Estrogen promotes benzo[a]pyrene-induced lung carcinogenesis through oxidative stress damage and cytochrome c-mediated caspase-3 activation pathways in female mice

Cancer Letters

Volumn 308, Issue 1, 2011, Pages 14-22

  Chen, Zhaoli ^a   Zhang, Yunxiao ^b   Yang, Jie ^c   Jin, Min ^a   Wang, Xin Wei ^a   Shen, Zhi Qiang ^a   Qiu, Zhigang ^a   Zhao, Guofan ^b   Wang, Jingfeng ^a   Li, Jun Wen ^a  

^a INSTITUTE OF HEALTH AND ENVIRONMENTAL MEDICINE   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Benzo a pyrene; Estrogen; Lung cancer; Mitochondrial pathway; Oxidative stress damage

Indexed keywords

BENZO[A]PYRENE; CASPASE 3; CYTOCHROME C; ESTRADIOL; ESTROGEN; PROTEIN BAX; PROTEIN BCL 2; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVATION; FEMALE; GENE SEQUENCE; HORMONE ACTION; LUNG CANCER; LUNG CARCINOGENESIS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; BENZO(A)PYRENE; CASPASE 3; CYTOCHROMES C; DISEASE MODELS, ANIMAL; DNA DAMAGE; DRUG SYNERGISM; ENZYME ACTIVATION; ESTRADIOL; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; MITOCHONDRIA; OXIDATIVE STRESS; RANDOM ALLOCATION;

MUS;

EID: 79958173705     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.04.007     Document Type: Article

References (68)

