The role of the C-terminus of human α-synuclein: Intra-disulfide bonds between the C-terminus and other regions stabilize non-fibrillar monomeric isomers

FEBS Letters

Volumn 585, Issue 3, 2011, Pages 561-566

  Hong, Dong Pyo ^a   Xiong, Wei ^a   Chang, Jui Yoa ^a   Jiang, Chuantao ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Synuclein; Aggregation; C Terminus; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; CYSTEINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; DISULFIDE BOND; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROPHOBICITY; ISOMER; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; ULTRAVIOLET RADIATION;

ALPHA-SYNUCLEIN; CIRCULAR DICHROISM; CYSTEINE; CYSTINE; FLUORESCENT DYES; HUMANS; ISOMERISM; KINETICS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; OXIDATION-REDUCTION; PARKINSON DISEASE; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE; THIAZOLES;

EID: 79551483725     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.01.009     Document Type: Article

References (52)

1. A.L. Fink Protein aggregation: folding aggregates, inclusion bodies and amyloid Fold. Des. 3 1998 R9 23
2. C.M. Dobson Protein misfolding, evolution and disease Trends Biochem. Sci. 24 1999 329 332
3. J.N. Buxbaum The systemic amyloidoses Curr. Opin. Rheumatol. 16 2004 67 75
4. D. Hamada, and C.M. Dobson A kinetic study of beta-lactoglobulin amyloid fibril formation promoted by urea Protein Sci. 11 2002 2417 2426
5. M. Fandrich, M.A. Fletcher, and C.M. Dobson Amyloid fibrils from muscle myoglobin Nature 410 2001 165 166
6. F. Chiti, P. Webster, N. Taddei, A. Clark, M. Stefani, G. Ramponi, and C.M. Dobson Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc. Natl. Acad. Sci. USA 96 1999 3590 3594
7. M.G. Spillantini, R.A. Crowther, R. Jakes, M. Hasegawa, and M. Goedert 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
8. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41 2000 415 427
9. V.N. Uversky A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders J. Biomol. Struct. Dyn. 21 2003 211 234
10. V.N. Uversky Alpha-synuclein misfolding and neurodegenerative diseases Curr. Protein Pept. Sci. 9 2008 507 540
11. M.H. Polymeropoulos, C. Lavedan, E. Leroy, S.E. Ide, A. Dehejia, A. Dutra, B. Pike, H. Root, J. Rubenstein, and R. Boyer Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047
12. R. Kruger, W. Kuhn, T. Muller, D. Woitalla, M. Graeber, S. Kosel, H. Przuntek, J.T. Epplen, L. Schols, and O. Riess Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18 1998 106 108
13. D.W. Miller, S.M. Hague, J. Clarimon, M. Baptista, K. Gwinn-Hardy, M.R. Cookson, and A.B. Singleton Alpha-synuclein in blood and brain from familial Parkinson disease with SNCA locus triplication Neurology 62 2004 1835 1838
14. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, and R. Nussbaum Alpha-synuclein locus triplication causes Parkinson's disease Science 302 2003 841
15. J. Fuchs, C. Nilsson, J. Kachergus, M. Munz, E.M. Larsson, B. Schule, J.W. Langston, F.A. Middleton, O.A. Ross, and M. Hulihan Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication Neurology 68 2007 916 922
16. M.C. Chartier-Harlin, J. Kachergus, C. Roumier, V. Mouroux, X. Douay, S. Lincoln, C. Levecque, L. Larvor, J. Andrieux, and M. Hulihan Alpha-synuclein locus duplication as a cause of familial Parkinson's disease Lancet 364 2004 1167 1169
17. E. Masliah, E. Rockenstein, I. Veinbergs, M. Mallory, M. Hashimoto, A. Takeda, Y. Sagara, A. Sisk, and L. Mucke Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders Science 287 2000 1265 1269
18. P.H. van der, K.H. Wiederhold, A. Probst, S. Barbieri, C. Mistl, S. Danner, S. Kauffmann, K. Hofele, W.P. Spooren, and M.A. Ruegg Neuropathology in mice expressing human alpha-synuclein J. Neurosci. 20 2000 6021 6029
19. M.B. Feany, and W.W. Bender A Drosophila model of Parkinson's disease Nature 404 2000 394 398
20. J.Q. Trojanowski, and V.M. Lee Parkinson's disease and related alpha-synucleinopathies are brain amyloidoses Ann. N.Y. Acad. Sci. 991 2003 107 110
21. A. Iwai, M. Yoshimoto, E. Masliah, and T. Saitoh Non-A beta component of Alzheimer's disease amyloid (NAC) is amyloidogenic Biochemistry 34 1995 10139 10145
22. Z. Qin, D. Hu, S. Han, D.P. Hong, and A.L. Fink Role of different regions of alpha-synuclein in the assembly of fibrils Biochemistry 46 2007 13322 13330
23. M. Zhu, and A.L. Fink Lipid binding inhibits alpha-synuclein fibril formation J. Biol. Chem. 278 2003 16873 16877
24. M. Zhu, J. Li, and A.L. Fink The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation J. Biol. Chem. 278 2003 40186 40197
25. W.S. Davidson, A. Jonas, D.F. Clayton, and J.M. George Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes J. Biol. Chem. 273 1998 9443 9449
