Single-molecule spectroscopy of protein folding dynamics-expanding scope and timescales

Current Opinion in Structural Biology

Volumn 23, Issue 1, 2013, Pages 36-47

  Schuler, Benjamin ^a   Hofmann, Hagen ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE;

DIFFUSION; DYNAMICS; ELECTRON TRANSPORT; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; IN VIVO STUDY; MICROFLUIDIC ANALYSIS; PHOTO-INDUCED ELECTRON TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SINGLE MOLECULE SPECTROSCOPY; SPECTROSCOPY;

KINETICS; PROTEIN FOLDING; PROTEINS; SPECTROMETRY, FLUORESCENCE;

EID: 84873527015     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2012.10.008     Document Type: Review

References (111)

1. Sosnick T.R., Barrick D. The folding of single domain proteins--have we reached a consensus?. Curr Opin Struct Biol 2011, 21:12-24.
2. Onuchic J.N., Wolynes P.G. Theory of protein folding. Curr Opin Struct Biol 2004, 14:70-75.
3. Dill K.A., Ozkan S.B., Shell M.S., Weikl T.R. The protein folding problem. Annu Rev Biophys 2008, 37:289-316.
4. Shaw D.E., Maragakis P., Lindorff-Larsen K., Piana S., Dror R.O., Eastwood M.P., Bank J.A., Jumper J.M., Salmon J.K., Shan Y., et al. Atomic-level characterization of the structural dynamics of proteins. Science 2010, 330:341-346.
5. Thirumalai D., O'Brien E.P., Morrison G., Hyeon C. Theoretical perspectives on protein folding. Annu Rev Biophys 2010, 39:159-183.
6. Freddolino P.L., Harrison C.B., Liu Y., Schulten K. Challenges in protein folding simulations: timescale, representation, and analysis. Nat Phys 2010, 6:751-758.
7. Bowman G.R., Voelz V.A., Pande V.S. Taming the complexity of protein folding. Curr Opin Struct Biol 2011, 21:4-11.
8. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005, 6:197-208.
9. Uversky V.N., Oldfield C.J., Dunker A.K. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Biophys 2008, 37:215-246.
10. Borgia A., Williams P.M., Clarke J. Single-molecule studies of protein folding. Annu Rev Biochem 2008, 77:101-125.
11. Rief M. Force as a Single Molecule Probe of Multidimensional Protein Energy Landscapes. Curr. Opin. Struct. Biol. 2013, 23:48-57.
12. Selvin P.R., Ha T. Single-Molecule Techniques: A Laboratory Manual 2008, Cold Spring Harbor Laboratory Press, New York.
13. Hummer G., Szabo A. Free energy surfaces from single-molecule force spectroscopy. Acc Chem Res 2005, 38:504-513.
14. Dill K.A., Shortle D. Denatured states of proteins. Annu Rev Biochem 1991, 60:795-825.
15. Hagen S.J., Hofrichter J., Szabo A., Eaton W.A. Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding. Proc Natl Acad Sci USA 1996, 93:11615-11617.
16. Kubelka J., Hofrichter J., Eaton W.A. The protein folding 'speed limit'. Curr Opin Struct Biol 2004, 14:76-88.
17. Bieri O., Wirz J., Hellrung B., Schutkowski M., Drewello M., Kiefhaber T. The speed limit for protein folding measured by triplet-triplet energy transfer. Proc Natl Acad Sci USA 1999, 96:9597-9601.
18. Schuler B., Müller-Späth S., Soranno A., Nettels D. Application of Confocal Single-Molecule FRET to Intrinsically Disordered Proteins. Intrinsically Disordered Protein Analysis: Volume 2, Methods and Experimental Tools 2012, vol 896:21-45. Springer.
19. Ferreon A.C.M., 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.
20. Schneider R., Huang J.R., Yao M., Communie G., Ozenne V., Mollica L., Salmon L., Jensen M.R., Blackledge M. Towards a robust description of intrinsic protein disorder using nuclear magnetic resonance spectroscopy. Mol Biosyst 2012, 8:58-68.
21. Schuler B., Eaton W.A. Protein folding studied by single-molecule FRET. Curr Opin Struct Biol 2008, 18:16-26.
22. Haran G. How, when and why proteins collapse: the relation to folding. Curr Opin Struct Biol 2012, 22:14-20.
23. Ferreon A.C., Moran C.R., Gambin Y., Deniz A.A. Single-molecule fluorescence studies of intrinsically disordered proteins. Methods Enzymol 2010, 472:179-204.
