Guanidine hydrochloride denaturation of dopamine-induced α-synuclein oligomers: A small-angle X-ray scattering study

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 1, 2014, Pages 10-21

  Pham, Chi L L ^a   Kirby, Nigel ^b   Wood, Kathleen ^c   Ryan, Timothy ^d   Roberts, Blaine ^d   Sokolova, Anna ^c   Barnham, Kevin J ^d   Masters, Colin L ^d   Knott, Robert B ^c   Cappai, Roberto ^a   Curtain, Cyril C ^a,d   Rekas, Agata ^c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTRALIAN SYNCHROTRON   (Australia)

^c AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

synuclein; Dopamine; Oligomers; Parkinson's disease; Small angle X ray scattering

Indexed keywords

ALPHA SYNUCLEIN; DOPAMINE; GUANIDINE; MELANIN; OLIGOMER; SODIUM DIHYDROGEN PHOSPHATE;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CHEMICAL ANALYSIS; COVALENT BOND; DNA SEQUENCE; ESCHERICHIA COLI; HYDROGEN BOND; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NEUTRON SCATTERING; PARKINSON DISEASE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DENATURATION; X RAY CRYSTALLOGRAPHY;

DOPAMINE; OLIGOMERS; PARKINSON'S DISEASE; SMALL-ANGLE X-RAY SCATTERING; Α-SYNUCLEIN;

ALPHA-SYNUCLEIN; BRAIN; CLUSTER ANALYSIS; DOPAMINE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GUANIDINE; HUMANS; MODELS, CHEMICAL; PARKINSON DISEASE; PROTEIN DENATURATION; SCATTERING, RADIATION; ULTRACENTRIFUGATION;

EID: 84890127656     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24332     Document Type: Article

References (78)

