Modest influence of FRET chromophores on the properties of unfolded proteins

Biophysical Journal

Volumn 107, Issue 7, 2014, Pages 1654-1660

  Zerze, Gül H ^a   Best, Robert B ^b   Mittal, Jeetain ^a  

^a Lehigh University   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; SOLVENT;

CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR DYNAMICS; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING;

FLUORESCENCE RESONANCE ENERGY TRANSFER; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; SOLVENTS;

EID: 84908192215     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.07.071     Document Type: Article

References (48)

1. T. Förster Intermolecular energy migration and fluorescence [Zwischenmolekulare energiewanderung und fluoreszenz] Ann. Phys. 2 1948 55 75
2. T. Förster Delocalized excitation and excitation transfer O. Sinanoglu, Modern Quantum Chemistry: Istanbul Lectures. Part III, Action of Light and Organic Crystals 1965 Academic Press New York
3. E.V. Kuzmenkina, C.D. Heyes, and G.U. Nienhaus Single-molecule Forster resonance energy transfer study of protein dynamics under denaturing conditions Proc. Natl. Acad. Sci. USA 102 2005 15471 15476
4. E.V. Kuzmenkina, C.D. Heyes, and G.U. Nienhaus Single-molecule FRET study of denaturant induced unfolding of RNase H J. Mol. Biol. 357 2006 313 324
5. E. Sherman, and G. Haran Coil-globule transition in the denatured state of a small protein Proc. Natl. Acad. Sci. USA 103 2006 11539 11543
6. K.A. Merchant, and R.B. Best W.A. Eaton Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations Proc. Natl. Acad. Sci. USA 104 2007 1528 1533
7. D. Nettels, A. Hoffmann, and B. Schuler Unfolded protein and peptide dynamics investigated with single-molecule FRET and correlation spectroscopy from picoseconds to seconds J. Phys. Chem. B 112 2008 6137 6146
8. D. Nettels, and S. Müller-Späth B. Schuler Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins Proc. Natl. Acad. Sci. USA 106 2009 20740 20745
9. G. Ziv, D. Thirumalai, and G. Haran Collapse transition in proteins Phys. Chem. Chem. Phys. 11 2009 83 93
10. A. Dhar, and A. Samiotakis M.S. Cheung Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding Proc. Natl. Acad. Sci. USA 107 2010 17586 17591
11. B. Schuler, and H. Hofmann Single-molecule spectroscopy of protein folding dynamics - expanding scope and timescales Curr. Opin. Struct. Biol. 23 2013 36 47
12. B. Schuler, and W.A. Eaton Protein folding studied by single-molecule FRET Curr. Opin. Struct. Biol. 18 2008 16 26
13. G.D. Scholes Long-range resonance energy transfer in molecular systems Annu. Rev. Phys. Chem. 54 2003 57 87
14. K.W. Plaxco, and I.S. Millett D. Baker Chain collapse can occur concomitantly with the rate-limiting step in protein folding Nat. Struct. Biol. 6 1999 554 556
15. M.L. Scalley, and S. Nauli D. Baker Structural transitions in the protein L denatured state ensemble Biochemistry 38 1999 15927 15935
16. C. Magg, and F.X. Schmid Rapid collapse precedes the fast two-state folding of the cold shock protein J. Mol. Biol. 335 2004 1309 1323
17. C. Magg, and J. Kubelka F.X. Schmid Specificity of the initial collapse in the folding of the cold shock protein J. Mol. Biol. 360 2006 1067 1080
18. T.Y. Yoo, and S.P. Meisburger K. Plaxco Small-angle x-ray scattering and single-molecule FRET spectroscopy produce highly divergent views of the low-denaturant unfolded state J. Mol. Biol. 418 2012 226 236
19. B. Schuler, E.A. Lipman, and W.A. Eaton Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Nature 419 2002 743 747
20. J. Jacob, and R.S. Dothager T.R. Sosnick Fully reduced ribonuclease A does not expand at high denaturant concentration or temperature J. Mol. Biol. 367 2007 609 615
21. B. Schuler, and E.A. Lipman W.A. Eaton Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence Proc. Natl. Acad. Sci. USA 102 2005 2754 2759
