Manganese exposure induces α-synuclein aggregation in the frontal cortex of non-human primates

Toxicology Letters

Volumn 217, Issue 3, 2013, Pages 177-183

  Verina, Tatyana ^a   Schneider, Jay S ^b   Guilarte, Tomás R ^a,c  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c Columbia University ^*  (United States)

Author keywords

synuclein; Frontal cortex; Manganese; Neurotoxicity; Non human primates; Synucleinopathies

Indexed keywords

ALPHA SYNUCLEIN; MANGANESE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL SIZE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FRONTAL CORTEX; GLIA CELL; GRAY MATTER; IMMUNOREACTIVITY; MACACA; MALE; NERVE CELL; NEURITE; NEUROTOXICITY; NISSL STAINING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PYRAMIDAL NERVE CELL; WHITE MATTER;

ALPHA-SYNUCLEIN; ANIMALS; FRONTAL LOBE; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MALE; MANGANESE; NEURODEGENERATIVE DISEASES;

EID: 84873272610     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.12.006     Document Type: Article

References (53)

1. Bertolino A., Esposito G., Callicott J.H., Mattay V.S., Horn J.D., Frank J.A., Berman K.F., Weinberger D.R. Specific relationship between prefrontal neuronal N-acetylaspartate and activation of the working memory cortical network in schizophrenia. American Journal of Psychiatry 2000, 157:26-33.
2. Block W., Traber F., Flacke S., Jessen F., Pohl C., Schild H. In vivo proton MR-spectroscopy of the human brain: assessment of N-acetylaspartate (NAA) reduction as a marker for neurodegeneration. Amino Acids 2002, 23:317-323.
3. Bowler R.M., Gysens S., Diamond E., Booty A., Hartney C., Roels H.A. Neuropsychological sequelae of exposure to welding fumes in a group of occupationally exposed men. International Journal of Hygiene and Environmental Health 2003, 206:517-529.
4. Bowler R.M., Gysens S., Diamond E., Nakagawa S., Drezgic M., Roels H.A. Manganese exposure: neuropsychological and neurological symptoms and effects in welders. Neurotoxicology 2006, 27:315-326.
5. Bowler R.M., Roels H.A., Nakagawa S., Drezgic M., Diamond E., Park R., Koller W., Bowler R.P., Mergler D., Bouchard M., Smith D., Gwiazda R., Doty R.L. Dose-effect relationships between manganese exposure and neurological, neuropsychological and pulmonary function in confined space bridge welders. Occupational and Environmental Medicine 2007, 64:167-177.
6. Breydo L., Uversky V.N. Role of metal ions in aggregation of intrinsically disordered proteins in neurodegenerative diseases. Metallomics 2011, 3:1163-1180.
7. Burton N.C., Schneider J.S., Syversen T., Guilarte T.R. Effects of chronic manganese exposure on glutamatergic and GABAergic neurotransmitter markers in the non-human primate brain. Toxicological Sciences 2009, 111:131-139.
8. Cai T., Yao T., Zheng G., Chen Y., Du K., Cao Y., Shen X., Chen J., Luo W. Manganese induces the overexpression of α-synuclein in PC12 cells via ERK activation. Brain Research 2010, 1359:201-207.
9. Chesi A., Kilaru A., Fang X., Cooper A.A., Gitler A.D. The role of the Parkinson's disease gene PARK9 in essential cellular pathways and the manganese homeostasis network in yeast. PLoS ONE 2012, 7:e34178.
10. Chu Y., Kordower J.H. Age-associated increases of α-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: is it the target for Parkinson's disease?. Neurobiology of Disease 2007, 25:134-149.
11. Clark J.B. N-acetylaspartate: a marker for neuronal loss or mitochondrial dysfunction. Developmental Neuroscience 1998, 20:271-276.
12. Colisimo C., Guidi M. Parkinsonism due to ephedrone neurotoxicity: a case report. European Journal of Neurology 2009, 16:e114-e115.
13. De Bie R.M.A., Gladstone R.M., Strafella A.P., Ko J.H., Lang A.E. Manganese-induced parkinsonism associated with methcathinone (Ephedrone) abuse. Archives of Neurology 2007, 64:886-889.
