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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 8210734, 18 pages
https://doi.org/10.1155/2017/8210734
Review Article

The Central Role of Biometals Maintains Oxidative Balance in the Context of Metabolic and Neurodegenerative Disorders

1Jessenius Faculty of Medicine in Martin, Biomedical Center Martin JFM CU, Comenius University in Bratislava, Bratislava, Slovakia
2Department of Pathophysiology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Bratislava, Slovakia

Correspondence should be addressed to Alžbeta Kráľová Trančíková; ks.abinu.demfj@avokicnart.atebzla

Received 24 February 2017; Revised 19 May 2017; Accepted 28 May 2017; Published 2 July 2017

Academic Editor: Rhian Touyz

Copyright © 2017 Michal Pokusa and Alžbeta Kráľová Trančíková. 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. S. Satapati, B. Kucejova, J. A. Duarte et al., “Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver,” The Journal of Clinical Investigation, vol. 125, pp. 4447–4462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Warolin, K. R. Coenen, J. L. Kantor et al., “The relationship of oxidative stress, adiposity and metabolic risk factors in healthy Black and White American youth,” Pediatric Obesity, vol. 9, pp. 43–52, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Fridovich, “Oxygen: how do we stand it?” Medical Principles and Practice, vol. 22, pp. 131–137, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. K. J. Cho, J. M. Seo, and J. H. Kim, “Bioactive lipoxygenase metabolites stimulation of NADPH oxidases and reactive oxygen species,” Molecules and Cells, vol. 32, pp. 1–5, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. V. P. Skulachev, “Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants,” Quarterly Reviews of Biophysics, vol. 29, pp. 169–202, 1996. View at Publisher · View at Google Scholar
  6. S. Di Meo, T. T. Reed, P. Venditti, and V. M. Victor, “Role of ROS and RNS sources in physiological and pathological conditions,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 1245049, 44 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Gandhi and A. Y. Abramov, “Mechanism of oxidative stress in neurodegeneration,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 428010, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. H. L. Persson, T. Kurz, J. W. Eaton, and U. T. Brunk, “Radiation-induced cell death: importance of lysosomal destabilization,” The Biochemical Journal, vol. 389, pp. 877–884, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. J. Coon, X. X. Ding, S. J. Pernecky, and A. D. Vaz, “Cytochrome P450: progress and predictions,” The FASEB Journal, vol. 6, pp. 669–673, 1992. View at Google Scholar
  10. J. R. Reed and W. L. Backes, “Formation of P450. P450 complexes and their effect on P450 function,” Pharmacology & Therapeutics, vol. 133, pp. 299–310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. V. G. Grivennikova and A. D. Vinogradov, “Mitochondrial production of reactive oxygen species,” Biochemistry (Mosc), vol. 78, pp. 1490–1511, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Mitchell and J. Moyle, “Stoichiometry of proton translocation through the respiratory chain and adenosine triphosphatase systems of rat liver mitochondria,” Nature, vol. 208, pp. 147–151, 1965. View at Publisher · View at Google Scholar · View at Scopus
  13. J. F. Turrens, “Mitochondrial formation of reactive oxygen species,” The Journal of Physiology, vol. 552, pp. 335–344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Singh, “Biochemistry of peroxisomes in health and disease,” Molecular and Cellular Biochemistry, vol. 167, pp. 1–29, 1997. View at Publisher · View at Google Scholar
  15. V. D. Antonenkov, S. Grunau, S. Ohlmeier, and J. K. Hiltunen, “Peroxisomes are oxidative organelles,” Antioxidants & Redox Signaling, vol. 13, pp. 525–537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Rokka, V. D. Antonenkov, R. Soininen et al., “Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane,” PLoS One, vol. 4, article e5090, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Boveris, N. Oshino, and B. Chance, “The cellular production of hydrogen peroxide,” The Biochemical Journal, vol. 128, pp. 617–630, 1972. View at Publisher · View at Google Scholar
  18. J. Li, Y. Huang, Y. Hou, X. Li, H. Cao, and Z. Cui, “Novel gene clusters and metabolic pathway involved in 3,5,6-trichloro-2-pyridinol degradation by Ralstonia sp. strain T6,” Applied and Environmental Microbiology, vol. 79, pp. 7445–7453, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Emerit, M. Edeas, and F. Bricaire, “Neurodegenerative diseases and oxidative stress,” Biomedicine & Pharmacotherapy, vol. 58, pp. 39–46, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Hemmens and B. Mayer, “Enzymology of nitric oxide synthases,” Methods in Molecular Biology, vol. 100, pp. 1–32, 1998. View at Google Scholar
  21. B. Mayer and B. Hemmens, “Biosynthesis and action of nitric oxide in mammalian cells,” Trends in Biochemical Sciences, vol. 22, pp. 477–481, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Nathan and Q. W. Xie, “Nitric oxide synthases: roles, tolls, and controls,” Cell, vol. 78, pp. 915–918, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Brieger, S. Schiavone, F. J. Miller Jr., and K. H. Krause, “Reactive oxygen species: from health to disease,” Swiss Medical Weekly, vol. 142, article w13659, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. L. J. Ignarro, G. M. Buga, K. S. Wood, R. E. Byrns, and G. Chaudhuri, “Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, pp. 9265–9269, 1987. View at Google Scholar
  25. M. H. Zheng, J. Xu, P. Robbins et al., “Gene expression of vascular endothelial growth factor in giant cell tumors of bone,” Human Pathology, vol. 31, pp. 804–812, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Harman, “Origin and evolution of the free radical theory of aging: a brief personal history, 1954-2009,” Biogerontology, vol. 10, pp. 773–781, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. I. Fridovich, “Fundamental aspects of reactive oxygen species, or what’s the matter with oxygen?” Annals of the New York Academy of Sciences, vol. 893, pp. 13–18, 1999. View at Publisher · View at Google Scholar
