DOPAL derived alpha-synuclein oligomers impair synaptic vesicles physiological function

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Plotegher, N ^a,h   Berti, G ^a   Ferrari, E ^b,c   Tessari, I ^a   Zanetti, M ^d,e   Lunelli, L ^d,e   Greggio, E ^a   Bisaglia, M ^a   Veronesi, M ^f   Girotto, S ^f   Dalla Serra, M ^d   Perego, C ^g   Casella, L ^b   Bubacco, L ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c INSTITUTE OF BIOMEDICAL TECHNOLOGIES   (Italy)

^d CNR   (Italy)

^e FONDAZIONE BRUNO KESSLER   (Italy)

^f ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^g UNIVERSITY OF MILAN   (Italy)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 3,4-DIHYDROXYPHENYLACETALDEHYDE; ALPHA SYNUCLEIN; PROTEIN AGGREGATE; PROTEIN BINDING;

ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECT; HUMAN; METABOLISM; MOUSE; NERVE CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERMEABILITY; PROTEIN MULTIMERIZATION; PROTEINOSIS; SYNAPSE VESICLE; TANDEM MASS SPECTROMETRY; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

3,4-DIHYDROXYPHENYLACETIC ACID; ALPHA-SYNUCLEIN; ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; NEURONS; PERMEABILITY; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SYNAPTIC VESICLES; TANDEM MASS SPECTROMETRY;

EID: 85009484076     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40699     Document Type: Article

References (52)

