Fast Calculation of Protein–Protein Binding Free Energies Using Umbrella Sampling with a Coarse-Grained Model
Abstract
Determination of protein-protein binding affinity values is key to understanding various underlying biological phenomena, such as how missense variations change protein-protein binding. Most existing nonrigorous (fast) and rigorous (slow) methods that rely on all-atom representation of the proteins force the user to choose between speed and accuracy. In an attempt to achieve balance between speed and accuracy, we have combined rigorous umbrella sampling molecular dynamics simulation with a coarse-grained protein model. We predicted the effect of missense variations on binding affinity by selecting three protein-protein systems and comparing results to empirical relative binding affinity values and to nonrigorous modeling approaches. We obtained significant improvement both in our ability to discern stabilizing from destabilizing missense variations and in the correlation between predicted and experimental values compared to nonrigorous approaches. Overall our results suggest that using a rigorous affinity calculation method with coarse-grained protein models could offer fast and reliable predictions of protein-protein binding free energies.
- Authors:
-
- Center for Modeling Complex Interactions, University of Idaho, Moscow, Idaho 83844, United States
- Department of Physics, University of Idaho, Moscow, Idaho 83844, United States
- Publication Date:
- Research Org.:
- Univ. of Idaho, Moscow, ID (United States)
- Sponsoring Org.:
- USDOE Office of Nuclear Energy (NE)
- OSTI Identifier:
- 1417063
- Alternate Identifier(s):
- OSTI ID: 1508328
- Grant/Contract Number:
- AC07-05ID14517
- Resource Type:
- Published Article
- Journal Name:
- Journal of Chemical Theory and Computation
- Additional Journal Information:
- Journal Name: Journal of Chemical Theory and Computation Journal Volume: 14 Journal Issue: 2; Journal ID: ISSN 1549-9618
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Patel, Jagdish Suresh, and Ytreberg, F. Marty. Fast Calculation of Protein–Protein Binding Free Energies Using Umbrella Sampling with a Coarse-Grained Model. United States: N. p., 2018.
Web. doi:10.1021/acs.jctc.7b00660.
Patel, Jagdish Suresh, & Ytreberg, F. Marty. Fast Calculation of Protein–Protein Binding Free Energies Using Umbrella Sampling with a Coarse-Grained Model. United States. https://doi.org/10.1021/acs.jctc.7b00660
Patel, Jagdish Suresh, and Ytreberg, F. Marty. Tue .
"Fast Calculation of Protein–Protein Binding Free Energies Using Umbrella Sampling with a Coarse-Grained Model". United States. https://doi.org/10.1021/acs.jctc.7b00660.
@article{osti_1417063,
title = {Fast Calculation of Protein–Protein Binding Free Energies Using Umbrella Sampling with a Coarse-Grained Model},
author = {Patel, Jagdish Suresh and Ytreberg, F. Marty},
abstractNote = {Determination of protein-protein binding affinity values is key to understanding various underlying biological phenomena, such as how missense variations change protein-protein binding. Most existing nonrigorous (fast) and rigorous (slow) methods that rely on all-atom representation of the proteins force the user to choose between speed and accuracy. In an attempt to achieve balance between speed and accuracy, we have combined rigorous umbrella sampling molecular dynamics simulation with a coarse-grained protein model. We predicted the effect of missense variations on binding affinity by selecting three protein-protein systems and comparing results to empirical relative binding affinity values and to nonrigorous modeling approaches. We obtained significant improvement both in our ability to discern stabilizing from destabilizing missense variations and in the correlation between predicted and experimental values compared to nonrigorous approaches. Overall our results suggest that using a rigorous affinity calculation method with coarse-grained protein models could offer fast and reliable predictions of protein-protein binding free energies.},
doi = {10.1021/acs.jctc.7b00660},
journal = {Journal of Chemical Theory and Computation},
number = 2,
volume = 14,
place = {United States},
year = {Tue Jan 16 00:00:00 EST 2018},
month = {Tue Jan 16 00:00:00 EST 2018}
}
https://doi.org/10.1021/acs.jctc.7b00660
Web of Science
Figures / Tables:
Works referenced in this record:
Coarse-grain modelling of protein–protein interactions
journal, December 2013
- Baaden, Marc; Marrink, Siewert J.
