Oligomerization and membrane-binding properties of covalent adducts formed by the interaction of α-synuclein with the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde (DOPAL)

Journal of Biological Chemistry

Volumn 290, Issue 46, 2015, Pages 27660-27679

  Follmer, Cristian ^a,b   Coelho Cerqueira, Eduardo ^a   Yatabe Franco, Danilo Y ^a   Araujo, Gabriel D T ^a   Pinheiro, Anderson S ^a   Domont, Gilberto B ^a   Eliezer, David ^b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADDITION REACTIONS; AMINES; BINDING ENERGY; BINS; NEURONS; NEUROPHYSIOLOGY; OLIGOMERIZATION; PROTEINS;

DOPAMINERGIC NEURONS; LIPID COMPOSITION; MICHAEL ADDITIONS; OXIDATIVE DEAMINATION; PARKINSON DISEASE; SMALL UNILAMELLAR VESICLE; SUBSTANTIA NIGRA; SYNERGISTIC TOXICITY;

OLIGOMERS;

ACETALDEHYDE; ALDEHYDE 3,4 DIHYDROXYPHENYLACETALDEHYDE; ALPHA SYNUCLEIN; AMYLOID; DOPAMINE; LYSINE; METHIONINE; METHIONINE SULFOXIDE; UNCLASSIFIED DRUG; 3,4 DIHYDROXYPHENYLACETIC ACID; 3,4-DIHYDROXYPHENYLACETALDEHYDE; MEMBRANE LIPID; SCHIFF BASE;

ADDUCTION; ALPHA HELIX; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CROSS LINKING; DOPAMINE METABOLISM; LIPID MEMBRANE; MEMBRANE BINDING; MICHAEL ADDITION; NONHUMAN; OLIGOMERIZATION; OXIDATION; PERIODIC ACID SCHIFF STAIN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN LIPID INTERACTION; PROTEIN MODIFICATION; RAT; SYNAPSE VESICLE; ANALOGS AND DERIVATIVES; ANIMAL; CELL MEMBRANE; CHEMISTRY; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PARKINSON DISEASE; PATHOLOGY; SUBSTANTIA NIGRA;

3,4-DIHYDROXYPHENYLACETIC ACID; ALPHA-SYNUCLEIN; AMYLOID; ANIMALS; CELL MEMBRANE; DOPAMINE; DOPAMINERGIC NEURONS; HUMANS; LYSINE; MEMBRANE LIPIDS; OXIDATION-REDUCTION; PARKINSON DISEASE; RATS; SCHIFF BASES; SUBSTANTIA NIGRA;

EID: 84946925419     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.686584     Document Type: Article

References (62)

