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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 9251303, 12 pages
https://doi.org/10.1155/2017/9251303
Research Article

Arsenite Effects on Mitochondrial Bioenergetics in Human and Mouse Primary Hepatocytes Follow a Nonlinear Dose Response

1Department of Pharmacology, Toxicology and Therapeutics, University of Kansas Medical Center, Kansas City, KS 66160, USA
2Department of Clinical Biochemistry, Christian Medical College, Vellore 632004, India
3Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, KS 66160, USA

Correspondence should be addressed to Partha Krishnamurthy; ude.cmuk@irutsakp

Received 15 September 2016; Revised 10 November 2016; Accepted 20 November 2016; Published 9 January 2017

Academic Editor: Rodrigo Franco

Copyright © 2017 Hemantkumar Chavan 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. World-Health-Organisation, “Arsenic and arsenic compounds beds,” in Environmental Health Criteria, WHO, 2004. View at Google Scholar
  2. 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
  3. P. Wild, E. Bourgkard, and C. Paris, “Lung cancer and exposure to metals: the epidemiological evidence,” Methods in Molecular Biology, vol. 472, pp. 139–167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Straif, L. Benbrahim-Tallaa, R. Baan et al., “A review of human carcinogens—part C: metals, arsenic, dusts, and fibres,” The lancet oncology, vol. 10, no. 5, pp. 453–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. A. H. Smith and C. M. Steinmaus, “Health effects of arsenic and chromium in drinking water: recent human findings,” Annual Review of Public Health, vol. 30, pp. 107–122, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. U. Schuhmacher-Wolz, H. H. Dieter, D. Klein, and K. Schneider, “Oral exposure to inorganic arsenic: evaluation of its carcinogenic and non-carcinogenic effects,” Critical Reviews in Toxicology, vol. 39, no. 4, pp. 271–298, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. R. R. Walvekar, S. V. Kane, M. S. Nadkarni, I. N. Bagwan, D. A. Chaukar, and A. K. D'Cruz, “Chronic arsenic poisoning: a global health issue—a report of multiple primary cancers,” Journal of Cutaneous Pathology, vol. 34, no. 2, pp. 203–206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. H.-S. Yu, W.-T. Liao, and C.-Y. Chai, “Arsenic carcinogenesis in the skin,” Journal of Biomedical Science, vol. 13, no. 5, pp. 657–666, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Tapio and B. Grosche, “Arsenic in the aetiology of cancer,” Mutation Research, vol. 612, no. 3, pp. 215–246, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. M. Cohen, L. L. Arnold, B. D. Beck, A. S. Lewis, and M. Eldan, “Evaluation of the carcinogenicity of inorganic arsenic,” Critical Reviews in Toxicology, vol. 43, no. 9, pp. 711–752, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. J. C. States, S. Srivastava, Y. Chen, and A. Barchowsky, “Arsenic and cardiovascular disease,” Toxicological Sciences, vol. 107, no. 2, pp. 312–323, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Taeger, G. Johnen, T. Wiethege et al., “Major histopathological patterns of lung cancer related to arsenic exposure in German uranium miners,” International Archives of Occupational and Environmental Health, vol. 82, no. 7, pp. 867–875, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J. S. Petrick, F. M. Blachere, O. Selmin, and R. C. Lantz, “Inorganic arsenic as a developmental toxicant: in utero exposure and alterations in the developing rat lungs,” Molecular Nutrition and Food Research, vol. 53, no. 5, pp. 583–591, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Aggarwal, P. B. Wangikar, S. N. Sarkar et al., “Effects of low-level arsenic exposure on the developmental toxicity of anilofos in rats,” Journal of Applied Toxicology, vol. 27, no. 3, pp. 255–261, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Rahman, M. Vahter, A. H. Smith et al., “Arsenic exposure during pregnancy and size at birth: a prospective cohort study in Bangladesh,” American Journal of Epidemiology, vol. 169, no. 3, pp. 304–312, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. W.-Y. Au, S. Tam, B. M. W. Fong, T. S. K. Wan, S.-F. Yip, and Y.-L. Kwong, “Second hematological malignancies during arsenic trioxide therapy of B-cell lymphomas,” Leukemia Research, vol. 33, no. 1, pp. 191–193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. 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
