Alpha-synuclein ferrireductase activity is detectible in vivo, is altered in Parkinson's disease and increases the neurotoxicity of DOPAL

Molecular and Cellular Neuroscience

Volumn 85, Issue , 2017, Pages 1-11

  McDowall, Jennifer S ^a   Ntai, Ioanna ^a   Honeychurch, Kevin C ^b   Hart, John P ^b   Colin, Philippe ^c   Schneider, Bernard L ^c   Brown, David R ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^c EPFL   (Switzerland)

Author keywords

DOPAL; Ferrireductase; Iron; Neurotoxicity; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; FERRIREDUCTASE; LEVODOPA; OXIDOREDUCTASE; UNCLASSIFIED DRUG; FERRIC CITRATE IRON REDUCTASE; FLAVINE MONONUCLEOTIDE REDUCTASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL VIABILITY; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; DRUG EFFECT; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; METABOLITE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; RAT; SUBSTANTIA NIGRA PARS COMPACTA; ANIMAL; BRAIN; MALE; METABOLISM; SPRAGUE DAWLEY RAT;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; FEMALE; FMN REDUCTASE; HUMANS; MALE; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85027523959     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2017.08.001     Document Type: Article

References (49)

1. Abeliovich, A., Schmitz, Y., Farinas, I., Choi-Lundberg, D., Ho, W.H., Castillo, P.E., Shinsky, N., Verdugo, J.M., Armanini, M., Ryan, A., Hynes, M., Phillips, H., Sulzer, D., Rosenthal, A., Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25 (2000), 239–252.
2. Bartels, T., Choi, J.G., Selkoe, D.J., Alpha-synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477 (2011), 107–110.
3. Binolfi, A., Rasia, R.M., Bertoncini, C.W., Ceolin, M., Zweckstetter, M., Griesinger, C., Jovin, T.M., Fernandez, C.O., 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 (2006), 9893–9901.
4. Burke, W.J., 3,4-dihydroxyphenylacetaldehyde: a potential target for neuroprotective therapy in Parkinson's disease. Curr. Drug Targets CNS Neurol. Disord. 2 (2003), 143–148.
5. Burke, W.J., Li, S.W., Williams, E.A., Nonneman, R., Zahm, D.S., 3,4-Dihydroxyphenylacetaldehyde is the toxic dopamine metabolite in vivo: implications for Parkinson's disease pathogenesis. Brain Res. 989 (2003), 205–213.
6. Burre, J., Sharma, M., Tsetsenis, T., Buchman, V., Etherton, M.R., Sudhof, T.C., Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329 (2010), 1663–1667.
7. Chiba-Falek, O., Lopez, G.J., Nussbaum, R.L., Levels of alpha-synuclein mRNA in sporadic Parkinson disease patients. Mov. Disord. 21 (2006), 1703–1708.
8. Davies, P., Wang, X., Sarell, C.J., Drewett, A., Marken, F., Viles, J.H., Brown, D.R., The synucleins are a family of redox active copper binding proteins. Biochemistry 50 (2011), 37–47.
9. Davies, P., Moualla, D., Brown, D.R., Alpha-synuclein is a cellular ferrireductase. PLoS One, 6, 2011, e15814.
10. Dettmer, U., Newman, A.J., Luth, E.S., Bartels, T., Selkoe, D., In vivo crosslinking reveals principally oligomeric forms of alpha-synuclein and beta-synuclein in neurons and non-neural cells. J. Biol. Chem. 288 (2013), 6371–6385.
11. Dexter, D.T., Wells, F.R., Agid, F., Agid, Y., Lees, A.J., Jenner, P., Marsden, C.D., Increased nigral iron content in postmortem parkinsonian brain. Lancet 2 (1987), 1219–1220.
12. Dexter, D.T., Wells, F.R., Lees, A.J., Agid, F., Agid, Y., Jenner, P., Marsden, C.D., Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J. Neurochem. 52 (1989), 1830–1836.
13. Dexter, D.T., Carayon, A., Vidailhet, M., Ruberg, M., Agid, F., Agid, Y., Lees, A.J., Wells, F.R., Jenner, P., Marsden, C.D., Decreased ferritin levels in brain in Parkinson's disease. J. Neurochem. 55 (1990), 16–20.
14. Dexter, D.T., Carayon, A., Javoy-Agid, F., Agid, Y., Wells, F.R., Daniel, S.E., Lees, A.J., Jenner, P., Marsden, C.D., 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 (1991), 1953–1975.
