Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016, Article ID 2548792, 18 pages
http://dx.doi.org/10.1155/2016/2548792
Review Article

Potential Role of Epigenetic Mechanism in Manganese Induced Neurotoxicity

1Environmental Health Division, CSIR-National Environmental Engineering Research Institute, Nagpur 440020, India
2Visvesvaraya National Institute of Technology (VNIT), Nagpur 440010, India

Received 17 February 2016; Accepted 8 May 2016

Academic Editor: Andrei Surguchov

Copyright © 2016 Prashant Tarale 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. C. Cotzias, “Manganese in health and disease,” Physiological Reviews, vol. 38, no. 3, pp. 503–532, 1958. View at Google Scholar · View at Scopus
  2. A. Takeda, “Manganese action in brain function,” Brain Research Reviews, vol. 41, no. 1, pp. 79–87, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. K. M. Erikson, D. C. Dorman, L. H. Lash, and M. Aschner, “Manganese inhalation by rhesus monkeys is associated with brain regional changes in biomarkers of neurotoxicity,” Toxicological Sciences, vol. 97, no. 2, pp. 459–466, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Tamm, F. Sabri, and S. Ceccatelli, “Mitochondrial-mediated apoptosis in neural stem cells exposed to manganese,” Toxicological Sciences, vol. 101, no. 2, pp. 310–320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. M. Antonini, A. B. Santamaria, N. T. Jenkins, E. Albini, and R. Lucchini, “Fate of manganese associated with the inhalation of welding fumes: potential neurological effects,” NeuroToxicology, vol. 27, no. 3, pp. 304–310, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. B. Goldhaber, “Trace element risk assessment: essentiality vs. Toxicity,” Regulatory Toxicology and Pharmacology, vol. 38, no. 2, pp. 232–242, 2003. View at Publisher · View at Google Scholar
  7. J. Rodier, “Manganese poisoning in Moroccan miners,” British Journal of Industrial Medicine, vol. 12, no. 1, pp. 21–35, 1955. View at Google Scholar · View at Scopus
  8. R. Settivari, N. VanDuyn, J. LeVora, and R. Nass, “The Nrf2/SKN-1-dependent glutathione S-transferase π homologue GST-1 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of manganism,” NeuroToxicology, vol. 38, pp. 51–60, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Gorell, E. L. Peterson, B. A. Rybicki, and C. C. Johnson, “Multiple risk factors for Parkinson's disease,” Journal of the Neurological Sciences, vol. 217, no. 2, pp. 169–174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Gorell, C. C. Johnson, B. A. Rybicki et al., “Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease,” NeuroToxicology, vol. 20, no. 2-3, pp. 239–248, 1999. View at Google Scholar · View at Scopus
  11. D. J. Betteridge, “What is oxidative stress?” Metabolism, vol. 49, no. 2, pp. 3–8, 2000. View at Google Scholar · View at Scopus
  12. V. V. Dukhande, G. H. Malthankar-Phatak, J. J. Hugus, C. K. Daniels, and J. C. K. Lai, “Manganese-induced neurotoxicity is differentially enhanced by glutathione depletion in astrocytoma and neuroblastoma cells,” Neurochemical Research, vol. 31, no. 11, pp. 1349–1357, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Orrenius, V. Gogvadze, and B. Zhivotovsky, “Mitochondrial oxidative stress: implications for cell death,” Annual Review of Pharmacology and Toxicology, vol. 47, pp. 143–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Schnekenburger, G. Talaska, and A. Puga, “Chromium cross-links histone deacetylase 1-DNA methyltransferase 1 complexes to chromatin, inhibiting histone-remodeling marks critical for transcriptional activation,” Molecular and Cellular Biology, vol. 27, no. 20, pp. 7089–7101, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Abel and R. S. Zukin, “Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders,” Current Opinion in Pharmacology, vol. 8, no. 1, pp. 57–64, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. F. D. Dick, G. De Palma, A. Ahmadi et al., “Environmental risk factors for Parkinson's disease and parkinsonism: the Geoparkinson study,” Occupational and Environmental Medicine, vol. 64, no. 10, pp. 666–672, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Cai, T. Yao, G. Zheng et al., “Manganese induces the overexpression of α-synuclein in PC12cells via ERK activation. Brain Research,” Brain Research Bulletin, vol. 1359, pp. 201–210, 2010. View at Publisher · View at Google Scholar
  18. Y. Li, L. Sun, T. Cai et al., “α-Synuclein overexpression during manganese-induced apoptosis in SH-SY5Y neuroblastoma cells,” Brain Research Bulletin, vol. 81, no. 4-5, pp. 428–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Baccarelli and V. Bollati, “Epigenetics and environmental chemicals,” Current Opinion in Pediatrics, vol. 21, no. 2, pp. 243–251, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Lucchini and N. Zimmerman, “Lifetime cumulative exposure as a threat for neurodegeneration: need for prevention strategies on a global scale,” NeuroToxicology, vol. 30, no. 6, pp. 1144–1148, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. K. S. Crump, “Manganese exposures in Toronto during use of the gasoline additive, methylcyclopentadienyl manganese tricarbonyl,” Journal of Exposure Analysis and Environmental Epidemiology, vol. 10, no. 3, pp. 227–239, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. D. R. Lynam, J. W. Roos, G. D. Pfeifer, B. F. Fort, and T. G. Pullin, “Environmental effects and exposures to manganese from use of methylcyclopentadienyl manganese tricarbonyl (MMT) in gasoline,” NeuroToxicology, vol. 20, no. 2-3, pp. 145–150, 1999. View at Google Scholar · View at Scopus
  23. J. Zayed, M. Gerin, S. Loranger, P. Sierra, D. Begin, and G. Kennedy, “Occupational and environmental exposure of garage workers and taxi drivers to airborne manganese arising from the use of methylcyclopentadienyl manganese tricarbonyl in unleaded gasoline,” American Industrial Hygiene Association Journal, vol. 55, no. 1, pp. 53–58, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. WHO, “Guidelines for Drinking-Water Quality,” Incorporating First Addendum, 2006, http://www.who.int/water_sanitation_health/dwq/gdwq0506begin.pdf.
  25. K. Ljung and M. Vahter, “Time to re-evaluate the guideline value for manganese in drinking water?” Environmental Health Perspectives, vol. 115, no. 11, pp. 1533–1538, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. M. F. Bouchard, S. Sauvé, B. Barbeau et al., “Intellectual impairment in school-age children exposed to manganese from drinking water,” Environmental Health Perspectives, vol. 119, no. 1, pp. 138–143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Sharma and S. Pervez, “Toxic metals status in human blood and breast milk samples in an integrated steel plant environment in Central India,” Environmental Geochemistry and Health, vol. 27, no. 1, pp. 39–45, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. ATSDR, Toxicological Profile for Manganese, United States Department of Health and Human Services, Atlanta, Ga, USA, 2012.
