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Fast protein folding kinetics

Published online by Cambridge University Press:  18 March 2014

Hannah Gelman  and
Martin Gruebele
Hannah Gelman
Affiliation:
Departments of Physics, Chemistry, and Center for Biophysics and Computational Biology, University of Illinois, Urbana, IL 61801, USA
Martin Gruebele*
Affiliation:
Departments of Physics, Chemistry, and Center for Biophysics and Computational Biology, University of Illinois, Urbana, IL 61801, USA
*
*Author for Correspondence: Martin Gruebele, Departments of Physics, Chemistry, and Center for Biophysics and Computational Biology, University of Illinois, 600 S. Mathews Avenue, RAL 29A, Urbana, IL 61801, USA. Tel: (217) 333-6136; Fax: (217) 244-3186; Email: mgruebel@illinois.edu
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Abstract

Fast-folding proteins have been a major focus of computational and experimental study because they are accessible to both techniques: they are small and fast enough to be reasonably simulated with current computational power, but have dynamics slow enough to be observed with specially developed experimental techniques. This coupled study of fast-folding proteins has provided insight into the mechanisms, which allow some proteins to find their native conformation well <1 ms and has uncovered examples of theoretically predicted phenomena such as downhill folding. The study of fast folders also informs our understanding of even ‘slow’ folding processes: fast folders are small; relatively simple protein domains and the principles that govern their folding also govern the folding of more complex systems. This review summarizes the major theoretical and experimental techniques used to study fast-folding proteins and provides an overview of the major findings of fast-folding research. Finally, we examine the themes that have emerged from studying fast folders and briefly summarize their application to protein folding in general, as well as some work that is left to do.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 47 , Issue 2 , May 2014 , pp. 95 - 142
Copyright
Copyright © Cambridge University Press 2014 

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References

7. References

Abbruzzetti, S., Carcelli, M., Pelagatti, P., Rogolino, D. & Viappiani, C. (2001a). Photoinduced alkaline pH-jump on the nanosecond time scale. Chemical Physics Letters 344, 387–394.CrossRefGoogle Scholar
Abbruzzetti, S., Viappiani, C., Small, J. R., Libertini, L. J. & Small, E. W. (2001b). Kinetics of histidine deligation from the heme in GuHCl-unfolded Fe(III) Cytochrome c studied by a laser-induced pH-jump technique. Journal of American Chemical Society 123, 6649–6653.Google Scholar
Ansari, A., Jones, C. M., Henry, E. R., Hofrichter, J. & Eaton, W. A. (1992). The role of solvent viscosity in the dynamics of protein conformational changes. Science 256, 1797–1798.Google Scholar
Arora, P., Oas, T. G. & Myers, J. K. (2004). Fast and faster: a designed variant of the B-domain of protein A folds in 3 microsec. Protein Science 13, 847–853.Google Scholar
Ballew, R. M., Sabelko, J. & Gruebele, M. (1996). Direct observation of fast protein folding: the initial collapse of apomyoglobin. Proceedings of the National Academy of Sciences of the United States of America 93, 5759–5764.Google Scholar
Bartels, T., Choi, J. G. & Selkoe, D. J. (2011). Alpha-synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477, 107.Google Scholar
Barua, B., Lin, J. C., Williams, V. D., Kummler, P., Neidigh, J. W. & Andersen, N. H. (2005). The Trp-cage: opitmizing the stability of a globular miniprotein. Protein Engineering, Design, and Selection 21, 171–185.Google Scholar
Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N. & Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research 28, 235–242.Google Scholar
Best, R. B. & Hummer, G. (2010). Coordinate-dependent diffusion in protein folding. Proceedings of the National Academy of Sciences of the United States of America 107, 1088–1093.Google Scholar
Blanco, F. J., Rivas, G. & Serrano, L. (1994). A short linear peptide that folds into a native stable β-hairpin in aqueous solution. Nature Structural Biology 1, 584–590.Google Scholar
Bowman, G. R., Beauchamp, K. A., Boxer, G. & Pande, V. S. (2009). Progress and challenges in the automated construction of Markov state models for full protein systems. Journal of Chemical Physics 131, 124101.Google Scholar
Bowman, G. R., Voelz, V. A. & Pande, V. S. (2010). Atomistic folding simulations of the five-helix bundle protein λ 6–85. Journal of the American Chemical Society 133, 664–667.Google Scholar
Brewer, S. H., Song, B., Raleigh, D. P. & Dyer, R. B. (2007). Residue specific resolution of protein folding dynamics using isotope-edited infrared temperature jump spectroscopy. Biochemistry 46, 3279–3285.Google Scholar
Bryngelson, J. D., Onuchic, J. N., Socci, N. D. & Wolynes, P. G. (1995). Funnels, pathways and the energy landscape of protein folding: a synthesis. Proteins: Structure, Function, and Genetics 21, 167–195.Google Scholar
Bryson, J. W., Desjarlais, J. R., Handel, T. M. & Degrado, W. F. (1998). From coiled coils to small globular proteins: design of a native-like three-helix bundle. Protein Science 7, 1404–1417.Google Scholar
Bunagan, M. R., Yang, X., Saven, J. G. & Gai, F. (2006). Ultrafast folding of a computationally designed Trp-cage mutant: Trp 2-cage. Journal of Physical Chemistry B 110, 3759–3763.CrossRefGoogle Scholar
Burton, R. E., Huang, G. S., Daugherty, M. A., Fullbright, P. W. & Oas, T. G. (1996). Microsecond protein folding through a compact transition state. Journal of Molecular Biology 263, 311–322.CrossRefGoogle ScholarPubMed
