Unfolded states under folding conditions accommodate sequence-specific conformational preferences with random coil-like dimensions

Peran, Ivan; Holehouse, Alex S.; Carrico, Isaac S.; Pappu, Rohit V.; Bilsel, Osman; Raleigh, Daniel P.

doi:10.1073/pnas.1818206116

Title: Unfolded states under folding conditions accommodate sequence-specific conformational preferences with random coil-like dimensions

Journal Article · Wed Jun 05 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1818206116· OSTI ID:1545860

Peran, Ivan ^[1];

^[2]; Carrico, Isaac S. ^[1];

^[2]; Bilsel, Osman ^[3]; Raleigh, Daniel P. ^[4]

Stony Brook Univ., NY (United States). Dept. of Chemistry
Washington Univ., St. Louis, MO (United States)
Univ. of Massachusetts, Worcester, MA (United States)
Stony Brook Univ., NY (United States). Dept. of Chemistry; Univ. College London (United Kingdom)

Proteins are marginally stable molecules that fluctuate between folded and unfolded states. Here, we provide a high-resolution description of unfolded states under refolding conditions for the N-terminal domain of the L9 protein (NTL9). We use a combination of time-resolved Förster resonance energy transfer (FRET) based on multiple pairs of minimally perturbing labels, time-resolved small-angle X-ray scattering (SAXS), all-atom simulations, and polymer theory. Upon dilution from high denaturant, the unfolded state undergoes rapid contraction. Although this contraction occurs before the folding transition, the unfolded state remains considerably more expanded than the folded state and accommodates a range of local and nonlocal contacts, including secondary structures and native and nonnative interactions. Paradoxically, despite discernible sequence-specific conformational preferences, the ensemble-averaged properties of unfolded states are consistent with those of canonical random coils, namely polymers in indifferent (theta) solvents. These findings are concordant with theoretical predictions based on coarse-grained models and inferences drawn from single-molecule experiments regarding the sequence-specific scaling behavior of unfolded proteins under folding conditions.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1545860

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, Issue 25; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 36 works

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References (114)

Single-Molecule Studies of Intrinsically Disordered Proteins Brucale, Marco; Schuler, Benjamin; Samorì, Bruno Chemical Reviews, Vol. 114, Issue 6 https://doi.org/10.1021/cr400297g	journal	January 2014
Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water Riback, Joshua A.; Bowman, Micayla A.; Zmyslowski, Adam M. Science, Vol. 358, Issue 6360 https://doi.org/10.1126/science.aan5774	journal	October 2017
Comment on “Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water” Fuertes, Gustavo; Banterle, Niccolo; Ruff, Kiersten M. Science, Vol. 361, Issue 6405 https://doi.org/10.1126/science.aau8230	journal	August 2018
Structural origin of slow diffusion in protein folding Chung, H. S.; Piana-Agostinetti, S.; Shaw, D. E. Science, Vol. 349, Issue 6255 https://doi.org/10.1126/science.aab1369	journal	September 2015
How Fast-Folding Proteins Fold Lindorff-Larsen, K.; Piana, S.; Dror, R. O. Science, Vol. 334, Issue 6055 https://doi.org/10.1126/science.1208351	journal	October 2011
Single-Molecule FRET Spectroscopy and the Polymer Physics of Unfolded and Intrinsically Disordered Proteins Schuler, Benjamin; Soranno, Andrea; Hofmann, Hagen Annual Review of Biophysics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-biophys-062215-010915	journal	July 2016