24. Sisamakis E., Valeri A., Kalinin S., Rothwell P.J., Seidel C.A.M. Accurate Single-Molecule FRET Studies Using Multiparameter Fluorescence Detection. Methods Enzymol 2010, 475:455-514.
25. Soranno A., Buchli B., Nettels D., Müller-Späth S., Cheng R.R., Pfeil S.H., Hoffmann A., Lipman E.A., Makarov D.E., Schuler B. Quantifying internal friction in unfolded and intrinsically disordered proteins with single molecule spectroscopy. Proc Natl Acad Sci USA 2012, early edition. 10.1073/pnas.1117368109.
26. Gopich I.V., Szabo A. Single-molecule FRET with diffusion and conformational dynamics. J Phys Chem B 2007, 111:12925-12932.
27. Gopich I.V., Szabo A Theory of photon counting in single-molecule spectroscopy. Theory and Evaluation of Single-Molecule Signals 2009, 1-64. World Scientific Pub. Co. E. Barkai, F.L.H. Brown, M. Orrit, H. Yang (Eds.).
28. Gopich I.V., Nettels D., Schuler B., Szabo A. Protein dynamics from single-molecule fluorescence intensity correlation functions. J Chem Phys 2009, 131:095102.
29. Gopich I.V., Szabo A. Decoding the pattern of photon colors in single-molecule FRET. J Phys Chem B 2009, 113:10965-10973.
30. Gopich I.V., Szabo A. FRET efficiency distributions of multistate single molecules. J Phys Chem B 2010, 114:15221-15226.
31. Kalinin S., Valeri A., Antonik M., Felekyan S., Seidel C.A. Detection of structural dynamics by FRET: a photon distribution and fluorescence lifetime analysis of systems with multiple states. J Phys Chem B 2010, 114:7983-7995.
32. Hyeon C., Lee J., Yoon J., Hohng S., Thirumalai D. Hidden complexity in the isomerization dynamics of holliday junctions. Nature Chem 2012, 4:907-914.
33. Gopich I.V., Szabo A. Theory of the energy transfer efficiency and fluorescence lifetime distribution in single-molecule FRET. Proc Natl Acad Sci USA 2012, 109:7747-7752.
34. Laurence T.A., Kong X.X., Jager M., Weiss S. Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins. Proc Natl Acad Sci USA 2005, 102:17348-17353.
35. Hoffmann A., Kane A., Nettels D., Hertzog D.E., Baumgärtel P., Lengefeld J., Reichardt G., Horsley D.A., Seckler R., Bakajin O., et al. Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. Proc Natl Acad Sci USA 2007, 104:105-110.
36. Chung H.S., Gopich I.V., McHale K., Cellmer T., Louis J.M., Eaton W.A. Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. J Phys Chem A 2011, 115:3642-3656.
37. Hoffmann A., Nettels D., Clark J., Borgia A., Radford S.E., Clarke J., Schuler B. Quantifying heterogeneity and conformational dynamics from single molecule FRET of diffusing molecules: recurrence analysis of single particles (RASP). Phys Chem Chem Phys 2011, 13:1857-1871.
38. Deniz A.A., Laurence T.A., Beligere G.S., Dahan M., Martin A.B., Chemla D.S., Dawson P.E., Schultz P.G., Weiss S. Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc Natl Acad Sci USA 2000, 97:5179-5184.
39. Schuler B., Lipman E.A., Eaton W.A. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 2002, 419:743-747.
40. O'Brien E.P., Ziv G., Haran G., Brooks B.R., Thirumalai D. Effects of denaturants and osmolytes on proteins are accurately predicted by the molecular transfer model. Proc Natl Acad Sci USA 2008, 105:13403-13408.
41. Hofmann H, Soranno A, Borgia A, Gast K, Nettels D, Schuler B: Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single molecule spectroscopy. Proc Natl Acad Sci USA, 109, 16155-16160.
42. Nettels D., Müller-Späth S., Küster F., Hofmann H., Haenni D., Rüegger S., Reymond L., Hoffmann A., Kubelka J., Heinz B., et al. Single molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proc Natl Acad Sci USA 2009, 106:20740-20745.
43. Best R.B., Mittal J. Protein simulations with an optimized water model: cooperative helix formation and temperature-induced unfolded state collapse. J Phys Chem B 2010, 114:14916-14923.
44. Müller-Späth S., Soranno A., Hirschfeld V., Hofmann H., Rüegger S., Reymond L., Nettels D., Schuler B. Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc Natl Acad Sci USA 2010, 107:14609-14614.