  18. M.-J. Hosseini, F. Shaki, M. Ghazi-Khansari, and J. Pourahmad, “Toxicity of arsenic (III) on isolated liver mitochondria: a new mechanistic approach,” Iranian Journal of Pharmaceutical Research, vol. 12, pp. 119–136, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Naranmandura, S. Xu, T. Sawata et al., “Mitochondria are the main target organelle for trivalent monomethylarsonous acid (MMA III)-induced cytotoxicity,” Chemical Research in Toxicology, vol. 24, no. 7, pp. 1094–1103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Nohara, T. Suzuki, S. Takumi, and K. Okamura, “Increase in incidence of hepatic tumors caused by oncogenic somatic mutation in mice maternally exposed to inorganic arsenic and the multigenerational and transgenerational effects of inorganic arsenic,” Nihon Eiseigaku Zasshi, vol. 69, no. 2, pp. 92–96, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Dopp, U. von Recklinghausen, R. Diaz-Bone, A. V. Hirner, and A. W. Rettenmeier, “Cellular uptake, subcellular distribution and toxicity of arsenic compounds in methylating and non-methylating cells,” Environmental Research, vol. 110, no. 5, pp. 435–442, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Styblo, L. M. Del Razo, E. L. LeCluyse et al., “Metabolism of arsenic in primary cultures of human and rat hepatocytes,” Chemical Research in Toxicology, vol. 12, no. 7, pp. 560–565, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. C. M. Schmidt, C. N. Cheng, A. Marino, R. Konsoula, and F. A. Barile, “Hormesis effect of trace metals on cultured normal and immortal human mammary cells,” Toxicology and Industrial Health, vol. 20, no. 1–5, pp. 57–68, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Schmeisser, K. Schmeisser, S. Weimer et al., “Mitochondrial hormesis links low-dose arsenite exposure to lifespan extension,” Aging Cell, vol. 12, no. 3, pp. 508–517, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. E. J. Calabrese and L. A. Baldwin, “Inorganics and hormesis,” Critical Reviews in Toxicology, vol. 33, no. 3-4, pp. 215–304, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. K. T. Kitchin and J. L. Brown, “Dose-response relationship for rat liver DNA damage caused by 1,2-dimethylhydrazine,” Toxicology, vol. 114, no. 2, pp. 113–124, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Scialò, A. Sriram, D. Fernández-Ayala et al., “Mitochondrial ROS produced via reverse electron transport extend animal lifespan,” Cell Metabolism, vol. 23, no. 4, pp. 725–734, 2016. View at Publisher · View at Google Scholar
  28. S.-J. Lee, A. B. Hwang, and C. Kenyon, “Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity,” Current Biology, vol. 20, no. 23, pp. 2131–2136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Chavan and P. Krishnamurthy, “Polycyclic aromatic hydrocarbons (PAHs) mediate transcriptional activation of the ATP binding cassette transporter ABCB6 gene via the aryl hydrocarbon receptor (AhR),” Journal of Biological Chemistry, vol. 287, no. 38, pp. 32054–32068, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Xie, M. R. McGill, K. Dorko et al., “Mechanisms of acetaminophen-induced cell death in primary human hepatocytes,” Toxicology and Applied Pharmacology, vol. 279, no. 3, pp. 266–274, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. R. B. McCleskey, D. K. Nordstrom, and A. S. Maest, “Preservation of water samples for arsenic(III/V) determinations: an evaluation of the literature and new analytical results,” Applied Geochemistry, vol. 19, no. 7, pp. 995–1009, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Chavan, M. Oruganti, and P. Krishnamurthy, “The ATP-binding cassette transporter ABCB6 is induced by arsenic and protects against arsenic cytotoxicity,” Toxicological Sciences, vol. 120, no. 2, pp. 519–528, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Han, N. Hanawa, B. Saberi, and N. Kaplowitz, “Hydrogen