Table of Contents
ISRN Hepatology
Volume 2013, Article ID 817693, 13 pages
http://dx.doi.org/10.1155/2013/817693
Research Article

In Vivo Effect of Arsenic Trioxide on Keap1-p62-Nrf2 Signaling Pathway in Mouse Liver: Expression of Antioxidant Responsive Element-Driven Genes Related to Glutathione Metabolism

1Radiation Genetics and Chemical Mutagenesis Laboratory, Department of Zoology, Centre for Advanced Studies, Visva-Bharati University, Santiniketan, West Bengal 731235, India
2Environmental Toxicology Laboratory, Department of Zoology, Centre for Advanced Studies, Visva-Bharati University, Santiniketan, West Bengal 731235, India
3UGC-DAE Consortium for Scientific Research, Kolkata Centre, 3/LB-8, Bidhan Nagar, Kolkata, West Bengal 700098, India

Received 7 May 2013; Accepted 11 June 2013

Academic Editors: J. J. Marin, Z. Mathe, and Y. Yano

Copyright © 2013 Ritu Srivastava 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. P. B. Tchounwou, A. K. Patlolla, and J. A. Centeno, “Carcinogenic and systemic health effects associated with arsenic exposure: a critical review,” Toxicologic Pathology, vol. 31, no. 6, pp. 575–588, 2003. View at Google Scholar · View at Scopus
  2. J. Fu, C. G. Woods, E. Yehuda-Shnaidman et al., “Low-level arsenic impairs glucose-stimulated insulin secretion in pancreatic beta cells: involvement of cellular adaptive response to oxidative stress,” Environmental Health Perspectives, vol. 118, no. 6, pp. 864–870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Sun, X. Li, J. Pi et al., “Current research problems of chronic arsenicosis in China,” Journal of Health, Population and Nutrition, vol. 24, no. 2, pp. 176–181, 2006. View at Google Scholar · View at Scopus
  4. 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
  5. D. N. G. Mazumder, R. Haque, N. Ghosh et al., “Arsenic levels in drinking water and the prevalence of skin lesions in West Bengal, India,” International Journal of Epidemiology, vol. 27, no. 5, pp. 871–877, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. World Health Organization International Agency for Research on Cancer, Some Metals and Metallic Compounds: IARC Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Man, vol. 23, WHO Press, IARC, Lyon, France, 1980.
  7. Z. Wang and T. G. Rossman, “The carcinogenicity of arsenic,” in Toxicology of Metals, W. C. Louis, Ed., pp. 219–227, CRC Press, Boca Raton, Fla, USA, 1996. View at Google Scholar
  8. H. Tinwell, S. C. Stephens, and J. Ashby, “Arsenite as the probable active species in the human carcinogenicity of arsenic: mouse micronucleus assays on Na and K arsenite, orpiment, and Fowler's solution,” Environmental Health Perspectives, vol. 95, pp. 205–210, 1991. View at Google Scholar · View at Scopus
  9. 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
  10. J. Liu, L. Yu, E. J. Tokar et al., “Arsenic-induced aberrant gene expression in fetal mouse primary liver-cell cultures,” Annals of the New York Academy of Sciences, vol. 1140, pp. 368–375, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Wu, J. Liu, M. P. Waalkes et al., “High dietary fat exacerbates arsenic-induced liver fibrosis in mice,” Experimental Biology and Medicine, vol. 233, no. 3, pp. 377–384, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Jiang, Z. Huang, J. Y. Chan, and D. D. Zhang, “Nrf2 protects against As(III)-induced damage in mouse liver and bladder,” Toxicology and Applied Pharmacology, vol. 240, no. 1, pp. 8–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. National Research Council and National Academy of Sciences, Arsenic in Drinking Water, National Academy Press, Washington, DC, USA, 1999.
  14. D. N. G. Mazumder, “Effect of chronic intake of arsenic-contaminated water on liver,” Toxicology and Applied Pharmacology, vol. 206, no. 2, pp. 169–175, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Xu, Y. Wang, Q. 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
  16. A. Santra, J. Das Gupta, B. K. De, B. Roy, and D. N. G. Mazumder, “Hepatic manifestations in chronic arsenic toxicity,” Indian Journal of Gastroenterology, vol. 18, no. 4, pp. 152–155, 1999. View at Google Scholar · View at Scopus
  17. S. Roy and S. Bhattacharya, “Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus,” Ecotoxicology and Environmental Safety, vol. 65, no. 2, pp. 218–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Shi, X. Shi, and K. J. Liu, “Oxidative mechanism of arsenic toxicity and carcinogenesis,” Molecular and Cellular Biochemistry, vol. 255, no. 1-2, pp. 67–78, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Das, A. Santra, S. Lahiri, and D. N. Guha Mazumder, “Implications of oxidative stress and hepatic cytokine (TNF-α and IL-6) response in the pathogenesis of hepatic collagenesis in chronic arsenic toxicity,” Toxicology and Applied Pharmacology, vol. 204, no. 1, pp. 18–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. 