1. Edwards B.K., Brown M.L., Wingo P.A., Howe H.L., Ward E., Ries L.A., Schrag D., Jamison P.M., Jemal A., Wu X.C., Friedman C., Harlan L., Warren J., Anderson R.N., Pickle L.W. Annual report to the nation on the status of cancer, 1975-2002. Featuring population-based trends in cancer treatment. J. Natl. Cancer Inst. 2005, 97:1407-1427.
2. Jemal A., Siegel R., Ward E., Murray T., Xu J., Smigal C., Thun M.J. Cancer statistics, 2006. CA. Cancer J. Clin. 2006, 56(2006):106-130.
3. Koyi H., Hillerdal G., Branden E. A prospective study of a total material of lung cancer from a county in Sweden 1997-1999: gender, symptoms, type, stage, and smoking habits. Lung Cancer 2002, 36:9-14.
4. Yang L., Li L., Chen Y., Parkin D.M. Mortality time trends and the incidence and mortality estimation and projection for lung cancer in China. Zhongguo Fei Ai Za Zhi 2005, 8:274-278.
5. Henschke C.I., Yip R., Miettinen O.S. Women's susceptibility to tobacco carcinogens and survival after diagnosis of lung cancer. JAMA 2006, 296:180-184.
6. Doll R., Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J. Natl. Cancer Inst. 1981, 66:1191-1308.
7. Hammond E.C. Smoking in relation to the death rates of one million men and women. Natl. Cancer Inst. Monogr. 1966, 19:127-204.
8. Zang E.A., Wynder E.L. Differences in lung cancer risk between men and women: examination of the evidence. J. Natl. Cancer Inst. 1996, 88:183-192.
9. Bray F.I., Weiderpass E. Lung cancer mortality trends in 36 European countries: secular trends and birth cohort patterns by sex and region 1970-2007. Int. J. Cancer 2010, 126:1454-1466.
10. Kreuzer M., Boffetta P., Whitley E., Ahrens W., Gaborieau V., Heinrich J., Jockel K.H., Kreienbrock L., Mallone S., Merletti F., Roesch F., Zambon P., Simonato L. Gender differences in lung cancer risk by smoking: a multicentre case-control study in Germany and Italy. Brit. J. Cancer 2000, 82:227-233.
11. Thun M.J., Henley S.J., Calle E.E. Tobacco use and cancer: an epidemiologic perspective for geneticists. Oncogene 2002, 21:7307-7325.
12. Yang J., Wang L., Chen Z., Shen Z.Q., Jin M., Wang X.W., Zheng Y., Qiu Z.G., Wang J.F., Li J.W. Antioxidant intervention of smoking-induced lung tumor in mice by vitamin E and quercetin. BMC Cancer 2008, 8:383.
13. Kreuzer M., Gerken M., Heinrich J., Kreienbrock L., Wichmann H.E. Hormonal factors and risk of lung cancer among women?. Int. J. Epidemiol. 2003, 32:263-271.
14. Qing C., Chen Y.Z., Du Y.X. The trends in historical types of lung cancer during 1980-1988, Guangzhou, China. Lung Cancer 1997, 17:219-230.
15. Yang P., Cerhan J.R., Vierkant R.A., Olson J.E., Vachon C.M., Limburg P.J., Parker A.S., Anderson K.E., Sellers T.A. Adenocarcinoma of the lung is strongly associated with cigarette smoking: further evidence from a prospective study of women. Am. J. Epidemiol. 2002, 156:1114-1122.
16. Stabile L.P., Siegfried J.M. Estrogen receptor pathways in lung cancer. Curr. Oncol. Rep. 2004, 6:259-267.
17. Stabile L.P., Davis A.L., Gubish C.T., Hopkins T.M., Luketich J.D., Christie N., Finkelstein S., Siegfried J.M. Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor alpha and beta and show biological responses to estrogen. Cancer Res. 2002, 62:2141-2150.
18. Alexandrov K., Rojas M., Satarug S. The critical DNA damage by benzo(a)pyrene in lung tissues of smokers and approaches to preventing its formation. Toxicol. Lett. 2010, 198:63-68.
19. Hecht S.S., Kenney P.M., Wang M., Upadhyaya P. Dose-response study of myo-inositol as an inhibitor of lung tumorigenesis induced in A/J mice by benzo[a]pyrene and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Cancer Lett. 2001, 167:1-6.
20. Selvendiran K., Prince Vijeya Singh J., Sakthisekaran D. In vivo effect of piperine on serum and tissue glycoprotein levels in benzo(a)pyrene induced lung carcinogenesis in Swiss albino mice. Pulm. Pharmacol. Ther. 2006, 19:107-111.
21. Nesnow S., Nelson G., Padgett W.T., George M.H., Moore T., King L.C., Adams L.D., Ross J.A. Lack of contribution of covalent benzo[a]pyrene-7,8-quinone-DNA adducts in benzo[a]pyrene-induced mouse lung tumorigenesis. Chem. Biol. Interact. 2010, 186:157-165.