  29. K. A. Cockell, G. Bonacci, and B. Belonje, “Manganese content of soy or rice beverages is high in comparison to infant formulas,” Journal of the American College of Nutrition, vol. 23, no. 2, pp. 124–130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. A. W. Dobson, K. M. Erikson, and M. Aschner, “Manganese neurotoxicity,” Annals of the New York Academy of Sciences, vol. 1012, pp. 115–128, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. J. R. Roede, J. M. Hansen, Y.-M. Go, and D. P. Jones, “Maneb and paraquat-mediated neurotoxicity: involvement of peroxiredoxin/thioredoxin system,” Toxicological Sciences, vol. 121, no. 2, pp. 368–375, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Ritz and F. Yu, “Parkinson's disease mortality and pesticide exposure in California 1984–1994,” International Journal of Epidemiology, vol. 29, no. 2, pp. 323–329, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. D. A. Drechsel and M. Patel, “Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease,” Free Radical Biology and Medicine, vol. 44, no. 11, pp. 1873–1886, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Thompson, R. Molina, T. Donaghey, J. D. Brain, and M. Wessling-Resnick, “The influence of high iron diet on rat lung manganese absorption,” Toxicology and Applied Pharmacology, vol. 210, no. 1-2, pp. 17–23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. M. M. Finkelstein and M. Jerrett, “A study of the relationships between Parkinson's disease and markers of traffic-derived and environmental manganese air pollution in two Canadian cities,” Environmental Research, vol. 104, no. 3, pp. 420–432, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. E. L. Lucas, P. Bertrand, S. Guazzetti et al., “Impact of ferromanganese alloy plants on household dust manganese levels: implications for childhood exposure,” Environmental Research, vol. 138, pp. 279–290, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. G. A. Wasserman, X. Liu, F. Parvez et al., “Water manganese exposure and children's intellectual function in Araihazar, Bangladesh,” Environmental Health Perspectives, vol. 114, no. 1, pp. 124–129, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. B. A. Racette, S. R. Criswell, J. I. Lundin et al., “Increased risk of parkinsonism associated with welding exposure,” NeuroToxicology, vol. 33, no. 5, pp. 1356–1361, 2012. View at Publisher · View at Google Scholar
  39. S. R. Criswell, J. S. Perlmutter, T. O. Videen et al., “Reduced uptake of [18F]FDOPA PET in asymptomatic welders with occupational manganese exposure,” Neurology, vol. 76, no. 15, pp. 1296–1301, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. S. R. Criswell, J. S. Perlmutter, J. L. Huang et al., “Basal ganglia intensity indices and diffusion weighted imaging in manganese-exposed welders,” Occupational and Environmental Medicine, vol. 69, no. 6, pp. 437–443, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. R. G. Lucchini, E. Albini, L. Benedetti et al., “High prevalence of Parkinsonian disorders associated to manganese exposure in the vicinities of ferroalloy industries,” American Journal of Industrial Medicine, vol. 50, no. 11, pp. 788–800, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. R. G. Lucchini, S. Guazzetti, S. Zoni et al., “Neurofunctional dopaminergic impairment in elderly after lifetime exposure to manganese,” NeuroToxicology, vol. 45, pp. 309–317, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. WHO, Manganese. Environmental Health Criteria 17, World Health Organization, Geneva, Switzerland, 1981.
  44. D. A. Cory-Slechta, “Studying toxicants as single chemicals: does this strategy adequately identify neurotoxic risk?” NeuroToxicology, vol. 26, no. 4, pp. 491–510, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Sanchez-Betancourt, V. Anaya-Martínez, A. L. Gutierrez-Valdez et al., “Manganese mixture inhalation is a reliable Parkinson disease model in rats,” NeuroToxicology, vol. 33, no. 5, pp. 1346–1355, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Yamada, S. Ohno, I. Okayasu et al., “Chronic manganese poisoning: a neuropathological study with determination of manganese distribution in the brain,” Acta Neuropathologica, vol. 70, no. 3-4, pp. 273–278, 1986. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Choi, J. K. Park, N. H. Park et al., “Whole blood and red blood cell manganese reflected signal intensities of T1-weighted magnetic resonance images better than plasma manganese in liver cirrhotics,” Journal of Occupational Health, vol. 47, no. 1, pp. 68–73, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. J. D. Park, Y. H. Chung, C. Y. Kim et al., “Comparison of high MRI T1 signals with manganese concentration in brains of cynomolgus monkeys after 8 months of stainless steel welding-fume exposure,” Inhalation Toxicology, vol. 19, no. 11, pp. 965–971, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. J. A. Roth and M. D. Garrick, “Iron interactions and other biological reactions mediating the physiological and toxic actions of manganese,” Biochemical Pharmacology, vol. 66, no. 1, pp. 1–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. T. R. Guilarte, M.-K. Chen, J. L. McGlothan et al., “Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates,” Experimental Neurology, vol. 202, no. 2, pp. 381–390, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. T. R. Guilarte, N. C. Burton, J. L. McGlothan et al., “Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism,” Journal of Neurochemistry, vol. 107, no. 5, pp. 1236–1247, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. T. M. Peneder, P. Scholze, M. L. Berger et al., “Chronic exposure to manganese decreases striatal dopamine turnover in human alpha-synuclein transgenic mice,” Neuroscience, vol. 180, pp. 280–292, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Kim, J.-M. Kim, J.-W. Kim et al., “Dopamine transporter density is decreased in Parkinsonian patients with a history of manganese exposure: what does it mean?” Movement Disorders, vol. 17, no. 3, pp. 568–575, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. B. A. Racette, L. McGee-Minnich, S. M. Moerlein, J. W. Mink, T. O. Videen, and J. S. Perlmutter, “Welding-related parkinsonism: clinical-features, treatment, and pathophysiology,” Neurology, vol. 56, no. 1, pp. 8–13, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. W. C. Koller, K. E. Lyons, and W. Truly, “Effect of levodopa treatment for parkinsonism in welders: a double-blind study,” Neurology, vol. 62, no. 5, pp. 730–733, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. J. A. Garcia-Aranda, R. A. Wapnir, and F. Lifshitz, “In vivo intestinal absorption of manganese in the rat,” The Journal of Nutrition, vol. 113, no. 12, pp. 2601–2607, 1983. View at Google Scholar
