Stay Wet, Stay Stable? How Internal Water Helps the Stability of Thermophilic Proteins

Journal of Physical Chemistry B

Volumn 119, Issue 40, 2015, Pages 12760-12770

  Chakraborty, Debashree ^a   Taly, Antoine ^a   Sterpone, Fabio ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; HYDRATION; PROTEINS; WETTING;

COMPUTATIONAL INVESTIGATION; FREE-ENERGY CALCULATIONS; HOMOLOGOUS PROTEINS; MOLECULAR COMPLEXITY; MOLECULAR MECHANISM; THERMOPHILIC ENZYMES; THERMOPHILIC PROTEINS; WORKING TEMPERATURES;

STABILITY;

PROTEIN; WATER;

CHEMISTRY; MOLECULAR DYNAMICS; PROTEIN STABILITY;

MOLECULAR DYNAMICS SIMULATION; PROTEIN STABILITY; PROTEINS; WATER;

EID: 84944111716     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b05791     Document Type: Article

References (73)

1. Vieille, C.; Zeikus, G. J. Hyperthermophilic Enzymes: Sources, Uses, and Molecular Mechanisms for Thermostability Microbiol. Mol. Biol. Rev. 2001, 65, 1-43 10.1128/MMBR.65.1.1-43.2001
2. Kumar, S.; Nussinov, R. How do Thermophilic Proteins Deal with Heat? Cell. Mol. Life Sci. 2001, 58, 1216-1233 10.1007/PL00000935
3. Sterpone, F.; Melchionna, S. Thermophilic Proteins: Insight and Perspective from In Silico Experiments Chem. Soc. Rev. 2012, 41, 1665-1676 10.1039/C1CS15199A
4. Kumar, S.; Ma, B.; Tsai, C. J.; Nussinov, R. Electrostatic Strengths of Salt Bridges in Thermophilic and Mesophilic Glutamate Dehydrogenase Monomers Proteins: Struct., Funct., Genet. 2000, 38, 368-83 10.1002/(SICI)1097-0134(20000301)38:4<368::AID-PROT3>3.0.CO;2-R
5. Karshikoff, A.; Ladenstein, R. Ion Pairs and the Thermotolerance of Proteins from Hyperthermophiles: a Traffic Rule for Hot Roads Trends Biochem. Sci. 2001, 26, 550-6 10.1016/S0968-0004(01)01918-1
6. Chan, C.-H.; Yu, T.-H.; Wong, K.-B. Stabilizing Salt-Bridge Enhances Protein Thermostability by Reducing the Heat Capacity Change of Unfolding PLoS One 2011, 6, e21624 10.1371/journal.pone.0021624
7. Sanchez-Ruiz, J. M.; Makhatadze, G. I. To Charge or not to Charge? Trends Biotechnol. 2001, 19, 132-5 10.1016/S0167-7799(00)01548-1
8. Gribenko, A. V.; Patel, M. M.; Liu, J.; McCallum, S. A.; Wang, C.; Makhatadze, G. I. Rational Stabilization of Enzymes by Computational Redesign of Surface Charge-Charge Interactions Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 2601-6 10.1073/pnas.0808220106
9. Rathi, P. C.; Höffken, H. W.; Gohlke, H. Quality Matters: Extension of Clusters of Residues with Good Hydrophobic Contacts Stabilize (Hyper)Thermophilic Proteins J. Chem. Inf. Model. 2014, 54, 355-361 10.1021/ci400568c
10. Nojima, H.; Ikai, A.; Oshima, T.; Noda, H. Reversible Thermal Unfolding of Thermostable Phosphoglycerate Kinase. Thermostability Associated With Mean Zero Enthalpy Change J. Mol. Biol. 1977, 116, 429-442 10.1016/0022-2836(77)90078-X
11. Liu, C.-C.; LiCata, V. J. The stability of Taq DNA Polymerase Results from a Reduced Entropic Folding Penalty; Identification of other Thermophilic Proteins with Similar Folding Thermodynamics Proteins: Struct., Funct., Genet. 2014, 82, 785-793 10.1002/prot.24458
