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Published in: Digestive Diseases and Sciences 3/2012

01-03-2012 | Original Article

The Effect of Taurine on Hepatic Steatosis Induced by Thioacetamide in Zebrafish (Danio rerio)

Authors: Thais Ortiz Hammes, Gabriela Lima Pedroso, Carolina Rigatti Hartmann, Thayssa Dalla Costa Escobar, Laisa Beduschi Fracasso, Darlan Pase da Rosa, Norma Possa Marroni, Marilene Porawski, Themis Reverbel da Silveira

Published in: Digestive Diseases and Sciences | Issue 3/2012

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Abstract

Background

Nonalcoholic fatty liver disease is one of the most prevalent forms of chronic liver disease in the Western world. Taurine is a conditionally essential amino acid in humans that may be a promising therapy for treating this disease.

Aim

To evaluate the effect of taurine on hepatic steatosis induced by thioacetamide in Danio rerio.

Methods

Animals were divided into four groups: control (20 μl of saline solution), taurine (1,000 mg/kg), thioacetamide (300 mg/kg), and the taurine–thioacetamide group (1,000 + 300 mg/kg). Thioacetamide was injected intraperitoneally three times a week for 2 weeks. The mRNA expression, lipoperoxidation, antioxidant enzymatic activity, and histological analyses were evaluated in the liver and the triglyceride content was assessed in the serum.

Results

Thioacetamide injection induced steatosis, as indicated by histological analyses. The lipoperoxidation showed significant lipid damage in the thioacetamide group compared to the taurine–thioacetamide group (p < 0.001). Superoxide dismutase (SOD) activity in the taurine–thioacetamide group (5.95 ± 0.40) was significantly increased compared to the thioacetamide group (4.14 ± 0.18 U SOD/mg of protein) (p < 0.001). The mRNA expression of SIRT1 (0.5-fold) and Adiponectin receptor 2 (0.39-fold) were lower in the thioacetamide group than the control (p < 0.05). TNF-α mRNA expression was 6.4-fold higher in the thioacetamide group than the control (p < 0.05). SIRT1 mRNA expression was 2.6-fold higher in the taurine–thioacetamide group than in the thioacetamide group.

