Dual role of resveratrol in modulation of genotoxicity induced by sodium arsenite via oxidative stress and apoptosis

Food and Chemical Toxicology

Volumn 59, Issue , 2013, Pages 8-17

  Chen, Chengzhi ^a   Jiang, Xuejun ^a   Zhao, Wei ^a   Zhang, ZunZhen ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Apoptosis; Dual role; Genotoxcity; Oxidative stress; Resveratrol; Sodium arsenite

Indexed keywords

ARSENITE SODIUM; DNA; NUTRACEUTICAL; RESVERATROL; SUPEROXIDE DISMUTASE;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CHROMOSOME DAMAGE; DNA DAMAGE; EPITHELIUM CELL; GENOTOXICITY; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MODULATION; OXIDATIVE STRESS;

3-(45-DIMETHYL THIAZOL-2-YL)-25-DIPHENYL TETRAZOLIUM BROMIDE; 5,5′-DITHIOBIS-(2-NITROBENZOIC ACID); AOD; APOPTOSIS; AVERAGE OPTICAL DENSITY; DIMETHYLSULFOXIDE; DMEM; DMSO; DTNB; DUAL ROLE; DULBECCO'S MODIFIED EAGLE'S MEDIUM; FBS; FETAL BOVINE SERUM; GENOTOXCITY; GLUTATHIONE; GSH; MTT; NAASO(2); OLIVE TAIL MOMENT; OTM; OXIDATIVE STRESS; PBS; PHOSPHATE BUFFERED SALINE; PI; PROPIDIUM IODIDE; REACTIVE OXYGEN SPECIES; RESVERATROL; RIBONUCLEASE A; RNASE A; ROS; SOD; SODIUM ARSENITE; SUPEROXIDE DISMUTASE;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTIOXIDANTS; APOPTOSIS; ARSENITES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME BREAKAGE; COMET ASSAY; DNA DAMAGE; GLUTATHIONE; HUMANS; LUNG NEOPLASMS; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MUTAGENS; NEOPLASTIC STEM CELLS; OSMOLAR CONCENTRATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; SODIUM COMPOUNDS; STILBENES;

EID: 84879427014     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.05.030     Document Type: Article

References (59)