12. Razvi, A.; Scholtz, J. M. Lessons in Stability from Thermophilic Proteins Protein Sci. 2006, 15, 1569-1578 10.1110/ps.062130306
13. Samish, I.; MacDermaid, C. M.; Perez-Aguilar, J.; Saven, J. G. Theoretical and Computational Protein Design Annu. Rev. Phys. Chem. 2011, 62, 129-149 10.1146/annurev-physchem-032210-103509
14. Koga, N.; Tatsumi-Koga, R.; Liu, G.; Xiao, R.; Acton, T. B.; Montelione, G.; Baker, D. Principles for designing ideal protein structures Nature 2012, 491, 222-227 10.1038/nature11600
15. Kiss, G.; Celebi-Olcum, N.; Moretti, R.; Baker, D.; Houk, K. N. Computational Enzyme Design Angew. Chem., Int. Ed. 2013, 52, 5700-5725 10.1002/anie.201204077
16. Chennamsetty, N.; Voynov, V.; Kayser, V.; Helk, B.; Trout, B. L. Design of therapeutic proteins with enhanced stability Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 11937-11942 10.1073/pnas.0904191106
17. Xu, J.; Baase, W.; Quillin, M.; Baldwin, E.; Matthews, B. Structural and Thermodynamic Analysis of the Binding of Solvent at Internal Sites in T4 Lysozyme Protein Sci. 2001, 10, 1067-1078 10.1110/ps.02101
18. TM: Crystal Structures and Differential Scanning Calorimetry Experiments Give Hints of the Function of the Buried Water Molecules in Subtilisins J. Mol. Biol. 1994, 242, 193-202 10.1006/jmbi.1994.1572
19. Berndt, K.; Beunink, J.; Schroeder, W.; Wuethrich, K. Designed Replacement of an Internal Hydration Water Molecule in BPTI: Structural and Functional Implications of a Glycine-to-Serine Mutation Biochemistry 1993, 32, 4564-4570 10.1021/bi00068a012
20. Rahaman, O.; Kalimeri, M.; Melchionna, S.; Hénin, J.; Sterpone, F. Role of Internal Water on Protein Thermal Stability: The Case of Homologous G Domains J. Phys. Chem. B 2015, 119, 8939-8949 10.1021/jp507571u
21. Talon, R.; Coquelle, N.; Madern, D.; Girard, E. An Experimental Point of View on Hydration/Solvation in Halophilic Proteins Front. Microbiol. 2014, 5, 66 10.3389/fmicb.2014.00066
22. Ahmad, S.; Kamal, M. Z.; Sankaranarayanan, R.; Rao, N. M. Thermostable Bacillus Subtilis Lipases: In Vitro Evolution and Structural Insight J. Mol. Biol. 2008, 381, 324-40 10.1016/j.jmb.2008.05.063
23. Chi, Y. I.; Martinez-Cruz, L. A.; Jancarik, J.; Swanson, R. V.; Robertson, D. E.; Kim, S. H. Crystal Structure of the Beta-Glycosidase from the Hyperthermophile Thermosphaera Aggregans: Insights into its Activity and Thermostability FEBS Lett. 1999, 445, 375-383 10.1016/S0014-5793(99)00090-3
24. Melchionna, S.; Sinibaldi, R.; Briganti, G. Explanation of the Stability of Thermophilic Proteins Based on Unique Micromorphology Biophys. J. 2006, 90, 4204-12 10.1529/biophysj.105.078972
25. Sterpone, F.; Bertonati, C.; Briganti, G.; Melchionna, S. Key Role of Proximal Water in Regulating Thermostable Proteins J. Phys. Chem. B 2009, 113, 131-7 10.1021/jp805199c
26. Yin, H.; Hummer, G.; Rasaiah, J. C. Metastable Water Clusters in the Nonpolar Cavities of the Thermostable Protein Tetrabrachion J. Am. Chem. Soc. 2007, 129, 7369-77 10.1021/ja070456h