  57. S. J. Garcia, K. Gellein, T. Syversen, and M. Aschner, “Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain,” Toxicological Sciences, vol. 95, no. 1, pp. 205–214, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Latchoumycandane, V. Anantharam, M. Kitazawa, Y. Yang, A. Kanthasamy, and A. G. Kanthasamy, “Protein kinase Cδ is a key downstream mediator of manganese-induced apoptosis in dopaminergic neuronal cells,” Journal of Pharmacology and Experimental Therapeutics, vol. 313, no. 1, pp. 46–55, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Chtourou, K. Trabelsi, H. Fetoui, G. Mkannez, H. Kallel, and N. Zeghal, “Manganese induces oxidative stress, redox state unbalance and disrupts membrane bound ATPases on murine neuroblastoma cells in vitro: protective role of silymarin,” Neurochemical Research, vol. 36, no. 8, pp. 1546–1557, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. C. E. Gavin, K. K. Gunter, and T. E. Gunter, “Manganese and calcium transport in mitochondria: implications for manganese toxicity,” NeuroToxicology, vol. 20, no. 2-3, pp. 445–454, 1999. View at Google Scholar · View at Scopus
  61. Y. Kushnareva, A. N. Murphy, and A. Andreyev, “Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state,” Biochemical Journal, vol. 368, no. 2, pp. 545–553, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Bornhorst, S. Meyer, T. Weber et al., “Molecular mechanisms of Mn induced neurotoxicity: RONS generation, genotoxicity, and DNA-damage response,” Molecular Nutrition and Food Research, vol. 57, no. 7, pp. 1255–1269, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. R. S. Balaban, “Cardiac energy metabolism homeostasis: role of cytosolic calcium,” Journal of Molecular and Cellular Cardiology, vol. 34, pp. 11259–11271, 2002. View at Google Scholar
  64. T. E. Gunter, C. E. Gavin, M. Aschner, and K. K. Gunter, “Speciation of manganese in cells and mitochondria: a search for the proximal cause of manganese neurotoxicity,” Neurotoxicology, vol. 27, pp. 765–776, 2006. View at Google Scholar
  65. P. G. Haydon and G. Carmignoto, “Astrocyte control of synaptic transmission and neurovascular coupling,” Physiological Reviews, vol. 86, no. 3, pp. 1009–1031, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. G. Burnstock, U. Krügel, M. P. Abbracchio, and P. Illes, “Purinergic signalling: from normal behaviour to pathological brain function,” Progress in Neurobiology, vol. 95, no. 2, pp. 229–274, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Shirakawa, “Pathophysiological significance of canonical transient receptor potential (TRPC) subfamily in astrocyte activation,” Yakugaku Zasshi, vol. 132, no. 5, pp. 587–593, 2012. View at Publisher · View at Google Scholar
  68. K. M. Streifel, J. Miller, R. Mouneimne, and R. B. Tjalkens, “Manganese inhibits ATP-induced calcium entry through the transient receptor potential channel TRPC3 in astrocytes,” NeuroToxicology, vol. 34, no. 1, pp. 160–166, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Kitazawa, V. Anantharam, Y. Yang, Y. Hirata, A. Kanthasamy, and A. G. Kanthasamy, “Activation of protein kinase Cδ by proteolytic cleavage contributes to manganese-induced apoptosis in dopaminergic cells: protective role of Bcl-2,” Biochemical Pharmacology, vol. 69, no. 1, pp. 133–146, 2005. View at Publisher · View at Google Scholar
  70. C. Latchoumycandane, V. Anantharam, H. Jin, A. Kanthasamy, and A. Kanthasamy, “Dopaminergic neurotoxicant 6-OHDA induces oxidative damage through proteolytic activation of PKCδ in cell culture and animal models of Parkinson's disease,” Toxicology and Applied Pharmacology, vol. 256, no. 3, pp. 314–323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. D. Zhang, A. Kanthasamy, V. Anantharam, and A. Kanthasamy, “Effects of manganese on tyrosine hydroxylase (TH) activity and TH-phosphorylation in a dopaminergic neural cell line,” Toxicology and Applied Pharmacology, vol. 254, no. 2, pp. 65–71, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Kitazawa, J. R. Wagner, M. L. Kirby, V. Anantharam, and A. G. Kanthasamy, “Oxidative stress and mitochondrial-mediated apoptosis in dopaminergic cells exposed to methylcyclopentadienyl manganese tricarbonyl,” Journal of Pharmacology and Experimental Therapeutics, vol. 302, no. 1, pp. 26–35, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Bakthavatsalam, S. D. Sharma, M. Sonawane, V. Thirumalai, and A. Datta, “A zebrafish model of manganism reveals reversible and treatable symptoms that are independent of neurotoxicity,” Disease Models and Mechanisms, vol. 7, no. 11, pp. 1239–1251, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Wang, H. Lou, C. J. Pedersen, A. D. Smith, and R. G. Perez, “14-3-3ζ contributes to tyrosine hydroxylase activity in MN9D cells: localization of dopamine regulatory proteins to mitochondria,” The Journal of Biological Chemistry, vol. 284, no. 21, pp. 14011–14019, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. P. Zhang, A. Hatter, and B. Liu, “Manganese chloride stimulates rat microglia to release hydrogen peroxide,” Toxicology Letters, vol. 173, no. 2, pp. 88–100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. Xing, Z. Li, Y. Chen, J. B. Stock, P. D. Jeffrey, and Y. Shi, “Structural mechanism of demethylation and inactivation of protein phosphatase 2A,” Cell, vol. 133, no. 1, pp. 154–163, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Donaldson, F. S. LaBella, and D. Gesser, “Enhanced autoxidation of dopamine as a possible basis of manganese neurotoxicity,” Neurotoxicology L, no. 1, pp. 53–64, 1981. View at Google Scholar