Protein-folding dynamics Karplus, Martin; Weaver, David L. Nature, Vol. 260, Issue 5550 https://doi.org/10.1038/260404a0	journal	April 1976
Quantitative Assessments of the Distinct Contributions of Polypeptide Backbone Amides versus Side Chain Groups to Chain Expansion via Chemical Denaturation Holehouse, Alex S.; Garai, Kanchan; Lyle, Nicholas Journal of the American Chemical Society, Vol. 137, Issue 8 https://doi.org/10.1021/ja512062h	journal	February 2015
Charge interactions can dominate the dimensions of intrinsically disordered proteins Muller-Spath, S.; Soranno, A.; Hirschfeld, V. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1001743107	journal	July 2010
Expanding the Genetic code Wang, Lei; Xie, Jianming; Schultz, Peter G. Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.biophys.35.101105.121507	journal	June 2006
Polymer Principles in Protein Structure and Stability Chan, H. S.; Dill, K. A. Annual Review of Biophysics and Biophysical Chemistry, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.bb.20.060191.002311	journal	June 1991
Semiflexible chains under tension Ha, B. -Y.; Thirumalai, D. The Journal of Chemical Physics, Vol. 106, Issue 10 https://doi.org/10.1063/1.473128	journal	March 1997
Decoupling of size and shape fluctuations in heteropolymeric sequences reconciles discrepancies in SAXS vs. FRET measurements Fuertes, Gustavo; Banterle, Niccolò; Ruff, Kiersten M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 31 https://doi.org/10.1073/pnas.1704692114	journal	July 2017
Asymmetry in the Shapes of Folded and Denatured States of Proteins ^† Dima, Ruxandra I.; Thirumalai, D. The Journal of Physical Chemistry B, Vol. 108, Issue 21 https://doi.org/10.1021/jp037128y	journal	May 2004
Response to Comment on “Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water” Riback, Joshua A.; Bowman, Micayla A.; Zmyslowski, Adam Science, Vol. 361, Issue 6405 https://doi.org/10.1126/science.aar7949	journal	August 2018
Random-coil behavior and the dimensions of chemically unfolded proteins Kohn, J. E.; Millett, I. S.; Jacob, J. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0403643101	journal	August 2004
Clusters of isoleucine, leucine, and valine side chains define cores of stability in high-energy states of globular proteins: Sequence determinants of structure and stability: BASiC Clusters-Stability Cores of Proteins Kathuria, Sagar V.; Chan, Yvonne H.; Nobrega, R. Paul Protein Science, Vol. 25, Issue 3 https://doi.org/10.1002/pro.2860	journal	December 2015
Modeling the role of disulfide bonds in protein folding: Entropic barriers and pathways Camacho, Carlos J.; Thirumalai, D. Proteins: Structure, Function, and Genetics, Vol. 22, Issue 1 https://doi.org/10.1002/prot.340220105	journal	May 1995
How, when and why proteins collapse: the relation to folding Haran, Gilad Current Opinion in Structural Biology, Vol. 22, Issue 1 https://doi.org/10.1016/j.sbi.2011.10.005	journal	February 2012
Small-Angle X-ray Scattering of Reduced Ribonuclease A: Effects of Solution Conditions and Comparisons with a Computational Model of Unfolded Proteins Wang, Yuanyuan; Trewhella, Jill; Goldenberg, David P. Journal of Molecular Biology, Vol. 377, Issue 5 https://doi.org/10.1016/j.jmb.2008.02.009	journal	April 2008
Natively unfolded proteins: A point where biology waits for physics Uversky, V. N. Protein Science, Vol. 11, Issue 4 https://doi.org/10.1110/ps.4210102	journal	April 2002
A quantitative measure for protein conformational heterogeneity Lyle, Nicholas; Das, Rahul K.; Pappu, Rohit V. The Journal of Chemical Physics, Vol. 139, Issue 12 https://doi.org/10.1063/1.4812791	journal	September 2013
