From Protein Design to the Energy Landscape of a Cold Unfolding Protein

Pulavarti, Surya V.S.R.K.; Maguire, Jack B.; Yuen, Shirley; Harrison, Joseph S.; Griffin, Jermel; Premkumar, Lakshmanane; Esposito, Edward A.; Makhatadze, George I.; Garcia, Angel E.; Weiss, Thomas M.; Snell, Edward H.; Kuhlman, Brian; Szyperski, Thomas

doi:10.1021/acs.jpcb.1c10750

Title: From Protein Design to the Energy Landscape of a Cold Unfolding Protein

Journal Article · Mon Feb 07 00:00:00 EST 2022 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.1c10750· OSTI ID:1865037

Pulavarti, Surya V.S.R.K. ^[1]; Maguire, Jack B. ^[2]; Yuen, Shirley ^[3]; Harrison, Joseph S. ^[4]; Griffin, Jermel ^[5]; Premkumar, Lakshmanane ^[6]; Esposito, Edward A. ^[7];

^[8];

^[9]; Weiss, Thomas M. ^[10];

^[11];

^[6];

^[1]

State Univ. of New York (SUNY), Buffalo, NY (United States)
Univ. of North Carolina, Chapel Hill, NC (United States); Menten AI Inc., Palo Alto, CA (United States)
State Univ. of New York at Buffalo, NY (United States)
Univ. of North Carolina, Chapel Hill, NC (United States); Univ. of the Pacific, Stockton, CA (United States)
State Univ. of New York at Buffalo, NY (United States); Astrix Software Technology Inc., Red Bank, NJ (United States)
Univ. of North Carolina, Chapel Hill, NC (United States)
Malvern Panalytical Inc, Northhampton, MA (United States)
Rensselaer Polytechnic Inst., Troy, NY (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Stanford Univ., CA (United States)
Hauptman-Woodward Medical Research Inst. (HWI), Buffalo, NY (United States); State Univ. of New York at Buffalo, NY (United States)

Understanding protein folding is crucial for protein sciences. The conformational spaces and energy landscapes of cold (unfolded) protein states, as well as the associated transitions, are hardly explored. Furthermore, it is not known how structure relates to the cooperativity of cold transitions, if cold and heat unfolded states are thermodynamically similar, and if cold states play important roles for protein function. We created the cold unfolding 4-helix bundle DCUB1 with a de novo designed bipartite hydrophilic/hydrophobic core featuring a hydrogen bond network which extends across the bundle in order to study the relative importance of hydrophobic versus hydrophilic protein–water interactions for cold unfolding. Structural and thermodynamic characterization resulted in the discovery of a complex energy landscape for cold transitions, while the heat unfolded state is a random coil. Below ~0 °C, the core of DCUB1 disintegrates in a largely cooperative manner, while a near-native helical content is retained. The resulting cold core-unfolded state is compact and features extensive internal dynamics. Below -5 °C, two additional cold transitions are seen, that is, (i) the formation of a water-mediated, compact, and highly dynamic dimer, and (ii) the onset of cold helix unfolding decoupled from cold core unfolding. Our results suggest that cold unfolding is initiated by the intrusion of water into the hydrophilic core network and that cooperativity can be tuned by varying the number of core hydrogen bond networks. Protein design has proven to be invaluable to explore the energy landscapes of cold states and to robustly test related theories.

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Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: 89233218CNA000001; AC02-76SF00515; MCB-1615570; MCB-180104; GM131923; P30GM133894; S10OD021512; 1S10OD012254; 1231306

OSTI ID:: 1865037

Report Number(s):: LA-UR-21-32367

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Vol. 126, Issue 6; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (99)

