α-Lipoic acid inhibits liver fibrosis through the attenuation of ROS-triggered signaling in hepatic stellate cells activated by PDGF and TGF-β

Toxicology

Volumn 282, Issue 1-2, 2011, Pages 39-46

  Foo, Ning Ping ^a,b,c   Lin, Shu Huei ^a   Lee, Yu Hsuan ^a   Wu, Ming Jiuan ^d   Wang, Ying Jan ^a,e  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b CHI MEI MEDICAL CENTER   (Taiwan)

^c CHUNG HWA UNIVERSITY OF MEDICAL TECHNOLOGY   (Taiwan)

^d Chia Nan Psychiatric Center   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Lipoic acid; Dihydrolipoic acid; Hepatic stellate cell; Liver fibrosis; Reactive oxygen species

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; THIOACETAMIDE; THIOCTIC ACID; TRANSFORMING GROWTH FACTOR BETA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; ATTENUATION; CHRONIC LIVER DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; LIVER FIBROSIS; LIVER INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STELLATE CELL;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; CELL LINE; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION REGULATION; HEPATIC STELLATE CELLS; LIVER; LIVER CIRRHOSIS; MALE; MAP KINASE SIGNALING SYSTEM; OXIDATIVE STRESS; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; RNA, MESSENGER; THIOCTIC ACID; TRANSFORMING GROWTH FACTOR BETA;

RATTUS;

EID: 79951575880     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2011.01.009     Document Type: Article

References (66)