The Amyloid State of Proteins in Human Diseases Eisenberg, David; Jucker, Mathias Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.02.022	journal	March 2012
Crystal structure of prokaryotic ribosomal protein L9: a bi-lobed RNA-binding protein. Hoffman, D. W.; Davies, C.; Gerchman, S. E. The EMBO Journal, Vol. 13, Issue 1 https://doi.org/10.1002/j.1460-2075.1994.tb06250.x	journal	January 1994
A Rigorous and Efficient Method To Reweight Very Large Conformational Ensembles Using Average Experimental Data and To Determine Their Relative Information Content Leung, Hoi Tik Alvin; Bignucolo, Olivier; Aregger, Regula Journal of Chemical Theory and Computation, Vol. 12, Issue 1 https://doi.org/10.1021/acs.jctc.5b00759	journal	December 2015
SAXS versus FRET: A Matter of Heterogeneity? Ruff, Kiersten M.; Holehouse, Alex S. Biophysical Journal, Vol. 113, Issue 5 https://doi.org/10.1016/j.bpj.2017.07.024	journal	September 2017
Conformational Heterogeneity and FRET Data Interpretation for Dimensions of Unfolded Proteins Song, Jianhui; Gomes, Gregory-Neal; Shi, Tongfei Biophysical Journal, Vol. 113, Issue 5 https://doi.org/10.1016/j.bpj.2017.07.023	journal	September 2017
Collapse Precedes Folding in Denaturant-Dependent Assembly of Ubiquitin Reddy, Govardhan; Thirumalai, D. The Journal of Physical Chemistry B, Vol. 121, Issue 5 https://doi.org/10.1021/acs.jpcb.6b13100	journal	January 2017
Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy Hofmann, H.; Soranno, A.; Borgia, A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 40 https://doi.org/10.1073/pnas.1207719109	journal	September 2012
Global analysis of the effects of temperature and denaturant on the folding and unfolding kinetics of the N-terminal domain of the protein L9 1 1Edited by P. E. Wright Kuhlman, Brian; Luisi, Donna L.; Evans, Philip A. Journal of Molecular Biology, Vol. 284, Issue 5 https://doi.org/10.1006/jmbi.1998.2246	journal	December 1998
Proline-Rich Salivary Proteins Have Extended Conformations Boze, Hélène; Marlin, Thérèse; Durand, Dominique Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.04.050	journal	July 2010
Early Events in Protein Folding Explored by Rapid Mixing Methods Roder, Heinrich; Maki, Kosuke; Cheng, Hong Chemical Reviews, Vol. 106, Issue 5 https://doi.org/10.1021/cr040430y	journal	May 2006
Specific collapse followed by slow hydrogen-bond formation of -sheet in the folding of single-chain monellin Kimura, T.; Uzawa, T.; Ishimori, K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 8 https://doi.org/10.1073/pnas.0407982102	journal	February 2005
Dominant forces in protein folding Dill, Ken A. Biochemistry, Vol. 29, Issue 31 https://doi.org/10.1021/bi00483a001	journal	August 1990
The Protein-Folding Problem, 50 Years On Dill, K. A.; MacCallum, J. L. Science, Vol. 338, Issue 6110 https://doi.org/10.1126/science.1219021	journal	November 2012
How fast is protein hydrophobic collapse? Sadqi, M.; Lapidus, L. J.; Munoz, V. Proceedings of the National Academy of Sciences, Vol. 100, Issue 21 https://doi.org/10.1073/pnas.2033863100	journal	October 2003
Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering Tria, Giancarlo; Mertens, Haydyn D. T.; Kachala, Michael IUCrJ, Vol. 2, Issue 2 https://doi.org/10.1107/S205225251500202X	journal	February 2015
p K _a Values and the pH Dependent Stability of the N-Terminal Domain of L9 as Probes of Electrostatic Interactions in the Denatured State. Differentiation between Local and Nonlocal Interactions ^† Kuhlman, Brian; Luisi, Donna L.; Young, Paul Biochemistry, Vol. 38, Issue 15 https://doi.org/10.1021/bi982931h	journal	April 1999