1. Langston, J. W. (2006) The Parkinson's complex: Parkinsonism is just the tip of the iceberg. Ann. Neurol. 59, 591-596
2. Langston, J. W., Ballard, P., Tetrud, J. W., and Irwin, I. (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979-980
3. Sulzer, D. (2007) Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci. 30, 244-250
4. Spillantini, M. G., and Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) α-Synuclein in Lewy bodies. Nature 388, 839-840
5. Spillantini, M. G., and Crowther, R. A., Jakes, R., Hasegawa, M., and Goedert, M. (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U.S.A. 95, 6469-6473
6. Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., et al. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047
7. Xu, J., and Kao, S. Y., Lee, F. J., Song, W., Jin, L. W., Yankner, B. A. (2002) Dopamine-dependent neurotoxicity of α-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med. 8, 600-606
8. Hasegawa, T., Matsuzaki-Kobayashi, M., Takeda, A., Sugeno, N., Kikuchi, A., Furukawa, K., Perry, G., and Smith, M. A., and Itoyama, Y. (2006) α-Synuclein facilitates the toxicity of oxidized catechol metabolites: implications for selective neurodegeneration in Parkinson's disease. FEBS Lett. 580, 2147-2152
9. Filloux, F., and Townsend, J. J. (1993) Pre- and postsynaptic neurotoxic effects of dopamine demonstrated by intrastriatal injection. Exp. Neurol. 119, 79-88
10. Follmer, C. (2014) Monoamine oxidase and α-synuclein as targets in Parkinson's disease therapy. Exp. Rev. Neurother. 14, 703-716
11. Burke, W. J., and Li, S. W., Williams, E. A., Nonneman, R., and Zahm, D. S. (2003) 3, 4-Dihydroxyphenylacetaldehyde is the toxic dopamine metabolite in vivo: implications for Parkinson's disease pathogenesis. Brain Res. 989, 205-213
12. Goldstein, D. S., Sullivan, P., Holmes, C., Kopin, I. J., and Basile, M. J., and Mash, D. C. (2011) Catechols in post-mortem brain of patients with Parkinson disease. Eur. J. Neurol. 18, 703-710
13. Goldstein, D. S., Sullivan, P., Holmes, C., and Miller, G. W., Alter, S., Strong, R., Mash, D. C., Kopin, I. J., and Sharabi, Y. (2013) Determinants of buildup of the toxic dopamine metabolite DOPAL in Parkinson's disease. J. Neurochem. 126, 591-603
14. Fitzmaurice, A. G., and Rhodes, S. L., Lulla, A., Murphy, N. P., and Lam, H. A., O'Donnell, K. C., Barnhill, L., Casida, J. E., Cockburn, M., Sagasti, A., Stahl, M. C., Maidment, N. T., Ritz, B., and Bronstein, J. M. (2013) Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc. Natl. Acad. Sci. U.S.A. 110, 636-641
15. Burke, W. J., and Kumar, V. B., Pandey, N., and Panneton, W. M., Gan, Q., Franko, M. W., O'Dell, M., Li, S. W., Pan, Y., Chung, H. D., and Galvin, J. E. (2008) Aggregation of α-synuclein by DOPAL, the monoamine oxidase metabolite of dopamine. Acta Neuropathol. 115, 193-203
16. Coelho-Cerqueira, E., Carmo-Gonçalves, P., Pinheiro, A. S., Cortines, J., and Follmer, C. (2013) α-Synuclein as an intrinsically disordered monomer-fact or artefact? FEBS J. 280, 4915-4927
17. Anderson, D.G., Mariappan, S. V., Buettner, G.R., and Doorn, J. A. (2011) Oxidation of 3, 4-dihydroxyphenylacetaldehyde, a toxic dopaminergic metabolite, to a semiquinone radical and an ortho-quinone. J. Biol. Chem. 286, 26978-26986
18. Abramoff, M. D., and Magalhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophot. Int. 11, 36-42
19. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
20. Bermel, W., Bertini, I., Felli, I. C., Lee, Y. M., Luchinat, C., and Pierattelli, R. (2006) Protonless NMR experiments for sequence-specific assignment of backbone nuclei in unfolded proteins. J. Am. Chem. Soc. 128, 3918-3919
21. Chandra, S., Chen, X., Rizo, J., Jahn, R., and Südhof, T. (2003) A broken α-helix in folded α-synuclein. J. Biol. Chem. 278, 15313-15318
22. Eliezer, D., Kutluay, E., Bussell, R. Jr., and Browne, G. (2001) Conformational properties of α-synuclein in its free and lipid-associated states. J. Mol. Biol. 307, 1061-1073
23. Eliezer, D. (2012) Distance information for disordered proteins from NMR and ESR measurements using paramagnetic spin labels. Methods Mol. Biol. 895, 127-138