1. German, D. C., Manaye, K., Smith, W. K., Woodward, D. J. & Saper, C. B. Midbrain dopaminergic cell loss in Parkinson's disease: computer visualization. Ann Neurol 26, 507-514 (1989).
2. Bisaglia, M., Greggio, E., Beltramini, M. & Bubacco, L. Dysfunction of dopamine homeostasis: Clues in the hunt for novel Parkinson's disease therapies. FASEB J 27, 2101-2110 (2013).
3. Goldstein, D. S., Kopin, I. J. & Sharabi, Y. Catecholamine autotoxicity. Implications for pharmacology and therapeutics of Parkinson disease and related disorders. Pharmacol Ther 1110 (2014).
4. Galvin, J. E. Interaction of alpha-synuclein and dopamine metabolites in the pathogenesis of Parkinson's disease: A case for the selective vulnerability of the substantia nigra. Acta Neuropathol 112, 115-126 (2006).
5. Goldstein, D. S. et al. Determinants of buildup of the toxic dopamine metabolite DOPAL in Parkinson's disease. J Neurochem 126, 591-603 (2013).
6. Goldstein, D. S. et al. Catechols in post-mortem brain of patients with Parkinson disease. Eur J Neurol 18, 703-710 (2011).
7. Grünblatt, E. et al. Gene expression profiling of parkinsonian substantia nigra pars compacta; alterations in ubiquitin-proteasome, heat shock protein, iron and oxidative stress regulated proteins, cell adhesion/cellular matrix and vesicle trafficking genes. J Neural Transm 111, 1543-1573 (2004).
8. Liu, G. et al. Aldehyde dehydrogenase 1 defines and protects a nigrostriatal dopaminergic neuron subpopulation. J Clin Invest 124, 3032-3046 (2014).
9. Doorn, J. a., Florang, V. R., Schamp, J. H. & Vanle, B. C. Aldehyde dehydrogenase inhibition generates a reactive dopamine metabolite autotoxic to dopamine neurons. Park Relat Disord 20, S73-S75 (2014).
10. Fitzmaurice, A. G. et al. Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc Natl Acad Sci USA 110, 636-41 (2013).
11. Fitzmaurice, A. G., Rhodes, S. L., Cockburn, M., Ritz, B. & Bronstein, J. M. Aldehyde dehydrogenase variation enhances effect of pesticides associated with Parkinson disease. Neurology 82, 419-426 (2014).
12. Legros, H., Dingeval, M. G., Janin, F., Costentin, J. & Bonnet, J. J. Toxicity of a treatment associating dopamine and disulfiram for catecholaminergic neuroblastoma SH-SY5Y cells: Relationships with 3,4-dihydroxyphenylacetaldehyde formation. Neurotoxicology 25, 365-375 (2004).
13. Wey, M. C. Y. et al. Neurodegeneration and motor dysfunction in mice lacking cytosolic and mitochondrial aldehyde dehydrogenases: Implications for parkinson's disease. PLoS One 7 (2012).
14. Spillantini, M. G. et al. Alpha-synuclein in Lewy bodies. Nature 388, 839-840 (1997).
15. Kasten, M. & Klein, C. The many faces of alpha-synuclein mutations. Mov Disord 28, 697-701 (2013).
16. Nemani, V. M. et al. Article Increased Expression of a-Synuclein Reduces Neurotransmitter Release by Inhibiting Synaptic Vesicle Reclustering after Endocytosis. Neuron 65, 66-79 (2010).
17. Scott, D. & Roy, S.-Synuclein Inhibits Intersynaptic Vesicle Mobility and Maintains Recycling-Pool Homeostasis. J Neurosci 32, 10129-10135 (2012).
18. Burré, J. et al. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663-1667 (2010).
19. Abeliovich, a. et al. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239-252 (2000).
20. Outeiro, T. F. et al. Dopamine-Induced Conformational Changes in Alpha-Synuclein. PLoS One 4, 1-11 (2009).
21. Nakamura, K. Alpha-Synuclein and Mitochondria: Partners in CrimeNeurotherapeutics 10, 391-399 (2013).
22. Ebrahimi-Fakhari, D., Wahlster, L. & McLean, P. J. Protein degradation pathways in Parkinson's disease: Curse or blessing. Acta Neuropathol 124, 153-172 (2012).
23. Auluck, P. K., Caraveo, G. & Lindquist, S. -Synuclein: membrane interactions and toxicity in Parkinson's disease. Annu Rev Cell Dev Biol 26, 211-233 (2010).
24. Plotegher, N., Greggio, E., Bisaglia, M. & Bubacco, L. Biophysical groundwork as a hinge to unravel the biology of -synuclein aggregation and toxicity. Q Rev Biophys 1, 1-48 (2014).
25. Wilhelm, B. G. et al. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science (80-) 344, 1023-1028 (2014).
26. Theillet, F.-X. et al. Structural disorder of monomeric -synuclein persists in mammalian cells. Nature 530, 45-50 (2016).
27. Plotegher, N. & Bubacco, L. Lysines, Achilles' heel in alpha-synuclein conversion to a deadly neuronal endotoxin. Ageing Res Rev 26, 62-71 (2016).
28. Burke, W. J. et al. Aggregation of -synuclein by DOPAL, the monoamine oxidase metabolite of dopamine. Acta Neuropathol 115, 193-203 (2008).
29. Goldstein, D. S. et al. 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, 932-943 (2012).
30. Jinsmaa, Y. et al. Divalent metal ions enhance DOPAL-induced oligomerization of alpha-synuclein. Neurosci Lett 569, 27-32 (2014).
31. Follmer, C. et al. 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, jbc.M115.686584 (2015).
32. Daniele, F., Di Cairano, E. S., Moretti, S., Piccoli, G. & Perego, C. TIRFM and pH-sensitive GFP-probes to Evaluate Neurotransmitter Vesicle Dynamics in SH-SY5Y Neuroblastoma Cells: Cell Imaging and Data Analysis. J Vis Exp e52267, doi: 10.3791/52267 (2015).
33. Belluzzi, E. et al. LRRK2 phosphorylates pre-synaptic N-ethylmaleimide sensitive fusion (NSF) protein enhancing its ATPase activity and SNARE complex disassembling rate. Mol Neurodegener 11, 1 (2016).
34. Piccoli, G. et al. LRRK2 Controls Synaptic Vesicle Storage and Mobilization within the Recycling Pool. J Neurosci 31, 2225-2237 (2011).
35. Rees, J. N., Florang, V. R., Eckert, L. L. & Doorn, J. a. Protein reactivity of 3,4-dihydroxyphenylacetaldehyde, a toxic dopamine metabolite, is dependent on both the aldehyde and the catechol. Chem Res Toxicol 22, 1256-1263 (2009).
36. Lashuel, H. a. et al. -Synuclein, Especially the Parkinson'S Disease-Associated Mutants, Forms Pore-Like Annular and Tubular Protofibrils. J Mol Biol 322, 1089-1102 (2002).
37. Kim, H.-Y. et al. Structural Properties of Pore-Forming Oligomers of alpha-Synuclein. J-Amer Chem Soc 131, 17482-17489 (2009).
38. Quist, A. et al. Amyloid ion channels: A common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 102, 10427-10432 (2005).
39. Chen, S. W. et al. Structural characterization of toxic oligomers that are kinetically trapped during -synuclein fibril formation. Proc Natl Acad Sci USA 112, E1994-2003 (2015).
40. Plotegher, N. et al. The chaperone-like protein 14-3-3interacts with human -synuclein aggregation intermediates rerouting the amyloidogenic pathway and reducing -synuclein cellular toxicity. Hum Mol Genet 1-38, doi: 10.1093/hmg/ddu275 (2014).
41. Stöckl, M. T., Zijlstra, N. & Subramaniam, V. -Synuclein Oligomers: An Amyloid Pore-Insights into Mechanisms of -Synuclein Oligomer-Lipid Interactions. Mol Neurobiol 1-9, doi: 10.1007/s12035-012-8331-4 (2012).
42. Tosatto, L. et al. Alpha-synuclein pore forming activity upon membrane association. Biochim Biophys Acta-Biomembr 1818, 2876-2883 (2012).
43. De Franceschi, G. et al. Structural and morphological characterization of aggregated species of -synuclein induced by docosahexaenoic acid. J Biol Chem 286, 22262-22274 (2011).
44. Van Maarschalkerweerd, A., Vetri, V. & Vestergaard, B. Cholesterol facilitates interactions between -synuclein oligomers and charge-neutral membranes. FEBS Lett 589, 2661-2667 (2015).
45. Takamori, S. et al. Molecular Anatomy of a Trafficking Organelle. Cell 127, 831-846 (2006).
46. Jao, C. C., Der-Sarkissian, A., Chen, J. & Langen, R. Structure of membrane-bound -synuclein studied by site-directed spin labeling. Proc Natl Acad Sci USA 101, 8331-8336 (2004).
47. 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 USA 105, 19666-19671 (2008).
48. Tessari, I. et al. The reaction of -synuclein with tyrosinase: Possible implications for parkinson disease. J Biol Chem 283, 16808-16817 (2008).
49. Robbins, J. H. Preparation and Properties of p-Hydroxyphenylacetaldehyde and 3-Methoxy-4-Hydroxyphenylacetaldehyde. Arch Biochem Biophys 114, 576-584 (1966).
50. Dalla Serra, M. & Menestrina, G. Characterization of molecular properties of pore-forming toxins with planar lipid bilayers. Methods Mol Biol 145, 171-88 (2000).
51. Czajkowsky, D. M., Hotze, E. M., Shao, Z. & Tweten, R. K. Vertical collapse of a cytolysin prepore moves its transmembrane betahairpins to the membrane. EMBO J 23, 3206-15 (2004).
52. Nikonenko, A. G. & Skibo, G. G. Technique to quantify local clustering of synaptic vesicles using single section data. Microsc Res Tech 65, 287-291 (2004).