Alpha-Synuclein Regulates Neuronal Levels of Manganese and Calcium

ACS Chemical Neuroscience

Volumn 6, Issue 10, 2015, Pages 1769-1779

  Dučić, Tanja ^a   Carboni, Eleonora ^c,d   Lai, Barry ^b   Chen, Si ^b   Michalke, Bernhard ^e   Lázaro, Diana F ^c   Outeiro, Tiago F ^c   Bähr, Mathias ^c,d   Barski, Elisabeth ^c   Lingor, Paul ^c,d  

^a ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d Deutsche Forschungsgemeinschaft   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

alpha synuclein; calcium; manganese; X ray fluorescence; XANES spectroscopy

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM; CARRIER PROTEIN; CELL PROTEIN; COPPER; IRON; MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PHOSPHORUS; POTASSIUM ION; SULFUR; ZINC ION; CATION TRANSPORT PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL METABOLISM; CELL STRUCTURE; CELL SUSPENSION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; IMMUNOCYTOCHEMISTRY; MESENCEPHALON; NERVE CELL; NONHUMAN; OXIDATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; X RAY ABSORPTION SPECTROSCOPY; X RAY FLUORESCENCE; ANALYSIS OF VARIANCE; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; STATISTICS; WISTAR RAT;

ALPHA-SYNUCLEIN; ANALYSIS OF VARIANCE; ANIMALS; CALCIUM; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; CELLS, CULTURED; EMBRYO, MAMMALIAN; GREEN FLUORESCENT PROTEINS; MANGANESE; MESENCEPHALON; MICROSCOPY, CONFOCAL; NEURONS; RATS; RATS, WISTAR; STATISTICS AS TOPIC; TRANSFECTION; X-RAY ABSORPTION SPECTROSCOPY; X-RAY MICROTOMOGRAPHY;

EID: 84945580347     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.5b00093     Document Type: Article

References (56)