15. Follmer, C., Coelho-Cerqueira, E., Yatabe-Franco, D.Y., Araujo, G.D., Pinheiro, A.S., Domont, G.B., Eliezer, D., Oligomerization and membrane-binding properties of covalent adducts formed by the interaction of alpha-synuclein with the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde (DOPAL). J. Biol. Chem. 290 (2015), 27660–27679.
16. Gaugler, M.N., Genc, O., Bobela, W., Mohanna, S., Ardah, M.T., El-Agnaf, O.M., Cantoni, M., Bensadoun, J.C., Schneggenburger, R., Knott, G.W., Aebischer, P., Schneider, B.L., Nigrostriatal overabundance of alpha-synuclein leads to decreased vesicle density and deficits in dopamine release that correlate with reduced motor activity. Acta Neuropathol. 123 (2012), 653–669.
17. Goedert, M., Alpha-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2 (2001), 492–501.
18. Goldstein, D.S., Sullivan, P., Cooney, A., Jinsmaa, Y., Sullivan, R., Gross, D.J., Holmes, C., Kopin, I.J., Sharabi, Y., Vesicular uptake blockade generates the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde in PC12 cells: relevance to the pathogenesis of Parkinson's disease. J. Neurochem. 123 (2012), 932–943.
19. Grundemann, J., Schlaudraff, F., Haeckel, O., Liss, B., Elevated alpha-synuclein mRNA levels in individual UV-laser-microdissected dopaminergic substantia nigra neurons in idiopathic Parkinson's disease. Nucleic Acids Res., 36, 2008, e38.
20. Hoepken, H.H., Gispert, S., Azizov, M., Klinkenberg, M., Ricciardi, F., Kurz, A., Morales-Gordo, B., Bonin, M., Riess, O., Gasser, T., Kogel, D., Steinmetz, H., Auburger, G., Parkinson patient fibroblasts show increased alpha-synuclein expression. Exp. Neurol. 212 (2008), 307–313.
21. Itokawa, K., Sekine, T., Funayama, M., Tomiyama, H., Fukui, M., Yamamoto, T., Tamura, N., Matsuda, H., Hattori, N., Araki, N., A case of alpha-synuclein gene duplication presenting with head-shaking movements. Mov. Disord. 28 (2013), 384–387.
22. Jao, C.C., Der-Sarkissian, A., Chen, J., Langen, R., Structure of membrane-bound alpha-synuclein studied by site-directed spin labeling. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 8331–8336.
23. Jao, C.C., Hegde, B.G., Chen, J., Haworth, I.S., Langen, R., Structure of membrane-bound alpha-synuclein from site-directed spin labeling and computational refinement. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 19666–19671.
24. Jinsmaa, Y., Sullivan, P., Gross, D., Cooney, A., Sharabi, Y., Goldstein, D.S., Divalent metal ions enhance DOPAL-induced oligomerization of alpha-synuclein. Neurosci. Lett. 569 (2014), 27–32.
25. Jinsmaa, Y., Sullivan, P., Sharabi, Y., Goldstein, D.S., DOPAL is transmissible to and oligomerizes alpha-synuclein in human glial cells. Auton. Neurosci. 194 (2016), 46–51.
26. Kahle, P.J., Neumann, M., Ozmen, L., Muller, V., Jacobsen, H., Schindzielorz, A., Okochi, M., Leimer, U., van Der Putten, H., Probst, A., Kremmer, E., Kretzschmar, H.A., Haass, C., Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha-synuclein in human and transgenic mouse brain. J. Neurosci. 20 (2000), 6365–6373.
27. Lotharius, J., Brundin, P., Impaired dopamine storage resulting from alpha-synuclein mutations may contribute to the pathogenesis of Parkinson's disease. Hum. Mol. Genet. 11 (2002), 2395–2407.
28. Lotharius, J., Barg, S., Wiekop, P., Lundberg, C., Raymon, H.K., Brundin, P., Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J. Biol. Chem. 277 (2002), 38884–38894.
29. Maroteaux, L., Scheller, R.H., The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res. Mol. Brain Res. 11 (1991), 335–343.
30. Maroteaux, L., Campanelli, J.T., Scheller, R.H., Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8 (1988), 2804–2815.
31. McDowall, J.S., Ntai, I., Hake, J., Whitley, P.R., Mason, J.M., Pudney, C.R., Brown, D.R., Steady-state kinetics of alpha-synuclein ferrireductase activity identifies the catalytically competent species. Biochemistry 56 (2017), 2497–2505.
32. Mullin, S., Schapira, A., The genetics of Parkinson's disease. Br. Med. Bull. 114 (2015), 39–52.
