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Oxidative Medicine and Cellular Longevity
Volume 2013 (2013), Article ID 984546, 10 pages
http://dx.doi.org/10.1155/2013/984546
Research Article

Activation of the Nrf2 Pathway by Inorganic Arsenic in Human Hepatocytes and the Role of Transcriptional Repressor Bach1

Department of Occupational and Environmental Health, Liaoning Provincial Key Laboratory of Arsenic Biological Effect and Poisoning, School of Public Health, China Medical University, 92 North 2nd Road, Heping District, Shenyang 110001, China

Received 16 November 2012; Revised 10 April 2013; Accepted 12 April 2013

Academic Editor: Mi-Kyoung Kwak

Copyright © 2013 Dan Liu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Sun, Y. Xu, X. Li, Y. Jin, B. Li, and X. Sun, “Urinary arsenic metabolites in children and adults exposed to arsenic in drinking water in inner Mongolia, China,” Environmental Health Perspectives, vol. 115, no. 4, pp. 648–652, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Y. Xu, Y. Wang, Q. M. Zheng et al., “Clinical manifestations and arsenic methylation after a rare subacute arsenic poisoning accident,” Toxicological Sciences, vol. 103, no. 2, pp. 278–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. C. H. Tseng, “Blackfoot disease and arsenic: a never-ending story,” Journal of Environmental Science and Health C, vol. 23, no. 1, pp. 55–74, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. P. R. Taylor, Y. L. Qiao, A. Schatzkin et al., “Relation of arsenic exposure to lung cancer among tin miners in Yunnan Province, China,” British Journal of Industrial Medicine, vol. 46, no. 12, pp. 881–886, 1989. View at Google Scholar · View at Scopus
  5. S. Tabacova, E. S. Hunter III, and B. C. Gladen, “Developmental toxicity of inorganic arsenic in whole embryo culture: oxidation state, dose, time, and gestational age dependence,” Toxicology and Applied Pharmacology, vol. 138, no. 2, pp. 298–307, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. M. S. Golub, M. S. Macintosh, and N. Baumrind, “Developmental and reproductive toxicity of inorganic arsenic: animal studies and human concerns,” Journal of Toxicology and Environmental Health B, vol. 1, no. 3, pp. 199–241, 1998. View at Google Scholar · View at Scopus
  7. J. P. Mastin, “Environmental cardiovascular disease,” Cardiovascular Toxicology, vol. 5, no. 2, pp. 91–94, 2005. View at Google Scholar · View at Scopus
  8. A. M. Evens, M. S. Tallman, and R. B. Gartenhaus, “The potential of arsenic trioxide in the treatment of malignant disease: past, present, and future,” Leukemia Research, vol. 28, no. 9, pp. 891–900, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. E. M. Farber, “History of the treatment of psoriasis,” Journal of the American Academy of Dermatology, vol. 27, no. 4, pp. 640–645, 1992. View at Google Scholar · View at Scopus
  10. N. S. Carter and A. H. Fairlamb, “Arsenical-resistant trypanosomes lack an unusual adenosine transporter,” Nature, vol. 361, no. 6408, pp. 173–176, 1993. View at Publisher · View at Google Scholar · View at Scopus
  11. K. T. Kitchin, “Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites,” Toxicology and Applied Pharmacology, vol. 172, no. 3, pp. 249–261, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Baird and A. T. Dinkova-Kostova, “The cytoprotective role of the Keap1-Nrf2 pathway,” Archives of Toxicology, vol. 85, no. 4, pp. 241–272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Itoh, T. Chiba, S. Takahashi et al., “An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements,” Biochemical and Biophysical Research Communications, vol. 236, no. 2, pp. 313–322, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Kobayashi and M. Yamamoto, “Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation,” Antioxidants & Redox Signaling, vol. 7, no. 3-4, pp. 385–394, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Pi, W. Qu, J. M. Reece, Y. Kumagai, and M. P. Waalkes, “Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide,” Experimental Cell Research, vol. 290, no. 2, pp. 234–245, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. X. He, M. G. Chen, G. X. Lin et al., “Arsenic induces NAD(P)H-quinone oxidoreductase 1 by disrupting the Nrf2·Keap1·Cul3 complex and recruiting Nrf2·Maf to the antioxidant response element enhancer,” The Journal of Biological Chemistry, vol. 281, no. 33, pp. 23620–23631, 2006. View at Google Scholar
  17. B. Li, X. Li, B. Zhu et al., “Sodium arsenite induced reactive oxygen species generation, nuclear factor (erythroid-2 related) factor 2 activation, heme oxygenase-1 expression, and glutathione elevation in Chang human hepatocytes,” Environmental Toxicology, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Liu and M. P. Waalkes, “Liver is a target of arsenic carcinogenesis,” Toxicological Sciences, vol. 105, no. 1, pp. 24–32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. P. Geubel, M. C. Mairlot, J. P. Buchet, C. Dive, and R. Lauwerys, “Abnormal methylation capacity in human liver cirrhosis,” International Journal of Clinical Pharmacology Research, vol. 8, no. 2, pp. 117–122, 1988. View at Google Scholar · View at Scopus
