SDS-Induced Fibrillation of α-Synuclein: An Alternative Fibrillation Pathway

Journal of Molecular Biology

Volumn 401, Issue 1, 2010, Pages 115-133

  Giehm, Lise ^a,b   Oliveira, Cristiano Luis Pinto ^a   Christiansen, Gunna ^a   Pedersen, Jan Skov ^a   Otzen, Daniel E ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AALBORG UNIVERSITY   (Denmark)

Author keywords

Fibrillation; SAXS; SDS; Surfactant; synuclein

Indexed keywords

ALPHA SYNUCLEIN; DODECYL SULFATE SODIUM; THIOFLAVINE;

ALPHA HELIX; ARTICLE; HUMAN; MICELLE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FIBRILLATION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

EID: 77954758860     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.05.060     Document Type: Article

References (66)

1. Moore D.J., West A.B., Dawson V.L., Dawson T.M. Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 2005, 28:57-87.
2. Baba M., Nakajo S., Tu P.H., Tomita T., Nakaya K., Lee V.M., et al. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 1998, 152:879-884.
3. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997, 388:839-840.
4. Weinreb P.H., Zhen W., Poon A.W., Conway K.A., Lansbury P.T. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 1996, 35:13709-13715.
5. Crowther R.A., Jakes R., Spillantini M.G., Goedert M. Synthetic filaments assembled from C-terminally truncated alpha-synuclein. FEBS Lett. 1998, 436:309-312.
6. Conway K.A., Harper J.D., Lansbury P.T. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 2000, 39:2552-2563.
7. Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 1998, 4:1318-1320.
8. Forno L.S., DeLanney L.E., Irwin I., Langston J.W. Similarities and differences between MPTP-induced parkinsonism and Parkinson's disease. Neuropathologic considerations. Adv. Neurol. 1993, 60:600-608.
9. Maroteaux L., Campanelli J.T., Scheller R.H. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 1988, 8:2804-2815.
10. Maroteaux L., Scheller R.H. The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res. Mol. Brain Res. 1991, 11:335-343.
11. Jakes R., Spillantini M.G., Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett. 1994, 345:27-32.
12. 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 1995, 14:467-475.
13. George J.M., Jin H., Woods W.S., Clayton D.F. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 1995, 15:361-372.
14. Murphy D.D., Rueter S.M., Trojanowski J.Q., Lee V.M. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 2000, 20:3214-3220.
15. Chandra S., Gallardo G., Fernandez-Chacon R., Schluter O.M., Sudhof T.C. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 2005, 123:383-396.
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 2000, 25:239-252.
17. Cooper A.A., Gitler A.D., Cashikar A., Haynes C.M., Hill K.J., Bhullar B., et al. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006, 313:324-328.
18. Jensen P.H., Nielsen M.S., Jakes R., Dotti C.G., Goedert M. Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J. Biol. Chem. 1998, 273:26292-26294.
19. Sharon R., Goldberg M.S., Bar-Josef I., Betensky R.A., Shen J., Selkoe D.J. Alpha-synuclein occurs in lipid-rich high molecular weight complexes, binds fatty acids, and shows homology to the fatty acid-binding proteins. Proc. Natl Acad. Sci. USA 2001, 98:9110-9115.
20. 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 2008, 105:19666-19671.
21. Kjaer L., Giehm L., Heimburg T., Otzen D. The influence of vesicle size and composition on alpha-synuclein structure and stability. Biophys. J. 2009, 96:2857-2870.
