Mimicking titration experiments with MD simulations: A protocol for the investigation of pH-dependent effects on proteins

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Socher, Eileen ^a   Sticht, Heinrich ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MICROCOCCAL NUCLEASE;

CHEMISTRY; COMPUTER SIMULATION; ENZYMOLOGY; MOLECULAR DYNAMICS; PH; STAPHYLOCOCCUS;

BACTERIAL PROTEINS; COMPUTER SIMULATION; HYDROGEN-ION CONCENTRATION; MICROCOCCAL NUCLEASE; MOLECULAR DYNAMICS SIMULATION; STAPHYLOCOCCUS;

EID: 84960145532     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22523     Document Type: Article

References (42)

1. Hong, W. Wu, Y. E. Fu, X., Chang, Z. Chaperone-dependent mechanisms for acid resistance in enteric bacteria. Trends Microbiol. 20, 328-335 (2012).
2. Roche, S. Bressanelli, S. Rey, F. A., Gaudin, Y. Crystal Structure of the Low-pH Form of the Vesicular Stomatitis Virus Glycoprotein G. Science (Washington, DC, US) 313, 187-191 (2006).
3. White, J., Helenius, A. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc. Natl. Acad. Sci. USA 77, 3273-3277 (1980).
4. Thomson, C. A., Ananthanarayanan, V. S. Structure-function studies on Hsp47: pH-dependent inhibition of collagen fibril formation in vitro. Biochem. J. 349 Pt 3, 877-883 (2000).
5. Tournaire-Roux, C. et al. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature (London, UK) 425, 393-397 (2003).
6. Mongan, J. Case, D. A., McCammon, J. A. Constant pH Molecular Dynamics in Generalized Born Implicit Solvent. J. Comput. Chem. 25, 2038-2048 (2004).
7. Mongan, J., Case, D. A. Biomolecular simulations at constant pH. Curr. Opin. Struct. Biol. 15, 157-163 (2005).
8. Case, D. A. et al. AMBER 12 (University of California, San Francisco, 2012).
9. Chu, W.-T. et al. Constant pH molecular dynamics (CpHMD) and molecular docking studies of CquiOBP1 pH-induced ligand releasing mechanism. J. Mol. Model. 19, 1301-1309 (2013).
10. Vila-Vicosa, D. Teixeira, V. H. Santos, H. A. F., Machuqueiro, M. Conformational Study of GSH and GSSG Using Constant-pH Molecular Dynamics Simulations. J. Phys. Chem. B 117, 7507-7517 (2013).
11. Williams, S. L. Blachly, P. G., McCammon, J. A. Measuring the successes and deficiencies of constant pH molecular dynamics: A blind prediction study. Proteins: Struct. Funct. Bioinf. 79, 3381-3388 (2011).
12. Swails, J. M. York, D. M., Roitberg, A. E. Constant pH Replica Exchange Molecular Dynamics in Explicit Solvent Using Discrete Protonation States: Implementation, Testing, and Validation. J. Chem. Theory Comput. 10, 1341-1352 (2014).
13. Meng, Y., Roitberg, A. E. Constant pH replica exchange molecular dynamics in biomolecules using a discrete protonation model. J. Chem. Theory Comput. 6, 1401-1412 (2010).
14. Dashti, D. S. Meng, Y., Roitberg, A. E. pH-Replica Exchange Molecular Dynamics In Proteins Using A Discrete Protonation Method. J. Phys. Chem. B 116, 8805-8811 (2012).
15. Lee, J. Miller, B. T. Damjanovi, A., Brooks, B. R. Enhancing Constant-pH Simulation in Explicit Solvent with a Two-Dimensional Replica Exchange Method. J. Chem. Theory Comput. 11, 2560-2574 (2015).
16. Castaneda, C. A. et al. Molecular determinants of the pKa values of Asp and Glu residues in staphylococcal nuclease. Proteins: Struct. Funct. Bioinf. 77, 570-588 (2009).
17. Demchuk, E., Wade, R. C. Improving the Continuum Dielectric Approach to Calculating pKas of Ionizable Groups in Proteins. J. Phys. Chem. 100, 17373-17387 (1996).
18. Webb, H. et al. Remeasuring HEWL pKa values by NMR spectroscopy: Methods, analysis, accuracy, and implications for theoretical pKa calculations. Proteins: Struct. Funct. Bioinf. 79, 685-702 (2011).
19. Gajiwala, K. S., Burley, S. K. HDEA, a Periplasmic Protein that Supports Acid Resistance in Pathogenic Enteric Bacteria. J. Mol. Biol. 295, 605-612 (2000).