peroxide and redox modulation sensitize primary mouse hepatocytes to TNF-induced apoptosis,” Free Radical Biology and Medicine, vol. 41, no. 4, pp. 627–639, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. W. C. Bowen, A. W. Michalopoulos, A. Orr, M. Q. Ding, D. B. Stolz, and G. K. Michalopoulos, “Development of a chemically defined medium and discovery of new mitogenic growth factors for mouse hepatocytes: mitogenic effects of FGF1/2 and PDGF,” PLoS ONE, vol. 9, no. 4, Article ID e95487, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. C. B. Klein, J. Leszczynska, C. Hickey, and T. G. Rossman, “Further evidence against a direct genotoxic mode of action for arsenic-induced cancer,” Toxicology and Applied Pharmacology, vol. 222, no. 3, pp. 289–297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. E. V. Komissarova, P. Li, A. N. Uddin, X. Chen, A. Nadas, and T. G. Rossman, “Gene expression levels in normal human lymphoblasts with variable sensitivities to arsenite: identification of GGT1 and NFKBIE expression levels as possible biomarkers of susceptibility,” Toxicology and Applied Pharmacology, vol. 226, no. 2, pp. 199–205, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. 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
  38. S. B. Berman, S. C. Watkins, and T. G. Hastings, “Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: evidence for reduced sensitivity of brain mitochondria,” Experimental Neurology, vol. 164, no. 2, pp. 415–425, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Bustamante, L. Nutt, S. Orrenius, and V. Gogvadze, “Arsenic stimulates release of cytochrome c from isolated mitochondria via induction of mitochondrial permeability transition,” Toxicology and Applied Pharmacology, vol. 207, supplement 2, pp. S110–S116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. Y.-H. Jiao, Q. Zhang, L.-L. Pan et al., “Rat liver mitochondrial dysfunction induced by an organic arsenical compound 4-(2-nitrobenzaliminyl) phenyl arsenoxide,” Journal of Membrane Biology, vol. 248, no. 6, pp. 1071–1078, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Santra, A. Chowdhury, S. Ghatak, A. Biswas, and G. K. Dhali, “Arsenic induces apoptosis in mouse liver is mitochondria dependent and is abrogated by N-acetylcysteine,” Toxicology and Applied Pharmacology, vol. 220, no. 2, pp. 146–155, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. P. R. Gentry, T. B. McDonald, D. E. Sullivan, A. M. Shipp, J. W. Yager, and H. J. Clewell III, “Analysis of genomic dose-response information on arsenic to inform key events in a mode of action for carcinogenicity,” Environmental and Molecular Mutagenesis, vol. 51, no. 1, pp. 1–14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Finkel, “Signal transduction by mitochondrial oxidants,” Journal of Biological Chemistry, vol. 287, no. 7, pp. 4434–4440, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Finkel, “Signal transduction by reactive oxygen species,” Journal of Cell Biology, vol. 194, no. 1, pp. 7–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Scialo, V. Mallikarjun, R. Stefanatos, and A. Sanz, “Regulation of lifespan by the mitochondrial electron transport chain: reactive oxygen species-dependent and reactive oxygen species-independent mechanisms,” Antioxidants and Redox Signaling, vol. 19, no. 16, pp. 1953–1969, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Stefanatos and A. Sanz, “Mitochondrial complex I: a central regulator of the aging process,” Cell Cycle, vol. 10, no. 10, pp. 1528–1532, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. E. T. Snow, P. Sykora, T. R. Durham, and C. B. Klein, “Arsenic, mode of action at biologically plausible low doses: what are the implications for low dose cancer risk?” Toxicology and Applied Pharmacology, vol. 207, no. 2, pp. 557–564, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. T.-C. Zhang, M. T. Schmitt, and J. L. Mumford, “Effects of arsenic on telomerase and telomeres in relation to cell proliferation and apoptosis in human keratinocytes and leukemia cells in vitro,” Carcinogenesis, vol. 24, no. 11, pp. 1811–1817, 2003. View at Publisher · View at Google Scholar · View at Scopus