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, vol. 13, no. 4, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Jomova, Z. Jenisova, M. Feszterova et al., “Arsenic: toxicity, oxidative stress and human disease,” Journal of Applied Toxicology, vol. 31, no. 2, pp. 95–107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Delnomdedieu, M. M. Basti, J. D. Otvos, and D. J. Thomas, “Reduction and binding of arsenate and dimethylarsinate by glutathione: a magnetic resonance study,” Chemico-Biological Interactions, vol. 90, no. 2, pp. 139–155, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. M. F. Hughes, “Arsenic toxicity and potential mechanisms of action,” Toxicology Letters, vol. 133, no. 1, pp. 1–16, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Lau, N. F. Villeneuve, Z. Sun, P. K. Wong, and D. D. Zhang, “Dual roles of Nrf2 in cancer,” Pharmacological Research, vol. 58, no. 5-6, pp. 262–270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. J. D. Hayes and M. McMahon, “NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer,” Trends in Biochemical Sciences, vol. 34, no. 4, pp. 176–188, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. 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
  27. 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
  28. X. He, M. G. Chen, G. X. Lin, and Q. Ma, “Arsenic induces NAD(P)H-quinone oxidoreductase I 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
  29. 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
  30. X.-J. Wang, Z. Sun, W. Chen, Y. Li, N. F. Villeneuve, and D. D. Zhang, “Activation of Nrf2 by arsenite and monomethylarsonous acid is independent of Keap1-C151: enhanced Keap1-Cul3 interaction,” Toxicology and Applied Pharmacology, vol. 230, no. 3, pp. 383–389, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Endo, Y. Sugioka, Y. Nakagi, Y. Saijo, and T. Yoshida, “A novel role of the NRF2 transcription factor in the regulation of arsenite-mediated keratin 16 gene expression in human keratinocytes,” Environmental Health Perspectives, vol. 116, no. 7, pp. 873–879, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. 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
  33. E. Beutler, O. Duron, and B. M. Kelly, “Improved method for the determination of blood glutathione,” The Journal of Laboratory and Clinical Medicine, vol. 61, pp. 882–888, 1963. View at Google Scholar · View at Scopus
  34. W. H. Habig, M. J. Pabst, and W. B. Jakoby, “Glutathione S transferases. The first enzymatic step in mercapturic acid formation,” Journal of Biological Chemistry, vol. 249, no. 22, pp. 7130–7139, 1974. View at Google Scholar · View at Scopus
  35. J. A. Buege and S. D. Aust, “Microsomal lipid peroxidation,” in Methods in Enzymology, S. Fleisher and L. Packer, Eds., pp. 302–310, Academic Press, New York, NY, USA, 1978. View at Google Scholar
  36. H. Aebi, “Catalase in vitro,” in Methods in Enzymology, L. Packer, Ed., pp. 121–126, Academic Press, Orlando, Fla, USA, 1984. View at Google Scholar
  37. N. Kawamura, “Catalase,” in Experimental Protocols for Reactive Oxygen and Nitrogen Species, J. M. C. Gutteridge and N. Taniguchi, Eds., pp. 77–78, Oxford University Press, New York, NY, USA, 1999. View at Google Scholar
  38. A. Chattopadhyay, S. Podder, S. Agarwal, and S. Bhattacharya, “Fluoride-induced histopathology and synthesis of stress protein in liver and kidney of mice,” Archives of Toxicology, vol. 85, no. 4, pp. 327–335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  40. N. Li, J. Alam, M. I. Venkatesan et al., “Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals,” Journal of Immunology, vol. 173, no. 5, pp. 3467–3481, 2004. View at Google Scholar · View at Scopus
  41. K. Shimano, M. Satake, A. Okaya et al., “Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1,” American Journal of Pathology, vol. 163, no. 1, pp. 3–9, 2003. View at Google Scholar · View at Scopus
  42. 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
  43. H. Harada, R. Sugimoto, A. Watanabe et al., “Differential roles for Nrf2 and AP-1 in upregulation of HO-1 expression by arsenite in murine embryonic fibroblasts,” Free Radical Research, vol. 42, no. 4, pp. 297–304, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Singh, D. Kumar, K. Lal, S. Raisuddin, and A. P. Sahu, “Adverse health effects due to arsenic exposure: modification by dietary supplementation of jaggery in mice,” Toxicology and Applied Pharmacology, vol. 242, no. 3, pp. 247–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Santra, A. Maiti, S. Das, S. Lahiri, S. K. Charkaborty, and D. N. Guha Mazumder, “Hepatic damage caused by chronic arsenic toxicity in experimental animals,” Journal of Toxicology, vol. 38, no. 4, pp. 395–405, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. Z. Drobná, F. S. Walton, D. S. Paul, W. Xing, D. J. Thomas, and M. Stýblo, “Metabolism of arsenic in human liver: the role of membrane transporters,” Archives of Toxicology, vol. 84, pp. 3–16, 2010. View at Google Scholar
  47. N. Tandan, M. Roy, and S. Roy, “Ameliorative potential of Psidium guajava on hemato-biochemical alterations in arsenic-exposed wistar rats,” Toxicology International, vol. 19, pp. 121–124, 2012. View at Google Scholar