20. Hong, W. et al. Periplasmic Protein HdeA Exhibits Chaperone-like Activity Exclusively within Stomach pH Range by Transforming into Disordered Conformation. J. Biol. Chem. 280, 27029-27034 (2005).
21. Ahlstrom, L. S. Law, S. M. Dickson, A., Brooks, Charles L 3rd. Multiscale Modeling of a Conditionally Disordered pH-Sensing Chaperone. J. Mol. Biol. 427, 1670-1680 (2015).
22. Garrison, M. A., Crowhurst, K. A. NMR-monitored titration of acid-stress bacterial chaperone HdeA reveals that Asp and Glu charge neutralization produces a loosened dimer structure in preparation for protein unfolding and chaperone activation. Protein Sci. 23, 167-178 (2014).
23. Baptista, A. M. Martel, P. J., Petersen, S. B. Simulation of Protein Conformational Freedom as a Function of pH: Constant-pH Molecular Dynamics Using Implicit Titration. Proteins: Struct. Funct. Genet. 27, 523-544 (1997).
24. Baptista, A. M. Teixeira, V. H., Soares, C. M. Constant-pH molecular dynamics using stochastic titration. J. Chem. Phys. 117, 4184 (2002).
25. Lee, M. S. Salsbury, F. R. JR & Brooks, C. L. S. Constant-pH Molecular Dynamics Using Continuous Titration Coordinates. Proteins: Struct. Funct. Bioinf. 56, 738-752 (2004).
26. Donnini, S. Tegeler, F. Groenhof, G., Grubmuller, H. Constant pH Molecular Dynamics in Explicit Solvent with lambda-Dynamics. J. Chem. Theory Comput. 7, 1962-1978 (2011).
27. Khandogin, J., Brooks, C. L. S. Constant pH molecular dynamics with proton tautomerism. Biophys. J. 89, 141-157 (2005).
28. Khandogin, J., Brooks, C. L. S. Toward the Accurate First-Principles Prediction of Ionization Equilibria in Proteins. Biochemistry 45, 9363-9373 (2006).
29. Berman, H. M. et al. The Protein Data Bank. Nucleic Acids Res. 28, 235-242 (2000).
30. Artymiuk, P. J. Blake, C. C. F. Rice, D. W., Wilson, K. S. The Structures of the Monoclinic and Orthorhombic Forms of Hen Egg-White Lysozyme at 6 A Resolution. Acta Crystallogr. Sect. B: Struct. Crystallogr. Cryst. Chem. 38, 778-783 (1982).
31. Yang, F. Gustafson, K. R. Boyd, M. R., Wlodawer, A. Crystal structure of Escherichia coli HdeA. Nat. Struct. Biol. 5, 763-764 (1998).
32. Case, D. A. et al. AMBER 14 (University of California, San Francisco, 2014).
33. Hornak, V. et al. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters. Proteins: Struct. Funct. Bioinf. 65, 712-725 (2006).
34. Roe, D. R., Cheatham, T. E., III PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data. J. Chem. Theory Comput. 9, 3084-3095 (2013).
35. Humphrey, W. Dalke, A., Schulten, K. VMD: Visual Molecular Dynamics. J. Mol. Graphics 14, 33-38 (1996).
36. Onufriev, A. Case, D. A., Ullmann, G. M. A Novel View of pH Titration in Biomolecules. Biochemistry 40, 3413-3419 (2001).
37. Olsson, M. H. M. Sondergaard, C. R. Rostkowski, M., Jensen, J. H. PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions. J. Chem. Theory Comput. 7, 525-537 (2011).
38. Sondergaard, C. R. Olsson, M. H. M. Rostkowski, M., Jensen, J. H. Improved Treatment of Ligands and Coupling Effects in Empirical Calculation and Rationalization of pKa Values. J. Chem. Theory Comput. 7, 2284-2295 (2011).
39. Bashford, D. Case, D. A. Dalvit, C. Tennant, L., Wright, P. E. Electrostatic Calculations of Side-Chain pKa Values in Myoglobin and Comparison with NMR Data for Histidines. Biochemistry. Biochemistry 32, 8045-8056 (1993).
40. McNutt, M. Mullins, L. S. Raushel, F. M., Pace, C. N. Contribution of Histidine Residues to the Conformational Stability of Ribonuclease T1 and Mutant Glu-58-Ala. Biochemistry 29, 7572-7576 (1990).
41. Stryer, L. Biochemie. 4th ed. (Spektrum Akad. Verl. Heidelberg [u.a. 1996).
42. Fitch, C. A. et al. Experimental pKa Values of Buried Residues: Analysis with Continuum Methods and Role of Water Penetration. Biophys. J. 82, 3289-3304 (2002).