Buscaglia, M., Schuler, B., Lapidus, L. J., Eaton, W. A. & Hofrichter, J. (2003). Kinetics of intramolecular contact formation in a denatured protein. Journal of Molecular Biology 332, 9–12.Google Scholar
Campos, L. A., Liu, J. & Muñoz, V. (2009). The importance of being quantitative. Proceedings of the National Academy of Sciences of the United States of America 106, E139–E140.Google Scholar
Cellmer, T., Henry, E. R., Hofrichter, J. & Eaton, W. A. (2008). Measuring internal friction of an ultrafast-folding protein. Proceedings of the National Academy of Sciences of the United States of America 105, 18320–18325.Google Scholar
Cerminara, M., Desai, T. M., Sadqi, M. & Munoz, V. (2012). Downhill protein folding modules as scaffolds for broad-range ultrafast biosensors Journal of the American Chemical Society 134, 8010–8013.Google Scholar
Chahine, J., Oliveira, R. J., Leite, V. B. P. & Wang, J. (2007). Configuration dependent diffusion can shift the kinetic transition state and barrier height of protein folding. Proceedings of the National Academy of Sciences of the United States of America 104, 14646–14651.Google Scholar
Chan, C. K., Hofrichter, J. & Eaton, W. A. (1996). Optical triggers of protein folding. Science 274, 628–629.Google Scholar
Chan, C.-K., Hu, Y., Takahashi, S., Rousseau, D. L., Eaton, W. A. & Hofrichter, J. (1997). Submillisecond protein folding kinetics studied by ultrarapid mixing. Proceedings of the National Academy of Sciences of the United States of America 94, 1779–1784.Google Scholar
Chandler, D. (1987). Introduction to Modern Statistical Mechanics. New York, NY: Oxford University Press.Google Scholar
Chiu, T. K., Kubelka, J., Herbst-Irmer, R., Eaton, W. A., Hofrichter, J. & Davies, D. R. (2005). High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Proceedings of the National Academy of Sciences of the United States of America 102, 7517–7522.CrossRefGoogle ScholarPubMed
Cho, J., O'Connell, N., Raleigh, D. P. & Palmer, A. G. (2010). ϕ-Value analysis for ultrafast folding proteins by NMR relaxation dispersion. Journal of the American Chemical Society 132, 450–451.Google Scholar
Cho, S. S., Weinkam, P. & Wolynes, P. G. (2008). Origins of barriers and barrierless folding in BBL. Proceedings of the National Academy of Sciences of the United States of America 105, 118–123.Google Scholar
Chowdary, P. D. & Gruebele, M. (2009). Molecules: what kind of a bag of atoms? Journal of Physical Chemistry A 113, 13139–13143.Google Scholar
Chung, H. S., Gopich, I. V., McHale, K., Cellmer, T., Louis, J. M. & Eaton, W. A. (2011). Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. Journal of Physical Chemistry A 115, 3642–3656.CrossRefGoogle ScholarPubMed
Chung, H. S., Louis, J. M. & Eaton, W. A. (2009). Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories. Proceedings of the National Academy of Sciences of the United States of America 106, 11837–11844.Google Scholar
Chung, H. S., McHale, K., Louis, J. M. & Eaton, W. A. (2012). Single-molecule fluorescence experiments determine protein folding transition path times. Science 335, 981–984.Google Scholar
Clarke, N. D., Kissinger, C. R., Desjarlais, J., Gilliland, G. L. & Pabo, C. O. (1994). Structural studies of the engrailed homeodomain. Protein Science 3, pp. 1779–1787.Google Scholar
Cochran, A. G., Skelton, N. J. & Starovasnik, M. A. (2001). Tryptophan zippers: stable, monomeric beta-hairpins. Proceedings of the National Academy of Sciences of the United States of America 98, 5578–5583.Google Scholar
Crane, J. C., Koepf, E. K., Kelly, J. W. & Gruebele, M. (2000). Mapping the transition state of the WW domain beta-sheet. Journal of Molecular Biology 298, 283–292.Google Scholar
Culik, R. M., Serrano, A. L., Bunagan, M. R. & Gai, F. (2011). Achieving secondary structural resolution in kinetic measurements of protein folding: a case study of the folding mechanism of Trp-cage. Angewandte Chemie International Edition 50, 10884–10887.Google Scholar
Davis, C. M., Xiao, S., Raleigh, D. P. & Dyer, R. B. (2012). Raising the speed limit for beta-hairpin formation Journal of the American Chemical Society 134, 14476–14482.Google Scholar
DeCamp, S. J., Naganathan, A. N., Waldauer, S. A., Bakajin, O. & Lapidus, L. J. (2009). Direct observation of downhill folding of lambda-repressor in a microfluidic mixer. Biophysical Journal 97, 1772–1777.Google Scholar
Delbrück, H., Mueller, U., Perl, D., Schmid, F. X. & Heinemann, U. (2001). Crystal structures of mutant forms of the Bacillus caldolyticus cold shock protein differing in thermal stability. Journal of Molecular Biology 313, 359–369.CrossRefGoogle ScholarPubMed
Dhar, A., Samiotakis, A., Ebbinghaus, S., Nienhaus, L., Homouz, D., Gruebele, M. & Cheung, M. S. (2010). Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding. Proceedings of the National Academy of Sciences of the United States of America 107, 17586–17591.Google Scholar
Dill, K. A., Bromberg, S., Yue, K., Fiebig, K. M., Yee, D. P., Thomas, P. D. & Chan, H. S. (1995). Principles of protein folding – a perspective from simple exact models. Protein Science 4, 561–602.CrossRefGoogle ScholarPubMed
Dimitriadis, G., Drysdale, A., Myers, J. K., Arora, P., Radford, S. E., Oas, T. G. & Smith, D. A. (2004). Microsecond folding dynamics of the F13W G29A mutant of the B domain of staphylococcal protein A by laser-induced temperature jump. Proceedings of the National Academy of Sciences of the United States of America 101, 3809–3814.Google Scholar
Dobson, C. M. & Hore, P. J. (1998). Kinetic studies of protein folding using NMR spectroscopy. Nature Structural Biology 5, 504–507.Google Scholar