  78. X. Liu, K. A. Sullivan, J. E. Madl, M. Legare, and R. B. Tjalkens, “Manganese-induced neurotoxicity: the role of astroglial-derived nitric oxide in striatal interneuron degeneration,” Toxicological Sciences, vol. 91, no. 2, pp. 521–531, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. T. R. Guilarte, “Manganese neurotoxicity: new perspectives from behavioral, neuroimaging, and neuropathological studies in humans and non-human primates,” Frontiers in Aging Neuroscience, vol. 5, article 23, pp. 1–10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Matsushima, J. Kuroda, T. Ago et al., “Increased oxidative stress in the nucleus caused by Nox4 mediates oxidation of HDAC4 and cardiac hypertrophy,” Circulation Research, vol. 112, no. 4, pp. 651–663, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. D. Milatovic and M. Aschner, “Measurement of isoprostanes as markers of oxidative stress in neuronal tissue,” Current Protocols in Toxicology, vol. 12, no. 14, pp. 1–12, 2009. View at Google Scholar
  82. D. Milatovic, S. Zaja-Milatovic, R. C. Gupta, Y. Yu, and M. Aschner, “Oxidative damage and neurodegeneration in manganese-induced neurotoxicity,” Toxicology and Applied Pharmacology, vol. 240, no. 2, pp. 219–225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Liu, H.-M. Gao, J.-Y. Wang, G.-H. Jeohn, C. L. Cooper, and J.-S. Hong, “Role of nitric oxide in inflammation-mediated neurodegeneration,” Annals of the New York Academy of Sciences, vol. 962, pp. 318–331, 2002. View at Publisher · View at Google Scholar · View at Scopus
  84. M. G. Tansey, M. K. McCoy, and T. C. Frank-Cannon, “Neuroinflammatory mechanisms in Parkinson's disease: potential environmental triggers, pathways, and targets for early therapeutic intervention,” Experimental Neurology, vol. 208, no. 1, pp. 1–25, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Cuschieri and R. V. Maier, “Mitogen-activated protein kinase (MAPK),” Critical Care Medicine, vol. 33, no. 12, pp. S417–S419, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. H. R. Rezvani, S. Dedieu, S. North et al., “Hypoxia-inducible factor-1α, a key factor in the keratinocyte response to UVB exposure,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 16413–16422, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Hirata, K. Adachi, and K. Kiuchi, “Phosphorylation and activation of p70 S6 kinase by manganese in PC12 cells,” NeuroReport, vol. 9, no. 13, pp. 3037–3040, 1998. View at Publisher · View at Google Scholar · View at Scopus
  88. J. A. McCubrey, M. M. LaHair, and R. A. Franklin, “Reactive oxygen species-induced activation of the MAP kinase signaling pathways,” Antioxidants and Redox Signaling, vol. 8, no. 9-10, pp. 1775–1789, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. K. M. Erikson, D. C. Dorman, V. Fitsanakis, L. H. Lash, and M. Aschner, “Alterations of oxidative stress biomarkers due to in utero and neonatal exposures of airborne manganese,” Biological Trace Element Research, vol. 111, no. 1–3, pp. 199–215, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. V. Exil, L. Ping, Y. Yu et al., “Activation of MAPK and FoxO by Manganese (Mn) in rat neonatal primary astrocyte cultures,” PLoS ONE, vol. 9, no. 5, article e94753, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Hirata, “Manganese-induced apoptosis in PC12 cells,” Neurotoxicology and Teratology, vol. 24, no. 5, pp. 639–653, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. W.-C. Chen and C.-C. Chen, “Signal transduction of arginine vasopressin-induced arachidonic acid release in H9c2 cardiac myoblasts: role of Ca2+ and the protein kinase C-dependent activation of p42 mitogen-activated protein kinase,” Endocrinology, vol. 140, no. 4, pp. 1639–1648, 1999. View at Google Scholar · View at Scopus
  93. S. C. Frasch, P. M. Henson, J. M. Kailey et al., “Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cδ,” Journal of Biological Chemistry, vol. 275, no. 30, pp. 23065–23073, 2000. View at Publisher · View at Google Scholar · View at Scopus
  94. I. Vancurova, V. Miskolci, and D. Davidson, “NF-κB activation in tumor necrosis factor α-stimulated neutrophils is mediated by protein kinase Cδ. Correlation to nuclear IκBα,” The Journal of Biological Chemistry, vol. 276, no. 23, pp. 19746–19752, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. H. S. Chun, H. Lee, and J. H. Son, “Manganese induces endoplasmic reticulum (ER) stress and activates multiple caspases in nigral dopaminergic neuronal cells, SN4741,” Neuroscience Letters, vol. 316, no. 1, pp. 5–8, 2001. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Sidoryk-Wegrzynowicz and M. Aschner, “Manganese toxicity in the central nervous system: the glutamine/glutamate-γ-aminobutyric acid cycle,” Journal of Internal Medicine, vol. 273, no. 5, pp. 466–477, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. B. Dipasquale, A. M. Marini, and R. J. Youle, “Apoptosis and DNA degradation induced by 1-methyl-4-phenylpyridinium in neurons,” Biochemical and Biophysical Research Communications, vol. 181, no. 3, pp. 1442–1448, 1991. View at Publisher · View at Google Scholar · View at Scopus
  98. C. Ma, S. N. Schneider, M. Miller et al., “Manganese accumulation in the mouse ear following systemic exposure,” Journal of Biochemical and Molecular Toxicology, vol. 22, no. 5, pp. 305–310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. J. Salazar, N. Mena, S. Hunot et al., “Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 47, pp. 18578–18583, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. D. Ding, J. Roth, and R. Salvi, “Manganese is toxic to spiral ganglion neurons and hair cells in vitro,” NeuroToxicology, vol. 32, no. 2, pp. 233–241, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. B. Li, M. Carey, and J. L. Workman, “The role of chromatin during transcription,” Cell, vol. 128, no. 4, pp. 707–719, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Kouzarides, “Chromatin modifications and their function,” Cell, vol. 128, no. 4, pp. 693–705, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Martinez-Zamudio and H. C. Ha, “Environmental epigenetics in metal exposure,” Epigenetics, vol. 6, no. 7, pp. 820–827, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. B. A. Fowler, M. H. Whittaker, M. Lipsky, G. Wang, and X.-Q. Chen, “Oxidative stress induced by lead, cadmium and arsenic mixtures: 30-day, 90-day, and 180-day drinking water studies in rats: an overview,” BioMetals, vol. 17, no. 5, pp. 567–568, 2004. View at Publisher · View at Google Scholar · View at Scopus
