The DOI matches its Crossref record; 130 of the 130 references it cites were found in a registry or an index.
Funnels, pathways, and the energy landscape of protein folding: A synthesis
Open accessAbstract
The understanding, and even the description of protein folding is impeded by the complexity of the process. Much of this complexity can be described and understood by taking a statistical approach to the energetics of protein conformation, that is, to the energy landscape. The statistical energy landscape approach explains when and why unique behaviors, such as specific folding pathways, occur in some proteins and more generally explains the distinction between folding processes common to all sequences and those peculiar to individual sequences. This approach also gives new, quantitative insights into the interpretation of experiments and simulations of protein folding thermodynamics and kinetics. Specifically, the picture provides simple explanations for folding as a two-state first-order phase transition, for the origin of metastable collapsed unfolded states and for the curved Arrhenius plots observed in both laboratory experiments and discrete lattice simulations. The relation of these quantitative ideas to folding pathways, to uniexponential vs. multiexponential behavior in protein folding experiments and to the effect of mutations on folding is also discussed. The success of energy landscape ideas in protein structure prediction is also described. The use of the energy landscape approach for analyzing data is illustrated with a quantitative analysis of some recent simulations, and a qualitative analysis of experiments on the folding of three proteins. The work unifies several previously proposed ideas concerning the mechanism protein folding and delimits the regions of validity of these ideas under different thermodynamic conditions.
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“The statistical energy landscape theory was developed to study protein folding.1,128–131”
From Protein Ensembles: How Does Nature Harness Thermodynamic Fluctuations for Life? The Diverse Functional Roles of Conformational Ensembles in the Cell (2016) · cites this paper as [129]
In the citing paper
“The minimum frustration principle implies that nature has optimized protein folding,129,174 thus the effect of point mutations on the energy landscape is analogous to thermal perturbations.175”
From Protein Ensembles: How Does Nature Harness Thermodynamic Fluctuations for Life? The Diverse Functional Roles of Conformational Ensembles in the Cell (2016) · cites this paper as [129]
In the citing paper
“Levinthal argued that there is no need to search this vast space since the energy landscape is funnel-like, rather than flat, and thus can guide sampling toward the biological conformational basin.”
From AlphaFold, Artificial Intelligence (AI), and Allostery (2022) · cites this paper as [153]
Citations
Cites
Optimization by Simulated Annealing
Kirkpatrick, S., Gelatt, C. D., & Vecchi, M. P. (1983) · Science · doi:10.1126/science.220.4598.671 · Cited by 45,134 · cited 1×
“If the latter possibility is correct then one approach to predicting structure is simulated annealing [34].”
Background(1979) · Cited by 43,841
Principles of polymer chemistry
(1995) · Choice Reviews Online · doi:10.5860/choice.33-2140 · Cited by 15,292
Spin glasses: Experimental facts, theoretical concepts, and open questions
Binder, K., & Young, A. P. (1986) · Reviews of Modern Physics · doi:10.1103/revmodphys.58.801 · Cited by 5,191
Spin Glass Theory and Beyond: An Introduction to the Replica Method and Its Applications
Mezard, M., Parisi, G., & Virasoro, M. (1986) · World Scientific Lecture Notes in Physics · doi:10.1142/0271 · Cited by 3,653
Lifshitz, E., & LANDAU, L. D. (1958) · Cited by 2,823
Mézard, M., Giorgio Parisi, A., VIRASORO, M. A., & Thouless, D. J. (1988) · Physics Today · doi:10.1063/1.2811676 · Cited by 2,683
Introduction to Protein Structure
Brändén, C.-I., & Tooze, J. (2012) · Garland Science eBooks · doi:10.1201/9781136969898 · Cited by 2,398
Moore, J. W., Pearson, R. G., & Frost, A. A. (1961) · Andalas University Repository (Andalas University) · Cited by 2,342
Stability of Proteins Small Globular Proteins
Privalov, P. L. (1979) · Advances in protein chemistry · doi:10.1016/s0065-3233(08)60460-x · Cited by 2,163 · cited 1×
“The concluding section then summarizes the results, and discusses the significance of the energy landscape for understanding protein folding, for protein structure prediction and for protein engineering.”
