Heme oxygenase-1 mediates the protective role of quercetin against ethanol-induced rat hepatocytes oxidative damage

Toxicology in Vitro

Volumn 26, Issue 1, 2012, Pages 74-80

  Liu, Shuang ^a,b   Hou, Wei ^a   Yao, Ping ^a   Li, Na ^a,b   Zhang, Biyun ^a,b   Hao, Liping ^a   Nüssler, Andreas K ^c   Liu, Liegang ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Hubei Center for Disease Control and Prevention   (China)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Ethanol; Extracellular signal regulated kinase; Heme oxygenase 1; Nuclear factor erythroid 2 related factor 2; Oxidative damage; Quercetin

Indexed keywords

ALCOHOL; HEME OXYGENASE 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTOPORPHYRIN ZINC; PROTOPORPHYRIN ZINC 9; QUERCETIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; CYTOSOLIC FRACTION; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; LIVER CELL; LIVER TOXICITY; MALE; NONHUMAN; NUCLEAR FRACTION; OXIDATIVE STRESS; PARAMETERS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIOXIDANTS; ASPARTATE AMINOTRANSFERASES; CATALASE; CELLS, CULTURED; ETHANOL; GLUTATHIONE; HEME OXYGENASE-1; HEPATOCYTES; L-LACTATE DEHYDROGENASE; MALE; MALONDIALDEHYDE; MAP KINASE SIGNALING SYSTEM; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

RATTUS;

EID: 84855343368     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2011.10.013     Document Type: Article

References (50)