  105. K. V. Donkena, C. Y. F. Young, and D. J. Tindall, “Oxidative stress and DNA methylation in prostate cancer,” Obstetrics and Gynecology International, vol. 2010, Article ID 302051, 14 pages, 2010. View at Publisher · View at Google Scholar
  106. P. W. Turk, A. Laayoun, S. S. Smith, and S. A. Weitzman, “DNA adduct 8-hydroxyl-2′-deoxyguanosine (8-hydroxyguanine) affects function of human DNA methyltransferase,” Carcinogenesis, vol. 16, no. 5, pp. 1253–1255, 1995. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, “Free radicals, metals and antioxidants in oxidative stress-induced cancer,” Chemico-Biological Interactions, vol. 160, no. 1, pp. 1–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. X. Nan, H.-H. Ng, C. A. Johnson et al., “Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex,” Nature, vol. 393, no. 6683, pp. 386–389, 1998. View at Publisher · View at Google Scholar · View at Scopus
  109. P. L. Jones, G. J. C. Veenstra, P. A. Wade et al., “Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription,” Nature Genetics, vol. 19, no. 2, pp. 187–191, 1998. View at Publisher · View at Google Scholar · View at Scopus
  110. W.-G. Zhu, K. Srinivasan, Z. Dai et al., “Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21Cip1 promoter,” Molecular and Cellular Biology, vol. 23, no. 12, pp. 4056–4065, 2003. View at Publisher · View at Google Scholar · View at Scopus
  111. V. Valinluck, H.-H. Tsai, D. K. Rogstad, A. Burdzy, A. Bird, and L. C. Sowers, “Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2),” Nucleic Acids Research, vol. 32, no. 14, pp. 4100–4108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  112. X.-M. Shen and G. Dryhurst, “Iron- and manganese-catalyzed autoxidation of dopamine in the presence of L-cysteine: possible insights into iron- and manganese-mediated dopaminergic neurotoxicity,” Chemical Research in Toxicology, vol. 11, no. 7, pp. 824–837, 1998. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. Niu, T. L. DesMarais, Z. Tong, Y. Yao, and M. Costa, “Oxidative stress alters global histone modification and DNA methylation,” Free Radical Biology and Medicine, vol. 82, pp. 22–28, 2015. View at Publisher · View at Google Scholar · View at Scopus
  114. J. He, M. Wang, Y. Jiang et al., “Chronic arsenic exposure and angiogenesis in human bronchial epithelial cells via the ROS/miR-199a-5p/HIF-1α/COX-2 pathway,” Environmental Health Perspectives, vol. 122, no. 3, pp. 255–261, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Giatromanolaki, M. I. Koukourakis, E. Sivridis et al., “Relation of hypoxia inducible factor 1α and 2α in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival,” British Journal of Cancer, vol. 85, no. 6, pp. 881–890, 2001. View at Publisher · View at Google Scholar · View at Scopus
  116. H.-W. Hwang, L. L. Baxter, S. K. Loftus et al., “Distinct microRNA expression signatures are associated with melanoma subtypes and are regulated by HIF1A,” Pigment Cell and Melanoma Research, vol. 27, no. 5, pp. 777–787, 2014. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Nakayama, C. J. Bennett, J. L. Hicks et al., “Hypermethylation of the human glutathione S-transferase-π gene (GSTP1) CpG island is present in a subset of proliferative inflammatory atrophy lesions but not in normal or hyperplastic epithelium of the prostate: a detailed study using laser-capture microdissection,” The American Journal of Pathology, vol. 163, no. 3, pp. 923–933, 2003. View at Publisher · View at Google Scholar · View at Scopus
  118. M. Valko, M. Izakovic, M. Mazur, C. J. Rhodes, and J. Telser, “Role of oxygen radicals in DNA damage and cancer incidence,” Molecular and Cellular Biochemistry, vol. 266, no. 1-2, pp. 37–56, 2004. View at Publisher · View at Google Scholar · View at Scopus
  119. S.-O. Lim, J.-M. Gu, M. S. Kim et al., “Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter,” Gastroenterology, vol. 135, no. 6, pp. 2128–2140, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Chahrour, Y. J. Sung, C. Shaw et al., “MeCP2, a key contributor to neurological disease, activates and represses transcription,” Science, vol. 320, no. 5880, pp. 1224–1229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. W. J. Lukiw and A. I. Pogue, “Induction of specific micro RNA (miRNA) species by ROS-generating metal sulfates in primary human brain cells,” Journal of Inorganic Biochemistry, vol. 101, no. 9, pp. 1265–1269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  122. S. L. Berger, “The complex language of chromatin regulation during transcription,” Nature, vol. 447, no. 7143, pp. 407–412, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. L. Cantone, F. Nordio, L. Hou et al., “Inhalable metal-rich air particles and histone H3K4 dimethylation and H3K9 Acetylation in a Cross-sectional Study of Steel Workers,” Environmental Health Perspectives, vol. 119, no. 7, pp. 964–969, 2011. View at Publisher · View at Google Scholar · View at Scopus
  124. H. Braak, E. Ghebremedhin, U. Rüb, H. Bratzke, and K. Del Tredici, “Stages in the development of Parkinson's disease-related pathology,” Cell and Tissue Research, vol. 318, no. 1, pp. 121–134, 2004. View at Publisher · View at Google Scholar · View at Scopus
  125. W. Dauer and S. Przedborski, “Parkinson's disease: mechanisms and models,” Neuron, vol. 39, no. 6, pp. 889–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  126. K. F. Winklhofer and C. Haass, “Mitochondrial dysfunction in Parkinson's disease,” Biochimica et Biophysica Acta, vol. 1802, no. 1, pp. 29–44, 2010. View at Publisher · View at Google Scholar
  127. G. S. Tanner and S. M. Goldman, “Epidemiology of Parkinson's disease,” Neurologic Clinics, vol. 14, no. 2, pp. 317–335, 1996. View at Publisher · View at Google Scholar
  128. M. G. Spillantini, M. L. Schmidt, V. M.-Y. Lee, J. Q. Trojanowski, R. Jakes, and M. Goedert, “α-Synuclein in lewy bodies,” Nature, vol. 388, no. 6645, pp. 839–840, 1997. View at Publisher · View at Google Scholar · View at Scopus
  129. M. V. Padmaja, M. Jayaraman, A. V. Srinivasan, C. R. S. Srisailapathy, and A. Ramesh, “PARK2 gene mutations in early onset Parkinson's disease patients of South India,” Neuroscience Letters, vol. 523, no. 2, pp. 145–147, 2012. View at Publisher · View at Google Scholar · View at Scopus