14. 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., Mo X.-A., Meier D., Harezlak J., Aschner M., Murdoch J.B., Zheng W. In vivo measurement of brain GABA concentrations by magnetic resonance spectroscopy in smelters occupationally exposed to manganese. Environmental Health Perspectives 2011, 119:219-224.
15. Fellner L., Jellinger K.A., Wenning G.K., Stefanova N. Glial dysfunction in the pathogenesis of α-synucleinopathies: emerging concepts. Acta Neuropathologica 2011, 121:675-693.
16. Gitler A.D., Chesi A., Geddie M.L., Strathearn K.E., Hamamichi S., Hill K.J., Caldwell K.A., Caldwell G.A., Cooper A.A., Rochet J.-C., Lindquist S. α-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nature Genetics 2009, 41:308-315.
17. Guilarte T.R. Manganese and Parkinson's disease: a critical review and new findings. Environmental Health Perspectives 2010, 118:1071-1080.
18. Guilarte T.R., Chen M.-K., McGlothan J.L., Verina T., Wong D.F., Zhou Y., Alexander M., Rohde C.A., Syversen T., Decamp E., Koser A.J., Fritz S., Gonczi H., Anderson D.W., Schneider J.S. Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates. Experimental Neurology 2006, 202:381-390.
19. 1H-MRS and MRI study. Toxicological Sciences 2006, 94:351-358.
20. Guilarte T.R., Burton N.C., Verina T., Prabhu V.V., Becker K.G., Syversen T., Schneider J.S. Increased APLP1 expression and neurodegeneration in the frontal cortex of manganese-exposed non-human primates. Journal of Neurochemistry 2008, 105:1948-1959.
21. Guilarte T.R., Burton N.C., McGlothan J.L., Verina T., Zhou Y., Alexander M., Pham L., Griswold M., Wong D.F., Syversen T., Schneider J.S. Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism. Journal of Neurochemistry 2008, 107:1236-1247.
22. Iqbal M., Monaghan T., Redmond J. Manganese toxicity with ephedrone abuse manifesting as parkinsonism: a case report. Journal of Medical Case Reports 2012, 6:52.
23. Khan K., Wasserman G.A., Liu X., Ahmed E., Parvez F., Slavkovich V., Levy D., Mey J., van Geen A., Graziano J.H., Factor-Litvak P. Manganese exposure from drinking water and children's academic achievement. Neurotoxicology 2012, 33:91-97.
24. Klos K.J., Chandler K., Kumar N., Ahiskog J.E., Josephs K.A. Neuropsychological profiles of manganese neurotoxicity. European Journal of Neurology 2006, 13:1139-1141.
25. Li Y., Sun L., Cai T., Zhang Y., Lv S., Wang Y., Ye L. α-synuclein overexpression during manganese-induced apoptosis in SH-SY5Y neuroblastoma cells. Brain Research Bulletin 2010, 81:428-433.
26. Meral H., Kutukcu Y., Atmaca B., Ozer F., Hamancioglu K. Parkinsonism caused by chronic usage of intravenous potassium permanganate. Neurologist 2007, 13:92-94.
27. Mergler D., Baldwin M. Early manifestations of manganese neurotoxicity in humans: an update. Environmental Research 1997, 73:90-104.
28. Peneder T.M., Scholze P., Berger M.L., Riether H., Heinze G., Bertl J., Bauer J., Richfield E.K., Hornykiewicz O., Pifl C. Chronic exposure to manganese decreases striatal dopamine turnover in human α-synuclein transgenic mice. Neuroscience 2011, 180:280-292.
29. Perl D.P., Olanow C.W. The neuropathology of manganese-induced parkinsonism. Journal of Neuropathology and Experimental Neurology 2007, 66:675-682.
30. Pfil C., Kjorchide M., Kattinger A., Reither H., Hardy J., Hornykiewicz O. α-synuclein selectively increases manganese-induced viability loss in SK-N-MC neuroblastoma cells expressing the human dopamine transporter. Neuroscience Letters 2004, 354:34-37.
31. Rentschler G., Covolo L., Haddad A.A., Lucchini R.G., Zoni S., Broberg K. ATP13A2 (PARK9) polymorphisms influence the neurotoxic effects of manganese. Neurotoxicology 2012, 33:697-702.
32. Sanotsky Y., Lesyk R., Fedoryshyn L., Komnatska I., Matviyenko Y., Fahn S. Manganic encephalopathy due to ephedrone abuse. Movement Disorders 2007, 22:1337-1343.
33. Santos-Burgoa C., Rios C., Mercado L.A., Arechiga-Serrano R., Cano-Valle F., Eden-Wynter R.A., Texcalac-Sangrador J.L., Villa-Boragar J.P., Rodriguez-Agudelo Y., Montes S. Exposure to manganese: health effects on the general population, a pilot study in central Mexico. Environmental Research 2001, 85:90-104.