Background
Flagged first, then by citations
Research works printed but not linked: 10
- Levinthal C., 1969, Mossbauer Spectroscopy in Biological Systems, 22
- Pauling L. C., 1970, General Chemistry, 381
- Lewis G. N., 1961, Thermodynamics, 138
- Landau L. D., 1980, Statistical Physics, Part I, 531
- Creighton T. E., 1984, Proteins, 231
- Ptitsyn O. B., 1992, Protein Folding, 243
- Glasstone S., 1941, The Theory of Rate Processes
- Leffler J. E., 1963, Rates and Equilibria of Organic Reactions, 156
- Nall B. T., 1990, Protein Folding: Deciphering the Second Half of the Genetic Code, 198
- Nall B. T., 1994, Mechanisms of Protein Folding, 137
Cited by
Sorted by citations
Items 701–800 of 1,005
Statistical Mechanics of the Combinatorial Synthesis and Analysis of Folding Macromolecules
Saven, J. G., & Wolynes, P. G. (1997) · The Journal of Physical Chemistry B · doi:10.1021/jp971707j · Cited by 56
Self-citationBrownian dynamics simulations of protein folding: Access to milliseconds time scale and beyond
Rojnuckarin, A., Kim, S., & Subramaniam, S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4288 · Cited by 56
Reversible Aggregation Plays a Crucial Role on the Folding Landscape of p53 Core Domain
Ishimaru, D., Lima, L. M. T. R., Maia, L. F., Lopez, P. M., Bom, A. P. A., Valente, A. P., & Silva, J. L. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.044685 · Cited by 56
“…essential for directing the protein folding to the native state, or misfolded structures trapped in physiologically nonrelevant local energy minima (Kim and Baldwin, 1990; Bryngelson et al., 1995; Carra and Privalov, 1996; Creighton et al., 1996; Dill and Chan, 1997; Wagner and Kiefhaber, 1999).”
BackgroundDesigning Protein Energy Landscapes
Saven, J. G. (2001) · Chemical Reviews · doi:10.1021/cr000058w · Cited by 56
Schonbrun, J., & Dill, K. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1735417100 · Cited by 55
Sequential vs. parallel protein-folding mechanisms: experimental tests for complex folding reactions
WALLACE, L. A., & Matthews, C. R. (2002) · Biophysical Chemistry · doi:10.1016/s0301-4622(02)00155-2 · Cited by 56
Making connections between ultrafast protein folding kinetics and molecular dynamics simulations
Cellmer, T., Buscaglia, M., Henry, E. R., Hofrichter, J., & Eaton, W. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019552108 · Cited by 55
“In this so-called downhill scenario (44), we would expect to observe probe-dependent kinetics (45, 46).”
BackgroundA Perspective on Deep Learning for Molecular Modeling and Simulations
Zhang, J., Lei, Y.-K., Zhang, Z., Chang, J., Li, M., Han, X., Yang, L., Yang, Y., & Gao, Y. Q. (2020) · The Journal of Physical Chemistry A · doi:10.1021/acs.jpca.0c04473 · Cited by 55
Eastwood, M. P., Hardin, C., Luthey-Schulten, Z. A., & Wolynes, P. G. (2002) · The Journal of Chemical Physics · doi:10.1063/1.1494417 · Cited by 55
Self-citationLarge deviations for multiscale diffusion via weak convergence methods
Dupuis, P. G., & Spiliopoulos, K. (2012) · Stochastic Processes and their Applications · doi:10.1016/j.spa.2011.12.006 · Cited by 55
Fedurco, M., Augustyński, J., Indiani, C., Smulevich, G., Antalı́k, M., Bánó, M., Sedlák, E., Glascock, M. C., & Dawson, J. H. (2004) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2004.09.013 · Cited by 55
Jana, B., Morcos, F., & Onuchic, J. N. (2014) · Physical Chemistry Chemical Physics · doi:10.1039/c3cp55275f · Cited by 55
“(principle of minimal frustration) (4, 13).”