  130. B. C. L. Lai, S. A. Marion, K. Teschke, and J. K. C. Tsui, “Occupational and environmental risk factors for Parkinson's disease,” Parkinsonism and Related Disorders, vol. 8, no. 5, pp. 297–309, 2002. View at Publisher · View at Google Scholar · View at Scopus
  131. T. R. Guilarte and K. K. Gonzales, “Manganese-induced parkinsonism is not idiopathic Parkinson's disease: environmental and genetic evidence,” Toxicological Sciences, vol. 146, no. 2, pp. 204–212, 2015. View at Publisher · View at Google Scholar · View at Scopus
  132. G. Xiromerisiou, E. Dardiotis, V. Tsimourtou et al., “Genetic basis of Parkinson disease,” Neurosurgical Focus, vol. 28, no. 1, article E7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. E.-K. Tan and L. M. Skipper, “Pathogenic mutations in Parkinson disease,” Human Mutation, vol. 28, no. 7, pp. 641–653, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. B. I. Giasson and V. M.-Y. Lee, “Are ubiquitination pathways central to Parkinson's disease?” Cell, vol. 114, no. 1, pp. 1–8, 2003. View at Publisher · View at Google Scholar · View at Scopus
  135. C. Au, A. Benedetto, and M. Aschner, “Manganese transport in eukaryotes: the role of DMT1,” NeuroToxicology, vol. 29, no. 4, pp. 569–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  136. M. Aschner, T. R. Guilarte, J. S. Schneider, and W. Zheng, “Manganese: recent advances in understanding its transport and neurotoxicity,” Toxicology and Applied Pharmacology, vol. 221, no. 2, pp. 131–147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. J. A. Roth, S. Singleton, J. Feng, M. Garrick, and P. N. Paradkar, “Parkin regulates metal transport via proteasomal degradation of the 1B isoforms of divalent metal transporter 1,” Journal of Neurochemistry, vol. 113, no. 2, pp. 454–464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  138. A. D. Gitler, A. Chesi, M. L. Geddie et al., “α-Synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity,” Nature Genetics, vol. 41, pp. 308–315, 2009. View at Publisher · View at Google Scholar
  139. R. Kumaran, J. Vandrovcova, C. Luk et al., “Differential DJ-1 gene expression in Parkinson's disease,” Neurobiology of Disease, vol. 36, no. 2, pp. 393–400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  140. J. Choi, M. C. Sullards, J. A. Olzmann et al., “Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases,” Journal of Biological Chemistry, vol. 281, no. 16, pp. 10816–10824, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. J. C. Greene, A. J. Whitworth, I. Kuo, L. A. Andrews, M. B. Feany, and L. J. Pallanck, “Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4078–4083, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. I. Irrcher, H. Aleyasin, E. L. Seifert et al., “Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics,” Human Molecular Genetics, vol. 19, no. 19, pp. 3734–3746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  143. E. Miñones-Moyano, S. Porta, G. Escaramís et al., “MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function,” Human Molecular Genetics, vol. 20, no. 15, pp. 3067–3078, 2011. View at Publisher · View at Google Scholar · View at Scopus
  144. J. J. Palacino, D. Sagi, M. S. Goldberg et al., “Mitochondrial dysfunction and oxidative damage in parkin-deficient mice,” The Journal of Biological Chemistry, vol. 279, no. 18, pp. 18614–18622, 2004. View at Publisher · View at Google Scholar · View at Scopus
  145. Y. Pesah, T. Pham, H. Burgess et al., “Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress,” Development, vol. 131, no. 9, pp. 2183–2194, 2004. View at Publisher · View at Google Scholar · View at Scopus
  146. L. Petrucelli, C. O'Farrell, P. J. Lockhart et al., “Parkin protects against the toxicity associated with mutant α-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons,” Neuron, vol. 36, no. 6, pp. 1007–1019, 2002. View at Publisher · View at Google Scholar · View at Scopus
  147. A. K. Berger, G. P. Cortese, K. D. Amodeo, A. Weihofen, A. Letai, and M. J. LaVoie, “Parkin selectively alters the intrinsic threshold for mitochondrial cytochrome c release,” Human Molecular Genetics, vol. 18, no. 22, pp. 4317–4328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  148. D. R. Green and G. Kroemer, “The pathophysiology of mitochondrial cell death,” Science, vol. 305, no. 5684, pp. 626–629, 2004. View at Publisher · View at Google Scholar · View at Scopus
  149. D. Eliezer, E. Kutluay, R. Bussell Jr., and G. Browne, “Conformational properties of α-synuclein in its free and lipid-associated states,” Journal of Molecular Biology, vol. 307, no. 4, pp. 1061–1073, 2001. View at Publisher · View at Google Scholar · View at Scopus
  150. S.-I. Kubo, V. M. Nemani, R. J. Chalkley et al., “A combinatorial code for the interaction of α-synuclein with membranes,” The Journal of Biological Chemistry, vol. 280, no. 36, pp. 31664–31672, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. M. R. Cookson, “α-Synuclein and neuronal cell death,” Molecular Neurodegeneration, vol. 4, no. 1, article 4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  152. A. Recchia, P. Debetto, A. Negro, D. Guidolin, S. D. Skaper, and P. Giusti, “α-Synuclein and Parkinson's disease,” The FASEB Journal, vol. 18, no. 6, pp. 617–626, 2004. View at Publisher · View at Google Scholar · View at Scopus
  153. W. P. Gai, H. X. Yuan, X. Q. Li, J. T. H. Power, P. C. Blumbergs, and P. H. Jensen, “In situ and in vitro study of colocalization and segregation of α-synuclein, ubiquitin, and lipids in Lewy bodies,” Experimental Neurology, vol. 166, no. 2, pp. 324–333, 2000. View at Publisher · View at Google Scholar · View at Scopus
  154. M. Hashimoto, L. J. Hsu, Y. Xia et al., “Oxidative stress induces amyloid-like aggregate formation of NACP/α- synuclein in vitro,” NeuroReport, vol. 10, no. 4, pp. 717–721, 1999. View at Publisher · View at Google Scholar · View at Scopus
  155. J. Xu, S.-Y. Kao, F. J. S. Lee, W. Song, L.-W. Jin, and B. A. Yankner, “Dopamine-dependent neurotoxicity of α-synuclein: a mechanism for selective neurodegeneration in Parkinson disease,” Nature Medicine, vol. 8, no. 6, pp. 600–606, 2002. View at Publisher · View at Google Scholar · View at Scopus
