The Protective Effect of Glycyrrhetinic Acid on Carbon Tetrachloride-Induced Chronic Liver Fibrosis in Mice via Upregulation of Nrf2

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Chen, Shaoru ^a   Zou, Liyi ^a   Li, Li ^a   Wu, Tie ^a  

^a GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; AMINE OXIDASE (FLAVIN CONTAINING); ASCORBIC ACID; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; CATALASE; GLUTATHIONE PEROXIDASE 2; GLYCYRRHETINIC ACID; MESSENGER RNA; SILYMARIN; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD SAMPLING; CELL INFILTRATION; CHRONIC LIVER DISEASE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; HISTOPATHOLOGY; INFLAMMATORY CELL; LIPID PEROXIDATION; LIVER FIBROSIS; LIVER MICROSOME; LIVER NODULE; LIVER PROTECTION; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCAVENGING SYSTEM; SIGNAL TRANSDUCTION; SUPERNATANT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BIPHENYL COMPOUNDS; CHRONIC DISEASE; CYTOPROTECTION; FERROUS COMPOUNDS; FLUOROCARBONS; GLYCYRRHETINIC ACID; LIPID PEROXIDATION; LIVER; LIVER CIRRHOSIS; MALE; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PICRATES; RNA, MESSENGER; UP-REGULATION;

MUS;

EID: 84872288510     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053662     Document Type: Article

References (85)

1. Kim HK, Li L, Lee HS, Park MO, Bilehal D, et al. (2009) Protective effects of Chlorella vulgaris Extract on carbon tetrachloride-induced acute liver injury in mice. Food Sci Biotechnol 18: 1186-1192.
2. Guyton AC, Hall JE (2006) The liver as an organ. In: Guyton AC, Hall JE editors. Textbook of Medical Physiology. 11th ed. Philadelphia: Saunders Elsevier. 859-864.
3. Friedman SL (2003) Hepatic fibrosis. In: Schiff ER, Sorrell MF, Maddrey WC editors. Schiff's Diseases of the Liver. 9th ed. Philadelphia: Lippinocott Williams & Wilkins. 409-427.
4. Poli G, (2000) Pathogenesis of liverfibrosis: role of oxidative stress. Mol Aspects Med 21: 49-98.
5. Ivanov AV, Smirnova OA, Ivanova ON, Masalova OV, Kochetkov SN, et al. (2011) Hepatitis C Virus Proteins Activate NRF2/ARE Pathway by Distinct ROS Dependent and Independent Mechanisms in HUH7 Cells. PLoS ONE 6(9): e24957 doi:10.1371/journal.pone.0024957.
6. Zhu H, Jia ZQ, Hara M, Li YR, (2012) Oxidative stress and redox signaling mechanisms of alcoholic liver disease: Updated experimental and clinical evidence. J Digest Dis 13: 133-142.
7. Sikorska K, Romanowski T, Stalke P, Swieszewska EI, Bielawski KP, (2011) Iron overload and HFE gene mutations in Polish patients with liver cirrhosis. Hepatobiliary Pancreat Dis Int 10: 270-275.
8. Mizrahi M, Lalazar G, Horwich Y, Adar T, Safadi R, (2008) Benign recurrent intrahepatic cholestasis type- II- a rare cause of direct hyperbilirubinemia exacerbations with hepatic fibrosis. Harefuah 147: 381-383.
9. He SX, Luo JY, Wang YP, Wang YL, Fu H, et al. (2006) Effects of extract from Ginkgo biloba on carbon tetrachloride- induced liver injury in rats. World J Gastroentero 12: 3924-3928.
10. Yang YS, Anh TH, Lee JC, Moon CJ, Kim SH, et al. (2008) Protective effects of Pycnogenol on carbon tetrachloride- induced hepatotoxicity in Sprague-Dawley rats. Food Chem Toxicol 46: 380-387.
11. Zhu W, Fung PCW, (2000) The roles played by crucial free radicals like lipid free radicals, nitric oxide, and enzymes NOS and NADPH in CCl4-induced acute liver injury of mice. Free Radical Bio Med 29: 870-880.
12. Copple IM, Goldring CE, Kitteringham NR, Park BK, (2008) The Nrf2-Keapl defence pathway: Role in protection against drug- induced toxicity. Toxicology 246: 24-33.
13. Wang YP, Cheng ML, Zhang BF, Mu M, Wu J, (2010) Effects of blueberry on hepatic fibrosis and transcription factor Nrf2 in rats. WJG 16 (21): 2657-2663.
14. Tanigawa S, Fu JM, Hou DX, (2007) Action of Nrf2 and Keapl in ARE-mediated NQO1 expression by quercetin. Free Radic Biol Med 42: 1690-1703.