22. Carey M.A., Card J.W., Voltz J.W., Arbes S.J., Germolec D.R., Korach K.S., Zeldin D.C. It's all about sex: gender, lung development and lung disease. Trends Endocrinol. Metab. 2007, 18:308-313.
23. Taioli E., Wynder E.L. Re: endocrine factors and adenocarcinoma of the lung in women. J. Natl. Cancer Inst. 1994, 86:869-870.
24. Patel J.D., Bach P.B., Kris M.G. Lung cancer in US women. A contemporary epidemic. JAMA 2004, 291:1763-1768.
25. Hershberger P.A., Vasquez A.C., Kanterewicz B., Land S., Siegfried J.M., Nichols M. Regulation of endogenous gene expression in human non-small cell lung cancer cells by estrogen receptor ligands. Cancer Res. 2005, 65:1598-1605.
26. Bird C.E., Masters V., Sterns E.E., Clark A.F. Effects of Tamoxifen on testosteron metabolism in postmenopausal women with breast cancer. Clin. Invest. Med. 1985, 8:97-102.
27. Speirs V., Kerin M.J., Walton D.S., Newton C.S., Desai S.B., Atkin S.L. Direct activation of oestrogen receptor-alpha by interleukin-6 in primary cultures of breast cancer epithelial cells. Brit. J. Cancer 2000, 82:1312-1316.
28. Osborne C.K. Tamoxifen in the treatment of breast cancer. New Engl. J. Med. 1998, 339:1609-1618.
29. Hecht S.S., Isaacs S., Trushin N. Lung tumor induction in A/J mice by the tobacco smoke carcinogens 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and benzo[a]pyrene: a potentially useful model for evaluation of chemopreventive agents. Carcinogenesis 1994, 15:2721-2725.
30. Sticha K.R., Kenney P.M., Boysen G., Liang H., Su X., Wang M., Upadhyaya P., Hecht S.S. Effects of benzyl isothiocyanate and phenethyl isothiocyanate on DNA adduct formation by a mixture of benzo[a]pyrene and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in A/J mouse lung. Carcinogenesis 2002, 23:1433-1439.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
32. Kaiserman M.J., Rickert W.S. Carcinogens in tobacco smoke: benzo[a]pyrene from Canadian cigarettes and cigarette tobacco. Am. J. Public Health 1992, 82:1023-1026.
33. Hecht S.S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 1999, 91:1194-1210.
34. Jiang Y.G., Chen J.K., Wu Z.L. Promotive effect of diethylstilbestrol on urethan-induced mouse lung tumorigenesis. Chemosphere 2000, 41:187-190.
35. Singh S.V., Benson P.J., Hu X., Pal A., Xia H., Srivastava S.K., Awasthi S., Zaren H.A., Orchard J.L., Awasthi Y.C. Gender-related differences in susceptibility of A/J mouse to benzo[a]pyrene-induced pulmonary and forestomach tumorigenesis. Cancer Lett. 1998, 128:197-204.
36. Li J.J., Mueller G.C., Sekely L.I. Workshop report from the Division of Cancer Etiology, National Cancer Institute, National Institutes of Health. Current perspectives and future trends in hormonal carcinogenesis. Cancer Res. 1991, 51:3626-3629.
37. Gao F.M., Jiang H.Y., Yu L. Studies on mechanisms, antagonistic methods for female hormones carcinogenesis. Chinese Sci., B ed. 1993, 23:283.
38. Anandakumar P., Kamaraj S., Jagan S., Ramakrishnan G., Vinodhkumar R., Devaki T. Capsaicin modulates pulmonary antioxidant defense system during benzo(a)pyrene-induced lung cancer in Swiss albino mice. Phytother. Res. 2008, 22:529-533.
39. Kim K.B., Lee B.M. Oxidative stress to DNA, protein, and antioxidant enzymes (superoxide dismutase and catalase) in rats treated with benzo(a)pyrene. Cancer Lett. 1997, 113:205-212.
40. Rajendran P., Ekambaram G., Sakthisekaran D. Cytoprotective effect of mangiferin on benzo(a)pyrene-induced lung carcinogenesis in swiss albino mice. Basic Clin. Pharmacol. Toxicol. 2008, 103:137-142.
41. Samarth R.M., Panwar M., Kumar A. Modulatory effects of Mentha piperita on lung tumor incidence, genotoxicity, and oxidative stress in benzo[a]pyrene-treated Swiss albino mice. Environ. Mol. Mutagen 2006, 47:192-198.
42. Mense S.M., Singh B., Remotti F., Liu X., Bhat H.K. Vitamin C and alpha-naphthoflavone prevent estrogen-induced mammary tumors and decrease oxidative stress in female ACI rats. Carcinogenesis 2009, 30:1202-1208.
43. Singh B., Mense S.M., Remotti F., Liu X., Bhat H.K. Antioxidant butylated hydroxyanisole inhibits estrogen-induced breast carcinogenesis in female ACI rats. J. Biochem. Mol. Toxicol. 2009, 23:202-211.
