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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 8923860, 8 pages
http://dx.doi.org/10.1155/2016/8923860
Research Article

Nrf2/ARE Pathway Involved in Oxidative Stress Induced by Paraquat in Human Neural Progenitor Cells

School of Public Health and Key Laboratory of Public Health Safety of the Ministry of Education, Fudan University, Shanghai 200032, China

Received 11 June 2015; Accepted 8 July 2015

Academic Editor: Michela Battistelli

Copyright © 2016 Tingting Dou 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. Y.-W. Chen, Y.-T. Yang, D.-Z. Hung, C.-C. Su, and K.-L. Chen, “Paraquat induces lung alveolar epithelial cell apoptosis via Nrf-2-regulated mitochondrial dysfunction and ER stress,” Archives of Toxicology, vol. 86, no. 10, pp. 1547–1558, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. R. J. Dinis-Oliveira, F. Remião, H. Carmo et al., “Paraquat exposure as an etiological factor of Parkinson's disease,” NeuroToxicology, vol. 27, no. 6, pp. 1110–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. C.-Y. Lee, C.-H. Lee, C.-C. Shih, and H.-H. Liou, “Paraquat inhibits postsynaptic AMPA receptors on dopaminergic neurons in the substantia nigra pars compacta,” Biochemical Pharmacology, vol. 76, no. 9, pp. 1155–1164, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Prasad, E. Tarasewicz, J. Mathew et al., “Toxicokinetics and toxicodynamics of paraquat accumulation in mouse brain,” Experimental Neurology, vol. 215, no. 2, pp. 358–367, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. Registration Eligibility Decision (RED), Office of Prevention, Pesticides and Toxic Substances, United States Environmental Protection Agency, EPA 738-F-96-018: Paraquat dichloride, US EPA, Washington, DC, USA, 1997, http://www.epa.gov/pesticides/reregistration/status.htm.
  6. K. R. Reuhl, “Delayed expression of neurotoxicity: the problem of silent damage,” NeuroToxicology, vol. 12, no. 3, pp. 341–346, 1991. View at Google Scholar · View at Scopus
  7. B. K. Barlow, D. A. Cory-Slechta, E. K. Richfield, and M. Thiruchelvam, “The gestational environment and Parkinson's disease: evidence for neurodevelopmental origins of a neurodegenerative disorder,” Reproductive Toxicology, vol. 23, no. 3, pp. 457–470, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. A. M. Tsatsakis, K. Perakis, and E. Koumantakis, “Experience with acute paraquat poisoning in Crete,” Veterinary and Human Toxicology, vol. 38, no. 2, pp. 113–117, 1996. View at Google Scholar · View at Scopus
  9. X. Chang, W. Lu, T. Dou et al., “Paraquat inhibits cell viability via enhanced oxidative stress and apoptosis in human neural progenitor cells,” Chemico-Biological Interactions, vol. 206, no. 2, pp. 248–255, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. J. S. Bus, S. D. Aust, and J. E. Gibson, “Superoxide- and singlet oxygen-catalyzed lipid peroxidation as a possible mechanism for paraquat (methyl viologen) toxicity,” Biochemical and Biophysical Research Communications, vol. 58, no. 3, pp. 749–755, 1974. View at Publisher · View at Google Scholar · View at Scopus
  11. J. S. Bus, S. Z. Cagen, M. Olgaard, and J. E. Gibson, “A mechanism of paraquat toxicity in mice and rats,” Toxicology and Applied Pharmacology, vol. 35, no. 3, pp. 501–513, 1976. View at Publisher · View at Google Scholar · View at Scopus
  12. C.-S. Lai and L. H. Piette, “Hydroxyl radical production involved in lipid peroxidation of rat liver microsomes,” Biochemical and Biophysical Research Communications, vol. 78, no. 1, pp. 51–59, 1977. View at Publisher · View at Google Scholar · View at Scopus
  13. D. A. Drechsel and M. Patel, “Chapter 21 paraquat-induced production of reactive oxygen species in brain mitochondria,” Methods in Enzymology, vol. 456, pp. 381–393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Zaidi, D. Fernandes, J. L. Bean, and M. L. Michaelis, “Effects of paraquat-induced oxidative stress on the neuronal plasma membrane Ca2+-ATPase,” Free Radical Biology and Medicine, vol. 47, no. 10, pp. 1507–1514, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. Q. Chen, Y. Niu, R. Zhang et al., “The toxic influence of paraquat on hippocampus of mice: involvement of oxidative stress,” NeuroToxicology, vol. 31, no. 3, pp. 310–316, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Adrain and S. J. Martin, “The mitochondrial apoptosome: a killer unleashed by the cytochrome seas,” Trends in Biochemical Sciences, vol. 26, no. 6, pp. 390–397, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Sadasivam, S. Gupta, V. Radha, K. Batta, T. K. Kundu, and G. Swarup, “Caspase-1 activator Ipaf is a p53-inducible gene involved in apoptosis,” Oncogene, vol. 