GB1 hairpin kinetics: capturing the folding pathway with molecular dynamics, replica exchange and optimal dimensionality reduction

References

• Ahalawat, N., & Mondal, J. (2018). Assessment and optimization of collective variables for protein conformational landscape: GB1 beta-hairpin as a case study. The Journal of Chemical Physics, 149(9), 094101.
   PubMed Web of Science ®Google Scholar
• Best, R. B., & Mittal, J. (2011). Free-energy landscape of the GB1 hairpin in all-atom explicit solvent simulations with different force fields: Similarities and differences. Proteins, 79(4), 1318–1328. https://doi.org/10.1002/prot.22972
   PubMed Web of Science ®Google Scholar
• Blanco, F. J., Jimenez, M. A., Pineda, A., Rico, M., Santoro, J., & Nieto, J. L. (1994). NMR solution structure of the isolated N-terminal fragment of protein-G B1 domain. Evidence of trifluoroethanol induced native-like beta-hairpin formation. Biochemistry, 33(19), 6004–6014. https://doi.org/10.1021/bi00185a041
   PubMed Web of Science ®Google Scholar
• Buchete, N. V., & Hummer, G. (2008). Coarse master equations for peptide folding dynamics. The Journal of Physical Chemistry B, 112(19), 6057–6069. https://doi.org/10.1021/jp0761665
   PubMed Web of Science ®Google Scholar
• Cai, X., & Han, W. (2022). Development of a hybrid-resolution force field for peptide self-assembly simulations: Optimizing peptide-peptide and peptide-solvent interactions. Journal of Chemical Information and Modeling, 62(11), 2744–2760. https://doi.org/10.1021/acs.jcim.2c00066
   PubMed Web of Science ®Google Scholar
• Daidone, I., Thukral, L., Smith, J. C., & Amadei, A. (2015). Monitoring the folding kinetics of a beta-hairpin by time-resolved IR spectroscopy in silico. The Journal of Physical Chemistry B, 119(14), 4849–4856. https://doi.org/10.1021/acs.jpcb.5b01477
   PubMed Web of Science ®Google Scholar
• Darden, T., Perera, L., Li, L. P., & Pedersen, L. (1999). New tricks for modelers from the crystallography toolkit: The particle mesh Ewald algorithm and its use in nucleic acid simulations. Structure, 7(3), R55–R60. https://doi.org/10.1016/S0969-2126(99)80033-1
   PubMed Web of Science ®Google Scholar
• De Sancho, D., Mittal, J., & Best, R. B. (2013). Folding kinetics and unfolded state dynamics of the GB1 hairpin from molecular simulation. Journal of Chemical Theory and Computation, 9(3), 1743–1753. https://doi.org/10.1021/ct301033r
   PubMed Web of Science ®Google Scholar
• Dellago, C., Bolhuis, P. G., & Geissler, P. L. (2002). Transition path sampling. Advances in Chemical Physics. 123, 1–78.
   Web of Science ®Google Scholar
• Du, D., Zhu, Y., Huang, C. Y., & Gai, F. (2004). Understanding the key factors that control the rate of beta-hairpin folding. Proceedings of the National Academy of Sciences of the United States of America, 101(45), 15915–15920. https://doi.org/10.1073/pnas.0405904101
   PubMed Web of Science ®Google Scholar
• Eaton, W. A. (2021). Modern kinetics and mechanism of protein folding: A retrospective. The Journal of Physical Chemistry B, 125(14), 3452–3467. https://doi.org/10.1021/acs.jpcb.1c00206
   PubMed Web of Science ®Google Scholar
• Gronenborn, A. M., Filpula, D. R., Essig, N. Z., Achari, A., Whitlow, M., Wingfield, P. T., & Clore, G. M. (1991). A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science (New York, N.Y.), 253(5020), 657–661. https://doi.org/10.1126/science.1871600
   PubMed Web of Science ®Google Scholar
• Hazel, A. J., Walters, E. T., Rowley, C. N., & Gumbart, J. C. (2018). Folding free energy landscapes of beta-sheets with non-polarizable and polarizable CHARMM force fields. The Journal of Chemical Physics, 149(7), 072317.
