A shorter peptide model from staphylococcal nuclease for the folding–unfolding equilibrium of a β-hairpin shows that unfolded state has significant contribution from compact conformational states

Amadei, 1993, Essential dynamics of proteins, Proteins, 17, 412, 10.1002/prot.340170408 Amadei, 1999, On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins’ molecular dynamics simulations, Proteins, 36, 419, 10.1002/(SICI)1097-0134(19990901)36:4<419::AID-PROT5>3.0.CO;2-U Anil, 2006, The unfolded state of NTL9 is compact in the absence of denaturant, Biochemistry, 45, 10110, 10.1021/bi060636o Bai, 2001, Structural and dynamic characterization of an unfolded state of poplar apo-plastocyanin formed under nondenaturing conditions, Protein Sci., 10, 1056, 10.1110/ps.00601 Berendsen, 1981, Interaction Models for Water in Relation to Protein Hydration, 331 Berendsen, 1984, Molecular dynamics with coupling to an external bath, J. Chem. Phys., 81, 3684, 10.1063/1.448118 Bolhuis, 2005, Kinetic pathways of beta-hairpin (un)folding in explicit solvent, Biophys. J., 88, 50, 10.1529/biophysj.104.048744 Ceruso, 1999, Mechanics and dynamics of B1 domain of protein G: role of packing and surface hydrophobic residues, Protein Sci., 8, 147, 10.1110/ps.8.1.147 Choy, 2002, Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques, J. Mol. Biol., 316, 101, 10.1006/jmbi.2001.5328 Daggett, 2002, Molecular dynamics simulations of the protein unfolding/folding reaction, Acc. Chem. Res., 35, 422, 10.1021/ar0100834 Daggett, 2006, Protein folding-simulation, Chem. Rev., 106, 1898, 10.1021/cr0404242 Dai, 2004, Searching for folding initiation sites of staphylococcal nuclease: a study of N-terminal short fragments, Biopolymers, 75, 229, 10.1002/bip.20121 Daidone, 2004, Beta-hairpin conformation of fibrillogenic peptides: structure and alpha-beta transition mechanism revealed by molecular dynamics simulations, Proteins, 57, 198, 10.1002/prot.20178 Daidone, 2005, Thermodynamic and kinetic characterization of a beta-hairpin peptide in solution: an extended phase space sampling by molecular dynamics simulations in explicit water, Proteins, 59, 510, 10.1002/prot.20427 Darden, 1993, Particle mesh Ewald: an N-log(N) method for Ewald sums in large systems, J. Chem. Phys., 98, 10089, 10.1063/1.464397 de Groot, 1996, An extended sampling of the configurational space of HPr from E. coli, Proteins, 26, 314, 10.1002/(SICI)1097-0134(199611)26:3<314::AID-PROT7>3.0.CO;2-D Dill, 1995, Principles of protein folding—a perspective from simple exact models, Protein Sci., 4, 561, 10.1002/pro.5560040401 Dinner, 1999, Understanding beta-hairpin formation, Proc. Natl. Acad. Sci. USA, 96, 9068, 10.1073/pnas.96.16.9068 Dobson, 1998, Protein folding: a perspective from theory and experiment., Angew. Chem. Int. Ed., 37, 869, 10.1002/(SICI)1521-3773(19980420)37:7<868::AID-ANIE868>3.0.CO;2-H Du, 2004, Understanding the key factors that control the rate of beta-hairpin folding, Proc. Natl. Acad. Sci. USA, 101, 15915, 10.1073/pnas.0405904101 Du, 2006, Understanding the mechanism of beta-hairpin folding via phi-value analysis, Biochemistry, 45, 2668, 10.1021/bi052039s Eaton, 1996, Fast events in protein folding, Structure, 4, 1133, 10.1016/S0969-2126(96)00121-9 Essmann, 1995, A smooth particle mesh Ewald method, J. Chem. Phys., 103, 8577, 10.1063/1.470117 Feng, 2003, Native-like partially folded conformations and folding process revealed in the N-terminal large fragments of staphylococcal nuclease: a study by NMR spectroscopy, J. Mol. Biol., 330, 821, 10.1016/S0022-2836(03)00660-0 Fierz, 2007, Loop formation in unfolded polypeptide chains on the picoseconds to microseconds time scale, Proc. Natl. Acad. Sci. USA, 104, 2163, 10.1073/pnas.0611087104 Francis, 2006, Characterization of the residual structure in the unfolded state of the Delta131Delta fragment of staphylococcal nuclease, Proteins, 65, 145, 10.1002/prot.21077 Fuchs, 2006, Kinetics and thermodynamics of type VIII beta-turn formation: a CD, NMR, and microsecond explicit molecular dynamics study of the GDNP tetrapeptide, Biophys. J., 90, 2745, 10.1529/biophysj.105.074401 Galzitskaya, 2002, Alpha-helix and beta-hairpin Folding from experiment, analytical theory and