  48. S. J. S. Flora, S. C. Pant, P. R. Malhotra, and G. M. Kannan, “Biochemical and histopathological changes in arsenic-intoxicated rats coexposed to ethanol,” Alcohol, vol. 14, no. 6, pp. 563–568, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Ferzand, J. A. Gadahi, S. Saleha, and Q. Ali, “Histological and haematological disturbance caused by arsenic toxicity in mice model,” Pakistan Journal of Biological Sciences, vol. 11, no. 11, pp. 1405–1413, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. R. N. P. Das Neves, F. Carvalho, M. Carvalho et al., “Protective activity of hesperidin and lipoic acid against sodium arsenite acute toxicity in mice,” Toxicologic Pathology, vol. 32, no. 5, pp. 527–535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. 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
  52. S. J. S. Flora, S. Bhadauria, S. C. Pant, and R. K. Dhaked, “Arsenic induced blood and brain oxidative stress and its response to some thiol chelators in rats,” Life Sciences, vol. 77, no. 18, pp. 2324–2337, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. S. J. S. Flora, S. Bhadauria, G. M. Kannan, and N. Singh, “Arsenic induced oxidative stress and the role of antioxidant supplementation during chelation: a review,” Journal of Environmental Biology, vol. 28, no. 2, pp. 333–347, 2007. View at Google Scholar · View at Scopus
  54. M. E. Vahter, “Interactions between arsenic-induced toxicity and nutrition in early life,” Journal of Nutrition, vol. 137, no. 12, pp. 2798–2804, 2007. View at Google Scholar · View at Scopus
  55. E. O. Farombi, O. A. Adelowo, and Y. R. Ajimoko, “Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River,” International Journal of Environmental Research and Public Health, vol. 4, no. 2, pp. 158–165, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Bashir, Y. Sharma, M. Irshad, S. D. Gupta, and T. D. Dogra, “Arsenic-induced cell death in liver and brain of experimental rats,” Basic and Clinical Pharmacology and Toxicology, vol. 98, no. 1, pp. 38–43, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Mittal and S. J. S. Flora, “Effects of individual and combined exposure to sodium arsenite and sodium fluoride on tissue oxidative stress, arsenic and fluoride levels in male mice,” Chemico-Biological Interactions, vol. 162, no. 2, pp. 128–139, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. C.-H. Guo, W.-S. Ko, P.-C. Chen, G.-S. W. Hsu, C.-Y. Lin, and C.-L. Wang, “Alterations in trace elements and oxidative stress in uremic patients with dementia,” Biological Trace Element Research, vol. 131, no. 1, pp. 13–24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Y. Zhang, N. Q. Liu, F. L. Li et al., “Characterization of Fe, Cu and Zn in organs of PDAPP transgenic mice by XRF spectrometry,” X-Ray Spectrometry, vol. 35, no. 4, pp. 253–256, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Kowalik-Jankowska, M. Ruta-Dolejsz, K. Wisniewska, L. Lankiewicz, and H. Kozlowski, “Possible involvement of Copper(II) in Alzheimer disease,” Environmental Health Perspectives, vol. 110, no. 5, pp. 869–870, 2002. View at Google Scholar · View at Scopus
  61. O. A. Levander, “Metabolic interrelationships between arsenic and selenium,” Environmental Health Perspectives, vol. 19, pp. 159–164, 1977. View at Google Scholar · View at Scopus
  62. T. G. Rossman and A. N. Uddin, “Selenium prevents spontaneous and arsenite-induced mutagenesis,” International Congress Series, vol. 1275, pp. 173–179, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Molin, P. Frisk, and N.-G. Ilbäck, “Sequential effects of daily arsenic trioxide treatment on essential and nonessential trace elements in tissues in mice,” Anti-Cancer Drugs, vol. 19, no. 8, pp. 812–818, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Molin, P. Frisk, and N.-G. Ilback, “Arsenic trioxide affects the trace element balance in tissues in infected and healthy mice differently,” Anticancer Research, vol. 29, no. 1, pp. 83–90, 2009. View at Google Scholar · View at Scopus
  65. M. Haidari, E. Javadi, A. Sanati, M. Hajilooi, and J. Ghanbili, “Association of increased ferritin with premature coronary stenosis in men,” Clinical Chemistry, vol. 47, no. 9, pp. 1666–1672, 2001. View at Google Scholar · View at Scopus
  66. Z. Durackova, L. Bergendi, A. Liptakova, and J. Muchova, “Free radicals derived from oxygen and medicine,” Bratislava Medical Journal, vol. 94, pp. 419–434, 1993. View at Google Scholar
  67. M. Ahmad, M. A. Khan, and A. S. Khan, “Oxidative stress and level of-iron indices in coronary heart disease patients,” Journal of Ayub Medical College, Abbottabad, vol. 21, no. 2, pp. 56–59, 2009. View at Google Scholar · View at Scopus
  68. A. Jain, T. Lamark, E. Sjøttem et al., “p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription,” Journal of Biological Chemistry, vol. 285, no. 29, pp. 22576–22591, 2010. View at Publisher · View at Google Scholar · View at Scopus