   PubMed Web of Science ®Google Scholar
• Hegefeld, W. A., Chen, S. E., DeLeon, K. Y., Kuczera, K., & Jas, G. S. (2010). Helix formation in a pentapeptide experiment and force-field dependent dynamics. The Journal of Physical Chemistry A, 114(47), 12391–12402. https://doi.org/10.1021/jp102612d
   PubMed Web of Science ®Google Scholar
• Howlett, D. R. (2003). Misfolding in disease: Cause or response? Current Medicinal Chemistry-Immunology, Endocrine & Metabolic Agents, 3(4), 371–383. https://doi.org/10.2174/1568013033483285
   Google Scholar
• Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., de Groot, B. L., Grubmuller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73. https://doi.org/10.1038/nmeth.4067
   PubMed Web of Science ®Google Scholar
• Hummer, G., & Szabo, A. (2015). Optimal dimensionality reduction of multistate kinetic and Markov-state models. The Journal of Physical Chemistry B, 119(29), 9029–9037. https://doi.org/10.1021/jp508375q
   PubMed Web of Science ®Google Scholar
• Jas, G. S., Childs, E. W., & Kuczera, K. (2021b). Probing coupled motions of peptides in solution with fluorescence anisotropy decay and molecular dynamics simulation. Chemical Physics, 541, 111018.
   Web of Science ®Google Scholar
• Jas, G. S., Childs, E. W., Middaugh, C. R., & Kuczera, K. (2021a). Dissecting multiple pathways in the relaxation dynamics of helix < = = >coil transitions with optimum dimensionality reduction. Biomolecules, 11(9), 1351.
   PubMed Web of Science ®Google Scholar
• Jas, G. S., Eaton, W. A., & Hofrichter, J. (2001). Effect of viscosity on the kinetics of alpha-helix and beta-hairpin formation. The Journal of Physical Chemistry B, 105(1), 261–272. https://doi.org/10.1021/jp0022048
   Web of Science ®Google Scholar
• Jas, G. S., Hegefeld, W. A., Middaugh, C. R., Johnson, C. K., & Kuczera, K. (2014a). Detailed microscopic unfolding pathways of an alpha-helix and a beta-hairpin: Direct observation and molecular dynamics. The Journal of Physical Chemistry B, 118(26), 7233–7246. https://doi.org/10.1021/jp500955z
   PubMed Web of Science ®Google Scholar
• Jas, G. S., & Kuczera, K. (2018a). Helix-coil transition courses through multiple pathways and intermediates: Fast kinetic measurements and dimensionality reduction. The Journal of Physical Chemistry B, 122(48), 10806–10816. https://doi.org/10.1021/acs.jpcb.8b07924
   PubMed Web of Science ®Google Scholar
• Jas, G. S., & Kuczera, K. (2018b). Deprotonation of a single amino acid residue induces significant stability in an alpha-helical heteropeptide. The Journal of Physical Chemistry B, 122(49), 11508–11518. https://doi.org/10.1021/acs.jpcb.8b07418
   PubMed Web of Science ®Google Scholar
• Jas, G. S., Middaugh, C. R., & Kuczera, K. (2014b). Non-exponential kinetics and a complete folding pathway of an alpha-helical heteropeptide: Direct observation and comprehensive molecular dynamics. The Journal of Physical Chemistry B, 118(2), 639–647. https://doi.org/10.1021/jp410934g
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of Simple Potential Functions for Simulating Liquid Water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kmiecik, S., & Kolinski, A. (2008). Folding pathway of the B1 domain of protein G explored by multiscale modeling. Biophysical Journal, 94(3), 726–736. https://doi.org/10.1529/biophysj.107.116095
   PubMed Web of Science ®Google Scholar
• Kube, S., & Weber, M. (2007). A coarse graining method for the identification of transition rates between molecular conformations. The Journal of Chemical Physics, 126(2), 024103.
