Statistical and molecular dynamics studies of buried waters in globular proteins

Proteins: Structure, Function and Genetics

Volumn 60, Issue 3, 2005, Pages 450-463

  Park, Sheldon ^a   Saven, Jeffery G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Buried water; FKBP12; Hydrogen bonding; Structural coupling

Indexed keywords

ALANINE; ASPARAGINE; GLOBULAR PROTEIN; GLUTAMINE; SERINE; TACROLIMUS; WATER;

ALPHA HELIX; ARTICLE; BETA SHEET; HYDRATION; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACIDS; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MODELS, STATISTICAL; MOLECULAR CONFORMATION; MUTATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PROTEOMICS; SOFTWARE; TACROLIMUS BINDING PROTEIN 1A; WATER;

EID: 23044435317     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20511     Document Type: Article

References (65)

1. Kauzmann, W. Some factors in the interpretation of protein denaturation. Adv Protein Chem 1959;14:1-63.
2. Dill KA. Dominant forces in protein folding. Biochemistry 1990;29: 7133-7155.
3. Rose GD, Geselowitz AR, Lesser GJ, Lee RH, Zehfus MH. Hydrophobicity of amino acid residues in globular proteins. Science 1985;229:834-838.
4. Miller S, Janin J, Lesk AM, Chothia C. Interior and surface of monomeric proteins. J Mol Biol 1987;196:641-656.
5. Blaber M, Lindstrom JD, Gassner N, Xu J, Heinz DW, Matthews BW. Energetic cost and structural consequences of burying a hydroxyl group within the core of a protein determined from Ala→Ser and Val→Thr substitutions in T4 lysozyme. Biochemistry 1993;32:11363-11373.
6. Bolon DN, Mayo SL. Polar residues in the protein core of Escherichia coli thioredoxin are important for fold specificity. Biochemistry 2001;40:10047-10053.
7. McDonald IK, Thornton JM. Satisfying hydrogen bonding potential in proteins. J Mol Biol 1994;238:777-793.
8. Takano K, Yamagata Y, Yutani K. Buried water molecules contribute to the conformational stability of a protein. Protein Eng 2003;16:5-9.
9. Denisov VP, Halle B. Protein hydration dynamics in aqueous solution: a comparison of bovine pancreatic trypsin inhibitor and ubiquitin by oxygen-17 spin relaxation dispersion. J Mol Biol 1995;245:682-697.
10. Hubbard SJ, Gross KH, Argos P. Intramolecular cavities in globular proteins. Protein Eng 1994;7:613-626.
11. Williams MA, Goodfellow JM, Thornton JM. Buried waters and internal cavities in monomeric proteins. Protein Sci 1994;3:1224-1235.
12. Rashin AA, Iofin M, Honig B. Internal cavities and buried waters in globular proteins. Biochemistry 1986;25:3619-3625.
13. Baker EN, Hubbard RE. Hydrogen bonding in globular proteins. Prog Biophys Mol Biol 1984;44:97-179.
14. Papoian GA, Ulander J, Wolynes PG. Role of water mediated interactions in protein-protein recognition landscapes. J Am Chem Soc 2003;125:9170-9178.
15. Papoian GA, Ulander J, Eastwood MP, Luthey-Schulten Z, Wolynes PG. Water in protein structure prediction. Proc Natl Acad Sci USA 2004;101:3352-3357.
16. Kale L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, Krawetz N, Phillips J, Shinozaki A, Varadarajan K, Schulten K. NAMD2: greater scalability for parallel molecular dynamics. J Comput Phys 1999;151:283-312.
17. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, and others. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
18. Hubbard RE, Thornton JM. NACCESS. Computer Program. University College London, Department of Biochemistry and Molecular Biology. 1993.
19. Lee B, Richards FM. The interpretation of protein structures: estimation of static accessibility. J Mol Biol 1971;55:379-400.
20. Janin J. Surface and inside volumes in globular proteins. Nature 1979;277:491-492.
