Diverse metastable structures formed by small oligomers of α-synuclein probed by force spectroscopy

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Neupane, Krishna ^a   Solanki, Allison ^a   Sosova, Iveta ^b   Belov, Miro ^b   Woodside, Michael T ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; DIMER; MONOMER; OLIGOMER; TETRAMER; PROTEIN AGGREGATE; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME KINETICS; MATHEMATICAL COMPUTING; MOLECULAR PROBE; MOLECULAR STABILITY; NONHUMAN; OLIGOMERIZATION; OPTICAL TWEEZERS; PARKINSON DISEASE; PARTICLE SIZE; PROTEIN AGGREGATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; KINETICS; METABOLISM; PROCEDURES; PROTEIN ENGINEERING; PROTEIN QUATERNARY STRUCTURE; PROTEIN UNFOLDING; THERMODYNAMICS;

ALPHA-SYNUCLEIN; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; KINETICS; OPTICAL TWEEZERS; PROTEIN AGGREGATES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN UNFOLDING; RECOMBINANT PROTEINS; SPECTRUM ANALYSIS; THERMODYNAMICS;

EID: 84898972476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086495     Document Type: Article

References (72)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366. (Pubitemid 44118036)
2. Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nature Med 10: s10-s17. (Pubitemid 38901862)
3. Eichner T, Radford SE (2011) A diversity of assembly mechanisms of a generic amyloid fold. Mol Cell 43: 8-18.
4. Lashuel HA, Lansbury PT (2006) Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q Rev Biophys 39: 167-201. (Pubitemid 44711851)
5. Cremades N, Cohen Samuel IA, Deas E, Abramov Andrey Y, Chen Allen Y, et al. (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell 149: 1048-1059.
6. Borgia A, Williams PM, Clarke J (2008) Single-molecule studies of protein folding. Annu Rev Biochem 77: 101-125.
7. Stigler J, Ziegler F, Gieseke A, Gebhardt JCM, Rief M (2011) The complex folding network of single calmodulin molecules. Science 334: 512.
8. Hoffmann A, Woodside MT (2011) Signal-pair correlation analysis of single-molecule trajectories. Angew Chem Int Ed 50: 12643-12646.
9. Yu H, Liu X, Neupane K, Gupta AN, Brigley AM, et al. (2012) Direct observation of multiple misfolding pathways in a single prion protein molecule. Proc Natl Acad Sci USA 109: 5283-5288.
10. Yu H, Dee DR, Woodside MT (2013) Single-molecule approaches to prion protein misfolding. Prion 7: 140-146.
11. Hoffmann A, Neupane K, Woodside MT (2013) Single-molecule assays for investigating protein misfolding and aggregation. Phys Chem Chem Phys 15: 7934-7948.
12. Orte A, Birkett NR, Clarke RW, Devlin GL, Dobson CM, et al. (2008) Direct characterization of amyloidogenic oligomers by single-molecule fluorescence. Proc Natl Acad Sci USA 105: 14424-14429.
13. Takahashi Y, Okamoto Y, Popiel HA, Fujikake N, Toda T, et al. (2007) Detection of polyglutamine protein oligomers in cells by fluorescence correlation spectroscopy. J Biol Chem 282: 24039-24048. (Pubitemid 47328008)
14. Nath S, Meuvis J, Hendrix J, Carl SA, Engelborghs Y (2010) Early aggregation steps in α-synuclein as measured by FCS and FRET: evidence for a contagious conformational change. Biophys J 98: 1302-1311.
15. Hillger F, Nettels D, Dorsch S, Schuler B (2007) Detection and analysis of protein aggregation with confocal single molecule fluorescence spectroscopy. J Fluoresc 17: 759-765. (Pubitemid 350075694)
16. Narayan P, Orte A, Clarke RW, Bolognesi B, Hook S, et al. (2012) The extracellular chaperone clusterin sequesters oligomeric forms of the amyloid-β1-40 peptide. Nat Struct Mol Biol 19: 79-83.
17. Bechtluft P, van Leeuwen RGH, Tyreman M, Tomkiewicz D, Nouwen N, et al. (2007) Direct observation of chaperone-induced changes in a protein folding pathway. Science 318: 1458-1461. (Pubitemid 350208958)
18. Greenleaf WJ, Woodside MT, Block SM (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu Rev Biophys Biomol Struct 36: 171-190. (Pubitemid 46998115)
19. Uversky VN (2008) α-Synuclein misfolding and neurodegenerative diseases. Curr Protein Pept Sci 9: 507-540.
20. Weinreb PH, Zhen W, Poon AW, Conway KA, Lansbury PT (1996) NACP, a protein implicated in alzheimer's disease and learning, is natively unfolded. Biochemistry 35: 13709-13715. (Pubitemid 26363912)
21. Davidson WS, Jonas A, Clayton DF, George JM (1998) Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 273: 9443-9449. (Pubitemid 28183026)
22. Bartels T, Choi JG, Selkoe DJ (2011) α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477: 107-110.
23. Wang W, Perovic I, Chittuluru J, Kaganovich A, Nguyen LTT, et al. (2011) A soluble α-synuclein construct forms a dynamic tetramer. Proc Natl Acad Sci USA 108: 17797-17802.