45. Hofmann H., Golbik R.P., Ott M., Hübner C.G., Ulbrich-Hofmann R. Coulomb forces control the density of the collapsed unfolded state of barstar. J Mol Biol 2008, 376:597-605.
46. Mao A.H., Crick S.L., Vitalis A., Chicoine C.L., Pappu R.V. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc Natl Acad Sci USA 2010, 107:8183-8188.
47. Huang F., Rajagopalan S., Settanni G., Marsh R.J., Armoogum D.A., Nicolaou N., Bain A.J., Lerner E., Haas E., Ying L., et al. Multiple conformations of full-length p53 detected with single-molecule fluorescence resonance energy transfer. Proc Natl Acad Sci USA 2009, 106:20758-20763.
48. Lum J.K., Neuweiler H., Fersht A.R. Long-range modulation of chain motions within the intrinsically disordered transactivation domain of tumor suppressor p53. J Am Chem Soc 2012, 134:1617-1622.
49. Milles S., Lemke E.A. Single molecule study of the intrinsically disordered FG-repeat nucleoporin 153. Biophys J 2011, 101:1710-1719.
50. Sherman E., Haran G. Coil-globule transition in the denatured state of a small protein. Proc Natl Acad Sci USA 2006, 103:11539-11543.
51. Ziv G., Thirumalai D., Haran G. Collapse transition in proteins. Phys Chem Chem Phys 2009, 11:83-93.
52. Nettels D., Gopich I.V., Hoffmann A., Schuler B. Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc Natl Acad Sci USA 2007, 104:2655-2660.
53. Nettels D., Hoffmann A., Schuler B. Unfolded protein and peptide dynamics investigated with single-molecule FRET and correlation spectroscopy from picoseconds to seconds. J Phys Chem B 2008, 112:6137-6146.
54. Wahl M., Rahn H.-J., Röhlicke T., Kell G., Nettels D., Hillger F., Schuler B., Erdmann R. Scalable time-correlated photon counting system with multiple independent input channels. Rev Sci Instrum 2008, 79:123113.
55. Doi M., Edwards S.F. The Theory of Polymer Dynamics 1988, Oxford University Press, New York, USA.
56. Khatri B.S., McLeish T.C.B. Rouse model with internal friction: a coarse grained framework for single biopolymer dynamics. Macromolecules 2007, 40:6770-6777.
57. Shoemaker B.A., Portman J.J., Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci USA 2000, 97:8868-8873.
58. Chung H.S., McHale K., Louis J.M., Eaton W.A. Single-molecule fluorescence experiments determine protein folding transition path times. Science 2012, 335:981-984.
59. Cellmer T., Henry E.R., Kubelka J., Hofrichter J., Eaton W.A. Relaxation rate for an ultrafast folding protein is independent of chemical denaturant concentration. J Am Chem Soc 2007, 129:14564-14565.
60. Doose S., Neuweiler H., Sauer M. Fluorescence quenching by photoinduced electron transfer: a reporter for conformational dynamics of macromolecules. Chemphyschem 2009, 10:1389-1398.
61. Lapidus L.J., Eaton W.A., Hofrichter J. Measuring the rate of intramolecular contact formation in polypeptides. Proc Natl Acad Sci USA 2000, 97:7220-7225.
62. Noe F., Doose S., Daidone I., Lollmann M., Sauer M., Chodera J.D., Smith J.C. Dynamical fingerprints for probing individual relaxation processes in biomolecular dynamics with simulations and kinetic experiments. Proc Natl Acad Sci USA 2011, 108:4822-4827.
63. Neuweiler H., Lollmann M., Doose S., Sauer M. Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. J Mol Biol 2007, 365:856-869.
64. Neuweiler H., Banachewicz W., Fersht A.R. Kinetics of chain motions within a protein-folding intermediate. Proc Natl Acad Sci USA 2010, 107:22106-22110.
65. Neuweiler H., Johnson C.M., Fersht A.R. Direct observation of ultrafast folding and denatured state dynamics in single protein molecules. Proc Natl Acad Sci USA 2009, 106:18569-18574.
66. Chung H.S., Cellmer T., Louis J.M., Eaton W.A. Measuring ultrafast protein folding rates from photon-by-photon analysis of single molecule fluorescence trajectories. Chem Phys 2012, 10.1016/j.chemphys.2012.08.005.
67. Rhoades E., Cohen M., Schuler B., Haran G. Two-state folding observed in individual protein molecules. J Am Chem Soc 2004, 126:14686-14687.