1. Schapira AH. Pathogenesis of Parkinson's disease. Baillieres Clin Neurol 1997;6(1):15-36.
2. Uversky VN. A protein-chameleon: conformational plasticity of a-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 2003;21(2):211-234.
3. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997;276(5321):2045-2047.
4. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, Llorens V, Gomez Tortosa E, del Ser T, Munoz DG, de Yebenes JG. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 2004;55(2):164-173.
5. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, Levecque C, Larvor L, Andrieux J, Hulihan M, Waucquier N, Defebvre L, Amouyel P, Farrer M, Destee A. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 2004;364(9440):1167-1169.
6. Singleton AB, 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 MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K. alpha-Synuclein locus triplication causes Parkinson's disease. Science 2003;302(5646):841.
7. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, Lichtner P, Scholz SW, Hernandez DG, Kruger R, Federoff M, Klein C, Goate A, Perlmutter J, Bonin M, Nalls MA, Illig T, Gieger C, Houlden H, Steffens M, Okun MS, Racette BA, Cookson MR, Foote KD, Fernandez HH, Traynor BJ, Schreiber S, Arepalli S, Zonozi R, Gwinn K, van der Brug M, Lopez G, Chanock SJ, Schatzkin A, Park Y, Hollenbeck A, Gao J, Huang X, Wood NW, Lorenz D, Deuschl G, Chen H, Riess O, Hardy JA, Singleton AB, Gasser T. Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 2009;41(12):1308-1312.
8. Sidhu A, Wersinger C, Vernier P. Does alpha-synuclein modulate dopaminergic synaptic content and tone at the synapse? FASEB J 2004;18(6):637-647.
9. Sidhu A, Wersinger C, Vernier P. Alpha-synuclein regulation of the dopaminergic transporter: a possible role in the pathogenesis of Parkinson's disease. FEBS Lett 2004;565(1-3):1-5.
10. Sidhu A, Wersinger C, Moussa CE, Vernier P. The role of alpha-synuclein in both neuroprotection and neurodegeneration. Ann N Y Acad Sci 2004;1035:250-270.
11. Bisaglia M, Mammi S, Bubacco L. Kinetic and structural analysis of the early oxidation products of dopamine: analysis of the interactions with alpha-synuclein. J Biol Chem 2007;282(21):15597-15605.
12. Garner CD, Nachtman JP. Manganese catalyzed auto-oxidation of dopamine to 6-hydroxydopamine in vitro. Chemico-biological interactions 1989;69(4):345-351.
13. Stokes AH, Hastings TG, Vrana KE. Cytotoxic and genotoxic potential of dopamine. J Neurosci Res 1999;55(6):659-665.
14. Kienzl E, Puchinger L, Jellinger K, Linert W, Stachelberger H, Jameson RF. The role of transition metals in the pathogenesis of Parkinson's disease. J Neurolog Sci 1995;134 Suppl:69-78.
15. Ben-Shachar D, Riederer P, Youdim MB. Iron-melanin interaction and lipid peroxidation: implications for Parkinson's disease. J Neurochem 1991;57(5):1609-1614.
16. Norris EH, Giasson BI, Hodara R, Xu S, Trojanowski JQ, Ischiropoulos H, Lee VM. Reversible inhibition of alpha-synuclein fibrillization by dopaminochrome-mediated conformational alterations. J Biol Chem 2005;280(22):21212-21219.
17. Pham CL, Leong SL, Ali FE, Kenche VB, Hill AF, Gras SL, Barnham KJ, Cappai R. Dopamine and the dopamine oxidation product 5, 6-dihydroxylindole promote distinct on-pathway and off-pathway aggregation of alpha-synuclein in a pH-dependent manner. J Mol Biol 2009;387(3):771-785.
18. Leong SL, Pham CL, Galatis D, Fodero-Tavoletti MT, Perez K, Hill AF, Masters CL, Ali FE, Barnham KJ, Cappai R. Formation of dopamine-mediated alpha-synuclein-soluble oligomers requires methionine oxidation. Free Rad Biol Med 2009;46(10):1328-1337.
19. Rekas A, Knott RB, Sokolova A, Barnham KJ, Perez KA, Masters CL, Drew SC, Cappai R, Curtain CC, Pham CL. The structure of dopamine induced alpha-synuclein oligomers. Eur Biophys J 2010;39(10):1407-1419.
20. Bisaglia M, Greggio E, Maric D, Miller DW, Cookson MR, Bubacco L. Alpha-synuclein overexpression increases dopamine toxicity in BE2-M17 cells. BMC Neurosci 2010;11:41.
21. Xu J, Kao SY, Lee FJ, Song W, Jin LW, Yankner BA. Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med 2002;8(6):600-606.
22. Ito S, Nakaso K, Imamura K, Takeshima T, Nakashima K. Endogenous catecholamine enhances the dysfunction of unfolded protein response and alpha-synuclein oligomerization in PC12 cells overexpressing human alpha-synuclein. Neurosci Res 2010;66(1):124-130.
23. Mazzulli JR, Mishizen AJ, Giasson BI, Lynch DR, Thomas SA, Nakashima A, Nagatsu T, Ota A, Ischiropoulos H. Cytosolic catechols inhibit alpha-synuclein aggregation and facilitate the formation of intracellular soluble oligomeric intermediates. J Neurosci 2006;26(39):10068-10078.
24. Yamakawa K, Izumi Y, Takeuchi H, Yamamoto N, Kume T, Akaike A, Takahashi R, Shimohama S, Sawada H. Dopamine facilitates alpha-synuclein oligomerization in human neuroblastoma SH-SY5Y cells. Biochem Biophys Res Comm 2010;391(1):129-134.
