Energy landscape in protein folding and unfolding

Mallamace, Francesco; Corsaro, Carmelo; Mallamace, Domenico; Vasi, Sebastiano; Vasi, Cirino; Baglioni, Piero; Buldyrev, Sergey V.; Chen, Sow -Hsin; Stanley, H. Eugene

doi:10.1073/pnas.1524864113

Title: Energy landscape in protein folding and unfolding

Journal Article · Tue Mar 08 00:00:00 EST 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1524864113· OSTI ID:1437126

Mallamace, Francesco ^[1]; Corsaro, Carmelo ^[2]; Mallamace, Domenico ^[3]; Vasi, Sebastiano ^[4]; Vasi, Cirino ^[5]; Baglioni, Piero ^[6]; Buldyrev, Sergey V. ^[7]; Chen, Sow -Hsin ^[8]; Stanley, H. Eugene ^[9]

CNR-Istituto per i Processi Chimico Fisici Messina, Messina (Italy); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Boston Univ., Boston, MA (United States)
CNR-Istituto per i Processi Chimico Fisici Messina, Messina (Italy); Univ. di Messina, Messina (Italy)
Consorzio per lo Sviluppo dei Sistemi a Grande Interfase, Catania (Italy)
Univ. di Messina, Messina (Italy)
CNR-Istituto per i Processi Chimico Fisici Messina, Messina (Italy)
Univ. di Firenze and Consorzio per lo Sviluppo dei Sistemi a Grande Interfase, Florence (Italy)
Yeshiva Univ., New York, NY (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Boston Univ., Boston, MA (United States)

Protein folding represents an open question in science, and the free-energy landscape framework is one way to describe it. In particular, the role played by water in the processes is of special interest. To clarify these issues we study, during folding–unfolding, the temperature evolution of the magnetization for hydrophilic and hydrophobic groups of hydrated lysozyme using NMR spectroscopy. Our findings confirm the validity of the theoretical scenario of a process dominated by different energetic routes, also explaining the water role in the protein configuration stability. Here, we also highlight that the protein native state limit is represented by the water singular temperature that characterizes its compressibility and expansivity and is the origin of the thermodynamical anomalies of its liquid state.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-90ER45429

OSTI ID:: 1437126

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 12; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 72 works

Citation information provided by
Web of Science

References (41)

