Aflatoxin G1-induced oxidative stress causes DNA damage and triggers apoptosis through MAPK signaling pathway in A549 cells

Food and Chemical Toxicology

Volumn 62, Issue , 2013, Pages 661-669

  Shen, Haitao ^a   Liu, Jing ^a   Wang, Yuan ^a   Lian, Hongguang ^a   Wang, Juan ^a   Xing, Lingxiao ^a   Yan, Xia ^a   Wang, Junling ^a   Zhang, Xianghong ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

Author keywords

Aflatoxin; Alveolar type II cells; Apoptosis; Mitogen activated protein kinases; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; AFLATOXIN G1; CASPASE 3; CASPASE 8; FAS ANTIGEN; FAS LIGAND; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; AFLATOXIN; BAX PROTEIN, HUMAN;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; ENZYME ACTIVATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TOXIN ANALYSIS; UPREGULATION; ALVEOLAR TYPE II CELLS; DRUG EFFECT; METABOLISM; TUMOR CELL LINE;

AFLATOXIN; ALVEOLAR TYPE II CELLS; APOPTOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATIVE STRESS;

ACETYLCYSTEINE; AFLATOXINS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE, TUMOR; DNA DAMAGE; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES;

EID: 84886280182     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.09.030     Document Type: Article

References (49)