  28. B. Uttara, A. V. Singh, P. Zamboni, and R. T. Mahajan, “Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options,” Current Neuropharmacology, vol. 7, pp. 65–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, pp. 239–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. G. E. Borgstahl, H. E. Parge, M. J. Hickey, W. F. Beyer Jr., R. A. Hallewell, and J. A. Tainer, “The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles,” Cell, vol. 71, pp. 107–118, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. J. S. Richardson, K. A. Thomas, and D. C. Richardson, “Alpha-carbon coordinates for bovine Cu, Zn superoxide dismutase,” Biochemical and Biophysical Research Communications, vol. 63, pp. 986–992, 1975. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Wolonciej, E. Milewska, and W. Roszkowska-Jakimiec, “Trace elements as an activator of antioxidant enzymes,” Postȩpy Higieny I Medycyny Doświadczalnej (Online), vol. 70, pp. 1483–1498, 2016. View at Publisher · View at Google Scholar
  33. I. Gouaref, Z. Bellahsene, S. Zekri, B. Alamir, and E. A. Koceir, “The link between trace elements and metabolic syndrome/oxidative stress in essential hypertension with or without type 2 diabetes,” Annales de Biologie Clinique (Paris), vol. 74, pp. 233–243, 2016. View at Google Scholar
  34. H. Vural, H. Demirin, Y. Kara, I. Eren, and N. Delibas, “Alterations of plasma magnesium, copper, zinc, iron and selenium concentrations and some related erythrocyte antioxidant enzyme activities in patients with Alzheimer’s disease,” Journal of Trace Elements in Medicine and Biology, vol. 24, pp. 169–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. D. P. Jones, “Extracellular redox state: refining the definition of oxidative stress in aging,” Rejuvenation Research, vol. 9, pp. 169–181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. G. E. Mann, J. Niehueser-Saran, A. Watson et al., “Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: implications for atherosclerosis and preeclampsia,” Sheng li Xue Bao, vol. 59, pp. 117–127, 2007. View at Google Scholar
  37. J. B. Morais, J. S. Severo, L. R. Santos et al., “Role of magnesium in oxidative stress in individuals with obesity,” Biological Trace Element Research, vol. 176, no. 1, pp. 20–26, 2016. View at Google Scholar
  38. N. J. Almeida Cardelli, M. Elisa Lopes-Pires, P. H. Bonfitto, H. H. Ferreira, E. Antunes, and S. Marcondes, “Cross-talking between lymphocytes and platelets and its regulation by nitric oxide and peroxynitrite in physiological condition and endotoxemia,” Life Sciences, vol. 172, pp. 2–7, 2016. View at Google Scholar
  39. K. Roy, Y. Wu, J. L. Meitzler et al., “NADPH oxidases and cancer,” Clinical Science (London, England), vol. 128, pp. 863–875, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. R. S. Frey, M. Ushio-Fukai, and A. B. Malik, “NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology,” Antioxidants & Redox Signaling, vol. 11, pp. 791–810, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Hosogai, A. Fukuhara, K. Oshima et al., “Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation,” Diabetes, vol. 56, pp. 901–911, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Xia, Q. Meng, L. Z. Liu, Y. Rojanasakul, X. R. Wang, and B. H. Jiang, “Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor,” Cancer Research, vol. 67, pp. 10823–10830, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Tacchini, E. Gammella, C. De Ponti, S. Recalcati, and G. Cairo, “Role of HIF-1 and NF-kappaB transcription factors in the modulation of transferrin receptor by inflammatory and anti-inflammatory signals,” The Journal of Biological Chemistry, vol. 283, pp. 20674–20686, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. P. van Uden, N. S. Kenneth, and S. Rocha, “Regulation of hypoxia-inducible factor-1alpha by NF-kappaB,” The Biochemical Journal, vol. 412, pp. 477–484, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Halberg, T. Khan, M. E. Trujillo et al., “Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue,” Molecular and Cellular Biology, vol. 29, pp. 4467–4483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Ye, “Role of insulin in the pathogenesis of free fatty acid-induced insulin resistance in skeletal muscle,” Endocrine, Metabolic & Immune Disorders Drug Targets, vol. 7, pp. 65–74, 2007. View at Publisher · View at Google Scholar
  47. C. Jiang, A. Qu, T. Matsubara et al., “Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat diet-fed mice,” Diabetes, vol. 60, pp. 2484–2495, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Scherer, C. Lindtner, E. Zielinski, J. O'Hare, N. Filatova, and C. Buettner, “Short term voluntary overfeeding disrupts brain insulin control of adipose tissue lipolysis,” The Journal of Biological Chemistry, vol. 287, pp. 33061–33069, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Beltowski, “Leptin and the regulation of endothelial function in physiological and pathological conditions,” Clinical and Experimental Pharmacology & Physiology, vol. 39, pp. 168–178, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. S. S. Martin, A. Qasim, and M. P. Reilly, “Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease,” Journal of the American College of Cardiology, vol. 52, pp. 1201–1210, 2008. View at Google Scholar
