Resveratrol suppresses oxidative stress and inflammatory response in diethylnitrosamine-initiated rat hepatocarcinogenesis

Cancer Prevention Research

Volumn 3, Issue 6, 2010, Pages 753-763

  Bishayee, Anupam ^a   Barnes, Kendra F ^a   Bhatia, Deepak ^a   Darvesh, Altaf S ^a   Carroll, Richard T ^a  

^a NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; DIETHYLNITROSAMINE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; RESVERATROL; TRANSCRIPTION FACTOR NRF2; 3-NITROTYROSINE; ANTIOXIDANT; CARCINOGEN; NOS2 PROTEIN, RAT; PHENOBARBITAL; STILBENE DERIVATIVE; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; FEMALE; INFLAMMATION; LIPID PEROXIDATION; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; DRUG EFFECTS; DRUG SCREENING; DRUG-INDUCED LIVER INJURY; ENZYME INDUCTION; GENETICS; HYPERPLASIA; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; METABOLISM; PATHOLOGY; PRECANCER; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; CARCINOGENS; DIETHYLNITROSAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG-INDUCED LIVER INJURY; ENZYME INDUCTION; FEMALE; HYPERPLASIA; INFLAMMATION; LIPID PEROXIDATION; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; NF-E2-RELATED FACTOR 2; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PHENOBARBITAL; PRECANCEROUS CONDITIONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STILBENES; TYROSINE;

EID: 77953229913     PISSN: 19406207     EISSN: None     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-09-0171     Document Type: Article

