba macdonaldi at different levels of protein using stable isotopes and a non-digestible protein source as a filler. Aquaculture 503, 550561.
53.Mochizuki, H, Oda, H & Yokogoshi, H (2001) Dietary taurine potentiates polychlorinated biphenyl-induced hypercholesterolemia in rats. J Nutr Biochem 12, 109115.
54.Nishimura, N, Umeda, C, Oda, H, et al. (2002) The effect of taurine on plasma cholesterol concentration in genetic type 2 diabetic GK rats. J Nutr Sci Vitaminol 48, 483490.
55.Yokogoshi, H, Mochizuki, H, Nanami, K, et al. (1999) Dietary taurine enhances cholesterol degradation and reduces serum and liver cholesterol concentrations in rats fed a high-cholesterol diet. J Nutr 129, 17051712.
56.Murakami, S, Kondo, Y & Nagate, T (2000) Effects of long-term treatment with taurine in mice fed a high-fat diet: improvement in cholesterol metabolism and vascular lipid accumulation by taurine. Adv Exp Med Biol 483, 177186.
57.Chen, W, Suruga, K, Nishimura, N, et al. (2005) Comparative regulation of major enzymes in bile acids biosynthesis pathways by cholesterol, cholic acid and taurine in mice and rats. Life Sci 77, 746757.
58.Chapman, MJ (1986) Comparative analysis of mammalian plasma lipoproteins. Methods Enzymol 128, 70143.
59.Clay, MA, Pyle, DH, Rye, KA, et al. (2000) Formation of spherical, reconstituted high density lipoproteins containing both apolipoproteins A-I and A-II is mediated by lecithin:cholesterol acyltransferase. J Biol Chem 275, 90199025.
60.Kosek, AB, Durbin, D & Jonas, A (1999) Binding affinity and reactivity of lecithin cholesterol acyltransferase with native lipoproteins. Biochem Biophys Res Commun 258, 548551.
61.Hirsch-Reinshagen, V, Donkin, J, Stukas, S, et al. (2009) LCAT synthesized by primary astrocytes esterifies cholesterol on glia-derived lipoproteins. J Lipid Res 50, 885893.
62.Walsh, MT, Iqbal, J, Josekutty, J, et al. (2015) Novel abetalipoproteinemia missense mutation highlights the importance of the N-terminal β-barrel in microsomal triglyceride transfer protein function. Circ Cardiovasc Genet 8, 677687.
63.Chang, YY, Chou, CH, Chiu, CH, et al. (2011) Preventive effects of taurine on development of hepatic steatosis induced by a high-fat/cholesterol dietary habit. J Agric Food Chem 59, 450457.
64.Murakami, S (2015) Role of taurine in the pathogenesis of obesity. Mol Nutr Food Res 59 13531363.
65.Chen, W, Matuda, K, Nishimura, N, et al. (2004) The effect of taurine on cholesterol degradation in mice fed a high-cholesterol diet. Life Sci 74, 18891898.
66.Chen, W, Guo, J, Zhang, Y, et al. (2016) The beneficial effects of taurine in preventing metabolic syndrome. Food Funct 7, 18491863.
67.Espe, M, Ruohonen, K & El-Mowafi, A (2012) Effect of taurine supplementation on the metabolism and body lipid-to-protein ratio in juvenile Atlantic salmon (Salmo salar). Aquac Res 43, 349360.
68.Lunger, AN, McLean, E, Gaylord, TG, et al. (2007) Taurine supplementation to alternative dietary proteins used in fish meal replacement enhances growth of juvenile cobia (Rachycentron canadum). Aquaculture 271, 401410.
69.Qi, G, Ai, Q, Mai, K, et al. (2012) Effects of dietary taurine supplementation to a casein-based diet on growth performance and taurine distribution in two sizes of juvenile turbot (Scophthalmus maximus L.). Aquaculture 358–359, 122128.
70.Salze, GP, Spangler, E, Cobine, PA, et al. (2016) Investigation of biomarkers of early taurine deficiency in Florida pompano Trachinotus carolinus. Aquaculture 451, 254265.
71.Espe, M, Ruohonen, K & El-Mowafi, A (2012) Hydrolysed fish protein concentrate (FPC) reduces viscera mass in Atlantic salmon (Salmo salar) fed plant-protein-based diets. Aquacult Nutr 18, 599609.
72.Johnson, RB, Kim, SK, Watson, AM, et al. (2015) Effects of dietary taurine supplementation on growth, feed efficiency, and nutrient composition of juvenile sablefish (Anoplopoma fimbria) fed plant based feeds. Aquaculture 445, 7985.
73.Huxtable, RJ (1992) Physiological actions of taurine. Physiol Rev 72, 101163.
74.Bouckenooghe, T, Remacle, C & Reusens, B (2006) Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care 9, 728733.
75.Richard, N, Colen, R & Aragão, C (2017) Supplementing taurine to plant-based diets improves lipid digestive capacity and amino acid retention of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 468, 94101.
76.Puigserver, P, Wu, Z, Park, CW, et al. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829839.
77.Fukuda, N, Yoshitama, A, Sugita, S, et al. (2011) Dietary taurine reduces hepatic secretion of cholesteryl ester and enhances fatty acid oxidation in rats fed a high-cholesterol diet. J Nutr Sci Vitaminol 57, 144149.
78.Pasantes-Morales, H, Chatagner, F & Mandel, P (1980) Synthesis of taurine in rat liver and brain in vivo. Neurochem Res 5, 441451.
79.Kuriyama, K (1980) Taurine as a neuromodulator. Fed Proc 39, 26802684.
80.Hoang, MH, Jia, Y, Jun, HJ, et al. (2012) Taurine is a liver X receptor-α ligand and activates transcription of key genes in the reverse cholesterol transport without inducing hepatic lipogenesis. Mol Nutr Food Res 56, 900911.
81.Lehmann, JM, Kliewer, SA, Moore, LB, et al. (1997) Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem 272, 31373140.
82.Stroup, D, Crestani, M & Chiang, JYL (1997) Identification of a bile acid response element in the cholesterol 7 alpha-hydroxylase gene CYP7A. Am J Physiol 273, G508G517.
83.Peet, DJ, Truly, SD, Ma, W, et al. (1998) Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell 93, 693704.
84.Chiang, JYL, Kimmel, R & Stroup, D (2001) Regulation of cholesterol 7alpha-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRalpha). Gene 262, 257265.
85.Miyazaki, T, Honda, A & Matsuzaki, Y (2014) Regulation of taurine conjugation and biosynthesis by bile acids through farnesoid X receptor activation. Hepatol Res 44, E1E2.
86.Park, S, Kim, H & Kim, S-J (2001) Stimulation of ERK2 by taurine with enhanced alkaline phosphatase activity and collagen synthesis in osteoblast-like UMR-106 cells. Biochem Pharmacol 62, 11071111.
87.Yuan, LQ, Lu, Y, Luo, XH, et al. (2007) Taurine promotes connective tissue growth factor (CTGF) expression in osteoblasts through the ERK signal pathway. Amino Acids 32, 425430.


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Dietary taurine stimulates the hepatic biosynthesis of both bile acids and cholesterol in the marine teleost, tiger puffer (Takifugu rubripes)

  • Houguo Xu (a1) (a2), Qinggong Zhang (a1), Shin-Kwon Kim (a3), Zhangbin Liao (a1), Yuliang Wei (a1) (a2), Bo Sun (a1), Linlin Jia (a1), Shuyan Chi (a4) and Mengqing Liang (a1) (a2)...


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