Role of hydrophilic and hydrophobic contacts in folding of the second β‐hairpin fragment of protein G: Molecular dynamics simulation studies of an all‐atom model

Yaoqi Zhou; Apichart Linhananta

doi:10.1002/prot.10065

journal article Feb 28, 2002

Role of hydrophilic and hydrophobic contacts in folding of the second β‐hairpin fragment of protein G: Molecular dynamics simulation studies of an all‐atom model

Yaoqi Zhou

Apichart Linhananta

Proteins: Structure, Function, and Bioinformatics Vol. 47 No. 2 pp. 154-162 · Wiley

View at Publisher Save 10.1002/prot.10065

Abstract

AbstractPredicting the folding mechanism of the second β‐hairpin fragment of the Ig‐binding domain B of streptococcal protein G is unexpectedly challenging for simplified reduced models because the models developed so far indicated a different folding mechanism from what was suggested from high‐temperature unfolding and equilibrium free‐energy surface analysis based on established all‐atom empirical force fields in explicit or implicit solvent. This happened despite the use of empirical residue‐based interactions, multibody hydrophobic interactions, and inclusions of hydrogen bonding effects in the simplified models. This article employs a recently developed all‐atom (except nonpolar hydrogens) model interacting with simple square‐well potentials to fold the peptide fragment by molecular dynamics simulation methods. In this study, 193 out of 200 trajectories are folded at two reduced temperatures (3.5 and 3.7) close to the transition temperature T* ∼ 4.0. Each simulation takes <7 h of CPU time on a Pentium 800‐MHz PC. Folding of the new all‐atom model is found to be initiated by collapse before the formation of main‐chain hydrogen bonds. This verifies the mechanism proposed from previous all‐atom unfolding and equilibrium simulations. The new model further predicts that the collapse is initiated by two nucleation contacts (a hydrophilic contact between D46 and T49 and a hydrophobic contact between Y45 and F52), in agreement with recent NMR measurements. The results suggest that atomic packing and native contact interactions play a dominant role in folding mechanism. Proteins 2002;47:154–162. © 2002 Wiley‐Liss, Inc.

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References

44

[1]

Molecular dynamics simulations of unfolding and refolding of a β-hairpin fragment of protein G

Vijay S. Pande, Daniel S. Rokhsar

Proceedings of the National Academy of Sciences 10.1073/pnas.96.16.9062

[2]

Understanding β-hairpin formation

Aaron R. Dinner, Themis Lazaridis, Martin Karplus

Proceedings of the National Academy of Sciences 10.1073/pnas.96.16.9068

[3]

A molecular dynamics study of the 41‐56 β‐hairpin from B1 domain of protein G

Danilo Roccatano, Andrea Amadei, Alfredo Di Nola et al.

Protein Science 10.1110/ps.8.10.2130

[4]

Molecular dynamics simulations of a β-hairpin fragment of protein G: balance between side-chain and backbone forces 1 1Edited by F. E. Cohen

Buyong Ma, Ruth Nussinov

Journal of Molecular Biology 10.1006/jmbi.2000.3518

[5]

Exploring the energy landscape of a ? hairpin in explicit solvent

Angel E. Garc�a, Kevin Y. Sanbonmatsu

Proteins: Structure, Function, and Bioinformatics 10.1002/1097-0134(20010215)42:3<345::aid-prot50>3.0.co;2-h

[6]

Folding dynamics and mechanism of β-hairpin formation

Victor Muñoz, Peggy A. Thompson, James Hofrichter et al.

Nature 10.1038/36626

[7]

A simple model for calculating the kinetics of protein folding from three-dimensional structures

Victor Muñoz, William A. Eaton

Proceedings of the National Academy of Sciences 10.1073/pnas.96.20.11311

[8]

10.1002/(sici)1097-0134(19991115)37:3<325::aid-prot2>3.0.co;2-e

[9]

10.1006/jmbi.1999.3446

[10]

10.1073/pnas.190324897

[11]

10.1002/jcc.540070216

[12]

CHARMM: A program for macromolecular energy, minimization, and dynamics calculations

Bernard R. Brooks, Robert E. Bruccoleri, Barry D. Olafson et al.