  51. P. Mandal, B. T. Pratt, M. Barnes, M. R. McMullen, and L. E. Nagy, “Molecular mechanism for adiponectin-dependent M2 macrophage polarization: link between the metabolic and innate immune activity of full-length adiponectin,” The Journal of Biological Chemistry, vol. 286, pp. 13460–13469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. R. M. Blumer, C. P. van Roomen, A. J. Meijer, J. H. Houben-Weerts, H. P. Sauerwein, and P. F. Dubbelhuis, “Regulation of adiponectin secretion by insulin and amino acids in 3T3-L1 adipocytes,” Metabolism, vol. 57, pp. 1655–1662, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. X. Wu, H. Motoshima, K. Mahadev, T. J. Stalker, R. Scalia, and B. J. Goldstein, “Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes,” Diabetes, vol. 52, pp. 1355–1363, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Abbasi, C. Lamendola, T. McLaughlin, J. Hayden, G. M. Reaven, and P. D. Reaven, “Plasma adiponectin concentrations do not increase in association with moderate weight loss in insulin-resistant, obese women,” Metabolism, vol. 53, pp. 280–283, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. J. V. Silha, M. Krsek, J. V. Skrha, P. Sucharda, B. L. Nyomba, and L. J. Murphy, “Plasma resistin, adiponectin and leptin levels in lean and obese subjects: correlations with insulin resistance,” European Journal of Endocrinology, vol. 149, pp. 331–335, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Wang, W. S. Chu, C. Hemphill, and S. C. Elbein, “Human resistin gene: molecular scanning and evaluation of association with insulin sensitivity and type 2 diabetes in Caucasians,” The Journal of Clinical Endocrinology and Metabolism, vol. 87, pp. 2520–2524, 2002. View at Publisher · View at Google Scholar
  57. A. Z. Jamurtas, A. Stavropoulos-Kalinoglou, S. Koutsias, Y. Koutedakis, and I. Fatouros, “Adiponectin, resistin, and visfatin in childhood obesity and exercise,” Pediatric Exercise Science, vol. 27, pp. 454–462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. R. R. Banerjee, S. M. Rangwala, J. S. Shapiro et al., “Regulation of fasted blood glucose by resistin,” Science, vol. 303, pp. 1195–1198, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. M. J. Ribeiro, J. F. Sacramento, C. Gonzalez, M. P. Guarino, E. C. Monteiro, and S. V. Conde, “Carotid body denervation prevents the development of insulin resistance and hypertension induced by hypercaloric diets,” Diabetes, vol. 62, pp. 2905–2916, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. E. J. Anderson, M. E. Lustig, K. E. Boyle et al., “Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans,” The Journal of Clinical Investigation, vol. 119, pp. 573–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. K. H. Fisher-Wellman and P. D. Neufer, “Linking mitochondrial bioenergetics to insulin resistance via redox biology,” Trends in Endocrinology and Metabolism, vol. 23, pp. 142–153, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. S. D. Martin and S. L. McGee, “The role of mitochondria in the aetiology of insulin resistance and type 2 diabetes,” Biochimica et Biophysica Acta, vol. 1840, pp. 1303–1312, 2014. View at Google Scholar
  63. D. Abdali, S. E. Samson, and A. K. Grover, “How effective are antioxidant supplements in obesity and diabetes?” Medical Principles and Practice, vol. 24, pp. 201–215, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. S. H. Lee, S. A. Park, S. H. Ko et al., “Insulin resistance and inflammation may have an additional role in the link between cystatin C and cardiovascular disease in type 2 diabetes mellitus patients,” Metabolism, vol. 59, pp. 241–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. J. S. Bhatti, G. K. Bhatti, and P. H. Reddy, “Mitochondrial dysfunction and oxidative stress in metabolic disorders - a step towards mitochondria based therapeutic strategies,” Biochimica et Biophysica Acta, vol. 1863, no. 5, pp. 1066–1077, 2016. View at Google Scholar
  66. D. A. Chistiakov, I. A. Sobenin, V. V. Revin, A. N. Orekhov, and Y. V. Bobryshev, “Mitochondrial aging and age-related dysfunction of mitochondria,” BioMed Research International, vol. 2014, Article ID 238463, 7 pages, 2014. View at Google Scholar
  67. R. Ventura-Clapier, A. Garnier, and V. Veksler, “Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha,” Cardiovascular Research, vol. 79, pp. 208–217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. B. G. Ha, D. S. Moon, H. J. Kim, and Y. H. Shon, “Magnesium and calcium-enriched deep-sea water promotes mitochondrial biogenesis by AMPK-activated signals pathway in 3T3-L1 preadipocytes,” Biomedicine & Pharmacotherapy, vol. 83, pp. 477–484, 2016. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Grinstein and A. Klip, “Calcium homeostasis and the activation of calcium channels in cells of the immune system,” Bulletin of the New York Academy of Medicine, vol. 65, pp. 69–79, 1989. View at Google Scholar
  70. N. Maouche, D. Meskine, B. Alamir, and E. A. Koceir, “Trace elements profile is associated with insulin resistance syndrome and oxidative damage in thyroid disorders: manganese and selenium interest in Algerian participants with dysthyroidism,” Journal of Trace Elements in Medicine and Biology, vol. 32, pp. 112–121, 2015. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Rayssiguier, E. Gueux, W. Nowacki, E. Rock, and A. Mazur, “High fructose consumption combined with low dietary magnesium intake may increase the incidence of the metabolic syndrome by inducing inflammation,” Magnesium Research, vol. 19, pp. 237–243, 2006. View at Google Scholar
  72. D. Agay, R. A. Anderson, C. Sandre et al., “Alterations of antioxidant trace elements (Zn, Se, Cu) and related metallo-enzymes in plasma and tissues following burn injury in rats,” Burns, vol. 31, pp. 366–371, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. Q. Shazia, Z. H. Mohammad, T. Rahman, and H. U. Shekhar, “Correlation of oxidative stress with serum trace element levels and antioxidant enzyme status in beta thalassemia major patients: a review of the literature,” Anemia, vol. 2012, Article ID 270923, 7 pages, 2012. View at Google Scholar
  74. J. Bertinato, C. W. Xiao, W. M. Ratnayake et al., “Lower serum magnesium concentration is associated with diabetes, insulin resistance, and obesity in South Asian and white Canadian women but not men,” Food & Nutrition Research, vol. 59, article 25974, 2015. View at Google Scholar
