Copper, Iron, and Manganese Toxicity in Neuropsychiatric Conditions
Abstract
:1. Introduction
2. Copper Toxicosis
2.1. Neuropsychiatric Diseases Associated with Copper Toxicosis
Wilson’s Disease
3. Iron Toxicosis
3.1. Neuropsychiatric Diseases Associated with Iron Toxicosis
3.1.1. Aceruloplasminaemia
3.1.2. Neuroferritinopathy
3.1.3. Pantothenate Kinase-Associated Neurodegeneration (PKAN) and Other Very Rare Classical NBIA Forms
3.1.4. Friedreich’s Ataxia (FRDA)
4. Manganese Homeostasis and Neurotoxicity
4.1. Neuropsychiatric Diseases Associated with Manganese Toxicosis
4.1.1. Manganism
4.1.2. Attention-Deficit/Hyperactivity Disorder
4.1.3. Ephedrone Encephalopathy
4.1.4. HMNDYT1-SLC30A10 Deficiency
4.1.5. HMNDYT2-SLC39A14 Deficiency
4.1.6. CDG2N-SLC39A8 Deficiency
4.1.7. Hepatic Encephalopathy (HE)
5. Neuropsychiatric Diseases Associated with Other Metal Toxicosis
5.1. Prion Disease and “Prion-Like Disease”—Metal Overload
5.1.1. Transmissible Spongiform Encephalopathies—Prion Disease
5.1.2. Amyotrophic Lateral Sclerosis
5.1.3. Huntington’s Disease
5.1.4. Depression
6. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Gromadzka, G.; Tarnacka, B.; Flaga, A.; Adamczyk, A. Copper Dyshomeostasis in Neurodegenerative Diseases—Therapeutic Implications. Int. J. Mol. Sci. 2020, 21, 9259. [Google Scholar] [CrossRef]
- Li, D.D.; Zhang, W.; Wang, Z.Y.; Zhao, P. Serum Copper, Zinc, and Iron Levels in Patients with Alzheimer’s Disease: A Meta-Analysis of Case-Control Studies. Front. Aging Neurosci. 2017, 9. [Google Scholar] [CrossRef] [Green Version]
- Bagheri, S.; Squitti, R.; Haertlé, T.; Siotto, M.; Saboury, A.A. Role of Copper in the Onset of Alzheimer’s Disease Compared to Other Metals. Front. Aging Neurosci. 2018, 9. [Google Scholar] [CrossRef]
- Chen, P.; Totten, M.; Zhang, Z.; Bucinca, H.; Erikson, K.; Santamaría, A.; Bowman, A.B.; Aschner, M. Iron and Manganese-Related CNS Toxicity: Mechanisms, Diagnosis and Treatment. Expert Rev. Neurother. 2019, 19, 243–260. [Google Scholar] [CrossRef] [PubMed]
- Huat, T.J.; Camats-Perna, J.; Newcombe, E.A.; Valmas, N.; Kitazawa, M.; Medeiros, R. Metal Toxicity Links to Alzheimer’s Disease and Neuroinflammation. J. Mol. Biol. 2019, 431, 1843–1868. [Google Scholar] [CrossRef] [PubMed]
- Mezzaroba, L.; Alfieri, D.F.; Colado Simão, A.N.; Vissoci Reiche, E.M. The Role of Zinc, Copper, Manganese and Iron in Neurodegenerative Diseases. Neurotoxicology 2019, 74, 230–241. [Google Scholar] [CrossRef]
- Jomova, K.; Vondrakova, D.; Lawson, M.; Valko, M. Metals, Oxidative Stress and Neurodegenerative Disorders. Mol. Cell. Biochem. 2010, 345, 91–104. [Google Scholar] [CrossRef]
- Marreilha dos Santos, A.; Andrade, V.; Aschner, M. Neuroprotective and Therapeutic Strategies for Manganese-Induced Neurotoxicity. Clin. Pharmacol. Transl. Med. 2017, 1, 54. [Google Scholar]
- Leal, M.F.C.; Catarino, R.I.L.; Pimenta, A.M.; Souto, M.R.S. Roles of Metal Microelements in Neurodegenerative Diseases. Neurophysiology 2020, 52, 80–88. [Google Scholar] [CrossRef]
- Roeser, H.P.; Lee, G.R.; Nacht, S.; Cartwright, G.E. The Role of Ceruloplasmin in Iron Metabolism. J. Clin. Investig. 1970, 49, 2408–2417. [Google Scholar] [CrossRef]
- Pierson, H.; Muchenditsi, A.; Kim, B.E.; Ralle, M.; Zachos, N.; Huster, D.; Lutsenko, S. The Function of ATPase Copper Transporter ATP7B in Intestine. Gastroenterology 2018, 154, 168–180.e5. [Google Scholar] [CrossRef] [Green Version]
- Kardos, J.; Héja, L.; Simon, Á.; Jablonkai, I.; Kovács, R.; Jemnitz, K. Copper Signalling: Causes and Consequences 06 Biological Sciences 0601 Biochemistry and Cell Biology. Cell Commun. Signal. 2018, 71, 1–22. [Google Scholar] [CrossRef] [Green Version]
- Lange, S.C.; Bak, L.K.; Waagepetersen, H.S.; Schousboe, A.; Norenberg, M.D. Primary Cultures of Astrocytes: Their Value in Understanding Astrocytes in Health and Disease. Neurochem. Res. 2012, 37, 2569–2588. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marmolino, D.; Manto, M. Pregabalin Antagonizes Copper-Induced Toxicity in the Brain: In Vitro and in Vivo Studies. NeuroSignals 2011, 18, 210–222. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Wang, X.-P. Does Ceruloplasmin Defend Against Neurodegenerative Diseases? Curr. Neuropharmacol. 2018, 17, 539–549. [Google Scholar] [CrossRef]
- Członkowska, A.; Litwin, T.; Dusek, P.; Ferenci, P.; Lutsenko, S.; Medici, V.; Rybakowski, J.K.; Weiss, K.H.; Schilsky, M.L. Wilson Disease. Nat. Rev. Dis. Prim. 2018, 4, 21. [Google Scholar] [CrossRef]
- Litwin, T.; Dusek, P.; Szafrański, T.; Dzieżyc, K.; Członkowska, A.; Rybakowski, J.K. Psychiatric Manifestations in Wilson’s Disease: Possibilities and Difficulties for Treatment. Ther. Adv. Psychopharmacol. 2018, 8, 199–211. [Google Scholar] [CrossRef] [Green Version]
- Litwin, T.; Dusek, P.; Czlonkowska, A. Neurological Manifestations in Wilson’s Disease –Possible Treatment Options for Symptoms. Expert Opin. Orphan Drugs 2016, 7, 287–294. [Google Scholar] [CrossRef]
- Rupp, C.; Stremmel, W.; Weiss, K.H. Novel Perspectives on Wilson Disease Treatment. In Handbook of Clinical Neurology; Elsevier: Amsterdam, The Netherlands, 2017; Volume 142, pp. 225–230. [Google Scholar] [CrossRef]
- Ferreira, J.J.; Katzenschlager, R.; Bloem, B.R.; Bonuccelli, U.; Burn, D.; Deuschl, G.; Dietrichs, E.; Fabbrini, G.; Friedman, A.; Kanovsky, P.; et al. Summary of the Recommendations of the EFNS/MDS-ES Review on Therapeutic Management of Parkinson’s Disease. Eur. J. Neurol. 2013, 20, 5–15. [Google Scholar] [CrossRef]
- Kalpouzos, G. Accumulation de Fer Dans Le Cerveau et Déclin Moteur et Cognitif Dans Le Vieillissement Normal. Rev. Neuropsychol. 2018, 10, 205. [Google Scholar] [CrossRef]
- Ward, R.J.; Zucca, F.A.; Duyn, J.H.; Crichton, R.R.; Zecca, L. The Role of Iron in Brain Ageing and Neurodegenerative Disorders. Lancet Neurol. 2014, 13, 1045–1060. [Google Scholar] [CrossRef] [Green Version]
- Piloni, N.E.; Fermandez, V.; Videla, L.A.; Puntarulo, S. Acute Iron Overload and Oxidative Stress in Brain. Toxicology 2013, 314, 174–182. [Google Scholar] [CrossRef]