1. Aggarwal B.B., Bhardwaj A., Aggarwal R.S., Seeram N.P., Shishodia S., Takada Y. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res. 2004, 24:2783-2840.
2. Anderson M.E. Glutathione: an overview of biosynthesis and modulation. Chem. Biol. Interact. 1998, 111-112:1-14.
3. Beutler E., Duron O., Kelly B.M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 1963, 61:882-888.
4. Bishayee A. Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev. Res. (Philadelphia, Pa.) 2009, 2:409-418.
5. Brown K.G., Ross G.L. Arsenic, drinking water, and health: a position paper of the american council on science and health. Regul. Toxicol. Pharmacol. 2002, 36:162-174.
6. Burkitt M.J., Duncan J. Effects of trans-resveratrol on copper-dependent hydroxyl-radical formation and DNA damage: evidence for hydroxyl-radical scavenging and a novel, glutathione-sparing mechanism of action. Arch. Biochem. Biophys. 2000, 381:253-263.
7. Chen H., Hao Y., Wang L., Jia D., Ruan Y., Gu J. Sodium arsenite down-regulates the expression of X-linked inhibitor of apoptosis protein via translational and post-translational mechanisms in hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 2012, 422:721-726.
8. Clark D., Tuor U.I., Thompson R., Institoris A., Kulynych A., Zhang X., Kinniburgh D.W., Bari F., Busija D.W., Barber P.A. Protection against recurrent stroke with resveratrol: endothelial protection. PLoS ONE 2012, 7:e47792.
9. Clarke P.R., Allan L.A. Cell-cycle control in the face of damage - a matter of life or death. Trends Cell Biol. 2009, 19:89-98.
10. Cordes N., van Beuningen D. Arrest of human lung fibroblasts in G2 phase after irradiation is regulated by converging phosphatidylinositol-3 kinase and beta1-integrin signaling in vitro. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58:453-462.
11. Cui X., Kobayashi Y., Akashi M., Okayasu R. Metabolism and the paradoxical effects of arsenic: carcinogenesis and anticancer. Curr. Med. Chem. 2008, 15:2293-2304.
12. Donnelly L.E., Newton R., Kennedy G.E., Fenwick P.S., Leung R.H., Ito K., Russell R.E., Barnes P.J. Anti-inflammatory effects of resveratrol in lung epithelial cells: molecular mechanisms. American journal of physiology. Lung Cell. Mol. Physiol. 2004, 287:L774-783.
13. Flora S.J.S. Arsenic-induced oxidative stress and its reversibility. Free Radical Biol. Med. 2011, 51:257-281.
14. Frémont L. Biological effects of resveratrol. Life Sci. 2000, 66:663-673.
15. Fried J., Perez A.G., Clarkson B.D. Flow cytofluorometric analysis of cell cycle distributions using propidium iodide. Properties of the method and mathematical analysis of the data. J. Cell Biol. 1976, 71:172-181.
16. Giovannelli L., Pitozzi V., Jacomelli M., Mulinacci N., Laurenzana A., Dolara P., Mocali A. Protective effects of resveratrol against senescence-associated changes in cultured human fibroblasts. The journals of gerontology. Ser A, Biol. Sci. Med. Sci. 2011, 66:9-18.
17. Hei T.K., Filipic M. Role of oxidative damage in the genotoxicity of arsenic. Free Radical Biol. Med. 2004, 37:574-581.
18. Herbert K.J., Snow E.T. Modulation of arsenic-induced epidermal growth factor receptor pathway signalling by resveratrol. Chem. Biol. Interact. 2012, 198:38-48.
19. Hughes M.F., Beck B.D., Chen Y., Lewis A.S., Thomas D.J. Arsenic exposure and toxicology: a historical perspective. Toxicol. Sci. Off. J. Soc. Toxicol. 2011, 123:305-332.
20. Hung L.-M., Chen J.-K., Huang S.-S., Lee R.-S., Su M.-J. Cardioprotective effect of resveratrol, a natural antioxidant derived from grapes. Cardiovasc. Res. 2000, 47:549-555.
21. Ivanov V.N., Wen G., Hei T.K. Sodium arsenite exposure inhibits AKT and Stat3 activation, suppresses self-renewal and induces apoptotic death of embryonic stem cells. Apoptosis 2013, 18:188-200.