27. Mou, Z.; Ding, Y.; Wang, X.; Cai, Y. Comparison of Protein-water Interactions in Psychrophilic, Mesophilic, and Thermophilic Fe-SOD Protein Pept. Lett. 2014, 21, 578-583 10.2174/0929866521666140108110050
28. Roche, J.; Caro, J. A.; Norberto, D. R.; Barthe, P.; Roumestand, C.; Schlessman, J. L.; Garcia, A. E.; García-Moreno, B. E.; Royer, C. A. Cavities Determine the Pressure Unfolding of Proteins Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 6945-6950 10.1073/pnas.1200915109
29. Nisius, L.; Grzesiek, S. Key Stabilizing Elements of Protein Structure Identified through Pressure and Temperature Perturbation of its Hydrogen Bond Network Nat. Chem. 2012, 4, 711-717 10.1038/nchem.1396
30. Takano, K.; Funahashi, J.; Yamagata, Y.; Fujii, S.; Yutani, K. Contribution of Water Molecules in the Interior of a Protein to the Conformational Stability J. Mol. Biol. 1997, 274, 132-142 10.1006/jmbi.1997.1365
31. Hickey, D. R.; Berghuis, A. M.; Lafond, G.; Jaeger, J. A.; Cardillo, T. S.; McLendon, D.; Das, G.; Sherman, F.; Brayer, G. D.; McLendon, G. Enhanced Thermodynamic Stabilities of Yeast Iso-1-Cytochromes C with Amino Acid Replacements at Positions 52 and 102 J. Biol. Chem. 1991, 266, 11686-11694 10.1021/ba-1991-0228.ch011
32. Vriend, G.; Berendsen, H.; van der Zee, J.; van den Burg, B.; Venema, G.; Eijsink, V. Stabilization of the Neutral Protease of Bacillus Stearothermophilus by Removal of a Buried Water Molecule Protein Eng., Des. Sel. 1991, 4, 941-945 10.1093/protein/4.8.941
33. Wade, R. C.; Mazor, M. H.; McCammon, J. A.; Quiocho, F. A. A Molecular Dynamics Study of Thermodynamic and Structural Aspects of the Hydration of Cavities in Proteins Biopolymers 1991, 31, 919-931 10.1002/bip.360310802
34. Roux, B.; Nina, M.; Pomes, R.; Smith, J. Thermodynamic Stability of Water Molecules in the Bacteriorhodopsin Proton Channel: a Molecular Dynamics Free Energy Perturbation Study Biophys. J. 1996, 71, 670-681 10.1016/S0006-3495(96)79267-6
35. Sterpone, F.; Ceccarelli, M.; Marchi, M. Dynamics of Hydration in Hen Egg White Lysozyme J. Mol. Biol. 2001, 311, 409-19 10.1006/jmbi.2001.4860
36. Olano, L. R.; Rick, S. W. Hydration Free Energies and Entropies for Water in Protein Interiors J. Am. Chem. Soc. 2004, 126, 7991-8000 10.1021/ja049701c
37. Rasaiah, J. C.; Garde, S.; Hummer, G. Water in Nonpolar Confinement: from Nanotubes to Proteins and beyond Annu. Rev. Phys. Chem. 2008, 59, 713-40 10.1146/annurev.physchem.59.032607.093815
38. Damjanovic, A.; Schlessman, J.; Fitch, C.; Garcia, A.; Garcia-Moreno, E. Role of Flexibility and Polarity as Determinants of the Hydration of Internal Cavities and Pockets in Proteins Biophys. J. 2007, 93, 2791-2804 10.1529/biophysj.107.104182
39. Chakrabarty, S.; Warshel, A. Capturing the Energetics of Water Insertion in Biological Systems: The Water Flooding Approach Proteins: Struct., Funct., Genet. 2013, 81, 93-106 10.1002/prot.24165
40. Oikawa, M.; Yonetani, Y. Molecular Dynamics Free Energy Calculations to Assess the Possibility of Water Existence in Protein Nonpolar Cavities Biophys. J. 2010, 98, 2974-2983 10.1016/j.bpj.2010.01.029