- Current Opinion in Structural Biology, Vol. 23, Issue 6
Protein–protein interactions: scoring schemes and binding affinity
journal, June 2017
- Gromiha, M. Michael; Yugandhar, K.; Jemimah, Sherlyn
- Current Opinion in Structural Biology, Vol. 44
Present and future challenges and limitations in protein-protein docking: Challenges in Protein-Protein Docking
journal, August 2009
- Pons, Carles; Grosdidier, Solène; Solernou, Albert
- Proteins: Structure, Function, and Bioinformatics, Vol. 78, Issue 1
Protein-protein recognition: Crystal structural analysis of a barnase-barstar complex at 2.0-.ANG. resolution
journal, August 1994
- Buckle, Ashley M.; Schreiber, Gideon; Fersht, Alan R.
- Biochemistry, Vol. 33, Issue 30
Initiating a watch list for Ebola virus antibody escape mutations
journal, January 2016
- Miller, Craig R.; Johnson, Erin L.; Burke, Aran Z.
- PeerJ, Vol. 4
Efficient Determination of Protein–Protein Standard Binding Free Energies from First Principles
journal, July 2013
- Gumbart, James C.; Roux, Benoît; Chipot, Christophe
- Journal of Chemical Theory and Computation, Vol. 9, Issue 8
Molecular ‘time-machines’ to unravel key biological events for drug design: Molecular ‘time-machines’ for drug design
journal, May 2017
- Ganesan, Aravindhan; Coote, Michelle L.; Barakat, Khaled
- Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 7, Issue 4
Applying Physics-Based Scoring to Calculate Free Energies of Binding for Single Amino Acid Mutations in Protein-Protein Complexes
journal, December 2013
- Beard, Hege; Cholleti, Anuradha; Pearlman, David
- PLoS ONE, Vol. 8, Issue 12
GROMACS: Fast, flexible, and free
journal, January 2005
- Van Der Spoel, David; Lindahl, Erik; Hess, Berk
- Journal of Computational Chemistry, Vol. 26, Issue 16
Lipid-Modulated Sequence-Specific Association of Glycophorin A in Membranes
journal, July 2010
- Janosi, Lorant; Prakash, Anupam; Doxastakis, Manolis
- Biophysical Journal, Vol. 99, Issue 1
Comparative Protein Structure Modeling Using MODELLER
journal, June 2016
- Webb, Benjamin; Sali, Andrej
- Current Protocols in Bioinformatics, Vol. 54, Issue 1
Coarse-Graining Methods for Computational Biology
journal, May 2013
- Saunders, Marissa G.; Voth, Gregory A.
- Annual Review of Biophysics, Vol. 42, Issue 1
Interplay between binding affinity and kinetics in protein-protein interactions: Affinity-Kinetics Correlation of PPIs
journal, April 2016
- Cao, Huaiqing; Huang, Yongqi; Liu, Zhirong
- Proteins: Structure, Function, and Bioinformatics, Vol. 84, Issue 7
Conformational Changes in the Epidermal Growth Factor Receptor: Role of the Transmembrane Domain Investigated by Coarse-Grained MetaDynamics Free Energy Calculations
journal, August 2016
- Lelimousin, Mickaël; Limongelli, Vittorio; Sansom, Mark S. P.