24, no. 4, pp. 627–636, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Munday and C. M. Munday, “Induction of phase II detoxification enzymes in rats by plant-derived isothiocyanates: comparison of allyl isothiocyanate with sulforaphane and related compounds,” Journal of Agricultural and Food Chemistry, vol. 52, no. 7, pp. 1867–1871, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. J. A. Rubiolo, G. Mithieux, and F. V. Vega, “Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes,” European Journal of Pharmacology, vol. 591, no. 1–3, pp. 66–72, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. K. Kim, J. W. Yang, M. R. Kim et al., “Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells,” Free Radical Biology and Medicine, vol. 45, no. 4, pp. 537–546, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. H.-Y. Cho, A. E. Jedlicka, S. P. M. Reddy et al., “Role of NRF2 in protection against hyperoxic lung injury in mice,” The American Journal of Respiratory Cell and Molecular Biology, vol. 26, no. 2, pp. 175–182, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Claudio, W. C. Kwa, A. L. Russell, and D. Wallinga, “Testing methods for developmental neurotoxicity of environmental chemicals,” Toxicology and Applied Pharmacology, vol. 164, no. 1, pp. 1–14, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. H. A. Tilson, “Neurotoxicology risk assessment guidelines: developmental neurotoxicology,” NeuroToxicology, vol. 21, no. 1-2, pp. 189–194, 2000. View at Google Scholar · View at Scopus
  24. B. A. Reynolds, W. Tetzlaff, and S. Weiss, “A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes,” Journal of Neuroscience, vol. 12, no. 11, pp. 4565–4574, 1992. View at Google Scholar · View at Scopus
  25. R. Donato, E. A. Miljan, S. J. Hines et al., “Differential development of neuronal physiological responsiveness in two human neural stem cell lines,” BMC Neuroscience, vol. 8, article 36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. J.-M. Zhang, H.-C. Wang, H.-X. Wang et al., “Oxidative stress and activities of caspase-8, -9, and -3 are involved in cryopreservation-induced apoptosis in granulosa cells,” European Journal of Obstetrics & Gynecology and Reproductive Biology, vol. 166, no. 1, pp. 52–55, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Min, S. He, Q. Chen, F. Peng, H. Peng, and M. Xie, “Comparative proteomic analysis of cellular response of human airway epithelial cells (A549) to benzo(a)pyrene,” Toxicology Mechanisms and Methods, vol. 21, no. 5, pp. 374–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. M. Hussain and J. M. Frazier, “Cellular toxicity of hydrazine in primary rat hepatocytes,” Toxicological Sciences, vol. 69, no. 2, pp. 424–432, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Karakashev, L. Petrov, and A. Alexandrova, “Paraquat-induced lipid peroxidation and injury in Ehrlich ascites tumor cells,” Neoplasma, vol. 47, no. 2, pp. 122–124, 2000. View at Google Scholar · View at Scopus
  30. J. Li, D. Johnson, M. Calkins, L. Wright, C. Svendsen, and J. Johnson, “Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells,” Toxicological Sciences, vol. 83, no. 2, pp. 313–328, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. H.-C. Huang, T. Nguyen, and C. B. Pickett, “Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription,” The Journal of Biological Chemistry, vol. 277, no. 45, pp. 42769–42774, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Peter, M. Wartena, H. H. Kampinga, and A. W. T. Konings, “Role of lipid peroxidation and DNA damage in paraquat toxicity and the interaction of paraquat with ionizing radiation,” Biochemical Pharmacology, vol. 43, no. 4, pp. 705–715, 1992. View at Publisher · View at Google Scholar · View at Scopus
  33. C.-C. Lin, C.-L. Kuo, M.-H. Lee et al., “Wogonin triggers apoptosis in human osteosarcoma U-2 OS cells through the endoplasmic reticulum stress, mitochondrial dysfunction and caspase-3-dependent signaling pathways,” International Journal of Oncology, vol. 39, no. 1, pp. 217–224, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Liang and J. P. Sundberg, “SHARPIN regulates mitochondria-dependent apoptosis in keratinocytes,” Journal of Dermatological Science, vol. 63, no. 3, pp. 148–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Tsukamoto, Y. Tampo, M. Sawada, and M. Yonaha, “Paraquat-induced oxidative stress and dysfunction of the glutathione redox cycle in pulmonary microvascular endothelial cells,” Toxicology and Applied Pharmacology, vol. 178, no. 2, pp. 82–92, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Weidauer, T. Lehmann, A. Rämisch, E. Röhrdanz, and H. Foth, “Response of rat alveolar type II cells and human lung tumor cells