  156. J. Gründemann, F. Schlaudraff, O. Haeckel, and B. Liss, “Elevated α-synuclein mRNA levels in individual UV-laser-microdissected dopaminergic substantia nigra neurons in idiopathic Parkinson's disease,” Nucleic Acids Research, vol. 36, no. 7, article e38, 2008. View at Publisher · View at Google Scholar · View at Scopus
  157. I. Mizuta, W. Satake, Y. Nakabayashi et al., “Multiple candidate gene analysis identifies α-synuclein as a susceptibility gene for sporadic Parkinson's disease,” Human Molecular Genetics, vol. 15, no. 7, pp. 1151–1158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  158. A. Jowaed, I. Schmitt, O. Kaut, and U. Wüllner, “Methylation regulates alpha-synuclein expression and is decreased in Parkinson's disease patients' brains,” The Journal of Neuroscience, vol. 30, no. 18, pp. 6355–6359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  159. L. Matsumoto, H. Takuma, A. Tamaoka et al., “CpG demethylation enhances alpha-synuclein expression and affects the pathogenesis of Parkinson's disease,” PLoS ONE, vol. 5, no. 11, Article ID e15522, 2010. View at Publisher · View at Google Scholar · View at Scopus
  160. G. E. Voutsinas, E. F. Stavrou, G. Karousos et al., “Allelic imbalance of expression and epigenetic regulation within the alpha-synuclein wild-type and p.Ala53Thr alleles in Parkinson disease,” Human Mutation, vol. 31, no. 6, pp. 685–691, 2010. View at Publisher · View at Google Scholar · View at Scopus
  161. D. Bönsch, B. Lenz, J. Kornhuber, and S. Bleich, “DNA hypermethylation of the alpha synuclein promoter in patients with alcoholism,” Neuroreport, vol. 16, no. 2, pp. 167–170, 2005. View at Publisher · View at Google Scholar
  162. H. Frieling, A. Gozner, K. D. Römer et al., “Global DNA hypomethylation and DNA hypermethylation of the alpha synuclein promoter in females with anorexia nervosa,” Molecular Psychiatry, vol. 12, no. 3, pp. 229–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  163. E. Junn, K.-W. Lee, S. J. Byeong, T. W. Chan, J.-Y. Im, and M. M. Mouradian, “Repression of α-synuclein expression and toxicity by microRNA-7,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 31, pp. 13052–13057, 2009. View at Publisher · View at Google Scholar · View at Scopus
  164. S. Vartiainen, P. Pehkonen, M. Lakso, R. Nass, and G. Wong, “Identification of gene expression changes in transgenic C. elegans overexpressing human α-synuclein,” Neurobiology of Disease, vol. 22, no. 3, pp. 477–486, 2006. View at Publisher · View at Google Scholar · View at Scopus
  165. E. Doxakis, “Post-transcriptional regulation of α-synuclein expression by mir-7 and mir-153,” The Journal of Biological Chemistry, vol. 285, no. 17, pp. 12726–12734, 2010. View at Publisher · View at Google Scholar · View at Scopus
  166. S. Asikainen, M. Rudgalvyte, L. Heikkinen et al., “Global microRNA expression profiling of caenorhabditis elegans Parkinson's disease models,” Journal of Molecular Neuroscience, vol. 41, no. 1, pp. 210–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  167. F. Gillardon, M. Mack, W. Rist et al., “MicroRNA and proteome expression profiling in early-symptomatic α-synuclein(A30P)-transgenic mice,” Proteomics, vol. 2, no. 5, pp. 697–705, 2008. View at Publisher · View at Google Scholar · View at Scopus
  168. J. Kim, K. Inoue, J. Ishii et al., “A microRNA feedback circuit in midbrain dopamine neurons,” Science, vol. 317, no. 5842, pp. 1220–1224, 2007. View at Publisher · View at Google Scholar · View at Scopus
  169. G. Wang, J. M. van der Walt, G. Mayhew et al., “Variation in the miRNA-433 binding site of FGF20 confers risk for Parkinson disease by overexpression of α-synuclein,” The American Journal of Human Genetics, vol. 82, no. 2, pp. 283–289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  170. P. Foulds, D. M. A. Mann, J. D. Mitchell, and D. Allsop, “Parkinson disease: progress towards a molecular biomarker for Parkinson disease,” Nature Reviews Neurology, vol. 6, no. 7, pp. 359–361, 2010. View at Publisher · View at Google Scholar · View at Scopus
  171. W. J. Schulz-Schaeffer, “The synaptic pathology of α-synuclein aggregation in dementia with Lewy bodies, Parkinson's disease and Parkinson's disease dementia,” Acta Neuropathologica, vol. 120, no. 2, pp. 131–143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  172. R. E. Burke, “Programmed cell death and new discoveries in the genetics of parkinsonism,” Journal of Neurochemistry, vol. 104, no. 4, pp. 875–890, 2008. View at Publisher · View at Google Scholar · View at Scopus
  173. C. Zhou, Y. Huang, and S. Przedborski, “Oxidative stress in Parkinson's disease: a mechanism of pathogenic and therapeutic significance,” Annals of the New York Academy of Sciences, vol. 1147, pp. 93–104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  174. J. P. Covy and B. I. Giasson, “α-Synuclein, leucine-rich repeat kinase-2, and manganese in the pathogenesis of parkinson disease,” NeuroToxicology, vol. 32, no. 5, pp. 622–629, 2011. View at Publisher · View at Google Scholar · View at Scopus
  175. R. Cappai, S.-L. Leek, D. J. Tew et al., “Dopamine promotes α-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway,” FASEB Journal, vol. 19, no. 10, pp. 1377–1379, 2005. View at Publisher · View at Google Scholar · View at Scopus
  176. M. Lakso, S. Vartiainen, A.-M. Moilanen et al., “Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human α-synuclein,” Journal of Neurochemistry, vol. 86, no. 1, pp. 165–172, 2003. View at Publisher · View at Google Scholar · View at Scopus
  177. M. J. Volles and P. T. Lansbury Jr., “Zeroing in on the pathogenic form of α-Synuclein and its mechanism of neurotoxicity in Parkinson's disease,” Biochemistry, vol. 42, no. 26, pp. 7871–7878, 2003. View at Publisher · View at Google Scholar · View at Scopus
  178. J.-H. Seo, J.-C. Rah, S. H. Choi et al., “Alpha-synuclein regulates neuronal survival via Bcl-2 family expression and PI3/Akt kinase pathway,” The FASEB Journal, vol. 16, no. 13, pp. 1826–1828, 2002. View at Google Scholar · View at Scopus
  179. J. Goers, A. B. Manning-Bog, A. L. McCormack et al., “Nuclear localization of α-synuclein and its interaction with histones,” Biochemistry, vol. 42, no. 28, pp. 8465–8471, 2003. View at Publisher · View at Google Scholar · View at Scopus