  75. A. Lecube, J. A. Baena-Fustegueras, J. M. Fort, D. Pelegri, C. Hernandez, and R. Simo, “Diabetes is the main factor accounting for hypomagnesemia in obese subjects,” PLoS One, vol. 7, article e30599, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Kolisek, A. C. Montezano, G. Sponder et al., “PARK7/DJ-1 dysregulation by oxidative stress leads to magnesium deficiency: implications in degenerative and chronic diseases,” Clinical Science (London, England), vol. 129, pp. 1143–1150, 2015. View at Publisher · View at Google Scholar · View at Scopus
  77. C. C. Lin, G. J. Tsweng, C. F. Lee, B. H. Chen, and Y. L. Huang, “Magnesium, zinc, and chromium levels in children, adolescents, and young adults with type 1 diabetes,” Clinical Nutrition, vol. 35, pp. 880–884, 2016. View at Publisher · View at Google Scholar · View at Scopus
  78. Z. Asemi, M. Karamali, M. Jamilian et al., “Magnesium supplementation affects metabolic status and pregnancy outcomes in gestational diabetes: a randomized, double-blind, placebo-controlled trial,” The American Journal of Clinical Nutrition, vol. 102, pp. 222–229, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. H. Rodriguez-Hernandez, M. Cervantes-Huerta, M. Rodriguez-Moran, and F. Guerrero-Romero, “Oral magnesium supplementation decreases alanine aminotransferase levels in obese women,” Magnesium Research, vol. 23, pp. 90–96, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Zhang, H. J. Forman, and J. Choi, “Gamma-glutamyl transpeptidase in glutathione biosynthesis,” Methods in Enzymology, vol. 401, pp. 468–483, 2005. View at Google Scholar
  81. Y. Yavuz, H. Mollaoglu, Y. Yurumez et al., “Therapeutic effect of magnesium sulphate on carbon monoxide toxicity-mediated brain lipid peroxidation,” European Review for Medical and Pharmacological Sciences, vol. 17, Supplement 1, pp. 28–33, 2013. View at Google Scholar
  82. Y. J. Huang, D. Walker, W. Chen, M. Klingbeil, and R. Komuniecki, “Expression of pyruvate dehydrogenase isoforms during the aerobic/anaerobic transition in the development of the parasitic nematode Ascaris suum: altered stoichiometry of phosphorylation/inactivation,” Archives of Biochemistry and Biophysics, vol. 352, pp. 263–270, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. K. M. Kelley, E. S. Gray, K. Siharath, C. S. Nicoll, and H. A. Bern, “Experimental diabetes mellitus in a teleost fish. II. Roles of insulin, growth hormone (GH), insulin-like growth factor-I, and hepatic GH receptors in diabetic growth inhibition in the goby, Gillichthys mirabilis,” Endocrinology, vol. 132, pp. 2696–2702, 1993. View at Publisher · View at Google Scholar · View at Scopus
  84. L. M. Gommers, J. G. Hoenderop, R. J. Bindels, and J. H. de Baaij, “Hypomagnesemia in type 2 diabetes: a vicious circle?” Diabetes, vol. 65, pp. 3–13, 2016. View at Google Scholar
  85. A. V. Nair, B. Hocher, S. Verkaart et al., “Loss of insulin-induced activation of TRPM6 magnesium channels results in impaired glucose tolerance during pregnancy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 11324–11329, 2012. View at Google Scholar
  86. G. Cao, K. P. Lee, J. van der Wijst et al., “Methionine sulfoxide reductase B1 (MsrB1) recovers TRPM6 channel activity during oxidative stress,” The Journal of Biological Chemistry, vol. 285, pp. 26081–26087, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. V. P. Chauhan, J. A. Tsiouris, A. Chauhan, A. M. Sheikh, W. T. Brown, and M. Vaughan, “Increased oxidative stress and decreased activities of Ca(2+)/Mg(2+)-ATPase and Na(+)/K(+)-ATPase in the red blood cells of the hibernating black bear,” Life Sciences, vol. 71, pp. 153–161, 2002. View at Publisher · View at Google Scholar · View at Scopus
  88. G. A. Vinogradov, E. V. Borisovskaia, and A. G. Lapirov, “The calcium and magnesium ion metabolic characteristics of water plants in different taxonomic groups,” Zhurnal Obshcheĭ Biologii, vol. 61, pp. 163–172, 2000. View at Google Scholar
  89. B. Chaigne-Delalande, F. Y. Li, G. M. O'Connor et al., “Mg2+ regulates cytotoxic functions of NK and CD8 T cells in chronic EBV infection through NKG2D,” Science, vol. 341, pp. 186–191, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. F. Y. Li, B. Chaigne-Delalande, H. Su, G. Uzel, H. Matthews, and M. J. Lenardo, “XMEN disease: a new primary immunodeficiency affecting Mg2+ regulation of immunity against Epstein-Barr virus,” Blood, vol. 123, pp. 2148–2152, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. C. Malpuech-Brugere, E. Rock, C. Astier, W. Nowacki, A. Mazur, and Y. Rayssiguier, “Exacerbated immune stress response during experimental magnesium deficiency results from abnormal cell calcium homeostasis,” Life Sciences, vol. 63, pp. 1815–1822, 1998. View at Publisher · View at Google Scholar · View at Scopus
  92. B. M. Altura, N. C. Shah, G. Shah et al., “Short-term magnesium deficiency upregulates ceramide synthase in cardiovascular tissues and cells: cross-talk among cytokines, Mg2+, NF-kappaB, and de novo ceramide,” American Journal Physiology Heart Circulatory Physiology, vol. 302, pp. H319–H332, 2012. View at Google Scholar
  93. F. I. Bussiere, W. Zimowska, E. Gueux, Y. Rayssiguier, and A. Mazur, “Stress protein expression cDNA array study supports activation of neutrophils during acute magnesium deficiency in rats,” Magnesium Research, vol. 15, pp. 37–42, 2002. View at Google Scholar
  94. F. C. Mooren, S. W. Golf, and K. Volker, “Effect of magnesium on granulocyte function and on the exercise induced inflammatory response,” Magnesium Research, vol. 16, pp. 49–58, 2003. View at Google Scholar
  95. F. I. Bussiere, A. Mazur, J. L. Fauquert, A. Labbe, Y. Rayssiguier, and A. Tridon, “High magnesium concentration in vitro decreases human leukocyte activation,” Magnesium Research, vol. 15, pp. 43–48, 2002. View at Google Scholar
  96. C. Andreini and I. Bertini, “A bioinformatics view of zinc enzymes,” Journal of Inorganic Biochemistry, vol. 111, pp. 150–156, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Sharif, P. Thomas, P. Zalewski, and M. Fenech, “The role of zinc in genomic stability,” Mutation Research, vol. 733, pp. 111–121, 2012. View at Google Scholar