- Journal of the American Chemical Society, Vol. 138, Issue 33
SKEMPI: a Structural Kinetic and Energetic database of Mutant Protein Interactions and its use in empirical models
journal, August 2012
- Moal, Iain H.; Fernández-Recio, Juan
- Bioinformatics, Vol. 28, Issue 20
Toward Optimized Potential Functions for Protein–Protein Interactions in Aqueous Solutions: Osmotic Second Virial Coefficient Calculations Using the MARTINI Coarse-Grained Force Field
journal, August 2013
- Stark, Austin C.; Andrews, Casey T.; Elcock, Adrian H.
- Journal of Chemical Theory and Computation, Vol. 9, Issue 9
Comparison of multiple Amber force fields and development of improved protein backbone parameters
journal, November 2006
- Hornak, Viktor; Abel, Robert; Okur, Asim
- Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 3
PLUMED 2: New feathers for an old bird
journal, February 2014
- Tribello, Gareth A.; Bonomi, Massimiliano; Branduardi, Davide
- Computer Physics Communications, Vol. 185, Issue 2
Structure of an antibody-antigen complex: crystal structure of the HyHEL-10 Fab-lysozyme complex.
journal, August 1989
- Padlan, E. A.; Silverton, E. W.; Sheriff, S.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 15
Characterization of single-nucleotide polymorphisms in coding regions of human genes
journal, July 1999
- Cargill, Michele; Altshuler, David; Ireland, James
- Nature Genetics, Vol. 22, Issue 3
Another Coarse Grain Model for Aqueous Solvation: WAT FOUR?
journal, November 2010
- Darré, Leonardo; Machado, Matías R.; Dans, Pablo D.
- Journal of Chemical Theory and Computation, Vol. 6, Issue 12
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Prediction of Protein-Protein Interface Sequence Diversity Using Flexible Backbone Computational Protein Design
journal, December 2008
- Humphris, Elisabeth L.; Kortemme, Tanja
- Structure, Vol. 16, Issue 12
The Free Energy Landscape of Dimerization of a Membrane Protein, NanC
journal, January 2014
- Dunton, Thomas A.; Goose, Joseph E.; Gavaghan, David J.
- PLoS Computational Biology, Vol. 10, Issue 1
Perspective on the Martini model
journal, January 2013
- Marrink, Siewert J.; Tieleman, D. Peter
- Chemical Society Reviews, Vol. 42, Issue 16
Are Scoring Functions in Protein−Protein Docking Ready To Predict Interactomes? Clues from a Novel Binding Affinity Benchmark
journal, May 2010
- Kastritis, Panagiotis L.; Bonvin, Alexandre M. J. J.
- Journal of Proteome Research, Vol. 9, Issue 5
X-ray crystal structure of the complex of human leukocyte elastase (PMN elastase) and the third domain of the turkey ovomucoid inhibitor.
journal, October 1986
- Bode, W.; Wei, A. Z.; Huber, R.
- The EMBO Journal, Vol. 5, Issue 10
A knowledge-based forcefield for protein-protein interface design
journal, October 2007
- Clark, Louis A.; van Vlijmen, Herman W. T.
- Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 4
Computational Design of Protein Interfaces with Receptor Flexibility
journal, January 2010
- Meroueh, Samy; Liang, Shide; Li, Liwei
- Biophysical Journal, Vol. 98, Issue 3
Canonical sampling through velocity rescaling
journal, January 2007
- Bussi, Giovanni; Donadio, Davide; Parrinello, Michele
- The Journal of Chemical Physics, Vol. 126, Issue 1
Predicting the Effect of Mutations on Protein-Protein Binding Interactions through Structure-Based Interface Profiles
journal, October 2015
- Brender, Jeffrey R.; Zhang, Yang
- PLOS Computational Biology, Vol. 11, Issue 10
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993
- Darden, Tom; York, Darrin; Pedersen, Lee
- The Journal of Chemical Physics, Vol. 98, Issue 12
The FoldX web server: an online force field
journal, July 2005
- Schymkowitz, J.; Borg, J.; Stricher, F.