- Zecca, L.; Youdim, M.B.H.; Riederer, P.; Connor, J.R.; Crichton, R.R. Iron, Brain Ageing and Neurodegenerative Disorders. Nat. Rev. Neurosci. 2004, 5, 863–873. [Google Scholar] [CrossRef]
- Pantopoulos, K.; Porwal, S.K.; Tartakoff, A.; Devireddy, L. Mechanisms of Mammalian Iron Homeostasis. Biochemistry 2012, 51, 5705–5724. [Google Scholar] [CrossRef]
- Pelizzoni, I.; Macco, R.; Morini, M.F.; Zacchetti, D.; Grohovaz, F.; Codazzi, F. Iron Handling in Hippocampal Neurons: Activity-Dependent Iron Entry and Mitochondria-Mediated Neurotoxicity. Aging Cell 2011, 10, 172–183. [Google Scholar] [CrossRef] [PubMed]
- Sripetchwandee, J.; Sanit, J.; Chattipakorn, N.; Chattipakorn, S.C. Mitochondrial Calcium Uniporter Blocker Effectively Prevents Brain Mitochondrial Dysfunction Caused by Iron Overload. Life Sci. 2013, 92, 298–304. [Google Scholar] [CrossRef]
- Connor, J.R.; Kettenmann, H.; Ransom, B.R. Iron and Glia. In Neuroglia, 3rd ed.; Oxford University Press: Oxford, UK, 2013; pp. 586–602. [Google Scholar] [CrossRef]
- Möller, H.E.; Bossoni, L.; Connor, J.R.; Crichton, R.R.; Does, M.D.; Ward, R.J.; Zecca, L.; Zucca, F.A.; Ronen, I. Iron, Myelin, and the Brain: Neuroimaging Meets Neurobiology. Trends Neurosci. 2019, 42, 384–401. [Google Scholar] [CrossRef]
- Hinarejos, I.; Machuca-Arellano, C.; Sancho, P.; Espinós, C. Mitochondrial Dysfunction, Oxidative Stress and Neuroinflammation in Neurodegeneration with Brain Iron Accumulation (Nbia). Antioxidants 2020, 9, 1020. [Google Scholar] [CrossRef]
- Zecca, L.; Stroppolo, A.; Gatti, A.; Tampellini, D.; Toscani, M.; Gallorini, M.; Giaveri, G.; Arosio, P.; Santambrogio, P.; Fariello, R.G.; et al. The Role of Iron and Copper Molecules in the Neuronal Vulnerability of Locus Coeruleus and Substantia Nigra during Aging. Proc. Natl. Acad. Sci. USA 2004, 101, 9843–9848. [Google Scholar] [CrossRef] [Green Version]
- Haacke, E.M.; Cheng, N.Y.C.; House, M.J.; Liu, Q.; Neelavalli, J.; Ogg, R.J.; Khan, A.; Ayaz, M.; Kirsch, W.; Obenaus, A. Imaging Iron Stores in the Brain Using Magnetic Resonance Imaging. Magn. Reson. Imaging 2005, 23, 1–25. [Google Scholar] [CrossRef]
- Ravanfar, P.; Loi, S.M.; Syeda, W.T.; Van Rheenen, T.E.; Bush, A.I.; Desmond, P.; Cropley, V.L.; Lane, D.J.R.; Opazo, C.M.; Moffat, B.A.; et al. Systematic Review: Quantitative Susceptibility Mapping (QSM) of Brain Iron Profile in Neurodegenerative Diseases. Front. Neurosci. 2021, 15, 41. [Google Scholar] [CrossRef]
- Stelten, B.M.L.; Van Ommen, W.; Keizer, K. Neurodegeneration with Brain Iron Accumulation: A Novel Mutation in the Ceruloplasmin Gene. JAMA Neurol. 2019, 76, 229–230. [Google Scholar] [CrossRef] [PubMed]
- Miyajima, H. Aceruloplasminemia. Neuropathology 2015, 35, 83–90. [Google Scholar] [CrossRef] [PubMed]
- McNeill, A.; Birchall, D.; Hayflick, S.J.; Gregory, A.; Schenk, J.F.; Zimmerman, E.A.; Shang, H.; Miyajima, H.; Chinnery, P.F. T2* and FSE MRI Distinguishes Four Subtypes of Neurodegeneration with Brain Iron Accumulation. Neurology 2008, 70, 1614–1619. [Google Scholar] [CrossRef]
- Watanabe, H.; Takaya, N.; Miyajima, H.M.F. Iron Mapping in the Brain of a Patient with Aceruloplasminemia. In Proceedings of the 54th Experiment Nuclear Magnetic Resonance Conference, Pacific Grove, CA, USA, 14–19 April 2013. [Google Scholar]
- Skidmore, F.M.; Drago, V.; Foster, P.; Schmalfuss, I.M.; Heilman, K.M.; Streiff, R.R. Aceruloplasminaemia with Progressive Atrophy without Brain Iron Overload: Treatment with Oral Chelation. J. Neurol. Neurosurg. Psychiatry 2008, 79, 467–470. [Google Scholar] [CrossRef]
- Miyajima, H.; Takahashi, Y.; Kamata, T.; Shimizu, H.; Sakai, N.; Gitlin, J.D. Use of Desferrioxamine in the Treatment of Aceruloplasminemia. Ann. Neurol. 1997, 41, 404–407. [Google Scholar] [CrossRef] [PubMed]
- Kuhn, J.; Bewermeyer, H.; Miyajima, H.; Takahashi, Y.; Kuhn, K.F.; Hoogenraad, T.U. Treatment of Symptomatic Heterozygous Aceruloplasminemia with Oral Zinc Sulphate. Brain Dev. 2007, 29, 450–453. [Google Scholar] [CrossRef]
- Hayashida, M.; Hashioka, S.; Miki, H.; Nagahama, M.; Wake, R.; Miyaoka, T.; Horiguchi, J. Aceruloplasminemia with Psychomotor Excitement and Neurological Sign Was Improved by Minocycline (Case Report). Medicine 2016, 95, e3594. [Google Scholar] [CrossRef]
- Zanardi, A.; Conti, A.; Cremonesi, M.; D’Adamo, P.; Gilberti, E.; Apostoli, P.; Cannistraci, C.V.; Piperno, A.; David, S.; Alessio, M. Ceruloplasmin Replacement Therapy Ameliorates Neurological Symptoms in a Preclinical Model of Aceruloplasminemia. EMBO Mol. Med. 2018, 10, 91–106. [Google Scholar] [CrossRef] [PubMed]
- Keogh, M.J.; Singh, B.; Chinnery, P.F. Early Neuropsychiatry Features in Neuroferritinopathy. Mov. Disord. 2013, 28, 1310–1313. [Google Scholar] [CrossRef]
- Hesketh, S.; Sassoon, J.; Knight, R.; Brown, D.R. Elevated Manganese Levels in Blood and CNS in Human Prion Disease. Mol. Cell. Neurosci. 2008, 37, 590–598. [Google Scholar] [CrossRef]
- McNeill, A.; Gorman, G.; Khan, A.; Horvath, R.; Blamire, A.M.; Chinnery, P.F. Progressive Brain Iron Accumulation in Neuroferritinopathy Measured by the Thalamic T2* Relaxation Rate. Am. J. Neuroradiol. 2012, 33, 1810–1813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chinnery, P.F.; Crompton, D.E.; Birchall, D.; Jackson, M.J.; Coulthard, A.; Lombès, A.; Quinn, N.; Wills, A.; Fletcher, N.; Mottershead, J.P.; et al. Clinical Features and Natural History of Neuroferritinopathy Caused by the FTL1 460InsA Mutation. Brain 2007, 130, 110–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hartig, M.B.; Hörtnagel, K.; Garavaglia, B.; Zorzi, G.; Kmiec, T.; Klopstock, T.; Rostasy, K.; Svetel, M.; Kostic, V.S.; Schuelke, M.; et al. Genotypic and Phenotypic Spectrum of PANK2 Mutations in Patients with Neurodegeneration with Brain Iron Accumulation. Ann. Neurol. 2006, 59, 248–256. [Google Scholar] [CrossRef]
- Rohani, M.; Razmeh, S.; Shahidi, G.A.; Orooji, M. A Pilot Trial of Deferiprone in Pantothenate Kinase-Associated Neurodegeneration Patients. Neurol. Int. 2018, 9, 79–81. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Cordoba, M.; Villanueva-Paz, M.; Villalón-García, I.; Povea-Cabello, S.; Suárez-Rivero, J.M.; Talaverón-Rey, M.; Abril-Jaramillo, J.; Vintimilla-Tosi, A.; Sánchez-Alcázar, J.A. Precision Medicine in Pantothenate Kinase-Associated Neurodegeneration. Neural Regen. Res. 2019, 14, 1177–1185. [Google Scholar] [CrossRef] [PubMed]