BackgroundSelf-citationThere and back again: Two views on the protein folding puzzle
Finkelstein, A. V., Badretdin, A. J., Galzitskaya, O. V., Ivankov, D. N., Bogatyreva, N. S., & Garbuzynskiy, S. O. (2017) · Physics of Life Reviews · doi:10.1016/j.plrev.2017.01.025 · Cited by 55
Ferguson, A. L. (2017) · Journal of Computational Chemistry · doi:10.1002/jcc.24800 · Cited by 56
Onaran, H., Scheer, A., Cotecchia, S., & Costa, T. (2000) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-57081-0_9 · Cited by 54
Walsh, T. R., & Wales, D. J. (1998) · The Journal of Chemical Physics · doi:10.1063/1.477319 · Cited by 55
On Hydrophobicity Correlations in Protein Chains
Irbäck, A., & Sandelin, E. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76472-1 · Cited by 55
“Most such studies have been directed toward identifying physical characteristics of good folders, and in this important area some progress has been made (Săli et al., 1994; Bryngelson et al., 1995; Klimov and Thirumalai, 1998; Nymeyer et al., 1998).”
BackgroundUversky, V. N. (2013) · Biopolymers · doi:10.1002/bip.22298 · Cited by 56
After Fifty Years, Why Are Protein X-ray Crystallographers Still in Business?
Mitchell, S. D., & Gronenborn, A. M. (2015) · The British Journal for the Philosophy of Science · doi:10.1093/bjps/axv051 · Cited by 54
Sinha, K. K., & Udgaonkar, J. B. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.04.061 · Cited by 53
Exploring one-state downhill protein folding in single molecules
Liu, J., Campos, L. A., Cerminara, M., Wang, X., Ramanathan, R., English, D. S., & Muñoz, V. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111164109 · Cited by 54
“Another important application is the characterization of the downhill folding scenario predicted by energy landscape theory (1).”
BackgroundInfluentialFerguson, A., Liu, Z., & Chan, H. S. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.04.011 · Cited by 54
Perspectives on the simulation of protein–surface interactions using empirical force field methods
Latour, R. A. (2014) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2014.06.050 · Cited by 54
Microsecond folding experiments and simulations: a match is made
Prigozhin, M. B., & Gruebele, M. (2013) · Physical Chemistry Chemical Physics · doi:10.1039/c3cp43992e · Cited by 56
Monitoring protein folding through high pressure NMR spectroscopy
Roche, J., Royer, C. A., & Roumestand, C. (2017) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2017.05.003 · Cited by 53
Mechanism of Solvent Control of Protein Dynamics
Mukherjee, S., Mondal, S., & Bagchi, B. (2019) · Physical Review Letters · doi:10.1103/physrevlett.122.058101 · Cited by 54
Origins of Chevron Rollovers in Non-Two-State Protein Folding Kinetics
Kaya, H., & Chan, H. S. (2003) · Physical Review Letters · doi:10.1103/physrevlett.90.258104 · Cited by 54
Dynamics and thermodynamics of supercooled liquids and glasses from a model energy landscape
Wales, D. J., & Doye, J. P. K. (2001) · Physical review. B, Condensed matter · doi:10.1103/physrevb.63.214204 · Cited by 54
Submicrosecond real-time fluorescence sampling: application to protein folding
Ervin, J., Sabelko, J. J., & Gruebele, M. (2000) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/s1011-1344(00)00002-6 · Cited by 54
Protein folding: bringing theory and experiment closer together
Vendruscolo, M., & Paci, E. (2003) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(03)00007-1 · Cited by 54
Kinetics of proteinlike models: The energy landscape factors that determine folding
Betancourt, M. R., & Onuchic, J. N. (1995) · The Journal of Chemical Physics · doi:10.1063/1.470109 · Cited by 54