Duan, Y., Wang, L. & Kollman, P. A. (1998). The early stage of folding of villin headpiece subdomain observed in a 200-nanosecond fully solvated molecular dynamics simulation. Proceedings of the National Academy of Sciences of the United States of America 95, 9897–9902.Google Scholar
Dumont, C., Emilsson, T. & Gruebele, M. (2009). Reaching the protein folding speed limit with large, sub-microsecond pressure jumps. Nature Methods 6, 515–519.Google Scholar
Dumont, C., Matsumura, Y., Kim, S. J., Li, J. S., Kondrashkina, E., Kihara, H. & Gruebele, M. (2006). Solvent-tuning the collapse and helix formation time scales of λ 6–85. Protein Science 15, 2596–2604.Google Scholar
Dyer, R. B., Gai, F., Woodruff, W. H., Gilmanshin, R. & Callender, R. H. (1998). Infrared studies of fast events in protein folding. Accounts of Chemical Research 31, 709–716.Google Scholar
Ebbinghaus, S., Kim, S. J., Heyden, M., Yu, X., Heugen, U., Gruebele, M., Leitner, L. & Havenith, M. (2007). An extended dynamical hydration shell around proteins. Proceedings of the National Academy of Sciences of the United States of America 104, 20749–20752.Google Scholar
Eigen, M. & Maeyer, L. D. (1963). Relaxation Methods. In Technique of Organic Chemistry (ed. Weissberger, A.), pp. 895–1054. New York: Interscience.Google Scholar
Enright, M. B. & Leitner, D. M. (2005). Mass fractal dimension and the compactness of proteins. Physical Review E 71, 011912.Google Scholar
Ensign, D. L. & Pande, V. S. (2009). The Fip35 WW domain folds with structural and mechanistic heterogeneity in molecular dynamics simulations. Biophysical Journal 96, 53–55.Google Scholar
Espinosa, J. F., Muñoz, V. & Gellman, S. H. (2001). Interplay between hydrophobic cluster and loop propensity in β-hairpin formation. Journal of Molecular Biology 306, 397–402.Google Scholar
Fan, L., Fuss, J. O., Cheng, Q. J., Arvai, A. S., Hammel, M., Roberts, V. A., Cooper, P. K. & Tainer, J. A. (2008). XPD helicase structures and activities. Cell 133, 789–900.Google Scholar
Ferguson, N., Schartau, P. J., Sharpe, T. D., Sato, S. & Fersht, A. R. (2004). One-state downhill versus conventional protein folding. Journal of Molecular Biology 344, 295–301.Google Scholar
Ferguson, N., Sharpe, T. D., Schartau, P. J., Sato, S., Allen, M. D., Johnson, C. M., Rutherford, T. J. & Fersht, A. R. (2005). Ultra-fast barrier-limited folding in the peripheral subunit-binding domain family. Journal of Molecular Biology 353, 427–446.Google Scholar
Freddolino, P. L., Liu, F., Gruebele, M. & Schulten, K. (2008). Ten-microsecond molecular dynamics simulation of a fast-folding WW domain. Biophysical Journal 94, 75–77.Google Scholar
Freddolino, P. L., Park, S., Roux, B. & Schulten, K. (2009). Force field bias in protein folding simulations. Biophysical Journal 96, 3772–3780.Google Scholar
Fuller, A. A., Du, D., Liu, F., Davoren, J. E., Bhabha, G., Kroon, G., Case, D. A., Dyson, H. J., Powers, E. T., Wipf, P., Gruebele, M. & Kelly, J. W. (2009). Evaluating®-turn mimics as β-sheet folding nucleators. Proceedings of the National Academy of Sciences of the United States of America 106, 11067–11072.Google Scholar
Fung, A., Li, P., Godoy-Ruiz, R., Sanchez-Ruiz, J. M. & Munoz, V. (2008). Expanding the realm of ultrafast protein folding. Journal of the American Chemical Society 130, 7489–7495.Google Scholar
Gambin, Y., VanDelinder, V., Ferreon, A. C. M., Lemke, E. A., Groisman, A. & Deniz, A. A. (2011). Visualizing a one-way protein encounter by ultrafast single-molecule mixing. Nature Methods 8, 239–241.Google Scholar
Garcia-Mira, M. M., Sadqi, M., Fischer, N., Sanchez-Ruiz, J. M. & Muñoz, V. (2002). Experimental identification of downhill protein folding. Journal of the American Chemical Society 298, 2191–2195.Google Scholar
Ghaemmaghami, S., Word, J. M., Burton, R. E., Richardson, J. S. & Oas, T. G. (1998). Folding kinetics of a fluorescent variant of monomeric λ repressor. Biochemistry 37, 9179–9185.CrossRefGoogle ScholarPubMed
Gillespie, B., Vu, D. M., Shah, P. S., Marshall, S. A., Dyer, R. B., Mayo, S. L. & Plaxco, K. W. (2003). NMR and temperature-jump measurements of de novo designed proteins demonstrate rapid folding in the absence of explicit selection for kinetics. Journal of Molecular Biology 330, 813–819.Google Scholar
Gouda, H., Torigoe, H., Saito, A., Sato, M., Arata, Y. & Shimada, I. (1992). Three-dimensional solution structure of the B domain of staphylococcal protein A: comparisons of the solution and crystal structures. Biochemistry 31, 9665–9672.Google Scholar
Gruebele, M. (1999). The fast protein folding problem. Annual Review of Physical Chemistry 50, 485–516.Google Scholar
Gruebele, M. (2007). Comment on: ‘Probe-dependent and nonexponential relaxation kinetics: unreliable signatures of downhill protein folding’. Proteins: Structure, Function, and Bioinformatics 70, 1099–1102.Google Scholar
Gruebele, M. (2008). Comment on: ‘Probe-dependent and nonexponential relaxation kinetics: unreliable signatures of downhill protein folding’. Proteins: Structure, Function, and Bioinformatics 70, 1099–1102.CrossRefGoogle ScholarPubMed
Guo, Z., Brooks, C. L. & Boczko, E. M. (1997). Exploring the folding free energy surface of a three-helix bundle protein. Proceedings of the National Academy of Sciences of the United States of America 94, 10161–10166.Google Scholar
Hagen, S. (2007). Probe-dependent and nonexponential relaxation kinetics: unreliable signatures of downhill protein folding. Proteins: Structure, Function, and Bioinformatics 68, 205–217.Google Scholar