molecular dynamics simulations, Curr. Protein Pept. Sci., 3, 191, 10.2174/1389203024605340 Garcia, 2001, Exploring the energy landscape of a beta hairpin in explicit solvent, Proteins, 42, 345, 10.1002/1097-0134(20010215)42:3<345::AID-PROT50>3.0.CO;2-H Garcia, 2001, NMR and SAXS characterization of the denatured state of the chemotactic protein CheY: implications for protein folding initiation, Protein Sci., 10, 1100, 10.1110/ps.52701 Hammarstrom, 2000, Is the unfolded state the Rosetta Stone of the protein folding problem?, Biochem. Biophys. Res. Commun., 276, 393, 10.1006/bbrc.2000.3360 Hess, 1997, LINCS: a linear constraint solver for molecular simulations, J. Comp. Chem., 18, 1463, 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H Hughes, 2006, Model systems for beta-hairpins and beta-sheets, Curr. Opin. Struct. Biol., 16, 514, 10.1016/j.sbi.2006.06.008 Humphrey, W., Dalke, A., Schulten, K., 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1), 33–38, 27–28. Kabsch, 1983, Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features, Biopolymers, 22, 2577, 10.1002/bip.360221211 Karplus, 1995, Theoretical studies of protein folding and unfolding, Curr. Opin. Struct. Biol., 5, 58, 10.1016/0959-440X(95)80010-X Klein-Seetharaman, 2002, Long-range interactions within a nonnative protein, Science, 295, 1719, 10.1126/science.1067680 Klimov, 2000, Mechanisms and kinetics of beta-hairpin formation, Proc. Natl. Acad. Sci. USA, 97, 2544, 10.1073/pnas.97.6.2544 Kohn, 2004, Random-coil behavior and the dimensions of chemically unfolded proteins, Proc. Natl. Acad. Sci. USA, 101, 12491, 10.1073/pnas.0403643101 Lindahl, 2001, Gromacs 3.0: a package for molecular simulation and trajectory analysis, J. Mol. Model., 7, 306, 10.1007/s008940100045 Loll, 1989, The crystal structure of the ternary complex of staphylococcal nuclease, Ca2+, and the inhibitor pdTp, refined at 1.65Å, Proteins, 5, 183, 10.1002/prot.340050302 Luisi, 1999, Conformational analysis of a set of peptides corresponding to the entire primary sequence of the N-terminal domain of the ribosomal protein L9: evidence for stable native-like secondary structure in the unfolded state, J. Mol. Biol., 287, 395, 10.1006/jmbi.1999.2595 Mayor, 2003, The denatured state of Engrailed Homeodomain under denaturing and native conditions, J. Mol. Biol., 333, 977, 10.1016/j.jmb.2003.08.062 Merlino, 2002, Global and local motions in ribonuclease A: a molecular dynamics study, Biopolymers, 65, 274, 10.1002/bip.10225 Mok, 1999, NOE data demonstrating a compact unfolded state for an SH3 domain under non-denaturing conditions, J. Mol. Biol., 289, 619, 10.1006/jmbi.1999.2769 Nguyen, 2005, Free energy landscape and folding mechanism of a beta-hairpin in explicit water: a replica exchange molecular dynamics study, Proteins, 61, 795, 10.1002/prot.20696 Ohnishi, 2004, Direct demonstration of structural similarity between native and denatured eglin C, Biochemistry, 43, 4064, 10.1021/bi049879b Olsen, 2005, Hairpin folding rates reflect mutations within and remote from the turn region, Proc. Natl. Acad. Sci. USA, 102, 15483, 10.1073/pnas.0504392102 Patel, 2007, Loop propensity of the sequence YKGQP from staphylococcal nuclease: implications for the folding of nuclease, J. Pept. Sci., 13, 679, 10.1002/psc.907 Patel, 2006, Beta-Hairpins with native-like and non-native hydrogen bonding patterns could form during the refolding of staphylococcal nuclease, J. Mol. Graph. Model., 25, 103, 10.1016/j.jmgm.2005.11.007 Qi, 1998, The burst phase in ribonuclease A folding and solvent dependence of the unfolded state, Nat. Struct. Biol., 5, 882, 10.1038/2321 Radford, 2000, Protein folding: progress made and promises ahead, Trends Biochem. Sci., 25, 611, 10.1016/S0968-0004(00)01707-2 Religa, 2005, Solution structure of a protein denatured state and folding intermediate, Nature, 437, 1053, 10.1038/nature04054 Roccatano, 2004, Structural and dynamic properties of the CAGQW peptide in water: a molecular dynamics simulation study using different force fields, J. Phys. Chem. B, 108, 18734, 10.1021/jp0475077 Roder, H., Maki, K., Latypov, R.F., Cheng, H., Shastry, M.C.R., 2005. In: Buchner, J.K.T. (Ed.), Protein Folding Handbook, vol. 1. Wiley-VCH, pp. 