Effects of salvianolic acids on oxidative stress and hepatic fibrosis in rats

Toxicology and Applied Pharmacology

Volumn 242, Issue 2, 2010, Pages 155-164

  Tsai, Ming Kuei ^a   Lin, Yun Lian ^b   Huang, Yi Tsau ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL RESEARCH INSTITUTE OF CHINESE MEDICINE   (Taiwan)

Author keywords

Hepatic fibrosis; Hepatic stellate cells; Nicotinamide adenine dinucleotide phosphate (NADPH) oxidase; Oxidative stress; Platelet derived growth factor; Salvianolic acid

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA SMOOTH MUSCLE ACTIN; ASPARTATE AMINOTRANSFERASE; BENZOFURAN DERIVATIVE; COLLAGEN; DICHLOROFLUORESCEIN; HEME OXYGENASE 1; HYDROGEN PEROXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MALONALDEHYDE; PLATELET DERIVED GROWTH FACTOR; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; S ADENOSYLMETHIONINE; SALVIANOLIC ACID A; SALVIANOLIC ACID B; THIOACETAMIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BIOACCUMULATION; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; ENZYME INHIBITION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; LIVER FIBROSIS; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; STELLATE CELL; WESTERN BLOTTING;

ACTINS; ANIMALS; BENZOFURANS; BLOTTING, WESTERN; CAFFEIC ACIDS; HYDROGEN PEROXIDE; LACTATES; LIVER CIRRHOSIS; MALE; OXIDATIVE STRESS; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 71049180223     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.10.002     Document Type: Article

References (52)

