Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1

Food and Chemical Toxicology

Volumn 46, Issue 4, 2008, Pages 1279-1287

  Farombi, E Olatunde ^a   Shrotriya, Sangeeta ^a   Na, Hye Kyung ^a   Kim, Sung Hoon ^b   Surh, Young Joon ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

Author keywords

ARE; Curcumin; Heme oxygenase 1; Hepatoprotection; Nrf2; Tetrahydrocurcumin

Indexed keywords

CURCUMIN; DIMETHYLNITROSAMINE; HEME OXYGENASE 1; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; GEL MOBILITY SHIFT ASSAY; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LIVER INJURY; LIVER PROTECTION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTICARCINOGENIC AGENTS; BLOTTING, WESTERN; CARCINOGENS; CURCUMIN; DIMETHYLNITROSAMINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME INDUCTION; ENZYMES; GLUTATHIONE; HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MALE; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; RATS; RATS, WISTAR; UP-REGULATION;

CURCUMA LONGA; RATTUS; ZINGIBERACEAE;

EID: 39149106003     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2007.09.095     Document Type: Article

References (48)

1. Aeschbach R., Loliger J., Scott B.C., Murcia A., Butler J., Halliwell B., and Aruoma O.I. Antioxidant actions of thymol, carvacrol, 6-gingerol, zingerone and hydroxytyrosol. Food Chem. Toxicol. 32 (1994) 31-36
2. Alam J., and Cook J.L. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr. Pharm. Des. 9 (2003) 2499-2511
3. Andreadi C.K., Howells L.M., Atherfold P.A., and Manson M.M. Involvement of Nrf2, p38, B-Raf, and nuclear factor-kappaB, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols. Mol. Pharmacol. 69 (2006) 1033-1040
4. Araujo C.C., and Leon L.L. Biological activities of Curcuma longa L. Mem. Inst. Oswaldo Cruz 96 (2001) 723-728
5. Balogun E., Hoque M., Gong P., Killeen E., Green C.J., Foresti R., Alam J., and Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J. 371 (2003) 887-895
6. Buege J.A., and Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 52 (1978) 302-310
7. Chainani-Wu N. Safety and anti-inflammatory activity of curcumin: a component of tumeric (Curcuma longa). J. Altern. Complement Med. 9 (2003) 161-168
8. Chuang S.E., Kuo M.L., Hsu C.H., Chen C.R., Lin J.K., Lai G.M., Hsieh C.Y., and Cheng A.L. Curcumin-containing diet inhibits diethylnitrosamine-induced murine hepatocarcinogenesis. Carcinogenesis 21 (2000) 331-335
9. Chun K.-S., Keum Y.-S., Han S.S., Song Y.S., Kim S.H., and Surh Y.-J. Curcumin inhibits phorbol ester-induced expression of cyclooxygenase-2 in mouse skin through suppression of extracellular signal-regulated kinase activity and NF-κB activation. Carcinogenesis 24 (2003) 1515-1524
10. Dinkova-Kostova A.T., Massiah M.A., Bozak R.E., Hicks R.J., and Talalay P. Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc. Natl. Acad. Sci. USA 98 (2001) 3404-3409
11. Frei E., Kuchenmeister F., Gliniorz R., Breuer A., and Schmezer P. N-nitrososdimethylamine is activated in microsomes from hepatocytes to reactive metabolites which damage DNA of non-parenchymal cells in rat liver. Toxicol. Lett. 123 (2001) 227-234
12. Gaedeke J., Noble N.A., and Border W.A. Curcumin blocks fibrosis in anti-Thy 1 glomerulonephritis through up-regulation of heme oxygenase 1. Kidney Int. 68 (2005) 2042-2049
13. George J., Rao K.R., Stern R., and Chandrakasan G. Dimethylnitrosamine-induced liver injury in rats: the early deposition of collagen. Toxicology 156 (2001) 129-138