22. Jang M., Cai L., Udeani G.O., Slowing K.V., Thomas C.F., Beecher C.W.W., Fong H.H.S., Farnsworth N.R., Kinghorn A.D., Mehta R.G., Moon R.C., Pezzuto J.M. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997, 275:218-220.
23. Kimura Y., Okuda H. Resveratrol isolated from Polygonum cuspidatum root prevents tumor growth and metastasis to lung and tumor-induced neovascularization in Lewis lung carcinoma-bearing mice. J. Nutr. 2001, 131:1844-1849.
24. Kozuki Y., Miura Y., Yagasaki K. Resveratrol suppresses hepatoma cell invasion independently of its anti-proliferative action. Cancer Lett. 2001, 167:151-156.
25. Kuwajerwala N., Cifuentes E., Gautam S., Menon M., Barrack E.R., Reddy G.P. Resveratrol induces prostate cancer cell entry into s phase and inhibits DNA synthesis. Cancer Res. 2002, 62:2488-2492.
26. 3-induced oxidative stress and cycle progression in a human intestinal epithelial cell line (Caco-2). Toxicol. in vitro Int. J. Published Assoc. BIBRA 2008, 22:444-449.
27. Liu S.X., Athar M., Lippai I., Waldren C., Hei T.K. Induction of oxyradicals by arsenic: implication for mechanism of genotoxicity. Proc. Nat. Acad. Sci. USA 2001, 98:1643-1648.
28. McCollum G., Keng P.C., States J.C., McCabe M.J. Arsenite delays progression through each cell cycle phase and induces apoptosis following G2/M arrest in U937 myeloid leukemia cells. J. Pharmacol. Exp. Ther. 2005, 313:877-887.
29. McNeely S.C., Belshoff A.C., Taylor B.F., Fan T.W., McCabe M.J., Pinhas A.R., States J.C. Sensitivity to sodium arsenite in human melanoma cells depends upon susceptibility to arsenite-induced mitotic arrest. Toxicol. Appl. Pharmacol. 2008, 229:252-261.
30. Mei N., Lee J., Sun X., Xing J.Z., Hanson J., Le X.C., Weinfeld M. Genetic predisposition to the cytotoxicity of arsenic: the role of DNA damage and ATM. FASEB J. 2003, 17:2310-2312.
31. Nakagawa H., Kiyozuka Y., Uemura Y., Senzaki H., Shikata N., Hioki K., Tsubura A. Resveratrol inhibits human breast cancer cell growth and may mitigate the effect of linoleic acid, a potent breast cancer cell stimulator. J. Cancer Res. Clin. Oncol. 2001, 127:258-264.
32. Pellegatta F., Bertelli A.A., Staels B., Duhem C., Fulgenzi A., Ferrero M.E. Different short- and long-term effects of resveratrol on nuclear factor-kappaB phosphorylation and nuclear appearance in human endothelial cells. Am. J. Clin. Nutr. 2003, 77:1220-1228.
33. Peltz L., Gomez J., Marquez M., Alencastro F., Atashpanjeh N., Quang T., Bach T., Zhao Y. Resveratrol exerts dosage and duration dependent effect on human mesenchymal stem cell development. PLoS ONE 2012, 7:e37162.
34. Rahman M.M., Ng J.C., Naidu R. Chronic exposure of arsenic via drinking water and its adverse health impacts on humans. Environ. Geochem. Health 2009, 31(Suppl 1):189-200.
35. Rossman T.G. Mechanism of arsenic carcinogenesis: an integrated approach. Mutat. Res. 2003, 533:37-65.
36. Rossman T.G., Klein C.B. Genetic and epigenetic effects of environmental arsenicals. Metallomics 2011, 3:1135-1141.
37. Ruiz-Ramos R., Lopez-Carrillo L., Rios-Perez A.D., De Vizcaya-Ruíz A., Cebrian M.E. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-κB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2009, 674:109-115.
38. Saravanan B.C., Sreekumar C., Bansal G.C., Ray D., Rao J.R., Mishra A.K. A rapid MTT colorimetric assay to assess the proliferative index of two Indian strains of Theileria annulata. Vet. Parasitol. 2003, 113:211-216.
39. Schneider Y., Duranton B., Gosse F., Schleiffer R., Seiler N., Raul F. Resveratrol inhibits intestinal tumorigenesis and modulates host-defense-related gene expression in an animal model of human familial adenomatous polyposis. Nutr. Cancer 2001, 39:102-107.