15. Farombi EO, Shrotriva S, Na HK, Kim SH, Surh YJ, (2008) Curcumin attenuates dimethylnitrosamine- induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food Chem Toxicol 46: 1279-1287.
16. Hong Y, Yan W, Chen S, Sun C, Zhang J, (2010) The role of Nrf2 signaling in the regulation of antioxidants and detoxifying enzymes after traumatic brain injury in rats and mice. Acta Pharmacol Sin 31: 1421-1430.
17. Jiang T, Huang Zh P, Chan JY, Zhang DD, (2009) Nrf2 protects against As(III)-induced damage in mouse liver and bladder. Toxicol Appl Pharmacol 240: 8-14.
18. Xu W, Hellerbrand C, Köhler UA, Bugnon P, Kan YW, et al. (2008) The Nrf2 transcription factor protects from toxin-induced liver injury and fibrosis. Lab Invest 88: 1068-1078.
19. Jin M, Wu H, (2009) Advancement on Pharmacological Action of Glycyrrhetinic Acid. Medical Recapitulate 15: 1712-1715.
20. Kobashi K, Nanba T, Hattori Y (1984) Preparation of 3-epi-glycyrrhetinic acid [P]. JP: 5914799.
21. Chen J, Pang JL, Qin YM, Liang NC, (2011) Effects of 18β-glycyrrhetinic acid on the proliferation, adhesion and invasion in HO-8910PM cells. ShanDong Med J 51: 12-14.
22. Gong XL, Luo Y, Tang DC, Sun XF, (2008) Research progress in glycyrrhetic acid and its derivatives. Strait Pharmaceutical J 20: 4-7.
23. Luo Y, Zhu ML, Sun XF, Liang ZQ, (2008) Preparation of water-soluble sodium salt of glycyrrhetinic acid and 11-deoxyglycyrrhetinic acid and research on anti-inflammatory effect. Practical Pharmacy And Clinical Remedies 11: 182-184.
24. Van Rossum TG, Vulto AG, de Man RA, Brouwer JT, Schalm SW, (1998) Review article: glycyrrhizin as a potential treatment for chronic hepatitis C. Aliment-Pharmacol-Ther. 12: 199-205.
25. Kan ZM, Cai Y, (2007) The Protective Effect of DG on the Damage of Liver Induced by Cadmium in Mice. TianJin Medical J 35: 361-362.
26. Wang JY, Zhang QS, Guo JS, Hu MY, (2001) Effects of glycyrrhetinic acid on collagen metabolism of hepatic stellate cells at different stages of liver fibrosis in rats. World J Gastroentero 7: 115-119.
27. Choi HK, Pokharel YR, Lim SC, Han HK, Ryu CS, et al. (2009) Inhibition of liver fibrosis by solubilized coenzyme Q10: Role of Nrf2 activation in inhibiting transforming growth factor-ß1 expression. Toxicol Appl Pharm 240: 377-384.
28. Xu W, Hellerbrand C, Kohler UA, Bugnon P, Kan YW, et al. (2008) The Nrf2 transcription factor protects from toxin-onduced liver injury and fibrosis. Lab Invest 88: 1068-1078.
29. Thompson K, Maltby J, Fallowfield J, Mcaulay M, Millward-Sadler H, et al. (1998) Interleukin-10 Expression and Function in Experimental Murine Liver Inflammation and Fibrosis. Hepatology 28: 1597-1606.
30. Kim HJ, Yu MH, Lee IS, (2008) Inhibitory effects of methanol extract of plum (Prunus salicina L., cv. 'Soldam') fruits against benzo (a{ogonek}) pyrene-induced toxicity in mice. Food Chem Toxicol 46: 3407-3413.
31. Tipton KF, Boyce S, O'Sullivan J, Davey GP, Healy J, (2004) Monoamine oxidases: certainties and uncertainties. Curr Med Chem 11: 1965-1982.
32. Edmondson DE, Mattevi A, Binda C, Li M, Hubálek F, (2004) Structure and mechanism of monoamine oxidase. Curr Med Chem 11: 1983-1993.
33. Hare MLC, (1928) Tyramine oxidase: A new enzyme system in liver. Biochem J 22: 968-979.
34. Slotkin TA, (1999) Mary Bernheim and the discovery of monoamine oxidase. Brain Res Bull 50: 373-373.
35. Li L, Li W, Kim YH, Lee YW, (2011) Chlorella vulgaris extract ameliorates carbon tetrachloride- induced acute hepatic injury in mice. Exp Toxicol Pathol 4: 1-7.
36. Li CY, Xu SY, Wang Z, (2006) Measuring the Antiradical Efficiency of Proanthocyanidin From Grape Seed by the DPPH •Assay. Journal of Food Science and Biotechnology 25: 1673-1689.