Hagen, S. J., Hofrichter, J., Szabo, A. & Eaton, W. A. (1996). Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding. Proceedings of the National Academy of Sciences of the United States of America 93, 11615–11617.Google Scholar
Halle, B. & Davidovic, M. (2003). Biomolecular hydration: from water dynamics to hydrodynamics. Proceedings of the National Academy of Sciences of the United States of America 100, 12135–12140.CrossRefGoogle ScholarPubMed
Hansmann, U. H. E. (1997). Parallel tempering algorithm for conformational studies of biological molecules. Chemical Physics Letters 281, 140–150.Google Scholar
Hawley, S. A. (1971). Reversible pressure-temperature unfolding of chymotrypsinogen. Biochemistry 10, 2436–2442.Google Scholar
Hoffmann, A., Kane, A., Nettels, D., Hertzog, D. E., Baumgartel, P., Lengefeld, J., Reichardt, G., Horsley, D. A., Seckler, R., Bakajin, O. & Schuler, B. (2007). Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 104, 105–110.CrossRefGoogle ScholarPubMed
Homouz, D., Perham, M., Samiotakis, A., Cheung, M. S. & Wittung-Stafshede, P. (2008). Crowded, cell-like environment induces shape changes in aspherical protein. Proceedings of the National Academy of Sciences of the United States of America 105, 11754–11759.Google Scholar
Hopkins, F. G. (1930). Denaturation of proteins by urea and related substances. Nature 126, 328–330.Google Scholar
Horng, J.-C., Moroz, V. & Raleigh, D. P. (2003). Rapid cooperative two-state folding of a miniature α–β protein and design of a thermostable variant. Journal of Molecular Biology 326, 1261–1270.Google Scholar
Hu, W., Walters, B. T., Kan, Z. Y., Mayne, L., Rosen, L. E., Marqusee, S. & Englander, S. W. (2013). Stepwise protein folding at near amino acid resolution by hydrogen exchange and mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 110, 7684–7689.Google Scholar
Huang, F., Ying, L. & Fersht, A. R. (2009). Direct observation of barrier-limited folding of BBL by single-molecule fluorescence resonance energy transfer. Proceedings of the National Academy of Sciences of the United States of America 106, 16239–16244.Google Scholar
Huang, G. S. & Oas, T. G. (1995a). Structure and stability of monomeric lambda repressor: NMR evidence for two-state folding. Biochemistry 34, 3884–3892.Google Scholar
Huang, G. S. & Oas, T. G. (1995b). Submillisecond folding of monomeric lambda repressor. Proceedings of the National Academy of Sciences of the United States of America 92, 6878–6882.Google Scholar
Hubner, I. A., Deeds, E. J. & Shakhnovich, E. I. (2006). Understanding ensemble protein folding at atomic detail. Proceedings of the National Academy of Sciences of the United States of America 103, 17747–17752.Google Scholar
Hummer, G. (2005). Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica exchange molecular dynamics simulations. New Journal of Physics 7, Art. No. 34.Google Scholar
Jackson, S. E. & Fersht, A. R. (1991). Folding of chymotrypsin Inhibitor-2 .I. Evidence for a 2-state transition. Biochemistry 30, 10428–10435.Google Scholar
Jäger, M., Nguyen, H., Crane, J. C., Kelly, J. W. & Gruebele, M. (2001). The folding mechanism of a beta-sheet: the WW domain. Journal of Molecular Biology 311, 373–393.Google Scholar
Jäger, M., Zhang, Y., Bieschke, J., Nguyen, H., Dendle, M., Bowman, M. E., Noel, J. P., Gruebele, M. & Kelly, J. W. (2006). Structure–function-folding relationship in a WW domain. Proceedings of the National Academy of Sciences of the United States of America 103, 10648–10653.Google Scholar
Jas, G., Eaton, W. A. & Hofrichter, J. (2001). Effect of viscosity on the kinetics of [alpha]-helix and [beta]-hairpin formation. Journal of Physical Chemistry B 105, 261–272.Google Scholar
Jennings, P. A. & Wright, P. E. (1993). Formation of a molten globule intermediate early in the kinetic folding pathway of Apomyoglobin. Science 262, 892–896.Google Scholar
Johansson, M. U., de Château, M., Björck, L., Forsén, S., Drakenberg, T. & Wikström, M. (1995). The GA module, a mobile albumin-binding bacterial domain, adopts a three-helix-bundle structure. FEBS Letters 374, 257–261.Google Scholar
Jones, C. M., Ansari, A., Henry, E. R., Christoph, G. W., Hofrichter, J. & Eaton, W. A. (1992). Speed of intersubunit communication in proteins. Biochemistry 31, 6692–6702.Google Scholar
Karanicolas, J. & Brooks, C. L. (2003). The structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding protein: lessons for protein design? Proceedings of the National Academy of Sciences of the United States of America 100, 3955–3959.Google Scholar
Kim, S. J., Matsumura, Y., Dumont, C., Kihara, H. & Gruebele, M. (2009). Slowing down downhill folding: a three-probe study. Biophysical Journal 97, 295–302.Google Scholar
Kimura, T., Lee, J. C., Gray, H. B. & Winkler, J. R. (2009). Folding energy landscape of cytochrome cb562. Proceedings of the National Academy of Sciences of the United States of America 106, 7834–1839.CrossRefGoogle ScholarPubMed
Klepeis, J. L., Lindorff-Larsen, K., Dror, R. O. & Shaw, D. E. (2009). Long-timescale molecular dynamics simulations of protein structure and function. Current Opinion in Structural Biology 19, 120–127.Google Scholar
Knight, J. B., Vishwanath, A., Brody, J. P. & Austin, R. H. (1997). Hydrodynamic focusing on a silicon chip: mixing nanoliters in microseconds. Physical Review Letter 80, 3863–3866.Google Scholar
Kramers, H. A. (1940). Brownian motion in a field of force and the diffusion model of chemical reactions. Physica 7, 284.Google Scholar
Kriwacki, R. W., Hengst, L., Tennant, L., Reed, S. T. & Wright, P. E. (1996). Structural studies of p21(Waf1/Cip1/Sdi1) in the free and Cdk2-bound state. Proceedings of the National Academy of Sciences of the United States of America 93, 11504–11509.Google Scholar