  98. P. I. Oteiza, “Zinc and the modulation of redox homeostasis,” Free Radical Biology & Medicine, vol. 53, pp. 1748–1759, 2012. View at Publisher · View at Google Scholar · View at Scopus
  99. P. Bonaventura, G. Benedetti, F. Albarede, and P. Miossec, “Zinc and its role in immunity and inflammation,” Autoimmunity Reviews, vol. 14, pp. 277–285, 2015. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Summersgill, H. England, G. Lopez-Castejon et al., “Zinc depletion regulates the processing and secretion of IL-1beta,” Cell Death & Disease, vol. 5, article e1040, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. U. Doboszewska, B. Szewczyk, M. Sowa-Kucma et al., “Alterations of bio-elements, oxidative, and inflammatory status in the zinc deficiency model in rats,” Neurotoxicity Research, vol. 29, pp. 143–154, 2016. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Hamasaki, Y. Kawashima, and H. Yanai, “Serum Zn/Cu ratio is associated with renal function, glycemic control, and metabolic parameters in Japanese patients with and without type 2 diabetes: a cross-sectional study,” Frontiers in Endocrinology (Lausanne), vol. 7, p. 147, 2016. View at Google Scholar
  103. S. Korkmaz-Icoz, S. Al Said, T. Radovits et al., “Oral treatment with a zinc complex of acetylsalicylic acid prevents diabetic cardiomyopathy in a rat model of type-2 diabetes: activation of the Akt pathway,” Cardiovascular Diabetology, vol. 15, p. 75, 2016. View at Google Scholar
  104. J. Chen, S. Wang, M. Luo et al., “From the cover: zinc deficiency worsens and supplementation prevents high-fat diet induced vascular inflammation, oxidative stress, and pathological remodeling,” Toxicological Sciences, vol. 153, pp. 124–136, 2016. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Yadav, P. A. Manjrekar, A. Agarwal, A. Ahmad, A. Hegde, and R. M. Srikantiah, “Association of Serum Selenium, zinc and magnesium levels with glycaemic indices and insulin resistance in pre-diabetes: a cross-sectional study from South India,” Biological Trace Element Research, vol. 175, pp. 65–71, 2017. View at Publisher · View at Google Scholar
  106. B. Halliwell, “Oxidative stress and neurodegeneration: where are we now?” Journal of Neurochemistry, vol. 97, pp. 1634–1658, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. R. A. Floyd and J. M. Carney, “Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress,” Annals of Neurology, vol. 32, Supplement, pp. S22–S27, 1992. View at Publisher · View at Google Scholar · View at Scopus
  108. G. H. Kim, J. E. Kim, S. J. Rhie, and S. Yoon, “The role of oxidative stress in neurodegenerative diseases,” Experimental Neurobiology, vol. 24, pp. 325–340, 2015. View at Publisher · View at Google Scholar
  109. D. S. Bredt, C. E. Glatt, P. M. Hwang, M. Fotuhi, T. M. Dawson, and S. H. Snyder, “Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase,” Neuron, vol. 7, pp. 615–624, 1991. View at Publisher · View at Google Scholar · View at Scopus
  110. T. Nakamura, S. Tu, M. W. Akhtar, C. R. Sunico, S. Okamoto, and S. A. Lipton, “Aberrant protein s-nitrosylation in neurodegenerative diseases,” Neuron, vol. 78, pp. 596–614, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Lafon-Cazal, S. Pietri, M. Culcasi, and J. Bockaert, “NMDA-dependent superoxide production and neurotoxicity,” Nature, vol. 364, pp. 535–537, 1993. View at Publisher · View at Google Scholar
  112. G. T. Liberatore, V. Jackson-Lewis, S. Vukosavic et al., “Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease,” Nature Medicine, vol. 5, pp. 1403–1409, 1999. View at Publisher · View at Google Scholar · View at Scopus
  113. X. Wang and E. K. Michaelis, “Selective neuronal vulnerability to oxidative stress in the brain,” Frontiers in Aging Neuroscience, vol. 2, p. 12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. E. Cadenas and K. J. Davies, “Mitochondrial free radical generation, oxidative stress, and aging,” Free Radical Biology & Medicine, vol. 29, pp. 222–230, 2000. View at Publisher · View at Google Scholar · View at Scopus
  115. M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, pp. 787–795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. A. H. Tsang and K. K. Chung, “Oxidative and nitrosative stress in Parkinson’s disease,” Biochimica et Biophysica Acta, vol. 1792, pp. 643–650, 2009. View at Google Scholar
  117. K. K. Chung, V. L. Dawson, and T. M. Dawson, “The role of the ubiquitin-proteasomal pathway in Parkinson’s disease and other neurodegenerative disorders,” Trends in Neurosciences, vol. 24, pp. S7–14, 2001. View at Publisher · View at Google Scholar
  118. R. Kavya, R. Saluja, S. Singh, and M. Dikshit, “Nitric oxide synthase regulation and diversity: implications in Parkinson’s disease,” Nitric Oxide, vol. 15, pp. 280–294, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. A. H. Schapira, J. M. Cooper, D. Dexter, P. Jenner, J. B. Clark, and C. D. Marsden, “Mitochondrial complex I deficiency in Parkinson’s disease,” Lancet, vol. 1, p. 1269, 1989. View at Google Scholar
  120. D. Sulzer, “Multiple hit hypotheses for dopamine neuron loss in Parkinson’s disease,” Trends in Neurosciences, vol. 30, pp. 244–250, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. M. Vila and S. Przedborski, “Targeting programmed cell death in neurodegenerative diseases,” Nature Reviews. Neuroscience, vol. 4, pp. 365–375, 2003. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Cunnane, S. Nugent, M. Roy et al., “Brain fuel metabolism, aging, and Alzheimer’s disease,” Nutrition, vol. 27, pp. 3–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. A. M. Jauhiainen, T. Kangasmaa, M. Rusanen et al., “Differential hypometabolism patterns according to mild cognitive impairment subtypes,” Dementia and Geriatric Cognitive Disorders, vol. 26, pp. 490–498, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. M. T. Davis and W. J. Bartfay, “Ebselen decreases oxygen free radical production and iron concentrations in the hearts of chronically iron-overloaded mice,” Biological Research for Nursing, vol. 6, pp. 37–45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  125. T. Kitada, S. Asakawa, N. Hattori et al., “Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism,” Nature, vol. 392, pp. 605–608, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. C. B. Lucking, A. Durr, V. Bonifati et al., “Association between early-onset Parkinson’s disease and mutations in the parkin gene,” The New England Journal of Medicine, vol. 342, pp. 1560–1567, 2000. View at Publisher · View at Google Scholar · View at Scopus