Conclusions

Taurine seems to improve hepatic steatosis by reducing oxidative stress and increasing SIRT1 expression.
Literature
1.
go back to reference Roberts EA. Pediatric nonalcoholic fatty liver disease (NAFLD): a “growing” problem? J Hepatol. 2007;46:1133–1142.PubMedCrossRef Roberts EA. Pediatric nonalcoholic fatty liver disease (NAFLD): a “growing” problem? J Hepatol. 2007;46:1133–1142.PubMedCrossRef
3.
go back to reference Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–1395.PubMedCrossRef Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–1395.PubMedCrossRef
4.
go back to reference Moretto M, Kupski C, Mottin CC, et al. Hepatic steatosis in patients undergoing bariatric surgery and its relationship to body mass index and co-morbidities. Obes Surg. 2003;13:622–624.PubMedCrossRef Moretto M, Kupski C, Mottin CC, et al. Hepatic steatosis in patients undergoing bariatric surgery and its relationship to body mass index and co-morbidities. Obes Surg. 2003;13:622–624.PubMedCrossRef
5.
go back to reference Cotrim HP, Parise ER, Oliveira CP, et al. Nonalcoholic fatty liver disease in Brazil. Clinical and histological profile. Ann Hepatol. 2011;10:33–37.PubMed Cotrim HP, Parise ER, Oliveira CP, et al. Nonalcoholic fatty liver disease in Brazil. Clinical and histological profile. Ann Hepatol. 2011;10:33–37.PubMed
6.
go back to reference OH MK, Winn J, Poordad F. Review article: diagnosis and treatment of non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2008;28:503–522.PubMedCrossRef OH MK, Winn J, Poordad F. Review article: diagnosis and treatment of non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2008;28:503–522.PubMedCrossRef
7.
go back to reference Huxtable RJ. Physiological actions of taurine. Physiol Rev. 1992;72:101–163.PubMed Huxtable RJ. Physiological actions of taurine. Physiol Rev. 1992;72:101–163.PubMed
8.
go back to reference Balkan J, Dogru-Abbasoglu S, Kanbagli O, et al. Taurine has a protective effect against thioacetamide-induced liver cirrhosis by decreasing oxidative stress. Hum Exp Toxicol. 2001;20:251–254.PubMedCrossRef Balkan J, Dogru-Abbasoglu S, Kanbagli O, et al. Taurine has a protective effect against thioacetamide-induced liver cirrhosis by decreasing oxidative stress. Hum Exp Toxicol. 2001;20:251–254.PubMedCrossRef
9.
go back to reference Chen SW, Chen YX, Shi J, et al. The restorative effect of taurine on experimental nonalcoholic steatohepatitis. Dig Dis Sci. 2006;51:2225–2234.PubMedCrossRef Chen SW, Chen YX, Shi J, et al. The restorative effect of taurine on experimental nonalcoholic steatohepatitis. Dig Dis Sci. 2006;51:2225–2234.PubMedCrossRef
10.
go back to reference Lam SH, Gong Z. Modeling liver cancer using zebrafish: a comparative oncogenomics approach. Cell Cycle. 2006;5:573–577.PubMedCrossRef Lam SH, Gong Z. Modeling liver cancer using zebrafish: a comparative oncogenomics approach. Cell Cycle. 2006;5:573–577.PubMedCrossRef
11.
go back to reference Passeri MJ, Cinaroglu A, Gao C, et al. Hepatic steatosis in response to acute alcohol exposure in zebrafish requires sterol regulatory element binding protein activation. Hepatology. 2009;49:443–452.PubMedCrossRef Passeri MJ, Cinaroglu A, Gao C, et al. Hepatic steatosis in response to acute alcohol exposure in zebrafish requires sterol regulatory element binding protein activation. Hepatology. 2009;49:443–452.PubMedCrossRef
12.
go back to reference Rekha RD, Amali AA, Her GM, et al. Thioacetamide accelerates steatohepatitis, cirrhosis and HCC by expressing HCV core protein in transgenic zebrafish Danio rerio. Toxicology. 2008;243:11–22.PubMedCrossRef Rekha RD, Amali AA, Her GM, et al. Thioacetamide accelerates steatohepatitis, cirrhosis and HCC by expressing HCV core protein in transgenic zebrafish Danio rerio. Toxicology. 2008;243:11–22.PubMedCrossRef
13.
go back to reference Amali AA, Rekha RD, Lin CJ, et al. Thioacetamide induced liver damage in zebrafish embryo as a disease model for steatohepatitis. J Biomed Sci. 2006;13:225–232.PubMedCrossRef Amali AA, Rekha RD, Lin CJ, et al. Thioacetamide induced liver damage in zebrafish embryo as a disease model for steatohepatitis. J Biomed Sci. 2006;13:225–232.PubMedCrossRef
14.
go back to reference McGrath P, Li CQ. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today. 2008;13:394–401.PubMedCrossRef McGrath P, Li CQ. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today. 2008;13:394–401.PubMedCrossRef
15.
go back to reference Kinkel AD, Fernyhough ME, Helterline DL, et al. Oil red-O stains non-adipogenic cells: a precautionary note. Cytotechnology. 2004;46:49–56.PubMedCrossRef Kinkel AD, Fernyhough ME, Helterline DL, et al. Oil red-O stains non-adipogenic cells: a precautionary note. Cytotechnology. 2004;46:49–56.PubMedCrossRef
16.
go back to reference Jagadeeswaran P, Sheehan JP, Craig FE, et al. Identification and characterization of zebrafish thrombocytes. Br J Haematol. 1999;107:731–738.PubMedCrossRef Jagadeeswaran P, Sheehan JP, Craig FE, et al. Identification and characterization of zebrafish thrombocytes. Br J Haematol. 1999;107:731–738.PubMedCrossRef
18.