Relating sequence encoded information to form and function of intrinsically disordered proteins Das, Rahul K.; Ruff, Kiersten M.; Pappu, Rohit V. Current Opinion in Structural Biology, Vol. 32 https://doi.org/10.1016/j.sbi.2015.03.008	journal	June 2015
Polypeptide chain collapse and protein folding Udgaonkar, Jayant B. Archives of Biochemistry and Biophysics, Vol. 531, Issue 1-2 https://doi.org/10.1016/j.abb.2012.10.003	journal	March 2013
The effects of nonnative interactions on protein folding rates: Theory and simulation Clementi, Cecilia; Plotkin, Steven S. Protein Science, Vol. 13, Issue 7 https://doi.org/10.1110/ps.03580104	journal	July 2004
Coil-globule transition in the denatured state of a small protein Sherman, E.; Haran, G. Proceedings of the National Academy of Sciences, Vol. 103, Issue 31 https://doi.org/10.1073/pnas.0601395103	journal	July 2006
Conformational Distribution of a 14-Residue Peptide in Solution: A Fluorescence Resonance Energy Transfer Study Tucker, Matthew J.; Oyola, Rolando; Gai, Feng The Journal of Physical Chemistry B, Vol. 109, Issue 10 https://doi.org/10.1021/jp044347q	journal	March 2005
Microsecond Barrier-Limited Chain Collapse Observed by Time-Resolved FRET and SAXS Kathuria, Sagar V.; Kayatekin, Can; Barrea, Raul Journal of Molecular Biology, Vol. 426, Issue 9 https://doi.org/10.1016/j.jmb.2014.02.020	journal	May 2014
Commonly used FRET fluorophores promote collapse of an otherwise disordered protein Riback, Joshua A.; Bowman, Micayla A.; Zmyslowski, Adam M. Proceedings of the National Academy of Sciences, Vol. 116, Issue 18 https://doi.org/10.1073/pnas.1813038116	journal	April 2019
Non-native interactions play an effective role in protein folding dynamics: Non-Native Interactions in Protein Folding Faísca, Patrícia F. N.; Nunes, Ana; Travasso, Rui D. M. Protein Science, Vol. 19, Issue 11 https://doi.org/10.1002/pro.498	journal	October 2010
Factors governing the foldability of proteins Klimov, D. K.; Thirumalai, D. Proteins: Structure, Function, and Genetics, Vol. 26, Issue 4 https://doi.org/10.1002/(SICI)1097-0134(199612)26:4<411::AID-PROT4>3.0.CO;2-E	journal	December 1996
A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins Kikhney, Alexey G.; Svergun, Dmitri I. FEBS Letters, Vol. 589, Issue 19PartA https://doi.org/10.1016/j.febslet.2015.08.027	journal	August 2015
Direct observation of barrier-limited folding of BBL by single-molecule fluorescence resonance energy transfer Huang, F.; Ying, L.; Fersht, A. R. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0909126106	journal	September 2009
Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Schuler, Benjamin; Lipman, Everett A.; Eaton, William A. Nature, Vol. 419, Issue 6908 https://doi.org/10.1038/nature01060	journal	October 2002
Collapse Transitions of Proteins and the Interplay Among Backbone, Sidechain, and Solvent Interactions Holehouse, Alex S.; Pappu, Rohit V. Annual Review of Biophysics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-biophys-070317-032838	journal	May 2018
Monomeric Huntingtin Exon 1 Has Similar Overall Structural Features for Wild-Type and Pathological Polyglutamine Lengths Warner, John B.; Ruff, Kiersten M.; Tan, Piau Siong Journal of the American Chemical Society, Vol. 139, Issue 41 https://doi.org/10.1021/jacs.7b06659	journal	October 2017
Microsecond acquisition of heterogeneous structure in the folding of a TIM barrel protein Wu, Y.; Kondrashkina, E.; Kayatekin, C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 36 https://doi.org/10.1073/pnas.0802788105	journal	August 2008
Consistent View of Polypeptide Chain Expansion in Chemical Denaturants from Multiple Experimental Methods Borgia, Alessandro; Zheng, Wenwei; Buholzer, Karin Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b05917	journal	September 2016