  180. S. Xu, M. Zhou, S. Yu et al., “Oxidative stress induces nuclear translocation of C-terminus of α-synuclein in dopaminergic cells,” Biochemical and Biophysical Research Communications, vol. 342, no. 1, pp. 330–335, 2006. View at Publisher · View at Google Scholar · View at Scopus
  181. H. Jin, A. Kanthasamy, A. Ghosh, Y. Yang, V. Anantharam, and A. G. Kanthasamy, “α-Synuclein negatively regulates protein kinase Cδ expression to suppress apoptosis in dopaminergic neurons by reducing p300 histone acetyltransferase activity,” The Journal of Neuroscience, vol. 31, no. 6, pp. 2035–2051, 2011. View at Publisher · View at Google Scholar · View at Scopus
  182. P. J. Jensen, B. J. Alter, and K. L. O'Malley, “α-synuclein protects naive but not dbcAMP-treated dopaminergic cell types from 1-methyl-4-phenylpyridinium toxicity,” Journal of Neurochemistry, vol. 86, no. 1, pp. 196–209, 2003. View at Publisher · View at Google Scholar · View at Scopus
  183. E. Kontopoulos, J. D. Parvin, and M. B. Feany, “α-Synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity,” Human Molecular Genetics, vol. 15, no. 20, pp. 3012–3023, 2006. View at Publisher · View at Google Scholar · View at Scopus
  184. V. Anantharam, M. Kitazawa, J. Wagner, S. Kaul, and A. G. Kanthasamy, “Caspase-3-dependent proteolytic cleavage of protein kinase Cdelta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl,” Journal of Neuroscience, vol. 22, no. 5, pp. 1738–1751, 2012. View at Google Scholar
  185. S. Kaul, A. Kanthasamy, M. Kitazawa, V. Anantharam, and A. G. Kanthasamy, “Caspase-3 dependent proteolytic activation of protein kinase Cδ mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration,” European Journal of Neuroscience, vol. 18, no. 6, pp. 1387–1401, 2003. View at Publisher · View at Google Scholar · View at Scopus
  186. A. G. Kanthasamy, M. Kitazawa, A. Kanthasamy, and V. Anantharam, “Role of proteolytic activation of protein kinase Cδ in oxidative stress-induced apoptosis,” Antioxidants and Redox Signaling, vol. 5, no. 5, pp. 609–620, 2003. View at Publisher · View at Google Scholar · View at Scopus
  187. S. K. Kidd and J. S. Schneider, “Protection of dopaminergic cells from MPP+-mediated toxicity by histone deacetylase inhibition,” Brain Research, vol. 1354, pp. 172–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  188. T. F. Outeiro, E. Kontopoulos, S. M. Altmann et al., “Sirtuin 2 inhibitors rescue α-synuclein-mediated toxicity in models of Parkinson's disease,” Science, vol. 317, no. 5837, pp. 516–519, 2007. View at Publisher · View at Google Scholar · View at Scopus
  189. N. Ostrerova, L. Petrucelli, M. Farrer et al., “α-Synuclein shares physical and functional homology with 14-3-3 proteins,” Journal of Neuroscience, vol. 19, no. 14, pp. 5782–5791, 1999. View at Google Scholar · View at Scopus
  190. P. Desplats, B. Spencer, E. Coffee et al., “α-synuclein sequesters Dnmt1 from the nucleus: a novel mechanism for epigenetic alterations in Lewy body diseases,” Journal of Biological Chemistry, vol. 286, no. 11, pp. 9031–9037, 2011. View at Publisher · View at Google Scholar · View at Scopus
  191. M. Covic, E. Karaca, and D. C. Lie, “Epigenetic regulation of neurogenesis in the adult hippocampus,” Heredity, vol. 105, no. 1, pp. 122–134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  192. J. Sun, J. Sun, G.-L. Ming, and H. Song, “Epigenetic regulation of neurogenesis in the adult mammalian brain,” European Journal of Neuroscience, vol. 33, no. 6, pp. 1087–1093, 2011. View at Publisher · View at Google Scholar · View at Scopus
  193. L. Wang, T. Ohishi, A. Shiraki et al., “Developmental exposure to manganese chloride induces sustained aberration of neurogenesis in the hippocampal dentate gyrus of mice,” Toxicological Sciences, vol. 127, no. 2, pp. 508–521, 2012. View at Publisher · View at Google Scholar · View at Scopus
  194. L. Wang, A. Shiraki, M. Itahashi et al., “Aberration in epigenetic gene regulation in hippocampal neurogenesis by developmental exposure to manganese chloride in mice,” Toxicological Sciences, vol. 136, no. 1, pp. 154–165, 2013. View at Publisher · View at Google Scholar · View at Scopus
  195. K. R. Saradalekshmi, N. V. Neetha, S. Sathyan, I. V. Nair, C. M. Nair, and M. Banerjee, “DNA methyl transferase (DNMT) gene polymorphisms could be a primary event in epigenetic susceptibility to schizophrenia,” PLoS ONE, vol. 9, no. 5, article e98182, 2014. View at Publisher · View at Google Scholar · View at Scopus
  196. E. A. Kim, H.-K. Cheong, K.-D. Joo et al., “Effect of manganese exposure on the neuroendocrine system in welders,” NeuroToxicology, vol. 28, no. 2, pp. 263–269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  197. Y. X. Zheng, P. Chan, Z. F. Pan et al., “Polymorphism of metabolic genes and susceptibility to occupational chronic manganism,” Biomarkers, vol. 7, no. 4, pp. 337–346, 2002. View at Publisher · View at Google Scholar · View at Scopus
  198. N. Vinayagamoorthy, K. Krishnamurthi, S. S. Devi et al., “Genetic polymorphism of CYP2D6*2 C→T 2850, GSTM1, NQO1 genes and their correlation with biomarkers in manganese miners of Central India,” Chemosphere, vol. 81, no. 10, pp. 1286–1291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  199. I. Mena, K. Horiuchi, K. Burke, and G. C. Cotzias, “Chronic manganese poisoning: individual susceptibility and absorption of iron,” Neurology, vol. 19, no. 10, pp. 1000–1006, 1969. View at Publisher · View at Google Scholar · View at Scopus
  200. E. H. Hanson, G. Imperatore, and W. Burke, “HFE gene and hereditary hemochromatosis: a HuGE review. Human Genome Epidemiology,” American Journal of Epidemiology, vol. 154, no. 3, pp. 193–206, 2001. View at Publisher · View at Google Scholar
  201. J. N. Feder, D. M. Penny, A. Irrinki et al., “The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1472–1477, 1998. View at Publisher · View at Google Scholar · View at Scopus
  202. B. Claus Henn, J. Kim, M. Wessling-Resnick et al., “Associations of iron metabolism genes with blood manganese levels: a population-based study with validation data from animal models,” Environmental Health: A Global Access Science Source, vol. 10, article 97, 2011. View at Publisher · View at Google Scholar · View at Scopus