Self-citationApaydın, M. S., Brutlag, D. L., Guestrin, C., Hsu, D., & Latombe, J. (2002) · doi:10.1145/565196.565199 · Cited by 54
The anatomy of protein β-sheet topology 1 1Edited by J. Thornton
Zhang, C., & Kim, S. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3678 · Cited by 55
Fast protein folding is governed by memory-dependent friction
Dalton, B. A., Ayaz, C., Kiefer, H., Klimek, A., Tepper, L., & Netz, R. R. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2220068120 · Cited by 57
Tzul, F. O., Schweiker, K. L., & Makhatadze, G. I. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1410424112 · Cited by 53
Gianni, S., Camilloni, C., Giri, R., Toto, A., Bonetti, D., Morrone, A., Sormanni, P., Brunori, M., & Vendruscolo, M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405233111 · Cited by 53
“The free energy landscape of proteins tends to exhibit a strong bias toward the native states (2, 4, 5).”
BackgroundJarmolinska, A. I., Perlinska, A. P., Runkel, R., Trefz, B., Ginn, H. M., Virnau, P., & Sulkowska, J. I. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.10.012 · Cited by 53
Searching the landscape of flux vacua with genetic algorithms
Cole, A., Schachner, A., & Shiu, G. (2019) · OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) · doi:10.17863/cam.79204 · Cited by 59
Ma, B., Guo, J., & Zhang, H. (2006) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21140 · Cited by 51
Zhou, Y., Zhang, C., Stell, G. R., & Wang, J. (2003) · Journal of the American Chemical Society · doi:10.1021/ja029855x · Cited by 53
Nonatomic solvent‐driven voronoi tessellation of proteins: An open tool to analyze protein folds
Angelov, B., Sadoc, J.-F., Jullien, R., Soyer, A., Mornon, J., & Chomilier, J. (2002) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.10220 · Cited by 54
Taddei, N., Chiti, F., Fiaschi, T., Bucciantini, M., Capanni, C., Stefani, M., Serrano, L., Dobson, C. M., & Ramponi, G. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3870 · Cited by 53
Is Protein Folding a Thermodynamically Unfavorable, Active, Energy-Dependent Process?
Sorokina, I., Mushegian, A. R., & Koonin, E. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23010521 · Cited by 50
Makarov, D. E. (2013) · The Journal of Chemical Physics · doi:10.1063/1.4773283 · Cited by 52
Laederach, A., Shcherbakova, I., Jonikas, M. A., Altman, R. B., & Brenowitz, M. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608765104 · Cited by 52
Zhao, F., & Xu, J. (2012) · Structure · doi:10.1016/j.str.2012.04.003 · Cited by 52
“, 1997; Sippl, 1990; Tanaka and Scheraga, 1976; Zhang and Zhang, 2010; Zhou and Zhou, 2002) compare favorably to physics-based potentials (Brooks et al., 2009; Bryngelson et al., 1995; Case et al., 2005; Dill, 1985, 1997; Dobson et al., 1998; Schuler et al., 2001; Shakhnovich, 2006) in many applications including ab i…”
BackgroundHaenni, D., Zosel, F., Reymond, L., Nettels, D., & Schuler, B. (2013) · The Journal of Physical Chemistry B · doi:10.1021/jp402352s · Cited by 52
McMorran, L. M., Brockwell, D. J., & Radford, S. E. (2014) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2014.02.011 · Cited by 51
Naganathan, A. N. (2012) · Journal of Chemical Theory and Computation · doi:10.1021/ct300676w · Cited by 52
Schönfelder, J., Pérez‐Jiménez, R., & Muñoz, V. (2016) · Nature Communications · doi:10.1038/ncomms11777 · Cited by 52
“rotein folding can be portrayed as the diffusive search for the biologically functional three-dimensional structure on a corrugated folding free-energy landscape (FFEL) that has an overall funneled shape towards the native state 1 .”