1. Bergmeyer H.U., Horder M., Rej R. International Federation of Clinical Chemistry (IFCC) Scientific Committee, Analytical Section: approved recommendation (1985) on IFCC methods for the measurement of catalytic concentration of enzymes. Part 2. IFCC method for aspartate aminotransferase (L-aspartate: 2-oxoglutarate aminotransferase, EC 2.6.1.1). J. Clin. Chem. Clin. Biochem. 1986, 24:497-510.
2. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
3. Calabrese V., Renis M., Calderone A., Russo A., Barcellona M.L., Rizza V. Stress proteins and SH-groups in oxidant-induced cell damage after acute ethanol administration in rat. Free Radical Biol. Med. 1996, 20:391-397.
4. Caro A.A., Cederbaum A.I. Oxidative stress, toxicology, and pharmacology of CYP2E1. Annu. Rev. Pharmacol. Toxicol. 2004, 44:27-42.
5. Cederbaum A.I., Wu D., Mari M., Bai J. CYP2E1-dependent toxicity and oxidative stress in HepG2 cells. Free Radical Biol. Med. 2001, 31:1539-1543.
6. 2-induced apoptosis via anti-oxidant activity and heme oxygenase 1 gene expression in macrophages. Biochem. Pharmacol. 2005, 69:1839-1851.
7. Dias A.S., Porawski M., Alonso M., Marroni N., Collado P.S., Gonzalez-Gallego J. Quercetin decreases oxidative stress, NF-kappaB activation, and iNOS overexpression in liver of streptozotocin-induced diabetic rats. J. Nutr. 2005, 135:2299-2304.
8. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
9. Dore S. Decreased activity of the antioxidant heme oxygenase enzyme: implications in ischemia and in Alzheimer's disease. Free Radical Biol. Med. 2002, 32:1276-1282.
10. Figliomeni M.L., Abdel-Rahman M.S. Ethanol does not increase the hepototoxicity of cocaine in primary rat hepatocyte culture. Toxicology 1998, 129:125-135.
11. Goth L. A simple method for determination of serum catalase activity and revision of reference range. Clin. Chim. Acta 1991, 196:143-151.
12. Immenschuh S., Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem. Pharmacol. 2000, 60:1121-1128.
13. Kahraman A., Erkasap N., Koken T., Serteser M., Aktepe F., Erkasap S. The antioxidative and antihistaminic properties of quercetin in ethanol-induced gastric lesions. Toxicology 2003, 183:133-142.
14. Kietzmann T., Samoylenko A., Immenschuh S. Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J. Biol. Chem. 2003, 278:17927-17936.
15. Kono Y. Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch. Biochem. Biophys. 1978, 186:189-195.
16. Lin H.C., Cheng T.H., Chen Y.C., Juan S.H. Mechanism of heme oxygenase-1 gene induction by quercetin in rat aortic smooth muscle cells. Pharmacology 2004, 71:107-112.
17. Liu L.G., Yan H., Zhang W., Yao P., Zhang X.P., Sun X.F., Nüssler A.K. Induction of heme oxygenase-1 in human hepatocytes to protect them from ethanol-induced cytotoxicity. Biomed. Environ. Sci. 2004, 17:315-326.
18. Liu S., Hou W., Yao P., Zhang B., Sun S., Nüssler A.K., Liu L. Quercetin protects against ethanol-induced oxidative damage in rat primary hepatocytes. Toxicol. in Vitro 2010, 24:516-522.
19. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
20. Mancuso C. Heme oxygenase and its products in the nervous system. Antioxid. Redox Signal. 2004, 6:878-887.
21. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., De Galarreta C.M., Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-Kinase/Akt Pathway and the Nrf2 Transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 2004, 279:8919-8929.
22. McCoubrey W.K.J., Huang T.J., Maines M.D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 1997, 247:725-732.
23. McCuskey R.S., Bethea N.W., Wong J., McCuskey M.K., Abril E.R., Wang X., Ito Y., Deleve L.D. Ethanol binging exacerbates sinusoidal endothelial and parenchymal injury elicited by acetaminophen. J. Hepatol. 2005, 42:371-377.
24. Molina M.F., Sanchez-Reus I., Iglesias I., Benedi J. Quercetin, a flavonoid antioxidant, prevents and protects against ethanol-induced oxidative stress in mouse liver. Biol. Pharm. Bull. 2003, 26:1398-1402.
25. Moron M.S., Depierre J.W., Mannervik B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta 1979, 582:67-78.
26. 2)-induced NF-kappaB DNA binding activity and DNA damage in HepG2 cells. Carcinogenesis 1998, 19:1583-1589.
27. Nakahira K., Takahashi T., Shimizu H., Maeshima K., Uehara K., Fujii H., Nakatsuka H., Yokoyama M., Akagi R., Morita K. Protective role of heme oxygenase-1 induction in carbon tetrachloride-induced hepatotoxicity. Biochem. Pharmacol. 2003, 66:1091-1105.
28. Nakaso K., Yano H., Fukuhara Y., Takeshima T., Isoe K.W., Nakashima K. PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Lett. 2003, 546:181-184.
29. Nguyen T., Yang C.S., Pickett C.B. The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radical Biol. Med. 2004, 37:433-441.
30. Nordmann R., Ribiere C., Rouach H. Implication of free radical mechanisms in ethanol-induced cellular injury. Free Radical Biol. Med. 1992, 12:219-240.
31. Noroozi M., Angerson W.J., Lean M.E. Effect of flavonoids and vitamin C on oxidative DNA damage to human lymphocytes. Am. J. Clin. Nutr. 1998, 67:1210-1218.
32. Ohlmann A., Giffhorn-Katz S., Becker I., Katz N., Immenschuh S. Regulation of heme oxygenase-1 gene expression by anoxia and reoxygenation in primary rat hepatocyte cultures. Exp. Biol. Med. (Maywood) 2003, 228:584-589.
33. Ohyashiki T., Satoh E., Okada M., Takadera T., Sahara M. Nerve growth factor protects against aluminum-mediated cell death. Toxicology 2002, 176:195-207.
34. Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biol. Med. 1996, 20:933-956.
35. Ryter S.W., Kim H.P., Nakahira K., Zuckerbraun B.S., Morse D., Choi A.M. Protective functions of heme oxygenase-1 and carbon monoxide in the respiratory system. Antioxid. Redox Signal. 2007, 9:2157-2173.
36. Scapagnini G., Foresti R., Calabrese V., Stella A.M., Green C.J., Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 2002, 61:554-561.
37. Shan Y., Pepe J., Lu T.H., Elbirt K.K., Lambrecht R.W., Bonkovsky H.L. Induction of the heme oxygenase-1 gene by metalloporphyrins. Arch. Biochem. Biophys. 2000, 380:219-227.
38. Suematsu M., Goda N., Sano T., Kashiwagi S., Egawa T., Shinoda Y., Ishimura Y. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J. Clin. Invest. 1995, 96:2431-2437.
39. Torres M., Forman H.J. Redox signaling and the MAP kinase pathways. BioFactors 2003, 17:287-296.
40. Tuschl G., Mueller S.O. Effects of cell culture conditions on primary rat hepatocytes-cell morphology and differential gene expression. Toxicology 2006, 218:205-215.
41. Tüzüner E., Liu L., Shimada M., Yilmaz E., Glanemann M., Settmacher U., Langrehr J.M., Jonas S., Neuhaus P., Nüssler A.K. Heme oxygenase-1 protects human hepatocytes in vitro against warm and cold hypoxia. J. Hepatol. 2004, 41:764-772.
42. Wagener F.A., Volk H.D., Willis D., Abraham N.G., Soares M.P., Adema G.J., Figdor C.G. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol. Rev. 2003, 55:551-571.
43. Williams R.J., Spencer J.P., Rice-Evans C. Flavonoids: antioxidants or signalling molecules?. Free Radical Biol. Med. 2004, 36:838-849.
44. Willis D., Moore A.R., Willoughby D.A. Heme oxygenase isoform expression in cellular and antibody-mediated models of acute inflammation in the rat. J. Pathol. 2000, 190:627-634.
45. Wung B.S., Hsu M.C., Wu C.C., Hsieh C.W. Piceatannol upregulates endothelial heme oxygenase-1 expression via novel protein kinase C and tyrosine kinase pathways. Pharmacol. Res. 2006, 53:113-122.
46. Yachie A., Niida Y., Wada T., Igarashi, Kaneda H., Toma T., Ohta K., Kasahara Y., Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 1999, 103:129-135.
47. Yao P., Li K., Song F., Zhou S., Sun X., Zhang X., Nüssler A.K., Liu L. Heme oxygenase-1 upregulated by Ginkgo biloba extract: potential protection against ethanol-induced oxidative liver damage. Food Chem. Toxicol. 2007, 45:1333-1342.
48. Yao P., Nussler A., Liu L., Hao L., Song F., Schirmeier A., Nussler N. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J. Hepatol. 2007, 47:253-261.
49. Yoshida T., Migita C.T. Mechanism of heme degradation by heme oxygenase. J. Inorg. Biochem. 2000, 82:33-41.
50. Zhang F.K., Zhang J.Y., Jia J.D. Treatment of patients with alcoholic liver disease. Hepatobiliary Pancreat Dis. Int. 2005, 4:12-17.