Measurement of energy landscape roughness of folded and unfolded proteins

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

Volumn 109, Issue 48, 2012, Pages 19563-19568

  Milanesi, Lilia ^a   Waltho, Jonathan P ^a,b   Hunter, Christopher A ^a   Shaw, Daniel J ^c,e   Beddard, Godfrey S ^c   Reid, Gavin D ^c   Dev, Sagarika ^d,f   Volk, Martin ^d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^f MCM DAV College for Women   (India)

Author keywords

Photochemical trigger; Subdiffusion

Indexed keywords

ARTICLE; CHEMICAL INTERACTION; DISULFIDE BOND; ENERGY; LANDSCAPE; LIGAND BINDING; MOLECULAR DYNAMICS; MOTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTROSCOPY;

MODELS, MOLECULAR; PROTEIN FOLDING; PROTEINS;

EID: 84870347216     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211764109     Document Type: Article

References (55)

1. Sosnick TR, Barrick D (2011) The folding of single domain proteins - have we reached a consensus? Curr Opin Struct Biol 21(1):12-24.
2. McCarney ER, Kohn JE, Plaxco KW (2005) Is there or isn't there? The case for (and against) residual structure in chemically denatured proteins. Crit Rev Biochem Mol Biol 40(4):181-189.
3. Krishna MMG, Englander SW (2007) A unified mechanism for protein folding: Predetermined pathways with optional errors. Protein Sci 16(3):449-464.
4. Brockwell DJ, Radford SE (2007) Intermediates: Ubiquitous species on folding energy landscapes? Curr Opin Struct Biol 17(1):30-37.
5. Sabelko J, Ervin J, Gruebele M (1999) Observation of strange kinetics in protein folding. Proc Natl Acad Sci USA 96(11):6031-6036.
6. Eaton WA (1999) Searching for "downhill scenarios" in protein folding. Proc Natl Acad Sci USA 96(11):5897-5899.
7. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE (2011) How fast-folding proteins fold. Science 334(6055):517-520.
8. Shaw DE, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330(6002):341-346.
9. Ansari A, et al. (1985) Protein states and proteinquakes. Proc Natl Acad Sci USA 82(15): 5000-5004.
10. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254(5038):1598-1603.
11. Onuchic JN, Wolynes PG (2004) Theory of protein folding. Curr Opin Struct Biol 14(1):70-75.
12. Hagen SJ (2010) Solvent viscosity and friction in protein folding dynamics. Curr Protein Pept Sci 11(5):385-395.
13. Liu F, Nakaema M, Gruebele M (2009) The transition state transit time of WWdomain folding is controlled by energy landscape roughness. J Chem Phys 131(19):195101.
14. Cellmer T, Henry ER, Hofrichter J, Eaton WA (2008) Measuring internal friction of an ultrafast-folding protein. Proc Natl Acad Sci USA 105(47):18320-18325.
15. Lapidus LJ, Eaton WA, Hofrichter J (2000) Measuring the rate of intramolecular contact formation in polypeptides. Proc Natl Acad Sci USA 97(13):7220-7225.
16. Möglich A, Krieger F, Kiefhaber T (2005) Molecular basis for the effect of urea and guanidinium chloride on the dynamics of unfolded polypeptide chains. J Mol Biol 345(1):153-162.
17. Fierz B, et al. (2007) Loop formation in unfolded polypeptide chains on the picoseconds to microseconds time scale. Proc Natl Acad Sci USA 104(7):2163-2168.
18. Singh VR, Kopka M, Chen Y, Wedemeyer WJ, Lapidus LJ (2007) Dynamic similarity of the unfolded states of proteins L and G. Biochemistry 46(35):10046-10054.
19. Soranno A, Longhi R, Bellini T, Buscaglia M (2009) Kinetics of contact formation and endto- end distance distributions of swollen disordered peptides. Biophys J 96(4):1515-1528.
20. Nettels D, Hoffmann A, Schuler B (2008) Unfolded protein and peptide dynamics investigated with single-molecule FRET and correlation spectroscopy from picoseconds to seconds. J Phys Chem B 112(19):6137-6146.
21. Hagen SJ, Carswell CW, Sjolander EM (2001) Rate of intrachain contact formation in an unfolded protein: temperature and denaturant effects. J Mol Biol 305(5):1161-1171.
22. Volk M, et al. (1997) Peptide conformational dynamics and vibrational Stark effects following photoinitiated disulfide cleavage. J Phys Chem B 101(42):8607-8616.
23. VolkM (2001) Fast initiation of peptide and protein folding processes. Eur J Org Chem 2001(13):2605-2621.
24. Kolano C, Helbing J, Bucher G, Sander W, Hamm P (2007) Intramolecular disulfide bridges as a phototrigger to monitor the dynamics of small cyclic peptides. J Phys Chem B 111(38):11297-11302.