26. C.W. Bertoncini, Y.S. Jung, C.O. Fernandez, W. Hoyer, C. Griesinger, T.M. Jovin, and M. Zweckstetter Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein Proc. Natl. Acad. Sci. USA 102 2005 1430 1435
27. C. Jiang, and J.Y. Chang Isomers of human alpha-synuclein stabilized by disulfide bonds exhibit distinct structural and aggregative properties Biochemistry 46 2007 602 609
28. V.N. Uversky, G. Yamin, P.O. Souillac, J. Goers, C.B. Glaser, and A.L. Fink Methionine oxidation inhibits fibrillation of human alpha-synuclein in vitro FEBS Lett. 517 2002 239 244
29. H. Naiki, K. Higuchi, M. Hosokawa, and T. Takeda Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1 Anal. Biochem. 177 1989 244 249
30. H. Naiki, K. Higuchi, K. Matsushima, A. Shimada, W.H. Chen, M. Hosokawa, and T. Takeda Fluorometric examination of tissue amyloid fibrils in murine senile amyloidosis: use of the fluorescent indicator, thioflavine T Lab. Invest. 62 1990 768 773
31. J.Y. Chang, B.Y. Lu, and L. Li Conformational impurity of disulfide proteins: detection, quantification, and properties Anal. Biochem. 342 2005 78 85
32. J.Y. Chang Conformational isomers of denatured and unfolded proteins: methods of production and applications Protein J. 28 2009 44 56
33. M. Friedman, L.H. Krull, and J.F. Cavins The chromatographic determination of cystine and cysteine residues in proteins as s-beta-(4-pyridylethyl)cysteine J. Biol. Chem. 245 1970 3868 3871
34. A.K. Ahmed, S.W. Schaffer, and D.B. Wetlaufer Nonenzymeic reactivation of reduced bovine pancreatic ribonuclease by air oxidation and by glutathione oxidoreduction buffer J. Biol. Chem. 250 1975 8477 8482
35. K.A. Conway, J.C. Rochet, R.M. Bieganski, and P.T. Lansbury Jr. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct Science 294 2001 1346 1349
36. D.P. Hong, A.L. Fink, and V.N. Uversky Smoking and Parkinson's disease: does nicotine affect alpha-synuclein fibrillation? Biochim. Biophys. Acta 1794 2009 282 290
37. D.P. Hong, A.L. Fink, and V.N. Uversky Structural characteristics of alpha-synuclein oligomers stabilized by the flavonoid baicalein J. Mol. Biol. 383 2008 214 223
38. J. Li, M. Zhu, S. Rajamani, V.N. Uversky, and A.L. Fink Rifampicin inhibits alpha-synuclein fibrillation and disaggregates fibrils Chem. Biol. 11 2004 1513 1521
39. J. Li, M. Zhu, A.B. Manning-Bog, D.A. Di Monte, and A.L. Fink Dopamine and L-dopa disaggregate amyloid fibrils: implications for Parkinson's and Alzheimer's disease FASEB J. 18 2004 962 964
40. M. Zhu, S. Rajamani, J. Kaylor, S. Han, F. Zhou, and A.L. Fink The flavonoid baicalein inhibits fibrillation of alpha-synuclein and disaggregates existing fibrils J. Biol. Chem. 279 2004 26846 26857
41. M. Zhu, S. Han, F. Zhou, S.A. Carter, and A.L. Fink Annular oligomeric amyloid intermediates observed by in situ atomic force microscopy J. Biol. Chem. 279 2004 24452 24459
42. Z. Qin, D. Hu, S. Han, S.H. Reaney, D.A. Di Monte, and A.L. Fink Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation J. Biol. Chem. 282 2007 5862 5870
43. M.M. Dedmon, J. Christodoulou, M.R. Wilson, and C.M. Dobson Heat shock protein 70 inhibits alpha-synuclein fibril formation via preferential binding to prefibrillar species J. Biol. Chem. 280 2005 14733 14740
44. V.N. Uversky, J. Li, and A.L. Fink Evidence for a partially folded intermediate in alpha-synuclein fibril formation J. Biol. Chem. 276 2001 10737 10744
45. M.M. Dedmon, K. Lindorff-Larsen, J. Christodoulou, M. Vendruscolo, and C.M. Dobson Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations J. Am. Chem. Soc. 127 2005 476 477
46. W. Hoyer, D. Cherny, V. Subramaniam, and T.M. Jovin Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro Biochemistry 43 2004 16233 16242
47. R. Lowe, D.L. Pountney, P.H. Jensen, W.P. Gai, and N.H. Voelcker Calcium(II) selectively induces alpha-synuclein annular oligomers via interaction with the C-terminal domain Protein Sci. 13 2004 3245 3252
48. I.V. Murray, B.I. Giasson, S.M. Quinn, V. Koppaka, P.H. Axelsen, H. Ischiropoulos, J.Q. Trojanowski, and V.M. Lee Role of alpha-synuclein carboxy-terminus on fibril formation in vitro Biochemistry 42 2003 8530 8540
49. W. Zhou, C. Long, S.H. Reaney, D.A. Di Monte, A.L. Fink, and V.N. Uversky Methionine oxidation stabilizes non-toxic oligomers of alpha-synuclein through strengthening the auto-inhibitory intra-molecular long-range interactions Biochim. Biophys. Acta 1802 2010 322 330
50. C.J. Oldfield, Y. Cheng, M.S. Cortese, C.J. Brown, V.N. Uversky, and A.K. Dunker Comparing and combining predictors of mostly disordered proteins Biochemistry 44 2005 1989 2000
51. L.M. Iakoucheva, C.J. Brown, J.D. Lawson, Z. Obradovic, and A.K. Dunker Intrinsic disorder in cell-signaling and cancer-associated proteins J. Mol. Biol. 323 2002 573 584
52. C. Jiang, W. Xiong, B.Y. Lu, M.A. Gonda, and J.Y. Chang Synthesis and immune response of non-native isomers of vascular endothelial growth factor Biochemistry 49 2010 6550 6556