44. Borras C., Gambini J., Lopez-Grueso R., Pallardo F.V., Vina J. Direct antioxidant and protective effect of estradiol on isolated mitochondria. Biochim. Biophys. Acta 2010, 1802:205-211.
45. Topcuoglu A., Uzun H., Balci H., Karakus M., Coban I., Altug T., Aydin S., Topcuoglu D., Cakatay U. Effects of estrogens on oxidative protein damage in plasma and tissues in ovariectomised rats. Clin. Invest. Med. 2009, 32:E133-143.
46. Mukherjee J.J., Gupta S.K., Sikka H., Kumar S. Inhibition of benzopyrene-diol-epoxide (BPDE)-induced bax and caspase-9 by cadmium: role of mitogen activated protein kinase. Mutat. Res. 2009, 661:41-46.
47. Movassagh M., Foo R.S. Simplified apoptotic cascades. Heart Fail. Rev. 2008, 13:111-119.
48. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
49. Liu X.Y., Yang Z.H., Pan X.J., Zhu M.X., Xie J.P. Crotonaldehyde induces oxidative stress and caspase-dependent apoptosis in human bronchial epithelial cells. Toxicol. Lett. 2010, 195:90-98.
50. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 1997, 326(Pt 1):1-16.
51. Ko C.B., Kim S.J., Park C., Kim B.R., Shin C.H., Choi S., Chung S.Y., Noh J.H., Jeun J.H., Kim N.S., Park R. Benzo(a)pyrene-induced apoptotic death of mouse hepatoma Hepa1c1c7 cells via activation of intrinsic caspase cascade and mitochondrial dysfunction. Toxicology 2004, 199:35-46.
52. Albright C.D., Borgman C., Craciunescu C.N. Activation of a caspase-dependent oxidative damage response mediates TGFbeta1 apoptosis in rat hepatocytes. Exp. Mol. Pathol. 2003, 74:256-261.
53. Shi H., Hudson L.G., Liu K.J. Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radic. Biol. Med. 2004, 37:582-593.
54. Storz P. Reactive oxygen species in tumor progression. Front. Biosci. 2005, 10:1881-1896.
55. Franco R., Sánchez-Olea R., Reyes-Reyes E.M., Panayiotidis M.I. Environmental toxicity, oxidative stress and apoptosis: ménage à trois. Mutat. Res. 2009, 674:3-22.
56. Cullinan S.B., Diehl J.A. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 2006, 38:317-332.
57. Conaway C.C., Nie G., Hussain N.S., Fiala E.S. Comparison of oxidative damage to rat liver DNA and RNA by primary nitroalkanes, secondary nitroalkanes, cyclopentanone oxime, and related compounds. Cancer Res. 1991, 51:3143-3147.
58. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 1992, 267:166-172.
59. Ames B.N., Gold L.S. Animal cancer tests and cancer prevention. J. Natl. Cancer Inst. Monogr. 1992, 12:125-132.
60. Guyton K.Z., Kensler T.W. Oxidative mechanisms in carcinogenesis. Brit. Med. Bull. 1993, 49:523-544.
61. Schulte-Hermann R., Timmermann-Trosiener I., Barthel G., Bursch W. DNA synthesis, apoptosis, and phenotypic expression as determinants of growth of altered foci in rat liver during phenobarbital promotion. Cancer Res. 1990, 50:5127-5135.
62. Klaunig J.E., Xu Y., Isenberg J.S., Bachowski S., Kolaja K.L., Jiang J., Stevenson D.E., Walborg E.F. The role of oxidative stress in chemical carcinogenesis. Environ. Health Perspect. 1998, 106(Suppl. 1):289-295.
63. Reuter S., Gupta S.C., Chaturvedi M.M., Aggarwal B.B. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 2010, 49:1603-1616.
64. Long Gerald G., Cohen Ilene R., Gries Christian L., Young Jamie K., Francis Paul C., Capen C.C. Proliferative lesions of ovarian granulosa cells and reversible hormonal changes induced in rats by a selective estrogen receptor modulator. Toxicol. Pathol. 2001, 29:719-726.
65. Kennel C., Pallen E., Barale-Thomas G., Espuna R., Bars Tamoxifen. 28-day oral toxicity study in the rat based on the Enhanced OECD Test Guideline 407 to detect endocrine effects. Arch. Toxicol. 2003, 77:487-499.
66. Li Z., Carrier L., Rowan B.G. Methylseleninic acid synergizes with tamoxifen to induce caspase-mediated apoptosis in breast cancer cells. Mol. Cancer Ther. 2008, 7:3056-3063.
67. Parvez S., Tabassum H., Rehman H., Banerjee B.D., Athar M., Raisuddin S. Catechin prevents tamoxifen-induced oxidative stress and biochemical perturbations in mice. Toxicology 2006, 225:109-118.
68. Siedlakowski P., McLachlan-Burgess A., Griffin C., Tirumalai S.S., McNulty J., Pandey S. Synergy of pancratistatin and tamoxifen on breast cancer cells in inducing apoptosis by targeting mitochondria. Cancer Biol. Ther. 2008, 7:376-384.