Intrinsically unstructured proteins and their functions Dyson, H. Jane; Wright, Peter E. Nature Reviews Molecular Cell Biology, Vol. 6, Issue 3 https://doi.org/10.1038/nrm1589	journal	March 2005
How accurate are polymer models in the analysis of Förster resonance energy transfer experiments on proteins? O’Brien, Edward P.; Morrison, Greg; Brooks, Bernard R. The Journal of Chemical Physics, Vol. 130, Issue 12 https://doi.org/10.1063/1.3082151	journal	March 2009
Dissecting the Non-specific and Specific Components of the Initial Folding Reaction of Barstar by Multi-site FRET Measurements Sinha, Kalyan K.; Udgaonkar, Jayant B. Journal of Molecular Biology, Vol. 370, Issue 2 https://doi.org/10.1016/j.jmb.2007.04.061	journal	July 2007
Early Collapse is not an Obligate Step in Protein Folding Jacob, Jaby; Krantz, Bryan; Dothager, Robin S. Journal of Molecular Biology, Vol. 338, Issue 2 https://doi.org/10.1016/j.jmb.2004.02.065	journal	April 2004
Quantifying internal friction in unfolded and intrinsically disordered proteins with single-molecule spectroscopy Soranno, A.; Buchli, B.; Nettels, D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1117368109	journal	April 2012
The folding of single domain proteins—have we reached a consensus? Sosnick, Tobin R.; Barrick, Doug Current Opinion in Structural Biology, Vol. 21, Issue 1 https://doi.org/10.1016/j.sbi.2010.11.002	journal	February 2011
Coordinate-dependent diffusion in protein folding Best, R. B.; Hummer, G. Proceedings of the National Academy of Sciences, Vol. 107, Issue 3 https://doi.org/10.1073/pnas.0910390107	journal	December 2009
Collapse of a polymer chain in poor solvents De Gennes, P. G. Journal de Physique Lettres, Vol. 36, Issue 3 https://doi.org/10.1051/jphyslet:0197500360305500	journal	January 1975
Sequence Determinants of the Conformational Properties of an Intrinsically Disordered Protein Prior to and upon Multisite Phosphorylation Martin, Erik W.; Holehouse, Alex S.; Grace, Christy R. Journal of the American Chemical Society, Vol. 138, Issue 47 https://doi.org/10.1021/jacs.6b10272	journal	November 2016
Comment on “Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water” Best, Robert B.; Zheng, Wenwei; Borgia, Alessandro Science, Vol. 361, Issue 6405 https://doi.org/10.1126/science.aar7101	journal	August 2018
Folding versus aggregation: Polypeptide conformations on competing pathways Jahn, Thomas R.; Radford, Sheena E. Archives of Biochemistry and Biophysics, Vol. 469, Issue 1 https://doi.org/10.1016/j.abb.2007.05.015	journal	January 2008
Molecular dimensions and their distributions in early folding intermediates Bilsel, O.; Matthews, C. Current Opinion in Structural Biology, Vol. 16, Issue 1 https://doi.org/10.1016/j.sbi.2006.01.007	journal	February 2006
Energetically significant networks of coupled interactions within an unfolded protein Cho, J. -H.; Meng, W.; Sato, S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33 https://doi.org/10.1073/pnas.1402054111	journal	August 2014
Experiments and simulations show how long-range contacts can form in expanded unfolded proteins with negligible secondary structure Meng, W.; Lyle, N.; Luan, B. Proceedings of the National Academy of Sciences, Vol. 110, Issue 6 https://doi.org/10.1073/pnas.1216979110	journal	January 2013
Site-specific time-resolved FRET reveals local variations in the unfolding mechanism in an apparently two-state protein unfolding transition Bhatia, Sandhya; Krishnamoorthy, G.; Udgaonkar, Jayant B. Physical Chemistry Chemical Physics, Vol. 20, Issue 5 https://doi.org/10.1039/C7CP06214A	journal	January 2018