41. De Simone, A.; Dodson, G. G.; Verma, C. S.; Zagari, A.; Fraternali, F. Prion and Water: Tight and Dynamical Hydration Sites Have a Key Role in Structural Stability Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 7535-7540 10.1073/pnas.0501748102
42. Baudry, J.; Tajkhorshid, E.; Molnar, F.; Phillips, J.; Schulten, K. Molecular Dynamics Study of Bacteriorhodopsin and the Purple Membrane J. Phys. Chem. B 2001, 105, 905-918 10.1021/jp000898e
43. Tashiro, M.; Stuchebrukhov, A. A. Thermodynamic Properties of Internal Water Molecules in the Hydrophobic Cavity around the Catalytic Center of Cytochrome c Oxidase J. Phys. Chem. B 2005, 109, 1015-1022 10.1021/jp0462456
44. Pisliakov, A. V.; Sharma, P. K.; Chu, Z. T.; Haranczyk, M.; Warshel, A. Electrostatic Basis for the Unidirectionality of the Primary Proton Transfer in Cytochrome C Oxidase Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 7726-7731 10.1073/pnas.0800580105
45. Lee, H. J.; Svahn, E.; Swanson, J. M. J.; Lepp, H.; Voth, G. A.; Brzezinski, P.; Gennis, R. B. Intricate Role of Water in Proton Transport through Cytochrome c Oxidase J. Am. Chem. Soc. 2010, 132, 16225-16239 10.1021/ja107244g
46. Helms, V.; Wade, R. Thermodynamics of Water Mediating Protein-Ligand Interactions in Cytochrome P450cam: a Molecular Dynamics Study Biophys. J. 1995, 69, 810-824 10.1016/S0006-3495(95)79955-6
47. Li, Z.; Lazaridis, T. Thermodynamic Contributions of the Ordered Water Molecule in HIV-1 Protease J. Am. Chem. Soc. 2003, 125, 6636-6637 10.1021/ja0299203
48. Baron, R.; Setny, P.; McCammon, J. A. Water in Cavity-Ligand Recognition J. Am. Chem. Soc. 2010, 132, 12091-12097 10.1021/ja1050082
49. Szep, S.; Park, S.; Boder, E. T.; van Duyne, G. D.; Saven, J. G. Structural Coupling between FKBP12 and Buried Water Proteins: Struct., Funct., Genet. 2009, 74, 603-611 10.1002/prot.22176
50. Prakash, P.; Sayyed-Ahmad, A.; Gorfe, A. A. The Role of Conserved Waters in Conformational Transitions of Q61H K-ras PLoS Comput. Biol. 2012, 8, e1002394 10.1371/journal.pcbi.1002394
51. Scorciapino, M. A.; Robertazzi, A.; Casu, M.; Ruggerone, P.; Ceccarelli, M. Heme proteins: the role of solvent in the dynamics of gates and portals J. Am. Chem. Soc. 2010, 132, 5156-63 10.1021/ja909822d
52. Rahaman, O.; Melchionna, S.; Laage, D.; Sterpone, F. The Effect of Protein Composition on Hydration Dynamics Phys. Chem. Chem. Phys. 2013, 15, 3570-3576 10.1039/c3cp44582h
53. Kalimeri, M.; Rahaman, O.; Melchionna, S.; Sterpone, F. How Conformational Flexibility Stabilizes the Hyperthermophilic Elongation Factor G-Domain J. Phys. Chem. B 2013, 117, 13775-13785 10.1021/jp407078z
54. Pechkova, E.; Sivozhelezov, V.; Nicolini, C. Protein Thermal Stability: the Role of Protein Structure and Aqueous Environment Arch. Biochem. Biophys. 2007, 466, 40-8 10.1016/j.abb.2007.07.016
55. Kalimeri, M.; Girard, E.; Madern, D.; Sterpone, F. Interface Matters: The Stiffness Route to Stability of a Thermophilic Tetrameric Malate Dehydrogenase PLoS One 2014, 9, e113895 10.1371/journal.pone.0113895