Combined Covalent-Electrostatic Model of Hydrogen Bonding Improves Structure Prediction with Rosetta O’Meara, Matthew J.; Leaver-Fay, Andrew; Tyka, Michael D. Journal of Chemical Theory and Computation, Vol. 11, Issue 2 https://doi.org/10.1021/ct500864r	journal	January 2015
BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra Micsonai, András; Wien, Frank; Bulyáki, Éva Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky497	journal	June 2018
A1H-NMR thermometer suitable for cryoprobes Findeisen, M.; Brand, T.; Berger, S. Magnetic Resonance in Chemistry, Vol. 45, Issue 2 https://doi.org/10.1002/mrc.1941	journal	January 2007
Hyperbolic Pressure–Temperature Phase Diagram of the Zinc-Finger Protein apoKti11 Detected by NMR Spectroscopy Klamt, Andi; Nagarathinam, Kumar; Tanabe, Mikio The Journal of Physical Chemistry B, Vol. 123, Issue 4 https://doi.org/10.1021/acs.jpcb.8b11019	journal	January 2019
Contact order, transition state placement and the refolding rates of single domain proteins 1 1Edited by P. E. Wright Plaxco, Kevin W.; Simons, Kim T.; Baker, David Journal of Molecular Biology, Vol. 277, Issue 4 https://doi.org/10.1006/jmbi.1998.1645	journal	April 1998
Statistical survey of the buried waters in the Protein Data Bank Carugo, Oliviero Amino Acids, Vol. 48, Issue 1 https://doi.org/10.1007/s00726-015-2064-4	journal	August 2015
On the cooperative formation of non-hydrogen-bonded water at molecular hydrophobic interfaces Davis, Joel G.; Rankin, Blake M.; Gierszal, Kamil P. Nature Chemistry, Vol. 5, Issue 9 https://doi.org/10.1038/nchem.1716	journal	July 2013
Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy Micsonai, András; Wien, Frank; Kernya, Linda Proceedings of the National Academy of Sciences, Vol. 112, Issue 24 https://doi.org/10.1073/pnas.1500851112	journal	June 2015
Temperature Dependence of the Thermodynamics of Helix–Coil Transition Richardson, John M.; Makhatadze, George I. Journal of Molecular Biology, Vol. 335, Issue 4 https://doi.org/10.1016/j.jmb.2003.11.027	journal	January 2004
Rapid Sampling of Hydrogen Bond Networks for Computational Protein Design Maguire, Jack B.; Boyken, Scott E.; Baker, David Journal of Chemical Theory and Computation, Vol. 14, Issue 5 https://doi.org/10.1021/acs.jctc.8b00033	journal	March 2018
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers Abraham, Mark James; Murtola, Teemu; Schulz, Roland SoftwareX, Vol. 1-2 https://doi.org/10.1016/j.softx.2015.06.001	journal	September 2015
Aromatic Ring-Flipping in Supercooled Water: Implications for NMR-Based Structural Biology of Proteins Skalicky, Jack J.; Mills, Jeffrey L.; Sharma, Surabhi Journal of the American Chemical Society, Vol. 123, Issue 3 https://doi.org/10.1021/ja003220l	journal	December 2000
Computational investigation of cold denaturation in the Trp-cage miniprotein Kim, Sang Beom; Palmer, Jeremy C.; Debenedetti, Pablo G. Proceedings of the National Academy of Sciences, Vol. 113, Issue 32 https://doi.org/10.1073/pnas.1607500113	journal	July 2016
The Role of Hydration in Protein Stability: Comparison of the Cold and Heat Unfolded States of Yfh1 Adrover, Miquel; Martorell, Gabriel; Martin, Stephen R. Journal of Molecular Biology, Vol. 417, Issue 5 https://doi.org/10.1016/j.jmb.2012.02.002	journal	April 2012
α-helix stabilization by alanine relative to glycine: Roles of polar and apolar solvent exposures and of backbone entropy López-Llano, J.; Campos, L. A.; Sancho, J. Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3 https://doi.org/10.1002/prot.21041	journal	June 2006
The Protein Folding Problem: The Role of Theory Nassar, Roy; Dignon, Gregory L.; Razban, Rostam M. Journal of Molecular Biology, Vol. 433, Issue 20 https://doi.org/10.1016/j.jmb.2021.167126	journal	October 2021