go back to reference Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170–3175.PubMed Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170–3175.PubMed
19.
go back to reference Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J. 1973;134:707–716.PubMed Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J. 1973;134:707–716.PubMed
20.
go back to reference Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.PubMedCrossRef Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.PubMedCrossRef
21.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[−delta delta C(T)] method. Methods. 2001;25:402–408.PubMedCrossRef Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[−delta delta C(T)] method. Methods. 2001;25:402–408.PubMedCrossRef
22.
go back to reference Lewis J, Mohanty S. Nonalcoholic fatty liver disease: a review and update. Dig Dis Sci. 2010;55:560–578.PubMedCrossRef Lewis J, Mohanty S. Nonalcoholic fatty liver disease: a review and update. Dig Dis Sci. 2010;55:560–578.PubMedCrossRef
23.
24.
25.
go back to reference Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol. 2010;5:145–171.PubMedCrossRef Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol. 2010;5:145–171.PubMedCrossRef
26.
go back to reference Chilakapati J, Shankar K, Korrapati MC, et al. Saturation toxicokinetics of thioacetamide: role in initiation of liver injury. Drug Metab Dispos. 2005;33:1877–1885.PubMed Chilakapati J, Shankar K, Korrapati MC, et al. Saturation toxicokinetics of thioacetamide: role in initiation of liver injury. Drug Metab Dispos. 2005;33:1877–1885.PubMed
27.
go back to reference Tunez I, Munoz MC, Villavicencio MA, et al. Hepato- and neurotoxicity induced by thioacetamide: protective effects of melatonin and dimethylsulfoxide. Pharmacol Res. 2005;52:223–228.PubMedCrossRef Tunez I, Munoz MC, Villavicencio MA, et al. Hepato- and neurotoxicity induced by thioacetamide: protective effects of melatonin and dimethylsulfoxide. Pharmacol Res. 2005;52:223–228.PubMedCrossRef
28.
go back to reference Dogru-Abbasoglu S, Kanbagli O, Balkan J, et al. The protective effect of taurine against thioacetamide hepatotoxicity of rats. Hum Exp Toxicol. 2001;20:23–27.PubMedCrossRef Dogru-Abbasoglu S, Kanbagli O, Balkan J, et al. The protective effect of taurine against thioacetamide hepatotoxicity of rats. Hum Exp Toxicol. 2001;20:23–27.PubMedCrossRef
30.
go back to reference Yamaguchi K, Yang L, McCall S, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology. 2007;45:1366–1374.PubMedCrossRef Yamaguchi K, Yang L, McCall S, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology. 2007;45:1366–1374.PubMedCrossRef
31.
go back to reference Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of non-alcoholic fatty liver disease. Qjm. 2010;103:71–83.PubMedCrossRef Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of non-alcoholic fatty liver disease. Qjm. 2010;103:71–83.PubMedCrossRef
32.
go back to reference Assy N, Kaita K, Mymin D, et al. Fatty infiltration of liver in hyperlipidemic patients. Dig Dis Sci. 2000;45:1929–1934.PubMedCrossRef Assy N, Kaita K, Mymin D, et al. Fatty infiltration of liver in hyperlipidemic patients. Dig Dis Sci. 2000;45:1929–1934.PubMedCrossRef
33.
go back to reference Tasci I, Mas N, Mas MR, et al. Ultrastructural changes in hepatocytes after taurine treatment in CCl4 induced liver injury. World J Gastroenterol. 2008;14:4897–4902.PubMedCrossRef Tasci I, Mas N, Mas MR, et al. Ultrastructural changes in hepatocytes after taurine treatment in CCl4 induced liver injury. World J Gastroenterol. 2008;14:4897–4902.PubMedCrossRef
34.
go back to reference Chen X, Sebastian BM, Tang H, et al. Taurine supplementation prevents ethanol-induced decrease in serum adiponectin and reduces hepatic steatosis in rats. Hepatology. 2009;49:1554–1562.PubMedCrossRef Chen X, Sebastian BM, Tang H, et al. Taurine supplementation prevents ethanol-induced decrease in serum adiponectin and reduces hepatic steatosis in rats. Hepatology. 2009;49:1554–1562.PubMedCrossRef
35.
go back to reference Schaffer SW, Azuma J, Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol. 2009;87:91–97.PubMedCrossRef Schaffer SW, Azuma J, Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol. 2009;87:91–97.PubMedCrossRef
36.
go back to reference Lakshmi Devi S, Anuradha CV. Mitochondrial damage, cytotoxicity and apoptosis in iron-potentiated alcoholic liver fibrosis: amelioration by taurine. Amino Acids. 2010;38:869–879.PubMedCrossRef Lakshmi Devi S, Anuradha CV. Mitochondrial damage, cytotoxicity and apoptosis in iron-potentiated alcoholic liver fibrosis: amelioration by taurine. Amino Acids. 2010;38:869–879.PubMedCrossRef
37.
go back to reference Rosemberg DB, da Rocha RF, Rico EP, et al. Taurine prevents enhancement of acetylcholinesterase activity induced by acute ethanol exposure and decreases the level of markers of oxidative stress in zebrafish brain. Neuroscience. 2010;171:683–692.PubMedCrossRef Rosemberg DB, da Rocha RF, Rico EP, et al. Taurine prevents enhancement of acetylcholinesterase activity induced by acute ethanol exposure and decreases the level of markers of oxidative stress in zebrafish brain. Neuroscience. 2010;171:683–692.PubMedCrossRef