Kubelka, J., Chiu, T. K., Davies, D. R., Eaton, W. A. & Hofrichter, J. (2006). Sub-microsecond protein folding. Journal of Molecular Biology 359, 546–553.Google Scholar
Kubelka, J., Eaton, W. A. & Hofrichter, J. (2003). Experimental tests of villin subdomain folding simulations. Journal of Molecular Biology 329, 625–630.Google Scholar
Kubelka, J., Hofrichter, J. & Eaton, W. A. (2004). The protein folding speed limit. Current Opinion in Structural Biology 14, 76–88.Google Scholar
Kuzmenkina, E. V., Heyes, C. D. & Nienhaus, G. U. (2005). Single-molecule Forster resonance energy transfer study of protein dynamics under denaturing conditions. Proceedings of the National Academy of Sciences of the United States of America 102, 15471–15476.Google Scholar
Lapidus, L. J., Yao, S., McGarrity, K. S., Hertzog, D. E., Tubman, E. & Bakajin, O. (2007). Protein hydrophobic collapse and early folding steps observed in a microfluidic mixer. Biophysical Journal 93, 218–224.Google Scholar
Lee, C. L., Lin, C. T., Stell, G. & Wang, J. (2003). Diffusion dynamics, moments, and distribution of first-passage time on the protein folding energy landscape, with applications to single molecules. Physical Review E 67, 041905.Google Scholar
Leeson, D. T., Gai, F., Rodriguez, H. M., Gregoret, L. M. & Dyer, R. B. (2000). Protein folding and unfolding on a complex energy landscape. Proceedings of the National Academy of Sciences of the United States of America 97, 2527–2532.Google Scholar
Levinthal, C. (1969). How to fold graciously. In Molecular Spectroscopy in Biological Systems: Proceeds of a Meeting held at Allerton House (eds. Debrunner, J. T. P. & Munck, E.), pp. 22–24. Urbana, IL: University of Illinois Press.Google Scholar
Liang, J. & Dill, K. A. (2001). Are proteins well-packed. Biophysical Journal 81, 751–766.Google Scholar
Lin, C. W., Culik, R. M. & Gai, F. (2013). Using VIP T-jump to distinguish between different folding mechanisms: application to BBL and a Trpzip. Journal of the American Chemical Society 135, 7668–7673.Google Scholar
Lindorff-Larsen, K., Maragakis, P., Piana, S., Eastwood, M. P., Dror, R. O. & Shaw, D. E. (2012). Systematic validation of protein force fields against experimental data. PLoS ONE 7, e32131.Google Scholar
Lindorff-Larsen, K., Piana, S., Dror, R. O. & Shaw, D. E. (2011). How fast-folding proteins fold. Science 334, 517–520.Google Scholar
Lipman, E. A., Schuler, B., Bakajin, O. & Eaton, W. A. (2003). Single-molecule measurement of protein folding kinetics. Science 301, 1233–1235.Google Scholar
Liu, F., Du, D., Fuller, A. A., Davoren, J. E., Wipf, P., Kelly, J. W. & Gruebele, M. (2008). An experimental survey of the transition between two-state and downhill protein folding scenarios. Proceedings of the National Academy of Sciences of the United States of America 105, 2369–2374.Google Scholar
Liu, F., Dumont, C., Zhu, Y., DeGrado, W. F., Gai, F. & Gruebele, M. (2009a). A one-dimensional free energy surface does not account for two-probe folding kinetics of protein alpha(3)D. Journal of Chemical Physics 130, 061101.CrossRefGoogle Scholar
Liu, F., Gao, Y. G. & Gruebele, M. (2010). A survey of lambda repressor fragments from two-state to downhill folding. Journal of Molecular Biology 397, 789–798.Google Scholar
Liu, F. & Gruebele, M. (2007). Tuning λ 6–85 towards downhill folding at its melting temperature. Journal of Molecular Biology 370, 574–584.Google Scholar
Liu, F. & Gruebele, M. (2008). Downhill dynamics and the molecular rate of protein folding. Chemical Physics Letters 461, 1–8.Google Scholar
Liu, F., Nakaema, M. & Gruebele, M. (2009b). The transition state transit time of WW domain folding is controlled by energy landscape roughness. Journal of Chemical Physics 131, 195101.Google Scholar
Ma, H. & Gruebele, M. (2005). Kinetics are probe-dependent during downhill folding of an engineered λ 6–85 protein. Proceedings of the National Academy of Sciences of the United States of America 102, 2283–2287.Google Scholar
Magg, C., Kubelka, J., Holtermann, G., Haas, E. & Schmid, F. X. (2006). Specificity of the initial collapse in the folding of the cold shock protein. Journal of Molecular Biology 360, 1067–1080.Google Scholar
Magg, C. & Schmid, F. X. (2004). Rapid collapse precedes the fast two-state folding of the cold shock protein. Journal of Molecular Biology 335, 1309–1323.Google Scholar
Mayor, U., Günter Grossmann, J., Foster, N. W., Freund, S. M. V. & Fersht, A. R. (2003a). The denatured state of engrailed homeodomain under denaturing and native conditions. Journal of Molecular Biology 333, 977–991.CrossRefGoogle ScholarPubMed
Mayor, U., Guydosh, N. R., Johnson, C. M., Grossmann, J. G., Sato, S., Jas, G. S., Freund, S. M. V., Alonso, D. O. V., Daggett, V. & Fersht, A. R. (2003b). The complete folding pathway of a protein from nanoseconds to microseconds. Nature 421, 863–867.Google Scholar
Mayor, U., Johnson, C. M., Daggett, V. & Fersht, A. R. (2000). Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proceedings of the National Academy of Sciences of the United States of America 97, 13518–13522.Google Scholar
McCallister, E. L., Alm, E. & Baker, D. (2000). Critical role of beta-hairpin formation in protein G folding. Nature Structural Biology 7, 669–673.Google Scholar
McConkey, E. (1982). Molecular evolution, intracellular organization, and the quinary structure of proteins. Proceedings of the National Academy of Sciences of the United States of America 79, 3236–3240.CrossRefGoogle ScholarPubMed
McGuffee, S. R. & Elcock, A. H. (2010). Diffusion, crowding, and protein stability in a dynamic molecular model of the bacterial cytoplasm. PLoS Computational Biology 6, e1000694.Google Scholar