- Hogarth, P.; Kurian, M.A.; Gregory, A.; Csányi, B.; Zagustin, T.; Kmiec, T.; Wood, P.; Klucken, A.; Scalise, N.; Sofia, F.; et al. Consensus Clinical Management Guideline for Pantothenate Kinase-Associated Neurodegeneration (PKAN). Mol. Genet. Metab. 2017, 120, 278–287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reetz, K.; Dogan, I.; Costa, A.S.; Dafotakis, M.; Fedosov, K.; Giunti, P.; Parkinson, M.H.; Sweeney, M.G.; Mariotti, C.; Panzeri, M.; et al. Biological and Clinical Characteristics of the European Friedreich’s Ataxia Consortium for Translational Studies (EFACTS) Cohort: A Cross-Sectional Analysis of Baseline Data. Lancet Neurol. 2015, 14, 174–182. [Google Scholar] [CrossRef]
- Branda, S.S.; Yang, Z.Y.; Chew, A.; Isaya, G. Mitochondrial Intermediate Peptidase and the Yeast Frataxin Homolog Together Maintain Mitochondrial Iron Homeostasis in Saccharomyces Cerevisiae. Hum. Mol. Genet. 1999, 8, 1099–1110. [Google Scholar] [CrossRef] [Green Version]
- Cook, A.; Giunti, P. Friedreich’s Ataxia: Clinical Features, Pathogenesis and Management. Br. Med. Bull. 2017, 124, 19–30. [Google Scholar] [CrossRef] [PubMed]
- Mollá, B.; Muñoz-Lasso, D.C.; Riveiro, F.; Bolinches-Amorós, A.; Pallardó, F.V.; Fernandez-Vilata, A.; De la Iglesia-Vaya, M.; Palau, F.; Gonzalez-Cabo, P. Reversible Axonal Dystrophy by Calcium Modulation in Frataxin-Deficient Sensory Neurons of YG8R Mice. Front. Mol. Neurosci. 2017, 10, 264. [Google Scholar] [CrossRef]
- Mincheva-Tasheva, S.; Obis, E.; Tamarit, J.; Ros, J. Apoptotic Cell Death and Altered Calcium Homeostasis Caused by Frataxin Depletion in Dorsal Root Ganglia Neurons Can Be Prevented by BH4 Domain of Bcl-XL Protein. Hum. Mol. Genet. 2014, 23, 1829–1841. [Google Scholar] [CrossRef] [Green Version]
- Piermarini, E.; Cartelli, D.; Pastore, A.; Tozzi, G.; Compagnucci, C.; Giorda, E.; D’Amico, J.; Petrini, S.; Bertini, E.; Cappelletti, G.; et al. Frataxin Silencing Alters Microtubule Stability in Motor Neurons: Implications for Friedreich’s Ataxia. Hum. Mol. Genet. 2016, 25, 4288–4301. [Google Scholar] [CrossRef] [PubMed]
- Shidara, Y.; Hollenbeck, P.J. Defects in Mitochondrial Axonal Transport and Membrane Potential without Increased Reactive Oxygen Species Production in a Drosophila Model of Friedreich Ataxia. J. Neurosci. 2010, 30, 11369–11378. [Google Scholar] [CrossRef] [Green Version]
- Shan, Y.; Schoenfeld, R.A.; Hayashi, G.; Napoli, E.; Akiyama, T.; Iodi Carstens, M.; Carstens, E.E.; Pook, M.A.; Cortopassi, G.A. Frataxin Deficiency Leads to Defects in Expression of Antioxidants and Nrf2 Expression in Dorsal Root Ganglia of the Friedreich’s Ataxia YG8R Mouse Model. Antioxid. Redox Signal. 2013, 19, 1481–1493. [Google Scholar] [CrossRef] [Green Version]
- Carletti, B.; Piermarini, E.; Tozzi, G.; Travaglini, L.; Torraco, A.; Pastore, A.; Sparaco, M.; Petrillo, S.; Carrozzo, R.; Bertini, E.; et al. Frataxin Silencing Inactivates Mitochondrial Complex I in NSC34 Motoneuronal Cells and Alters Glutathione Homeostasis. Int. J. Mol. Sci. 2014, 15, 5789. [Google Scholar] [CrossRef] [Green Version]
- Petrillo, S.; Piermarini, E.; Pastore, A.; Vasco, G.; Schirinzi, T.; Carrozzo, R.; Bertini, E.; Piemonte, F. Nrf2-Inducers Counteract Neurodegeneration in Frataxin-Silenced Motor Neurons: Disclosing New Therapeutic Targets for Friedreich’s Ataxia. Int. J. Mol. Sci. 2017, 18, 2173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Igoillo-Esteve, M.; Gurgul-Convey, E.; Hu, A.; Dos Santos, L.R.B.; Abdulkarim, B.; Chintawar, S.; Marselli, L.; Marchetti, P.; Jonas, J.C.; Eizirik, D.L.; et al. Unveiling a Common Mechanism of Apoptosis in β-Cells and Neurons in Friedreich’s Ataxia. Hum. Mol. Genet. 2015, 24, 2274–2286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katsu-Jiménez, Y.; Loría, F.; Corona, J.C.; Díaz-Nido, J. Gene Transfer of Brain-Derived Neurotrophic Factor (BDNF) Prevents Neurodegeneration Triggered by FXN Deficiency. Mol. Ther. 2016, 24, 877–889. [Google Scholar] [CrossRef] [PubMed]
- Bolinches-Amorós, A.; Mollá, B.; Pla-Martín, D.; Palau, F.; González-Cabo, P. Mitochondrial Dysfunction Induced by Frataxin Deficiency Is Associated with Cellular Senescence and Abnormal Calcium Metabolism. Front. Cell. Neurosci. 2014, 8. [Google Scholar] [CrossRef] [Green Version]
- Edenharter, O.; Schneuwly, S.; Navarro, J.A. Mitofusin-Dependent ER Stress Triggers Glial Dysfunction and Nervous System Degeneration in a Drosophila Model of Friedreich’s Ataxia. Front. Mol. Neurosci. 2018, 11, 38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Llorens, J.V.; Soriano, S.; Calap-Quintana, P.; Gonzalez-Cabo, P.; Moltó, M.D. The Role of Iron in Friedreich’s Ataxia: Insights From Studies in Human Tissues and Cellular and Animal Models. Front. Neurosci. 2019, 13, 75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fahey, M.C.; Cremer, P.D.; Aw, S.T.; Millist, L.; Todd, M.J.; White, O.B.; Halmagyi, M.; Corben, L.A.; Collins, V.; Churchyard, A.J.; et al. Vestibular, Saccadic and Fixation Abnormalities in Genetically Confirmed Friedreich Ataxia. Brain 2008, 131, 1035–1045. [Google Scholar] [CrossRef] [Green Version]
- Fortuna, F.; Barboni, P.; Liguori, R.; Valentino, M.L.; Savini, G.; Gellera, C.; Mariotti, C.; Rizzo, G.; Tonon, C.; Manners, D.; et al. Visual System Involvement in Patients with Friedreich’s Ataxia. Brain 2009, 132, 116–123. [Google Scholar] [CrossRef] [Green Version]
- Nieto, A.; Correia, R.; De Nóbrega, E.; Montón, F.; Hess, S.; Barroso, J. Cognition in Friedreich Ataxia. Cerebellum 2012, 11, 834–844. [Google Scholar] [CrossRef] [PubMed]
- Nieto, A.; Hernández-Torres, A.; Pérez-Flores, J.; Montón, F. Síntomas Depresivos En La Ataxia de Friedreich. Int. J. Clin. Health Psychol. 2018, 18, 18–26. [Google Scholar] [CrossRef] [PubMed]
- Williams, C.T.; De Jesus, O. Friedreich Ataxia. StatPearls. 2021. Available online: https://www.statpearls.com/ArticleLibrary/viewarticle/21969 (accessed on 31 May 2021).
