Reversal and prevention of arsenic-induced human bronchial epithelial cell malignant transformation by microRNA-200b

Toxicological Sciences

Volumn 121, Issue 1, 2011, Pages 110-122

  Wang, Zhishan ^a   Zhao, Yong ^a   Smith, Eric ^b   Goodall, Gregory J ^b   Drew, Paul A ^c   Brabletz, Thomas ^d   Yang, Chengfeng ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c FLINDERS UNIVERSITY   (Australia)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Arsenic; Cell transformation; Chemical carcinogenesis; miRNA 200; ZEB

Indexed keywords

AGAR; ARSENIC; ARSENIC TRIOXIDE; MICRORNA; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CARCINOGENESIS; CELL IMMORTALIZATION; CELL TRANSFORMATION; COLONY FORMATION; CONTROLLED STUDY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MESENCHYME CELL; MOUSE; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

MUS MUSCULUS;

EID: 79955373842     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr029     Document Type: Article

References (45)

1. Arita, A., and Costa, M. (2009). Epigenetics in metal carcinogenesis: Nickel, Arsenic, Chromium and Cadmium. Metallomics 1, 222-228.
2. Benbrahim-Tallaa, L., and Waalkes, M. P. (2008). Inorganic arsenic and human prostate cancer. Environ. Health Perspect. 116, 158-164.
3. Beyersmann, D., and Hartwig, A. (2008). Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch. Toxicol. 82, 493-512.
4. Bracken, C. P., Gregory, P. A., Kolesnikoff, N., Bert, A. G., Wang, J., Shannon, M. F., and Goodall, G. J. (2008). A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial- mesenchymal transition. Cancer Res. 68, 7846-7854.
5. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589.
6. Calin, G. A., and Croce, C. M. (2006). MicroRNA signatures in human cancers. Nat. Rev. Cancer. 6, 857-866.
7. Celik, I., Gallicchio, L., Boyd, K., Lam, T. K., Matanoski, G., Tao, X., Shiels, M., Hammond, E., Chen, L., Robinson, K. A., et al. (2008). Arsenic in drinking water and lung cancer: a systematic review. Environ. Res. 108, 48-55.
8. Ceppi, P., Mudduluru, G., Kumarswamy, R., Rapa, I., Scagliotti, G. V., Papotti, M., and Allgayer, H. (2010). Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol. Cancer Res. 8, 1207-1216.
9. Chen, T. (2010). The role of MicroRNA in chemical carcinogenesis. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 28, 89-124.
10. Damiani, L. A., Yingling, C. M., Leng, S., Romo, P. E., Nakamura, J., and Belinsky, S. A. (2008). Carcinogen-induced gene promoter hypermethyla- tion is mediated by DNMT1 and causal for transformation of immortalized bronchial epithelial cells. Cancer Res. 68, 9005-9014.
11. Gaur, A., Jewell, D. A., Liang, Y., Ridzon, D., Moore, J. H., Chen, C., Ambros, V. R., and Israel, M. A. (2007). Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 67, 2456-2468.
12. Gibbons, D. L., Lin, W., Creighton, C. J., Rizvi, Z. H., Gregory, P. A., Goodall, G. J., Thilaganathan, N., Du, L., Zhang, Y., Pertsemlidis, A., et al. (2009). Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev. 23, 2140-2151.
13. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601.
14. Hernandez, L. G., van Steeg, H., Luijten, M., and van Benthem, J. (2009). Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach. Mutat. Res. 682, 94-109.
15. Hobert, O. (2008). Gene regulation by transcription factors and microRNAs. Science 319, 1785-1786.
16. Jiang, Y., Wu, Y., Greenlee, A. R., Wu, J., Han, Z., Li, X., and Zhao, Y. (2011). miR-106a-mediated malignant transformation of cells induced by anti-benzo[a]pyrene-trans-7,8-diol-9,10-epoxide. Toxicol. Sci. 119, 50-60.
17. Kitchin, K. T., and Conolly, R. (2010). Arsenic-induced carcinogenesis- oxidative stress as a possible mode of action and future research needs for more biologically based risk assessment. Chem. Res. Toxicol. 23, 327-335.
18. Korpal, M., Lee, E. S., Hu, G., and Kang, Y. (2008). The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283, 14910-14914.
19. Kumar, M. S., Lu, J., Mercer, K. L., Golub, T. R., and Jacks, T. (2007). Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673-677.
20. Lee, J. M., Dedhar, S., Kalluri, R., and Thompson, E. W. (2006). The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172, 973-981.
21. Li, A., Omura, N., Hong, S. M., Vincent, A., Walter, K., Griffith, M., Borges, M., and Goggins, M. (2010). Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res. 70, 5226-5237.
