Counteracting chemical chaperone effects on the single-molecule α-synuclein structural landscape

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 44, 2012, Pages 17826-17831

  Ferreon, Allan Chris M ^a   Moosa, Mahdi Muhammad ^a   Gambin, Yann ^a,b   Deniz, Ashok A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Parkinson's disease; Protein folding; SmFRET; Urea TMAO counteraction

Indexed keywords

ALPHA SYNUCLEIN; TRIMETHYLAMINE OXIDE; UREA;

ARTICLE; FLUORESCENCE RESONANCE ENERGY TRANSFER; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ALPHA-SYNUCLEIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; METHYLAMINES; MOLECULAR CHAPERONES; PROTEIN CONFORMATION; UREA;

EID: 84868091323     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201802109     Document Type: Article

References (72)

1. Wolynes P, Onuchic J, Thirumalai D (1995) Navigating the folding routes. Science 267:1619-1620.
2. Prabhu N, Sharp K (2006) Protein-solvent interactions. Chem Rev 106:1616-1623.
3. Harries D, Rösgen J (2008) A practical guide on how osmolytes modulate macromolecular properties. Methods in Cell Biology, eds JJ Correia and HW Detrich, III (Academic, San Diego), Vol 84, pp 679-735.
4. Zhou H-X, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375-397.
5. Dyson HJ,Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54-60.
6. Frankel AD, Smith CA (1998) Induced folding in RNA-protein recognition: More than a simple molecular handshake. Cell 92:149-151.
7. Luque I, Freire E (2000) Structural stability of binding sites: Consequences for binding affinity and allosteric effects. Proteins Suppl 4:63-71.
8. Yancey P, Clark M, Hand S, Bowlus R, Somero G (1982) Living with water stress: Evolution of osmolyte systems. Science 217:1214-1222.
9. Yancey PH, Fyfe-Johnson AL, Kelly RH, Walker VP, Auñón MT (2001) Trimethylamine oxide counteracts effects of hydrostatic pressure on proteins of deep-sea teleosts. J Exp Zool 289:172-176.
10. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579-599.
11. Yancey PH (2001) Water stress, osmolytes and proteins. Am Zool 41:699-709.
12. Kenneth BS (1997) Organic solutes in freezing tolerance. Comp Biochem Physiol A Physiol 117:319-326.
13. Saha N, Ratha BK (1989) Comparative study of ureogenesis in freshwater, airbreathing teleosts. J Exp Zool 252:1-8.
14. Gordon MS, Tucker VA (1968) Further observations on the physiology of salinity adaptation in the crab-eating frog (Rana cancrivora). J Exp Biol 49:185-193.
15. Romspert AP, McClanahan LL (1981) Osmoregulation of the terrestrial salamander, Ambystoma tigrinum, in hypersaline media. Copeia 1981:400-405.
16. Withers PC (1998) Urea: Diverse functions of a "waste" product. Clin Exp Pharmacol Physiol 25:722-727.
17. Gordon JA, Jencks WP (1963) The relationship of structure to the effectiveness of denaturing agents for proteins. Biochemistry 2:47-57.
18. Bagnasco S, Balaban R, Fales HM, Yang YM, Burg M (1986) Predominant osmotically active organic solutes in rat and rabbit renal medullas. J Biol Chem 261:5872-5877.
19. Garcia-Perez A, Burg MB (1991) Renal medullary organic osmolytes. Physiol Rev 71:1081-1115.
20. Yancey PH, Somero GN (1979) Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem J 183:317-323.
21. Bolen DW, Rose GD (2008) Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu Rev Biochem 77:339-362.
22. Hu C, Rösgen J, Pettitt BM (2010) Osmolyte influence on protein stability: Perspectives of theory and experiment. Modeling Solvent Environments (Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim), pp 77-92.