  127. D. M. Maraganore, T. G. Lesnick, A. Elbaz et al., “UCHL1 is a Parkinson’s disease susceptibility gene,” Annals of Neurology, vol. 55, pp. 512–521, 2004. View at Publisher · View at Google Scholar · View at Scopus
  128. J. Choi, A. I. Levey, S. T. Weintraub et al., “Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson’s and Alzheimer’s diseases,” The Journal of Biological Chemistry, vol. 279, pp. 13256–13264, 2004. View at Publisher · View at Google Scholar · View at Scopus
  129. K. K. Chung, B. Thomas, X. Li et al., “S-nitrosylation of parkin regulates ubiquitination and compromises parkin’s protective function,” Science, vol. 304, pp. 1328–1331, 2004. View at Publisher · View at Google Scholar · View at Scopus
  130. D. Yao, Z. Gu, T. Nakamura et al., “Nitrosative stress linked to sporadic Parkinson’s disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, pp. 10810–10814, 2004. View at Google Scholar
  131. K. Nishikawa, H. Li, R. Kawamura et al., “Alterations of structure and hydrolase activity of parkinsonism-associated human ubiquitin carboxyl-terminal hydrolase L1 variants,” Biochemical and Biophysical Research Communications, vol. 304, pp. 176–183, 2003. View at Publisher · View at Google Scholar · View at Scopus
  132. K. Ozawa, A. T. Komatsubara, Y. Nishimura et al., “S-nitrosylation regulates mitochondrial quality control via activation of parkin,” Scientific Reports, vol. 3, p. 2202, 2013. View at Google Scholar
  133. T. Kabuta, A. Furuta, S. Aoki, K. Furuta, and K. Wada, “Aberrant interaction between Parkinson disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy,” The Journal of Biological Chemistry, vol. 283, pp. 23731–23738, 2008. View at Publisher · View at Google Scholar · View at Scopus
  134. S. Tanaka, T. Uehara, and Y. Nomura, “Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death,” The Journal of Biological Chemistry, vol. 275, pp. 10388–10393, 2000. View at Publisher · View at Google Scholar · View at Scopus
  135. T. Uehara, T. Nakamura, D. Yao et al., “S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration,” Nature, vol. 441, pp. 513–517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. A. K. Walker, M. A. Farg, C. R. Bye, C. A. McLean, M. K. Horne, and J. D. Atkin, “Protein disulphide isomerase protects against protein aggregation and is S-nitrosylated in amyotrophic lateral sclerosis,” Brain, vol. 133, pp. 105–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  137. X. Chen, X. Zhang, C. Li et al., “S-nitrosylated protein disulfide isomerase contributes to mutant SOD1 aggregates in amyotrophic lateral sclerosis,” Journal of Neurochemistry, vol. 124, pp. 45–58, 2013. View at Publisher · View at Google Scholar · View at Scopus
  138. Y. K. Al-Hilaly, T. L. Williams, M. Stewart-Parker et al., “A central role for dityrosine crosslinking of amyloid-beta in Alzheimer’s disease,” Acta Neuropathologica Communications, vol. 1, p. 83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  139. J. Naslund, A. Schierhorn, U. Hellman et al., “Relative abundance of Alzheimer A beta amyloid peptide variants in Alzheimer disease and normal aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, pp. 8378–8382, 1994. View at Google Scholar
  140. R. Radi, A. Cassina, and R. Hodara, “Nitric oxide and peroxynitrite interactions with mitochondria,” Biological Chemistry, vol. 383, pp. 401–409, 2002. View at Publisher · View at Google Scholar · View at Scopus
  141. Q. Liu, M. A. Smith, J. Avila et al., “Alzheimer-specific epitopes of tau represent lipid peroxidation-induced conformations,” Free Radical Biology & Medicine, vol. 38, pp. 746–754, 2005. View at Publisher · View at Google Scholar · View at Scopus
  142. M. R. Reynolds, R. W. Berry, and L. I. Binder, “Site-specific nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: implications for Alzheimer’s disease,” Biochemistry, vol. 44, pp. 1690–1700, 2005. View at Publisher · View at Google Scholar · View at Scopus
  143. M. R. Reynolds, T. J. Lukas, R. W. Berry, and L. I. Binder, “Peroxynitrite-mediated tau modifications stabilize preformed filaments and destabilize microtubules through distinct mechanisms,” Biochemistry, vol. 45, pp. 4314–4326, 2006. View at Publisher · View at Google Scholar · View at Scopus
  144. S. M. Alavi Naini and N. Soussi-Yanicostas, “Tau hyperphosphorylation and oxidative stress, a critical vicious circle in neurodegenerative tauopathies?” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 151979, 17 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  145. W. Xiang, J. C. Schlachetzki, S. Helling et al., “Oxidative stress-induced posttranslational modifications of alpha-synuclein: specific modification of alpha-synuclein by 4-hydroxy-2-nonenal increases dopaminergic toxicity,” Molecular and Cellular Neurosciences, vol. 54, pp. 71–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  146. P. Dusek, P. M. Roos, T. Litwin, S. A. Schneider, T. P. Flaten, and J. Aaseth, “The neurotoxicity of iron, copper and manganese in Parkinson’s and Wilson’s diseases,” Journal of Trace Elements in Medicine and Biology, vol. 31, pp. 193–203, 2015. View at Publisher · View at Google Scholar · View at Scopus
  147. S. J. Dixon and B. R. Stockwell, “The role of iron and reactive oxygen species in cell death,” Nature Chemical Biology, vol. 10, pp. 9–17, 2014. View at Publisher · View at Google Scholar · View at Scopus
  148. C. Hidalgo and M. T. Nunez, “Calcium, iron and neuronal function,” IUBMB Life, vol. 59, pp. 280–285, 2007. View at Publisher · View at Google Scholar · View at Scopus