24. Shvadchak, V. V., Falomir-Lockhart, L. J., Yushchenko, D. A., and Jovin, T. M. (2011a) Specificity and kinetics of α-synuclein binding to model membranes determined with fluorescent excited state intramolecular proton transfer (ESIPT) probe. J. Biol. Chem. 286, 13023-13032
25. Ysselstein, D., Joshi, M., Mishra, V., Griggs, A. M., and Asiago, J. M., McCabe, G.P., Stanciu, L. A., Post, C.B., and Rochet, J. C. (2015) Effects of impaired membrane interactions on α-synuclein aggregation and neurotoxicity. Neurobiol. Dis. 79, 150-163
26. Scholtz, J. M., Qian, H., York, E. J., and Stewart, J. M., and Baldwin, R. L. (1991) Parameters of helix-coil transition theory for alanine-based peptides of varying chain lengths in water. Biopolymers 31, 1463-1470
27. Shvadchak, V.V., Yushchenko, D. A., Pievo, R., and Jovin, T. M. (2011b) The mode of α-synuclein binding to membranes depends on lipid composition and lipid to protein ratio. FEBS Lett. 585, 3513-3519
28. Guang, H. M., and Du, G. H. (2006) High-throughput screening for monoamine oxidase - A and monoamine oxidase-B inhibitors using one-step fluorescence assay. Acta Pharmacol. Sin. 27, 760-766
29. Dixon, H. B., and Perham, R. N. (1968) Reversible blocking of free amines with citraconic anhydride. Biochem. J. 109, 312-314
30. Follmer, C., Romão, L., and Einsiedler, C. M., Porto, T. C., Lara, F. A., Moncores, M., Weissmüller, G., Lashuel, H. A., Lansbury, P., Neto, V. M., Silva, J. L., and Foguel, D. (2007) Dopamine affects the stability, hydration and packing of protofibrils and fibrils of wild-type and variants of α-synuclein. Biochemistry 46, 472-482
31. Coelho-Cerqueira, E., Pinheiro, A. S., and Follmer, C. (2014) Pitfalls associated with the use of thioflavin-T to monitor anti-fibrillogenic activity. Bioorg. Med. Chem. Lett. 24, 3194-3198
32. Yagi, H., Kusaka, E., Hongo, K., Mizobata, T., and Kawata, Y. (2005) Amyloid fibril formation of α-synuclein is accelerated by preformed amyloid seeds of other proteins: implications for the mechanism of transmissible conformational diseases. J. Biol. Chem. 280, 38609-38616
33. Uversky, V. N., Li, J., and Fink, A. L. (2001) Evidence for a partially folded intermediate in α-synuclein fibril formation. J. Biol. Chem. 276, 10737-10744
34. Leong, S. L., and Pham, C. L., Galatis, D., Fodero-Tavoletti, M. T., Perez, K., Hill, A. F., Masters, C. L., Ali, F. E., Barnham, K. J., and Cappai R (2009) Formation of dopamine-mediated α-synuclein-soluble oligomers requires methionine oxidation. Free Radic. Biol. Med. 46, 1328-1337
35. Zhou, W., Long, C., and Reaney, S. H., Di Monte, D. A., Fink, A. L., and Uversky, V. N. (2010) Met residues oxidation stabilizes non-toxic oligomers of α-synuclein through strengthening the auto-inhibitory intra-molecular long-range interactions. Biochim. Biophys. Acta 1802, 322-330
36. Carmo-Gonçalves, P., Pinheiro, A. S., Romão, L., Cortines, J., and Follmer, C. (2014) UV-induced selective oxidation of Met-5 to Met-sulfoxide leads to the formation of neurotoxic fibril-incompetent α-synuclein oligomers. Amyloid 21, 163-174
37. Rauniyar, N., and Prokai, L. (2009) Detection and identification of 4-hydroxy-2-nonenal Schiff-base adducts along with products of Michael addition using data-dependent neutral loss-driven MS3 acquisition: method evaluation through an in vitro study on cytochrome c oxidase modifications. Proteomics 9, 5188-5193
38. Li, H. T., and Lin, D. H., Luo, X. Y., Zhang, F., Ji, L. N., Du, H. N., Song, G. Q., Hu, J., Zhou, J. W., and Hu, H. Y. (2005) Inhibition of α-synuclein fibrillization by dopamine analogs via reaction with the amino group of α-synuclein. Implication for dopaminergic neurodegeneration. FEBS J. 272, 3661-3672
39. Lin, D., and Lee, H. G., Liu, Q., Perry, G., Smith, M. A., and Sayre, L. M. (2005) 4-Oxo-2-nonenal is both more neurotoxic and more protein reactive than 4-hydroxy-2-nonenal. Chem. Res. Toxicol. 18, 1219-1231
40. Sung, Y. H., and Eliezer, D. (2007) Residual structure, backbone dynamics, and interactions within the synuclein family. J. Mol. Biol. 372, 689-707
41. Kjaergaard, M., and Poulsen, F. M. (2011a) Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution. J. Biomol. NMR 50, 157-165
42. Kjaergaard, M., Brander, S., and Poulsen, F. M. (2011b) Random coil chemical shifts for intrinsically disordered proteins: effects of temperature and pH. J. Biomol. NMR 49, 139-149