References (62)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-105.
2. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 2004;127:S27-34.
3. American Cancer Society. Cancer facts and figures 2009. Atlanta: American Cancer Society; 2009.
4. Schütte K, Bornschein J, Malfertheiner P. Hepatocellular carcinoma - epidemiological trends and risk factors. Dig Dis 2009;27:80-92.
5. Paraskevi A, Ronald A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 2006;6:1-14.
6. Bartsch H, Montesano R. Relevance of nitrosamines to human cancer. Carcinogenesis 1984;5:1381-93.
7. Kensler TW, Egner PA, Wang JB, et al. Chemoprevention of hepatocellular carcinoma in aflatoxin endemic areas. Gastroenterology 2004;127:S310-8.
8. Yates MS, Kensler TW. Keap1 eye on the target: chemoprevention of liver cancer. Acta Pharmacol Sin 2007;28:1331-42.
9. Vidavalur R, Otani H, Singal PK, Maulik N. Significance of wine and resveratrol in cardiovascular disease: French paradox revisited. Exp Clin Cardiol 2006;11:217-25.
10. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 2006;5:493-506.
11. Saiko P, Szakmary A, Jaeger W, Szekeres T. Resveratrol and its analogs: defense against cancer, coronary disease and neurodegenerative maladies or just a fad? Mutat Res 2008;658:68-94.
12. Athar M, Back JH, Kopelovich L, Bickers DR, Kim AL. Multiple molecular targets of resveratrol: anti-carcinogenic mechanisms. Arch Biochem Biophys 2009;486:95-102.
13. Kundu JK, Surh Y-J. Cancer chemopreventive and therapeutic potential of resveratrol: mechanistic perspectives. Cancer Lett 2008;269:243-61.
14. Bishayee A. Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev Res 2009;2:409-18.
15. Bishayee A, Politis T, Darvesh AS. Resveratrol in the chemoprevention and treatment of hepatocellular carcinoma. Cancer Treat Rev 2010;36:43-53.
16. Bishayee A, Dhir N. Resveratrol-mediated chemoprevention of diethylnitrosamine-initiated hepatocarcinogenesis: inhibition of cell proliferation and induction of apoptosis. Chem Biol Interact 2009;179:131-44.
17. Kawanishi S, Hiraku Y, Pinlaor S, Ma N. Oxidative stress and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem 2006;387:365-72.
18. Rubiolo JA, Mithieux G, Vega FV. Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur J Pharmacol 2008;591:66-72.
19. Das S, Das DK. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Target 2007;6:168-73.
20. Osburn WO, Kensler TW. Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat Res 2008;659:31-9.
21. Liu H, Dinkova-Kostova AT, Talalay P. Coordinate regulation of enzyme markers for inflammation and for protection against oxidants and electrophiles. Proc Natl Acad Sci U S A 2008;105:15926-31.
22. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reactions. Anal Biochem 1979;95:351-8.
23. Ueno S, Aoki D, Kubo F, et al. Roxithromyc inhibits constitutive activation of nuclear factor κB by diminishing oxidative stress in a rat model of hepatocellular carcinoma. Clin Cancer Res 2005;11:5645-50.
24. Naugler WE, Sakurai T, Kim S, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007;317:121-4. (Pubitemid 47056470)
25. Karimov KY, Inoyatova FK, Mukhamedova MT. Changes in some indices of the synthesis of nitric oxide during early stages of hepatocarcinogenesis. Exp Toxic Pathol 2002;55:17-9.
26. Archer MC. Mechanisms of action of N-nitroso compounds. Cancer Surv 1989;8:241-50.
27. Marnett LJ. Oxy radicals, lipid peroxidation and DNA damage. Toxicology 2002;181-2:219-22.
28. Lee KW, Wang HJ, Murphy PA, Hendrich S. Soybean isoflavone extract suppresses early but not later promotion of hepatocarcinogenesis by phenobarbital in female rat liver. Nutr Cancer 1995;24:267-78.
29. Scholz W, Schutze K, Kunz W, Schwartz M. Phenobarbital enhances the formation of reactive oxygen in neoplastic liver nodules. Cancer Res 1990;50:7015-22.
30. Sarkar A, Bishayee A, Chatterjee M. β-Carotene prevents lipid peroxidation and red blood cell membrane protein damage in experimental hepatocarcinogenesis. Cancer Biochem Biophys 1995;15:111-25.
31. Jeyabal PVS, Syed MB, Venkataraman M, Sambandham JK, Sakthisekaran D. Apigenin inhibits oxidative stress-induced macromolecular damage in N-nitrosodiethylamine (NDNA)-induced hepatocellular carcinogenesis in Wistar albino rats. Mol Carcinog 2005;44:11-20.
32. Shahjahan M, Vani G, Shyamaladevi CS. Effect of Solanum trilobatum on the antioxidant status during diethyl nitrosamine induced and phenobarbital promoted hepatocarcinogenesis in rat. Chem Biol Interact 2005;156:113-23.
33. Yadav AM, Bhatnagar D. Chemo-preventive effect of star anise in N-nitrosodiethylamine initiated and phenobarbital promoted hepato- carcinogenesis. Chem Biol Interact 2007;169:207-14.