21. Gothel SF, Marahiel MA. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 1999;55:423-436.
22. Futer O, DeCenzo MT, Aldape RA, Livingston DJ. FK506 binding protein mutational analysis. Defining the surface residue contributions to stability of the calcineurin co-complex. J Biol Chem 1995;270:18935-18940.
23. DeCenzo MT, Park ST, Jarrett BP, Aldape RA, Futer O, Murcko MA, Livingston DJ. FK506-binding protein mutational analysis: defining the active-site residue contributions to catalysis and the stability of ligand complexes. Protein Eng 1996;9:173-180.
24. Clackson T, Yang W, Rozamus LW, Hatada M, Amara JF, Rollins CT, Stevenson LF, Magari SR, Wood SA, Courage NL, and others. Redesigning an FKBP-ligand interface to generate chemical dimerizers with novel specificity. Proc Natl Acad Sci USA 1998;95:10437-10442.
25. Michnick SW, Rosen MK, Wandless TJ, Karplus M, Schreiber SL. Solution structure of FKBP, a rotamase enzyme and receptor for FK506 and rapamycin. Science 1991;252:836-839.
26. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 1993;229:105-124.
27. Burkhard P, Taylor P, Walkinshaw MD. X-ray structures of small ligand-FKBP complexes provide an estimate for hydrophobic interaction energies. J Mol Biol 2000;295:953-962.
28. Liang J, Hung DT, Schreiber SL, Clardy J. Structure of the human 25 kDa FK506 binding protein complexed with rapamycin. J Am Chem Soc 1996;118:1231-1232.
29. Fulton KF, Jackson SE, Buckle AM. Energetic and structural analysis of the role of tryptophan 59 in FKBP12. Biochemistry 2003;42:2364-2372.
30. Bryson JW, Desjarlais JR, Handel TM, DeGrado WF. From coiled coils to small globular proteins: Design of a native-like three-helix bundle. Protein Sci 1998;7:1404-1414.
31. Hendsch ZS, Jonsson T, Sauer RT, Tidor B. Protein stabilization by removal of unsatisfied polar groups: computational approaches and experimental tests. Biochemistry 1996;35:7621-7625.
32. Waldburger CD, Jonsson T, Sauer RT. Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure. Proc Natl Acad Sci USA 1996;93:2629-2634.
33. Cupp-Vickery JR, Han O, Hutchinson CR, Poulos TL. Substrate-assisted catalysis in cytochrome P450eryF. Nat Struct Biol 1996;3: 632-637.
34. Shaltiel S, Cox S, Taylor SS. Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A. Proc Natl Acad Sci USA 1998;95:484-491.
35. Miller MD, Cai J, Krause KL. The active site of Serratia endonuclease contains a conserved magnesium-water cluster. J Mol Biol 1999;288:975-987.
36. Hubbard SJ, Argos P. A functional role for protein cavities in domain: domain motions. J Mol Biol 1996;261:289-300.
37. Petrone PM, Garcia AE. MHC-peptide binding is assisted by bound water molecules. J Mol Biol 2004;338:419-435.
38. Finney JL. The organization and function of water in protein crystals. Philos Trans R Soc Lond B Biol Sci 1977;278:3-32.
39. Edsall JT, McKenzie HA. Water and proteins. II. The location and dynamics of water in protein systems and its relation to their stability and properties. Adv Biophys 1983;16:53-183.
40. Sreenivasan U, Axelsen PH. Buried water in homologous serine proteases. Biochemistry 1992;31:12785-12791.
41. Loris R, Langhorst U, De Vos S, Decanniere K, Bouckaert J, Maes D, Transue TR, Steyaert J. Conserved water molecules in a large family of microbial ribonucleases. Proteins 1999;36:117-134.
42. Eriksson AE, Baase WA, Zhang XJ, Heinz DW, Blaber M, Baldwin EP, Matthews BW. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 1992;255:178-183.
43. Buckle AM, Henrick K, Fersht AE. Crystal structural analysis of mutations in the hydrophobic cores of barnase. J Mol Biol 1993;234:847-860.