1. Abdel-Wahhab M.A., Aly S.E. Antioxidants and radical scavenging properties of vegetable extracts in rats fed aflatoxin-contaminated diet. J. Agric. Food Chem. 2003, 51:2409-2414.
2. Bintvihok A., Ponpornpisit A., Tangtrongpiros J., Panichkriangkrai W., Rattanapanee R., Doi K., Kumagai S. Aflatoxin contamination in shrimp feed and effects of aflatoxin addition to feed on shrimp production. J. Food Prot. 2003, 66:882-885.
3. Benhar M., Dalyot I., Engelberg D., Levitzki A. Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol. Cell Biol. 2001, 21:6913-6926.
4. Bosco E.E., Mayhew C.N., Hennigan R.F., Sage J., Jacks T., Knudsen E.S. RB signaling prevents replication-dependent DNA double-strand breaks following genotoxic insult. Nucleic Acids Res. 2004, 32:25-34.
5. Brahmi D., Bouaziz C., Ayed Y., Ben Mansour H., Zourgui L., Bacha H. Chemopreventive effect of cactus Opuntia ficus indica on oxidative stress and genotoxicity of aflatoxin B1. Nutr. Metab (Lond). 2011, 18:73.
6. Chaudhari M., Jayaraj R., Bhaskar A.S., Lakshmana Rao P.V. Oxidative stress induction by T-2 toxin causes DNA damage and triggers apoptosis via caspase pathway in human cervical cancer cells. Toxicology 2009, 262:153-161.
7. Chuang C.Y., Chen T.L., Cherng Y.G., Tai Y.T., Chen T.G., Chen R.M. Lipopolysaccharide induces apoptotic insults to human alveolar epithelial A549 cells through reactive oxygen species-mediated activation of an intrinsic mitochondrion - dependent pathway. Arch Toxicol. 2011, 85(3):209-218.
8. De Paepe M.E., Mao Q., Chao Y., Powell J.L., Rubin L.P., Sharma S. Hyperoxia-induced apoptosis and Fas/FasL expression in lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2005, 289:647-L659.
9. Donnelly P.J., Devereux T.R., Foley J.F., Maronpot R.R., Anderson M.W., Massey T.E. Activation of K-ras in aflatoxin B1-induced lung tumors from AC3F1 (A/J×C3H/HeJ) mice. Carcinogenesis 1996, 17:1735-1740.
10. Espinoza L.A., Tenzin F., Cecchi A.O., Chen Z., Witten M.L., Smulson M.E. Expression of JP-8-induced inflammatory genes in AEII cells is mediated by NF kappaB and PARP-1. Am. J. Respir. Cell Mol. Biol. 2006, 35:479-487.
11. Fazekas B., Tar A., Kovacs M. Aflatoxin and ochratoxin A content of spices in Hungary. Food Addit. Contam. 2005, 22:856-863.
12. Groopman J.D., Kensler T.W. Role of metabolism and viruses in aflatoxin-induced liver cancer. Toxicol. Appl. Pharmacol. 2005, 206:131-137.
13. Guindon K.A., Bedard L.L., Massey T.E. Elevation of 8-hydroxydeoxyguanosine in DNA from isolated mouse lung cells following in vivo treatment with aflatoxin B (1). Toxicol. Sci. 2007, 98:57-62.
14. He Z., Ma W.Y., Hashimoto T., Bode A.M., Yang C.S., Dong Z. Induction of apoptosis by caffeine is mediated by the p53, Bax, and caspase 3 pathways. Cancer Res. 2003, 63:4396-4401.
15. Huang X.H., Zhang X.H., Li Y.H., Wang J.L., Yan X., Xing L.X., Wang F.R. ExperimentalPlease check whether the references 'Huang et al. (2004), Shen et al. (2005) and Zhang et al. (2003)' are okay as typeset, and correct if necessary. lung carcinogenic in vivo study of aflatoxin G1 in NIH mice. Zhonghua Bing Li Xue Za Zhi. 2004, 33:260-263.
16. Jin D., Ojcius D.M., Sun D., Dong H., Luo Y., Mao Y., Yan J. Leptospira interrogans induces apoptosis in macrophages via caspase-8- and caspase-3-dependent pathways. Infect Immun. 2009, 77(2):799-809.
17. Kannan S., Wu M. Respiratory stem cells and progenitors: overview, derivation, differentiation, carcinogenesis, regeneration and therapeutic application. Curr. Stem Cell Res. Ther. 2006, 1:37-46.
18. Ki Y.W., Park J.H., Lee J.E. Shin IC., Koh HC. JNK and p38 MAPK regulate oxidative stress and the inflammatory response in chlorpyrifos-induced apoptosis. Toxicol. Lett. 2013, 218(3):235-245.
19. Kirby J.E. Anthrax lethal toxin induces human endothelial cell apoptosis. Infect Immun. 2004, 72(1):430-439.
20. Kleinsasser N.H., Wallner B.C., Harréus U.A., Zwickenpflug W., Richter E. Genotoxic effects of myosmine in human lymphocytes and upper aerodigestive tract epithelial cells. Toxicology 2003, 192:171-177.
21. Krokan H.E., Standal R., Slupphaug G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 1997, 325:1-16.
22. LaChapelle A.M., Ruygrok M.L., Toomer M., Oost J.J., Monnie M.L., Swenson J.A., Compton A.A., Stebbins-Boaz B. The hormonal herbicide, 2,4-dichlorophenoxyacetic acid, inhibits Xenopus oocyte maturation by targetingtranslational and post-translational mechanisms. Reprod. Toxicol. 2007, 23:20-31.
23. Lan A.P., Xiao L.C., Yang Z.L., Yang C.T., Wang X.Y., Chen P.X., Gu M.F., Feng J.Q. Interaction between ROS and p38MAPK contributes to chemical hypoxia-induced injuries in PC12 cells. Mol. Med. Rep. 2012, 5(1):250-255.
24. Liao W., McNutt M.A., Zhu W.G. The Comet assay: a sensitive method for detecting DNA damage in individual cells. Methods 2009, 48:46-53.
25. Lei K., Nimnual A., Zong W.X. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH (2)-terminal kinase. Mol. Cell Biol. 2002, 22:4929-4942.