491–535. Roder, 2006, Early events in protein folding explored by rapid mixing methods, Chem. Rev., 106, 1836, 10.1021/cr040430y Rose, G.D. (Ed.), 2002. Unfolded proteins, Adv. Protein Chem. 62, 1–389. Sali, 1994, How does a protein fold?, Nature, 369, 248, 10.1038/369248a0 Sallum, 2005, Sensitivity of NMR residual dipolar couplings to perturbations in folded and denatured staphylococcal nuclease, Biochemistry, 44, 6392, 10.1021/bi0473410 Santiveri, 2004, Beta-hairpin folding and stability: molecular dynamics simulations of designed peptides in aqueous solution, J. Pept. Sci., 10, 546, 10.1002/psc.564 Schonbrun, 2003, Fast protein folding kinetics, Proc. Natl. Acad. Sci. USA, 100, 12678, 10.1073/pnas.1735417100 Scott, 1999, The GROMOS biomolecular simulation program package, J. Phys. Chem. A, 103, 3596, 10.1021/jp984217f Segel, 1999, Characterization of transient intermediates in lysozyme folding with time-resolved small-angle X-ray scattering, J. Mol. Biol., 288, 489, 10.1006/jmbi.1999.2703 Seshasayee, 2006, Role of hydrophobic interactions and salt-bridges in beta-hairpin folding, J. Mol. Model., 12, 197, 10.1007/s00894-005-0018-6 Shortle, 2001, Persistence of native-like topology in a denatured protein in 8M urea, Science, 293, 487, 10.1126/science.1060438 Sosnick, 1996, Molecular collapse: the rate-limiting step in two-state cytochrome c folding, Proteins, 24, 413, 10.1002/(SICI)1097-0134(199604)24:4<413::AID-PROT1>3.0.CO;2-F Sosnick, 1997, Ultrafast signals in protein folding and the polypeptide contracted state, Proc. Natl. Acad. Sci. USA, 94, 8545, 10.1073/pnas.94.16.8545 Spector, 1999, Conformational analysis of peptide fragments derived from the peripheral subunit-binding domain from the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus: evidence for nonrandom structure in the unfolded state, Biopolymers, 49, 29, 10.1002/(SICI)1097-0282(199901)49:1<29::AID-BIP4>3.0.CO;2-7 Tang, 2004, Peptide models provide evidence for significant structure in the denatured state of a rapidly folding protein: the villin headpiece subdomain, Biochemistry, 43, 3264, 10.1021/bi035652p Tang, 2006, NMR characterization of a peptide model provides evidence for significant structure in the unfolded state of the villin headpiece helical subdomain, Biochemistry, 45, 6940, 10.1021/bi052484n van Gunsteren, 1996 van Gunsteren, 2001, The key to solving the protein-folding problem lies in an accurate description of the denatured state, Angew. Chem. Int. Ed., 40, 352, 10.1002/1521-3773(20010119)40:2<351::AID-ANIE351>3.0.CO;2-6 Wang, 2006, Probing the folding capacity and residual structures in 1–79 residues fragment of staphylococcal nuclease by biophysical and NMR methods, Biochimie, 88, 1343, 10.1016/j.biochi.2006.05.002 Wickstrom, 2006, The unfolded state of the villin headpiece helical subdomain: computational studies of the role of locally stabilized structure, J. Mol. Biol., 360, 1094, 10.1016/j.jmb.2006.04.070 Wright, 1988, Conformation of peptide fragments of proteins in aqueous solution: implications for initiation of protein folding, Biochemistry, 27, 7167, 10.1021/bi00419a001 Wu, 2004, Beta-hairpin folding mechanism of a nine-residue peptide revealed from molecular dynamics simulations in explicit water, Biophys. J., 86, 1946, 10.1016/S0006-3495(04)74258-7 Wu, 2002, Direct observation of the folding and unfolding of a β-hairpin in explicit water through computer simulation, J. Am. Chem. Soc., 124, 5282, 10.1021/ja0257321 Yoda, 2007, Cooperative folding mechanism of a beta-hairpin peptide studied by a multicanonical replica-exchange molecular dynamics simulation, Proteins, 66, 846, 10.1002/prot.21264 Zagrovic, 2001, Beta-hairpin folding simulations in atomistic detail using an implicit solvent model, J. Mol. Biol., 313, 151, 10.1006/jmbi.2001.5033 Zagrovic, 2002, Native-like mean structure in the unfolded ensemble of small proteins, J. Mol. Biol., 323, 153, 10.1016/S0022-2836(02)00888-4 Zhang, 2006, Folding mechanism of beta-hairpins studied by replica exchange molecular simulations, Proteins, 62, 672, 10.1002/prot.20813 Zhou, 2001, The free energy landscape for beta hairpin folding in explicit water, Proc. Natl. Acad. Sci. USA, 98, 14931, 10.1073/pnas.201543998