Chronic exposure to combined carcinogens enhances breast cell carcinogenesis with mesenchymal and stemlike cell properties

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Pluchino, Lenora Ann ^a,b   Wang, Hwa Chain Robert ^a,b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ANTINEOPLASTIC AGENT; BENZO[A]PYRENE; CARCINOGEN; EPICATECHIN 3 GALLATE; EPIGALLOCATECHIN GALLATE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; UNCLASSIFIED DRUG; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; 4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; IMIDAZOLE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE; NITROSAMINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BREAST CARCINOGENESIS; BREAST CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER STEM CELL; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MCF 7 CELL LINE; MESENCHYME CELL; MONOTHERAPY; SIGNAL TRANSDUCTION; BREAST TUMOR; CARCINOGENESIS; DRUG EFFECTS; DRUG POTENTIATION; METABOLISM;

BENZO(A)PYRENE; BREAST NEOPLASMS; CARCINOGENESIS; CARCINOGENS; DNA DAMAGE; DRUG SYNERGISM; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMIDAZOLES; MCF-7 CELLS; NADPH OXIDASE; NITROSAMINES; RAS PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84910614563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108698     Document Type: Article

References (47)

1. Gray J, Evans N, Taylor B., Rizzo J, Walker M. (2009) State of the evidence: the connection between breast cancer and the environment. Int J Occup Env Health 15: 43-78.
2. Bray F, Ren JS, Masuyer E, Ferlay J. (2013) Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer 132: 1133-1145.
3. Guengerich FP (2000) Metabolism of chemical carcinogens. Carcinogenesis 21: 345-351.
4. Kelloff GJ, Hawk ET, Sigman C.C. (2005) Cancer chemoprevention: strategies for cancer chemoprevention. Vol 2. Totowa, New Jersey: Human Press. 528p.
5. DeBruin LS, Josephy P.D. (2002) Perspectives on the chemical etiology of breast cancer. Environ Health Perspect 110: 119-128.
6. Hecht SS (2002) Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen 39: 119-126.
7. Mehta RG (2000) Experimental basis for the prevention of breast cancer. Eur J Cancer 36: 1275-1282.
8. Sugimura T, Wakabayashi K, Nakagama H., Nagao M. (2004) Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci 95: 290-299.
9. Gooderham NJ, Creton S, Lauber S.N., Zhu H. (2007) Mechanisms of action of the carcinogenic heterocyclic amine PhIP. Toxicol Lett 168: 269-277.
10. Imaida K, Hagiwara A, Yada H., Masui T, Hasegawa R, et al (1996) Dose-dependent induction of mammary carcinomas in female Sprague-Dawley rats with 2-amino-1-methyl-6-phenylimidazol [4,5-b]pyridine. Jpn J Cancer Res 87: 1116-1120.
11. Nagao M, Ushijima T, Wakabayashi K., Ochiai M, Kushida H, et al (1994) Dietary carcinogens and mammary carcinogenesis. Induction of rat mammary carcinomas by administration of heterocyclic amines in cooked foods. Cancer 74: 1063-1069.
12. Zheng W, Lee S.A. (2009) Well-done meat intake, heterocyclic amine exposure, and cancer risk. Nutr Cancer 61: 437-446.
13. Zheng W, Gustafson DR, Sinha R, Hong C-P, Anderson KE, et al (1998) Well-done meat intake and the risk of breast cancer. J Natl Cancer Inst 90: 1724-1729.
14. Sinha R, Gustafson DR, Kulldorff M, Wen W.Q., Cerhan JR, et al. (2000) 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, a carcinogen in high-temperature-cooked meat, and breast cancer risk. J Natl Cancer Inst 92: 1352-1354.
15. Hecht SS (1988) Tobacco-specific nitrosamines, an important group of carcinogens in tobacco and tobacco smoke. Carcinogenesis 9: 875-884.
16. Hecht SS, Hoffman D. (1996) Recent studies on mechanisms of bioactivation and detoxification of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), a tobacco specific lung carcinogen. Crit Rev Toxicol 26: 163-181.
17. Hecht SS (1999) Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 91: 1194-1210.
18. Chhabra SK, Anderson LM, Perella C, Desai D., Amin S, et al. (2000) Coexposure to ethanol with N-nitrosodimethylamine or 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone during lactation of rats: Marked increase in O(6)-methylguanine-DNA adducts in maternal mammary gland and in suckling lung and kidney. Toxicol Appl Pharmacol 169: 191-200.
19. Ohnishi T, Fukamachi K, Ohshima Y., Jiegou X, Ueda S, et al (2007) Possible application of human c-Ha-ras proto-oncogene transgenic rats in a mediumterm bioassay model for carcinogens. Toxicol Pathol 35: 436-443.
20. Johnson KC, Miller AB, Collishaw N.E., Palmer JR, Hammond SK, et al. (2010) Active smoking and secondhand smoke increase breast cancer risk: the report of the Canadian Expert Panel on Tobacco Smoke and Breast Cancer Risk. Tobacco Control 20: e2.