34. de la Lastra CA, Villegas I. Resveratrol as an antioxidant and prooxidant agent: mechanisms and clinical applications. Biochem Soc Trans 2007;35:1156-60.
35. Rubiolo JA, Vega FV. Resveratrol protects primary rat hepatocytes against necrosis induced by reactive oxygen species. Biomed Pharmacother 2008;62:606-12.
36. Kasdallah-Grissa A, Mornagui B, Aouani E, et al. Resveratrol, a red wine polyphenol, attenuates ethanol-induced oxidative stress in rat liver. Life Sci 2007;80:1033-9.
37. Rivera H, Shibayama M, Tsutsumi V, Perez-Alvarez V, Muriel P. Resveratrol and trimethylated resveratrol protect from acute liver damage induced by CCl4 in the rat. J Appl Toxicol 2008;28:147-55.
38. Şehirli O, Tozan A, Omurtag GZ, et al. Protective effect of resveratrol against naphthalene-induced oxidative stress in mice. Ecotoxicol Environ Saf 2008;71:301-8.
39. Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1997;324:1-18.
40. 1 and high-risk for hepatocellular carcinoma. Cancer Lett 2008;263:212-22.
41. Granado-Serrano AB, Martin MA, Bravo L, Goya L, Ramos S. A diet rich in cocoa attenuates N-nitrosodiethylamine-induced liver injury in rats. Food Chem Toxicol 2009;47:2499-506.
42. Olas B, Nowak P, Kolodziejczyk J, Ponczek M, Wachowicz B. Protective effects of resveratrol against oxidative/nitrative modifications of plasma proteins and lipids exposed to peroxynitrite. J Nutr Biochem 2006;17:96-102. (Pubitemid 43082143)
43. Prieto J. Inflammation, HCC and sex: IL-6 in the centre of the triangle. J Hepatol 2008;48:380-1.
44. Kuo PC, Abe KY, Schroeder RA. Oxidative stress increases hepatocyte iNOS gene transcription and promoter activity. Biochem Biophys Res Commun 1997;234:289-92.
45. Ahn B, Han BS, Kim DJ, Ohshima H. Immunohistochemical localization of inducible nitric oxide synthase and 3-nitrotyrosine in rat liver tumors induced by N-nitrosodiethylamine. Carcinogenesis 1999;20:1337-44.
46. Calvisi DF, Pinna F, Ladu S, et al. Aberrant iNOS signaling is under genetic control in rodent liver cancer and potentially prognostic for the human disease. Carcinogenesis 2008;29:1639-47.
47. Zhao X, Zhang JJ, Wang X, Bu XY, Lou YQ, Zhang GL. Effect of berberine on hepatocyte proliferation, inducible nitric oxide synthase expression, cytochrome P450 2E1 and 1A2 activities in diethylnitrosamine- and phenobarbital-treated rats. Biomed Pharmacother 2008;62:567-72.
48. Yang Z, Yang S, Misner BJ, Chiu R, Liu F, Meyskens FL, Jr. Nitric oxide initiates progression of human melanoma via a feedback loop mediated by apurinic/apyrimidinic endonulease-1/redox factor-1, which is inhibited by resveratrol. Mol Cancer Ther 2008;7:3751-60.
49. Crowell JA, Steele VE, Sigman CC, Fay JR. Is inducible nitric oxide synthase a target for chemoprevention? Mol Cancer Ther 2003;2:815-23.
50. Alvarez B, Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids 2003;25:295-311.
51. Zhang H, Zhang J, Ungvari Z, Zhang C. Resveratrol improves endothelial function: role of TNFα and vascular oxidative stress. Arterioscler Thromb Vasc Biol 2009;29:1164-71.
52. Surh Y-J. NF-κB and Nrf2 as potential chemopreventive targets of some anti-inflammatory and antioxidative phytonutrients with anti-inflammatory and antioxidative activities. Asia Pac J Clin Nutr 2008;17:269-72.
53. Surh Y-J, Kundu JK, Na H. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med 2008;74:1526-39.
54. Li W, Kong AN. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 2009;48:91-104.
55. Khor TO, Yu S, Kong A-N. Dietary cancer chemopreventive agents - targeting inflammation and Nfr2 signaling pathway. Planta Med 2008;74:1540-7.
56. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, 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 U S A 2001;98:3404-9.
57. Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-1 pathway of antioxidant gene expression. Antioxid Redox Signal 2005;7:382-4.
58. Talaley P, Fahey JW. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr 2001;131:3027-33S.
59. Kitamura Y, Umemura T, Kanki K, et al. Increased susceptibility to hepatocarcinogenicity of Nrf2-deficient mice exposed to 2-amino-3- methylimidazo[4,5-f]quinoline. Cancer Sci 2007;98:19-24.
60. Chen CY, Jang J-H, Li M-H, Surh Y-J. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun 2005;331:993-1000.
61. Hsieh TC, Lu X, Wang Z, Wu JM. Induction of quinine reductase NQO1 by resveratrol in human K562 cells involves the antioxidant response element ARE and is accompanied by nuclear translocation of transcription factor Nrf2. Med Chem 2006;2:275-85.
62. Kode A, Rajendrasozhan S, Caito S, Yang S-R, Megson IL, Rahman I. Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2008;294:L478-88.