1. Adachi T., Togashi H., Suzuki A., Kasai S., Ito J., Sugahara K., and Kawata S. NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells. Hepatology 41 (2005) 1272-1281
2. Aram G., Potter J.J., Liu X., Torbenson M.S., and Mezey E. Lack of inducible nitric oxide synthase leads to increased hepatic apoptosis and decreased fibrosis in mice after chronic carbon tetrachloride administration. Hepatology 47 (2008) 2051-2058
3. Aram G., Potter J.J., Liu X., Wang L., Torbenson M.S., and Mezey E. Deficiency of nicotinamide adenine dinucleotide phosphate, reduced form oxidase enhances hepatocellular injury but attenuates fibrosis after chronic carbon tetrachloride administration. Hepatology 49 (2009) 911-919
4. Banai S., Wolf Y., Golomb G., Pearle A., Waltenberger J., Fishbein I., Schneider A., Gazit A., Perez L., Huber R., Lazarovichi G., Rabinovich L., Levitzki A., and Gertz S.D. PDGF-receptor tyrosine kinase blocker AG1295 selectively attenuates smooth muscle cell growth in vitro and reduces neointimal formation after balloon angioplasty in swine. Circulation 97 (1998) 1960-1969
5. Bataller R., Schwabe R.F., Choi Y.H., Yang L., Paik Y.H., Lindquist J., Qian T., Schoonhoven R., Hagedorn C.H., Lemasters J.J., and Brenner D.A. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J. Clin. Invest. 112 (2003) 1383-1394
6. Bedard K., and Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87 (2007) 245-313
7. Chilakapati J., Korrapati M.C., Shankar K., Hill R.A., Warbritton A., Latendresse J.R., and Mehendale H.M. Role of CYP2E1 and saturation kinetics in the bioactivation of thioacetamide: effects of diet restriction and phenobarbital. Toxicol. Appl. Pharmacol. 219 (2007) 72-84
8. Chong L.W., Hsu Y.C., Chiu Y.T., Yang K.C., and Huang Y.T. Anti-fibrotic effects of thalidomide on hepatic stellate cells and dimethylnitrosamine-intoxicated rats. J. Biomed. Sci. 13 (2006) 403-418
9. Christopher A.P., and Griendling K.K. Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc. Med. 17 (2007) 48-54
10. De Bleser P.J., Xu G., Rombouts K., Rogiers V., and Geerts A. Glutathione levels discriminate between oxidative stress and transforming growth factor-beta signaling in activated rat hepatic stellate cells. J. Biol. Chem. 274 (1999) 33881-33887
11. De Minicis S., and Brenner D.A. NOX in liver fibrosis. Arch. Biochem. Biophys. 462 (2007) 266-272
12. De Minicis S., Seki E., Oesterreicher C., Schnabl B., Schwabe R.F., and Brenner D.A. Reduced nicotinamide adenine dinucleotide phosphate oxidase mediates fibrotic and inflammatory effects of leptin on hepatic stellate cells. Hepatology 48 (2008) 2016-2026
13. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
14. Eipel C., Eisold M., Schuett H., and Vollmar B. Inhibition of heme oxygenase-1 protects against tissue injury in carbon tetrachloride exposed livers. J. Surg. Res. 139 (2007) 113-120
15. Friedman S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology 134 (2008) 1655-1669
16. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88 (2008) 125-172
17. Galli A., Svegliati-Baroni G., Ceni E., Milani S., Ridolfi F., Salzano R., Tarocchi M., Grappone C., Pellegrini G., Benedetti A., Surrenti C., and Casini A. Oxidative stress stimulates proliferation and invasiveness of hepatic stellate cells via a MMP2-mediated mechanism. Hepatology 41 (2005) 1074-1084
18. Garcia-Trevijano E.R., Iraburu M.J., Fontana L., Dominguez-Rosales J.A., Auster A., Covarrubias-Pinedo A., and Rojkind M. Transforming growth factor beta1 induces the expression of alpha1(I) procollagen mRNA by a hydrogen peroxide-C/EBPbeta-dependent mechanism in rat hepatic stellate cells. Hepatology 29 (1999) 960-970
19. Gebhardt R. Oxidative stress, plant-derived antioxidants and liver fibrosis. Planta Med. 68 (2002) 289-296
20. Henderson N.C., and Iredale J.P. Liver fibrosis: cellular mechanisms of progression and resolution. Clin. Sci. 112 (2007) 265-280
21. Hsu Y.C., Lin Y.L., Chiu Y.T., Shiao M.S., Lee C.Y., and Huang Y.T. Anti-fibrotic effects of Salvia miltiorrhiza on dimethylnitrosamine-intoxicated rats. J. Biomed. Sci. 12 (2005) 185-195
22. Hsu Y.C., Chiu Y.T., Cheng C.C., Wu C.F., Lin Y.L., and Huang Y.T. Antifibrotic effects of tetrandrine on hepatic stellate cells and rats with liver fibrosis. J. Gastroenterol. Hepatol. 22 (2007) 99-111
23. Jaeschke H., Gores G.J., Cederbaum A.I., Hinson J.A., Pessayre D., and Lemasters J.J. Mechanisms of hepatotoxicity. Toxicol. Sci. 65 (2002) 166-176
24. Kisseleva T., and Brenner D.A. Mechanisms of fibrogenesis. Exp. Biol. Med. 233 (2008) 109-122
25. Li L., Grenard P., Nhieu J.T., Julien B., Mallat A., Habib A., and Lotersztajn S. Heme oxygenase-1 is an antifibrogenic protein in human hepatic myofibroblasts. Gastroenterology 125 (2003) 460-469