McKnight, J. C., Doering, D. S., Matsudaira, P. T. & Kim, P. S. (1996). A thermostable 35-residue subdomain within villin headpiece. Journal of Molecular Biology 260, 126–134.Google Scholar
Mines, G. A., Pascher, T., Lee, S. C., Winkler, J. R. & Gray, H. B. (1996). Cytochrome c folding triggered by electron transfer. Chemistry and Biology 3, 491–497.CrossRefGoogle ScholarPubMed
Muñoz, V. & Eaton, W. A. (1999). A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proceedings of the National Academy of Sciences of the United States of America 96, 11311–11316.CrossRefGoogle ScholarPubMed
Muñoz, V., Eaton, W. A., Thompson, P. A. & Hofrichter, J. (1997). Folding dynamics and mechanism of β-hairpin formation. Nature 390, 196–199.Google Scholar
Myers, J. K. & Oas, T. G. (2001). Preorganized secondary structure as an important determinant of fast protein folding. Nature Structural Biology 8, 552–558.Google Scholar
Naganathan, A. N., Doshi, U., Fung, A., Sadqi, M. & Muñoz, V. (2006). Dynamics, energetics, and structure in protein folding. Biochemistry 45, 8466–8475.Google Scholar
Naganathan, A. N., Perez-Jimenez, R. L., Sanchez-Ruiz, J. M. & Muñoz, V. (2005). Robustness of downhill folding: guidelines for the analysis of equilibrium folding experiments on small proteins. Biochemistry 44, 7435–7449.Google Scholar
Neidigh, J. W., Fesinmeyer, R. M. & Andersen, N. H. (2002). Designing a 20-residue protein. Nature Structural Biology 9, 425–430.CrossRefGoogle ScholarPubMed
Nettels, D., Muller-Spath, S., Kuster, F., Hofmann, H., Haenni, D., Ruegger, S., Reymond, L., Hoffmann, A., Kubelka, J., Heinz, B., Gast, K., Best, R. B. & Schuler, B. (2009). Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proceedings of the National Academy of Sciences of the United States of America 106, 20740–20745.Google Scholar
Neudecker, P., Lundström, P. & Kay, L. E. (2009). Relaxation dispersion NMR spectroscopy as a tool for detailed studies of protein folding. Biophysical Journal 96, 2045–2054.Google Scholar
Neuweiler, H., Sharpe, T. D., Johnson, C. M., Teufel, D. P., Ferguson, N. & Fersht, A. R. (2009). Downhill versus barrier-limited folding of BBL 2: mechanistic insights from kinetics of folding monitored by independent tryptophan probes. Journal of Molecular Biology 387, 975–985.Google Scholar
Nguyen, H., Jäger, M., Moretto, A., Gruebele, M. & Kelly, J. W. (2003). Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation. Proceedings of the National Academy of Sciences of the United States of America 100, 3948–3953.Google Scholar
Nishimura, C., Dyson, H. J. & Wright, P. E. (2008). The kinetic and equilibrium molten globule intermediates of apoleghemoglobin differ in structure. Journal of Molecular Biology 378, 715–725.Google Scholar
Noé, F., Schutte, C., Vanden-Eijnden, E., Reich, L. & Weikl, T. R. (2009). Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations. Proceedings of the National Academy of Sciences of the United States of America 106, 19011–19016.Google Scholar
Onuchic, J. N., Wolynes, P. G., Luthey-Schulten, Z. & Socci, N. D. (1995). Toward an outline of the topography of a realistic protein-folding funnel. Proceedings of the National Academy of Sciences of the United States of America 92, 3626–3630.Google Scholar
Panchenko, A. R., Luthey-Schulten, Z. & Wolynes, P. G. (1996). Foldons, protein structural modules, and exons. Proceedings of the National Academy of Sciences of the United States of America 93, 2008–2013.Google Scholar
Park, S.-H., Shastry, M. C. R. & Roder, H. (1999). Folding dynamics of the B1 domain of protein G explored by ultrarapid mixing. Nature Structural Biology 6, 943–947.Google Scholar
Parker, M. J. & Marqusee, S. (1999). The cooperativity of burst phase reactions explored. Journal of Molecular Biology 293, 1195–1210.Google Scholar
Parker, M. J. & Marqusee, S. (2001). A kinetic folding intermediate probed by native state hydrogen exchange. Journal of Molecular Biology 305, 593–602.Google Scholar
Paschek, D., Hempel, S. & Garcia, A. E. (2008). Computing the stability diagram of the Trp-cage miniprotein. Proceedings of the National Academy of Sciences of the United States of America 105, 17754–17759.Google Scholar
Pascher, T., Chesick, J. P., Winkler, J. R. & Gray, H. B. (1996). Protein folding triggered by electron transfer. Science 271, 1558–1560.Google Scholar
Perl, D., Welker, C., Schindler, T. & Schröder, K. (1998). Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nature Structural Biology 5, 229–235.Google Scholar
Phillips, C. M., Mizutani, Y. & Hochstrasser, R. M. (1995). Ultrafast thermally induced unfolding of RNase A. Proceedings of the National Academy of Sciences of the United States of America 92, 7292–7296.Google Scholar
Piana, S., Lindorff-Larsen, K., Dirks, R. M., Salmon, J. K., Dror, R. O. & Shaw, D. E. (2012). Evaluating the effects of cutoffs and treatment of long-range electrostatics in protein folding simulations. PLoS ONE 7, e39918.Google Scholar
Piana, S., Lindorff-Larsen, K. & Shaw, D. E. (2013). Atomistic description of the folding of a dimeric protein. Journal of Physical Chemistry B 117, 12935–12942.Google Scholar
Piana, S., Sarkar, K., Lindorff-Larsen, K., Guo, M., Gruebele, M. & Shaw, D. E. (2011). Computational design and experimental testing of the fastest-folding β-sheet protein. Journal of Molecular Biology 405, 43–48.Google Scholar
Pogorelov, T. V. & Luthey-Schulten, Z. (2004). Variations in the fast folding rates of the lambda-repressor: a hybrid molecular dynamics study. Biophysical Journal 87, 207–214.CrossRefGoogle ScholarPubMed