34. 2+ toxicity to Saccharomyces cerevisiae lacking YPK9p the orthologue of human ATP13A2. Biochemical and Biophysical Research Communications 2009, 383:198-202.
35. Schneider J.S., Decamp E., Koser A.J., Fritz S., Gonczi H., Syversen T., Guilarte T.R. Effects of chronic manganese exposure on cognitive and motor functioning in non-human primates. Brain Research 2006, 1118:222-231.
36. Schneider J.S., Decamp E., Clark K., Bouquio C., Syversen T., Guilarte T.R. Effects of manganese exposure on working memory in non-human primates. Brain Research 2009, 1258:86-95.
37. Selikhova M., Fedoryshyn L., Matviyenko Y., Komnatska I., Kyrylchuk M., Krolicki L., Friedman A., Taylor A., Jager H.R., Lees A., Sanotsky Y. Parkinsonism and dystonia caused by the illicit use of Ephedrone-a longitudinal study. Movement Disorders 2008, 23:2224-2231.
38. Sikk K., Taba P., Haldre S., Bergquist J., Nyholm D., Askmark H., Danfors T., Sorensen J., Thurfjell L., Raininko R., Eriksson R., Flink R., Farnstrand C., Aquilonius S.-M. Clinical, neuroimaging and neuropsychological features in addicts with manganese-ephedrone exposure. Acta Neurologica Scandinavica 2010, 121:237-243.
39. Stefanova N., Bucke P., Duerr S., Wenning G.K. Multiple system atrophy: an update. Lancet Neurology 2009, 8:1172-1178.
40. Stepens A., Logina I., Liguts V., Aldins P., Eksteina I., Platkajis A., Martinsone I., Terauds E., Rozentale B., Donaghy M. A parkinsonian syndrome in methcathinone users and the role of manganese. New England Journal of Medicine 2008, 358:1009-1017.
41. Stepens A., Stagg C.J., Platkajis A., Boudrias M.-H., Johansen-Berg H., Donaghy M. White matter abnormalities in methcathinone abusers with an extrapyramidal syndrome. Brain 2010, 133:3676-3684.
42. Tan J., Zhang T., Jiang L., Chi J., Hu D., Pan Q., Wang D., Zhang Z. Regulation of intracellular manganese homeostasis by Kufor-Rabek syndrome-associated ATP13A2 protein. Journal of Biological Chemistry 2011, 286:29654-29662.
43. Tong M., Dong M., de la Monte S.M. Brain-insulin like growth factor and neurotrophin resistance in Parkinson's disease and dementia with Lewy bodies: potential role of manganese neurotoxicity. Journal of Alzheimer's Disease 2009, 16:585-599.
44. Usenovic M., Tresse E., Mazzulli J.R., Taylor J.P., Krainc D. Deficiency of ATP13A2 leads to lysosomal dysfunction, α-synuclein accumulation, and neurotoxicity. Journal of Neuroscience 2012, 32:4240-4246.
45. Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein. Journal of Biological Chemistry 2001, 276:44284-44296.
46. Vanacore N. Epidemiological evidence of multiple system atrophy. Journal of Neural Transmission 2005, 112:1605-1612.
47. Verina T., Kiihl S.F., Schneider J.S., Guilarte T.R. Manganese exposure induces microglia activation and dystrophy in the substantia nigra of non-human primates. Neurotoxicology 2011, 32:215-226.
48. Vidal L., Alfonso M., Campos F., Faro L.R.F., Cervantes R.C., Duran R. Effects of manganese on extracellular levels of dopamine in rat striatum: an analysis in vivo by brain microdialysis. Neurochemical Research 2005, 30:1147-1154.
49. Wakabayashi K., Takahashi H. Cellular pathology in multiple system atrophy. Neuropathology 2006, 26:338-345.
50. Wasserman G.A., Liu X., Parvez F., Ahsan H., Levy D., Factor-Litvak P., Kline J., van Geen A., Slavkovich V., Lolacono N.J., Cheng Z., Zhang Y., Graziano J.H. Water manganese exposure and children's intellectual function in Araihazar, Bangladesh. Environmental Health Perspectives 2006, 114:124-129.
51. Wenning G.K., Jellinger K.A. The role of α-synuclein in the pathogenesis of multiple system atrophy. Acta Neuropathologica 2005, 109:129-140.
52. Yildirim E.A., Essizoglu A., Koksal A., Dogu B., Baybas S., Gokalp P. Chronic manganese intoxication due to methcathinone (Ephedron) abuse: a case report. Turkish Journal of Psychology 2009, 20:294-298.
53. Yoshida M. Multiple system atrophy: α-synuclein and neuronal degeneration. Neuropathology 2007, 27:484-493.