22. Liao, W. T., Lin, P., Cheng, T. S., Yu, H. S., and Chang, L. W. (2007). Arsenic promotes centrosome abnormalities and cell colony formation in p53 compromised human lung cells. Toxicol. Appl. Pharmacol. 225, 162-170.
23. Liu, F., Killian, J. K., Yang, M., Walker, R. L., Hong, J. A., Zhang, M., Davis, S., Zhang, Y., Hussain, M., Xi, S., et al. (2010). Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene 29, 3650-3664.
24. Liu, J., and Waalkes, M. P. (2008). Liver is a target of arsenic carcinogenesis. Toxicol. Sci. 105, 24-32.
25. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715.
26. Marsit, C. J., Eddy, K., and Kelsey, K. T. (2006). MicroRNA responses to cellular stress. Cancer Res. 66, 10843-10848.
27. Miska, E. A. (2005). How microRNAs control cell division, differentiation and death. Curr. Opin. Genet. Dev. 15, 563-568.
28. Ohashi, S., Natsuizaka, M., Wong, G. S., Michaylira, C. Z., Grugan, K. D., Stairs, D. B., Kalabis, J., Vega, M. E., Kalman, R. A., Nakagawa, M., et al. (2010). Epidermal growth factor receptor and mutant p53 expand an esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors. Cancer Res. 70, 4174-4184.
29. Peinado, H., Olmeda, D., and Cano, A. (2007). Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer. 7, 415-428.
30. Ramirez, R. D., Sheridan, S., Girard, L., Sato, M., Kim, Y., Pollack, J., Peyton, M., Zou, Y., Kurie, J. M., Dimaio, J. M., et al. (2004). Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 64, 9027-9034.
31. Ren, X., McHale, C. M., Skibola, C. F., Smith, A. H., Smith, M. T., and Zhang, L. (2011). An emerging role for epigenetic dysregulation in arsenic toxicity and carcinogenesis. Environ. Health Perspect. 119, 11-19.
32. Sato, M., Vaughan, M. B., Girard, L., Peyton, M., Lee, W., Shames, D. S., Ramirez, R. D., Sunaga, N., Gazdar, A. F., Shay, J. W., et al. (2006). Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res. 66, 2116-2128.
33. Shen, Y. L., Jiang, Y. G., Greenlee, A. R., Zhou, L. L., and Liu, L. H. (2009). MicroRNA expression profiles and miR-10a target in anti-benzo[a] pyrene-7, 8-diol-9, 10-epoxide-transformed human 16HBE cells. Biomed. Environ. Sci. 22, 14-21.
34. Shenouda, S. K., and Alahari, S. K. (2009). MicroRNA function in cancer: oncogene or a tumor suppressor? Cancer Metastasis Rev. 28, 369-378.
35. Smith, E., Jones, M. E., and Drew, P. A. (2009). Quantitation of DNA methylation by melt curve analysis. BMC Cancer 9, 123.
36. States, J. C., Srivastava, S., Chen, Y., and Barchowsky, A. (2009). Arsenic and cardiovascular disease. Toxicol. Sci. 107, 312-23.
37. Tapio, S., and Grosche, B. (2006). Arsenic in the aetiology of cancer. Mutat. Res. 612, 215-246.
38. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
39. Tiscornia, G., Singer, O., and Verma, I. M. (2006). Production and purification of lentiviral vectors. Nat. Protoc. 1, 241-245.
40. Vrba, L., Jensen, T. J., Garbe, J. C., Heimark, R. L., Cress, A. E., Dickinson, S., Stampfer, M. R., and Futscher, B. W. (2010). Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS One 5, e8697.
41. Wellner, U., Schubert, J., Burk, U. C., Schmalhofer, O., Zhu, F., Sonntag, A., Waldvogel, B., Vannier, C., Darling, D., zur Hausen, A., et al. (2009). The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness- inhibiting microRNAs. Nat. Cell Biol. 11, 1487-1495.
42. Wiklund, E. D., Bramsen, J. B., Hulf, T., Dyrskjøt, L., Ramanathan, R., Hansen, T. B., Villadsen, S. B., Gao, S., Ostenfeld, M. S., Borre, M., et al. (2011). Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int. J. Cancer. 128, 1327-1334.
43. Yang, C., Liu, Y., Lemmon, M. A., and Kazanietz, M. G. (2006). Essential role for Rac in heregulin beta1 mitogenic signaling: a mechanism that involves epidermal growth factor receptor and is independent of ErbB4. Mol. Cell Biol. 26, 831-842.
44. Yang, C., Wu, J., Zhang, R., Zhang, P., Eckard, J., Yusuf, R., Huang, X., Rossman, T. G., and Frenkel, K. (2005). Caffeic acid phenethyl ester (CAPE) prevents transformation of human cells by arsenite (As) and suppresses growth of As-transformed cells. Toxicology 213, 81-96.
45. Zhao, Y., Tan, Y. S., Haslam, S. Z., and Yang, C. (2010). Perfluorooctanoic acid effects on steroid hormone and growth factor levels mediate stimulation of peripubertal mammary gland development in C57BL/6 mice. Toxicol. Sci. 115, 214-224.