Behind the folding funnel diagram Karplus, Martin Nature Chemical Biology, Vol. 7, Issue 7 https://doi.org/10.1038/nchembio.565	journal	June 2011
Protein folding studied by single-molecule FRET Schuler, Benjamin; Eaton, William A. Current Opinion in Structural Biology, Vol. 18, Issue 1 https://doi.org/10.1016/j.sbi.2007.12.003	journal	February 2008
Real-Time NMR Studies of Protein Folding van Nuland, Nico A. J.; Forge, Vincent; Balbach, Jochen Accounts of Chemical Research, Vol. 31, Issue 11 https://doi.org/10.1021/ar970079l	journal	November 1998
Heat capacity effects in protein folding and ligand binding: a re-evaluation of the role of water in biomolecular thermodynamics Cooper, Alan Biophysical Chemistry, Vol. 115, Issue 2-3 https://doi.org/10.1016/j.bpc.2004.12.011	journal	April 2005
Diffusion and Nuclear Spin Relaxation in Water Simpson, J. H.; Carr, H. Y. Physical Review, Vol. 111, Issue 5 https://doi.org/10.1103/PhysRev.111.1201	journal	September 1958
Levinthal's paradox. Zwanzig, R.; Szabo, A.; Bagchi, B. Proceedings of the National Academy of Sciences, Vol. 89, Issue 1 https://doi.org/10.1073/pnas.89.1.20	journal	January 1992
A singular thermodynamically consistent temperature at the origin of the anomalous behavior of liquid water Mallamace, Francesco; Corsaro, Carmelo; Stanley, H. Eugene Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00993	journal	December 2012
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
Folding and unfolding of a photoswitchable peptide from picoseconds to microseconds Ihalainen, J. A.; Bredenbeck, J.; Pfister, R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 13 https://doi.org/10.1073/pnas.0607748104	journal	March 2007
Matching speed and stability Baldwin, Robert L. Nature, Vol. 369, Issue 6477 https://doi.org/10.1038/369183a0	journal	May 1994
Microcalorimetry of biological macromolecules Privalov, Peter L.; Dragan, Anatoly I. Biophysical Chemistry, Vol. 126, Issue 1-3 https://doi.org/10.1016/j.bpc.2006.05.004	journal	March 2007
The Endothermic Effects during Denaturation of Lysozyme by Temperature Modulated Calorimetry and an Intermediate Reaction Equilibrium Salvetti, G.; Tombari, E.; Mikheeva, L. The Journal of Physical Chemistry B, Vol. 106, Issue 23 https://doi.org/10.1021/jp025587d	journal	June 2002
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
Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance Jane Dyson, H.; Ewright, Peter Unfolded Proteins https://doi.org/10.1016/S0065-3233(02)62012-1	book	January 2002
Transport properties of glass-forming liquids suggest that dynamic crossover temperature is as important as the glass transition temperature Mallamace, F.; Branca, C.; Corsaro, C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 52 https://doi.org/10.1073/pnas.1015340107	journal	December 2010
Supercooled liquids, glass transitions, and the Kauzmann paradox Stillinger, Frank H. The Journal of Chemical Physics, Vol. 88, Issue 12 https://doi.org/10.1063/1.454295	journal	June 1988
Water-inserted alpha-helical segments implicate reverse turns as folding intermediates Sundaralingam, M.; Sekharudu, Y. Science, Vol. 244, Issue 4910 https://doi.org/10.1126/science.2734612	journal	June 1989
The influence of water on protein properties Mallamace, Francesco; Baglioni, Piero; Corsaro, Carmelo The Journal of Chemical Physics, Vol. 141, Issue 16 https://doi.org/10.1063/1.4900500	journal	October 2014
Multiscale materials modelling at the mesoscale Yip, Sidney; Short, Michael P. Nature Materials, Vol. 12, Issue 9 https://doi.org/10.1038/nmat3746	journal	August 2013
Thermodynamic properties of bulk and confined water Mallamace, Francesco; Corsaro, Carmelo; Mallamace, Domenico The Journal of Chemical Physics, Vol. 141, Issue 18 https://doi.org/10.1063/1.4895548	journal	November 2014
The middle way Laughlin, R. B.; Pines, D.; Schmalian, J. Proceedings of the National Academy of Sciences, Vol. 97, Issue 1 https://doi.org/10.1073/pnas.97.1.32	journal	January 2000
Effect of flexibility and cis residues in single-molecule FRET studies of polyproline Best, R. B.; Merchant, K. A.; Gopich, I. V. Proceedings of the National Academy of Sciences, Vol. 104, Issue 48 https://doi.org/10.1073/pnas.0709567104	journal	November 2007
Multiscale complex network of protein conformational fluctuations in single-molecule time series Li, C. -B.; Yang, H.; Komatsuzaki, T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 2 https://doi.org/10.1073/pnas.0707378105	journal	January 2008
Negative activation enthalpies in the kinetics of protein folding. Oliveberg, M.; Tan, Y. J.; Fersht, A. R. Proceedings of the National Academy of Sciences, Vol. 92, Issue 19 https://doi.org/10.1073/pnas.92.19.8926	journal	September 1995
-Helix folding in the presence of structural constraints Ihalainen, J. A.; Paoli, B.; Muff, S. Proceedings of the National Academy of Sciences, Vol. 105, Issue 28 https://doi.org/10.1073/pnas.0712099105	journal	July 2008
The hydration of amides in helices; a comprehensive picture from molecular dynamics, IR, and NMR Walsh, S. T. R. Protein Science, Vol. 12, Issue 3 https://doi.org/10.1110/ps.0223003	journal	March 2003
Hydrogen Bonding in Biological Structures Jeffrey, George A.; Saenger, Wolfram https://doi.org/10.1007/978-3-642-85135-3	book	January 1991
Escaping free-energy minima Laio, A.; Parrinello, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.202427399	journal	September 2002
Intermediate States in Protein Folding Privalov, Peter L. Journal of Molecular Biology, Vol. 258, Issue 5 https://doi.org/10.1006/jmbi.1996.0280	journal	May 1996
Shoot-and-Trap: Use of specific x-ray damage to study structural protein dynamics by temperature-controlled cryo-crystallography Colletier, J. -P.; Bourgeois, D.; Sanson, B. Proceedings of the National Academy of Sciences, Vol. 105, Issue 33 https://doi.org/10.1073/pnas.0804828105	journal	August 2008
A Possible Role of Water in the Protein Folding Process Mallamace, Francesco; Corsaro, Carmelo; Mallamace, Domenico The Journal of Physical Chemistry B, Vol. 115, Issue 48 https://doi.org/10.1021/jp205285t	journal	December 2011
How does a protein fold? S˘ali, Andrej; Shakhnovich, Eugene; Karplus, Martin Nature, Vol. 369, Issue 6477 https://doi.org/10.1038/369248a0	journal	May 1994
High-resolution magic angle spinning NMR spectroscopy: Application to biomedical studies Lindon, John C.; Beckonert, Olaf P.; Holmes, Elaine Progress in Nuclear Magnetic Resonance Spectroscopy, Vol. 55, Issue 2 https://doi.org/10.1016/j.pnmrs.2008.11.004	journal	August 2009
The Dynamic Energy Landscape of Dihydrofolate Reductase Catalysis Boehr, D. D.; McElheny, D.; Dyson, H. J. Science, Vol. 313, Issue 5793, p. 1638-1642 https://doi.org/10.1126/science.1130258	journal	September 2006
Sequential proton NMR assignments and secondary structure of hen egg white lysozyme in solution Redfield, Christina; Dobson, Christopher M. Biochemistry, Vol. 27, Issue 1 https://doi.org/10.1021/bi00401a020	journal	January 1988
Hydrogen bonding in biological structures: G.A. Jeffrey and W. Saenger, Springer-Verlag; Berlin, 1991; xiv + 569 pages. DM 198.00. ISBN 3-540-50839-2 Hornby, David FEBS Letters, Vol. 323, Issue 3 https://doi.org/10.1016/0014-5793(93)81362-4	journal	June 1993
Protein folding studied by single-molecule FRET. Schuler, B.; Eaton, W. A. Elsevier https://doi.org/10.5167/uzh-4003	text	January 2008
Alpha-Helix folding in the presence of structural constraints Ihalainen, J. A.; Paoli, B.; Muff, S. National Academy of Sciences https://doi.org/10.5167/uzh-4761	text	January 2008
Sequential 1H NMR Assignments and Secondary Structure of Hen Egg White Lysozyme in Solution Redfield, Christina; Dobson, Christopher M. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr1093	dataset	January 1995
Protein Folding: A Perspective from Theory and Experiment Dobson, Christopher M.; Šali, Andrej; Karplus, Martin Angewandte Chemie International Edition, Vol. 37, Issue 7 https://doi.org/10.1002/(sici)1521-3773(19980420)37:7<868::aid-anie868>3.0.co;2-h	journal	April 1998
Erratum: Corrigendum: Behind the folding funnel diagram Karplus, Martin Nature Chemical Biology, Vol. 7, Issue 9 https://doi.org/10.1038/nchembio0911-648d	journal	August 2011