40. Scott E., Steward W.P., Gescher A.J., Brown K. Resveratrol in human cancer chemoprevention - choosing the 'right' dose. Mol. Nutr. Food Res. 2012, 56:7-13.
41. Sgambato A., Ardito R., Faraglia B., Boninsegna A., Wolf F.I., Cittadini A. Resveratrol, a natural phenolic compound, inhibits cell proliferation and prevents oxidative DNA damage. Mutat. Res. 2001, 496:171-180.
42. Simon H.U., Haj-Yehia A., Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5:415-418.
43. Smith A.H., Hopenhayn-Rich C., Bates M.N., Goeden H.M., Hertz-Picciotto I., Duggan H.M., Wood R., Kosnett M.J., Smith M.T. Cancer risks from arsenic in drinking water. Environ. Health Perspect. 1992, 97:259-267.
44. Stakleff K.S., Sloan T., Blanco D., Marcanthony S., Booth T.D., Bishayee A. Resveratrol exerts differential effects in vitro and in vivo against ovarian cancer cells. Asian Pac. J. Cancer Preven. APJCP 2012, 13:1333-1340.
45. Stergiou L., Hengartner M.O. Death and more: DNA damage response pathways in the nematode C. elegans. Cell Death Differ. 2004, 11:21-28.
46. Thorsen M., Jacobson T., Vooijs R., Navarrete C., Bliek T., Schat H., Tamás M.J. Glutathione serves an extracellular defence function to decrease arsenite accumulation and toxicity in yeast. Mol. Microbiol. 2012, 84:1177-1188.
47. Tolbert P.E., Shy C.M., Allen J.W. Micronuclei and other nuclear anomalies in buccal smears: methods development. Mutat. Res. 1992, 271:69-77.
48. Wang T.-S., Kuo C.-F., Jan K.-Y., Huang H. Arsenite induces apoptosis in chinese hamster ovary cells by generation of reactive oxygen species. J. Cell. Physiol. 1996, 169:256-268.
49. Wang Z.F., Guo X. Arsenite-induced apoptosis is prevented by selenite in A375 cell line. Biol. Trace Elem. Res. 2011, 140:7-17.
50. Win W., Cao Z., Peng X., Trush M.A., Li Y. Different effects of genistein and resveratrol on oxidative DNA damage in vitro. Mutat. Res. 2002, 513:113-120.
51. Wu M., Zhang Z., Che W. Suppression of a DNA base excision repair gene, hOGG1, increases bleomycin sensitivity of human lung cancer cell line. Toxicol. Appl. Pharmacol. 2008, 228:395-402.
52. Wylie P.G., Bowen W.P. Determination of cell colony formation in a high-content screening assay. Clin. Lab. Med. 2007, 27:193-199.
53. Yahata T., Takanashi T., Muguruma Y., Ibrahim A.A., Matsuzawa H., Uno T., Sheng Y., Onizuka M., Ito M., Kato S., Ando K. Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 2011, 118:2941-2950.
54. Yen Y.P., Tsai K.S., Chen Y.W., Huang C.F., Yang R.S., Liu S.H. Arsenic induces apoptosis in myoblasts through a reactive oxygen species-induced endoplasmic reticulum stress and mitochondrial dysfunction pathway. Arch. Toxicol. 2012, 86:923-933.
55. Yih L.H., Tseng Y.Y., Wu Y.C., Lee T.C. Induction of centrosome amplification during arsenite-induced mitotic arrest in CGL-2 cells. Cancer Res. 2006, 66:2098-2106.
56. Zeng X., Dai J., Remick D.G., Wang X. Homocysteine mediated expression and secretion of monocyte chemoattractant protein-1 and interleukin-8 in human monocytes. Circ. Res. 2003, 93:311-320.
57. Zhang W., Xue J., Ge M., Yu M., Liu L., Zhang Z. Resveratrol attenuates hepatotoxicity of rats exposed to arsenic trioxide. Food Chem. Toxicol. Int. J. Published Brit. Ind. Biol. Res. Assoc. 2013, 51:87-92.
58. Zhang Z., Wang X., Cheng S., Sun L., Son Y.O., Yao H., Li W., Budhraja A., Li L., Shelton B.J., Tucker T., Arnold S.M., Shi X. Reactive oxygen species mediate arsenic induced cell transformation and tumorigenesis through Wnt/beta-catenin pathway in human colorectal adenocarcinoma DLD1 cells. Toxicol. Appl. Pharmacol. 2011, 256:114-121.
59. Zhao X.Y., Li G.Y., Liu Y., Chai L.M., Chen J.X., Zhang Y., Du Z.M., Lu Y.J., Yang B.F. Resveratrol protects against arsenic trioxide-induced cardiotoxicity in vitro and in vivo. Br. J. Pharmacol. 2008, 154:105-113.