14. Gong P., Stewart D., Hu B., Li N., Cook J., Nel A., and Alam J. Activation of the mouse heme oxygenase-1 gene by 15-deoxy-Delta(12,14)-prostaglandin J(2) is mediated by the stress response elements and transcription factor Nrf2. Antioxid. Redox Signal 4 (2002) 249-257
15. Guengerich F.P., Kim D.H., and Iwasaki M. Role of human cytochrome P-450 IIE1 in the oxidation of many low molecular weight cancer suspects. Chem. Res. Toxicol. 4 (1991) 168-179
16. Hill-Kapturczak N., Thamilselvan V., Liu F., Nick H.S., and Agarwal A. Mechanism of heme oxygenase-1 gene induction by curcumin in human renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 281 (2001) F851-F859
17. Iqbal M., Sharma S.D., Okazaki Y., Fujisawa M., and Okada S. Dietary supplementation of curcumin enhances antioxidant and phase II metabolizing enzymes in ddY male mice: possible role in protection against chemical carcinogenesis and toxicity. Pharmacol. Toxicol. 92 (2003) 33-38
18. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., and Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13 (1999) 76-86
19. Jaiswal A.K. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36 (2004) 1199-1207
20. Joe B., Vijaykumar M., and Lokesh B.R. Biological properties of curcumin-cellular and molecular mechanisms of action. Crit. Rev. Food Sci. Nutr. 44 (2004) 97-111
21. Jones E.A., Shahed A., and Shoskes D.A. Modulation of apoptotic and inflammatory genes by bioflavonoids and angiotensin II inhibition in ureteral obstruction. Urology 56 (2000) 346-351
22. Kaur G., Tirkey N., Bharrhan S., Chanana V., Rishi P., and Chopra K. Inhibition of oxidative stress and cytokine activity by curcumin in amelioration of endotoxin-induced experimental hepatotoxicity in rodents. Clin. Exp. Immunol. 145 (2006) 313-321
23. Kwak M.K., Itoh K., Yamamoto M., Sutter T.R., and Kensler T.W. Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dimethiole-3-thione. Mol. Med. 7 (2001) 135-145
24. Lee-Hilz Y.Y., Boerboom A.M., Westphal A.H., Berkel W.J., Aarts J.M., and Rietjens J.M. Pro-oxidant activity of flavonoids induces EpRE-mediated gene expression. Chem. Res. Toxicol. 19 (2006) 1499-1505
25. Li N., Alam J., Venkatesan MI., Eiguren-Fernandez A., Schmitz D., Di Stefano E., Slaughter N., Killeen E., Wang X., Huang A., Wang M., Miguel A.H., Cho A., Sioutas C., and Nel A.E. Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals. J. Immunol. 173 (2004) 3467-3481
26. Maines M.D., and Gibbs P.E. 30 some years of heme oxygenase: from a molecular wrecking ball to a mesmerizing trigger of cellular events. Biochem. Biophys. Res. Commun. 338 (2005) 568-577
27. McNally S.J., Harrison E.M., Ross J.A., Garden O.J., and Wigmore S.J. Curcumin induces heme oxygenase-1 in hepatocytes and is protective in simulated cold preservation and warm reperfusion injury. Transplantation 81 (2006) 623-626
28. Motterlini R., Foresti R., Bassi R., and Green C.J. Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic. Biol. Med. 28 (2000) 1303-1312
29. Murugan P., and Pari L. Effect of tetrahydrocurcumin on plasma antioxidants in streptozotocin-nicotinamide experimental diabetes. J. Basic Clin. Physiol. Pharmacol. 17 (2006) 231-244
30. Nanji A.A., Jokelainen K., Tipoe G.L., Rahemtulla A., Thomas P., and Dannenberg A.J. Curcumin prevents alcohol-induced liver disease in rats by inhibiting the expression of NF-kappa B-dependent genes. Am. J. Physiol. Gastrointest. Liver Physiol. 284 (2003) G321-G327