  149. P. Munoz, A. Humeres, C. Elgueta, A. Kirkwood, C. Hidalgo, and M. T. Nunez, “Iron mediates N-methyl-D-aspartate receptor-dependent stimulation of calcium-induced pathways and hippocampal synaptic plasticity,” The Journal of Biological Chemistry, vol. 286, pp. 13382–13392, 2011. View at Publisher · View at Google Scholar · View at Scopus
  150. Y. Munoz, C. M. Carrasco, J. D. Campos, P. Aguirre, and M. T. Nunez, “Parkinson’s disease: the mitochondria-iron link,” Parkinsons Disease, vol. 2016, Article ID 7049108, 21 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  151. S. J. Chinta, M. J. Kumar, M. Hsu et al., “Inducible alterations of glutathione levels in adult dopaminergic midbrain neurons result in nigrostriatal degeneration,” The Journal of Neuroscience, vol. 27, pp. 13997–14006, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. D. Kaur, F. Yantiri, S. Rajagopalan et al., “Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson’s disease,” Neuron, vol. 37, pp. 899–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  153. N. P. Visanji, J. F. Collingwood, M. E. Finnegan, A. Tandon, E. House, and L. N. Hazrati, “Iron deficiency in parkinsonism: region-specific iron dysregulation in Parkinson’s disease and multiple system atrophy,” Journal of Parkinsons Disease, vol. 3, pp. 523–537, 2013. View at Publisher · View at Google Scholar · View at Scopus
  154. K. C. Chew, E. T. Ang, Y. K. Tai et al., “Enhanced autophagy from chronic toxicity of iron and mutant A53T alpha-synuclein: implications for neuronal cell death in Parkinson disease,” The Journal of Biological Chemistry, vol. 286, pp. 33380–33389, 2011. View at Publisher · View at Google Scholar · View at Scopus
  155. X. Wang, D. Moualla, J. A. Wright, and D. R. Brown, “Copper binding regulates intracellular alpha-synuclein localisation, aggregation and toxicity,” Journal of Neurochemistry, vol. 113, pp. 704–714, 2010. View at Publisher · View at Google Scholar · View at Scopus
  156. E. Deas, N. Cremades, P. R. Angelova et al., “Alpha-synuclein oligomers interact with metal ions to induce oxidative stress and neuronal death in Parkinson’s disease,” Antioxidants & Redox Signaling, vol. 24, pp. 376–391, 2016. View at Publisher · View at Google Scholar · View at Scopus
  157. M. S. Parihar, A. Parihar, M. Fujita, M. Hashimoto, and P. Ghafourifar, “Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells,” The International Journal of Biochemistry & Cell Biology, vol. 41, pp. 2015–2024, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. S. Ott, N. Dziadulewicz, and D. C. Crowther, “Iron is a specific cofactor for distinct oxidation- and aggregation-dependent Abeta toxicity mechanisms in a Drosophila model,” Disease Models & Mechanisms, vol. 8, pp. 657–667, 2015. View at Publisher · View at Google Scholar · View at Scopus
  159. T. Rival, R. M. Page, D. S. Chandraratna et al., “Fenton chemistry and oxidative stress mediate the toxicity of the beta-amyloid peptide in a Drosophila model of Alzheimer’s disease,” The European Journal of Neuroscience, vol. 29, pp. 1335–1347, 2009. View at Publisher · View at Google Scholar · View at Scopus
  160. S. Montes, S. Rivera-Mancia, A. Diaz-Ruiz, L. Tristan-Lopez, and C. Rios, “Copper and copper proteins in Parkinson’s disease,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 147251, 15 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  161. D. T. Dexter, A. Carayon, F. Javoy-Agid et al., “Alterations in the levels of iron, ferritin and other trace metals in Parkinson’s disease and other neurodegenerative diseases affecting the basal ganglia,” Brain: A Journal of Neurology, vol. 114, Part 4, pp. 1953–1975, 1991. View at Google Scholar
  162. K. Jomova, D. Vondrakova, M. Lawson, and M. Valko, “Metals, oxidative stress and neurodegenerative disorders,” Molecular and Cellular Biochemistry, vol. 345, pp. 91–104, 2010. View at Publisher · View at Google Scholar · View at Scopus
  163. V. N. Uversky, J. Li, and A. L. Fink, “Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson’s disease and heavy metal exposure,” The Journal of Biological Chemistry, vol. 276, pp. 44284–44296, 2001. View at Publisher · View at Google Scholar · View at Scopus
  164. C. Wang, L. Liu, L. Zhang, Y. Peng, and F. Zhou, “Redox reactions of the alpha-synuclein-Cu2+ complex and their effects on neuronal cell viability,” Biochemistry, vol. 49, pp. 8134–8142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  165. S. Shendelman, A. Jonason, C. Martinat, T. Leete, and A. Abeliovich, “DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation,” PLoS Biology, vol. 2, article e362, 2004. View at Publisher · View at Google Scholar · View at Scopus
  166. R. H. Kim, P. D. Smith, H. Aleyasin et al., “Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, pp. 5215–5220, 2005. View at Google Scholar
  167. A. Ramirez, A. Heimbach, J. Grundemann et al., “Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase,” Nature Genetics, vol. 38, pp. 1184–1191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  168. J. S. Park, B. Koentjoro, D. Veivers, A. Mackay-Sim, and C. M. Sue, “Parkinson’s disease-associated human ATP13A2 (PARK9) deficiency causes zinc dyshomeostasis and mitochondrial dysfunction,” Human Molecular Genetics, vol. 23, pp. 2802–2815, 2014. View at Publisher · View at Google Scholar · View at Scopus
  169. A. R. White, R. Reyes, J. F. Mercer et al., “Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice,” Brain Research, vol. 842, pp. 439–444, 1999. View at Publisher · View at Google Scholar · View at Scopus
  170. C. J. Maynard, R. Cappai, I. Volitakis et al., “Overexpression of Alzheimer’s disease amyloid-beta opposes the age-dependent elevations of brain copper and iron,” The Journal of Biological Chemistry, vol. 277, pp. 44670–44676, 2002. View at Publisher · View at Google Scholar · View at Scopus
  171. J. P. Covy and B. I. Giasson, “Alpha-synuclein, leucine-rich repeat kinase-2, and manganese in the pathogenesis of Parkinson disease,” Neurotoxicology, vol. 32, pp. 622–629, 2011. View at Publisher · View at Google Scholar · View at Scopus