- Delatycki, M.B.; Bidichandani, S.I. Friedreich Ataxia- Pathogenesis and Implications for Therapies. Neurobiol. Dis. 2019, 132, 104606. [Google Scholar] [CrossRef]
- Perdomini, M.; Belbellaa, B.; Monassier, L.; Reutenauer, L.; Messaddeq, N.; Cartier, N.; Crystal, R.G.; Aubourg, P.; Puccio, H. Prevention and Reversal of Severe Mitochondrial Cardiomyopathy by Gene Therapy in a Mouse Model of Friedreich’s Ataxia. Nat. Med. 2014, 20, 542–547. [Google Scholar] [CrossRef]
- Piguet, F.; De Montigny, C.; Vaucamps, N.; Reutenauer, L.; Eisenmann, A.; Puccio, H. Rapid and Complete Reversal of Sensory Ataxia by Gene Therapy in a Novel Model of Friedreich Ataxia. Mol. Ther. 2018, 26, 1940–1952. [Google Scholar] [CrossRef] [Green Version]
- Rocca, C.J.; Goodman, S.M.; Dulin, J.N.; Haquang, J.H.; Gertsman, I.; Blondelle, J.; Smith, J.L.M.; Heyser, C.J.; Cherqui, S. Transplantation of Wild-Type Mouse Hematopoietic Stem and Progenitor Cells Ameliorates Deficits in a Mouse Model of Friedreich’s Ataxia. Sci. Transl. Med. 2017, 9, eaaj2347. [Google Scholar] [CrossRef] [Green Version]
- Soragni, E.; Gottesfeld, J.M. Translating HDAC Inhibitors in Friedreich’s Ataxia. Expert Opin. Orphan Drugs 2016, 4, 961–970. [Google Scholar] [CrossRef] [Green Version]
- Cabantchik, Z.I.; Munnich, A.; Youdim, M.B.; Devos, D. Regional Siderosis: A New Challenge for Iron Chelation Therapy. Front. Pharmacol. 2013, 4, 167. [Google Scholar] [CrossRef] [Green Version]
- Singh, Y.P.; Pandey, A.; Vishwakarma, S.; Modi, G. A Review on Iron Chelators as Potential Therapeutic Agents for the Treatment of Alzheimer’s and Parkinson’s Diseases. Mol. Divers. 2019, 23, 509–526. [Google Scholar] [CrossRef] [PubMed]
- Mena, N.P.; García-Beltrán, O.; Lourido, F.; Urrutia, P.J.; Mena, R.; Castro-Castillo, V.; Cassels, B.K.; Núñez, M.T. The Novel Mitochondrial Iron Chelator 5-((Methylamino)Methyl)-8-Hydroxyquinoline Protects against Mitochondrial-Induced Oxidative Damage and Neuronal Death. Biochem. Biophys. Res. Commun. 2015, 463, 787–792. [Google Scholar] [CrossRef]
- García-Beltrán, O.; Mena, N.P.; Aguirre, P.; Barriga-González, G.; Galdámez, A.; Nagles, E.; Adasme, T.; Hidalgo, C.; Núñez, M.T. Development of an Iron-Selective Antioxidant Probe with Protective Effects on Neuronal Function. PLoS ONE 2017, 12, e0189043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tai, G.; Corben, L.A.; Yiu, E.M.; Milne, S.C.; Delatycki, M.B. Progress in the Treatment of Friedreich Ataxia. Neurol. Neurochir. Pol. 2018, 52, 129–139. [Google Scholar] [CrossRef] [PubMed]
- Nyarko-Danquah, I.; Pajarillo, E.; Digman, A.; Soliman, K.F.A.; Aschner, M.; Lee, E. Manganese Accumulation in the Brain via Various Transporters and Its Neurotoxicity Mechanisms. Molecules 2020, 25, 5880. [Google Scholar] [CrossRef] [PubMed]
- Pajarillo, E.; Johnson, J.; Rizor, A.; Nyarko-Danquah, I.; Adinew, G.; Bornhorst, J.; Stiboller, M.; Schwerdtle, T.; Son, D.S.; Aschner, M.; et al. Astrocyte-Specific Deletion of the Transcription Factor Yin Yang 1 in Murine Substantia Nigra Mitigates Manganese-Induced Dopaminergic Neurotoxicity. J. Biol. Chem. 2020, 295, 15662–15676. [Google Scholar] [CrossRef]
- Chen, C.J.; Ou, Y.C.; Lin, S.Y.; Liao, S.L.; Chen, S.Y.; Chen, J.H. Manganese Modulates Pro-Inflammatory Gene Expression in Activated Glia. Neurochem. Int. 2006, 49, 62–71. [Google Scholar] [CrossRef]
- Cordova, F.M.; Aguiar, A.S.; Peres, T.V.; Lopes, M.W.; Gonçalves, F.M.; Pedro, D.Z.; Lopes, S.C.; Pilati, C.; Prediger, R.D.S.; Farina, M.; et al. Manganese-Exposed Developing Rats Display Motor Deficits and Striatal Oxidative Stress That Are Reversed by Trolox. Arch. Toxicol. 2013, 87, 1231–1244. [Google Scholar] [CrossRef]
- Milatovic, D.; Gupta, R.C.; Yu, Y.; Zaja-Milatovic, S.; Aschner, M. Protective Effects of Antioxidants and Anti-Inflammatory Agents against Manganese-Induced Oxidative Damage and Neuronal Injury. Toxicol. Appl. Pharmacol. 2011, 256, 219–226. [Google Scholar] [CrossRef] [Green Version]
- Stephenson, A.P.; Schneider, J.A.; Nelson, B.C.; Atha, D.H.; Jain, A.; Soliman, K.F.A.; Aschner, M.; Mazzio, E.; Renee Reams, R. Manganese-Induced Oxidative DNA Damage in Neuronal SH-SY5Y Cells: Attenuation of Thymine Base Lesions by Glutathione and N-Acetylcysteine. Toxicol. Lett. 2013, 218, 299–307. [Google Scholar] [CrossRef] [Green Version]
- Harischandra, D.S.; Ghaisas, S.; Zenitsky, G.; Jin, H.; Kanthasamy, A.; Anantharam, V.; Kanthasamy, A.G. Manganese-Induced Neurotoxicity: New Insights into the Triad of Protein Misfolding, Mitochondrial Impairment, and Neuroinflammation. Front. Neurosci. 2019, 13, 654. [Google Scholar] [CrossRef] [Green Version]
- Smith, M.R.; Fernandes, J.; Go, Y.M.; Jones, D.P. Redox Dynamics of Manganese as a Mitochondrial Life-Death Switch. Biochem. Biophys. Res. Commun. 2017, 482, 388–398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Avila, D.S.; Benedetto, A.; Au, C.; Manarin, F.; Erikson, K.; Soares, F.A.; Rocha, J.B.T.; Aschner, M. Organotellurium and Organoselenium Compounds Attenuate Mn-Induced Toxicity in Caenorhabditis Elegans by Preventing Oxidative Stress. Free Radic. Biol. Med. 2012, 52, 1903–1910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merry, T.L.; Ristow, M. Nuclear Factor Erythroid-Derived 2-like 2 (NFE2L2, Nrf2) Mediates Exercise-Induced Mitochondrial Biogenesis and the Anti-Oxidant Response in Mice. J. Physiol. 2016, 594, 5195–5207. [Google Scholar] [CrossRef] [PubMed]
- Bouabid, S.; Tinakoua, A.; Lakhdar-Ghazal, N.; Benazzouz, A. Manganese Neurotoxicity: Behavioral Disorders Associated with Dysfunctions in the Basal Ganglia and Neurochemical Transmission. J. Neurochem. 2016, 136, 677–691. [Google Scholar] [CrossRef] [PubMed]
- Bowman, A.B.; Kwakye, G.F.; Herrero Hernández, E.; Aschner, M. Role of Manganese in Neurodegenerative Diseases. J. Trace Elem. Med. Biol. 2011, 25, 191–203. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, P.; Chakraborty, S.; Mukhopadhyay, S.; Lee, E.; Paoliello, M.M.B.; Bowman, A.B.; Aschner, M. Manganese Homeostasis in the Nervous System. J. Neurochem. 2015, 134, 601–610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kwakye, G.F.; Paoliello, M.M.B.; Mukhopadhyay, S.; Bowman, A.B.; Aschner, M. Manganese-Induced Parkinsonism and Parkinson’s Disease: Shared and Distinguishable Features. Int. J. Environ. Res. Public Health 2015, 12, 7519–7540. [Google Scholar] [CrossRef] [Green Version]
- O’Neal, S.L.; Zheng, W. Manganese Toxicity Upon Overexposure: A Decade in Review. Curr. Environ. Health Rep. 2015, 2, 315–328. [Google Scholar] [CrossRef] [Green Version]
- Prasad, S.; Shamim, U.; Minj, A.; Faruq, M.; Pal, P.K. Manganism without Parkinsonism: Isolated Unilateral Upper Limb Tremor in a Welder. J. Mov. Disord. 2019, 12, 135–137. [Google Scholar] [CrossRef]
- Guilarte, T.R. Manganese and Parkinson’s Disease: A Critical Review and New Findings. Environ. Health Perspect. 2010, 118, 1071–1080. [Google Scholar] [CrossRef] [Green Version]
- Cersosimo, M.G.; Koller, W.C. The Diagnosis of Manganese-Induced Parkinsonism. Neurotoxicology 2006, 27, 340–346. [Google Scholar] [CrossRef] [PubMed]
- Zheng, W.; Fu, S.X.; Dydak, U.; Cowan, D.M. Biomarkers of Manganese Intoxication. Neurotoxicology 2011, 32, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, D.; Gwiazda, R.; Bowler, R.; Roels, H.; Park, R.; Taicher, C.; Lucchini, R. Biomarkers of Mn Exposure in Humans. Am. J. Ind. Med. 2007, 50, 801–811. [Google Scholar] [CrossRef]
- Lucchini, R.; Placidi, D.; Cagna, G.; Fedrighi, C.; Oppini, M.; Peli, M.; Zoni, S. Manganese and Developmental Neurotoxicity. In Advances in Neurobiology; Springer: New York, NY, USA, 2017; Volume 18, pp. 13–34. [Google Scholar] [CrossRef]
- Laohaudomchok, W.; Lin, X.; Herrick, R.F.; Fang, S.C.; Cavallari, J.M.; Christiani, D.C.; Weisskopf, M.G. Toenail, Blood, and Urine as Biomarkers of Manganese Exposure. J. Occup. Environ. Med. 2011, 53, 506–510. [Google Scholar] [CrossRef] [Green Version]
- Coetzee, D.J.; McGovern, P.M.; Rao, R.; Harnack, L.J.; Georgieff, M.K.; Stepanov, I. Measuring the Impact of Manganese Exposure on Children’s Neurodevelopment: Advances and Research Gaps in Biomarker-Based Approaches. Environ. Health A Glob. Access Sci. Source. 2016, 15, 91. [Google Scholar] [CrossRef] [Green Version]
- Haynes, E.N.; Sucharew, H.; Kuhnell, P.; Alden, J.; Barnas, M.; Wright, R.O.; Parsons, P.J.; Aldous, K.M.; Praamsma, M.L.; Beidler, C.; et al. Manganese Exposure and Neurocognitive Outcomes in Rural School-Age Children: The Communities Actively Researching Exposure Study (Ohio, USA). Environ. Health Perspect. 2015, 123, 1066–1071. [Google Scholar] [CrossRef] [PubMed]
- Arora, M.; Bradman, A.; Austin, C.; Vedar, M.; Holland, N.; Eskenazi, B.; Smith, D.R. Determining Fetal Manganese Exposure from Mantle Dentine of Deciduous Teeth. Environ. Sci. Technol. 2012, 46, 5118–5125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gunier, R.B.; Arora, M.; Jerrett, M.; Bradman, A.; Harley, K.G.; Mora, A.M.; Kogut, K.; Hubbard, A.; Austin, C.; Holland, N.; et al. Manganese in Teeth and Neurodevelopment in Young Mexican-American Children. Environ. Res. 2015, 142, 688–695. [Google Scholar] [CrossRef] [Green Version]
- Andra, S.S.; Austin, C.; Arora, M. Tooth Matrix Analysis for Biomonitoring of Organic Chemical Exposure: Current Status, Challenges, and Opportunities. Environ. Res. 2015, 142, 387–406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lucchini, R.; Albini, E.; Placidi, D.; Gasparotti, R.; Pigozzi, M.G.; Montani, G.; Alessio, L. Brain Magnetic Resonance Imaging and Manganese Exposure. NeuroToxicology 2000, 21, 769–776. [Google Scholar]
- Dydak, U.; Jiang, Y.M.; Long, L.L.; Zhu, H.; Chen, J.; Li, W.M.; Edden, R.A.E.; Hu, S.; Fu, X.; Long, Z.; et al. In Vivo Measurement of Brain GABA Concentrations by Magnetic Resonance Spectroscopy in Smelters Occupationally Exposed to Manganese. Environ. Health Perspect. 2011, 119, 219–224. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, Y.; Zheng, W.; Long, L.; Zhao, W.; Li, X.; Mo, X.; Lu, J.; Fu, X.; Li, W.; Liu, S.; et al. Brain Magnetic Resonance Imaging and Manganese Concentrations in Red Blood Cells of Smelting Workers: Search for Biomarkers of Manganese Exposure. Neurotoxicology 2007, 28, 126–135. [Google Scholar] [CrossRef] [Green Version]
- Evans, G.R.; Masullo, L.N. Manganese Toxicity. StatPearls. 2020. Available online: https://www.statpearls.com/nurse/ce/activity/40086 (accessed on 1 June 2021).