22. Davidson W.S., Jonas A., Clayton D.F., George J.M. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 1998, 273:9443-9449.
23. Zhu M., Fink A.L. Lipid binding inhibits alpha-synuclein fibril formation. J. Biol. Chem. 2003, 278:16873-16877.
24. Chandra S., Chen X., Rizo J., Jahn R., Sudhof T.C. A broken alpha-helix in folded alpha-synuclein. J. Biol. Chem. 2003, 278:15313-15318.
25. Lee H.J., Choi C., Lee S.J. Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J. Biol. Chem. 2002, 277:671-678.
26. Eliezer D., Kutluay E., Bussell R., Browne G. Conformational properties of alpha-synuclein in its free and lipid-associated states. J. Mol. Biol. 2001, 307:1061-1073.
27. Zhu M., Li J., Fink A.L. The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. J. Biol. Chem. 2003, 278:40186-40197.
28. Rivers R.C., Kumita J.R., Tartaglia G.G., Dedmon M.M., Pawar A., Vendruscolo M., et al. Molecular determinants of the aggregation behavior of alpha- and beta-synuclein. Protein Sci. 2008, 17:887-898.
29. Ferreon A.C., Deniz A.A. Alpha-synuclein multistate folding thermodynamics: implications for protein misfolding and aggregation. Biochemistry 2007, 46:4499-4509.
30. Ferreon A.C., Gambin Y., Lemke E.A., Deniz A.A. Interplay of alpha-synuclein binding and conformational switching probed by single-molecule fluorescence. Proc. Natl Acad. Sci. USA 2009, 106:5645-5650.
31. Veldhuis G., Segers-Nolten I., Ferlemann E., Subramaniam V. Single-molecule FRET reveals structural heterogeneity of SDS-bound alpha-synuclein. ChemBioChem 2009, 10:436-439.
32. Veldhuis G., Segers-Nolten I.M.J., Ferlemann E., Subramaniam V. Single-molecule FRET reveals structural heterogeneity of SDS-bound α -synuclein. ChemBioChem 2009, 10:436-439.
33. El-Agnaf O.M., Jakes R., Curran M.D., Wallace A. Effects of the mutations Ala30 to Pro and Ala53 to Thr on the physical and morphological properties of alpha-synuclein protein implicated in Parkinson's disease. FEBS Lett. 1998, 440:67-70.
34. Serpell L.C., Berriman J., Jakes R., Goedert M., Crowther R.A. Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc. Natl Acad. Sci. USA 2000, 97:4897-4902.
35. Antony T., Hoyer W., Cherny D., Heim G., Jovin T.M., Subramaniam V. Cellular polyamines promote the aggregation of alpha-synuclein. J. Biol. Chem. 2003, 278:3235-3240.
36. Cohlberg J.A., Li J., Uversky V.N., Fink A.L. Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro. Biochemistry 2002, 41:1502-1511.
37. Necula M., Chirita C.N., Kuret J. Rapid anionic micelle-mediated alpha-synuclein fibrillization in vitro. J. Biol. Chem. 2003, 278:46674-46680.
38. Ahmad M.F., Ramakrishna T., Raman B., Rao Ch M. Fibrillogenic and non-fibrillogenic ensembles of SDS-bound human alpha-synuclein. J. Mol. Biol. 2006, 364:1061-1072.
39. Sehgal P., Mogensen J.E., Otzen D.E. Using micellar mole fractions to assess membrane protein stability in mixed micelles. Biochim. Biophys. Acta 2005, 1716:59-68.
40. Andrade M.A., Chacon P., Merelo J.J., Moran F. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 1993, 6:383-390.
41. Ananthapadmanabhan K.P., Goddard E.D., Turro N.J., Kuo P.L. Fluorescence probes for critical micelle concentration. Langmuir 1985, 1:352-355.
42. Kalyanasundaram K., Thomas J.K. Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems. J. Am. Chem. Soc. 1976, 99:2039-2044.
43. LeVine H. Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 1999, 309:274-284.
44. Merelo J.J., Andrade M.A., Prieto A., Moran F. Proteinotopic feature maps. Neurocomputing 1994, 6:443-454.