Protein collapse is encoded in the folded state architecture Samanta, Himadri S.; Zhuravlev, Pavel I.; Hinczewski, Michael Soft Matter, Vol. 13, Issue 19 https://doi.org/10.1039/C7SM00074J	journal	January 2017
Single-molecule spectroscopy reveals polymer effects of disordered proteins in crowded environments Soranno, Andrea; Koenig, Iwo; Borgia, Madeleine B. Proceedings of the National Academy of Sciences, Vol. 111, Issue 13 https://doi.org/10.1073/pnas.1322611111	journal	March 2014
Speeding protein folding beyond the G? model: How a little frustration sometimes helps Plotkin, Steven S. Proteins: Structure, Function, and Genetics, Vol. 45, Issue 4 https://doi.org/10.1002/prot.1154	journal	January 2001
Macromolecular clusters in poor-solvent polymer solutions Raos, Guido; Allegra, Giuseppe The Journal of Chemical Physics, Vol. 107, Issue 16 https://doi.org/10.1063/1.474306	journal	October 1997
Rapid Collapse Precedes the Fast Two-state Folding of the Cold Shock Protein Magg, Christine; Schmid, Franz X. Journal of Molecular Biology, Vol. 335, Issue 5 https://doi.org/10.1016/j.jmb.2003.11.050	journal	January 2004
An Adequate Account of Excluded Volume Is Necessary To Infer Compactness and Asphericity of Disordered Proteins by Förster Resonance Energy Transfer Song, Jianhui; Gomes, Gregory-Neal; Gradinaru, Claudiu C. The Journal of Physical Chemistry B, Vol. 119, Issue 49 https://doi.org/10.1021/acs.jpcb.5b09133	journal	November 2015
Probing Protein Folding Using Site-Specifically Encoded Unnatural Amino Acids as FRET Donors with Tryptophan Miyake-Stoner, Shigeki J.; Miller, Andrew M.; Hammill, Jared T. Biochemistry, Vol. 48, Issue 25 https://doi.org/10.1021/bi900426d	journal	June 2009
Kinetics and thermodynamics of folding in model proteins. Camacho, C. J.; Thirumalai, D. Proceedings of the National Academy of Sciences, Vol. 90, Issue 13 https://doi.org/10.1073/pnas.90.13.6369	journal	July 1993
Probing the Action of Chemical Denaturant on an Intrinsically Disordered Protein by Simulation and Experiment Zheng, Wenwei; Borgia, Alessandro; Buholzer, Karin Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b05443	journal	September 2016
Evidence for Initial Non-specific Polypeptide Chain Collapse During the Refolding of the SH3 Domain of PI3 Kinase Dasgupta, Amrita; Udgaonkar, Jayant B. Journal of Molecular Biology, Vol. 403, Issue 3 https://doi.org/10.1016/j.jmb.2010.08.046	journal	October 2010
Comprehensive structural and dynamical view of an unfolded protein from the combination of single-molecule FRET, NMR, and SAXS Aznauryan, Mikayel; Delgado, Leonildo; Soranno, Andrea Proceedings of the National Academy of Sciences, Vol. 113, Issue 37 https://doi.org/10.1073/pnas.1607193113	journal	August 2016
Microsecond Subdomain Folding in Dihydrofolate Reductase Arai, Munehito; Iwakura, Masahiro; Matthews, C. Robert Journal of Molecular Biology, Vol. 410, Issue 2 https://doi.org/10.1016/j.jmb.2011.04.057	journal	July 2011
Fine Structure Analysis of a Protein Folding Transition State; Distinguishing Between Hydrophobic Stabilization and Specific Packing Anil, Burcu; Sato, Satoshi; Cho, Jae-Hyun Journal of Molecular Biology, Vol. 354, Issue 3 https://doi.org/10.1016/j.jmb.2005.08.054	journal	December 2005
Molecular Simulation of ab Initio Protein Folding for a Millisecond Folder NTL9(1−39) Voelz, Vincent A.; Bowman, Gregory R.; Beauchamp, Kyle Journal of the American Chemical Society, Vol. 132, Issue 5 https://doi.org/10.1021/ja9090353	journal	February 2010
Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2 Deniz, A. A.; Laurence, T. A.; Beligere, G. S. Proceedings of the National Academy of Sciences, Vol. 97, Issue 10 https://doi.org/10.1073/pnas.090104997	journal	May 2000