   PubMed Web of Science ®Google Scholar
• Kuczera, K., Szoszkiewicz, R., He, J. Y., & Jas, G. S. (2021). Length dependent folding kinetics of alanine-based helical peptides from optimal dimensionality reduction. Life-Basel, 11(5), 385. https://doi.org/10.3390/life11050385
   PubMed Web of Science ®Google Scholar
• Kutzner, C., Pall, S., Fechner, M., Esztermann, A., de Groot, B. L., & Grubmuller, H. (2015). Best bang for your buck: GPU nodes for GROMACS biomolecular simulations. Journal of Computational Chemistry, 36(26), 1990–2008. https://doi.org/10.1002/jcc.24030
   PubMed Web of Science ®Google Scholar
• Lewandowska, A., Ołdziej, S., Liwo, A., & Scheraga, H. A. (2010). Mechanism of formation of the C-terminal beta-hairpin of the B3 domain of the immunoglobulin-binding protein G from Streptococcus. IV. Implication for the mechanism of folding of the parent protein. Biopolymers, 93(5), 469–480. https://doi.org/10.1002/bip.21365
   PubMed Web of Science ®Google Scholar
• Lewandowska, A., Ołdziej, S., Liwo, A., & Scheraga, H. A. (2010). beta-hairpin-forming peptides: Models of early stages of protein folding. Biophysical Chemistry, 151(1–2), 1–9. https://doi.org/10.1016/j.bpc.2010.05.001
   PubMed Web of Science ®Google Scholar
• Louis, J. M., Byeon, I. J., Baxa, U., & Gronenborn, A. M. (2005). The GB1 amyloid fibril: Recruitment of the peripheral beta-strands of the domain swapped dimer into the polymeric interface. Journal of Molecular Biology, 348(3), 687–698. https://doi.org/10.1016/j.jmb.2005.02.071
   PubMed Web of Science ®Google Scholar
• Lwin, T. Z., & Luo, R. (2006). Force field influences in beta-hairpin folding simulations. Protein Science: A Publication of the Protein Society, 15(11), 2642–2655. https://doi.org/10.1110/ps.062438006
   PubMed Web of Science ®Google Scholar
• Munoz, V., Thompson, P. A., Hofrichter, J., & Eaton, W. A. (1997). Folding dynamics and mechanism of beta-hairpin formation. Nature, 390(6656), 196–199. https://doi.org/10.1038/36626
   PubMed Web of Science ®Google Scholar
• Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/bioinformatics/btt055
   PubMed Web of Science ®Google Scholar
• Senne, M., Trendelkamp-Schroer, B., Mey, A. S. J. S., Schutte, C., & Noe, F. (2012). EMMA: A software package for Markov model building and analysis. Journal of Chemical Theory and Computation, 8(7), 2223–2238. https://doi.org/10.1021/ct300274u
   PubMed Web of Science ®Google Scholar
• Soranno, A., Cabassi, F., Orselli, M. E., Cellmer, T., Gori, A., Longhi, R., & Buscaglia, M. (2018). Dynamics of structural elements of GB1 beta-hairpin revealed by tryptophan-cysteine contact formation experiments. The Journal of Physical Chemistry B, 122(49), 11468–11477. https://doi.org/10.1021/acs.jpcb.8b07399
   PubMed Web of Science ®Google Scholar
• Thukral, L., Daidone, I., & Smith, J. C. (2011). Structured pathway across the transition state for peptide folding revealed by molecular dynamics simulations. PLoS Computational Biology, 7(9), e1002137. https://doi.org/10.1371/journal.pcbi.1002137
   PubMed Web of Science ®Google Scholar
• Vanden-Eijnden, E. (2014). Transition path theory. Advances in Experimental Medicine and Biology, 797, 91–100. https://doi.org/10.1007/978-94-007-7606-7_7
   PubMed Web of Science ®Google Scholar
• Wei, G. H., Mousseau, N., & Derreumaux, P. (2004). Complex folding pathways in a simple beta-hairpin. Proteins-Structure Function and Bioinformatics, 56(3), 464–474. https://doi.org/10.1002/prot.20127
   PubMed Web of Science ®Google Scholar
• Weinan, E., & Vanden-Eijnden, E. (2010). Transition-path theory and path-finding algorithms for the study of rare events. Annual Review of Physical Chemistry, 61, 391–420. https://doi.org/10.1146/annurev.physchem.040808.090412
   PubMed Web of Science ®Google Scholar