21. Luo J, Margolis KL, Wactawski-Wende J, Horn K., Messina C, et al. (2011) Association of active and passive smoking with risk of breast cancer among postmenopausal women: A prospective cohort study. BMJ 342: d1016.
22. Hartz AJ, He T. (2013) Cohort study of risk factors for breast cancer in post menopausal women. Epidemiol Health 35: e2013003.
23. Rubin H (2001) Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: A bio-historical perspective with updates. Carcinogenesis 22: 1903-1930.
24. Obana H, Hori S, Kashimoto T., Kunita N. (1981) Polycyclic aromatic hydrocarbons in human fat and liver. Bull Environ Contam Toxicol 27: 23-27.
25. Rundle A, Tang D, Hibshoosh H., Estabrook A, Schnabel F, et al (2000) The relationship between genetic damage from polycyclic aromatic hydrocarbons in breast tissue and breast cancer. Carcinogenesis 21: 1281-1289.
26. Morris JJ, Seifter E. (1992) The role of aromatic hydrocarbons in the genesis of breast cancer. Med Hypotheses 38: 177-184.
27. Gammon MD, Santella RM, Neugut A.I., Eng SM, Teitelbaum SL, et al. (2002) Environmental toxins and breast cancer on Long Island. I. Polycyclic aromatic hydrocarbon DNA adducts. Cancer Epidemiol Biomarkers Prev 11: 677-685.
28. Gammon MD, Sagiv SK, Eng S.M., Shantakumar S., Gaudet MM, et al. (2004) Polycyclic aromatic hydrocarbon-DNA adducts and breast cancer: a pooled analysis. Arch Environ Health 59: 640-649.
29. Mei J, Hu H, McEntee M., Plummer H, Song P, et al (2003) Transformation of noncancerous human breast epithelial cell MCF10A induced by the tobacco-specific carcinogen NNK. Breast Cancer Res Treat 79: 95-105.
30. Siriwardhana N, Wang H.C. (2008) Precancerous carcinogenesis of human breast epithelial cells by chronic exposure to benzo[a]pyrene. Mol Carcinogenesis 47: 338-48.
31. Siriwardhana N, Choudhary S, Wang H.C. (2008) Precancerous model of human breast epithelial cells induced by the tobacco-specific carcinogen NNK for prevention. Breast Cancer Res Treat 109: 427-441.
32. Song X, Siriwardhana N, Rathore K., Lin D, Wang H.C. (2010) Grape seed proanthocyanidin suppression of breast cell carcinogenesis induced by chronic exposure to combined 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and benzo[a]pyrene. Mol Carcinogenesis 49: 450-463.
33. Rathore K, Wang H.C. (2012) Green tea catechin extract in intervention of chronic breast cell carcinogenesis induced by environmental carcinogens. Mol Carcinogenesis 51: 280-289.
34. Rathore K, Choudhary S, Odoi A., Wang H.C. (2012) Green tea catechin intervention of reactive oxygen species-mediated ERK pathway activation and chronically induced breast cell carcinogenesis. Carcinogenesis 33: 174-183.
35. Choudhary S, Sood S, Donnell R.L., Wang H.C. (2012) Intervention of human breast cell carcinogenesis chronically induced by 2-amino-1-methyl-6-phenyli-midazo-[4,5-b]pyridine. Carcinogenesis 33: 876-885.
36. Rathore K, Wang H.C. (2013) Mesenchymal and stem-like cell properties targeted in suppression of chronically-induced breast cell carcinogenesis. Cancer Lett 333: 113-123.
37. Hanahan D, Weinberg R.A. (2011) The hallmarks of cancer: the next generation. Cell 144: 646-674.
38. Olive PL, Banath J.P. (2006) The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 1: 23-29.
39. Datta S, Hoenerhoff MJ, Bommi P, Sainger R., Guo W-J, et al. (2007) Bmi-1 cooperates with H-Ras to transform human mammary epithelial cells via dysregulation of multiple growth-regulatory pathways. Cancer Res 67: 10286-10295.
40. Dontu G, Abdallah WM, Foley J.M., Jackson KW, Clarke MF, et al. (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17: 1253-1270.
41. Ginestier A, Hur MH, Charafe-Jauffret E, Monville F., Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
42. Litvinov SV, Balzar M, Winter M.J., Bakker HA, Briaire-de Bruijn IH, et al. (1997) Epithelial cell adhesion molecule (Ep-CAM) modulates cell-cell interactions mediated by classic cadherins. J Cell Biol 139: 1337-1348.
43. Vuoriluoto K, Haugen H, Kiviluoto S., Mpindi JP, Nevo J, et al. (2011) Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 30: 1436-1448.
44. Yang CS, Wang X, Lu G., Picinich S.C. (2009) Cancer prevention by tea: animal studies, molecular mechanisms and human relevance. Nat Rev Cancer 9: 429-439.
45. Kurbitz C, Heise D, Redmer T., Goumas F, Arlt A, et al (2011) Epicatechin gallate and catechin gallate are superior to epigallocatechin gallate in growth suppression and anti-inflammatory activities in pancreatic tumor cells. Cancer Sci 102: 728-734.
46. Pan MH, Chiou YS, Wang Y.J., Ho CT, Lin J.K. (2011) Multistage carcinogenesis process as molecular targets in cancer chemoprevention by epicatechin-3-gallate. Food Funct 2: 101-10.
47. Al-Ejeh F., Smart CE, Morrison B.J., Chenevix-Trench G, López JA, et al. (2011) Breast cancer stem cells: treatment resistance and therapeutic opportunities. Carcinogenesis 32: 650-8.