37. Molyneux P, (2004) The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J Sci Technol 26: 211-218.
38. Pierce RA, Glaug MR, Greco RS, Mackenzie JW, Boyd CD, et al. (1987) Increased procollagen mRNA levels in carbon tetrachloride-induced liver fibrosis in rats. J Biol Chem 262: 1652-1658.
39. Brattin WJ, Glende EA Jr, Recknagel RO, (1985) Pathological mechanisms in carbon tetrachloride hepatotoxicity. J Free Radic Biol Med 1: 27-38.
40. Recknagel RO, Glende EA Jr, Dolak JA, Waller RL, (1989) Mechanisms of carbon tetrachloride toxicity. Pharmacol Ther 43: 139-154.
41. Recknagel RO, Glende JEA, Britton RS (1991) Free radical damage and lipid peroxidation. In: Meeks RG, editor. Hepatotoxicology. Florida: CRC Press. 401-436.
42. Williams AT, Burk RF, (1990) Carbon tetrachloride hepatotoxicity: an example of free radical-mediated injury. Semin Liver Dis 10: 279-284.
43. Jia N, Liu X, Wen J, Qian L, Qian X, et al. (2007) A proteomic method for analysis of CYP450s protein expression changes in carbon tetrachloride induced male rat liver microsomes. Toxicology 237: 1-11.
44. Brautbar N, Williams J, (2002) Industrial solvents and liver toxicity: risk assessment, risk factors and mechanisms. Int J Hyg Environ Health 205: 479-491.
45. Brent JA, Rumack BH, (1993) Role of free radicals in toxic hepatic injury. II. Are free radicals the cause of toxin-Induced liver injury? J Toxicol Clin Toxicol 31: 173-196.
46. Buettner GR, (1993) The Peaking order of Free radicals and Antioxidants: Lipid Peroxidation, a{ogonek}- Tocopherol, and Asorbate. Arch Biochem Biophys. 300: 535-543.
47. Cederbaum AI, Lu Y, Wu D, (2009) Role of oxidative stress in alcohol-induced liver injury. Arch Toxicol 83: 519-548.
48. Lai M, (2002) Hepatitis C virus proteins: direct link to hepatic oxidative stress, steatosis, carcinogenesis and more. Gastroenterology 122: 568-571.
49. Halliwell B, (2006) Oxidative stress and neurodegeneration; where are we now? J Neurochem 97: 1634-1658.
50. Aslan M, Ozben T, (2004) Reactive Oxygen and Nitrogen Species in Alzheimer's Disease. Curr Alzheimer Res 1: 111-119.
51. Bartsh H, Nair J, (2006) Chronic inflammation and oxidative stress in the genesis and perpetuation of cancer: role of lipid peroxidation, DNA damage, and repair. Lanqenbecks Arch Surq 391: 499-510.
52. Poli G, (2000) Pathogenesis of liver fibrosis: role of oxidative stress. Mol Aspects Med 21: 49-98.
53. Moro T, Shimoyama Y, Kushida M, Hong YY, Nakao S, et al. (2008) Glycyrrhizin and its metabolite inhibit Smad3-mediated type I collagen gene transcription and suppress experimental murine liver fibrosis. Life Sci 83: 531-539.
54. Zhang QS, Luk JM, Zhang J, Tian GY, (2005) Targeting glycyrrhetinic acid to hepatic stellate cells in treating rat liver fibrosis. ZhongHuaGanZangBinZaZhi 13: 664-667.
55. Ablise M, Leininger-Muller B, Wong CD, Siest G, Loppinet V, et al. (2004) Synthesis and in vitro antioxidant activity of glycyrrhetinic acid derivatives tested with the cytochrome P450/NADPH system. Chem Pharm Bull 52: 1436-1439.
56. Makino T, Ohtake N, Watanabe A, Tsuchiya N, Imamura S, et al. (2008) Down-Regulation of a Hepatic Transporter Multidrug Resistance-Associated Protein 2 Is Involved in Alteration of Pharmacokinetics of Glycyrrhizin and Its Metabolites in a Rat Model of Chronic Liver Injury. Drug Metab Dispos 36: 1438-1443.
57. Nguyen T, Nioi P, Pickett C, (2009) The Nrf2-Antioxidant Response Element Signaling Pathway and Its Activation by Oxidative Stress. Jbc 284: 13291-13295.
58. Gressner AM, Roebruck P, Tittor W, (1982) Validity of Monoamine Oxidase in Serum for Diagnosis of Liver Cirrhosis: Estimation of Predictive Values, Sensitivities and Specificities. J Clin Chem Clin Biochem 20: 509-514.
59. Ren M, Zou Jy, Gao GQ, Yang G, Chen RG, et al. (2010) Effect of bitter melon on liver fibrosis induced by carbon tetrachloride. Chinese Journal of Pathophysiology 26: 2222-2225.