68. Chung H.S., Louis J.M., Eaton W.A. Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories. Proc Natl Acad Sci USA 2009, 106:11837-11844.
69. Liu F., Nakaema M., Gruebele M. The transition state transit time of WW domain folding is controlled by energy landscape roughness. J Chem Phys 2009, 131:195101.
70. Wensley B.G., Batey S., Bone F.A.C., Chan Z.M., Tumelty N.R., Steward A., Kwa L.G., Borgia A., Clarke J. Experimental evidence for a frustrated energy landscape in a three-helix-bundle protein family. Nature 2010, 463. 685-U122.
71. Sherman E., Haran G. Fluorescence correlation spectroscopy of fast chain dynamics within denatured protein L. Chemphyschem 2011, 12:696-703.
72. Rhoades E., Gussakovsky E., Haran G. Watching proteins fold one molecule at a time. Proc Natl Acad Sci USA 2003, 100:3197-3202.
73. Pirchi M., Ziv G., Riven I., Cohen S.S., Zohar N., Barak Y., Haran G. Single-molecule fluorescence spectroscopy maps the folding landscape of a large protein. Nat Commun 2011, 2:493.
74. Kuzmenkina E.V., Heyes C.D., Nienhaus G.U. Single-molecule Forster resonance energy transfer study of protein dynamics under denaturing conditions. Proc Natl Acad Sci USA 2005, 102:15471-15476.
75. Garcia-Mira M.M., Sadqi M., Fischer N., Sanchez-Ruiz J.M., Muñoz V. Experimental identification of downhill protein folding. Science 2002, 298:2191-2195.
76. Huang F., Ying L., Fersht A.R. Direct observation of barrier-limited folding of BBL by single-molecule fluorescence resonance energy transfer. Proc Natl Acad Sci USA 2009, 106:16239-16244.
77. Liu J., Campos L.A., Cerminara M., Wang X., Ramanathan R., English D.S., Munoz V. Exploring one-state downhill protein folding in single molecules. Proc Natl Acad Sci USA 2012, 109:179-184.
78. Lipman E.A., Schuler B., Bakajin O., Eaton W.A. Single-molecule measurement of protein folding kinetics. Science 2003, 301:1233-1235.
79. Hamadani K.M., Weiss S. Nonequilibrium single molecule protein folding in a coaxial mixer. Biophys J 2008, 95:352-365.
80. Pfeil S.H., Wickersham C.E., Hoffmann A., Lipman E.A. A microfluidic mixing system for single-molecule measurements. Rev Sci Instrum 2009, 80:055105.
81. Gambin Y., Vandelinder V., Ferreon A.C., Lemke E.A., Groisman A., Deniz A.A. Visualizing a one-way protein encounter complex by ultrafast single-molecule mixing. Nat Methods 2011, 8:239-241.
82. Orte A., Craggs T.D., White S.S., Jackson S.E., Klenerman D. Evidence of an intermediate and parallel pathways in protein unfolding from single-molecule fluorescence. J Am Chem Soc 2008, 130:7898-7907.
83. Knight J.B., Vishwanath A., Brody J.P., Austin R.H. Hydrodynamic focusing on a silicon chip: mixing nanoliters in microseconds. Phys Rev Lett 1998, 80:3863-3866.
84. Duffy D.C., McDonald J.C., Schueller O.J.A., Whitesides G.M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal Chem 1998, 70:4974-4984.
85. Gambin Y., Simonnet C., VanDelinder V., Deniz A., Groisman A. Ultrafast microfluidic mixer with three-dimensional flow focusing for studies of biochemical kinetics. Lab Chip 2010, 10:598-609.
86. Hofmann H., Hillger F., Pfeil S.H., Hoffmann A., Streich D., Haenni D., Nettels D., Lipman E.A., Schuler B. Single-molecule spectroscopy of protein folding in a chaperonin cage. Proc Natl Acad Sci USA 2010, 107:11793-11798.
87. Sharma S., Chakraborty K., Muller B.K., Astola N., Tang Y.C., Lamb D.C., Hayer-Hartl M., Hartl F.U. Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 2008, 133:142-153.
88. Shtilerman M., Lorimer G.H., Englander S.W. Chaperonin function: folding by forced unfolding. Science 1999, 284:822-825.
89. Jia Y.W., Talaga D.S., Lau W.L., Lu H.S.M., DeGrado W.F., Hochstrasser R.M. Folding dynamics of single GCN4 peptides by fluorescence resonant energy transfer confocal microscopy. Chem Phys 1999, 247:69-83.