25. Li J, Zhu M, Manning-Bog AB, Di Monte DA, Fink AL. Dopamine and L-dopa disaggregate amyloid fibrils: implications for Parkinson's and Alzheimer's disease. FASEB J 2004;18(9):962-964.
26. Surguchov A. Synucleins: are they two-edged swords? J Neurosci Res 2013;91(2):161-166.
27. Oaks AW, Sidhu A. Synuclein modulation of monoamine transporters. FEBS Lett 2011;585(7):1001-1006.
28. Lee FJ, Liu F, Pristupa ZB, Niznik HB. Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J 2001;15(6):916-926.
29. Brueggemann N, Odin P, Gruenewald A, Tadic V, Hagenah J, Seidel G, Lohmann K, Klein C, Djarmati A. Re: alpha-synuclein gene duplication is present in sporadic Parkinson disease. Neurology 2008;71(16):1294; author reply 1294.
30. Shin CW, Kim HJ, Park SS, Kim SY, Kim JY, Jeon BS. Two Parkinson's disease patients with alpha-synuclein gene duplication and rapid cognitive decline. Mov Disord 2010;25(7):957-959.
31. Keri S, Moustafa AA, Myers CE, Benedek G, Gluck MA. Alpha-synuclein gene duplication impairs reward learning. Proc Natl Acad Sci USA 2010;107(36):15992-15994.
32. Surmeier DJ. Alpha-synuclein at the synaptic gate. Neuron 2010;65(1):3-4.
33. Whitehead RE, Ferrer JV, Javitch JA, Justice JB. Reaction of oxidized dopamine with endogenous cysteine residues in the human dopamine transporter. J Neurochem 2001;76(4):1242-1251.
34. Conway KA, Rochet JC, Bieganski RM, Lansbury PT, Jr. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 2001;294(5545):1346-1349.
35. Li HT, Lin DH, Luo XY, Zhang F, Ji LN, Du HN, Song GQ, Hu J, Zhou JW, Hu HY. Inhibition of alpha-synuclein fibrillization by dopamine analogs via reaction with the amino groups of alpha-synuclein. Implication for dopaminergic neurodegeneration. FEBS J 2005;272(14):3661-3672.
36. Bisaglia M, Tosatto L, Munari F, Tessari I, de Laureto PP, Mammi S, Bubacco L. Dopamine quinones interact with alpha-synuclein to form unstructured adducts. Biochem Biophys Res Commun 2010;394(2):424-428.
37. Herrera FE, Chesi A, Paleologou KE, Schmid A, Munoz A, Vendruscolo M, Gustincich S, Lashuel HA, Carloni P. Inhibition of alpha-synuclein fibrillization by dopamine is mediated by interactions with five C-terminal residues and with E83 in the NAC region. PLoS One 2008;3(10):e3394.
38. Latawiec D, Herrera F, Bek A, Losasso V, Candotti M, Benetti F, Carlino E, Kranjc A, Lazzarino M, Gustincich S, Carloni P, Legname G. Modulation of alpha-synuclein aggregation by dopamine analogs. PLoS One 2010;5(2):e9234.
39. Cappai R, Leck SL, Tew DJ, Williamson NA, Smith DP, Galatis D, Sharples RA, Curtain CC, Ali FE, Cherny RA, Culvenor JG, Bottomley SP, Masters CL, Barnham KJ, Hill AF. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. FASEB J 2005;19(10):1377-1379.
40. Brookes E, Demeler B, Rocco M. Developments in the US-SOMO bead modeling suite: new features in the direct residue-to-bead method, improved grid routines, and influence of accessible surface area screening. Macromol Biosci 2010;10(7):746-753.
41. Brookes E, Demeler B, Rosano C, Rocco M. The implementation of SOMO (SOlution MOdeller) in the UltraScan analytical ultracentrifugation data analysis suite: enhanced capabilities allow the reliable hydrodynamic modeling of virtually any kind of biomacromolecule. Eur Biophys J 2010;39(3):423-435.
42. Cookson D, Kirby N, Knott R, Lee M, Schultz D. Strategies for data collection and calibration with a pinhole-geometry SAXS instrument on a synchrotron beamline. J Synchrotron Radiat 2006;13(Pt 6):440-444.
43. Konarev PV, Petoukhov MV, Volkov VV, Svergun DI. A TSAS 2.1, a program package for small-angle scattering data analysis. J Appl Crystallogr 2006;39:277-286.
44. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. PRIMUS-a Windows-PC based system for small-angle scattering data analysis. J Appl Crystallogr 2003;36:1277-1282.
45. Konarev PV, Petoukhov MV, Svergun DI. MASSHA-a graphic system for rigid body modelling of macromolecular complexes against solution scattering data. J Appl Crystallogr 2001;34:527-532.
46. Svergun DI. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 1999;76(6):2879-2886.
47. Svergun DI, Petoukhov MV, Koch MH. Determination of domain structure of proteins from X-ray solution scattering. Biophys J 2001;80(6):2946-2953.
48. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HDT, Konarev PV, Svergun DI. New developments in the ATSAS program package for small angle scattering data analysis. J Appl Crystallogr 2012;45:342-350.
49. Hammel M. Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS). Eur Biophys J 2012;41(10):789-799.
50. Bernado P, Svergun DI. Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering. Mol Biosyst 2012;8(1):151-167.
51. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HDT, Konarev PV, Svergun DI. New developments in the ATSAS program package for small-angle scattering data analysis. J Appl Crystallogr 2012;45:342-350.
52. Lim WK, Rosgen J, Englander SW. Urea, but not guanidinium, destabilizes proteins by forming hydrogen bonds to the peptide group. Proc Natl Acad Sci USA 2009;106(8):2595-2600.