Lee, C.-L., Lin, C.-T., Stell, G. R., & Wang, J. (2003) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.67.041905 · Cited by 52
Temperature control for kinetic refolding of heat‐denatured ovalbumin
Tani, F., Shirai, N., Venelle, F., YASUMOTO, K., Onishi, T., & Doi, E. (1997) · Protein Science · doi:10.1002/pro.5560060713 · Cited by 52
“Folding kinetics of heat-denatured ovalbumin can be described in terms of a rugged energy landscape on the basis of statistical mechanical theories and Monte Carlo simulations of protein folding (Bryngelson et al., 1995; Dill et al., 1995; Wolynes et al., 1995).”
BackgroundClementi, C., Maritan, A., & Banavar, J. R. (1998) · Physical Review Letters · doi:10.1103/physrevlett.81.3287 · Cited by 52
Arrington, C. B., & Robertson, A. D. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3859 · Cited by 53
Exact dynamical coarse-graining without time-scale separation
Lu, J., & Vanden‐Eijnden, E. (2014) · The Journal of Chemical Physics · doi:10.1063/1.4890367 · Cited by 52
Understanding the mechanism of β‐sheet folding from a chemical and biological perspective
Jäger, M., Deechongkit, S., Koepf, E. K., Nguyen, H., Gao, J., Powers, E. T., Gruebele, M., & Kelly, J. W. (2008) · Biopolymers · doi:10.1002/bip.21101 · Cited by 51
A Molecular Interpretation of 2D IR Protein Folding Experiments with Markov State Models
Baiz, C. R., Lin, Y.-S., Peng, C. S., Beauchamp, K. A., Voelz, V. A., Pande, V. S., & Tokmakoff, A. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2014.02.008 · Cited by 51
A coarse‐grained α‐carbon protein model with anisotropic hydrogen‐bonding
Yap, E.-H., Fawzi, N. L., & Head-Gordon, T. L. (2007) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21515 · Cited by 51
Assessment of ab initio models of protein complexes by molecular dynamics
Radom, F., Plückthun, A., & Paci, E. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006182 · Cited by 47
Polarizable and non-polarizable force fields: Protein folding, unfolding, and misfolding
Kamenik, A. S., Handle, P. H., Hofer, F., Kahler, U., Kraml, J., & Liedl, K. R. (2020) · The Journal of Chemical Physics · doi:10.1063/5.0022135 · Cited by 50
Nonmonotonic relaxation kinetics of confined systems
Ryabov, Y., Puzenko, A. A., & Feldman, Y. D. (2004) · Physical Review B · doi:10.1103/physrevb.69.014204 · Cited by 51
Transmembrane Helices Have Rough Energy Surfaces
Janovjak, H., Knaus, H., & Müller, D. J. (2006) · Journal of the American Chemical Society · doi:10.1021/ja065684a · Cited by 51
A common folding mechanism in the cytochrome family
Travaglini‐Allocatelli, C., Gianni, S., & Brunori, M. (2004) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2004.08.004 · Cited by 51
Finite Size Effects on Thermal Denaturation of Globular Proteins
Li, M. S., Klimov, D. K., & Thirumalai, D. (2004) · Physical Review Letters · doi:10.1103/physrevlett.93.268107 · Cited by 51
Pokarowski, P., Koliński, A., & Skolnick, J. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74964-9 · Cited by 51
“The purpose of the rigorous math-type definition of the model is to provide a convenient and precise notation for the following section, where the model’s energy landscape (Bryngelson et al., 1995; Onuchic et al., 1997) is analyzed in considerable detail.”