26. Li L., Julien B., Grenard P., Teixeira-Clerc F., Mallat A., and Lotersztajn S. Molecular mechanisms regulating the antifibrogenic protein heme-oxygenase-1 in human hepatic myofibroblasts. J. Hepatol. 41 (2004) 407-413
27. Lieber C.S. S-adenosyl-l-methionine: its role in the treatment of liver disorders. Am. J. Clin. Nutr. 76 (2002) 1183S-1187S
28. Lin Y.L., Lee T.F., Huang Y.J., and Huang Y.T. Antiproliferative effect of salvianolic acid A on rat hepatic stellate cells. J. Pharm. Pharmacol. 58 (2006) 933-939
29. Lin Y.L., Wu C.H., Luo M.H., Huang Y.J., Wang C.N., Shiao M.S., and Huang Y.T. Effect of salvianolic acid B on oxidative damage in primary hepatocytes and hepatic stellate cells. J. Ethnopharmacol. 105 (2006) 215-222
30. Liu G.T., Zhang T.M., Wang B.E., and Wang Y.W. Protective action of seven natural phenolic compounds against peroxidative damage to biomembranes. Biochem. Pharmacol. 43 (1992) 147-152
31. Liu P., Hu Y., Liu C., and Zhu D. Effects of salvianolic acid A (SA-A) on liver injury: SA-A action on hepatic peroxidation. Liver 21 (2001) 384-390
32. Malaguarnera L., Madeddu R., Palio E., Arena N., and Malaguarnera M. Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J. Hepatol. 42 (2005) 585-591
33. Mantena S.K., King A.L., Andringa K.K., Eccleston H.B., and Bailey S.M. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases. Free Radic. Biol. Med. 44 (2008) 1259-1272
34. Mato J.M., and Lu S.C. Role of S-adenosyl-l-methionine in liver health and injury. Hepatology 45 (2007) 1306-1312
35. Mato J.M., Corrales F.J., Lu S.C., and Avila M.A. S-Adenosylmethionine: a control switch that regulates liver function. FASEB J. 16 (2002) 15-26
36. Nieto N. Oxidative-stress and IL-6 mediate the fibrogenic effects of rodent Kupffer cells on stellate cells. Hepatology 44 (2006) 1487-1501
37. Nieto N., Friedman S.L., and Cederbaum A.I. Stimulation and proliferation of primary rat hepatic stellate cells by cytochrome P450 2E1-derived oxygen species. Hepatology 35 (2002) 62-73
38. Ohkawa H., Ohishi N., and Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95 (1979) 351-358
39. Parola M., and Robino G. Oxidative stress-related molecules and liver fibrosis. J. Hepatol. 35 (2001) 297-306
40. Reif S., Aeed H., Shilo Y., Reich R., Kloog Y., Kweon Y.O., and Bruck R. Treatment of thioacetamide-induced liver cirrhosis by the Ras antagonist, farnesylthiosalicylic acid. J. Hepatol. 41 (2004) 235-241
41. Reinehr R., Becker S., Eberle A., Grether-Beck S., and Haussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J. Biol. Chem. 280 (2005) 27179-27194
42. Sanz-Cameno P., Medina J., García-Buey L., García-Sánchez A., Borque M.J., Martín-Vílchez S., Gamallo C., Jones E.A., and Moreno-Otero R. Enhanced intrahepatic inducible nitric oxide synthase expression and nitrotyrosine accumulation in primary biliary cirrhosis and autoimmune hepatitis. J. Hepatol. 37 (2002) 723-729
43. Scheuer P.J. Classification of chronic viral hepatitis: a need for reassessment. J. Hepatol. 13 (1991) 372-374
44. Svegliati Baroni G., D'Ambrosio L., Ferretti G., Casini A., Di Sario A., Salzano R., Ridolfi F., Saccomanno S., Jezequel A.M., and Benedetti A. Fibrogenic effect of oxidative stress on rat hepatic stellate cells. Hepatology 27 (1998) 720-726
45. Tilg H., Kaser A., and Moschen A.R. How to modulate inflammatory cytokines in liver diseases. Liver Int. 26 (2006) 1029-1039
46. Urtasun R., Cubero F.J., Vera M., and Nieto N. Reactive nitrogen species switch on early extracellular matrix remodeling via induction of MMP1 and TNFα. Gastroenterology 136 (2009) 1410-1422
47. Venkatraman A., Shiva S., Wigley A., Ulasova E., Chhieng D., Bailey S.M., and Darley-Usmar V.M. The role of iNOS in alcohol-dependent hepatotoxicity and mitochondrial dysfunction in mice. Hepatology 40 (2004) 565-573
48. Vogel S., Piantedosi R., Frnak J., Lalazar A., Rockey D.C., Friedman S.L., and Blaner W.S. An immortalized rat liver stellate cell (HSC-T6): a new cell model for the study of retinoid metabolism in vitro. J. Lipid Res. 41 (2000) 882-893
49. Wallace K., Burt A.D., and Wright M.C. Liver fibrosis. Biochem. J. 411 (2008) 1-18
50. Yao P., Nussler A., Liu L., Hao L., Song F., Schirmeier A., and Nussler N. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J. Hepatol. 47 (2007) 253-261
51. Yuan L., and Kaplowitz N. Glutathione in liver diseases and hepatotoxicity. Mol. Aspects Med. 30 (2009) 29-41
52. Zhan S.S., Jiang J.X., Wu J., Halsted C., Friedman S.L., Zern M.A., and Torok N.J. Phagocytosis of apoptotic bodies by hepatic stellate cells induces NADPH oxidase and is associated with liver fibrosis in vivo. Hepatology 43 (2006) 435-443