43. Lotharius, J., and Brundin, P. (2002) Pathogenesis of Parkinson's disease: dopamine, vesicles and α-synuclein. Nat. Rev. Neurosci. 3, 932-942
44. Fowler, J. S., and Volkow, N. D., Wang, G. J., Logan, J., Pappas, N., Shea, C., and MacGregor, R. (1997) Age-related increases in brain MAO B in healthy human subjects. Neurobiol. Aging 18, 431-435
45. Lamensdorf, I., Eisenhofer, G., Harvey-White, J., Hayakawa, Y., Kirk, K., and Kopin, I.J. (2000) Metabolic stress in PC12 cells induces the formation of the endogenous dopaminergic neurotoxin, 3, 4-dihydroxyphenylacetaldehyde. J. Neurosci. Res. 60, 552-558
46. Mizuno, Y., Ohta, S., Tanaka, M., Takamiya, S., Suzuki, K., Sato, T., Oya, H., Ozawa, T., and Kagawa, Y. (1989) Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem. Biophys. Res. Commun. 163, 1450-1455
47. Conway, K. A., Rochet, J. C., Bieganski, R. M., and Lansbury, P. T., Jr. (2001) Kinetic stabilization of the α-synuclein protofibril by a dopamine-α-synuclein adduct. Science 294, 1346-1349
48. Bisaglia, M., Tosatto, L., Munari, F., Tessari, I., de Laureto, P. P., Mammi, S., and Bubacco, L. (2010) Dopamine quinones interact with α-synuclein to form unstructured adducts. Biochem. Biophys. Res. Commun. 394, 424-428
49. Qin, Z., Hu, D., Han, S., Reaney, S. H., Di Monte, D. A., and Fink, A. L. (2007) Effect of 4-hydroxy-2-nonenal modification on α-synuclein aggregation. J. Biol. Chem. 282, 5862-5870
50. Rees, J. N., and Florang, V. R., Eckert, L. L., and Doorn, J. A. (2009) Protein reactivity of 3, 4-dihydroxyphenylacetaldehyde, a toxic dopamine metabolite, is dependent on both the aldehyde and catechol. Chem. Res. Toxicol. 22, 1256-1263
51. Umanah, G. K., Son, C., Ding, F., Naider, F., and Becker, J. M. (2009) Cross-linking of a DOPA-containing peptide ligand into its G protein-coupled receptor. Biochemistry 48, 2033-2044
52. Yu, M., Hwang, J., and Deming, T. J. (1999) Role of l-3, 4-dihydroxyphenylalanine in mussel adhesive proteins. J. Am. Chem. Soc. 121, 5825-5826
53. Georgieva, E. R., and Ramlall, T. F., Borbat, P. P., Freed, J. H., and Eliezer, D. (2008) Membrane-bound α-synuclein forms an extended helix: long-distance pulsed ESR measurements using vesicles, bicelles, and rodlike micelles. J. Am. Chem. Soc. 130, 12856-12857
54. Bussell, R., Jr., and Eliezer, D. (2003) structural and functional role for 11-mer repeats in α-synuclein and other exchangeable lipid binding proteins. J. Mol. Biol. 329, 763-778
55. Ulmer, T. S., Bax, A., Cole, N. B., and Nussbaum, R. L. (2005) Structure and dynamics of micelle-bound human α-synuclein. J. Biol. Chem. 280, 9595-9603
56. Snead, D., and Eliezer, D. (2014) α-Synuclein function and dysfunction on cellular membranes. Exp. Neurobiol. 23, 292-313
57. Burré, J., Sharma, M., and Südhof, T. C. (2012) Systematic mutagenesis of α-synuclein reveals distinct sequence requirements for physiological and pathological activities. J. Neurosci. 32, 15227-15242
58. Maltsev, A. S., Chen, J., Levine, R. L., and Bax, A. (2013) Site-specific interaction between α-synuclein and membranes probed by NMR-observed methionine oxidation rates. J. Am. Chem. Soc. 135, 2943-2946
59. Zarbiv, Y., Simhi-Haham, D., Israeli, E., and Elhadi, S. A., Grigoletto, J., and Sharon, R. (2014) Lysine residues at the first and second KTKEGV repeats mediate α-synuclein binding to membrane phospholipids. Neurobiol. Dis. 70, 90-98
60. Bussell, R., Jr., and Eliezer, D. (2004) Effects of Parkinson's disease-linked mutations on the structure of lipid-associated α-synuclein. Biochemistry 43, 4810-4818
61. Fares, M. B., Ait-Bouziad, N., Dikiy, I., and Mbefo, M. K., Jovicic, A., Kiely, A., Holton, J. L., and Lee, S. J., Gitler, A. D., Eliezer, D., and Lashuel, H. A. (2014) The novel Parkinson's disease linked mutation G51D attenuates in vitro aggregation and membrane binding of α-synuclein, and enhances its secretion and nuclear localization in cells. Hum. Mol. Genet. 23, 4491-4509
62. Bartels, T., Kim, N. C., Luth, E. S., and Selkoe, D. J. (2014)N-α-Acetylation of α-synuclein increases its helical folding propensity, GM1 binding specificity and resistance to aggregation. PLoS One 9, e103727