1. Greger, J. L. (1999) Nutrition versus toxicology of manganese in humans: Evaluation of potential biomarkers NeuroToxicology 20, 205-212
2. Guilarte, T. R. (2010) Manganese and Parkinson's disease: a critical review and new findings Environ. Health Perspect. 118, 1071-1080 10.1289/ehp.0901748
3. Pal, P. K., Samii, A., and Calne, D. B. (1999) Manganese neurotoxicity: A review of clinical features, imaging and pathology NeuroToxicology 20, 227-238
4. Weintraub, D., Comella, C. L., and Horn, S. (2008) Parkinson's disease-Part 1: Pathophysiology, symptoms, burden, diagnosis, and assessment Am. J. Manag Care 14, S40-8
5. Dexter, D., Carayon, A., Javoy-Agid, F., Agid, Y., Wells, F. R., Daniel, S. E., Lees, A. J., Jenner, P., and Marsden, C. D. (1991) Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia Brain 114, 1953-1975 10.1093/brain/114.4.1953
6. Gasser, T. (2007) Update on the genetics of Parkinson's disease Mov. Disord. 22, S343-S350 10.1002/mds.21676
7. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., Lincoln, S., Crawley, A., Hanson, M., Maraganore, D., Adler, C., Cookson, M. R., Muenter, M., Baptista, M., Miller, D., Blancato, J., Hardy, J., and Gwinn-Hardy, K. (2003) alpha-Synuclein locus triplication causes Parkinson's disease Science 302, 841-841 10.1126/science.1090278
8. Lu, Y., Prudent, M., Fauvet, B., Lashuel, H. A., and Girault, H. H. (2011) Phosphorylation of α-Synuclein at Y125 and S129 alters its metal binding properties: implications for understanding the role of α-Synuclein in the pathogenesis of Parkinson's Disease and related disorders ACS Chem. Neurosci. 2, 667-675 10.1021/cn200074d
9. Kostka, M., Högen, T., Danzer, K. M., Levin, J., Habeck, M., Wirth, A., Wagner, R., Glabe, C. G., Finger, S., Heinzelmann, U., Garidel, P., Duan, W., Ross, C. A., Kretzschmar, H., and Giese, A. (2008) Single particle characterization of iron-induced pore-forming alpha-synuclein oligomers J. Biol. Chem. 283, 10992-11003 10.1074/jbc.M709634200
10. HaMai, D., Campbell, A., and Bondy, S. C. (2001) Modulation of oxidative events by multivalent manganese complexes in brain tissue Free Radical Biol. Med. 31, 763-768 10.1016/S0891-5849(01)00639-6
11. Salditt, T. and Ducić, T. (2014) X-Ray Microscopy for Neuroscience: Novel Opportunities by Coherent Optics. In Super-Resolution Microscopy Techniques in the Neurosciences, pp 257-290, Humana Press, Totowa, NJ.
12. Ducić, T., Quintes, S., Nave, K.-A., Susini, J., Rak, M., Tucoulou, R., Alevra, M., Guttmann, P., and Salditt, T. (2011) Structure and composition of myelinated axons: a multimodal synchrotron spectro-microscopy study J. Struct. Biol. 173, 202-212 10.1016/j.jsb.2010.10.001
13. Ralle, M. and Lutsenko, S. (2009) Quantitative imaging of metals in tissues BioMetals 22, 197-205 10.1007/s10534-008-9200-5
14. Ortega, R., Bohic, S., Tucoulou, R., Somogyi, A., and Devès, G. (2004) Microchemical element imaging of yeast and human cells using synchrotron X-ray microprobe with Kirkpatrick-Baez optics Anal. Chem. 76, 309-314 10.1021/ac035037r
15. McRae, R., Lai, B., Vogt, S., and Fahrni, C. J. (2006) Correlative microXRF and optical immunofluorescence microscopy of adherent cells labeled with ultrasmall gold particles J. Struct. Biol. 155, 22-29 10.1016/j.jsb.2005.09.013
16. Roth, J., Ponzoni, S., and Aschner, M. (2013) Manganese homeostasis and transport Met Ions Life Sci. 12, 169-201 10.1007/978-94-007-5561-1
17. Binolfi, A., Rasia, R. M., Bertoncini, C. W., Ceolin, M., Zweckstetter, M., Griesinger, C., Jovin, T. M., and Fernández, C. O. (2006) Interaction of alpha-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity and fibrillation enhancement J. Am. Chem. Soc. 128, 9893-9901 10.1021/ja0618649
18. Paris, I. and Segura-Aguilar, J. (2012) The role of metal ions in dopaminergic neuron degeneration in Parkinsonism and Parkinson's disease. In Metal Ions in Neurological Systems, pp 31-39, Springer, Vienna, Vienna.
19. Binolfi, A., Rodriguez, E. E., Valensin, D., D'Amelio, N., Ippoliti, E., Obal, G., Duran, R., Magistrato, A., Pritsch, O., Zweckstetter, M., Valensin, G., Carloni, P., Quntanar, L., Griesinger, C., and Fernández, C.O. (2010) Bioinorganic chemistry of Parkinson's disease: structural determinants for the copper-mediated amyloid formation of alpha-synuclein Inorg. Chem. 49, 10668-79 10.1021/ic1016752
