Dopamine and the Dopamine Oxidation Product 5,6-Dihydroxylindole Promote Distinct On-Pathway and Off-Pathway Aggregation of α-Synuclein in a pH-Dependent Manner

Journal of Molecular Biology

Volumn 387, Issue 3, 2009, Pages 771-785

  Pham, Chi L L ^a,b,c   Leong, Su Ling ^a,b,c   Ali, Feda E ^a,b,c   Kenche, Vijaya B ^a,b,c   Hill, Andrew F ^a,b,c   Gras, Sally L ^a,b   Barnham, Kevin J ^a,b,c   Cappai, Roberto ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

amyloid; dopamine; oligomer; Parkinson's disease; synuclein

Indexed keywords

5,6 DIHYDROXYINDOLE; ALPHA SYNUCLEIN; DOPAMINE; DOPAMINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; OLIGOMERIZATION; OXIDATION; OXIDATION REDUCTION REACTION; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; X RAY DIFFRACTION;

EID: 62049084616     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.02.007     Document Type: Article

References (61)

1. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., and Goedert M. Alpha-synuclein in Lewy bodies. Nature 388 (1997) 839-840
2. Spillantini M.G., Crowther R.A., Jakes R., Hasegawa M., and Goedert M. Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl Acad. Sci. USA 95 (1998) 6469-6473
3. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18 (1998) 106-108
4. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
5. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., et al. Alpha-synuclein locus triplication causes Parkinson's disease. Science 302 (2003) 841
6. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55 (2004) 164-173
7. 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 (2006) 115-126
8. Eliezer D., Kutluay E., Bussell Jr. R., and Browne G. Conformational properties of alpha-synuclein in its free and lipid-associated states. J. Mol. Biol. 307 (2001) 1061-1073
9. Davidson W.S., Jonas A., Clayton D.F., and George J.M. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273 (1998) 9443-9449
10. Chandra S., Chen X., Rizo J., Jahn R., and Sudhof T.C. A broken alpha-helix in folded alpha-synuclein. J. Biol. Chem. 278 (2003) 15313-15318
11. Iwai A., Masliah E., Yoshimoto M., Ge N., Flanagan L., de Silva H.A., et al. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14 (1995) 467-475
12. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., et al. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA 90 (1993) 11282-11286
13. Giasson B.I., Murray I.V., Trojanowski J.Q., and Lee V.M. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J. Biol. Chem. 276 (2001) 2380-2386
14. Lotharius J., and Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat. Rev. Neurosci. 3 (2002) 932-942
15. Perez R.G., Waymire J.C., Lin E., Liu J.J., Guo F., and Zigmond M.J. A role for alpha-synuclein in the regulation of dopamine biosynthesis. J. Neurosci. 22 (2002) 3090-3099
16. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.E., et al. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25 (2000) 239-252
17. Sulzer D., Bogulavsky J., Larsen K.E., Behr G., Karatekin E., Kleinman M.H., et al. Neuromelanin biosynthesis is driven by excess cytosolic catecholamines not accumulated by synaptic vesicles. Proc. Natl Acad. Sci. USA 97 (2000) 11869-11874
18. Graham D.G., Tiffany S.M., Bell W.R., and Gutknecht W.F. Autooxidation versus covalent binding of quiones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds towards C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 14 (1978) 644-653
19. Bisaglia M., Mammi S., and Bubacco L. Kinetic and structural analysis of the early oxidation products of dopamine: analysis of the interactions with alpha-synuclein. J. Biol. Chem. 282 (2007) 15597-15605
20. Conway K.A., Harper J.D., and Lansbury Jr. P.T. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 39 (2000) 2552-2563
21. Conway K.A., Harper J.D., and Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 4 (1998) 1318-1320
22. Giasson B.I., Uryu K., Trojanowski J.Q., and Lee V.M. Mutant and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro. J. Biol. Chem. 274 (1999) 7619-7622
23. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., and Lansbury Jr. P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl Acad. Sci. USA 97 (2000) 571-576
24. Lashuel H.A., Hartley D., Petre B.M., Walz T., and Lansbury Jr. P.T. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418 (2002) 291
25. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., and Lansbury Jr. P.T. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322 (2002) 1089-1102
26. Ding T.T., Lee S.J., Rochet J.C., and Lansbury Jr. P.T. Annular alpha-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry 41 (2002) 10209-10217
27. Smith D.P., Tew D.J., Hill A.F., Bottomley S.P., Masters C.L., Barnham K.J., and Cappai R. Formation of a high affinity lipid-binding intermediate during the early aggregation phase of alpha-synuclein. Biochemistry 47 (2008) 1425-1434
28. Cappai R., Leck S.L., Tew D.J., Williamson N.A., Smith D.P., Galatis D., et al. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. FASEB J. 19 (2005) 1377-1379
