Arsenic induces vl30 retrotransposition: The involvement of oxidative stress and heat-shock protein 70

Toxicological Sciences

Volumn 134, Issue 2, 2013, Pages 312-322

  Markopoulos, Georgios ^a   Noutsopoulos, Dimitrios ^b   Mantziou, Stefania ^a   Vartholomatos, Georgios ^c   Monokrousos, Nikolaos ^b,d   Angelidis, Charalampos ^a   Tzavaras, Theodore ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

^c UNIVERSITY HOSPITAL OF IOANNINA   (Greece)

^d ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Arsenic; Cytotoxicity; Hsp70; Retrotransposition; Retrotransposon; VL30

Indexed keywords

ACETYLCYSTEINE; ARSENIC; EFAVIRENZ; ENHANCED GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70; NEVIRAPINE; TRANSCRIPTASE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA TRANSPOSITION; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; VL30 GENE;

ARSENIC; CYTOTOXICITY; HSP70.; RETROTRANSPOSITION; RETROTRANSPOSON; VL30;

ANIMALS; ARSENIC; GREEN FLUORESCENT PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MICE; NIH 3T3 CELLS; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; RETROELEMENTS; UP-REGULATION;

EID: 84880668458     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft118     Document Type: Article

References (43)

1. Angelidis, C. E.,Lazaridis, I., and Pagoulatos, G. N. (1988). Specific inhibition of simian virus 40 protein synthesis by heat and arsenite treatment. Eur. J. Biochem. 172, 27-34.
2. Angelidis, C. E., Lazaridis, I., and Pagoulatos, G. N. (1991). Constitutive expression of heat-shock protein 70 in mammalian cells confers thermoresistance. Eur. J. Biochem. 199, 35-39.
3. Bhattacharjee, P., Banerjee, M., and Giri, A. K. (2013). Role of genomic instability in arsenic-induced carcinogenicity. A review. Environ. Int. 53, 29-40.
4. Boeke, J. D., Garfinkel, D. J., Styles, C. A., and Fink, G. R. (1985). Ty elements transpose through an RNA intermediate. Cell 40, 491-500.
5. Brunmeir, R., Lagger, S., Simboeck, E., Sawicka, A., Egger, G., Hagelkruys, A., Zhang, Y., Matthias, P., Miller, W. J., and Seiser, C. (2010). Epigenetic regulation of a murine retrotransposon by a dual histone modification mark. PLoS Genet. 6, e1000927.
6. Costain, W. J., Rasquinha, I., Graber, T., Luebbert, C., Preston, E., Slinn, J., Xie, X., and MacManus, J. P. (2006). Cerebral ischemia induces neuronal expression of novel VL30 mouse retrotransposons bound to polyribosomes. Brain Res. 1094, 24-37.
7. Del Razo, L. M., Quintanilla-Vega, B., Brambila-Colombres, E., Calderón-Aranda, E. S., Manno, M., and Albores, A. (2001). Stress proteins induced by arsenic. Toxicol. Appl. Pharmacol. 177, 132-148.
8. Dimitrov, M., Venkov, P., and Pesheva, M. (2011). The positive response of Ty1 retrotransposition test to carcinogens is due to increased levels of reactive oxygen species generated by the genotoxins. Arch. Toxicol. 85, 67-74.
9. Druwe, I. L., and Vaillancourt, R. R. (2010). Influence of arsenate and arsenite on signal transduction pathways: An update. Arch. Toxicol. 84, 585-596.
10. El-Sawy, M., Kale, S. P., Dugan, C., Nguyen, T. Q., Belancio, V., Bruch, H., Roy-Engel, A. M., and Deininger, P. L. (2005). Nickel stimulates L1 retrotransposition by a post-transcriptional mechanism. J. Mol. Biol. 354, 246-257.