Journal of Computational Chemistry 10.1002/jcc.540040211

[13]

10.1021/jp984217f

[14]

Dynamics and Thermodynamics of β-Hairpin Assembly: Insights from Various Simulation Techniques

Andrzej Kolinski, Bartosz Ilkowski, Jeffrey Skolnick

Biophysical Journal 10.1016/s0006-3495(99)77127-4

[15]

Mechanisms and kinetics of β-hairpin formation

Dmitri K. Klimov, D. Thirumalai

Proceedings of the National Academy of Sciences 10.1073/pnas.97.6.2544

[16]

10.1063/1.464706

[17]

10.1016/s1359-0278(98)00018-2

[18]

10.1093/protein/10.8.843

[19]

10.1006/jmbi.1999.3051

[20]

10.1073/pnas.190103297

[21]

10.1063/1.1314868

[22]

A short linear peptide that folds into a native stable β-hairpin in aqueous solution

Francisco J. Blanco, Germán Rivas, Luis Serrano

Nature Structural & Molecular Biology 10.1038/nsb0994-584

[23]

Thermodynamics of a β-hairpin structure: evidence for cooperative formation of folding nucleus

Shinya Honda, Naohiro Kobayashi, Eisuke Munekata

Journal of Molecular Biology 10.1006/jmbi.1999.3346

[24]

Role of Side-chains in the Cooperative β-Hairpin Folding of the Short C−Terminal Fragment Derived from Streptococcal Protein G

Naohiro Kobayashi, Shinya Honda, Hirofumi Yoshii et al.

Biochemistry 10.1021/bi000013p

[25]

10.1021/jp013824r

[26]

STUDIES ON PROTEIN FOLDING, UNFOLDING AND FLUCTUATIONS BY COMPUTER SIMULATION

Hiroshi Taketomi, Yuzo Ueda, Nobuhiro Gō

International Journal of Peptide and Protein Resea... 10.1111/j.1399-3011.1975.tb02465.x

[27]

10.1073/pnas.94.26.14429

[28]

10.1073/pnas.95.4.1490

[29]

10.1126/science.1871600

[30]

10.1063/1.472061

[31]

10.1063/1.1674820

[32]

10.1063/1.1725884

[33]

10.1006/jmbi.2001.4586

[34]

10.1006/jmbi.1999.2936

[35]

10.1063/1.474186

[36]

Optimized Monte Carlo data analysis

Alan M. Ferrenberg, Robert H. Swendsen

Physical Review Letters 10.1103/physrevlett.63.1195

[37]

The speed limit for protein folding measured by triplet–triplet energy transfer

Oliver Bieri, Jakob Wirz, Bruno Hellrung et al.

Proceedings of the National Academy of Sciences 10.1073/pnas.96.17.9597

[38]

Christopher M. Dobson, Fabrizio Chiti, Niccolò Taddei et al.

Nature Structural Biology 10.1038/14890

[39]

Three key residues form a critical contact network in a protein folding transition state

Michele Vendruscolo, Emanuele Paci, Christopher M. Dobson et al.

Nature 10.1038/35054591

[40]

Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy

M. Kirsten Frank, G. Marius Clore, Angela M. Gronenborn

Protein Science 10.1002/pro.5560041218

[41]

MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures

P. J. Kraulis

Journal of Applied Crystallography 10.1107/s0021889891004399

[42]

β-hairpin folding simulations in atomistic detail using an implicit solvent model 1 1Edited by F. Cohen

Bojan Zagrovic, Eric J Sorin, Vijay Pande

Journal of Molecular Biology 10.1006/jmbi.2001.5033

[43]

10.1016/s0006-3495(01)75896-1

[44]

The free energy landscape for β hairpin folding in explicit water

Ruhong Zhou, Bruce J. Berne, Robert Germain

Proceedings of the National Academy of Sciences 10.1073/pnas.201543998

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References

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Published: Feb 28, 2002
Vol/Issue: 47(2)
Pages: 154-162
License: View

Authors

Y

Yaoqi Zhou

Chinese Academy of Sciences

A

Apichart Linhananta

Cite This Article

Yaoqi Zhou, Apichart Linhananta (2002). Role of hydrophilic and hydrophobic contacts in folding of the second β‐hairpin fragment of protein G: Molecular dynamics simulation studies of an all‐atom model. Proteins: Structure, Function, and Bioinformatics, 47(2), 154-162. https://doi.org/10.1002/prot.10065

Role of hydrophilic and hydrophobic contacts in folding of the second β‐hairpin fragment of protein G: Molecular dynamics simulation studies of an all‐atom model

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