20. Yuan, Y., Chen, S., Paunesku, T., Gleber, S. C., Liu, W. C., Doty, C. B., Mak, R., Deng, J., Jin, Q., Lai, B., Brister, K., Flachenecker, C., Jacobsen, C., Vogt, S., and Woloschak, G. E. (2013) Epidermal growth factor receptor targeted nuclear delivery and high-resolution whole cell X-ray imaging of Fe3O4@TiO2 nanoparticles in cancer cells ACS Nano 7, 10502-10517 10.1021/nn4033294
21. Ducić, T., Barski, E., Salome, M., Koch, J. C., Bähr, M., and Lingor, P. (2013) X-ray fluorescence analysis of iron and manganese distribution in primary dopaminergic neurons J. Neurochem. 124, 250-261 10.1111/jnc.12073
22. Kalia, K., Jiang, W., and Zheng, W. (2008) Manganese accumulates primarily in nuclei of cultured brain cells NeuroToxicology 29, 466-470 10.1016/j.neuro.2008.02.012
23. Carmona, A., Devès, G., Roudeau, S., Cloetens, P., Bohic, S., and Ortega, R. (2010) Manganese Accumulates within Golgi Apparatus in Dopaminergic Cells as Revealed by Synchrotron X-ray Fluorescence Nanoimaging ACS Chem. Neurosci. 1, 194-203 10.1021/cn900021z
24. Cai, T., Yao, T., Zheng, G., Chen, Y., Du, K., Cao, Y., Shen, X., Chen, J., and Luo, W. (2010) Manganese induces the overexpression of α-synuclein in PC12 cells via ERK activation Brain Res. 1359, 201-207 10.1016/j.brainres.2010.08.055
25. Li, Y., Sun, L., Cai, T., Zhang, Y., Lv, S., Wang, Y., and Ye, L. (2010) alpha-Synuclein overexpression during manganese-induced apoptosis in SH-SY5Y neuroblastoma cells Brain Res. Bull. 81, 428-433 10.1016/j.brainresbull.2009.11.007
26. Uversky, V. N., Li, J., and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure J. Biol. Chem. 276, 44284-44296 10.1074/jbc.M105343200
27. Verina, T., Schneider, J. S., and Guilarte, T. R. (2013) Manganese exposure induces α-synuclein aggregation in the frontal cortex of non-human primates Toxicol. Lett. 217, 177-183 10.1016/j.toxlet.2012.12.006
28. Bowman, A. B., Kwakye, G. F., Herrero Hernández, E., and Aschner, M. (2011) Role of manganese in neurodegenerative diseases J. Trace Elem. Med. Biol. 25, 191-203 10.1016/j.jtemb.2011.08.144
29. 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., and Lindquist, S. (2009) α-Synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity Nat. Genet. 41, 308-315 10.1038/ng.300
30. Carmona, A., Roudeau, S., Perrin, L., Veronesi, G., and Ortega, R. (2014) Environmental manganese compounds accumulate as Mn(ii) within the Golgi apparatus of dopamine cells: relationship between speciation, subcellular distribution, and cytotoxicity Metallomics 6, 822 10.1039/c4mt00012a
31. Sepúlveda, M. R., Wuytack, F., and Mata, A. M. (2012) High levels of Mn 2+inhibit secretory pathway Ca 2+/Mn 2+-ATPase (SPCA) activity and cause Golgi fragmentation in neurons and glia J. Neurochem. 123, 824-836 10.1111/j.1471-4159.2012.07888.x
32. Gavin, C. E., Gunter, K. K., and Gunter, T. E. (1999) Manganese and calcium transport in mitochondria: implications for manganese toxicity NeuroToxicology 20, 445-453
33. Fernández-Segura, E., Cañizares, F. J., Cubero, M. A., Warley, A., and Campos, A. (1999) Changes in Elemental Content During Apoptotic Cell Death Studied by Electron Probe X-Ray Microanalysis Exp. Cell Res. 253, 454-462 10.1006/excr.1999.4657
34. Ramos, J. M., Arrebola, F., Fernandez-Cervilla, F. J., Crespo, V., and Fernandez-Segura, E. (2011) Electron probe X-ray microanalysis of cisplatin-induced cell death in rat pheochromocytoma PC12 cells Histol. Histopathol. 26, 333-342
35. Streifel, K. M., Miller, J., Mouneimne, R., and Tjalkens, R. B. (2013) Manganese inhibits ATP-induced calcium entry through the transient receptor potential channel TRPC3 in astrocytes NeuroToxicology 34, 160-166 10.1016/j.neuro.2012.10.014
36. Narita, K., Kawasaki, F., and Kita, H. (1990) Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs Brain Res. 510, 289-295 10.1016/0006-8993(90)91379-U
37. Drapeau, P. and Nachshen, D. A. (1984) Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve endings isolated from rat brain J. Physiol. 348, 493 10.1113/jphysiol.1984.sp015121
38. Fitsanakis, V. A., Zhang, N., Garcia, S., and Aschner, M. (2010) Manganese (Mn) and iron (Fe): interdependency of transport and regulation Neurotoxic. Res. 18, 124-131 10.1007/s12640-009-9130-1
39. Kwik-Uribe, C. L., Reaney, S., Zhu, Z., and Smith, D. (2003) Alterations in cellular IRP-dependent iron regulation by in vitro manganese exposure in undifferentiated PC12 cells Brain Res. 973, 1-15 10.1016/S0006-8993(03)02457-0