Hydrodynamic Radii of Native and Denatured Proteins Measured by Pulse Field Gradient NMR Techniques ^† Wilkins, Deborah K.; Grimshaw, Shaun B.; Receveur, Véronique Biochemistry, Vol. 38, Issue 50 https://doi.org/10.1021/bi991765q	journal	December 1999
Abp1p and Fyn SH3 Domains Fold through Similar Low-Populated Intermediate States Korzhnev, Dmitry M.; Neudecker, Philipp; Zarrine-Afsar, Arash Biochemistry, Vol. 45, Issue 34 https://doi.org/10.1021/bi0611560	journal	August 2006
Water Determines the Structure and Dynamics of Proteins Bellissent-Funel, Marie-Claire; Hassanali, Ali; Havenith, Martina Chemical Reviews, Vol. 116, Issue 13 https://doi.org/10.1021/acs.chemrev.5b00664	journal	April 2016
Behind the folding funnel diagram Karplus, Martin Nature Chemical Biology, Vol. 7, Issue 7 https://doi.org/10.1038/nchembio.565	journal	June 2011
Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR Korzhnev, Dmitry M.; Salvatella, Xavier; Vendruscolo, Michele Nature, Vol. 430, Issue 6999 https://doi.org/10.1038/nature02655	journal	July 2004
Canonical sampling through velocity rescaling Bussi, Giovanni; Donadio, Davide; Parrinello, Michele The Journal of Chemical Physics, Vol. 126, Issue 1 https://doi.org/10.1063/1.2408420	journal	January 2007
Improved protein structure prediction using potentials from deep learning Senior, Andrew W.; Evans, Richard; Jumper, John Nature, Vol. 577, Issue 7792 https://doi.org/10.1038/s41586-019-1923-7	journal	January 2020
Water–protein dynamic coupling and new opportunities for probing it at low to physiological temperatures in aqueous solutions Mamontov, Eugene; Chu, Xiang-qiang Physical Chemistry Chemical Physics, Vol. 14, Issue 33 https://doi.org/10.1039/c2cp41443k	journal	January 2012
Non-linear rate-equilibrium free energy relationships and Hammond behavior in protein folding Sánchez, Ignacio E.; Kiefhaber, Thomas Biophysical Chemistry, Vol. 100, Issue 1-3 https://doi.org/10.1016/s0301-4622(02)00294-6	journal	December 2002
De novo design of protein homo-oligomers with modular hydrogen-bond network-mediated specificity Boyken, S. E.; Chen, Z.; Groves, B. Science, Vol. 352, Issue 6286 https://doi.org/10.1126/science.aad8865	journal	May 2016
Native protein sequences are close to optimal for their structures Kuhlman, B.; Baker, D. Proceedings of the National Academy of Sciences, Vol. 97, Issue 19 https://doi.org/10.1073/pnas.97.19.10383	journal	September 2000
Cold sensitivity of the SARS-CoV-2 spike ectodomain Edwards, Robert J.; Mansouri, Katayoun; Stalls, Victoria Nature Structural & Molecular Biology, Vol. 28, Issue 2 https://doi.org/10.1038/s41594-020-00547-5	journal	January 2021
Limited cooperativity in protein folding Muñoz, Victor; Campos, Luis A.; Sadqi, Mourad Current Opinion in Structural Biology, Vol. 36 https://doi.org/10.1016/j.sbi.2015.12.001	journal	February 2016
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Cooperative Cold Denaturation: The Case of the C-Terminal Domain of Ribosomal Protein L9 Luan, Bowu; Shan, Bing; Baiz, Carlos Biochemistry, Vol. 52, Issue 14 https://doi.org/10.1021/bi3016789	journal	March 2013
The Complex Energy Landscape of the Protein IscU Bothe, Jameson R.; Tonelli, Marco; Ali, Ibrahim K. Biophysical Journal, Vol. 109, Issue 5 https://doi.org/10.1016/j.bpj.2015.07.045	journal	September 2015
Perturbing the energy landscape for improved packing during computational protein design Maguire, Jack B.; Haddox, Hugh K.; Strickland, Devin Proteins: Structure, Function, and Bioinformatics, Vol. 89, Issue 4 https://doi.org/10.1002/prot.26030	journal	December 2020
Protein folding ‐ seeing is deceiving Rose, George D. Protein Science, Vol. 30, Issue 8 https://doi.org/10.1002/pro.4096	journal	May 2021
Unveiling invisible protein states with NMR spectroscopy Alderson, T. Reid; Kay, Lewis E. Current Opinion in Structural Biology, Vol. 60 https://doi.org/10.1016/j.sbi.2019.10.008	journal	February 2020
Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water Spolar, Ruth S.; Livingstone, Jeff R.; Record, M. Thomas Biochemistry, Vol. 31, Issue 16 https://doi.org/10.1021/bi00131a009	journal	April 1992
α-Helix stability in proteins Serrano, Luis; Sancho, Javier; Hirshberg, Miriam Journal of Molecular Biology, Vol. 227, Issue 2 https://doi.org/10.1016/0022-2836(92)90906-z	journal	September 1992
Towards a structural biology of the hydrophobic effect in protein folding Camilloni, Carlo; Bonetti, Daniela; Morrone, Angela Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28285	journal	July 2016
Unbiased Cold Denaturation: Low- and High-Temperature Unfolding of Yeast Frataxin under Physiological Conditions Pastore, Annalisa; Martin, Stephen R.; Politou, Anastasia Journal of the American Chemical Society, Vol. 129, Issue 17 https://doi.org/10.1021/ja0714538	journal	April 2007
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Converging concepts of protein folding in vitro and in vivo Hartl, F. Ulrich; Hayer-Hartl, Manajit Nature Structural & Molecular Biology, Vol. 16, Issue 6 https://doi.org/10.1038/nsmb.1591	journal	June 2009
Cooperative Thermal Denaturation of Proteins Designed by Binary Patterning of Polar and Nonpolar Amino Acids Roy, Sushmita; Hecht, Michael H. Biochemistry, Vol. 39, Issue 16 https://doi.org/10.1021/bi992328e	journal	March 2000
An ¹⁵ N NMR Spin Relaxation Dispersion Study of the Folding of a Pair of Engineered Mutants of Apocytochrome b ₅₆₂ Choy, Wing-Yiu; Zhou, Zheng; Bai, Yawen Journal of the American Chemical Society, Vol. 127, Issue 14 https://doi.org/10.1021/ja042560u	journal	March 2005
The Cold Denatured State Is Compact but Expands at Low Temperatures: Hydrodynamic Properties of the Cold Denatured State of the C-terminal Domain of L9 Li, Ying; Shan, Bing; Raleigh, Daniel P. Journal of Molecular Biology, Vol. 368, Issue 1 https://doi.org/10.1016/j.jmb.2007.02.011	journal	April 2007
Simulating electrostatic effects on electronic transitions in proteins Callis, Patrik R. Molecular Simulation, Vol. 41, Issue 1-3 https://doi.org/10.1080/08927022.2014.923571	journal	June 2014
Cold Denaturation of α-Synuclein Amyloid Fibrils Ikenoue, Tatsuya; Lee, Young-Ho; Kardos, József Angewandte Chemie International Edition, Vol. 53, Issue 30 https://doi.org/10.1002/anie.201403815	journal	June 2014
The Unfolded State of the C-Terminal Domain of L9 Expands at Low but Not at Elevated Temperatures Stenzoski, Natalie E.; Luan, Bowu; Holehouse, Alex S. Biophysical Journal, Vol. 115, Issue 4 https://doi.org/10.1016/j.bpj.2018.07.013	journal	August 2018
Macromolecular modeling and design in Rosetta: recent methods and frameworks Leman, Julia Koehler; Weitzner, Brian D.; Lewis, Steven M. Nature Methods, Vol. 17, Issue 7 https://doi.org/10.1038/s41592-020-0848-2	journal	June 2020
Protein Cold Denaturation in Implicit Solvent Simulations: A Transfer Free Energy Approach Arsiccio, Andrea; Shea, Joan-Emma The Journal of Physical Chemistry B, Vol. 125, Issue 20 https://doi.org/10.1021/acs.jpcb.1c01694	journal	May 2021
Psychrophiles: A journey of hope Tendulkar, Shivani; Hattiholi, Aishwarya; Chavadar, Mahesh Journal of Biosciences, Vol. 46, Issue 3 https://doi.org/10.1007/s12038-021-00180-4	journal	June 2021
An optimized strategy to measure protein stability highlights differences between cold and hot unfolded states Alfano, Caterina; Sanfelice, Domenico; Martin, Stephen R. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15428	journal	May 2017
Global analysis of the thermal and chemical denaturation of the N-terminal domain of the ribosomal protein L9 in H ₂ O and D ₂ O. Determination of the thermodynamic parameters, Δ H °, Δ S °, and Δ C ° _p , and evaluation of solvent isotope effects Kuhlman, Brian; Raleigh, Daniel P. Protein Science, Vol. 7, Issue 11 https://doi.org/10.1002/pro.5560071118	journal	November 1998