BackgroundExponential decay kinetics in “downhill” protein folding
Hagen, S. J. (2002) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.10261 · Cited by 51
Chu, X., Liu, F., Maxwell, B. A., Wang, Y., Suo, Z., Wang, H., Han, W., & Wang, J. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003804 · Cited by 51
“Certain types of SBM, satisfying the principle of minimally frustrated energy landscapes [43,44], have been used to study biomolecular folding and binding transitions toward formation of the unique native structure [45–49].”
BackgroundGhosh, R., Roy, S., & Bagchi, B. (2013) · The Journal of Physical Chemistry B · doi:10.1021/jp406255z · Cited by 50
Advances on protein folding simulations based on the lattice HP models with natural computing
Zhao, X. (2007) · Applied Soft Computing · doi:10.1016/j.asoc.2007.03.012 · Cited by 50
Free Energy of Membrane Protein Unfolding Derived from Single-Molecule Force Measurements
Preiner, J., Janovjak, H., Rankl, C., Knaus, H., Cisneros, D. A., Kedrov, A., Kienberger, F., Müller, D. J., & Hinterdorfer, P. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.096982 · Cited by 50
“3 which inherently probe the average behavior of large numbers of molecules, singlemolecule experiments detect co-existing unfolding pathways and non-accumulative folding intermediates that are populated in multi-dimensional energy landscapes and folding funnels (19-22).”
BackgroundThe structural basis for cancer treatment decisions
Nussinov, R., Jang, H., & Tsai, C. (2014) · Oncotarget · doi:10.18632/oncotarget.2439 · Cited by 51
Deacon, O. M., Karsisiotis, A. I., Chicano, T. M., Hough, M. A., Macdonald, C., Blumenschein, T. M. A., Wilson, M. T., Moore, G. R., & Worrall, J. A. R. (2017) · Biochemistry · doi:10.1021/acs.biochem.7b00890 · Cited by 51
Massimi, M., & McCoy, C. D. (2019) · Routledge eBooks · doi:10.4324/9781315145198 · Cited by 65
Kim, T. W., Lee, S. J., Jo, J., Kim, J. G., Ki, H., Kim, C. W., Cho, K. H., Choi, J., Lee, J. H., Wulff, M., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913442117 · Cited by 49
“Among various conceptual frameworks, it has been suggested that the funnel-like free-energy landscape with many microstates is a scheme pertinent to describing the protein folding (3, 4, 7, 10 – 12).”
Interdomain Contacts Control Native State Switching of RfaH on a Dual-Funneled Landscape
Ramírez‐Sarmiento, C. A., Noel, J. K., Valenzuela, S. L., & Artsimovitch, I. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004379 · Cited by 50
“Since then, several experimental [2,3] and theoretical approaches [4,5] have deepened our understanding of the energy landscape that guides a protein to its unique, thermodynamically-stable three-dimensional structure, the so-called native state, required to carry out its biological function [6].”
BackgroundMethodProtein folding by motion planning
Thomas, S., Song, G., & Amato, N. M. (2005) · Physical Biology · doi:10.1088/1478-3975/2/4/s09 · Cited by 50
Wallin, S., & Chan, H. S. (2006) · Journal of Physics Condensed Matter · doi:10.1088/0953-8984/18/14/s14 · Cited by 51
Computational protein folding: From lattice to all-atom
Duan, Y., & Kollman, P. A. (2001) · IBM Systems Journal · doi:10.1147/sj.402.0297 · Cited by 50
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Brun, L., Isom, D. G., Velu, P., García‐Moreno, B. E., & Royer, C. A. (2006) · Biochemistry · doi:10.1021/bi052638z · Cited by 50
“The kinetic and energetic basis of pressure-induced protein unfolding has also been analyzed previously (59) with energy landscape theory of protein folding (60), using a square well potential that includes a desolvation barrier (61;62).”