- Huang, C.C.; Chu, N.S.; Lu, C.S.; Chen, R.S.; Calne, D.B. Long-Term Progression in Chronic Manganism: Ten Years of Follow-Up. Neurology 1998, 50, 698–700. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.M.; Mo, X.A.; Du, F.Q.; Fu, X.; Zhu, X.Y.; Gao, H.Y.; Xie, J.L.; Liao, F.L.; Pira, E.; Zheng, W. Effective Treatment of Manganese-Induced Occupational Parkinsonism with p-Aminosalicylic Acid: A Case of 17-Year Follow-up Study. J. Occup. Environ. Med. 2006, 48, 644–649. [Google Scholar] [CrossRef]
- Tuschl, K.; Mills, P.B.; Clayton, P.T. Manganese and the Brain. In International Review of Neurobiology; Academic Press Inc.: Cambridge, MA, USA, 2013; Volume 110, pp. 277–312. [Google Scholar] [CrossRef]
- Tuschl, K.; Mills, P.B.; Parsons, H.; Malone, M.; Fowler, D.; Bitner-Glindzicz, M.; Clayton, P.T. Hepatic Cirrhosis, Dystonia, Polycythaemia and Hypermanganesaemia—A New Metabolic Disorder. J. Inherit. Metab. Dis. 2008, 31, 151–163. [Google Scholar] [CrossRef]
- Ommati, M.M.; Heidari, R.; Ghanbarinejad, V.; Abdoli, N.; Niknahad, H. Taurine Treatment Provides Neuroprotection in a Mouse Model of Manganism. Biol. Trace Elem. Res. 2019, 190, 384–395. [Google Scholar] [CrossRef]
- Ahmadi, N.; Ghanbarinejad, V.; Ommati, M.M.; Jamshidzadeh, A.; Heidari, R. Taurine Prevents Mitochondrial Membrane Permeabilization and Swelling upon Interaction with Manganese: Implication in the Treatment of Cirrhosis-Associated Central Nervous System Complications. J. Biochem. Mol. Toxicol. 2018, 32. [Google Scholar] [CrossRef]
- Lu, C.L.; Tang, S.; Meng, Z.J.; He, Y.Y.; Song, L.Y.; Liu, Y.P.; Ma, N.; Li, X.Y.; Guo, S.C. Taurine Improves the Spatial Learning and Memory Ability Impaired by Sub-Chronic Manganese Exposure. J. Biomed. Sci. 2014, 21. [Google Scholar] [CrossRef] [Green Version]
- Neely, M.D.; Davison, C.A.; Aschner, M.; Bowman, A.B. Manganese and Rotenone-Induced Oxidative Stress Signatures Differ in IPSC-Derived Human Dopamine Neurons. Toxicol. Sci. 2017, 159, 366–379. [Google Scholar] [CrossRef] [Green Version]
- Coghill, D.R.; Banaschewski, T.; Soutullo, C.; Cottingham, M.G.; Zuddas, A. Systematic Review of Quality of Life and Functional Outcomes in Randomized Placebo-Controlled Studies of Medications for Attention-Deficit/Hyperactivity Disorder. Eur. Child. Adolesc. Psychiatry 2017, 26, 1283–1307. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magnus, W.; Nazir, S.; Anilkumar, A.C.; Shaban, K. Attention Deficit Hyperactivity Disorder. StatPearls. 2021. Available online: https://www.ncbi.nlm.nih.gov/books/NBK441838/ (accessed on 1 June 2021).
- Kemper, A.R.; Maslow, G.R.; Hill, S.; Namdari, B.; LaPointe, N.M.A.; Goode, A.P.; Coeytaux, R.R.; Befus, D.; Kosinski, A.S.; Bowen, S.E.; et al. Attention Deficit Hyperactivity Disorder: Diagnosis and Treatment in Children and Adolescents; Agency for Healthcare Research and Quality (US): Rockville, MD, USA, 2018. [Google Scholar]
- Lam, J.; Lanphear, B.P.; Bellinger, D.; Axelrad, D.A.; McPartland, J.; Sutton, P.; Davidson, L.; Daniels, N.; Sen, S.; Woodruff, T.J. Developmental Pbde Exposure and IQ/ADHD in Childhood: A Systematic Review and Meta-Analysis. Environ. Health Perspect. 2017, 125, 086001. [Google Scholar] [CrossRef] [PubMed]
- Shih, J.H.; Zeng, B.Y.; Lin, P.Y.; Chen, T.Y.; Chen, Y.W.; Wu, C.K.; Tseng, P.T.; Wu, M.K. Association between Peripheral Manganese Levels and Attention-Deficit/Hyperactivity Disorder: A Preliminary Meta-Analysis. Neuropsychiatr. Dis. Treat. 2018, 14, 1831–1842. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cortese, S. The Neurobiology and Genetics of Attention-Deficit/Hyperactivity Disorder (ADHD): What Every Clinician Should Know. Eur. J. Paediatr. Neurol. 2012, 16, 422–433. [Google Scholar] [CrossRef] [PubMed]
- Akutagava-Martins, G.C.; Rohde, L.A.; Hutz, M.H. Genetics of Attention-Deficit/Hyperactivity Disorder: An Update. Expert Rev. Neurother. 2016, 16, 145–156. [Google Scholar] [CrossRef] [PubMed]
- Field, S.S. Interaction of Genes and Nutritional Factors in the Etiology of Autism and Attention Deficit/Hyperactivity Disorders: A Case Control Study. Med. Hypotheses 2014, 82, 654–661. [Google Scholar] [CrossRef]
- Cecil, C.A.; Walton, E.; Barker, E.D. Prenatal Diet and Childhood ADHD: Exploring the Potential Role of IGF2 Methylation. Epigenomics 2016, 8, 1573–1576. [Google Scholar] [CrossRef] [Green Version]
- Heilskov Rytter, M.J.; Andersen, L.B.B.; Houmann, T.; Bilenberg, N.; Hvolby, A.; Molgaard, C.; Michaelsen, K.F.; Lauritzen, L. Diet in the Treatment of ADHD in Children-A Systematic Review of the Literature. Nord. J. Psychiatry 2015, 69, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Robberecht, H.; Verlaet, A.A.J.; Breynaert, A.; De Bruyne, T.; Hermans, N. Magnesium, Iron, Zinc, Copper and Selenium Status in Attention-Deficit/Hyperactivity Disorder (ADHD). Molecules 2020, 25, 440. [Google Scholar] [CrossRef]
- Verlaet, A.A.J.; Maasakkers, C.M.; Hermans, N.; Savelkoul, H.F.J. Rationale for Dietary Antioxidant Treatment of ADHD. Nutrients 2018, 10, 405. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.J.; Yang, C.Y.; Chou, W.J.; Lee, M.J.; Chou, M.C.; Kuo, H.C.; Yeh, Y.M.; Lee, S.Y.; Huang, L.H.; Li, S.C. Gut Microbiota and Dietary Patterns in Children with Attention-Deficit/Hyperactivity Disorder. Eur. Child. Adolesc. Psychiatry 2020, 29, 287–297. [Google Scholar] [CrossRef] [PubMed]
- Schullehner, J.; Thygesen, M.; Kristiansen, S.M.; Hansen, B.; Pedersen, C.B.; Dalsgaard, S. Exposure to Manganese in Drinking Water during Childhood and Association with Attention-Deficit Hyperactivity Disorder: A Nationwide Cohort Study. Environ. Health Perspect. 2020, 128, 1–10. [Google Scholar] [CrossRef]
- Brown, K.A.; Samuel, S.; Patel, D.R. Pharmacologic Management of Attention Deficit Hyperactivity Disorder in Children and Adolescents: A Review for Practitioners. Transl. Pediatr. 2018, 7, 36–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolraich, M.L.; Chan, E.; Froehlich, T.; Lynch, R.L.; Bax, A.; Redwine, S.T.; Ihyembe, D.; Hagan, J.F. ADHD Diagnosis and Treatment Guidelines: A Historical Perspective. Pediatrics 2019, 144. [Google Scholar] [CrossRef] [Green Version]
- Siutka, D.; Siutka, K.; Fudala, M.; Brola, W. Ephedrone Encephalopathy—A Disease of 19th Century Miners in the Era of the Internet. Aktual. Neurol. 2020, 20, 39–43. [Google Scholar] [CrossRef]
- Asser, A.; Hikima, A.; Raki, M.; Bergström, K.; Rose, S.; Juurmaa, J.; Krispin, V.; Muldmaa, M.; Lilles, S.; Rätsep, H.; et al. Subacute Administration of Both Methcathinone and Manganese Causes Basal Ganglia Damage in Mice Resembling That in Methcathinone Abusers. J. Neural Transm. 2020, 127, 707–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Janocha-Litwin, J.; Marianska, K.; Serafinska, S.; Simon, K. Manganese Encephalopathy among Ephedron Abusers-Case Reports. J. Neuroimaging 2015, 25, 832–835. [Google Scholar] [CrossRef] [PubMed]
- Ennok, M.; Sikk, K.; Haldre, S.; Taba, P. Cognitive Profile of Patients with Manganese-Methcathinone Encephalopathy. Neurotoxicology 2020, 76, 138–143. [Google Scholar] [CrossRef] [PubMed]