How cooperative are protein folding and unfolding transitions?: Cooperativity in Protein Folding/Unfolding Reactions Malhotra, Pooja; Udgaonkar, Jayant B. Protein Science, Vol. 25, Issue 11 https://doi.org/10.1002/pro.3015	journal	September 2016
Role of Hydrophobic Hydration in Protein Stability: A 3D Water-Explicit Protein Model Exhibiting Cold and Heat Denaturation Matysiak, Silvina; Debenedetti, Pablo G.; Rossky, Peter J. The Journal of Physical Chemistry B, Vol. 116, Issue 28 https://doi.org/10.1021/jp3039175	journal	July 2012
An exceptionally stable helix from the ribosomal protein L9: implications for protein folding and stability Kuhlman, Brian; Yang, Hui Yu; Boice, Judith A. Journal of Molecular Biology, Vol. 270, Issue 5 https://doi.org/10.1006/jmbi.1997.1146	journal	August 1997
Cold Denaturation of Protein Privalov, Peter L. Critical Reviews in Biochemistry and Molecular Biology, Vol. 25, Issue 4 https://doi.org/10.3109/10409239009090612	journal	January 1990
An Antifreeze Protein Folds with an Interior Network of More Than 400 Semi-Clathrate Waters Sun, T.; Lin, F. -H.; Campbell, R. L. Science, Vol. 343, Issue 6172 https://doi.org/10.1126/science.1247407	journal	February 2014
Cold denaturation of a protein dimer monitored at atomic resolution Jaremko, Mariusz; Jaremko, Łukasz; Kim, Hai-Young Nature Chemical Biology, Vol. 9, Issue 4 https://doi.org/10.1038/nchembio.1181	journal	February 2013
The “cold revolution”. Present and future applications of cold-active enzymes and ice-binding proteins Mangiagalli, Marco; Brocca, Stefania; Orlando, Marco New Biotechnology, Vol. 55 https://doi.org/10.1016/j.nbt.2019.09.003	journal	March 2020
Yeast Frataxin Is Stabilized by Low Salt Concentrations: Cold Denaturation Disentangles Ionic Strength Effects from Specific Interactions Sanfelice, Domenico; Puglisi, Rita; Martin, Stephen R. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0095801	journal	May 2014
The Use of Circular Dichroism in the Investigation of Protein Structure and Function Kelly, Sharon; Price, Nicholas Current Protein & Peptide Science, Vol. 1, Issue 4, p. 349-384 https://doi.org/10.2174/1389203003381315	journal	December 2000
Tyrosine, Phenylalanine, and Disulfide Contributions to the Circular Dichroism of Proteins: Circular Dichroism Spectra of Wild-Type and Mutant Bovine Pancreatic Trypsin Inhibitor Sreerama, Narasimha; Manning, Mark C.; Powers, Michael E. Biochemistry, Vol. 38, Issue 33 https://doi.org/10.1021/bi990516z	journal	July 1999
D614G mutation in the SARS-CoV-2 spike protein enhances viral fitness by desensitizing it to temperature-dependent denaturation Yang, Tzu-Jing; Yu, Pei-Yu; Chang, Yuan-Chih Journal of Biological Chemistry, Vol. 297, Issue 4 https://doi.org/10.1016/j.jbc.2021.101238	journal	October 2021
Structure and Function of Water Molecules Buried in the Protein Core Carugo, Oliviero Current Protein & Peptide Science, Vol. 16, Issue 3 https://doi.org/10.2174/1389203716666150227162803	journal	March 2015
Protein folding by NMR Zhuravleva, Anastasia; Korzhnev, Dmitry M. Progress in Nuclear Magnetic Resonance Spectroscopy, Vol. 100 https://doi.org/10.1016/j.pnmrs.2016.10.002	journal	May 2017
Understanding Cold Denaturation: The Case Study of Yfh1 Adrover, Miquel; Esposito, Veronica; Martorell, Gabriel Journal of the American Chemical Society, Vol. 132, Issue 45 https://doi.org/10.1021/ja1070174	journal	October 2010
The temperature properties of human α2-macroglobulin in the range −15 to +37°C. An investigation of supercooled solutions using small-angle X-ray scattering and dilatometry Sjöberg, B.; Pap, S. International Journal of Biological Macromolecules, Vol. 7, Issue 4 https://doi.org/10.1016/0141-8130(85)90005-4	journal	August 1985