1. Adachi M., Brenner D.A. High molecular weight adiponectin inhibits proliferation of hepatic stellate cells via activation of adenosine monophosphate-activated protein kinase. Hepatology 2008, 47:677-685.
2. Adachi T., Togashi H., Suzuki A., Kasai S., Ito J., Sugahara K., Kawata S. NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells. Hepatology 2005, 41:1272-1281.
3. Aram G., Potter J.J., Liu X., Wang L., Torbenson M.S., Mezey E. Deficiency of nicotinamide adenine dinucleotide phosphate, reduced form oxidase enhances hepatocellular injury but attenuates fibrosis after chronic carbon tetrachloride administration. Hepatology 2009, 49:911-919.
4. Aydin A.F., Küskü-Kiraz Z., Doĝru-Abbasoĝlu S., Güllüoĝlu M., Uysal M., Koçak-Toker N. Effect of carnosine against thioacetamide-induced liver cirrhosis in rat. Peptides 2010, 31:67-71.
5. Balkan J., Dogru-Abbasoglu S., Kanbagli O., Cevikbas U., Aykac-Toker G., Uysal M. Taurine has a protective effect against thioacetamide-induced liver cirrhosis by decreasing oxidative stress. Hum. Exp. Toxicol. 2001, 20:251-254.
6. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
7. Bergmeyer H.U., Scheibe P., Wahlefeld A.W. Optimization of methods for asparate aminotransferase and alanine aminotransferase. Clin. Chem. 1978, 24:58-73.
8. Bissell D.M. Hepatic fibrosis as wound repair: a progress report. J. Gastroenterol. 1998, 33:295-302.
9. Boigk G., Stroedter L., Herbst H., Waldschmidt J., Riecken E.O., Schuppan D. Silymarin retards collagen accumulation in early and advanced biliary fibrosis secondary to complete bile duct obliteration in rats. Hepatology 1997, 26:643-649.
10. Borkham-Kamphorst E., Meurer S.K., Gressner A.M., Weiskirchen R. Disruption of intermolecular disulfide bonds in PDGF-BB dimers by N-acetyl-L-cysteine does not prevent PDGF signaling in cultured hepatic stellate cells. Biochem. Biophys. Res. Commun. 2005, 338:1711-1718.
11. Brown K.E., Poulos J.E., Li L., Soweid A.M., Ramm G.A., O'Neill R., Britton R.S., Bacon B.R. Effect of vitamin E supplementation on hepatic fibrogenesis in chronic dietary iron overload. Am. J. Physiol. 1997, 272:G116-123.
12. Bruck R., Shirin H., Aeed H., Matas Z., Hochman A., Pines M., Avni Y. Prevention of hepatic cirrhosis in rats by hydroxyl radical scavengers. J. Hepatol. 2001, 35:457-464.
13. Bruck R., Genina O., Aeed H., Alexiev R., Nagler A., Avni Y., Pines M. Halofuginone to prevent and treat thioacetamide-induced liver fibrosis in rats. Hepatology 2001, 33:379-386.
14. Bruck R., Aeed H., Schey R., Matas Z., Reifen R., Zaiger G., Hochman A., Avni Y. Pyrrolidine dithiocarbamate protects against thioacetamide-induced fulminant hepatic failure in rats. J. Hepatol. 2002, 36:370-377.
15. Bruck R., Aeed H., Avni Y., Shirin H., Matas Z., Shahmurov M., Avinoach I., Zozulya G., Weizman N., Hochman A. Melatonin inhibits nuclear factor kappa B activation and oxidative stress and protects against thioacetamide induced liver damage in rats. J. Hepatol. 2004, 40:86-93.
16. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 2002, 296:1655-1657.
17. Carter A.B., Hunninghake G.W. A constitutive active MEK→ERK pathway negatively regulates NF-kappa B-dependent gene expression by modulating TATA-binding protein phosphorylation. J. Biol. Chem. 2000, 275:27858-27864.
18. Chen C.S., Wu C.H., Lai Y.C., Lee W.S., Chen H.M., Chen R.J., Chen L.C., Ho Y.S., Wang Y.J. NF-kappaB-activated tissue transglutaminase is involved in ethanol-induced hepatic injury and the possible role of propolis in preventing fibrogenesis. Toxicology 2008, 246:148-157.
19. Dekel R., Zvibel I., Brill S., Brazovsky E., Halpern Z., Oren R. Gliotoxin ameliorates development of fibrosis and cirrhosis in a thioacetamide rat model. Dig. Dis. Sci. 2003, 48:1642-1647.
20. Fernandez-Checa J.C., Kaplowitz N., Garcia-Ruiz C., Colell A. Mitochondrial glutathione: importance and transport. Semin. Liver Dis. 1998, 18:389-401.
21. Finkel T. Oxygen radicals and signaling. Curr. Opin. Cell Biol. 1998, 10:248-253.
22. Friedman S.L. Seminars in medicine of the Beth Israel Hospital Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N. Engl. J. Med. 1993, 328:1828-1835.
23. Friedman S.L. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J. Biol. Chem. 2000, 275:2247-2250.
24. Friedman S.L. Liver fibrosis-from bench to bedside. J. Hepatol. 2003, 38 Suppl.(1):S38-53.
25. Gebhardt R. Oxidative stress, plant-derived antioxidants and liver fibrosis. Planta Med. 2002, 68:289-296.
26. Heck S., Lezoualc'h F., Engert S., Behl C. Insulin-like growth factor-1-mediated neuroprotection against oxidative stress is associated with activation of nuclear factor kappaB. J. Biol. Chem. 1999, 274:9828-9835.
27. Ho Y.S., Lai C.S., Liu H.I., Ho S.Y., Tai C., Pan M.H., Wang Y.J. Dihydrolipoic acid inhibits skin tumor promotion through anti-inflammation and anti-oxidation. Biochem. Pharmacol. 2007, 73:1786-1795.
28. Hori N., Okanoue T., Sawa Y., Mori T., Kashima K. Hemodynamic characterization in experimental liver cirrhosis induced by thioacetamide administration. Dig. Dis. Sci. 1993, 38:2195-2202.
29. Houglum K., Venkataramani A., Lyche K., Chojkier M. A pilot study of the effects of d-alpha-tocopherol on hepatic stellate cell activation in chronic hepatitis C. Gastroenterology 1997, 113:1069-1073.
30. Hunter A.L., Holscher M.A., Neal R.A. Thioacetamide-induced hepatic necrosis I. Involvement of the mixed-function oxidase enzyme system. J. Pharmacol. Exp. Ther. 1977, 200:439-448.
31. Iredale J.P. Cirrhosis: new research provides a basis for rational and targeted treatments. BMJ 2003, 327:143-147.
32. Jaeschke H., Gores G.J., Cederbaum A.I., Hinson J.A., Pessayre D., Lemasters J.J. Mechanisms of hepatotoxicity. Toxicol. Sci. 2002, 65:166-176.
