Molecular dynamics simulations of the hyperthermophilic protein Sac7d from Sulfolobus acidocaldarius: Contribution of salt bridges to thermostability

Journal of Molecular Biology

Volumn 285, Issue 4, 1999, Pages 1811-1830

  De Bakker, Paul I W ^a   Hünenberger, Philippe H ^b   McCammon, J Andrew ^b,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c San Diego   (United States)

Author keywords

Electrostatics; Molecular dynamics; Protein stability; Sac7d; Salt bridges

Indexed keywords

BACTERIAL PROTEIN; SOLVENT; WATER;

ARTICLE; CHEMICAL BOND; ENERGY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; SULFOLOBUS ACIDOCALDARIUS; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); SULFOLOBUS ACIDOCALDARIUS;

EID: 0344609869     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2397     Document Type: Article

References (84)

1. Åqvist J., Hansson T. On the validity of electrostatic linear response in polar solvents. J. Phys. Chem. 100:1996;9512-9521.
2. Åqvist J., Medina C., Samuelsson J.-E. A new method for predicting binding affinity in computer-aided drug design. Protein Eng. 7:1994;385-391.
3. Baumann H., Knapp S., Lundbäck T., Ladenstein R., Härd T. Solution structure and DNA-binding properties of a thermostable from the archaeon Sulfolobus solfataricus. Nature Struct. Biol. 1:1994;808-819.
4. Berendsen H. J. C., Postma J. P. M., van Gunsteren W. F., Hermans J. Interaction models for water in relation to protein hydration. Pullman B. Intermolecular Forces. 1981;331-342 Reidel, Dordrecht.
5. Berendsen H. J. C., Postma J. P. M., van Gunsteren W. F., DiNola A., Haak J. R. Molecular dynamics with coupling to an external heat bath. J. Chem. Phys. 81:1984;3684-3690.
6. Brunne R. M., van Gunsteren W. F. Dynamical properties of bovine pancreatic trypsin inhibitor from a molecular dynamics simulation at 5000 atm. FEBS Letters. 232:1993;215-217.
7. Caflisch A., Karplus M. Molecular dynamics simulation of protein denaturation: solvation of the hydrophobic cores and secondary structure of barnase. Proc. Natl Acad. Sci. USA. 91:1994;1746-1750.
8. Caflisch A., Karplus M. Acid and thermal denaturation of barnase investigated by molecular dynamics simulations. J. Mol. Biol. 252:1995;672-708.
9. Creighton T. E. Proteins: Structures and Molecular Properties. 1993;Freeman, New York.
10. Daggett V., Levitt M. A model of the molten globule state from molecular dynamics simulations. Proc. Natl Acad. Sci. USA. 89:1992;5142-5146.
11. Daggett V., Levitt M. Protein unfolding pathways explored through molecular dynamics simulations. J. Mol. Biol. 32:1993;600-619.
12. Danson M. J., Hough D. W., Russell R. J. M., Taylor G. L., Pearl L. Enzyme thermostability and thermoactivity. Protein Eng. 9:1996;629-630.
13. Dill K. A. Dominant forces in protein folding. Biochemistry. 29:1990;7133-7155.
14. Dill K. A. Folding proteins: finding a needle in a haystack. Curr. Opin. Struct. Biol. 3:1993;99-103.
15. Dobson C. M., Šali A., Karplus M. Protein folding: a perspective from theory and experiment. Angew Chem. Int. Ed. Engl. 37:1998;868-893.
16. Edmondson S. P., Qiu L., Shriver J. W. Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius. Biochemistry. 34:1995;13289-13304.
17. Elcock A. H. The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J. Mol. Biol. 284:1998;489-502.
18. Elcock A. H., McCammon J. A. Continuum solvation model for studying protein hydration thermodynamics at high temperatures. J. Phys. Chem. 101:1997;9624-9634.
19. Frömmel C., Sander C. Thermitase, a thermostable subtilisin: comparison of predicted and experimental structures and the molecular cause of thermostability. Proteins: Struct. Funct. Genet. 5:1989;22-37.