22. R.B. Best, and K.A. Merchant W.A. Eaton Effect of flexibility and cis residues in single-molecule FRET studies of polyproline Proc. Natl. Acad. Sci. USA 104 2007 18964 18969
23. H.S. Chung, J.M. Louis, and W.A. Eaton Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories Proc. Natl. Acad. Sci. USA 106 2009 11837 11844
24. R.B. Best, and J. Mittal Protein simulations with an optimized water model: cooperative helix formation and temperature-induced unfolded state collapse J. Phys. Chem. B 114 2010 14916 14923
25. J.L. Abascal, and C. Vega A general purpose model for the condensed phases of water: TIP4P/2005 J. Chem. Phys. 123 2005 234505
26. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
27. J. Wang, and R.M. Wolf D.A. Case Development and testing of a general amber force field J. Comput. Chem. 25 2004 1157 1174
28. M.J. Frisch, and G.W. Trucks J.A. Pople Gaussian 03, Rev. C.02 2004 Gaussian, Inc. Wallingford, CT
29. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190
30. U. Essmann, and L. Perera L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
31. J. Mittal, and T.H. Yoo T.M. Truskett Structural ensemble of an intrinsically disordered polypeptide J. Phys. Chem. B 117 2013 118 124
32. M. Knott, and R.B. Best A preformed binding interface in the unbound ensemble of an intrinsically disordered protein: evidence from molecular simulations PLOS Comput. Biol. 8 2012 e1002605
33. C. Miller, G.H. Zerze, and J. Mittal Molecular simulations indicate marked differences in the structure of amylin mutants, correlated with known aggregation propensity J. Phys. Chem. B 117 2013 16066 16075
34. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
35. S. Müller-Späth, and A. Soranno B. Schuler Charge interactions can dominate the dimensions of intrinsically disordered proteins Proc. Natl. Acad. Sci. USA 107 2010 14609 14614
36. K. Lindorff-Larsen, and S. Piana D.E. Shaw How fast-folding proteins fold Science 334 2011 517 520
37. R.B. Best, G. Hummer, and W.A. Eaton Native contacts determine protein folding mechanisms in atomistic simulations Proc. Natl. Acad. Sci. USA 110 2013 17874 17879
38. S. Piana, J.L. Klepeis, and D.E. Shaw Assessing the accuracy of physical models used in protein-folding simulations: quantitative evidence from long molecular dynamics simulations Curr. Opin. Struct. Biol. 24 2014 98 105
39. H.S. Ashbaugh, and N.J. Collett J.A. Staton Assessing the thermodynamic signatures of hydrophobic hydration for several common water models J. Chem. Phys. 132 2010 124504
40. Y. Duan, and C. Wu P. Kollman A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24 2003 1999 2012
41. W. Kremer, and B. Schuler H.R. Kalbitzer Solution NMR structure of the cold-shock protein from the hyperthermophilic bacterium Thermotoga maritima Eur. J. Biochem. 268 2001 2527 2539
42. N.D. Clarke, and L.J. Beamer C.O. Pabo The DNA binding arm of λ-repressor: critical contacts from a flexible region Science 254 1991 267 270
43. M. Cai, and R. Zheng A.M. Gronenborn Solution structure of the N-terminal zinc binding domain of HIV-1 integrase Nat. Struct. Biol. 4 1997 567 577
44. H. Flyvbjerg, and H.G. Petersen Error estimates on averages of correlated data J. Chem. Phys. 91 1989 461 466
45. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
46. L. Stryer, and R.P. Haugland Energy transfer: a spectroscopic ruler Proc. Natl. Acad. Sci. USA 58 1967 719 726
47. E.P. O'Brien, and G. Morrison D. Thirumalai How accurate are polymer models in the analysis of Förster resonance energy transfer experiments on proteins? J. Chem. Phys. 130 2009 124903
48. M. Hoefling, and N. Lima H. Grubmüller Structural heterogeneity and quantitative FRET efficiency distributions of polyprolines through a hybrid atomistic simulation and Monte Carlo approach PLoS ONE 6 2011 e19791