- Kałwa, A.; Habrat, B. Zaburzenia Funkcji Poznawczych Spowodowane Nadmierną Ekspozycją Na Związki Manganu. Zaburzenia Funkcji Poznawczych u Dozylnych Uzytkowników Preparatów Efedronu (Metkatynonu). Psychiatr. Pol. 2015, 49, 305–314. [Google Scholar] [CrossRef] [PubMed]
- Guilarte, T.R.; Gonzales, K.K. Manganese-Induced Parkinsonism Is Not Idiopathic Parkinson’s Disease: Environmental and Genetic Evidence. Toxicol. Sci. 2015, 146, 204–212. [Google Scholar] [CrossRef] [PubMed]
- Quadri, M.; Federico, A.; Zhao, T.; Breedveld, G.J.; Battisti, C.; Delnooz, C.; Severijnen, L.A.; Di Toro Mammarella, L.; Mignarri, A.; Monti, L.; et al. Mutations in SLC30A10 Cause Parkinsonism and Dystonia with Hypermanganesemia, Polycythemia, and Chronic Liver Disease. Am. J. Hum. Genet. 2012, 90, 467–477. [Google Scholar] [CrossRef] [Green Version]
- Tuschl, K.; Meyer, E.; Valdivia, L.E.; Zhao, N.; Dadswell, C.; Abdul-Sada, A.; Hung, C.Y.; Simpson, M.A.; Chong, W.K.; Jacques, T.S.; et al. Mutations in SLC39A14 Disrupt Manganese Homeostasis and Cause Childhood-Onset Parkinsonism-Dystonia. Nat. Commun. 2016, 7, 1–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Quadri, M.; Kamate, M.; Sharma, S.; Olgiati, S.; Graafland, J.; Breedveld, G.J.; Kori, I.; Hattiholi, V.; Jain, P.; Aneja, S.; et al. Manganese Transport Disorder: Novel SLC30A10 Mutations and Early Phenotypes. Mov. Disord. 2015, 30, 996–1001. [Google Scholar] [CrossRef]
- Zaki, M.S.; Issa, M.Y.; Elbendary, H.M.; El-Karaksy, H.; Hosny, H.; Ghobrial, C.; El Safty, A.; El-Hennawy, A.; Oraby, A.; Selim, L.; et al. Hypermanganesemia with Dystonia, Polycythemia and Cirrhosis in 10 Patients: Six Novel SLC30A10 Mutations and Further Phenotype Delineation. Clin. Genet. 2018, 93, 905–912. [Google Scholar] [CrossRef]
- Gulab, S.; Kayyali, H.R.; Al-Said, Y. Atypical Neurologic Phenotype and Novel SLC30A10 Mutation in Two Brothers with Hereditary Hypermanganesemia. Neuropediatrics 2018, 49, 72–75. [Google Scholar] [CrossRef]
- Avelino, M.A.; Fusão, E.F.; Pedroso, J.L.; Arita, J.H.; Ribeiro, R.T.; Pinho, R.S.; Tuschl, K.; Barsottini, O.G.P.; Masruha, M.R. Inherited Manganism: The “Cock-Walk” Gait and Typical Neuroimaging Features. J. Neurol. Sci. 2014, 341, 150–152. [Google Scholar] [CrossRef]
- Anagianni, S.; Tuschl, K. Genetic Disorders of Manganese Metabolism. Curr. Neurol. Neurosci. Rep. 2019, 19, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tuschl, K.; Clayton, P.T.; Gospe, S.M.; Gulab, S.; Ibrahim, S.; Singhi, P.; Aulakh, R.; Ribeiro, R.T.; Barsottini, O.G.; Zaki, M.S.; et al. Erratum: Syndrome of Hepatic Cirrhosis, Dystonia, Polycythemia, and Hypermanganesemia Caused by Mutations in SLC30A10, a Manganese Transporter in Man. Am. J. Hum. Genet. 2016, 99, 521. [Google Scholar] [CrossRef] [Green Version]
- Mukhtiar, K.; Ibrahim, S.; Tuschl, K.; Mills, P. Hypermanganesemia with Dystonia, Polycythemia and Cirrhosis (HMDPC) Due to Mutation in the SLC30A10 Gene. Brain Dev. 2016, 38, 862–865. [Google Scholar] [CrossRef]
- Park, J.H.; Hogrebe, M.; Grüneberg, M.; Duchesne, I.; Von Der Heiden, A.L.; Reunert, J.; Schlingmann, K.P.; Boycott, K.M.; Beaulieu, C.L.; Mhanni, A.A.; et al. SLC39A8 Deficiency: A Disorder of Manganese Transport and Glycosylation. Am. J. Hum. Genet. 2015, 97, 894–903. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boycott, K.M.; Beaulieu, C.L.; Kernohan, K.D.; Gebril, O.H.; Mhanni, A.; Chudley, A.E.; Redl, D.; Qin, W.; Hampson, S.; Küry, S.; et al. Autosomal-Recessive Intellectual Disability with Cerebellar Atrophy Syndrome Caused by Mutation of the Manganese and Zinc Transporter Gene SLC39A8. Am. J. Hum. Genet. 2015, 97, 886–893. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Riley, L.G.; Cowley, M.J.; Gayevskiy, V.; Roscioli, T.; Thorburn, D.R.; Prelog, K.; Bahlo, M.; Sue, C.M.; Balasubramaniam, S.; Christodoulou, J. A SLC39A8 Variant Causes Manganese Deficiency, and Glycosylation and Mitochondrial Disorders. J. Inherit. Metab. Dis. 2017, 40, 261–269. [Google Scholar] [CrossRef]
- Ferenci, P. Hepatic Encephalopathy. Gastroenterol. Rep. 2017, 5, 138–147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Butterworth, R.F.; Spahr, L.; Fontaine, S.; Layrargues, G.P. Manganese Toxicity, Dopaminergic Dysfunction and Hepatic Encephalopathy. Metab. Brain Dis. 1995, 10, 259–267. [Google Scholar] [CrossRef]
- Butterworth, R.F. Metal Toxicity, Liver Disease and Neurodegeneration. Neurotox. Res. 2010, 18, 100–105. [Google Scholar] [CrossRef] [PubMed]
- Ciećko-Michalska, I.; Szczepanek, M.; Słowik, A.; MacH, T. Pathogenesis of Hepatic Encephalopathy. Gastroenterol. Res. Pract. 2012, 2012, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Butterworth, R.F. Pathogenesis of Hepatic Encephalopathy in Cirrhosis: The Concept of Synergism Revisited. Metab. Brain Dis. 2016, 31, 1211–1215. [Google Scholar] [CrossRef]
- Prakash, R.; Mullen, K.D. Mechanisms, Diagnosis and Management of Hepatic Encephalopathy. Nat. Rev. Gastroenterol. Hepatol. 2010, 7, 15–525. [Google Scholar] [CrossRef]
- Rose, C.; Butterworth, R.F.; Zayed, J.; Normandin, L.; Todd, K.; Michalak, A.; Spahr, L.; Huet, P.M.; Pomier-Layrargues, G. Manganese Deposition in Basal Ganglia Structures Results from Both Portal-Systemic Shunting and Liver Dysfunction. Gastroenterology 1999, 117, 640–644. [Google Scholar] [CrossRef] [Green Version]
- Layrargues, G.P.; Shapcott, D.; Spahr, L.; Butterworth, R.F. Accumulation of Manganese and Copper in Pallidum of Cirrhotic Patients: Role in the Pathogenesis of Hepatic Encephalopathy? Metab. Brain Dis. 1995, 10, 353–356. [Google Scholar] [CrossRef]
- Chavarria, L.; Cordoba, J. Magnetic Resonance Imaging and Spectroscopy in Hepatic Encephalopathy. J. Clin. Exp. Hepatol. 2015, 5, S69–S74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alonso, J.; Córdoba, J.; Rovira, A. Brain Magnetic Resonance in Hepatic Encephalopathy. Semin. Ultrasound CT MRI 2014, 35, 136–152. [Google Scholar] [CrossRef] [PubMed]
- Spahr, L.; Butterworth, R.F.; Fontaine, S.; Bui, L.; Therrien, G.; Milette, P.C.; Lebrun, L.H.; Zayed, J.; Leblanc, A.; Pomier-Layrargues, G. Increased Blood Manganese in Cirrhotic Patients: Relationship to Pallidal Magnetic Resonance Signal Hyperintensity and Neurological Symptoms. Hepatology 1996, 24, 1116–1120. [Google Scholar] [CrossRef] [PubMed]
- Wijdicks, E.F.M. Hepatic Encephalopathy. N. Engl. J. Med. 2016, 375, 1660–1670. [Google Scholar] [CrossRef]
- Pazgan-Simon, M.; Zuwała-Jagiełło, J.; Serafińska, S.; Simon, K. Nutrition Principles and Recommendations in Different Types of Hepatic Encephalopathy. Clin. Exp. Hepatol. 2015, 4, 121–126. [Google Scholar] [CrossRef] [Green Version]
- Jin, H.; Harischandra, D.S.; Choi, C.; Martin, D.; Anantharam, V.; Kanthasamy, A.; Kanthasamy, A.G. Chapter 23. In Manganese and Prion Disease; RSC Publishing: Cambridge, UK, 2014; pp. 574–603. [Google Scholar] [CrossRef]