  172. J. A. Roth, “Homeostatic and toxic mechanisms regulating manganese uptake, retention, and elimination,” Biological Research, vol. 39, pp. 45–57, 2006. View at Google Scholar
  173. 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, pp. 131–147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  174. C. Au, A. Benedetto, and M. Aschner, “Manganese transport in eukaryotes: the role of DMT1,” Neurotoxicology, vol. 29, pp. 569–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  175. T. Cai, T. Yao, G. Zheng et al., “Manganese induces the overexpression of alpha-synuclein in PC12 cells via ERK activation,” Brain Research, vol. 1359, pp. 201–207, 2010. View at Publisher · View at Google Scholar · View at Scopus
  176. C. Pifl, M. Khorchide, A. Kattinger, H. Reither, J. Hardy, and O. Hornykiewicz, “Alpha-synuclein selectively increases manganese-induced viability loss in SK-N-MC neuroblastoma cells expressing the human dopamine transporter,” Neuroscience Letters, vol. 354, pp. 34–37, 2004. View at Publisher · View at Google Scholar · View at Scopus
  177. K. Hasegawa and H. Kowa, “Autosomal dominant familial Parkinson disease: older onset of age, and good response to levodopa therapy,” European Neurology, vol. 38, Supplement 1, pp. 39–43, 1997. View at Google Scholar
  178. J. P. Covy and B. I. Giasson, “The G2019S pathogenic mutation disrupts sensitivity of leucine-rich repeat kinase 2 to manganese kinase inhibition,” Journal of Neurochemistry, vol. 115, pp. 36–46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  179. B. Lovitt, E. C. Vanderporten, Z. Sheng, H. Zhu, J. Drummond, and Y. Liu, “Differential effects of divalent manganese and magnesium on the kinase activity of leucine-rich repeat kinase 2 (LRRK2),” Biochemistry, vol. 49, pp. 3092–3100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  180. J. P. Covy, E. A. Waxman, and B. I. Giasson, “Characterization of cellular protective effects of ATP13A2/PARK9 expression and alterations resulting from pathogenic mutants,” Journal of Neuroscience Research, vol. 90, pp. 2306–2316, 2012. View at Publisher · View at Google Scholar · View at Scopus
  181. A. D. Gitler, A. Chesi, M. L. Geddie et al., “Alpha-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 · View at Scopus
  182. S. R. Smith, F. Bai, C. Charbonneau, L. Janderova, and G. Argyropoulos, “A promoter genotype and oxidative stress potentially link resistin to human insulin resistance,” Diabetes, vol. 52, pp. 1611–1618, 2003. View at Publisher · View at Google Scholar
  183. T. Cai, H. Che, T. Yao et al., “Manganese induces tau hyperphosphorylation through the activation of ERK MAPK pathway in PC12 cells,” Toxicological Sciences, vol. 119, pp. 169–177, 2011. View at Publisher · View at Google Scholar · View at Scopus
  184. Y. Sun, P. Sukumaran, A. Schaar, and B. B. Singh, “TRPM7 and its role in neurodegenerative diseases,” Channels (Austin, Texas), vol. 9, pp. 253–261, 2015. View at Publisher · View at Google Scholar · View at Scopus
  185. A. Muroyama, M. Inaka, H. Matsushima, H. Sugino, Y. Marunaka, and Y. Mitsumoto, “Enhanced susceptibility to MPTP neurotoxicity in magnesium-deficient C57BL/6N mice,” Neuroscience Research, vol. 63, pp. 72–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  186. K. Oyanagi, E. Kawakami, K. Kikuchi-Horie et al., “Magnesium deficiency over generations in rats with special references to the pathogenesis of the parkinsonism-dementia complex and amyotrophic lateral sclerosis of Guam,” Neuropathology, vol. 26, pp. 115–128, 2006. View at Publisher · View at Google Scholar · View at Scopus
  187. M. Yasui, T. Kihira, and K. Ota, “Calcium, magnesium and aluminum concentrations in Parkinson’s disease,” Neurotoxicology, vol. 13, pp. 593–600, 1992. View at Google Scholar
  188. L. Lin, Z. Ke, M. Lv, R. Lin, B. Wu, and Z. Zheng, “Effects of MgSO4 and magnesium transporters on 6-hydroxydopamine-induced SH-SY5Y cells,” Life Sciences, vol. 172, pp. 48–54, 2016. View at Publisher · View at Google Scholar
  189. Y. Miyake, K. Tanaka, W. Fukushima et al., “Dietary intake of metals and risk of Parkinson’s disease: a case-control study in Japan,” Journal of the Neurological Sciences, vol. 306, pp. 98–102, 2011. View at Google Scholar
  190. J. H. de Baaij, J. G. Hoenderop, and R. J. Bindels, “Magnesium in man: implications for health and disease,” Physiological Reviews, vol. 95, pp. 1–46, 2015. View at Google Scholar
  191. L. Grycova, P. Sklenovsky, Z. Lansky et al., “ATP and magnesium drive conformational changes of the Na+/K+−ATPase cytoplasmic headpiece,” Biochimica et Biophysica Acta, vol. 1788, pp. 1081–1091, 2009. View at Publisher · View at Google Scholar · View at Scopus
  192. K. Toyoshima, K. Momma, and T. Nakanishi, “Fetal reversed constrictive effect of indomethacin and postnatal delayed closure of the ductus arteriosus following administration of transplacental magnesium sulfate in rats,” Neonatology, vol. 96, pp. 125–131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  193. Z. Zhou, Q. Sun, Z. Hu, and Y. Deng, “Nanobelt formation of magnesium hydroxide sulfate hydrate via a soft chemistry process,” The Journal of Physical Chemistry. B, vol. 110, pp. 13387–13392, 2006. View at Publisher · View at Google Scholar · View at Scopus
  194. H. J. Apell, T. Hitzler, and G. Schreiber, “Modulation of the Na, K-ATPase by magnesium ions,” Biochemistry, vol. 56, no. 7, pp. 1005–1016, 2017. View at Publisher · View at Google Scholar
  195. M. A. Lovell, J. D. Robertson, W. J. Teesdale, J. L. Campbell, and W. R. Markesbery, “Copper, iron and zinc in Alzheimer’s disease senile plaques,” Journal of the Neurological Sciences, vol. 158, pp. 47–52, 1998. View at Google Scholar
  196. K. Schmidt, D. M. Wolfe, B. Stiller, and D. A. Pearce, “Cd2+, Mn2+, Ni2+ and Se2+ toxicity to Saccharomyces cerevisiae lacking YPK9p the orthologue of human ATP13A2,” Biochemical and Biophysical Research Communications, vol. 383, pp. 198–202, 2009. View at Publisher · View at Google Scholar · View at Scopus