53. England JL, Haran G. Role of solvation effects in protein denaturation: from thermodynamics to single molecules and back. Annu Rev Phys Chem 2011;62:257-277.
54. Tanford C, Aune KC. Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride. 3. Dependence on temperature. Biochemistry 1970;9(2):206-211.
55. Salahuddin A, Tanford C. Thermodynamics of the denaturation of ribonuclease by guanidine hydrochloride. Biochemistry 1970;9(6):1342-1347.
56. Nozaki Y, Tanford C. The solubility of amino acids, diglycine, and triglycine in aqueous guanidine hydrochloride solutions. J Biol Chem 1970;245(7):1648-1652.
57. Fish WW, Reynolds JA, Tanford C. Gel chromatography of proteins in denaturing solvents. Comparison between sodium dodecyl sulfate and guanidine hydrochloride as denaturants. J Biol Chem 1970;245(19):5166-5168.
58. Eliezer D, Kutluay E, Bussell R, Jr, Browne G. Conformational properties of a-synuclein in its free and lipid-associated states. J Mol Biol 2001;307:1061-1073.
59. Croke RL, Sallum CO, Watson E, Watt ED, Alexandrescu AT. Hydrogen exchange of monomeric alpha-synuclein shows unfolded structure persists at physiological temperature and is independent of molecular crowding in Escherichia coli. Prot Sci 2008;17(8):1434-1445.
60. Grupi A, Haas E. Segmental conformational disorder and dynamics in the intrinsically disordered protein alpha-synuclein and its chain length dependence. J Mol Biol 2011;405(5):1267-1283.
61. Tashiro M, Kojima M, Kihara H, Kasai K, Kamiyoshihara T, Ueda K, Shimotakahara S. Characterization of fibrillation process of alpha-synuclein at the initial stage. Biochem Biophys Res Commun 2008;369(3):910-914.
62. Jha AK, Colubri A, Freed KF, Sosnick TR. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc Natl Acad Sci USA 2005;102(37):13099-13104.
63. Jha AK, Colubri A, Zaman MH, Koide S, Sosnick TR, Freed KF. Helix, sheet, and polyproline II frequencies and strong nearest neighbor effects in a restricted coil library. Biochemistry 2005;44(28):9691-9702.
64. Bernado P, Blackledge M. A self-consistent description of the conformational behavior of chemically denatured proteins from NMR and small angle scattering. Biophys J 2009;97(10):2839-2845.
65. Uversky VN, Fink AL. Protein misfolding, aggregation, and conformational diseases. Part A, Protein aggregation and conformational diseases. New York, NY: Springer; 2006. xviii, 419 pp.
66. Uversky VN, Fink AL. Protein misfolding, aggregation, and conformational diseases. Part B, molecular mechanisms of conformational diseases. New York; London: Springer; 2007. xxv, 537 pp.
67. Lovell SC, Davis IW, Arendall WB, III, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003;50(3):437-450.
68. Uversky VN, Yamin G, Souillac PO, Goers J, Glaser CB, Fink AL. Methionine oxidation inhibits fibrillation of human a-synuclein in vitro. FEBS Lett 2002;517(1-3):239-244.
69. Brookes E, Cao W, Demeler B. A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur Biophys J 2010;39(3):405-414.
70. Bernado P, Bertoncini CW, Griesinger C, Zweckstetter M, Blackledge M. Defining long-range order and local disorder in native alpha-synuclein using residual dipolar couplings. J Am Chem Soc 2005;127(51):17968-17969.
71. Bertoncini CW, Jung YS, Fernandez CO, Hoyer W, Griesinger C, Jovin TM, Zweckstetter M. Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc Natl Acad Sci USA 2005;102(5):1430-1435.
72. Bertoncini CW, Fernandez CO, Griesinger C, Jovin TM, Zweckstetter M. Familial mutants of alpha-synuclein with increased neurotoxicity have a destabilized conformation. J Biol Chem 2005;280(35):30649-30652.
73. Waxman EA, Giasson BI. Molecular mechanisms of alpha-synuclein neurodegeneration. Biochim Biophys Acta 2009;1792(7):616-624.
74. Sandal M, Valle F, Tessari I, Mammi S, Bergantino E, Musiani F, Brucale M, Bubacco L, Samori B. Conformational equilibria in monomeric alpha-synuclein at the single-molecule level. PLoS Biol 2008;6(1):e6.
75. Gallas JM, Littrell KC, Seifert S, Zajac GW, Thiyagarajan P. Solution structure of copper ion-induced molecular aggregates of tyrosine melanin. Biophys J 1999;77(2):1135-1142.
76. Baumann MH, Ayestas MA, Jr, Partilla JS, Sink JR, Shulgin AT, Daley PF, Brandt SD, Rothman RB, Ruoho AE, Cozzi NV. The designer methcathinone analogs, mephedrone and methylone, are substrates for monoamine transporters in brain tissue. Neuropsychopharmacology 2012;37(5):1192-1203.
77. Villemagne VL, Perez KA, Pike KE, Kok WM, Rowe CC, White AR, Bourgeat P, Salvado O, Bedo J, Hutton CA, Faux NG, Masters CL, Barnham KJ. Blood-borne amyloid-beta dimer correlates with clinical markers of Alzheimer's disease. J Neurosci 2010;30(18):6315-6322.
78. Haeffner F, Barnham KJ, Bush AI, Brinck T. Generation of soluble oligomeric beta-amyloid species via copper catalyzed oxidation with implications for Alzheimer's disease: a DFT study. J Mol Model 2010;16(6):1103-1108.