33. Javelaud D., Mauviel A. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 2005, 24:5742-5750.
34. Kaplowitz N. Biochemical and cellular mechanisms of toxic liver injury. Semin. Liver Dis. 2002, 22:137-144.
35. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 2000, 18:621-663.
36. Karsan H.A., Rojter S.E., Saab S. Primary prevention of cirrhosis. Public health strategies that can make a difference. Postgrad. Med. 2004, 115:25-30.
37. Kozlov A.V., Gille L., Staniek K., Nohl H. Dihydrolipoic acid maintains ubiquinone in the antioxidant active form by two-electron reduction of ubiquinone and one-electron reduction of ubisemiquinone. Arch. Biochem. Biophys. 1999, 363:148-154.
38. Lander H.M. An essential role for free radicals and derived species in signal transduction. FASEB J. 1997, 11:118-124.
39. Lee K.S., Buck M., Houglum K., Chojkier M. Activation of hepatic stellate cells by TGF alpha and collagen type I is mediated by oxidative stress through c-myb expression. J. Clin. Invest. 1995, 96:2461-2468.
40. Liu S.L., Degli Esposti S., Yao T., Diehl A.M., Zern M.A. Vitamin E therapy of acute CCl4-induced hepatic injury in mice is associated with inhibition of nuclear factor kappa B binding. Hepatology 1995, 22:1474-1481.
41. Lotersztajn S., Julien B., Teixeira-Clerc F., Grenard P., Mallat A. Hepatic fibrosis: molecular mechanisms and drug targets. Annu. Rev. Pharmacol. Toxicol. 2005, 45:605-628.
42. Madrid L.V., Wang C.Y., Guttridge D.C., Schottelius A.J., Baldwin A.S., Mayo M.W. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol. Cell. Biol. 2000, 20:1626-1638.
43. Marra F., Gentilini A., Pinzani M., Choudhury G.G., Parola M., Herbst H., Dianzani M.U., Laffi G., Abboud H.E., Gentilini P. Phosphatidylinositol 3-kinase is required for platelet-derived growth factor's actions on hepatic stellate cells. Gastroenterology 1997, 112:1297-1306.
44. Min A.K., Kim M.K., Seo H.Y., Kim H.S., Jang B.K., Hwang J.S., Choi H.S., Lee K.U., Park K.G., Lee I.K. Alpha-lipoic acid inhibits hepatic PAI-1 expression and fibrosis by inhibiting the TGF-beta signaling pathway. Biochem. Biophys. Res. Commun. 2010, 393:536-541.
45. Monteiro H.P., Stern A. Redox modulation of tyrosine phosphorylation-dependent signal transduction pathways. Free Radic. Biol. Med. 1996, 21:323-333.
46. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
47. Muller A., Machnik F., Zimmermann T., Schubert H. Thioacetamide-induced cirrhosis-like liver lesions in rats--usefulness and reliability of this animal model. Exp. Pathol. 1988, 34:229-236.
48. Muller D., Sommer M., Kretzschmar M., Zimmermann T., Buko V.U., Lukivskaya O., Dargel R. Lipid peroxidation in thioacetamide-induced macronodular rat liver cirrhosis. Arch. Toxicol. 1991, 65:199-203.
49. Packer L., Tritschler H.J., Wessel K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic. Biol. Med. 1997, 22:359-378.
50. Packer L., Witt E.H., Tritschler H.J. alpha-Lipoic acid as a biological antioxidant. Free Radic. Biol. Med. 1995, 19:227-250.
51. Pinzani M., Knauss T.C., Pierce G.F., Hsieh P., Kenney W., Dubyak G.R., Abboud H.E. Mitogenic signals for platelet-derived growth factor isoforms in liver fat-storing cells. Am. J. Physiol. 1991, 260:C485-491.
52. Poli G. Pathogenesis of liver fibrosis: role of oxidative stress. Mol. Aspects Med. 2000, 21:49-98.
53. Robinson M.J., Cobb M.H. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 1997, 9:180-186.
54. Roy S., Packer L. Redox regulation of cell functions by alpha-lipoate: biochemical and molecular aspects. Biofactors 1998, 8:17-21.
55. Shay K.P., Moreau R.F., Smith E.J., Smith A.R., Hagen T.M. Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim. Biophys. Acta 2009, 1790:1149-1160.
56. Sundaresan M., Yu Z.X., Ferrans V.J., Irani K., Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299.
57. Surapisitchat J., Hoefen R.J., Pi X., Yoshizumi M., Yan C., Berk B.C. Fluid shear stress inhibits TNF-alpha activation of JNK but not ERK1/2 or p38 in human umbilical vein endothelial cells: inhibitory crosstalk among MAPK family members. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6476-6481.
58. Suzuki Y.J., Forman H.J., Sevanian A. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 1997, 22:269-285.
59. Thannickal V.J., Day R.M., Klinz S.G., Bastien M.C., Larios J.M., Fanburg B.L. Ras-dependent and -independent regulation of reactive oxygen species by mitogenic growth factors and TGF-beta1. FASEB J. 2000, 14:1741-1748.
60. Toker A., Cantley L.C. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 1997, 387:673-676.
61. Vayalil P.K., Iles K.E., Choi J., Yi A.K., Postlethwait E.M., Liu R.M. Glutathione suppresses TGF-beta-induced PAI-1 expression by inhibiting p38 and JNK MAPK and the binding of AP-1, SP-1, and Smad to the PAI-1 promoter. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L1281-1292.
62. Vogel S., Piantedosi R., Frank J., Lalazar A., Rockey D.C., Friedman S.L., Blaner W.S. An immortalized rat liver stellate cell line (HSC-T6): a new cell model for the study of retinoid metabolism in vitro. J. Lipid Res. 2000, 41:882-893.
63. Wang Y.J., Yang M.C., Pan M.H. Dihydrolipoic acid inhibits tetrachlorohydroquinone-induced tumor promotion through prevention of oxidative damage. Food Chem. Toxicol. 2008, 46:3739-3748.
64. Wu D., Cederbaum A.I. Role of p38 MAPK in CYP2E1-dependent arachidonic acid toxicity. J. Biol. Chem. 2003, 278:1115-1124.
65. Wu J., Zern M.A. Hepatic stellate cells: a target for the treatment of liver fibrosis. J. Gastroenterol. 2000, 35:665-672.
66. Yin M.F., Lian L.H., Piao D.M., Nan J.X. Tetrandrine stimulates the apoptosis of hepatic stellate cells and ameliorates development of fibrosis in a thioacetamide rat model. World J. Gastroenterol. 2007, 13:1214-1220.