25. Milanesi L, et al. (2008) A method for the reversible trapping of proteins in non-native conformations. Biochemistry 47(51):13620-13634.
26. Ernsting NP (1990) Solvation of photolytically generated p-aminophenylthiyl radicals studied by sub-picosecond transient absorption. Chem Phys Lett 166(3):221-226.
27. Nettels D, Gopich IV, Hoffmann A, Schuler B (2007) Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc Natl Acad Sci USA 104(8):2655-2660.
28. Waldauer SA, Bakajin O, Lapidus LJ (2010) Extremely slow intramolecular diffusion in unfolded protein L. Proc Natl Acad Sci USA 107(31):13713-13717.
29. Shin KJ, Kapral R (1978) Kinetic theory of reactive pair dynamics in liquids. J Chem Phys 69(8):3685-3696.
30. Scott TW, Liu SN (1989) Picosecond geminate recombination of phenylthiyl freeradical pairs. J Phys Chem 93(4):1393-1396.
31. Metzler R, Klafter J (2004) The restaurant at the end of the random walk: Recent developments in the description of anomalous transport by fractional dynamics. J Phys Math Gen 37(31):R161-R208.
32. Seki K, Wojcik M, Tachiya M (2003) Recombination kinetics in subdiffusive media. J Chem Phys 119(14):7525-7533.
33. Metzler R, Klafter J (2000) The random walk's guide to anomalous diffusion: A fractional dynamics approach. Phys Rep 339(1):1-77.
34. Paciaroni A, et al. (2009) Coupled relaxations at the protein-water interface in the picosecond time scale. J R Soc Interface 6(Suppl 5):S635-S640.
35. Senet P, Maisuradze GG, Foulie C, Delarue P, Scheraga HA (2008) How main-chains of proteins explore the free-energy landscape in native states. Proc Natl Acad Sci USA 105(50):19708-19713.
36. Yang H, et al. (2003) Protein conformational dynamics probed by single-molecule electron transfer. Science 302(5643):262-266.
37. Luo G, Andricioaei I, Xie XS, Karplus M (2006) Dynamic distance disorder in proteins is caused by trapping. J Phys Chem B 110(19):9363-9367.
38. Serrano L, Bycroft M, Fersht AR (1991) Aromatic-aromatic interactions and protein stability. Investigation by double-mutant cycles. J Mol Biol 218(2):465-475.
39. Fersht AR (1987) The hydrogen bond in molecular recognition. Trends Biochem Sci 12(1):301-304.
40. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht AR (1990) Strength and co-operativity of contributions of surface salt bridges to protein stability. J Mol Biol 216(4):1031-1044.
41. Rico F, Moy VT (2007) Energy landscape roughness of the streptavidin-biotin interaction. J Mol Recognit 20(6):495-501.
42. Janovjak H, Knaus H, Muller DJ (2007) Transmembrane helices have rough energy surfaces. J Am Chem Soc 129(2):246-247.
43. Schlierf M, Rief M (2005) Temperature softening of a protein in single-molecule experiments. J Mol Biol 354(2):497-503.
44. Zwanzig R (1988) Diffusion in a rough potential. Proc Natl Acad Sci USA 85(7):2029-2030.
45. Reed MAC, et al. (2006) The denatured state under native conditions: A non-nativelike collapsed state of N-PGK. J Mol Biol 357(2):365-372.
46. Cliff MJ, et al. (2009) The denatured state of N-PGK is compact and predominantly disordered. J Mol Biol 385(1):266-277.
47. Redfield C (2004) Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins. Methods 34(1):121-132.
48. Mok KH, Nagashima T, Day IJ, Hore PJ, Dobson CM (2005) Multiple subsets of sidechain packing in partially folded states of alpha-lactalbumins. Proc Natl Acad Sci USA 102(25):8899-8904.
49. Mok KH, et al. (2007) A pre-existing hydrophobic collapse in the unfolded state of an ultrafast folding protein. Nature 447(7140):106-109.
50. Felitsky DJ, Lietzow MA, Dyson HJ, Wright PE (2008) Modeling transient collapsed states of an unfolded protein to provide insights into early folding events. Proc Natl Acad Sci USA 105(17):6278-6283.
51. Schroer MA, et al. (2010) High-pressure SAXS study of folded and unfolded ensembles of proteins. Biophys J 99(10):3430-3437.
52. Li L, Mirny LA, Shakhnovich EI (2000) Kinetics, thermodynamics and evolution of non-native interactions in a protein folding nucleus. Nat Struct Biol 7(4):336-342.
53. Viguera AR, Vega C, Serrano L (2002) Unspecific hydrophobic stabilization of folding transition states. Proc Natl Acad Sci USA 99(8):5349-5354.
54. Guigas G, Weiss M (2008) Sampling the cell with anomalous diffusion - the discovery of slowness. Biophys J 94(1):90-94.
55. Baker D (2000) A surprising simplicity to protein folding. Nature 405(6782):39-42.