90. Rasnik I., McKinney S.A., Ha T. Nonblinking and long-lasting single-molecule fluorescence imaging. Nat Methods 2006, 3:891-893.
91. Campos L.A., Liu J., Wang X., Ramanathan R., English D.S., Munoz V. A photoprotection strategy for microsecond-resolution single-molecule fluorescence spectroscopy. Nat Methods 2011, 8:143-146.
92. Ha T., Tinnefeld P. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu Rev Phys Chem 2012, 63:595-617.
93. Chung H.S., Louis J.M., Eaton W.A. Distinguishing between protein dynamics and dye photophysics in single-molecule FRET experiments. Biophys J 2010, 98:696-706.
94. Choi U.B., McCann J.J., Weninger K.R., Bowen M.E. Beyond the random coil: stochastic conformational switching in intrinsically disordered proteins. Structure 2011, 19:566-576.
95. Betancourt M.R., Thirumalai D. Exploring the kinetic requirements for enhancement of protein folding rates in the GroEL cavity. J Mol Biol 1999, 287:627-644.
96. Jewett A.I., Baumketner A., Shea J.E. Accelerated folding in the weak hydrophobic environment of a chaperonin cavity: creation of an alternate fast folding pathway. Proc Natl Acad Sci USA 2004, 101:13192-13197.
97. Takagi F., Koga N., Takada S. How protein thermodynamics and folding mechanisms are altered by the chaperonin cage: molecular simulations. Proc Natl Acad Sci USA 2003, 100:11367-11372.
98. Borgia M.B., Borgia A., Best R.B., Steward A., Nettels D., Wunderlich B., Schuler B., Clarke J. Single-molecule fluorescence reveals sequence-specific misfolding in multidomain proteins. Nature 2011, 474:662-665.
99. Oberhauser A.F., Marszalek P.E., Carrion-Vazquez M., Fernandez J.M. Single protein misfolding events captured by atomic force microscopy. Nat Struct Biol 1999, 6:1025-1028.
100. Wright C.F., Teichmann S.A., Clarke J., Dobson C.M. The importance of sequence diversity in the aggregation and evolution of proteins. Nature 2005, 438:878-881.
101. Gambin Y., Deniz A.A. Multicolor single-molecule FRET to explore protein folding and binding. Mol Biosyst 2010, 6:1540-1547.
102. Schuetz P., Wuttke R., Schuler B., Caflisch A. Free energy surfaces from single-distance information. J Phys Chem B 2010, 114:15227-15235.
103. Kamagata K., Kawaguchi T., Iwahashi Y., Baba A., Fujimoto K., Komatsuzaki T., Sambongi Y., Goto Y., Takahashi S. Long-term observation of fluorescence of free single molecules to explore protein-folding energy landscapes. J Am Chem Soc 2012, 134:11525-11532.
104. Lemke E.A. Site-specific labeling of proteins for single-molecule FRET measurements using genetically encoded ketone functionalities. Methods Mol Biol 2011, 751:3-15.
105. Chakraborty A., Wang D.Y., Ebright Y.W., Ebright R.H. Azide-specific labeling of biomolecules by Staudinger-Bertozzi ligation: phosphine derivatives of fluorescent probes suitable for single-molecule fluorescence spectroscopy. Methods in Enzymology, Vol 472: Single Molecule Tools, Pt A: Fluorescence Based Approaches 2010, 19-30.
106. Eid J., Fehr A., Gray J., Luong K., Lyle J., Otto G., Peluso P., Rank D., Baybayan P., Bettman B., et al. Real-time DNA sequencing from single polymerase molecules. Science 2009, 323:133-138.
107. Zappa F., Tisa S., Tosi A., Cova S. Principles and features of single-photon avalanche diode arrays. Sens. Actuators A: Phys. 2007, 140:103-112.
108. Gambin Y., Schug A., Lemke E.A., Lavinder J.J., Ferreon A.C.M., Magliery T.J., Onuchic J.N., Deniz A.A. Direct single-molecule observation of a protein living in two opposed native structures. Proc Natl Acad Sci USA 2009, 106:10153-10158.
109. Sakon J.J., Weninger K.R. Detecting the conformation of individual proteins in live cells. Nat Methods 2010, 7:203-205.
110. Gelman H., Platkov M., Gruebele M. Rapid perturbation of free-energy landscapes: from in vitro to in vivo. Chemistry 2012, 18:6420-6427.
111. Phillip Y., Kiss V., Schreiber G. Protein-binding dynamics imaged in a living cell. Proc Natl Acad Sci USA 2012, 109:1461-1466.