20. Goldman A. How to make my blood boil. Structure. 3:1995;1277-1279.
21. Graziano G., Barone G., Catanzano F., Riccio A. The extra-stability of thermophilic globular proteins: a thermodynamic approach. Thermochim. Acta. 269:1995;381-392.
22. Hawley S. A., Mitchell R. M. An electrophoretic study of reversible protein denaturation: chymotrypsinogen at high pressures. Biochemistry. 14:1975;3257-3264.
23. Hendsch Z. S., Tidor B. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3:1994;211-226.
24. Hennig M., Darimont B., Sterner R., Kirschner K., Jansonius J. N. 2.0 Å structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure. 3:1995;1295-1306.
25. Hockney R. W., Eastwood J. W. Computer Simulation Using Particles. 1988;Institute of Physics Publishing, Bristol.
26. Honig B., Yang A.-S. Free energy balance in protein folding. Advan. Protein Chem. 46:1995;27-58.
27. Horovitz A., Serrano L., Avron B., Bycroft M., Fersht A. R. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216:1990;1031-1044.
28. Hünenberger P. H., McCammon J. A. Effect of artificial periodicity in simulations of biomolecules under Ewald boundary conditions: a continuum electrostatics study. Biophys. Chem. 1998a.
29. Hünenberger P. H., McCammon J. A. Ewald artifacts in computer simulations of ionic solvation and ion-ion interactions: a continuum electrostatics study. J. Chem. Phys. 1998b.
30. Hünenberger P. H., van Gunsteren W. F. Alternative schemes for the inclusion of a reac tion-field correction into molecular dynamics simulations: influence on the simulated energetic, structural, and dielectric properties of liquid water. J. Phys. Chem. 108:1998;6117-6134.
31. Hünenberger P. H., Mark A. E., van Gunsteren W. F. Computational approaches to study protein unfolding: hen egg white lysozyme as a case study. Proteins: Struct. Funct. Genet. 21:1995;196-213.
32. Israelachvili J. N. Intermolecular and Surface Forces. 1992;Academic Press, San Diego.
33. Jaenicke R. Enzymes under extremes of physical conditions. Annu. Rev. Biophys. Bioeng. 10:1981;1-67.
34. Jaenicke R. Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem. 202:1991;715-728.
35. Jaenicke R. How do proteins acquire their three-dimensional structure and stability? Naturwissenschaften. 83:1996;544-554.
36. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
37. Kawamura S., Tanaka I., Kimura M. Contribution of a salt bridge to the thermostability of DNA binding protein HU from Bacillus stearothermophilus determined by stire-directed mutagenesis. J. Biochem. 121:1997;448-455.
38. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
39. Kurinov I. V., Harrison R. W. The influence of temperature on lysozyme crystals. Structure and dynamics of protein and water. Acta Crystallog. sect. D. 51:1995;98-109.
40. Lazaridis T., Archontis G., Karplus M. Enthalpic contribution to protein stability: insights from atom-based calculations and statistical mechanics. Advan. Protein Chem. 47:1995;231-306.
41. Lazaridis T., Lee I., Karplus M. Dynamics and unfolding pathways of a hyperthermophilic and a mesophilic rubredoxin. Protein Sci. 6:1997;2589-2605.
42. Li A., Daggett V. Molecular dynamics simulation of the unfolding of barnase: characterization of the major intermediate. J. Mol. Biol. 275:1998;677-694.
43. Li T. M., Hook J. W. III, Drickamer H. G., Weber G. Plurality of pressure-denatured forms in chymotrypsinogen and lysozyme. Biochemistry. 15:1976;5571-5580.
44. Lide D. R. CRC Handbook of Chemistry and Physics. 1995;CRC Press Inc. Boca Raton.