- Nucleic Acids Research, Vol. 33, Issue Web Server
Umbrella sampling: Umbrella sampling
journal, May 2011
- Kästner, Johannes
- Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 1, Issue 6
THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method
journal, October 1992
- Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal
- Journal of Computational Chemistry, Vol. 13, Issue 8
BeAtMuSiC: prediction of changes in protein–protein binding affinity on mutations
journal, May 2013
- Dehouck, Yves; Kwasigroch, Jean Marc; Rooman, Marianne
- Nucleic Acids Research, Vol. 41, Issue W1
The power of coarse graining in biomolecular simulations: The power of coarse graining in biomolecular simulations
journal, August 2013
- Ingólfsson, Helgi I.; Lopez, Cesar A.; Uusitalo, Jaakko J.
- Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 4, Issue 3
Lipid-mediated interactions tune the association of glycophorin A helix and its disruptive mutants in membranes
journal, January 2010
- Sengupta, Durba; Marrink, Siewert J.
- Physical Chemistry Chemical Physics, Vol. 12, Issue 40
Progress and challenges in predicting protein-protein interaction sites
journal, December 2008
- Ezkurdia, I.; Bartoli, L.; Fariselli, P.
- Briefings in Bioinformatics, Vol. 10, Issue 3
Dimerization of the EphA1 Receptor Tyrosine Kinase Transmembrane Domain: Insights into the Mechanism of Receptor Activation
journal, October 2014
- Chavent, Matthieu; Chetwynd, Alan P.; Stansfeld, Phillip J.
- Biochemistry, Vol. 53, Issue 42
Polymorphic transitions in single crystals: A new molecular dynamics method
journal, December 1981
- Parrinello, M.; Rahman, A.
- Journal of Applied Physics, Vol. 52, Issue 12
Comment on ‘protein–protein binding affinity prediction from amino acid sequence’
journal, October 2014
- Moal, Iain H.; Fernández-Recio, Juan
- Bioinformatics, Vol. 31, Issue 4
SIRAH: A Structurally Unbiased Coarse-Grained Force Field for Proteins with Aqueous Solvation and Long-Range Electrostatics
journal, January 2015
- Darré, Leonardo; Machado, Matías Rodrigo; Brandner, Astrid Febe
- Journal of Chemical Theory and Computation, Vol. 11, Issue 2
PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations
journal, July 2004
- Dolinsky, T. J.; Nielsen, J. E.; McCammon, J. A.
- Nucleic Acids Research, Vol. 32, Issue Web Server, p. W665-W667
Coarse-grained versus atomistic simulations: realistic interaction free energies for real proteins
journal, November 2013
- May, Ali; Pool, René; van Dijk, Erik
- Bioinformatics, Vol. 30, Issue 3
Enhanced sampling techniques in biomolecular simulations
journal, November 2015
- Spiwok, Vojtech; Sucur, Zoran; Hosek, Petr
- Biotechnology Advances, Vol. 33, Issue 6
Self-Association of Models of Transmembrane Domains of ErbB Receptors in a Lipid Bilayer
journal, December 2010
- Prakash, Anupam; Janosi, Lorant; Doxastakis, Manolis
- Biophysical Journal, Vol. 99, Issue 11
Predicting the Impact of Missense Mutations on Protein–Protein Binding Affinity
journal, March 2014
- Li, Minghui; Petukh, Marharyta; Alexov, Emil
- Journal of Chemical Theory and Computation, Vol. 10, Issue 4
SIRAH tools: mapping, backmapping and visualization of coarse-grained models
journal, January 2016
- Machado, Matías R.; Pantano, Sergio
- Bioinformatics, Vol. 32, Issue 10
Enhanced sampling techniques in molecular dynamics simulations of biological systems
journal, May 2015
- Bernardi, Rafael C.; Melo, Marcelo C. R.; Schulten, Klaus
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1850, Issue 5
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