23. Baskakov I, Wang A, Bolen DW (1998) Trimethylamine-N-Oxide counteracts urea effects on rabbit muscle lactate dehydrogenase function: A test of the counteraction hypothesis. Biophys J 74:2666-2673.
24. Doan-Nguyen V, Loria JP (2007) The effects of cosolutes on protein dynamics: The reversal of denaturant-induced protein fluctuations by trimethylamine N-oxide. Protein Sci 16:20-29.
25. Chakraborty K, et al. (2010) Chaperonin-catalyzed rescue of kinetically trapped states in protein folding. Cell 142:112-122.
26. Mello CC, Barrick D (2003) Measuring the stability of partly folded proteins using TMAO. Protein Sci 12:1522-1529.
27. Bandyopadhyay A, et al. (2012) Chemical chaperones assist intracellular folding to buffer mutational variations. Nat Chem Biol 8:238-245.
28. Chang Y-C, Oas TG (2010) Osmolyte-induced folding of an intrinsically disordered protein: Folding mechanism in the absence of ligand. Biochemistry 49:5086-5096.
29. Baskakov IV, et al. (1999) Trimethylamine N-Oxide-induced cooperative folding of an intrinsically unfolded transcription-activating fragment of human glucocorticoid receptor. J Biol Chem 274:10693-10696.
30. Baskakov I, Bolen DW (1998) Forcing thermodynamically unfolded proteins to fold. J Biol Chem 273:4831-4834.
31. Ferreon ACM, Deniz AA (2007) α-Synuclein multistate folding thermodynamics: Implications for protein misfolding and aggregation. Biochemistry 46:4499-4509.
32. Uversky VN, Eliezer D (2009) Biophysics of Parkinson's disease: Structure and aggregation of α-synuclein. Curr Protein Pept Sci 10:483-499.
33. Uversky VN, Li J, Fink AL (2001) Trimethylamine-N-oxide-induced folding of α-synuclein. FEBS Lett 509:31-35.
34. Deniz AA, Mukhopadhyay S, Lemke EA (2008) Single-molecule biophysics: At the interface of biology, physics and chemistry. J R Soc Interface 5:15-45.
35. Ferreon ACM, Deniz AA (2011) Protein folding at single-molecule resolution. Biochim Biophys Acta 1814:1021-1029.
36. Michalet X, Weiss S, Jäger M (2006) Single-molecule fluorescence studies of protein folding and conformational dynamics. Chem Rev 106:1785-1813.
37. Schuler B, Eaton WA(2008) Protein folding studied by single-molecule FRET. Curr Opin Struct Biol 18:16-26.
38. Rajagopalan S, Huang F, Fersht AR (2011) Single-molecule characterization of oligomerization kinetics and equilibria of the tumor suppressor p53. Nucleic Acids Res 39:2294-2303.
39. Ha T, Kozlov AG, Lohman TM (2012) Single-molecule views of protein movement on single-stranded DNA. Annu Rev Biophy 41:295-319.
40. Junker JP, Ziegler F, RiefM(2009) Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 323:633-637.
41. Walter NG, Huang C-Y, Manzo AJ, Sobhy MA (2008) Do-it-yourself guide: How to use the modern single-molecule toolkit. Nat Meth 5:475-489.
42. Lamboy JA, Kim H, Lee KS, Ha T, Komives EA (2011) Visualization of the nanospring dynamics of the IκBα ankyrin repeat domain in real time. Proc Natl Acad Sci USA 108:10178-10183.
43. Borwankar T, et al. (2011) Natural osmolytes remodel the aggregation pathway of mutant huntingtin exon 1. Biochemistry 50:2048-2060.
44. Mukhopadhyay S, Krishnan R, Lemke EA, Lindquist S, Deniz AA (2007) A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proc Natl Acad Sci USA 104:2649-2654.
45. Ferreon ACM, 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.
46. 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 Engl 49:3469-3472.
47. Gambin Y, et al. (2011) Visualizing a one-way protein encounter complex by ultrafast single-molecule mixing. Nat Meth 8:239-241.
48. Vandelinder V, Ferreon ACM, Gambin Y, Deniz AA, Groisman A (2009) High-resolution temperature-concentration diagram of α-synuclein conformation obtained from a single Förster resonance energy transfer image in a microfluidic device. Anal Chem 81:6929-6935.