The Cold-Unfolded State Is Expanded but Contains Long- and Medium-Range Contacts and Is Poorly Described by Homopolymer Models Stenzoski, Natalie E.; Zou, Junjie; Piserchio, Andrea Biochemistry, Vol. 59, Issue 36 https://doi.org/10.1021/acs.biochem.0c00469	journal	July 2020
Psychrophilic Enzymes: From Folding to Function and Biotechnology Feller, Georges Scientifica, Vol. 2013 https://doi.org/10.1155/2013/512840	journal	January 2013
Increasing Sequence Diversity with Flexible Backbone Protein Design: The Complete Redesign of a Protein Hydrophobic Core Murphy, Grant S.; Mills, Jeffrey L.; Miley, Michael J. Structure, Vol. 20, Issue 6 https://doi.org/10.1016/j.str.2012.03.026	journal	June 2012
Probing the Residual Structure of the Low Populated Denatured State of ADA2h under Folding Conditions by Relaxation Dispersion Nuclear Magnetic Resonance Spectroscopy Pustovalova, Yulia; Kukic, Predrag; Vendruscolo, Michele Biochemistry, Vol. 54, Issue 30 https://doi.org/10.1021/acs.biochem.5b00345	journal	July 2015
HYDRONMR: Prediction of NMR Relaxation of Globular Proteins from Atomic-Level Structures and Hydrodynamic Calculations Garcı́a de la Torre, J.; Huertas, M. L.; Carrasco, B. Journal of Magnetic Resonance, Vol. 147, Issue 1 https://doi.org/10.1006/jmre.2000.2170	journal	November 2000
Theory of cold denaturation of proteins Ben-Naim, Arieh Advances in Biological Chemistry, Vol. 03, Issue 01 https://doi.org/10.4236/abc.2013.31005	journal	January 2013
Dominant forces in protein folding Dill, Ken A. Biochemistry, Vol. 29, Issue 31 https://doi.org/10.1021/bi00483a001	journal	August 1990
The new view of hydrophobic free energy Baldwin, Robert L. FEBS Letters, Vol. 587, Issue 8 https://doi.org/10.1016/j.febslet.2013.01.006	journal	January 2013
Cold Denaturation of the HIV-1 Protease Monomer Rösner, Heike I.; Caldarini, Martina; Prestel, Andreas Biochemistry, Vol. 56, Issue 8 https://doi.org/10.1021/acs.biochem.6b01141	journal	February 2017
Combined NMR-observation of cold denaturation in supercooled water and heat denaturation enables accurate measurement of ΔC p of protein unfolding Szyperski, Thomas; Mills, Jeffrey L.; Perl, Dieter European Biophysics Journal, Vol. 35, Issue 4 https://doi.org/10.1007/s00249-005-0028-4	journal	October 2005
Room Temperature X-Ray Crystallography Reveals Conformational Heterogeneity of Engineered Proteins Szyperski, Thomas Structure, Vol. 25, Issue 5 https://doi.org/10.1016/j.str.2017.04.004	journal	May 2017
Heat capacity of proteins Makhatadze, G. I.; Privalov, P. L. Journal of Molecular Biology, Vol. 213, Issue 2 https://doi.org/10.1016/s0022-2836(05)80197-4	journal	May 1990
Dynamic hydration shell restores Kauzmann's 1959 explanation of how the hydrophobic factor drives protein folding Baldwin, Robert L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 36 https://doi.org/10.1073/pnas.1414556111	journal	August 2014
Water Mediation in Protein Folding and Molecular Recognition Levy, Yaakov; Onuchic, José N. Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.biophys.35.040405.102134	journal	June 2006
Cold Denaturation Unveiled: Molecular Mechanism of the Asymmetric Unfolding of Yeast Frataxin Sanfelice, Domenico; Morandi, Edoardo; Pastore, Annalisa ChemPhysChem, Vol. 16, Issue 17 https://doi.org/10.1002/cphc.201500765	journal	October 2015
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
Vapor-liquid equilibria from the triple point up to the critical point for the new generation of TIP4P-like models: TIP4P/Ew, TIP4P/2005, and TIP4P/ice Vega, C.; Abascal, J. L. F.; Nezbeda, I. The Journal of Chemical Physics, Vol. 125, Issue 3 https://doi.org/10.1063/1.2215612	journal	July 2006