24. Fauvet B, Mbefo MK, Fares MB, Desobry C, Michael S, et al. (2012) Alpha-synuclein in central nervous system and from erythrocytes, mammalian cells, and escherichia coli exists predominantly as disordered monomer. J Biol Chem 287: 15345-15364.
25. Sandal M, Valle F, Tessari I, Mammi S, Bergantino E, et al. (2008) Conformational equilibria in monomeric α-synuclein at the single-molecule level. PLoS Biol 6: 99.
26. Brucale M, Missimo S, Maio SD, Rampioni A, Tessari I, et al. (2009) Pathogenic mutations shift the equilibria of alpha-synuclein single molecules towards structured conformers. ChemBioChem 10: 176-183.
27. Hervas R, Oroz J, Galera-Prat A, Goni O, Valbuena A, et al. (2012) Common features at the start of the neurodegeneration cascade. PLoS Biol 10: e1001335.
28. Ferreon AC, Gambin Y, Lemke EA, Deniz AA (2009) Interplay of α-synuclein binding and conformational switching probed by single-molecule fluorescence. Proc Natl Acad Sci USA 106: 5645-5650.
29. Ferreon ACM, Moran CR, Ferreon JC, Deniz AA (2010) Alteration of the α-synuclein folding landscape by a mutation related to parkinson's disease. Angew Chem Int Ed 49: 3469-3472.
30. Trexler AJ, Rhoades E (2010) Single molecule characterization of α-synuclein in aggregation-prone states. Biophys J 99: 3048-3055.
31. Ahmad B, Chen Y, Lapidus LJ (2012) Aggregation of α-synuclein is kinetically controlled by intramolecular diffusion. Proc Natl Acad Sci USA 109: 2336-2341.
32. Yu J, Malkova S, Lyubchenko YL (2008) α-synuclein misfolding: single molecule AFM force spectroscopy study. J Mol Biol 384: 992-1001.
33. Krasnoslobodtsev AV, Peng J, Asiago JM, Hindupur J, Rochet JC, et al. (2012) Effect of spermidine on misfolding and interactions of alpha-synuclein. PLoS One 7: e38099.
34. Krasnoslobodtsev AV, Volkov IL, Asiago JM, Hindupur J, Rochet J-C, et al. (2013) α-Synuclein misfolding assessed with single molecule AFM force spectroscopy: effect of pathogenic mutations. Biochemistry 52: 7377-7386.
35. Bader R, Bamford R, Zurdo J, Luisi BF, Dobson CM (2006) Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation. J Mol Biol 356: 189-208. (Pubitemid 43069737)
36. Kellermayer MSZ, Bustamante C, Granzier HL (2003) Mechanics and structure of titin oligomers explored with atomic force microscopy. BBA-Bioenergetics 1604: 105-114. (Pubitemid 36588695)
37. Borgia MB, Borgia A, Best RB, Steward A, Nettels D, et al. (2011) Single-molecule fluorescence reveals sequence-specific misfolding in multidomain proteins. Nature 474: 662-665.
38. Speretta E, Jahn TR, Tartaglia GG, Favrin G, Barros TP, et al. (2012) Expression in drosophila of tandem amyloid beta peptides provides insights into links between aggregation and neurotoxicity. J Biol Chem 287: 20748-20754.
39. Laganowsky A, Liu C, Sawaya MR, Whitelegge JP, Park J, et al. (2012) Atomic view of a toxic amyloid small oligomer. Science 335: 1228-1231.
40. Simoneau S, Rezaei H, Sales N, Kaiser-Schulz G, Lefebvre-Roque M, et al. (2007) In vitro and in vivo neurotoxicity of prion protein oligomers. PLoS Pathogens 3: 1175-1186. (Pubitemid 47359094)
41. Fink AL (2006) The aggregation and fibrillation of alpha-synuclein. Acc Chem Res 39: 628-634.
42. Cecconi C, Shank E, Dahlquist F, Marqusee S, Bustamante C (2008) Protein-DNA chimeras for single molecule mechanical folding studies with the optical tweezers. Eur Biophys J 37: 729-738.
43. Neupane K, Yu H, Foster DA, Wang F, Woodside MT (2011) Single-molecule force spectroscopy of the add adenine riboswitch relates folding to regulatory mechanism. Nucleic Acids Res 39: 7677-7687.
44. Neuman KC, Block SM (2004) Optical trapping. Rev Sci Instrum 75: 2787-2809.
45. Wang MD, Yin H, Landick R, Gelles J, Block SM (1997) Stretching DNA with optical tweezers. Biophys J 72: 1335-1346. (Pubitemid 27113656)
46. Kim J, Zhang C-Z, Zhang X, Springer TA (2010) A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466: 992-995.
47. Pauling L, Corey RB (1951) The pleated sheet, a new layer configuration of polypeptide chains. Proc Natl Acad Sci USA 37: 251-256.
48. Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72: 1541-1555. (Pubitemid 27133095)
49. Kim B-H, Palermo NY, Lovas Sn, Zaikova T, Keana JFW, et al. (2011) Single-molecule atomic force microscopy force spectroscopy study of Aβ-40 interactions. Biochemistry 50: 5154-5162.
50. Ulmer TS, Bax A, Cole NB, Nussbaum RL (2005) Structure and dynamics of micelle-bound human α-synuclein. J Biol Chem 280: 9595-9603. (Pubitemid 40409655)
51. Jónsson Sigurour Æ, Mitternacht S, Irbäck A (2013) Mechanical resistance in unstructured proteins. Biophys J 104: 2725-2732.
52. Vilar M, Chou H-T, Lührs T, Maji SK, Riek-Loher D, et al. (2008) The fold of α-synuclein fibrils. Proc Natl Acad Sci USA 105: 8637-8642.
53. Uversky VN, Li J, Fink AL (2001) Evidence for a partially folded intermediate in α-synuclein fibril formation. J Biol Chem 276: 10737-10744. (Pubitemid 38089246)
54. Dedmon MM, Lindorff-Larsen K, Christodoulou J, Vendruscolo M, Dobson CM (2005) Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127: 476-477. (Pubitemid 40174345)
55. Bertoncini CW, Jung Y-S, Fernandez CO, Hoyer W, Griesinger C, et al. (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured α-synuclein. Proc Natl Acad Sci USA 102: 1430-1435. (Pubitemid 40209187)
56. Elms PJ, Chodera JD, Bustamante C, Marqusee S (2012) The molten globule state is unusually deformable under mechanical force. Proc Natl Acad Sci USA 109: 3796-3801.
57. Yu H, Gupta AN, Liu X, Neupane K, Brigley AM, et al. (2012) Energy landscape analysis of native folding of the prion protein yields the diffusion constant, transition path time, and rates. Proc Natl Acad Sci USA 109: 14452-14457.
58. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112. (Pubitemid 27218118)
59. Schlierf M, Li H, Fernandez JM (2004) The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques. Proc Natl Acad Sci USA 101: 7299-7304. (Pubitemid 38638027)
60. Jagannathan B, Elms PJ, Bustamante C, Marqusee S (2012) Direct observation of a force-induced switch in the anisotropic mechanical unfolding pathway of a protein. Proc Natl Acad Sci USA 109: 17820-17825.
61. Crampton N, Brockwell DJ (2010) Unravelling the design principles for single protein mechanical strength. Curr Opin Struc Biol 20: 508-517.
62. Carrion-Vazquez M, Li HB, Lu H, Marszalek PE, Oberhauser AF, et al. (2003) The mechanical stability of ubiquitin is linkage dependent. Nat Struct Biol 10: 738-743. (Pubitemid 37052413)
63. Cecconi C, Shank EA, Bustamante C, Marqusee S (2005) Direct observation of the three-state folding of a single protein molecule. Science 309: 2057-2060. (Pubitemid 41362324)
64. Gebhardt JCM, Bornschlögl T, Rief M (2010) Full distance-resolved folding energy landscape of one single protein molecule. Proc Natl Acad Sci USA 107: 2013-2018.
65. Fauerbach JA, Yushchenko DA, Shahmoradian SH, Chiu W, Jovin TM, et al. (2012) Supramolecular non-amyloid intermediates in the early stages of alpha-synuclein aggregation. Biophys J 102: 1127-1136.
66. Dong J, Castro CE, Boyce MC, Lang MJ, Lindquist S (2010) Optical trapping with high forces reveals unexpected behaviors of prion fibrils. Nat Struct Mol Biol 17: 1422-1430.
67. Wood SJ, Wypych J, Steavenson S, Louis J-C, Citron M, et al. (1999) α-Synuclein fibrillogenesis is nucleation-dependent. J Biol Chem 274: 19509-19512.
68. Li MS, Klimov DK, Thirumalai D (2004) Thermal denaturation and folding rates of single domain proteins: size matters. Polymer 45: 573-579. (Pubitemid 38082191)
69. Ivankov DN, Garbuzynskiy SO, Alm E, Plaxco KW, Baker D, et al. (2003) Contact order revisited: Influence of protein size on the folding rate. Protein Sci 12: 2057-2062. (Pubitemid 37022826)
70. Ivankov DN, Bogatyreva NS, Lobanov MY, Galzitskaya OV (2009) Coupling between properties of the protein shape and the rate of protein folding. PLoS ONE 4: e6476.
71. Kubelka J, Hofrichter J, Eaton WA (2004) The protein folding 'speed limit'. Curr Opin Struct Biol 14: 76-88.
72. Thirumalai D, O'Brien EP, Morrison G, Hyeon C (2010) Theoretical perspectives on protein folding. Annu Rev Biophys 39: 159-183.