49. Burns JN, et al. (2010) Rescue of glaucoma-causing mutant myocilin thermal stability by chemical chaperones. ACS Chem Biol 5:477-487.
50. Auton M, Ferreon ACM, Bolen DW (2006) Metrics that differentiate the origins of osmolyte effects on protein stability: A test of the surface tension proposal. J Mol Biol 361:983-992.
51. Deniz AA, et al. (2000) Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc Natl Acad Sci USA 97:5179-5184.
52. Qu Y, Bolen CL, Bolen DW (1998) Osmolyte-driven contraction of a random coil protein. Proc Natl Acad Sci USA 95:9268-9273.
53. Hu CY, Lynch GC, Kokubo H, Pettitt BM (2010) Trimethylamine N-oxide influence on the backbone of proteins: An oligoglycine model. Proteins 78:695-704.
54. Cho SS, Reddy G, Straub JE, Thirumalai D (2011) Entropic stabilization of proteins by TMAO. J Phys Chem B 115:13401-13407.
55. Ferreon ACM, Moran CR, Gambin Y, Deniz AA (2010) Single-molecule fluorescence studies of intrinsically disordered proteins. Methods in Enzymology, ed NG Walter (Academic Press, San Diego), Vol 472, pp 179-204.
56. Müller-Späth S, et al. (2010) Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc Natl Acad Sci USA 107:14609-14614.
57. Auton M, Rösgen J, Sinev M, Holthauzen LMF, Bolen DW (2011) Osmolyte effects on protein stability and solubility: A balancing act between backbone and side-chains. Biophys Chem 159:90-99.
58. Sackett DL (1997) Natural osmolyte trimethylamine N-oxide stimulates tubulin polymerization and reverses urea inhibition. Am J Physiol Regul Integr Comp Physiol 273:R669-R676.
59. Meersman F, Bowron D, Soper AK, Koch MHJ (2009) Counteraction of urea by trimethylamine N-oxide is due to direct interaction. Biophys J 97:2559-2566.
60. Meersman F, Bowron D, Soper AK, Koch MHJ (2011) An X-ray and neutron scattering study of the equilibrium between trimethylamine N-oxide and urea in aqueous solution. Phys Chem Chem Phys 13:13765-13771.
61. Rösgen J, Jackson-Atogi R (2012) Volume exclusion and H-bonding dominate the thermodynamics and solvation of trimethylamine-N-oxide in aqueous urea. J AmChem Soc 134:3590-3597.
62. Auton M, Bolen DW (2004) Additive transfer free energies of the peptide backbone unit that are independent of the model compound and the choice of concentration scale. Biochemistry 43:1329-1342.
63. Schellman JA (2005) Destabilization and stabilization of proteins. Q Rev Biophys 38:351-361.
64. Greene RF, Pace CN (1974) Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, α-chymotrypsin, and β-lactoglobulin. J Biol Chem 249:5388-5393.
65. Rösgen J (2007) Molecular basis of osmolyte effects on protein and metabolites. Methods in Enzymology, eds D Häussinger and H Sies (Academic Press, San Diego), Vol 428, pp 459-486.
66. Haran G (2012) How, when and why proteins collapse: The relation to folding. Curr Opin Struct Biol 22:14-20.
67. Özcan U, et al. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:1137-1140.
68. Welch WJ, Brown CR (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1:109-115.
69. Tanford C (1970) Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv Protein Chem 24:1-95.
70. Thirumalai D, O'Brien EP, Morrison G, Hyeon C (2010) Theoretical perspectives on protein folding. Annu Rev Biophys 39:159-183.
71. Qu Y, Bolen DW (2003) Hydrogen exchange kinetics of RNase A and the urea: TMAO paradigm. Biochemistry 42:5837-5849.
72. Gambin Y, et al. (2009) Direct single-molecule observation of a protein living in two opposed native structures. Proc Natl Acad Sci USA 106:10153-10158.