33. Munishkina, L.A., Ahmad, A., Fink, A.L., Uversky, V.N., Guiding protein aggregation with macromolecular crowding. Biochemistry 47 (2008), 8993–9006.
34. Nemani, V.M., Lu, W., Berge, V., Nakamura, K., Onoa, B., Lee, M.K., Chaudhry, F.A., Nicoll, R.A., Edwards, R.H., Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65 (2010), 66–79.
35. Perez, R.G., Waymire, J.C., Lin, E., Liu, J.J., Guo, F., Zigmond, M.J., A role for alpha-synuclein in the regulation of dopamine biosynthesis. J. Neurosci. 22 (2002), 3090–3099.
36. Rasia, R.M., Bertoncini, C.W., Marsh, D., Hoyer, W., Cherny, D., Zweckstetter, M., Griesinger, C., Jovin, T.M., Fernandez, C.O., Structural characterization of copper(II) binding to alpha-synuclein: insights into the bioinorganic chemistry of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 4294–4299.
37. Sendamarai, A.K., Ohgami, R.S., Fleming, M.D., Lawrence, C.M., Structure of the membrane proximal oxidoreductase domain of human Steap3, the dominant ferrireductase of the erythroid transferrin cycle. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 7410–7415.
38. Sidhu, A., Wersinger, C., Vernier, P., Does alpha-synuclein modulate dopaminergic synaptic content and tone at the synapse?. FASEB J. 18 (2004), 637–647.
39. Spillantini, M.G., Schmidt, M.L., Lee, V.M., Trojanowski, J.Q., Jakes, R., Goedert, M., Alpha-synuclein in Lewy bodies. Nature 388 (1997), 839–840.
40. Tokuda, T., Salem, S.A., Allsop, D., Mizuno, T., Nakagawa, M., Qureshi, M.M., Locascio, J.J., Schlossmacher, M.G., El-Agnaf, O.M., Decreased alpha-synuclein in cerebrospinal fluid of aged individuals and subjects with Parkinson's disease. Biochem. Biophys. Res. Commun. 349 (2006), 162–166.
41. Totterdell, S., Hanger, D., Meredith, G.E., The ultrastructural distribution of alpha-synuclein-like protein in normal mouse brain. Brain Res. 1004 (2004), 61–72.
42. Wang, X., Moualla, D., Wright, J.A., Brown, D.R., Copper binding regulates intracellular alpha-synuclein localisation, aggregation and toxicity. J. Neurochem. 113 (2010), 704–714.
43. Wey, M.C., Fernandez, E., Martinez, P.A., Sullivan, P., Goldstein, D.S., Strong, R., Neurodegeneration and motor dysfunction in mice lacking cytosolic and mitochondrial aldehyde dehydrogenases: implications for Parkinson's disease. PLoS One, 7, 2012, e31522.
44. Wilson, G.R., Sim, J.C., McLean, C., Giannandrea, M., Galea, C.A., Riseley, J.R., Stephenson, S.E., Fitzpatrick, E., Haas, S.A., Pope, K., Hogan, K.J., Gregg, R.G., Bromhead, C.J., Wargowski, D.S., Lawrence, C.H., James, P.A., Churchyard, A., Gao, Y., Phelan, D.G., Gillies, G., Salce, N., Stanford, L., Marsh, A.P., Mignogna, M.L., Hayflick, S.J., Leventer, R.J., Delatycki, M.B., Mellick, G.D., Kalscheuer, V.M., D'Adamo, P., Bahlo, M., Amor, D.J., Lockhart, P.J., Mutations in RAB39B cause X-linked intellectual disability and early-onset Parkinson disease with alpha-synuclein pathology. Am. J. Hum. Genet. 95 (2014), 729–735.
45. Winner, B., Jappelli, R., Maji, S.K., Desplats, P.A., Boyer, L., Aigner, S., Hetzer, C., Loher, T., Vilar, M., Campioni, S., Tzitzilonis, C., Soragni, A., Jessberger, S., Mira, H., Consiglio, A., Pham, E., Masliah, E., Gage, F.H., Riek, R., In vivo demonstration that alpha-synuclein oligomers are toxic. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4194–4199.
46. Wirdefeldt, K., Bogdanovic, N., Westerberg, L., Payami, H., Schalling, M., Murdoch, G., Expression of alpha-synuclein in the human brain: relation to Lewy body disease. Brain Res. Mol. Brain Res. 92 (2001), 58–65.
47. Wright, J.A., Wang, X., Brown, D.R., Unique copper-induced oligomers mediate alpha-synuclein toxicity. FASEB J. 23 (2009), 2384–2393.
48. Yu, S., Zuo, X., Li, Y., Zhang, C., Zhou, M., Zhang, Y.A., Ueda, K., Chan, P., Inhibition of tyrosine hydroxylase expression in alpha-synuclein-transfected dopaminergic neuronal cells. Neurosci. Lett. 367 (2004), 34–39.
49. Yu, S., Ueda, K., Chan, P., Alpha-synuclein and dopamine metabolism. Mol. Neurobiol. 31 (2005), 243–254.