- Wong, B.S.; Chen, S.G.; Colucci, M.; Xie, Z.; Pan, T.; Liu, T.; Li, R.; Gambetti, P.; Sy, M.S.; Brown, D.R. Aberrant Metal Binding by Prion Protein in Human Prion Disease. J. Neurochem. 2001, 78, 1400–1408. [Google Scholar] [CrossRef] [Green Version]
- Toni, M.; Massimino, M.L.; De Mario, A.; Angiulli, E.; Spisni, E. Metal Dyshomeostasis and Their Pathological Role in Prion and Prion-like Diseases: The Basis for a Nutritional Approach. Front. Neurosci. 2017, 11, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Siggs, O.M.; Cruite, J.T.; Du, X.; Rutschmann, S.; Masliah, E.; Beutler, B.; Oldstone, M.B.A. Disruption of Copper Homeostasis Due to a Mutation of Atp7a Delays the Onset of Prion Disease. Proc. Natl. Acad. Sci. USA 2012, 109, 13733–13738. [Google Scholar] [CrossRef] [Green Version]
- Benetti, F.; Biarnés, X.; Attanasio, F.; Giachin, G.; Rizzarelli, E.; Legname, G. Structural Determinants in Prion Protein Folding and Stability. J. Mol. Biol. 2014, 426, 3796–3810. [Google Scholar] [CrossRef]
- Salzano, G.; Giachin, G.; Legname, G. Structural Consequences of Copper Binding to the Prion Protein. Cells 2019, 8, 770. [Google Scholar] [CrossRef] [Green Version]
- Gasperini, L.; Meneghetti, E.; Pastore, B.; Benetti, F.; Legname, G. Prion Protein and Copper Cooperatively Protect Neurons by Modulating NMDA Receptor through S-Nitrosylation. Antioxidants Redox Signal. 2015, 22, 772–784. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Canello, T.; Friedman-Levi, Y.; Mizrahi, M.; Binyamin, O.; Cohen, E.; Frid, K.; Gabizon, R. Copper Is Toxic to PrP-Ablated Mice and Exacerbates Disease in a Mouse Model of E200K Genetic Prion Disease. Neurobiol. Dis. 2012, 45, 1010–1017. [Google Scholar] [CrossRef]
- Mitteregger, G.; Korte, S.; Shakarami, M.; Herms, J.; Kretzschmar, H.A. Role of Copper and Manganese in Prion Disease Progression. Brain Res. 2009, 1292, 155–164. [Google Scholar] [CrossRef] [PubMed]
- Basu, S.; Mohan, M.L.; Luo, X.; Kundu, B.; Kong, Q.; Singh, N. Modulation of Proteinase K-Resistant Prion Protein in Cells and Infectious Brain Homogenate by Redox Iron: Implications for Prion Replication and Disease Pathogenesis. Mol. Biol. Cell 2007, 18, 3302–3312. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.O.; Geschwind, M.D. Clinical Update of Jakob-Creutzfeldt Disease. Curr. Opin. Neurol. 2015, 28, 302–310. [Google Scholar] [CrossRef] [PubMed]
- Blennow, K.; Diaz-Lucena, D.; Zetterberg, H.; Villar-Pique, A.; Karch, A.; Vidal, E.; Hermann, P.; Schmitz, M.; Ferrer Abizanda, I.; Zerr, I.; et al. CSF Neurogranin as a Neuronal Damage Marker in CJD: A Comparative Study with AD. J. Neurol. Neurosurg. Psychiatry 2019, 90, 846–853. [Google Scholar] [CrossRef] [PubMed]
- Villar-Pique, A.; Zerr, I.; Llorens, F. Cerebrospinal Fluid Neurogranin as a New Player in Prion Disease Diagnosis and Prognosis. Neural Regen. Res. 2020, 15, 861–862. [Google Scholar] [CrossRef] [PubMed]
- Kurlander, H.M.; Patten, B.M. Metals in Spinal Cord Tissue of Patients Dying of Motor Neuron Disease. Ann. Neurol. 1979, 6, 21–24. [Google Scholar] [CrossRef]
- Caga, J.; Hsieh, S.; Lillo, P.; Dudley, K.; Mioshi, E. The Impact of Cognitive and Behavioral Symptoms on ALS Patients and Their Caregivers. Front. Neurol. 2019, 10, 192. [Google Scholar] [CrossRef] [PubMed]
- Strong, M.J.; Abrahams, S.; Goldstein, L.H.; Woolley, S.; Mclaughlin, P.; Snowden, J.; Mioshi, E.; Roberts-South, A.; Benatar, M.; HortobáGyi, T.; et al. Amyotrophic Lateral Sclerosis—Frontotemporal Spectrum Disorder (ALS-FTSD): Revised Diagnostic Criteria. Amyotroph. Lateral Scler. Front. Degener. 2017, 18, 153–174. [Google Scholar] [CrossRef] [PubMed]
- Shahheydari, H.; Ragagnin, A.; Walker, A.K.; Toth, R.P.; Vidal, M.; Jagaraj, C.J.; Perri, E.R.; Konopka, A.; Sultana, J.M.; Atkin, J.D. Protein Quality Control and the Amyotrophic Lateral Sclerosis/Frontotemporal Dementia Continuum. Front. Mol. Neurosci. 2017, 10, 119. [Google Scholar] [CrossRef] [PubMed]
- Rosen, D.R.; Siddique, T.; Patterson, D.; Figlewicz, D.A.; Sapp, P.; Hentati, A.; Donaldson, D.; Goto, J.; O’Regan, J.P.; Deng, H.X.; et al. Mutations in Cu/Zn Superoxide Dismutase Gene Are Associated with Familial Amyotrophic Lateral Sclerosis. Nature 1993, 362, 59–62. [Google Scholar] [CrossRef]
- Hayward, L.J.; Rodriguez, J.A.; Kim, J.W.; Tiwari, A.; Goto, J.J.; Cabelli, D.E.; Valentine, J.S.; Brown, R.H. Decreased Metallation and Activity in Subsets of Mutant Superoxide Dismutases Associated with Familial Amyotrophic Lateral Sclerosis. J. Biol. Chem. 2002, 277, 15923–15931. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lelie, H.L.; Liba, A.; Bourassa, M.W.; Chattopadhyay, M.; Chan, P.K.; Gralla, E.B.; Miller, L.M.; Borchelt, D.R.; Valentine, J.S.; Whitelegge, J.P. Copper and Zinc Metallation Status of Copper-Zinc Superoxide Dismutase from Amyotrophic Lateral Sclerosis Transgenic Mice. J. Biol. Chem. 2011, 286, 2795–2806. [Google Scholar] [CrossRef] [Green Version]
- Tokuda, E.; Okawa, E.; Watanabe, S.; Ono, S.I.; Marklund, S.L. Dysregulation of Intracellular Copper Homeostasis Is Common to Transgenic Mice Expressing Human Mutant Superoxide Dismutase-1s Regardless of Their Copper-Binding Abilities. Neurobiol. Dis. 2013, 54, 308–319. [Google Scholar] [CrossRef] [PubMed]
- Hottinger, A.F.; Fine, E.G.; Gurney, M.E.; Zurn, A.D.; Aebischer, P. The Copper Chelator D-Penicillamine Delays Onset of Disease and Extends Survival in a Transgenic Mouse Model of Familial Amyotrophic Lateral Sclerosis. Eur. J. Neurosci. 1997, 9, 1548–1551. [Google Scholar] [CrossRef]
- Andreassen, O.A.; Dedeoglu, A.; Friedlich, A.; Ferrante, K.L.; Hughes, D.; Szabo, C.; Beal, M.F. Effects of an Inhibitor of Poly(ADP-Ribose) Polymerase, Desmethylselegiline, Trientine, and Lipoic Acid in Transgenic ALS Mice. Exp. Neurol. 2001, 168, 419–424. [Google Scholar] [CrossRef]
- Nagano, S.; Fujii, Y.; Yamamoto, T.; Taniyama, M.; Fukada, K.; Yanagihara, T.; Sakoda, S. The Efficacy of Trientine or Ascorbate Alone Compared to That of the Combined Treatment with These Two Agents in Familial Amyotrophic Lateral Sclerosis Model Mice. Exp. Neurol. 2003, 179, 176–180. [Google Scholar] [CrossRef]
- Roberts, B.R.; Lim, N.K.H.; McAllum, E.J.; Donnelly, P.S.; Hare, D.J.; Doble, P.A.; Turner, B.J.; Price, K.A.; Lim, S.C.; Paterson, B.M.; et al. Oral Treatment with CuII(Atsm) Increases Mutant SOD1 in Vivo but Protects Motor Neurons and Improves the Phenotype of a Transgenic Mouse Model of Amyotrophic Lateral Sclerosis. J. Neurosci. 2014, 34, 8021–8031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Farrawell, N.E.; Yerbury, M.R.; Plotkin, S.S.; McAlary, L.; Yerbury, J.J. CuATSM Protects Against the in Vitro Cytotoxicity of Wild-Type-Like Copper-Zinc Superoxide Dismutase Mutants but Not Mutants That Disrupt Metal Binding. ACS Chem. Neurosci. 2019, 10, 1555–1564. [Google Scholar] [CrossRef]
- Phase 1 Dose Escalation and PK Study of Cu(II)ATSM in ALS/MND—Full Text View—ClinicalTrials.gov. Available online: https://clinicaltrials.gov/ct2/show/NCT02870634 (accessed on 8 June 2021).