11. Faulkner, G. J., Kimura, Y., Daub, C. O., Wani, S., Plessy, C., Irvine, K. M., Schroder, K., Cloonan, N., Steptoe, A. L., Lassmann, T., et al. (2009). The regulated retrotransposon transcriptome of mammalian cells. Nat. Genet. 41, 563-571.
12. Flora, S. J. (2011). Arsenic-induced oxidative stress and its reversibility. Free Radic. Biol. Med. 51, 257-281.
13. French, N. S., and Norton, J. D. (1997). Structure and functional properties of mouse VL30 retrotransposons. Biochim. Biophys. Acta 1352, 33-47.
14. Garen, A., and Song, X. (2008). Regulatory roles of tumor-suppressor proteins and noncoding RNA in cancer and normal cell functions. Int. J. Cancer 122, 1687-1689.
15. Gasior, S. L., Wakeman, T. P., Xu, B., and Deininger, P. L. (2006). The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol. 357, 1383-1393.
16. Georgiou, I., Noutsopoulos, D., Dimitriadou, E., Markopoulos, G., Apergi, A., Lazaros, L., Vaxevanoglou, T., Pantos, K., Syrrou, M., and Tzavaras, T. (2009). Retrotransposon RNA expression and evidence for retrotransposition events in human oocytes. Hum. Mol. Genet. 18, 1221-1228.
17. Ghosh, P., Banerjee, M., Giri, A. K., and Ray, K. (2008). Toxicogenomics of arsenic: Classical ideas and recent advances. Mutat. Res. 659, 293-301.
18. Goodier, J. L., and Kazazian, H. H., Jr. (2008). Retrotransposons revisited: The restraint and rehabilitation of parasites. Cell 135, 23-35.
19. Heidmann, T., Heidmann, O., and Nicolas, J. F. (1988). An indicator gene to demonstrate intracellular transposition of defective retroviruses. Proc. Natl. Acad. Sci. U. S. A. 85, 2219-2223.
20. Huang, R. N., Ho, I. C., Yih, L. H., and Lee, T. C. (1995). Sodium arsenite induces chromosome endoreduplication and inhibits protein phosphatase activity in human fibroblasts. Environ. Mol. Mutagen. 25, 188-196.
21. Khalil, S., Luciano, J., Chen, W., and Liu, A. Y. (2006). Dynamic regulation and involvement of the heat shock transcriptional response in arsenic carcinogenesis. J. Cell. Physiol. 207, 562-569.
22. Konisti, S., Mantziou, S., Markopoulos, G., Thrasyvoulou, S., Vartholomatos, G., Sainis, I., Kolettas, E., Noutsopoulos, D., and Tzavaras, T. (2012). H2O2 signals via iron induction of VL30 retrotransposition correlated with cytotoxicity. Free Radic. Biol. Med. 52, 2072-2081.
23. Kumagai, Y., and Sumi, D. (2007). Arsenic: Signal transduction, transcription factor, and biotransformation involved in cellular response and toxicity. Annu. Rev. Pharmacol. Toxicol. 47, 243-262.
24. Liu, J., Kadiiska, M. B., Liu, Y., Lu, T., Qu, W., and Waalkes, M. P. (2001). Stress-related gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 61, 314-320.
25. Liu, J. P. (1999). Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J. 13, 2091-2104.
26. Löbrich, M., and Jeggo, P. A. (2007). The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat. Rev. Cancer 7, 861-869.
27. Massa, P. E., Li, X., Hanidu, A., Siamas, J., Pariali, M., Pareja, J., Savitt, A. G., Catron, K. M., Li, J., and Marcu, K. B. (2005). Gene expression profiling in conjunction with physiological rescues of IKKalpha-null cells with wild type or mutant IKKalpha reveals distinct classes of IKKalpha/NF-kappaBdependent genes. J. Biol. Chem. 280, 14057-14069.
28. McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226, 792-801.