38.
go back to reference Oliveira MW, Minotto JB, de Oliveira MR, et al. Scavenging and antioxidant potential of physiological taurine concentrations against different reactive oxygen/nitrogen species. Pharmacol Rep. 2010;62:185–193.PubMed Oliveira MW, Minotto JB, de Oliveira MR, et al. Scavenging and antioxidant potential of physiological taurine concentrations against different reactive oxygen/nitrogen species. Pharmacol Rep. 2010;62:185–193.PubMed
39.
go back to reference Oliveira CP, Coelho AM, Barbeiro HV, et al. Liver mitochondrial dysfunction and oxidative stress in the pathogenesis of experimental nonalcoholic fatty liver disease. Braz J Med Biol Res. 2006;39:189–194.PubMed Oliveira CP, Coelho AM, Barbeiro HV, et al. Liver mitochondrial dysfunction and oxidative stress in the pathogenesis of experimental nonalcoholic fatty liver disease. Braz J Med Biol Res. 2006;39:189–194.PubMed
40.
go back to reference Videla LA, Rodrigo R, Orellana M, et al. Oxidative stress-related parameters in the liver of non-alcoholic fatty liver disease patients. Clin Sci (Lond). 2004;106:261–268.CrossRef Videla LA, Rodrigo R, Orellana M, et al. Oxidative stress-related parameters in the liver of non-alcoholic fatty liver disease patients. Clin Sci (Lond). 2004;106:261–268.CrossRef
41.
go back to reference Yesilova Z, Yaman H, Oktenli C, et al. Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2005;100:850–855.PubMedCrossRef Yesilova Z, Yaman H, Oktenli C, et al. Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2005;100:850–855.PubMedCrossRef
42.
go back to reference Chang YY, Chou CH, Chiu CH, et al. Preventive effects of taurine on development of hepatic steatosis induced by a high-fat/cholesterol dietary habit. J Agric Food Chem. 2011;59:450–457.PubMedCrossRef Chang YY, Chou CH, Chiu CH, et al. Preventive effects of taurine on development of hepatic steatosis induced by a high-fat/cholesterol dietary habit. J Agric Food Chem. 2011;59:450–457.PubMedCrossRef
43.
go back to reference Malaguarnera M, Di Rosa M, Nicoletti F, et al. Molecular mechanisms involved in NAFLD progression. J Mol Med. 2009;87:679–695.PubMedCrossRef Malaguarnera M, Di Rosa M, Nicoletti F, et al. Molecular mechanisms involved in NAFLD progression. J Mol Med. 2009;87:679–695.PubMedCrossRef
44.
go back to reference Jou J, Choi SS, Diehl AM. Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin Liver Dis. 2008;28:370–379.PubMedCrossRef Jou J, Choi SS, Diehl AM. Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin Liver Dis. 2008;28:370–379.PubMedCrossRef
45.
go back to reference Kaser S, Moschen A, Cayon A, et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut. 2005;54:117–121.PubMedCrossRef Kaser S, Moschen A, Cayon A, et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut. 2005;54:117–121.PubMedCrossRef
46.
go back to reference Banks AS, Kon N, Knight C, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8:333–341.PubMedCrossRef Banks AS, Kon N, Knight C, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8:333–341.PubMedCrossRef
47.
go back to reference Colak Y, Ozturk O, Senates E, et al. SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease. Med Sci Monit. 2011;17:HY5–HY9.PubMed Colak Y, Ozturk O, Senates E, et al. SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease. Med Sci Monit. 2011;17:HY5–HY9.PubMed
48.
go back to reference Pereira TCB, Rico EP, Rosemberg DB, et al. Zebrafish as a model organism to evaluate drugs potentially able to modulate sirtuin expression. Zebrafish. 2011;8:9–16.PubMedCrossRef Pereira TCB, Rico EP, Rosemberg DB, et al. Zebrafish as a model organism to evaluate drugs potentially able to modulate sirtuin expression. Zebrafish. 2011;8:9–16.PubMedCrossRef
49.
go back to reference Deng XQ, Chen LL, Li NX. The expression of SIRT1 in nonalcoholic fatty liver disease induced by high-fat diet in rats. Liver Int. 2007;27:708–715.PubMedCrossRef Deng XQ, Chen LL, Li NX. The expression of SIRT1 in nonalcoholic fatty liver disease induced by high-fat diet in rats. Liver Int. 2007;27:708–715.PubMedCrossRef
50.
go back to reference dos Costa CS, Hammes TO, Rohden F, et al. SIRT1 transcription is decreased in visceral adipose tissue of morbidly obese patients with severe hepatic steatosis. Obes Surg. 2010;20:633–639.CrossRef dos Costa CS, Hammes TO, Rohden F, et al. SIRT1 transcription is decreased in visceral adipose tissue of morbidly obese patients with severe hepatic steatosis. Obes Surg. 2010;20:633–639.CrossRef
Metadata
Title
The Effect of Taurine on Hepatic Steatosis Induced by Thioacetamide in Zebrafish (Danio rerio)
Authors
Thais Ortiz Hammes
Gabriela Lima Pedroso
Carolina Rigatti Hartmann
Thayssa Dalla Costa Escobar
Laisa Beduschi Fracasso
Darlan Pase da Rosa
Norma Possa Marroni
Marilene Porawski
Themis Reverbel da Silveira
Publication date
01-03-2012
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 3/2012
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-011-1931-4

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