- Nikseresht, S.; Hilton, J.B.W.; Kysenius, K.; Liddell, J.R.; Crouch, P.J. Copper-ATSM as a Treatment for ALS: Support from Mutant SOD1 Models and Beyond. Life 2020, 10, 271. [Google Scholar] [CrossRef] [PubMed]
- McColgan, P.; Tabrizi, S.J. Huntington’s Disease: A Clinical Review. Eur. J. Neurol. 2018, 25, 24–34. [Google Scholar] [CrossRef]
- Munoz-Sanjuan, I.; Bates, G.P. The Importance of Integrating Basic and Clinical Research toward the Development of New Therapies for Huntington Disease. J. Clin. Investig. 2011, 121, 476–483. [Google Scholar] [CrossRef] [Green Version]
- Squadrone, S.; Brizio, P.; Abete, M.C.; Brusco, A. Trace Elements Profile in the Blood of Huntington’ Disease Patients. J. Trace Elem. Med. Biol. 2020, 57, 18–20. [Google Scholar] [CrossRef]
- Vonsattel, J.P.G.; DiFiglia, M. Huntington Disease. J. Neuropathol. Exp. Neurol. 1998, 57, 369–384. [Google Scholar] [CrossRef] [Green Version]
- Andrich, J.; Saft, C.; Ostholt, N.; Müller, T. Complex Movement Behaviour and Progression of Huntington’s Disease. Neurosci. Lett. 2007, 416, 272–274. [Google Scholar] [CrossRef]
- Walker, F.O. Huntington’s Disease. Lancet 2007, 369, 218–228. [Google Scholar] [CrossRef]
- Novak, M.J.U.; Tabrizi, S.J. Huntington’s Disease. BMJ 2010, 340, 34–40. [Google Scholar] [CrossRef] [Green Version]
- Verny, C.; Allain, P.; Prudean, A.; Malinge, M.C.; Gohier, B.; Scherer, C.; Bonneau, D.; Dubas, F.; Le Gall, D. Cognitive Changes in Asymptomatic Carriers of the Huntington Disease Mutation Gene. Eur. J. Neurol. 2007, 14, 1344–1350. [Google Scholar] [CrossRef]
- Kumar, A.; Kumar, V.; Singh, K.; Kumar, S.; Kim, Y.S.; Lee, Y.M.; Kim, J.J. Therapeutic Advances for Huntington’s Disease. Brain Sci. 2020, 10, 43. [Google Scholar] [CrossRef] [Green Version]
- Dean, M.; Sung, V.W. Review of Deutetrabenazine: A Novel Treatment for Chorea Associated with Huntington’s Disease. Drug Des. Dev. Ther. 2018, 12, 313–319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- NICE Clinical Guidelines, No. 91. Depression in Adults with a Chronic Physical Health Problem: Recognition and Management. Available online: https://www.nice.org.uk/guidance/cg91/resources/depression-in-adults-with-a-chronic-physical-health-problem-recognition-and-management-pdf-975744316357 (accessed on 2 June 2021).
- Hayley, S.; Poulter, M.O.; Merali, Z.; Anisman, H. The Pathogenesis of Clinical Depression: Stressor- and Cytokine-Induced Alterations of Neuroplasticity. Neuroscience 2005, 135, 659–678. [Google Scholar] [CrossRef] [PubMed]
- Młyniec, K.; Davies, C.L.; De Agüero Sánchez, I.G.; Pytka, K.; Budziszewska, B.; Nowak, G. Essential Elements in Depression and Anxiety. Part I. Pharmacol. Rep. 2014, 66, 534–544. [Google Scholar] [CrossRef]
- Młyniec, K.; Gaweł, M.; Doboszewska, U.; Starowicz, G.; Pytka, K.; Davies, C.L.; Budziszewska, B. Essential Elements in Depression and Anxiety. Part II. Pharmacol. Rep. 2015, 67, 187–194. [Google Scholar] [CrossRef]
- Nakamura, M.; Miura, A.; Nagahata, T.; Shibata, Y.; Okada, E.; Ojima, T. Low Zinc, Copper, and Manganese Intake Is Associated with Depression and Anxiety Symptoms in the Japanese Working Population: Findings from the Eating Habit and Well-Being Study. Nutrients 2019, 11, 847. [Google Scholar] [CrossRef] [Green Version]
- Blecharz-Klin, K.; Piechal, A.; Joniec-Maciejak, I.; Pyrzanowska, J.; Widy-Tyszkiewicz, E. Effect of Intranasal Manganese Administration on Neurotransmission and Spatial Learning in Rats. Toxicol. Appl. Pharmacol. 2012, 265, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Bouabid, S.; Delaville, C.; De Deurwaerdère, P.; Lakhdar-Ghazal, N.; Benazzouz, A. Manganese-Induced Atypical Parkinsonism Is Associated with Altered Basal Ganglia Activity and Changes in Tissue Levels of Monoamines in the Rat. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [Green Version]
- Rubio-López, N.; Morales-Suárez-Varela, M.; Pico, Y.; Livianos-Aldana, L.; Llopis-González, A. Nutrient Intake and Depression Symptoms in Spanish Children: The ANIVA Study. Int. J. Environ. Res. Public Health 2016, 13, 352. [Google Scholar] [CrossRef] [Green Version]
- Miyake, Y.; Tanaka, K.; Okubo, H.; Sasaki, S.; Furukawa, S.; Arakawa, M. Manganese Intake Is Inversely Associated with Depressive Symptoms during Pregnancy in Japan: Baseline Data from the Kyushu Okinawa Maternal and Child Health Study. J. Affect. Disord. 2017, 211, 124–129. [Google Scholar] [CrossRef] [PubMed]
- Bajpai, A.; Verma, A.K.; Srivastava, M.; Srivastava, R. Oxidative Stress and Major Depression. J. Clin. Diagnostic Res. 2014, 8, CC04–CC07. [Google Scholar] [CrossRef]
- Liu, T.; Zhong, S.; Liao, X.; Chen, J.; He, T.; Lai, S.; Jia, Y. A Meta-Analysis of Oxidative Stress Markers in Depression. PLoS ONE 2015, 10, e0138904. [Google Scholar] [CrossRef] [PubMed]
- Johnson, F.; Giulivi, C. Superoxide Dismutases and Their Impact upon Human Health. Mol. Aspects Med. 2005, 26, 340–352. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tarnacka, B.; Jopowicz, A.; Maślińska, M. Copper, Iron, and Manganese Toxicity in Neuropsychiatric Conditions. Int. J. Mol. Sci. 2021, 22, 7820. https://doi.org/10.3390/ijms22157820
Tarnacka B, Jopowicz A, Maślińska M. Copper, Iron, and Manganese Toxicity in Neuropsychiatric Conditions. International Journal of Molecular Sciences. 2021; 22(15):7820. https://doi.org/10.3390/ijms22157820
Chicago/Turabian StyleTarnacka, Beata, Anna Jopowicz, and Maria Maślińska. 2021. "Copper, Iron, and Manganese Toxicity in Neuropsychiatric Conditions" International Journal of Molecular Sciences 22, no. 15: 7820. https://doi.org/10.3390/ijms22157820