45. Nielsen A.D., Arleth L., Westh P. Analysis of protein-surfactant interactions-a titration calorimetric and fluorescence spectroscopic investigation of interactions between Humicola insolens cutinase and an anionic surfactant. Biochim. Biophys. Acta 2005, 1752:124-132.
46. Andersen K.K., Westh P., Otzen D.E. Global study of myoglobin-surfactant interactions. Langmuir 2008, 24:399-407.
47. Andersen K.K., Oliveira C.L., Larsen K.L., Poulsen F.M., Callisen T.H., Westh P., et al. The role of decorated SDS micelles in sub-CMC protein denaturation and association. J. Mol. Biol. 2009, 391:207-226.
48. Otzen D.E., Sehgal P., Westh P. α -Lactalbumin is unfolded by all classes of detergents but with different mechanisms. J. Colloid Interface Sci. 2009, 329:273-283.
49. Nielsen M.M., Andersen K.K., Westh P., Otzen D.E. Unfolding of beta-sheet proteins in SDS. Biophys. J. 2007, 92:3674-3685.
50. Turro N.J., Lei X.G., Ananthapadmanabhan K.P., Aronson M. Spectroscopic probe analysis of protein-surfactant interactions: the BSA/SDS system. Langmuir 1995, 11:2525-2533.
51. Tanford C. The Hydrophobic Effect. Formation of Micelles and Biological Membranes 1980, Wiley and Sons, New York, NY. 2nd edit.
52. Sehgal P., Mogensen J.E., Otzen D.E. Using micellar mole fractions to assess membrane protein stability in mixed micelles. Biochim. Biophys. Acta 2005, 1716:59-68.
53. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., Lansbury 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 2000, 97:571-576.
54. Otzen D.E. Amyloid formation in surfactants and alcohols: membrane mimetics or structural switchers?. Curr. Protein Pept. Sci. 2010, 11:355-371.
55. Giasson B.I., Murray I.V.J., Trojanowski J.Q., Lee V.M.Y. A hydrophobic stretch of 12 amino acid residues in the middle of α -synuclein is essential for filament assembly. J. Biol. Chem. 2001, 276:2380-2386.
56. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., Lansbury P.T. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 2002, 322:1089-1102.
57. Huang C., Ren G., Zhou H., Wang C.C. A new method for purification of recombinant human alpha-synuclein in Escherichia coli. Protein Expression Purif. 2005, 42:173-177.
58. Nielsen A.D., Arleth L., Westh P. Interactions of Humicola insolens cutinase with an anionic surfactant studied by small-angle neutron scattering and isothermal titration calorimetry. Langmuir 2005, 21:4299-4307.
59. Pedersen J.S. A flux- and background-optimized version of the NanoSTAR small-angle X-ray scattering camera for solution scattering. J. Appl. Crystallogr. 2004, 37:369-380.
60. Pedersen J.S., Hansen S., Bauer R. The aggregation behavior of zinc-free insulin studied by small-angle neutron scattering. Eur. Biophys. J. 1994, 22:379-389.
61. Oliveira C.L., Behrens M.A., Pedersen J.S., Erlacher K., Otzen D., Pedersen J.S. A SAXS study of glucagon fibrillation. J. Mol. Biol. 2009, 387:147-161.
62. Glatter O. Computation of distance distribution functions and scattering functions of models for small-angle scattering experiments. Acta Phys. Austriaca 1980, 52:243-256.
63. Buchard W., Kajiwara K. The statistics of stiff chain molecules: I. The particle scattering factor. Proc. R. Soc. London Ser. A 1970, 316:185.
64. Pedersen J.S. Analysis of small-angle scattering data from colloids and polymer solutions: modeling and least-squares fitting. Adv. Colloid Interface Sci. 1997, 70:171-210.
65. Vass S., Plestil J., Laggner P., Gilanyi T., Borbely S., Kriechbaum M., et al. Models of micellar structure tested by SANS and SAXS (from a Kratky camera) in cesium dodecyl sulfate solution. J. Phys. Chem. B 2003, 107:12752-12761.
66. Debye P. Molecular-weight determination by light scattering. J. Phys. Chem. 1947, 51:18-32.