56. MacKerell, A. D.; Bashford, D.; Dunbrack, R.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D. et al. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616 10.1021/jp973084f
57. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802 10.1002/jcc.20289
58. Garcia, A. E.; Hummer, G. Water Penetration and Escape in Proteins Proteins: Struct., Funct., Genet. 2000, 38, 261-72 10.1002/(SICI)1097-0134(20000215)38:3<261::AID-PROT3>3.3.CO;2-H
59. Halle, B. Protein Hydration Dynamics in Solution: a Critical Survey Philos. Trans. R. Soc., B 2004, 359, 1207-23 10.1098/rstb.2004.1499
60. Persson, F.; Halle, B. Transient Access to the Protein Interior: Simulation versus NMR J. Am. Chem. Soc. 2013, 135, 8735-8748 10.1021/ja403405d
61. Tuckerman, M. Statistical Mechanics. Theory and Molecular Simulation; Oxford University Press: Oxford, England, 2010.
62. Cui, G.; Swails, J. M.; Manas, E. S. SPAM: A Simple Approach for Profiling Bound Water Molecules J. Chem. Theory Comput. 2013, 9, 5539-5549 10.1021/ct400711g
63. Huggins, D. J. Quantifying the Entropy of Binding for Water Molecules in Protein Cavities by Computing Correlations Biophys. J. 2015, 108, 928-936 10.1016/j.bpj.2014.12.035
64. Hummer, G.; Szabo, A. Calculation of freeenergy differences from computer simulations of initial and final states J. Chem. Phys. 1996, 105, 2004-2010 10.1063/1.472068
65. Petrone, P. M.; Garcia, A. E. MHC-Peptide Binding is Assisted by Bound Water Molecules J. Mol. Biol. 2004, 338, 419-435 10.1016/j.jmb.2004.02.039
66. Day, R.; García, A. E. Water penetration in the low and high pressure native states of ubiquitin Proteins: Struct., Funct., Genet. 2008, 70, 1175-84 10.1002/prot.21562
67. Tian, J.; García, A. E. Simulations of the confinement of ubiquitin in self-assembled reverse micelles J. Chem. Phys. 2011, 134, 225101 10.1063/1.3592712
68. Widom, B. Some topics in theory of fluids J. Chem. Phys. 1963, 39, 2802-2812 10.1063/1.1734110
69. Ludwig, M. L.; Metzger, A. L.; Pattridge, K. A.; Stallings, W. C. Manganese superoxide dismutase from Thermus thermophilus. A structural model refined at 1.8 A resolution J. Mol. Biol. 1991, 219, 335-358 10.1016/0022-2836(91)90569-R
70. Morley, K. L.; Kazlauskas, R. J. Improving enzyme properties: when are closer mutations better? Trends Biotechnol. 2005, 23, 231-237 10.1016/j.tibtech.2005.03.005
71. Takano, K.; Yamagata, Y.; Yutani, K. Buried water molecules contribute to the conformational stability of a protein Protein Eng., Des. Sel. 2003, 16, 5-9 10.1093/proeng/gzg001
72. Roche, J.; Dellarole, M.; Caro, J. A.; Norberto, D. R.; Garcia, A. E.; Garcia-Moreno, B. E.; Roumestand, C.; Royer, C. A. Effect of Internal Cavities on Folding Rates and Routes Revealed by Real-Time Pressure-Jump NMR Spectroscopy J. Am. Chem. Soc. 2013, 135, 14610-14618 10.1021/ja406682e
73. Denisov, V. P.; Peters, J.; Hörlein, H. D.; Halle, B. Using Buried Water Molecules to Explore the Energy Landscape of Proteins Nat. Struct. Biol. 1996, 3, 505-509 10.1038/nsb0696-505