45. Luty B. A., Davis M. E., Tironi I. G., van Gunsteren W. F. A comparison of particle-particle particle-mesh and Ewald methods for calculating electrostatic interactions in periodic molecular systems. Mol. Simul. 14:1994;11-20.
46. Luty B. A., Tironi I. G., van Gunsteren W. F. Lattice-sum methods for calculating electrostatic interactions in molecular simulations. J. Chem. Phys. 103:1995;3014-3021.
47. Madigan M. T., Marrs B. L. Extremophiles. Sci. Am. 276:1997;66-71.
48. Makhatadze G. I., Privalov P. L. Energetics of protein structure. Advan. Protein Chem. 47:1995;307-425.
49. Maras B., Consalvi V., Chiaraluce R., Politi L., De Rosa M., Bossa R., Scandurra R., Barra D. The protein sequence of glutamate dehydrogenase from Sulfolobus solfataricus, a thermoacidophilic archaebacterium. Is the presence of N-epsilon-methyllysine related to thermostability? Eur. J. Biochem. 203:1992;81-87.
50. Mark A. E., van Gunsteren W. F. Simulation of the thermal denaturation of henn egg white lysozyme: trapping the molten globule state. Biochemistry. 31:1992;7745-7748.
51. Matthews B. W. Structural and genetic analysis of protein stability. Annu. Rev. Biochem. 62:1993;139-160.
52. McAfee J. G., Edmondson S. P., Datta P. K., Shriver J. W., Gupta R. Gene cloning, expression, and characterization of the Sac7 proteins from the hyperthermophileSulfolobus acidocaldarius. Biochemistry. 34:1995;10063-10077.
53. McAfee J. G., Edmondson S. P., Zegar I., Shriver J. W. Equilibrium DNA binding of Sac7d protein from the hyperthermophile Sulfolobus acidocaldarius: fluorescence and circular dichroism studies. Biochemistry. 35:1996;4034-4045.
54. McCrary B. S., Edmondson S. P., Shriver J. W. Hyperthermophile protein folding thermodynamics: differential scanning calorimetry and chemical denaturation of Sac7d. J. Mol. Biol. 264:1996;784-805.
55. Onuchic J. N., Luthey-Schulten Z., Wolynes P. G. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48:1997;545-600.
56. Pappenberger G., Schurig H., Jaenicke R. Disruption of an ionic network leads to accelerated thermal denaturation of D -glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima. J. Mol. Biol. 274:1997;676-683.
57. Reddy T. R., Suryanarayana T. Novel histone-like DNA-binding protein in the nucleoid from the acidothermophilic archaebactriumSulfolobus acidocaldarius that protect DNA against thermal denaturation. Biochim. Biophys. Acta. 949:1988;87-96.
58. Rees D. C., Adams M. W. W. Hyperthermophiles: taking the heat and loving it. Structure. 3:1995;251-254.
59. Robinson H., Gao Y.-G., McCrary B. S., Edmondson S. P., Shriver J. W., Wang A. H.-J. The hyperthermophile chromosomal protein Sac7d sharply kinks DNA. Nature. 392:1998;202-205.
60. Roux B., Yu H.-A., Karplus M. Molecular basis for the Born model of ion solvation. J. Phys. Chem. 94:1990;4683-4688.
61. Ryckaert J.-P., Ciccotti G., Berendsen H. J. C. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:1977;327-341.
62. Šali D., Bycroft M., Fersht A. R. Surface electrostatic interactions contribute little to stability to barnase. J. Mol. Biol. 220:1991;779-788.
63. Schreiber H., Steinhauser O. Cutoff size does strongly influence molecular dynamics results on solvated polypeptides. Biochemistry. 31:1992a;5856-5860.
64. Schreiber H., Steinhauser O. Molecular dynamics studies of solvated polypeptides: why the cut-off scheme does not work. Chem. Phys. 168:1992b;75-89.
65. Smith P. E., Pettitt B. M. Peptides in ionic solutions: a comparison of the Ewald and switching function techniques. J. Chem. Phys. 95:1991;8430-8441.
66. Spassov V. Z., Karshikoff A. D., Ladenstein R. The optimization of protein-solvent interactions: thermostability and the role of hydrophobic and electrostatic interactions. Protein Sci. 4:1995;1516-1527.