44. 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.
45. Xu J, Baase WA, Quillin ML, Baldwin EP, Matthews BW. Structural and thermodynamic analysis of the binding of solvent at internal sites in T4 lysozyme. Protein Sci 2001;10:1067-1078.
46. Covalt JC Jr, Roy M, Jennings PA. Core and surface mutations affect folding kinetics, stability and cooperativity in IL-1 beta: does alteration in buried water play a role? J Mol Biol 2001;307: 657-669.
47. Berndt KD, Beunink J, Schroder W, Wuthrich 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.
48. Lett CM, Berghuis AM, Frey HE, Lepock JR, Guillemette JG. The role of a conserved water molecule in the redox-dependent thermal stability of iso-1-cytochrome c. J Biol Chem 1996;271:29088-29093.
49. Quillin ML, Arduini RM, Olson JS, Phillips GN Jr. High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin. J Mol Biol 1993;234:140-155.
50. Blake CC, Pulford WC, Artymiuk PJ. X-ray studies of water in crystals of lysozyme. J Mol Biol 1983;167:693-723.
51. Richards FM. The interpretation of protein structures: total volume, group volume distributions and packing density. J Mol Biol 1974;82:1-14.
52. Ernst JA, Clubb RT, Zhou HX, Gronenborn AM, Clore GM. Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science 1995;267:1813-1817.
53. Otting G, Liepinsh E, Wuthrich K. Protein hydration in aqueous solution. Science 1991;254:974-980.
54. Brunne RM, Berndt KD, Guntert P, Wuthrich K, van Gunsteren WF. Structure and internal dynamics of the bovine pancreatic trypsin inhibitor in aqueous solution from long-time molecular dynamics simulations. Proteins 1995;23:49-62.
55. Garcia AE, Hummer G. Water penetration and escape in proteins. Proteins 2000;38:261-272.
56. Tarek M, Tobias DJ. The dynamics of protein hydration water: a quantitative comparison of molecular dynamics simulations and neutron-scattering experiments. Biophys J 2000;79:3244-3257.
57. Denisov VP, Halle B, Peters J, Horlein HD. Residence times of the buried water molecules in bovine pancreatic trypsin inhibitor and its G36S mutant. Biochemistry 1995;34:9046-90451.
58. Brunne RM, Liepinsh E, Otting G, Wuthrich K, van Gunsteren WF. Hydration of proteins. A comparison of experimental residence times of water molecules solvating the bovine pancreatic trypsin inhibitor with theoretical model calculations. J Mol Biol 1993;231:1040-1048.
59. Higo J, Nakasako M. Hydration structure of human lysozyme investigated by molecular dynamics simulation and cryogenic X-ray crystal structure analyses: on the correlation between crystal water sites, solvent density, and solvent dipole. J Comput Chem 2002;23:1323-1336.
60. Massi F, Straub JE. Structural and dynamical analysis of the hydration of the Alzheimer's beta-amyloid peptide. J Comput Chem 2003;24:143-153.
61. Sanjeev BS, Vishveshwara S. Protein-water interactions in ribonuclease A and angiogenin: a molecular dynamics study. Proteins 2004;55:915-923.
62. Wade RC, Mazor MH, McCammon JA, Quiocho FA. A molecular dynamics study of thermodynamic and structural aspects of the hydration of cavities in proteins. Biopolymers 1991;31:919-931.
63. Likic VA, Juranic N, Macura S, Prendergast FG. A "structural" water molecule in the family of fatty acid binding proteins. Protein Sci 2000;9:497-504.
64. Higo J, Sasai M, Shirai H, Nakamura H, Kugimiya T. Large vortex-like structure of dipole field in computer models of liquid water and dipole-bridge between biomolecules. Proc Natl Acad Sci USA 2001;98:5961-5964.
65. Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997;18:2714-2723.