  20. K. Igarashi, H. Hoshino, A. Muto et al., “Multivalent DNA binding complex generated by small Maf and Bach1 as a possible biochemical basis for β-globin locus control region complex,” The Journal of Biological Chemistry, vol. 273, no. 19, pp. 11783–11790, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Sun, H. Hoshino, K. Takaku et al., “Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene,” EMBO Journal, vol. 21, no. 19, pp. 5216–5224, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Dhakshinamoorthy, A. K. Jain, D. A. Bloom, and A. K. Jaiswal, “Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants,” The Journal of Biological Chemistry, vol. 280, no. 17, pp. 16891–16900, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. H. J. Warnatz, D. Schmidt, T. Manke et al., “The BTB and CNC homology 1 (BACH1) target genes are involved in the oxidative stress response and in control of the cell cycle,” The Journal of Biological Chemistry, vol. 286, no. 26, pp. 23521–23532, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Li, Y. Sun, X. Sun et al., “Monomethylarsonous acid induced cytotoxicity and endothelial nitric oxide synthase phosphorylation in endothelial cells,” Bulletin of Environmental Contamination and Toxicology, vol. 78, no. 6, pp. 455–458, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. C. G. Woods, J. Fu, P. Xue et al., “Dose-dependent transitions in Nrf2-mediated adaptive response and related stress responses to hypochlorous acid in mouse macrophages,” Toxicology and Applied Pharmacology, vol. 238, no. 1, pp. 27–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Timm, C. Kondor-Koch, H. Lehrach, H. Riedel, J. E. Edström, and H. Garoff, “Expression of viral membrane proteins from cloned cDNA by microinjection into eukaryotic cell nuclei,” Methods in Enzymology, vol. 96, pp. 496–511, 1983. View at Publisher · View at Google Scholar · View at Scopus
  27. X. J. Wang, Z. Sun, W. Chen, K. E. Eblin, J. A. Gandolfi, and D. D. Zhang, “Nrf2 protects human bladder urothelial cells from arsenite and monomethylarsonous acid toxicity,” Toxicology and Applied Pharmacology, vol. 225, no. 2, pp. 206–213, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Meng, X. Wang, Q. Chang et al., “Arsenic promotes angiogenesis in vitro via a heme oxygenase-1-dependent mechanism,” Toxicology and Applied Pharmacology, vol. 244, no. 3, pp. 291–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Abiko, Y. Shinkai, D. Sumi, and Y. Kumagai, “Reduction of arsenic-induced cytotoxicity through Nrf2/HO-1 signaling in HepG2 cells,” Journal of Toxicological Sciences, vol. 35, no. 3, pp. 419–423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Aono, T. Yanagawa, K. Itoh et al., “Activation of Nrf2 and accumulation of ubiquitinated A170 by arsenic in osteoblasts,” Biochemical and Biophysical Research Communications, vol. 305, no. 2, pp. 271–277, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. A. A. Morales, D. Gutman, P. J. Cejas, K. P. Lee, and L. H. Boise, “Reactive oxygen species are not required for an arsenic trioxide-induced antioxidant response or apoptosis,” The Journal of Biological Chemistry, vol. 284, no. 19, pp. 12886–12895, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Massrieh, A. Derjuga, and V. Blank, “Induction of endogenous Nrf2/small Maf heterodimers by arsenic-mediated stress in placental choriocarcinoma cells,” Antioxidants & Redox Signaling, vol. 8, no. 1-2, pp. 53–59, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. Q. Liu, H. Zhang, L. Smeester et al., “The NRF2-mediated oxidative stress response pathway is associated with tumor cell resistance to arsenic trioxide across the NCI-60 panel,” BMC Medical Genomics, vol. 3, article 37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. F. Reichard, G. T. Motz, and A. Puga, “Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1,” Nucleic Acids Research, vol. 35, no. 21, pp. 7074–7086, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Miyazaki, Y. Kirino, M. Takeno et al., “Expression of heme oxygenase-1 in human leukemic cells and its regulation by transcriptional repressor Bach1,” Cancer Science, vol. 101, no. 6, pp. 1409–1416, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Sakamoto, K. Iwasaki, H. Sugiyama, and Y. Tsuji, “Role of the tumor suppressor PTEN in antioxidant responsive element-mediated transcription and associated histone modifications,” Molecular Biology of the Cell, vol. 20, no. 6, pp. 1606–1617, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. J. F. Reichard, M. A. Sartor, and A. Puga, “BACH1 is a specific repressor of HMOX1 that is inactivated by arsenite,” The Journal of Biological Chemistry, vol. 283, no. 33, pp. 22363–22370, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. J. W. Kaspar and A. K. Jaiswal, “Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression,” The Journal of Biological Chemistry, vol. 285, no. 1, pp. 153–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Zhu and Y. Li, “NAD(P)H: quinone oxidoreductase 1 and its potential protective role in cardiovascular diseases and related conditions,” Cardiovascular Toxicology, vol. 12, no. 1, pp. 39–45, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Paine, B. Eiz-Vesper, R. Blasczyk, and S. Immenschuh, “Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential,” Biochemical Pharmacology, vol. 80, no. 12, pp. 1895–1903, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Sass, R. Barikbin, and G. Tiegs, “The multiple functions of heme oxygenase-1 in the liver,” Zeitschrift Für Gastroenterologie, vol. 50, no. 1, pp. 34–40, 2012. View at Google Scholar
  42. D. Malhotra, E. Portales-Casamar, A. Singh et al., “Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through chip-seq profiling and network analysis,” Nucleic Acids Research, vol. 38, no. 17, pp. 5718–5734, 2010. View at Publisher · View at Google Scholar · View at Scopus