Cited By (9)

Influence of glycerol on the cooling effect of pair hydrophobicity in water: relevance to proteins’ stabilization at low temperature Dubey, Vikas; Daschakraborty, Snehasis Physical Chemistry Chemical Physics, Vol. 21, Issue 2 https://doi.org/10.1039/c8cp06513f	journal	January 2019
Quantum Approach to Fast Protein-Folding Time ^* Lu, Li-Hua; Li, You-Quan Chinese Physics Letters, Vol. 36, Issue 8 https://doi.org/10.1088/0256-307x/36/8/080305	journal	August 2019
The Role of Hydrogen Bonding in the Folding/Unfolding Process of Hydrated Lysozyme: A Review of Recent NMR and FTIR Results Mallamace, Domenico; Fazio, Enza; Mallamace, Francesco International Journal of Molecular Sciences, Vol. 19, Issue 12 https://doi.org/10.3390/ijms19123825	journal	November 2018
Crystal elasto-plasticity on the Poincaré half-plane Arbib, Edoardo; Biscari, Paolo; Bortoloni, Luca International Journal of Plasticity, Vol. 130 https://doi.org/10.1016/j.ijplas.2020.102728	journal	July 2020
Unfolding and Refolding of Protein by a Combination of Ionic and Nonionic Surfactants Saha, Debasish; Ray, Debes; Kohlbrecher, Joachim ACS Omega, Vol. 3, Issue 7 https://doi.org/10.1021/acsomega.8b00630	journal	July 2018
Genuine antiplasticizing effect of water on a glass-former drug Ruiz, Guadalupe N.; Romanini, Michela; Hauptmann, Astrid Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07643-5	journal	August 2017
Alpha-Synuclein is a Target of Fic-mediated Adenylylation/AMPylation: Implications for Parkinson's Disease Mattoo, Seema; Sanyal, Anwesha; Dutta, Sayan Journal of Molecular Biology https://doi.org/10.1101/525659	journal	January 2019
Glutamine Hydrolysis by Imidazole Glycerol Phosphate Synthase Displays Temperature Dependent Allosteric Activation Lisi, George P.; Currier, Allen A.; Loria, J. Patrick Frontiers in Molecular Biosciences, Vol. 5 https://doi.org/10.3389/fmolb.2018.00004	journal	February 2018
Searching the solution landscape by generalized high-index saddle dynamics Yin, Jianyuan; Yu, Bing; Zhang, Lei arXiv https://doi.org/10.48550/arxiv.2002.10690	text	January 2020

Similar Records

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 · OSTI ID:1437126

Pulavarti, Surya V.S.R.K.; Maguire, Jack B.; Yuen, Shirley; +10 more

Energy barriers, cooperativity, and hidden intermediates in the folding of small proteins

Journal Article · Fri Feb 17 00:00:00 EST 2006 · Biochemical and Biophysical Research Communications · OSTI ID:1437126

Yawen, Bai

pH-Induced denaturation of proteins: A single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme

Journal Article · Tue Mar 06 00:00:00 EST 1990 · Biochemistry; (USA) · OSTI ID:1437126

Anderson, D E; Becktel, W J; Dahlquist, F W

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
protein folding
proton NMR
energy landscape
hydration water

Title: Energy landscape in protein folding and unfolding

Citation Formats

References (41)

Cited By (9)

Similar Records

Related Subjects