29. Norris E.H., Giasson B.I., Hodara R., Xu S., Trojanowski J.Q., Ischiropoulos H., and Lee V.M. Reversible inhibition of alpha-synuclein fibrillization by dopaminochrome-mediated conformational alterations. J. Biol. Chem. 280 (2005) 21212-21219
30. Conway K.A., Rochet J.C., Bieganski R.M., and Lansbury Jr. P.T. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294 (2001) 1346-1349
31. Li J., Zhu M., Manning-Bog A.B., Di Monte D.A., and Fink A.L. Dopamine and l-DOPA disaggregate amyloid fibrils: implications for Parkinson's and Alzheimer's disease. FASEB J. 18 (2004) 962-964
32. Hoyer W., Antony T., Cherny D., Heim G., Jovin T.M., and Subramaniam V. Dependence of alpha-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322 (2002) 383-393
33. Graham D.G. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14 (1978) 633-643
34. Graham D.G., Tiffany S.M., Bell Jr. W.R., and Gutknecht W.F. Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 14 (1978) 644-653
35. Leong S.L., Pham C.L.L., Galatis D., Fodero-Tavoletti M.T., Perez K., Hill A.F., et al. Formation of dopamine-mediated α-synuclein soluble oligomers requires methionine oxidation. Free Radic. Biol. Med. (2009) 10.1016/j.freeradbiomed.2009.02.009
36. Glaser C.B., Yamin G., Uversky V.N., and Fink A.L. Methionine oxidation, alpha-synuclein and Parkinson's disease. Biochim. Biophys. Acta 1703 (2005) 157-169
37. Barth A., and Zscherp C. What vibrations tell us about proteins. Q. Rev. Biophys. 35 (2002) 369-430
38. Uversky V.N., Li J., and Fink A.L. Evidence for a partially folded intermediate in α-synuclein fibril formation. J. Biol. Chem. 276 (2001) 10737-10744
39. Antunes F., Hana D., Rettoria D., and Cadenas E. Mitochondrial damage by nitric oxide is potentiated by dopamine in PC12 cell. Biochim. Biophys. Acta 1556 (2002) 233-238
40. Spencer J.P.E., Jenner A., Butler J., Aruoma O.I., Dexter D.T., Jenner P., and Halliwell P. Evaluation of the pro-oxidant and antioxidant actions of l-DOPA and dopamine in vitro: implications for Parkinson's disease. Free Radical Res. 24 (1996) 95-105
41. Follmer C., Romao L., Einsiedler C.M., Porto T.C., Lara F.A., Moncores M., et al. Dopamine affects the stability, hydration, and packing of protofibrils and fibrils of the wild type and variants of alpha-synuclein. Biochemistry 46 (2007) 472-482
42. Hirsch E., Graybiel A.M., and Agid Y.A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334 (1988) 345-348
43. Zecca L., Zucca F.A., Wilms H., and Sulzer D. Neuromelanin of the substantia nigra: a neuronal black hole with protective and toxic characteristics. Trends Neurosci. 26 (2003) 578-580
44. Wood S.J., Wypych J., Steavenson S., Louis J.C., Citron M., and Biere A.L. Alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274 (1999) 19509-19512
45. Goldsbury C., Goldie K., Pellaud J., Seelig J., Frey P., Muller S.A., et al. Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 130 (2000) 352-362
46. Krebs M.R., Bromley E.H., and Donald A.M. The binding of thioflavin-T to amyloid fibrils: localisation and implications. J. Struct. Biol. 149 (2005) 30-37
47. Dzwolak W., and Pecul M. Chiral bias of amyloid fibrils revealed by the twisted conformation of thioflavin T: an induced circular dichroism/DFT study. FEBS Lett. 579 (2005) 6601-6603
48. Petkova A.T., Buntkowsky G., Dyda F., Leapman R.D., Yau W.M., and Tycko R. Solid state NMR reveals a pH-dependent antiparallel beta-sheet registry in fibrils formed by a beta-amyloid peptide. J. Mol. Biol. 335 (2004) 247-260
49. Petkova A.T., Ishii Y., Balbach J.J., Antzutkin O.N., Leapman R.D., Delaglio F., and Tycko R. A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl Acad. Sci. USA 99 (2002) 16742-16747
50. Petkova A.T., Leapman R.D., Guo Z., Yau W.M., Mattson M.P., and Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307 (2005) 262-265
51. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
52. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
53. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95 (1998) 6448-6453
54. Caughey B., and Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26 (2003) 267-298
55. Volles M.J., Lee S.J., Rochet J.C., Shtilerman M.D., Ding T.T., Kessler J.C., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40 (2001) 7812-7819
56. Volles M.J., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41 (2002) 4595-4602
57. Koga K., Mori A., Ohashi S., Kurihara N., Kitagawa H., Ishikawa M., et al. H MRS identifies lactate rise in the striatum of MPTP-treated C57BL/6 mice. Eur. J. Neurosci. 23 (2006) 1077-1081
58. Bowen B.C., Block R.E., Sanchez-Ramos J., Pattany P.M., Lampman D.A., Murdoch J.B., and Quencer R.M. Proton MR spectroscopy of the brain in 14 patients with Parkinson disease. AJNR Am. J. Neuroradiol. 16 (1995) 61-68
59. Nilsson M.R. Techniques to study amyloid fibril formation in vitro. Methods 34 (2004) 151-160
60. Sunde M., Serpell L.C., Bartlam M., Fraser P.E., Pepys M.B., and Blake C.C. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273 (1997) 729-739
61. Squires A.M., Devlin G.L., Gras S.L., Tickler A.K., MacPhee C.E., and Dobson C.M. X-ray scattering study of the effect of hydration on the cross-beta structure of amyloid fibrils. J. Am. Chem. Soc. 128 (2006) 11738-11739