40. Jomova, K., Vondrakova, D., Lawson, M., and Valko, M. (2010) Metals, oxidative stress and neurodegenerative disorders Mol. Cell. Biochem. 345, 91-104 10.1007/s11010-010-0563-x
41. Fernsebner, K., Zorn, J., Kanawati, B., Walker, A., and Michalke, B. (2014) Manganese leads to an increase in markers of oxidative stress as well as to a shift in the ratio of Fe(ii)/(iii) in rat brain tissue Metallomics 6, 921-931 10.1039/c4mt00022f
42. Salazar, J., Mena, N., Hunot, S., Prigent, A., Alvarez-Fischer, D., Arredondo, M., Duyckaerts, C., Sazdovitch, V., Zhao, L., Garrick, L. M., Nuñez, M. T., Garrick, M. D., Raisman-Vozari, R., and Hirsch, E. C. (2008) Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease Proc. Natl. Acad. Sci. U. S. A. 105, 18578-18583 10.1073/pnas.0804373105
43. Chew, K. C. M., Ang, E.-T., Tai, Y. K., Tsang, F., Lo, S. Q., Ong, E., Ong, W.-Y., Shen, H.-M., Lim, K.-L., Dawson, V. L., Dawson, T. M., and Soong, T. W. (2011) Enhanced autophagy from chronic toxicity of iron and mutant A53T α-synuclein: implications for neuronal cell death in Parkinson disease J. Biol. Chem. 286, 33380-33389 10.1074/jbc.M111.268409
44. Carboni, E. and Lingor, P. (2015) Insights on the interaction of alpha-synuclein and metals in the pathophysiology of Parkinson's disease Metallomics 7, 395-404 10.1039/C4MT00339J
45. Martinez-Finley, E. J., Gavin, C. E., Aschner, M., and Gunter, T. E. (2013) Manganese neurotoxicity and the role of reactive oxygen species Free Radical Biol. Med. 62, 65-75 10.1016/j.freeradbiomed.2013.01.032
46. Gunter, K. K., Aschner, M., Miller, L. M., Eliseev, R., Salter, J., Anderson, K., and Gunter, T. E. (2006) Determining the oxidation states of manganese in NT2 cells and cultured astrocytes Neurobiol. Aging 27, 1816-1826 10.1016/j.neurobiolaging.2005.10.003
47. Knöferle, J., Ramljak, S., Koch, J. C., Tönges, L., Asif, A. R., Michel, U., Wouters, F. S., Heermann, S., Krieglstein, K., Zerr, I., Bähr, M., and Lingor, P. (2010) TGF-beta 1 enhances neurite outgrowth via regulation of proteasome function and EFABP Neurobiol. Dis. 38, 395-404 10.1016/j.nbd.2010.02.011
48. Shimoda, K., Sauve, Y., Marini, A., Schwartz, J. P., and Commissiong, J. W. (1992) A high percentage yield of tyrosine hydroxylase-positive cells from rat E14 mesencephalic cell culture Brain Res. 586, 319-331 10.1016/0006-8993(92)91642-R
49. Taschenberger, G., Garrido, M., Tereshchenko, Y., Bähr, M., Zweckstetter, M., and Kügler, S. (2012) Aggregation of αSynuclein promotes progressive in vivo neurotoxicity in adult rat dopaminergic neurons Acta Neuropathol. 123, 671-683 10.1007/s00401-011-0926-8
50. Koch, J. C., Barski, E., Lingor, P., Bähr, M., and Michel, U. (2011) Plasmids containing NRSE/RE1 sites enhance neurite outgrowth of retinal ganglion cells via sequestration of REST independent of NRSE dsRNA expression FEBS J. 278, 3472-3483 10.1111/j.1742-4658.2011.08269.x
51. Lingor, P., Unsicker, K., and Krieglstein, K. (2000) GDNF and NT-4 Protect Midbrain Dopaminergic Neurons from Toxic Damage by Iron and Nitric Oxide Exp. Neurol. 163, 55-62 10.1006/exnr.2000.7339
52. Zierold, K. Cryotechniques for biological microanalysis. In Microbeam Analysis; Russel, P. E., Ed.; San Francisco Press Inc.: San Francisco, CA, 1989, pp 109-11
53. Chen, S., Deng, J., Yuan, Y., Flachenecker, C., Mak, R., Hornberger, B., Jin, Q., Shu, D., Lai, B., Maser, J., Roehrig, C., Paunesku, T., Gleber, S. C., Vine, D. J., Finney, L., Vonosinski, J., Bolbat, M., Spink, I., Chen, Z., Steele, J., Trapp, D., Irwin, J., Feser, M., Snyder, E., Brister, K., Jacobsen, C., Woloschak, G., and Vogt, S. (2014) The Bionanoprobe: hard X-ray fluorescence nanoprobe with cryogenic capabilities J. Synchrotron Radiat. 21, 66-75 10.1107/S1600577513029676
54. Vogt, S. (2003) MAPS: A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets J. Phys. IV 104, 635-638 10.1051/jp4:20030160
55. Lázaro, D. F., Rodrigues, E. F., Langohr, R., Shahpasandzadeh, H., Ribeiro, T., Guerreiro, P., Gerhardt, E., Kröhnert, K., Klucken, J., Pereira, M. D., Popova, B., Kruse, N., Mollenhauer, B., Rizzoli, S. O., Braus, G. H., Danzer, K. M., and Outeiro, T. F. (2014) Systematic comparison of the effects of alpha-synuclein mutations on its oligomerization and aggregation PLoS Genet. 10, e1004741 10.1371/journal.pgen.1004741
56. Vogt, S., Maser, J., and Jacobsen, C. (2003) Data analysis for X-ray fluorescence imaging J. Phys. IV 104, 617-622 10.1051/jp4:20030156