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
The Limited Role of Nonnative Contacts in the Folding Pathways of a Lattice Protein Gin, Brian C.; Garrahan, Juan P.; Geissler, Phillip L. Journal of Molecular Biology, Vol. 392, Issue 5 https://doi.org/10.1016/j.jmb.2009.06.058	journal	October 2009
Urea-Induced Unfolding of the Immunity Protein Im9 Monitored by spFRET Tezuka-Kawakami, Tomoko; Gell, Chris; Brockwell, David J. Biophysical Journal, Vol. 91, Issue 5 https://doi.org/10.1529/biophysj.106.088344	journal	September 2006
Single-Molecule Measurement of Protein Folding Kinetics Lipman, E. A. Science, Vol. 301, Issue 5637 https://doi.org/10.1126/science.1085399	journal	August 2003
Cryptic sequence features within the disordered protein p27 ^Kip1 regulate cell cycle signaling Das, Rahul K.; Huang, Yongqi; Phillips, Aaron H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 20 https://doi.org/10.1073/pnas.1516277113	journal	May 2016
Saxs Confirms that FRET Dyes Promote Collapse of an Otherwise Fully Disordered Protein Riback, Joshua A.; Bowman, Micayla A.; Zmyslowski, Adam M. Biophysical Journal, Vol. 114, Issue 3 https://doi.org/10.1016/j.bpj.2017.11.2040	journal	February 2018
Role of Backbone−Solvent Interactions in Determining Conformational Equilibria of Intrinsically Disordered Proteins Tran, Hoang T.; Mao, Albert; Pappu, Rohit V. Journal of the American Chemical Society, Vol. 130, Issue 23 https://doi.org/10.1021/ja710446s	journal	June 2008
Small-Angle X-ray Scattering and Single-Molecule FRET Spectroscopy Produce Highly Divergent Views of the Low-Denaturant Unfolded State Yoo, Tae Yeon; Meisburger, Steve P.; Hinshaw, James Journal of Molecular Biology, Vol. 418, Issue 3-4 https://doi.org/10.1016/j.jmb.2012.01.016	journal	May 2012
Denatured State Ensembles with the Same Radii of Gyration Can Form Significantly Different Long-Range Contacts Luan, Bowu; Lyle, Nicholas; Pappu, Rohit V. Biochemistry, Vol. 53, Issue 1 https://doi.org/10.1021/bi4008337	journal	December 2013
Are there pathways for protein folding? Levinthal, Cyrus Journal de Chimie Physique, Vol. 65 https://doi.org/10.1051/jcp/1968650044	journal	January 1968
The SARS-CoV-2 nucleocapsid protein is dynamic, disordered, and phase separates with RNA Cubuk, Jasmine; Alston, Jhullian J.; Incicco, J. Jeremías Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21953-3	journal	March 2021
Single-molecule FRET spectroscopy and the polymer physics of unfolded and intrinsically disordered proteins Schuler, Benjamin; Soranno, Andrea; Hofmann, Hagen Annual Reviews https://doi.org/10.5167/uzh-125099	text	January 2016
Probing the Action of Chemical Denaturant on an Intrinsically Disordered Protein by Simulation and Experiment Zheng, Wenwei; Borgia, Alessandro; Buholzer, Karin American Chemical Society (ACS) https://doi.org/10.5167/uzh-126516	text	January 2016
Consistent view of polypeptide chain expansion in chemical denaturants from multiple experimental methods Borgia, Alessandro; Zheng, Wenwei; Buholzer, Karin American Chemical Society (ACS) https://doi.org/10.5167/uzh-126517	text	January 2016
Comprehensive structural and dynamical view of an unfolded protein from the combination of single-molecule FRET, NMR, and SAXS Aznauryan, Mikayel; Delgado, Leonildo; Soranno, Andrea National Academy of Sciences https://doi.org/10.5167/uzh-126518	text	January 2016
Comment on "Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water" Best, Robert B.; Zheng, Wenwei; Borgia, Alessandro American Association for the Advancement of Science https://doi.org/10.5167/uzh-158211	text	January 2018
Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy Hofmann, Hagen; Soranno, Andrea; Borgia, Alessandro National Academy of Sciences https://doi.org/10.5167/uzh-65974	text	January 2012