26. Lu T.H., Chen C.H., Lee M.J., Ho T.J., Leung Y.M., Hung D.Z., Yen C.C., He T.Y., Chen Y.W. Methylmercury chloride induces alveolar type II epithelial cell damage through an oxidative stress-related mitochondrial cell death pathway. Toxicol. Lett. 2010, 194:70-78.
27. Lyle P.A., Mitsopoulos P., Suntres Z.E. n-Acetylcysteine modulates the cytotoxic effects of paclitaxel. Chemotherapy 2011, 57:289-304.
28. Mason R.J., Kalina M., Nielsen L.D., Malkinson A.M., Shannon J.M. Surfactant protein C expression in urethane-induced murine pulmonary tumors. Am. J. Pathol. 2000, 156:175-182.
29. Massey T.E., Smith G.B., Tam A.S. Mechanism of aflatoxin B1 lung tumorigenesis. Exp. Lung Res. 2000, 26:673-683.
30. Mazaheri M. Determination of aflatoxins in imported rice to Iran. Food Chem. Toxicol. 2009, 47:2064-2066.
31. Mills K.D., Ferguson D.O., Alt F.W. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 2003, 194:77-95.
32. Pan J., Chang Q., Wang X., Son Y., Zhang Z., Chen G., Luo J., Bi Y., Chen F., Shi X. Reactive oxygen species-activated Akt/ASK1/p38 signaling pathway in nickel compound-induced apoptosis in BEAS 2B cells. Chem. Res. Toxicol. 2010, 23:568-577.
33. Platt J.A., De Martini J.C. Alveolar type II cells expressing jaagsiekte sheep retrovirus capsid protein and surfactant proteins are the predominant neoplastic cell type in ovine pulmonary adenocarcinoma. Vet. Pathol. 2002, 39:341-352.
34. Ravindran J., Gupta N., Agrawal M., Bala Bhaskar A.S., Lakshmana Rao P.V. Modulation of ROS/MAPK signaling pathways by okadaic acid leads to cell death via, mitochondrial mediated caspase-dependent mechanism. Apoptosis 2011, 16:145-161.
35. Salnikow K., Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic, and chromium. Chem. Res. Toxicol. 2008, 21:28-44.
36. Shashi B., Jaswant S., Madhusudana R.J., Kumar S.A., Nabi Q.G. A novel lignan composition from Cedrus deodara induces apoptosis and early nitric oxide generation in human leukemia Molt-4 and HL-60 cells. Nitric Oxide. 2006, 14:72-88.
37. 1 in rat lungs. Food Chem. Toxicol. 2012, 50(9):3222-3228.
38. Shen H.T., Zhang X.H., Huang X.H., Li Y.H., Wang J., Yan X., Wang F. Histogenesis of lung adenocarcinoma induced by oral adminstration of mycotoxins in mice. Wei Sheng Yan Jiu 2005, 34:341-344.
39. Shen M., Lan Q., Zhang L., Chanock S., Li G., Vermeulen R., Rappaport S.M., Guo W., Hayes R.B., Linet M., Yin S., Yeager M., Welch R., Forrest M.S., Rothman N., Smith M.T. Polymorphisms in genes involved in DNA double-strand break repair pathway and susceptibility to benzene-induced hematotoxicity. Carcinogenesis 2006, 27:2083-2089.
40. Sigaud S., Evelson P., González-Flecha B. H2O2-induced proliferation of primary alveolar epithelial cells is mediated by MAP kinases. Antioxid Redox Signal. 2005, 7(1-2):6-13.
41. Ting C.M., Lee Y.M., Wong C.K., Wong A.S., Lung H.L., Lung M.L., Lo K.W., Wong R.N., Mak N.K. 2-Methoxyestradiol induces endoreduplication through the induction of mitochondrial oxidative stress and the activation of MAPK signaling pathways. Biochem. Pharmacol. 2010, 79:825-841.
42. Van der Toorn M., Rezayat D., Kauffman H.F., Bakker S.J., Gans R.O., Koeter G.H., Choi A.M., van Oosterhout A.J., Slebos D.J. Lipid-soluble components in cigarette smoke induce mitochondrial production of reactive oxygen species in lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2009, 297:109-114.
43. Vulimiri S.V., Misra M., Hamm J.T., Mitchell M., Berger A. Effects of main-stream cigarette smoke on the global metabolome of human lung epithelial cells. Chem. Res. Toxicol. 2009, 22:492-503.
44. Wang H., Yadav J.S. DNA damage, redox changes, and associated stress- inducible signaling events underlying the apoptosis and cytotoxicity in murine alveolar macrophage cell line MH-S by methanol-extracted Stachybotrys chartarum toxins. Toxicol. Appl. Pharmacol. 2006, 214:297-308.
45. Wang X., Martindale J.L., Liu Y., Holbrook N.J. The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem. J. 1998, 333:291-300.
46. Xie H., Wise S.S., Holmes A.L., Xu B., Wakeman T.P., Pelsue S.C., Singh N.P., Wise J.P. Carcinogenic lead chromate induces DNA double-strand breaks in human lung cells. Mutat. Res. 2005, 586:160-172.
47. Zhang X., Vallabhaneni R., Loughran P.A., Shapiro R., Yin X.M., Yuan Y., Billiar T.R. Changes in FADD levels, distribution, and phosphorylation in TNFalpha-induced apoptosis in hepatocytes is caspase-3, caspase-8 and BID dependent. Apoptosis 2008, 13:983-992.
48. Zhang X., Wang F., Wang J., Yan X., Huang X., Xie T., Zhang Z. Experimental lung carcinoma induced by fungi and mycotoxins - a review. Beijing Da Xue Xue Bao 2003, 35:4-6.
49. Zhuo W., Tao G., Zhang L., Chen Z. Vector-mediated selective expression of lethal factor, a toxic element of Bacillus anthracis, damages A549 cells via inhibition of MAPK and AKT pathways. Int. J. Med. Sci. 2013, 10(3):292-298.