60. Slater TF, (1984) Free-radical mechanisms in tissue injury. Biochem J 222: 1-15.
61. Fan J, Zeng M, Li J, (1997) Correlation between hepatic fat, lipid peroxidation and hepatic fibrosis in rats chronically fed with ethanol and/or high fat diet. Zhonghua Nei Ke Za Zhi 12: 808-811.
62. Tsukamoto H, Rippe R, Niemela O, Lin M, (1995) Roles of oxidative stress in activation of Kupffer and Ito cells in liver fibrogenesis. J Gastroen Hepatol 10: 50-53.
63. Esterbauer H, Schaur J, Zollner H, (1991) Chemistry and biochemistry of 4- hydroxynonenal malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128.
64. Cho HY, Reddy SP, Kleeberger SR, (2006) Nrf2 defends the lung from oxidative stress. Antioxid Redox Sign 8: 76-87.
65. Kang MI, Kobayashi A, Wakabayashi N, Kim SG, Yamamoto M, (2004) Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. P Natl Acad Sci USA 101: 2046-2051.
66. Mann GE, Niehueser-Saran J, Watson A, Gao L, Ishii T, et al. (2007) Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: Implications for atherosclerosis and preeclampsia. Acta Physiologica Sinica 59: 117-127.
67. Mulcahy RT, Wartman MA, Bailey HH, Gipp JJ, (1997) Contistitutive and ß-napthoflavonone-induced expression of the human gamma-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant respone element/TRE sequence. J Biol Chem 272: 7445-7454.
68. Jeong WS, Jun M, Kong AN, (2006) Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Sign 8: 99-106.
69. Farombi EO, Shrotriya S, Na HK, Kim SH, Surh YJ, (2008) Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-l. Food Chem Toxicol 46: 1279-1287.
70. Goldring CE, Kitteringham NR, Elsby R, Randle LE, Clement YN, et al. (2004) Activation of hepatic Nrf2 in vivo by acetaminophen in CD-1 mice. Hepatology 39: 1267-1276.
71. Patel R, Maru G, (2008) Polymeric black tea polyphenols induce phase II enzymes via Nrf2 in mouse liver and lungs. Free Radic Biol Med 44: 1897-1911.
72. Ju HS, Li XJ, Zhao BL, Hou JW, Han ZW, et al. (1990) Scavenging effects of sodium ferulate and 18 beta-glycyrrhetic acid on oxygen free radicals. Zhongguo Yao Li Xue Bao 11: 466-470.
73. Bardag-Gorce F, Oliva J, Lin A, Li J, French SW, et al. (2011) Proteasome Inhibitor Up Regulates Liver Antioxidative Enzymes in Rat Model of Alcoholic Liver Disease. Exp Mol Pathol 90 (1): 123-130.
74. Wu KC, Liu JJ, Klaassen CD, (2012) Nrf2 activation prevents cadmium-induced acute liver injury. Toxicol Appl Pharmacol 263: 14-20.
75. Singh B, Bhat HK, (2012) Superoxide dismutase 3 is induced by antioxidants, inhibits oxidative DNA damage and is associated with inhibition of estrogen-induced breast cancer. Carcinogenesis 33: 2601-2610.
76. Karlsson K, Marklund SL, (1988) Extracellular superoxide dismutase in the vascular systems of mammals. Biochem.J. 255: 223-228.
77. Karlsson K, Sandström J, Edlund A, Marklund SL, (1994) Turnover of extracellular-superoxide dismutase in tissues. Lab. Invest 70: 705-710.
78. Marklund SL, (1982) Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci U S A 79: 7634-7638.
79. Folz RJ, Crapo JD, (1994) Extracellular superoxide dismutase (SOD3): tissue-specific expression, genomic characterization, and computer-assisted sequence analysis of the human EC SOD gene. Genomics 22: 162-171.
80. Nanji AA, Griniuviene B, Sadrzadeh SM, Levitsky S, McCully JD, (1995) Effect of type of dietary fat and ethanol on antioxidant enzyme mRNA induction in rat liver. J Lipid Res 36: 736-744.
81. Reisman SA, Yeager RL, Yamamoto M, Klaassen CD, (2009) Increased Nrf2 activation in livers from Keap1-knockdown mice increases expression of cytoprotective genes that detoxify electrophiles more than those that detoxify reactive oxygen species. Toxicol Sci 108: 35-47.
82. Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, et al. (2003) Characterization of mammalian selenoproteomes. Science 300: 1439-1443.
83. Chu FF, Doroshow JH, Esworthy RS, (1993) Expression, characterization, and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI. J Biol Chem 268: 2571-2576.
84. Brigelius FR, (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27: 951-965.
85. Banning A, Deubel S, Kluth D, Zhou Z, Brigelius-Flohé R, (2005) The GI-GPx Gene Is a Target for Nrf2. Mol Cell Biol 25 (12): 4914-4923.