31. Naughton P., Foresti R., Bains S.K., Hoque M., Green C.J., and Motterlini R. Induction of heme oxygenase 1 by nitrosative stress. A role for nitroxyl anion. J. Biol. Chem. 277 (2002) 40666-40674
32. Okada K., Wangpoengtrakul C., Tanaka T., Toyokuni S., Uchida K., and Osawa T. Curcumin and especially tetrahydrocurcumin ameliorate oxidative stress-induced renal injury in mice. J. Nutr. 131 (2001) 2090-2095
33. Osawa T., and Kato Y. Protective role of antioxidative food factors in oxidative stress caused by hyperglycemia. Ann. NY. Acad. Sci . 1043 (2005) 440-451
34. Pari L., and Amali D.R. Protective role of tetrahydrocurcumin (THC) an active principle of turmeric on chloroquine induced hepatotoxicity in rats. J. Pharm. Pharm. Sci. 8 (2005) 115-123
35. Park E.J., Jeon C.H., Ko G., Kim J., and Sohn D.H. Protective effect of curcumin in rat liver injury induced by carbon tetrachloride. J. Pharm. Pharmacol. 52 (2000) 437-440
36. Perrella M.A., and Yet S.F. Role of heme oxygenase-1 in cardiovascular function. Curr. Pharm. Des. 9 (2003) 2479-2487
37. Prawan A., Kundu J.K., and Surh Y.J. Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxid. Redox Signal 7 (2005) 1688-1703
38. Ramos-Gomez M., Dolan P.M., Itoh K., Yamamoto M., and Kensler T.W. Interactive effects of nrf2 genotype and oltipraz on benzo a pyrene-DNA adducts and tumor yield in mice. Carcinogenesis 24 (2003) 461-467
39. Reys-Gordillo K., Segovia J., Shibayama M., Vergara P., Moreno M.G., and Muriel P. Curcumin protects against acute liver damage in the rat by inhibiting NF-kB, proinflammatory cytokines production and oxidative stress. Biochim. Biophys. Acta 1770 (2007) 989-996
40. Rukkumani R., Aruna K., Varma P.S., Rajasekaran K.N., and Menon V.P. Comparative effects of curcumin and an analog of curcumin on alcohol and PUFA induced oxidative stress. J. Pharm. Pharm. Sci. 7 (2004) 274-283
41. Rushworth S.A., Ogborne R.M., Charalambos C.A., and O'Connell M.A. Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem. Biophys. Res. Commun. 341 (2006) 1007-1016
42. Scapagnini G., Foresti R., Calabrese V., Giuffrida Stella A.M., Green C.J., and Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 61 (2002) 554-561
43. Shapiro H., Ashkenazi M., Weizman N., Shahmurov M., Aeed H., and Bruck R. Curcumin ameliorates acute thioacetamide-induced hepatotoxicity. J. Gastroenterol. Hepatol. 21 (2006) 358-366
44. Sreepriya M., and Bali G. Effects of administration of embelin and curcumin on lipid peroxidation, hepatic glutathione antioxidant defense and hematopoietic system during N-nitrosodiethylamine/Phenobarbital-induced hepatocarcinogenesis in Wistar rats. Mol. Cell. Biochem. 284 (2006) 49-55
45. Surh Y.J., Chun K.S., Cha H.H., Han S.S., Keum Y.S., Park K.K., and Lee S.S. Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-κB activation. Mutat. Res. (2001) 243-268
46. Teufelhofer O., Parzefall W., Kainzbauer E., Ferk F., Freiler C., Knasmüller S., Elbling L., Thurman R., and Schulte-Hermann R. Superoxide generation from Kupffer cells contributes to hepatocarcinogenesis: studies on NADPH oxidase knockout mice. Carcinogenesis 26 (2005) 319-329
47. Talalay P., and Fahey J.W. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J. Nutr. 131 (2001) 3027S-3033S
48. Vendemiale G., Grattagliano J., Caruso M.L., Serviddio G., Valentini A.M., Pirrelli M., and Altomare E. Increased oxidative stress in dimethylnitrosamine-induced liver fibrosis in the rat: effect of N-acetylcysteine and interferon-alpha. Toxicol. Appl. Pharmacol. 175 (2001) 130-139