Poland, D. & Scheraga, H. A. (1966). Kinetics of the helix-coil transition in polyamino acids. Journal of Chemical Physics 45, 2071–2090.Google Scholar
Prigozhin, M. B. & Gruebele, M. (2011). The fast and the slow: folding and trapping of λ 6–85. Journal of the American Chemical Society 133, 19338–19341.Google Scholar
Prigozhin, M. B., Liu, Y., Wirth, A. J., Kapoor, S., Winter, R., Schulten, K. & Gruebele, M. (2013). Misplaced helix slows down ultrafast pressure-jump protein folding. Proceedings of the National Academy of Sciences of the United States of America 110, 8087–8097.Google Scholar
Prigozhin, M. B., Sarkar, K., Law, D., Swope, W. C., Gruebele, M. & Pitera, J. (2011). Reducing lambda repressor to the core. Journal of Physical Chemistry B 115, 2090–2096.Google Scholar
Privalov, P. L., Khechinashvili, N. N. & Atanasov, B. P. (1971). Thermodynamic analysis of thermal transitions in globular proteins. I. Calorimetric study of ribotrypsinogen, ribonuclease and myoglobin. Biopolymers 10, 1865–1890.Google Scholar
Qiu, L., Pabit, S. A., Roitberg, A. E. & Hagen, S. J. (2002). Smaller and faster: the 20-residue Trp-cage protein folds in 4 μs. Journal of the American Chemical Society 124, 12952–12953.Google Scholar
Ranganathan, R., Lu, K. P., Hunter, T. & Noel, J. P. (1997). Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89, 875–886.Google Scholar
Raval, A., Piana, S., Eastwood, M. P., Dror, R. O. & Shaw, D. E. (2012). Refinement of protein structure homology models via long, all atom molecular dynamics simulations. Proteins: Structure, Function, and Genetics 80, 2071–2079.Google Scholar
Reichmann, D., Xu, Y., Cremers, C. M., Ilbert, M., Mittelman, R., Fitzgerald, M. C. & Jakob, U. (2012). Order out of disorder: working cycle of an intrinsically unfolded chaperone. Cell 148, 947–957.Google Scholar
Reiner, A., Henklein, P. & Kiefhaber, T. (2010). An unlocking/relocking barrier in conformational fluctuations of villin headpiece subdomain. Proceedings of the National Academy of Sciences of the United States of America 107, 4955–4960.Google Scholar
Religa, T. L. (2008). Comparison of multiple crystal structures with NMR data for engrailed homeodomain. Journal of Biomolecular NMR 40, 189–202.Google Scholar
Religa, T. L., Johnson, C. M., Vu, D. M., Brewer, S. H., Dyer, R. B. & Fersht, A. R. (2007). The helix-turn-helix motif as an ultrafast independently folding domain: the pathway of folding of Engrailed homeodomain. Proceedings of the National Academy of Sciences of the United States of America 104, 9272–9277.Google Scholar
Religa, T. L., Markson, J. S., Mayor, U., Freund, S. M. V. & Fersht, A. R. (2005). Solution structure of a protein denatured state and folding intermediate. Nature 437, 1053–1056.Google Scholar
Rhoades, E., Cohen, M., Schuler, B. & Haran, G. (2004). Two-state folding observed in individual protein molecules. Journal of the American Chemical Society 126, 14686–14687.Google Scholar
Robien, M. A., Clore, G. M., Omichinski, J. G., Perham, R. N., Appella, E., Sakaguchi, K. & Gronenborn, A. M. (1992). Three-dimensional solution structure of the E3-binding domain of the dihydrolipoamide succinyltransferase core from the 2-oxoglutarate dehydrogenase multienzyme complex of Escherichia coli. Biochemistry 31, 3463–3471.Google Scholar
Sabelko, J., Ervin, J. & Gruebele, M. (1999). Observation of strange kinetics in protein folding. Proceedings of the National Academy of Sciences of the United States of America 96, 6031–6036.Google Scholar
Sadqi, M., Fushman, D. & Muñoz, V. (2006). Atom-by-atom analysis of global downhill protein folding. Nature 442, 317–321.Google Scholar
Sauer, R. T., Jordan, S. R. & Pabo, C. O. (1990). λ repressor: a model system for understanding protein–DNA interactions and protein stability. Advances in Protein Chemistry 40, 1–61.Google Scholar
Sborgi, L., Verma, A., Munoz, V. & deAlba, E. (2011). Revisiting the NMR structure of the ultrafast downhill folding protein gpW from bacteriophage lambda. PLoS ONE 6, e26409.Google Scholar
Schindelin, H., Marahiel, M. A. & Heinemann, U. (1993). Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364, 164–168.Google Scholar
Schindler, T., Herrler, M., Marahiel, M. A. & Schmid, F. X. (1995). Extremely rapid protein folding in the absence of intermediates. Nature Structural Biology 2, 663–673.Google Scholar
Schuler, B. & Eaton, W. A. (2008). Protein folding by single-molecule FRET. Current Opinion in Structural Biology 18, 16–26.Google Scholar
Schuler, B., Lipman, E. A. & Eaton, W. A. (2002). Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419, 743–747.Google Scholar
Scott, G. & Gruebele, M. (2010). Solving the low dimensional smoluchowski equation with a singular value basis set. Journal of Computational Chemistry 31, 2428–2433.Google Scholar
Sekhar, A. & Kay, L. E. (2013). NMR paves the way for atomic level descriptions of sparsely populated, transiently formed biomolecular conformers. Proceedings of the National Academy of Sciences of the United States of America 110, 12867–12874.Google Scholar
Shah, P. S., Hom, G. K., Ross, S. A., Lassila, J. K., Crowhurst, K. A. & Mayo, S. L. (2007). Full-sequence computational design and solution structure of a thermostable protein variant. Journal of Molecular Biology 372, 1–6.Google Scholar
Shakhnovich, E., Farztdinov, G., Gutin, A. M. & Karplus, M. (1991). Protein folding bottlenecks: a lattice Monte Carlo simulation. Physical Review Letter 67, 1665–1668.Google Scholar
Shastry, M. C. R., Luck, S. D. & Roder, H. (1998). A continuous-flow capillary mixing method to monitor reactions on the microsecond time scale. Biophysical Journal 74, 2714–2721.Google Scholar