BackgroundCompetition between protein folding and aggregation: A three-dimensional lattice-model simulation
Bratko, D., & Blanch, H. W. (2001) · The Journal of Chemical Physics · doi:10.1063/1.1330212 · Cited by 50
Bu, Z., Cook, J. C., & Callaway, D. J. E. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.5006 · Cited by 50
“( 2 ) When QRg > 1, the chain dynamics follows the (Rouse-Zimm model): ˇ/ Q4 (Rouse model) due to the polymer chain conformation entropy effect, and when long-range intramolecular interactions are absent.26 Zimm has made a correction for a random coil with long-range hydrodynamic interactions in a dilute solution:27 ˇ…”
BackgroundMethodModern Kinetics and Mechanism of Protein Folding: A Retrospective
Eaton, W. A. (2021) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.1c00206 · Cited by 49
The ribosome stabilizes partially folded intermediates of a nascent multi-domain protein
Chan, S. H. S., Włodarski, T., Streit, J. O., Cassaignau, A. M. E., Woodburn, L. F., Ahn, M., von Sass, G. J. F., Waudby, C. A., Budiša, N., Cabrita, L. D., et al. (2022) · Nature Chemistry · doi:10.1038/s41557-022-01004-0 · Cited by 49
“…contacts used in structure-based potential as the only attractive non-bonded interactions that drive protein folding based on the principle of minimal frustration 57 , and which were defined based on the FLN5 crystal structure using the OV+rCSU method 58 and modelled with Lennard-Jones potential.”
Hsieh, M., & Luo, R. (2004) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.20133 · Cited by 49
“that a loss of entropy is usually associated with protein folding.(57,58) Thus, a failure of this type of model in discriminating a native structure usually means either the scoring function is not perfect or the model of the native state is poorly defined.”
BackgroundProtein unfolding mechanisms and their effects on folding experiments
Lapidus, L. J. (2017) · F1000Research · doi:10.12688/f1000research.12070.1 · Cited by 49
Is Poisson-Boltzmann theory insufficient for protein folding simulations?
Lwin, T. Z., Zhou, R., & Luo, R. (2006) · The Journal of Chemical Physics · doi:10.1063/1.2161202 · Cited by 50
Day, R. J., & Daggett, V. (2005) · Protein Science · doi:10.1110/ps.041226005 · Cited by 49
“…to enter a barrierless unfolding regime in which Equation 1 no longer holds; there is only one significantly populated state, and the rate of unfolding is determined by the local features of the free energy landscape as the protein diffuses toward this unfolded state (Bryngelson et al. 1995).”
BackgroundMukherjee, A., & Bagchi, B. (2003) · The Journal of Chemical Physics · doi:10.1063/1.1542599 · Cited by 49
Native States of Fast-Folding Proteins Are Kinetic Traps
Dickson, A., & Brooks, C. L. (2013) · Journal of the American Chemical Society · doi:10.1021/ja311077u · Cited by 47
Protein folding as an evolutionary process
Sharma, V., Kaila, V. R. I., & Annila, A. (2008) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2008.12.004 · Cited by 48
Chung, H. S., Cellmer, T., Louis, J. M., & Eaton, W. A. (2012) · Chemical Physics · doi:10.1016/j.chemphys.2012.08.005 · Cited by 48
“One such system is protein folding, in which theory predicts many different sequences of structural changes in the pathways that connect the folded and unfolded states [1].”
BackgroundMicrosecond Barrier-Limited Chain Collapse Observed by Time-Resolved FRET and SAXS
Kathuria, S. V., Kayatekin, C., Barrea, R. A., Kondrashkina, E., Graceffa, R., Guo, L., Nobrega, R. P., Chakravarthy, S., Matthews, C. R., Irving, T. C., et al. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.02.020 · Cited by 48
“The physical origin of the barrier in cytochrome c may arise from the reduction in conformational entropy [52,53], electrostatics [24,54], bond rotations [55] and desolvation [56] in the transition state.”