Single-molecule studies of intrinsically disordered proteins Marco, Brucale,; Benjamin, Schuler,; Bruno, Samorì, American Chemical Society https://doi.org/10.5167/uzh-96983	text	January 2014
Single-molecule spectroscopy reveals polymer effects of disordered proteins in crowded environments Soranno, Andrea; Koenig, Iwo; Borgia, Madeleine B. National Academy of Sciences https://doi.org/10.5167/uzh-97006	text	January 2014
Single-Molecule Spectroscopy Reveals Polymer Effects of Disordered Proteins in Crowded Environments Soranno, Andrea; Koenig, Iwo; Borgia, Madeleine B. Biophysical Journal, Vol. 106, Issue 2 https://doi.org/10.1016/j.bpj.2013.11.1572	journal	January 2014
Quantitative assessments of the distinct contributions of polypeptide backbone amides versus side chain groups to chain expansion via chemical denaturation S., Holehouse, Alex; Kanchan, Garai,; Nicholas, Lyle, American Chemical Society (ACS) https://doi.org/10.5167/uzh-112992	text	January 2015
Charge interactions can dominate the dimensions of intrinsically disordered proteins S., Müller-Späth,; A., Soranno,; V., Hirschfeld, National Academy of Sciences https://doi.org/10.5167/uzh-40012	text	January 2010
Charge Interactions Can Dominate the Dimensions of Intrinsically Disordered Proteins Soranno, Andrea; Müller-Späth, Sonja; Hirschfeld, Verena Biophysical Journal, Vol. 100, Issue 3 https://doi.org/10.1016/j.bpj.2010.12.278	journal	February 2011
How accurate are polymer models in the analysis of Forster resonance energy transfer experiments on proteins? O'Brien, E. P.; Morrison, G.; Brooks, B. R. arXiv https://doi.org/10.48550/arxiv.0905.0383	text	January 2009
Asymmetry in the shapes of folded and denatured states of proteins Dima, Ruxandra I.; Thirumalai, D. arXiv https://doi.org/10.48550/arxiv.q-bio/0310023	preprint	January 2003
How Does Melittin Permeabilize Membranes? Wimley, William C. Biophysical Journal, Vol. 114, Issue 2 https://doi.org/10.1016/j.bpj.2017.11.3738	journal	January 2018
Describing sequence–ensemble relationships for intrinsically disordered proteins Mao, Albert H.; Lyle, Nicholas; Pappu, Rohit V. Biochemical Journal, Vol. 449, Issue 2 https://doi.org/10.1042/bj20121346	journal	December 2012
To fold or expand—a charged question England, Jeremy L.; Haran, Gilad Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1008673107	journal	August 2010
Criterion that Determines the Foldability of Proteins Klimov, D. K.; Thirumalai, D. Physical Review Letters, Vol. 76, Issue 21 https://doi.org/10.1103/physrevlett.76.4070	journal	May 1996
Conformational Heterogeneity and FRET Data Interpretation for Dimensions of Unfolded Proteins Song, Jianhui; Gomes, Gregory-Neal; Shi, Tongfei arXiv https://doi.org/10.48550/arxiv.1705.06010	text	January 2017

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Protein folding while chaperone bound is dependent on weak interactions Wu, Kevin; Stull, Frederick; Lee, Changhan Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12774-6	journal	October 2019
Information theoretic measures for quantifying sequence–ensemble relationships of intrinsically disordered proteins Cohan, Megan C.; Ruff, Kiersten M.; Pappu, Rohit V. Protein Engineering, Design and Selection, Vol. 32, Issue 4 https://doi.org/10.1093/protein/gzz014	journal	April 2019
Polymer effects modulate binding affinities in disordered proteins Vancraenenbroeck, Renee; Harel, Yair S.; Zheng, Wenwei Proceedings of the National Academy of Sciences, Vol. 116, Issue 39 https://doi.org/10.1073/pnas.1904997116	journal	September 2019

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