29. Mosser, D. D., Caron, A. W., Bourget, L., Meriin, A. B., Sherman, M. Y., Morimoto, R. I., and Massie, B. (2000). The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol. Cell. Biol. 20, 7146-7159.
30. Nohara, K., Tateishi, Y., Suzuki, T., Okamura, K., Murai, H., Takumi, S., Maekawa, F., Nishimura, N., Kobori, M., and Ito, T. (2012). Late-onset increases in oxidative stress and other tumorigenic activities and tumors with a Ha-ras mutation in the liver of adult male C3H mice gestationally exposed to arsenic. Toxicol. Sci. 129, 293-304.
31. Nordstrom, D. K. (2002). Public health. Worldwide occurrences of arsenic in ground water. Science 296, 2143-2145.
32. Noutsopoulos, D., Markopoulos, G., Koliou, M., Dova, L., Vartholomatos, G., Kolettas, E., and Tzavaras, T. (2007). Vanadium induces VL30 retrotransposition at an unusually high level: A possible carcinogenesis mechanism. J. Mol. Biol. 374, 80-90.
33. Noutsopoulos, D., Markopoulos, G., Vartholomatos, G., Kolettas, E., Kolaitis, N., and Tzavaras, T. (2010). VL30 retrotransposition signals activation of a caspase-independent and p53-dependent death pathway associated with mitochondrial and lysosomal damage. Cell Res. 20, 553-562.
34. Noutsopoulos, D., Vartholomatos, G., Kolaitis, N., and Tzavaras, T. (2006). SV40 large T antigen up-regulates the retrotransposition frequency of virallike 30 elements. J. Mol. Biol. 361, 450-461.
35. Okudaira, N., Okamura, T., Tamura, M., Iijma, K., Goto, M., Matsunaga, A., Ochiai, M., Nakagama, H., Kano, S., Fujii-Kuriyama, Y., et al. (2012). Long interspersed element-1 is differentially regulated by food-borne carcinogens via the aryl hydrocarbon receptor. Oncogene. doi:10.1038/onc.2012.516.
36. Ostertag, E. M., Prak, E. T., DeBerardinis, R. J., Moran, J. V., and Kazazian, H. H., Jr. (2000). Determination of L1 retrotransposition kinetics in cultured cells. Nucleic Acids Res. 28, 1418-1423.
37. Puschendorf, M., Stein, P., Oakeley, E. J., Schultz, R. M., Peters, A. H., and Svoboda, P. (2006). Abundant transcripts from retrotransposons are unstable in fully grown mouse oocytes. Biochem. Biophys. Res. Commun. 347, 36-43.
38. Salnikow, K., and Zhitkovich, A. (2008). Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic, and chromium. Chem. Res. Toxicol. 21, 28-44.
39. Sciamanna, I., Landriscina, M., Pittoggi, C., Quirino, M., Mearelli, C., Beraldi, R., Mattei, E., Serafino, A., Cassano, A., Sinibaldi-Vallebona, P., et al. (2005). Inhibition of endogenous reverse transcriptase antagonizes human tumor growth. Oncogene 24, 3923-3931.
40. Tzavaras, T., Eftaxia, S., Tavoulari, S., Hatzi, P., and Angelidis, C. (2003). Factors influencing the expression of endogenous reverse transcriptases and viral-like 30 elements in mouse NIH3T3 cells. Int. J. Oncol. 23, 1237-1243.
41. Tzavaras, T., Kalogera, C., Eftaxia, S., Saragosti, S., and Pagoulatos, G. N. (1998). Clone-specific high-frequency retrotransposition of a recombinant virus containing a VL30 promoter in SV40-transformed NIH3T3 cells. Biochim. Biophys. Acta 1442, 186-198.
42. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40.
43. Wang, G., Cui, Y., Zhang, G., Garen, A., and Song, X. (2009). Regulation of proto-oncogene transcription, cell proliferation, and tumorigenesis in mice by PSF protein and a VL30 noncoding RNA. Proc. Natl. Acad. Sci. U. S. A. 106, 16794-16798.