67. Stetter K. O., Fiala G., Huber G., Huber R., Segerer A. Hyperthermophilic microorganisms. FEMS Microbiol. Rev. 75:1990;117-124.
68. Tanner J. J., Hecht R. M., Krause K. L. Determinants of enzyme thermostability observed in the molecular structure ofThermus aquaticusD -glyceraldehyde-3-phosphate dehydrogenase at 2.5 Å resolution. Biochemistry. 35:1996;2597-2609.
69. Tilton R. F. Jr, Dewan J. C., Petsko G. A. Effects of temperature of protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry. 31:1992;2469-2481.
70. Tirado-Rives J., Jorgensen W. L. Molecular dynamics simulations of the unfolding of apomyoglobin in water. Biochemistry. 32:1993;4175-4184.
71. Tomschy A., Böhm G., Jaenicke R. The effect of ion pairs on the thermal stability of D -glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima. Protein Eng. 7:1994;1471-1478.
72. van Gunsteren W. F., Billeter S. R., Eising A. A., Hünenberger P. H., Krüger P., Mark A. E., Scott W. R. P., Tironi I. G. Biomolecular Simulation: The GROMOS96 Manual and User Guide. 1996;BIOMOS, Zürich, Groningen.
73. Vetriani C., Maeder D. L., Tolliday N., Yip K. S.-P., Stillman T. J., Britton K. L., Rice D. W., Klump H. H., Robb F. T. Protein thermostability above 100 °C: a key role for ionic interactions. Proc. Natl Acad. Sci. USA. 95:1998;12300-12305.
74. Vieille C., Zeikus J. G. Thermozymes: identifying molecular determinants of protein structural and functional stability. Trends Biotechnol. 14:1996;183-191.
75. Vogt G., Woell S., Argos P. Protein thermal stability, hydrogen bonds, and ion pairs. J. Mol. Biol. 269:1997;631-643.
76. Wallon G., Kryger G., Lovett S. T., Oshima T., Ringe D., Petsko G. A. Crystal structures of Escherichia coli and Salmonella typhimurium 3-isopropylmalate dehydrogenase and comparison with their thermophilic counterpart from Thermus thermophilus. J. Mol. Biol. 266:1997;1016-1031.
77. Watanabe K., Chishiro K., Kitamura K., Suzuki Y. Proline residues responsible for thermostability occur with high frequency in the loop region of an extremely thermostable oligo-1,6-glucosidase. J. Biol. Chem. 266:1991;24287-24294.
78. Watanabe K., Hata Y., Kizaki H., Katsube Y., Suzuki Y. The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 Å resolution: structural characterization of proline-substitution sites for protein thermostabilization. J. Mol. Biol. 269:1997;142-153.
79. Weber G., Drickamer H. G. The effect of high pressure upon proteins and other biomolecules. Quart. Rev. Biophys. 16:1983;89-112.
80. Wimley W. C., Gawrisch K., Creamer T. P., White S. H. Direct measurement of salt-bridge solvation energies using a peptide model system: implications for protein stability. Proc. Natl Acad. Sci. USA. 93:1996;2985-2990.
81. Yip K. S., Stillman T. J., Britton K. L., Artymiuk P. J., Baker P. J., Sedelnikova S. E., Engel P. C., Pasquo A., Chiaraluce R., Consalvi V., Scandurra R., Rice D. W. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure. 3:1995;1147-1158.
82. Young A. C. M., Dewan J. C., Nave C., Tilton R. F. Comparison of the radiation-induced decay and structure refinement from X-ray data collected from lysozyme crystals at low and ambient temperatures. J. Appl. Crystallog. 26:1993;309-319.
83. Young A. C., Tilton R. F., Dewan J. C. Thermal expansion of hen egg-white lysozyme. Comparison of the 1.9 Å resolution structures of the tetragonal form of the enzyme at 100 K and 298 K. J. Mol. Biol. 235:1994;302-317.
84. Zipp A., Kauzmann W. Pressure denaturation of metmyoglobin. Biochemistry. 12:1973;4217-4228.