Yang, S., Levine, H., & Onuchic, J. N. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.06.062 · Cited by 50
Self-citationSisan, D. R., Halter, M. W., Hubbard, J. B., & Plant, A. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207544109 · Cited by 49
Dąbrowski-Tumański, P., Piejko, M., Niewieczerzał, S., Stasiak, A., & Sulkowska, J. I. (2018) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.8b07634 · Cited by 48
Silva, J. L., Cordeiro, Y., & Foguel, D. (2005) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2005.11.012 · Cited by 48
Fee, J. A., Chen, Y., Todaro, T. R., Bren, K. L., Patel, K. M., Hill, M. G., Gomez-Moran, E., Loehr, T. M., Ai, J., Thöny‐Meyer, L., et al. (2000) · Protein Science · doi:10.1110/ps.9.11.2074 · Cited by 48
“…of considerable interest as objects in the study of electron transfer reactions~Ferguson-Miller et al., 1979; Pan et al., 1993; Bjerrum et al., 1995; Geren et al., 1995; Winkler et al., 1995! and of protein folding~Sosnick et al., 1994; Bryngelson et al., 1995; Mines et al., 1996; Bai, 1999!.”
BackgroundValidity of Gō Models: Comparison with a Solvent-Shielded Empirical Energy Decomposition
Paci, E., Vendruscolo, M., & Karplus, M. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)75308-3 · Cited by 48
“Considerable progress has been made in achieving an understanding of the folding reaction by the use of simplified models (Bryngelson et al., 1995; Chan and Dill, 1998; Dinner et al., 2000).”
BackgroundIntrinsically disordered proteins: Ensembles at the limits of Anfinsen's dogma
Kulkarni, P., Leite, V. B. P., Roy, S., Bhattacharyya, S., Mohanty, A. R., Achuthan, S., Singh, D., Appadurai, R., Govindan Rangarajan, C., Weninger, K., et al. (2022) · Biophysics Reviews · doi:10.1063/5.0080512 · Cited by 49
Self-citationThe Folding Energy Landscape and Free Energy Excitations of Cytochrome c
Weinkam, P., Zimmermann, J., Romesberg, F. E., & Wolynes, P. G. (2010) · Accounts of Chemical Research · doi:10.1021/ar9002703 · Cited by 47
Self-citation
Metadata
- Authors
- Bryngelson, J. D., Onuchic, J. N., Socci, N. D., & Wolynes, P. G.
- Affiliations
- National Institutes of Health (US)
- University of California San Diego (US)
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Bryngelson, Joseph D.
- Venue
- Proteins: Structure, Function, and Bioinformatics
- Publisher
- Wiley
- Published
- 1995-03
- Volume
- 21
- Issue
- 3
- Pages
- 167-195
- ISSN
- 0887-3585 (ISSN-L)
- 1097-0134
- OpenAlex
- W2171755502
- Cited by
- 2,648
- References
- 130
- Citations by year
- 2026: 41 · 2025: 58 · 2024: 54 · 2023: 54 · 2022: 86 · 2021: 86 · 2020: 78 · 2019: 72 · 2018: 110 · 2017: 92 · 2016: 104 · 2015: 90 · 2014: 104 · 2013: 123 · 2012: 107
- FWCI
- 32.88
- Type
- journal article
- Language
- en
- Open access
- green
- arxiv.org
- Locations
- Proteins Structure Function and Bioinformatics (publishedVersion)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- arXiv (Cornell University)
- Funders
- National Institute of General Medical Sciences (1R01 GM44557, R01GM044557)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein purification and stability
- Keywords
- protein folding, energy landscape, folding funnel, folding pathways, Arrhenius plot, folding kinetics, folding thermodynamics, protein structure prediction, lattice simulation
- MeSH terms
- Amino Acid Sequence, Chemistry, Physical, Computer Simulation, Data Interpretation, Statistical, Kinetics, Models, Chemical, Molecular Sequence Data, Protein Conformation, Proteins, Thermodynamics, Protein Biosynthesis, Protein Folding, Chemical Phenomena
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