towards oxidative stress induced by hydrogen peroxide and paraquat,” Toxicology Letters, vol. 151, no. 1, pp. 69–78, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Peng, F. F. Stevenson, M. L. Oo, and J. K. Andersen, “Iron-enhanced paraquat-mediated dopaminergic cell death due to increased oxidative stress as a consequence of microglial activation,” Free Radical Biology & Medicine, vol. 46, no. 2, pp. 312–320, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Hertzmann, M. Wiens, D. Bowering, B. Snow, and D. Calne, “Parkinson's disease: a case-control study of occupational and environmental risk factors,” American Journal of Industrial Medicine, vol. 17, no. 3, pp. 349–355, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. K. M. Semchuk, E. J. Love, and R. G. Lee, “Parkinson's disease and exposure to agricultural work and pesticide chemicals,” Neurology, vol. 42, no. 7, pp. 1328–1335, 1992. View at Publisher · View at Google Scholar · View at Scopus
  40. H. T. Hogberg, A. Kinsner-Ovaskainen, T. Hartung, S. Coecke, and A. K. Bal-Price, “Gene expression as a sensitive endpoint to evaluate cell differentiation and maturation of the developing central nervous system in primary cultures of rat cerebellar granule cells (CGCs) exposed to pesticides,” Toxicology and Applied Pharmacology, vol. 235, no. 3, pp. 268–286, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Takizawa, K. Komori, Y. Tampo, and M. Yonaha, “Paraquat-induced oxidative stress and dysfunction of cellular redox systems including antioxidative defense enzymes glutathione peroxidase and thioredoxin reductase,” Toxicology in Vitro, vol. 21, no. 3, pp. 355–363, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Yang and E. Tiffany-Castiglioni, “The bipyridyl herbicide paraquat produces oxidative stress-mediated toxicity in human neuroblastoma SH-SY5Y cells: relevance to the dopaminergic pathogenesis,” Journal of Toxicology and Environmental Health A, vol. 68, no. 22, pp. 1939–1961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M. G. Purisai, A. L. McCormack, S. Cumine, J. Li, M. Z. Isla, and D. A. Di Monte, “Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration,” Neurobiology of Disease, vol. 25, no. 2, pp. 392–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Y. Wu, Y.-Z. Fang, S. Yang, J. R. Lupton, and N. D. Turner, “Glutathione metabolism and its implications for health,” Journal of Nutrition, vol. 134, no. 3, pp. 489–492, 2004. View at Google Scholar · View at Scopus
  45. T. Nguyen, P. J. Sherratt, and C. B. Pickett, “Regulatory mechanisms controlling gene expression mediated by the antioxidant response element,” Annual Review of Pharmacology and Toxicology, vol. 43, pp. 233–260, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. M. McMahon, N. Thomas, K. Itoh, M. Yamamoto, and J. D. Hayes, “Dimerization of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a ‘Tethering’ mechanism—a two-site interaction model for the Nrf2-Keap1 complex,” Journal of Biological Chemistry, vol. 281, no. 34, pp. 24756–24768, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Luo, A. L. Eggler, D. Liu, G. Liu, A. D. Mesecar, and R. B. van Breemen, “Sites of alkylation of human Keap1 by natural Chemoprevention agents,” Journal of the American Society for Mass Spectrometry, vol. 18, no. 12, pp. 2226–2232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. J.-P. Ren, Y.-W. Zhao, and X.-J. Sun, “Toxic influence of chronic oral administration of paraquat on nigrostriatal dopaminergic neurons in C57BL/6 mice,” Chinese Medical Journal, vol. 122, no. 19, pp. 2366–2371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. W. Yang, E. Tiffany-Castiglioni, M.-Y. Lee, and I.-H. Son, “Paraquat induces cyclooxygenase-2 (COX-2) implicated toxicity in human neuroblastoma SH-SY5Y cells,” Toxicology Letters, vol. 199, no. 3, pp. 239–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. P. L. Apopa, X. He, and Q. Ma, “Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells,” Journal of Biochemical and Molecular Toxicology, vol. 22, no. 1, pp. 63–76, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. C.-L. Huang, Y.-C. Lee, Y.-C. Yang, T.-Y. Kuo, and N.-K. Huang, “Minocycline prevents paraquat-induced cell death through attenuating endoplasmic reticulum stress and mitochondrial dysfunction,” Toxicology Letters, vol. 209, no. 3, pp. 203–210, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. Y.-C. Wang, C.-M. Lee, L.-C. Lee et al., “Mitochondrial dysfunction and oxidative stress contribute to the pathogenesis of spinocerebellar ataxia type 12 (SCA12),” The Journal of Biological Chemistry, vol. 286, no. 24, pp. 21742–21754, 2011. View at Publisher · View at Google Scholar · View at Scopus