Shoemaker, B. A., Portman, J. J. & Wolynes, P. G. (2000). Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proceedings of the National Academy of Sciences of the United States of America 97, 8868–8873.Google Scholar
Snow, C. D., Nguyen, H., Pande, V. S. & Gruebele, M. (2002). Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420, 102–106.Google Scholar
Snow, C. D., Qiu, L., Du, D., Gai, F., Hagen, S. J. & Pande, V. S. (2004). Trp zipper folding kinetics by molecular dynamics and temperature-jump spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 101, 4077–4082.Google Scholar
Socci, N. D. & Onuchic, J. N. (1995). Kinetic and thermodynamic analysis of proteinlike heteropolymers: Monte Carlo histogram technique. Journal of Chemical Physics 103, 4732–4744.Google Scholar
Struthers, M., Ottesen, J. J. & Imperiali, B. (1998). Design and NMR analyses of compact, independently folded BBA motifs. Folding Design 3, 95–103.Google Scholar
Struthers, M. D., Cheng, R. P. & Imperiali, B. (1996). Design of a monomeric 23-residue polypeptide with defined tertiary structure. Science 271, 342–345.Google Scholar
Sugase, K., Dyson, H. J. & Wright, P. E. (2007). Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447, 1021–1025.Google Scholar
Sugita, Y. & Okamoto, Y. (1999). Replica-exchange molecular dynamics method for protein folding. Chemical Physics Letters 314, 141–151.Google Scholar
Takada, S. (2001). Protein folding simulation with solvent-induced force field: folding pathway ensemble of three-helix-bundle proteins. Proteins: Structure, Function, and Bioinformatics 42, 85–98.Google Scholar
Tozzini, V. (2005). Coarse grained models for proteins. Current Opinion in Structural Biology 15, 144–150.Google Scholar
Trizac, E., Levy, Y. & Wolynes, P. G. (2010). Capillarity theory for the fly-casting mechanism. Proceedings of the National Academy of Sciences of the United States of America 107, 2746–2750.Google Scholar
Tuinstra, R. L., Peterson, F. C., Sutlesa, S., Elgin, E. S., Kron, M. A. & Volkman, B. F. (2008). Interconversion between two unrelated protein folds in the lymphotactin native state. Proceedings of the National Academy of Sciences of the United States of America 105, 5057–5062.Google Scholar
Uzawa, T., Nishimura, C., Akiyama, S., Ishimori, K., Takahashi, S., Dyson, H. J. & Wright, P. E. (2008). Hierarchical folding mechanism of apomyoglobin revealed by ultra-fast H/D exchange coupled with 2D NMR. Proceedings of the National Academy of Sciences of the United States of America 105, 13859–13864.Google Scholar
Voelz, V. A., Bowman, G. R., Beauchamp, K. & Pande, V. S. (2010). Molecular simulation of ab initio protein folding for a millisecond folder NTL9(1-39). Journal of the American Chemical Society 132, 1526–1528.Google Scholar
Vu, D. M., Myers, J. K., Oas, T. G. & Dyer, R. B. (2004). Probing the folding and unfolding dynamics of secondary and tertiary structures in a three-helix bundle protein. Biochemistry 43, 3582–3589.Google Scholar
Waldauer, S. A., Bakajin, O., Ball, T., Chen, Y., DeCamp, S. J., Kopka, M., Jager, M., Singh, V. R., Wedemeyer, W. J., Weiss, S., Yao, S. & Lapidus, L. J. (2008). Ruggedness in the folding landscape of protein L. HFSP Journal 2, 388–395.Google Scholar
Walsh, S. T., Cheng, H., Bryson, J. W., Roder, H. & DeGrado, W. F. (1999). Solution structure and dynamics of a de novo designed three-helix bundle protein. Proceedings of the National Academy of Sciences of the United States of America 96, 5486–5491.Google Scholar
Wang, M., Tang, Y., Sato, S., Vugmeyster, L., McKnight, J. C. & Raleigh, D. P. (2003). Dynamic NMR line-shape analysis demonstrates that the vilin headpiece subdomain folds on the microsecond time scale. Journal of the American Chemical Society 125, 6032–6033.Google Scholar
Wang, T., Zhu, Y. & Gai, F. (2004). Folding of a three-helix bundle at the folding speed limit. Journal of Physical Chemistry B 108, 3694–3697.Google Scholar
Williams, S., Causgrove, T. P., Gilmanshin, R., Fang, K. S., Callender, R. H., Woodruff, W. H. & Dyer, R. B. (1996). Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry 35, 691–697.Google Scholar
Yang, W. Y. & Gruebele, M. (2003). Folding at the speed limit. Nature 423, 193–197.Google Scholar
Yang, W. Y. & Gruebele, M. (2004a). Detection-dependent kinetics as a probe of folding landscape microstructure. Journal of the American Chemical Society 126, 7758–7759.CrossRefGoogle ScholarPubMed
Yang, W. Y. & Gruebele, M. (2004b). Folding [lambda]-repressor at its speed limit. Biophysical Journal 87, 596–608.Google Scholar
Yang, W. Y. & Gruebele, M. (2004c). Rate-temperature relationships in lambda-repressor fragment lambda 6–85 folding. Biochemistry 43, 13018–13025.Google Scholar
Yang, W. Y., Pitera, J. W., Swope, W. C. & Gruebele, M. (2004). Heterogeneous folding of the trpzip hairpin: full atom simulation and experiment. Journal of Molecular Biology 336, 241–251.Google Scholar
Zagrovic, B., Snow, C. D., Shirts, M. R. & Pande, V. S. (2002). Simulation of folding of a small alpha-helical protein in atomistic detail using worldwide-distributed computing. Journal of Molecular Biology 323, 927–937.Google Scholar
Zhou, R. H. (2003). Trp-cage: folding free energy landscape in explicit water. Proceedings of the National Academy of Sciences of the United States of America 100, 13280–13285.Google Scholar
Zhu, Y., Alonso, D. O. V., Maki, K., Huang, C.-Y., Lahr, S. J., Daggett, V., Roder, H., DeGrado, W. F. & Gai, F. (2003). Ultrafast folding of α3D: a de novo designed three-helix bundle protein. Proceedings of the National Academy of Sciences of the United States of America 100, 15486–15491.Google Scholar