The hydrophobic effect and its role in cold denaturation Dias, Cristiano L.; Ala-Nissila, Tapio; Wong-ekkabut, Jirasak Cryobiology, Vol. 60, Issue 1 https://doi.org/10.1016/j.cryobiol.2009.07.005	journal	February 2010
Protein Conformational Space Populated in Solution Probed with Aromatic Residual Dipolar ¹³ C- ¹ H Couplings Sathyamoorthy, Bharathwaj; Singarapu, Kiran K.; Garcia, Angel E. ChemBioChem, Vol. 14, Issue 6 https://doi.org/10.1002/cbic.201300016	journal	March 2013
Navigating the folding routes Wolynes, P.; Onuchic, J.; Thirumalai, D. Science, Vol. 267, Issue 5204 https://doi.org/10.1126/science.7886447	journal	March 1995
NMR spectroscopy of hydroxyl protons in supercooled carbohydrates Poppe, Leszek; Halbeek, Herman van Nature Structural & Molecular Biology, Vol. 1, Issue 4 https://doi.org/10.1038/nsb0494-215	journal	April 1994
Diffusion ordered nuclear magnetic resonance spectroscopy: principles and applications Johnson, C. S. Progress in Nuclear Magnetic Resonance Spectroscopy, Vol. 34, Issue 3-4 https://doi.org/10.1016/s0079-6565(99)00003-5	journal	May 1999
Supercooled Water Angell, C. A. Annual Review of Physical Chemistry, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.pc.34.100183.003113	journal	October 1983
Critical assessment of methods of protein structure prediction (CASP)—Round XIV Kryshtafovych, Andriy; Schwede, Torsten; Topf, Maya Proteins: Structure, Function, and Bioinformatics https://doi.org/10.1002/prot.26237	journal	October 2021
HullRad: Fast Calculations of Folded and Disordered Protein and Nucleic Acid Hydrodynamic Properties Fleming, Patrick J.; Fleming, Karen G. Biophysical Journal, Vol. 114, Issue 4 https://doi.org/10.1016/j.bpj.2018.01.002	journal	February 2018
NMR-based structural biology of proteins in supercooled water Szyperski, Thomas; Mills, Jeffrey L. Journal of Structural and Functional Genomics, Vol. 12, Issue 1 https://doi.org/10.1007/s10969-011-9111-5	journal	March 2011
Toward Structural Biology in Supercooled Water Skalicky, Jack J.; Sukumaran, Dinesh K.; Mills, Jeffrey L. Journal of the American Chemical Society, Vol. 122, Issue 13 https://doi.org/10.1021/ja9938884	journal	April 2000
Accessing protein conformational ensembles using room-temperature X-ray crystallography Fraser, J. S.; van den Bedem, H.; Samelson, A. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1111325108	journal	September 2011
Cooperative protein unfolding. A statistical-mechanical model for the action of denaturants Seelig, J. Biophysical Chemistry, Vol. 233 https://doi.org/10.1016/j.bpc.2017.12.001	journal	February 2018
The Cold Denatured State of the C-terminal Domain of Protein L9 Is Compact and Contains Both Native and Non-native Structure Shan, Bing; McClendon, Sebastian; Rospigliosi, Carla Journal of the American Chemical Society, Vol. 132, Issue 13 https://doi.org/10.1021/ja908104s	journal	March 2010
Hydrophobic-hydrophilic forces in protein folding Durell, Stewart R.; Ben-Naim, Arieh Biopolymers, Vol. 107, Issue 8 https://doi.org/10.1002/bip.23020	journal	June 2017

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Journal Article · Fri Feb 17 00:00:00 EST 2006 · Biochemical and Biophysical Research Communications · OSTI ID:1865037

Yawen, Bai

Precursory signatures of protein folding/unfolding: From time series correlation analysis to atomistic mechanisms

Journal Article · Wed May 28 00:00:00 EDT 2014 · Journal of Chemical Physics · OSTI ID:1865037

Hsu, P. J.; Cheong, S. A.

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59 BASIC BIOLOGICAL SCIENCES
cold denaturation
protein design
NMR
simulation
alkyls
molecular structure
molecules
noncovalent interactions
x-rays

Title: From Protein Design to the Energy Landscape of a Cold Unfolding Protein

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