Statistical analysis of protein structures suggests that buried ionizable residues in proteins are hydrogen bonded or form salt bridges

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 7, 2011, Pages 2027-2032

  Bush, Jeffrey ^a   Makhatadze, George I ^a  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Hydrogen bonding; Ion pairs salt bridges; Protein electrostatics; Protein structure; Solvent accessibility

Indexed keywords

AMINO ACID;

ARTICLE; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN STRUCTURE; SALT BRIDGE; STATIC ELECTRICITY; STATISTICAL ANALYSIS;

HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, CHEMICAL; MODELS, STATISTICAL; PROTEIN STABILITY; PROTEINS;

EID: 79958769952     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23067     Document Type: Article

References (38)

1. Lee B, Richards FM. The interpretation of protein structures: estimation of static accessibility. J Mol Biol 1971; 55: 379-400.
2. Rashin AA, Honig B. On the environment of ionizable groups in globular proteins. J Mol Biol 1984; 173: 515-521.
3. Barlow DJ, Thornton JM. Ion-pairs in proteins. J Mol Biol 1983; 168: 867-885.
4. Miller S, Janin J, Lesk AM, Chothia C. Interior and surface of monomeric proteins. J Mol Biol 1987; 196: 641-656.
5. Lesser GJ, Rose GD. Hydrophobicity of amino acid subgroups in proteins. Proteins 1990; 8: 6-13.
6. Chothia C. Hydrophobic bonding and accessible surface area in proteins. Nature 1974; 248: 338-339.
7. Cabani S, Gianni P, Mollica V, Lepori L. Group contributions to the thermodynamic properties of non-ionic organic solutes in dilute aqueous-solution. J Solution Chem 1981; 10: 563-595.
8. Makhatadze GI, Privalov PL. Energetics of protein structure. Adv Protein Chem 1995; 47: 307-425.
9. Privalov PL, Makhatadze GI. Contribution of hydration to protein folding thermodynamics. II. The entropy and Gibbs energy of hydration. J Mol Biol 1993; 232: 660-679.
10. Balaji S, Aruna S, Srinivasan N. Tolerance to the substitution of buried apolar residues by charged residues in the homologous protein structures. Proteins 2003; 53: 783-791.
11. Kajander T, Kahn PC, Passila SH, Cohen DC, Lehtio L, Adolfsen W, Warwicker J, Schell U, Goldman A. Buried charged surface in proteins. Structure 2000; 8: 1203-1214.
12. Kumar S, Nussinov R. Close-range electrostatic interactions in proteins. Chembiochem 2002; 3: 604-617.
13. Sitkoff D, Sharp KA, Honig B. Accurate calculation of hydration free-energies using macroscopic solvent models. J Phys Chem 1994; 98: 1978-1988.
14. Spassov VZ, Ladenstein R, Karshikoff AD. Optimization of the electrostatic interactions between ionized groups and peptide dipoles in proteins. Protein Sci 1997; 6: 1190-1196.
15. Kim J, Mao J, Gunner MR. Are acidic and basic groups in buriedproteins predicted to be ionized? J Mol Biol 2005; 348: 1283-1298.
16. Noguchi T, Akiyama Y. PDB-REPRDB: a database of representative protein chains from the protein data bank (PDB) in 2003. Nucleic Acids Res 2003; 31: 492-493.
17. Longhi S, Czjzek M, Cambillau C. Messages from ultrahigh resolution crystal structures. Curr Opin Struct Biol 1998; 8: 730-737.
18. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993; 234: 779-815.
19. Kaplan W, Littlejohn TG. Swiss-PDB viewer (deep view). Brief Bioinform 2001; 2: 195-197.
20. Hubbard SJ, Thornton JM. NACCESS, 2.1.1. London: Dept of Biochemistry and Molecular Biology, University College; 1993.
21. McDonald IK, Thornton JM. Satisfying hydrogen bonding potential in proteins. J Mol Biol 1994; 238: 777-793.
22. Baker EN, Hubbard RE. Hydrogen bonding in globular proteins. Prog Biophys Mol Biol 1984; 44: 97-179.
23. Warshel A. What about protein polarity? Nature 1987; 330: 15-16.
24. Loladze VV, Ermolenko DN, Makhatadze GI. Heat capacity changes upon burial of polar and nonpolar groups in proteins. Protein Sci 2001; 10: 1343-1352.
25. Loladze VV, Ermolenko DN, Makhatadze GI. Thermodynamic consequences of burial of polar and non-polar amino acid residues in the protein interior. J Mol Biol 2002; 320: 343-357.
26. Gilson MK, Honig BH. Calculation of electrostatic potentials in an enzyme active site. Nature 1987; 330: 84-86.
27. Sternberg MJ, Hayes FR, Russell AJ, Thomas PG, Fersht AR. Prediction of electrostatic effects of engineering of protein charges. Nature 1987; 330: 86-88.
28. Damjanovic A, Garcia-Moreno B, Lattman EE, Garcia AE. Molecular dynamics study of water penetration in staphylococcal nuclease. Proteins 2005; 60: 433-449.
29. Schlessman JL, Abe C, Gittis A, Karp DA, Dolan MA, Garcia-Moreno EB. Crystallographic study of hydration of an internal cavity in engineered proteins with buried polar or ionizable groups. Biophys J 2008; 94: 3208-3216.
30. Day R, Garcia AE. Water penetration in the low and high pressure native states of ubiquitin. Proteins 2008; 70: 1175-1184.
31. Tokuriki N, Stricher F, Serrano L, Tawfik DS. How protein stability and new functions trade off. PLoS Comput Biol 2008; 4: e1000002: 1-7.
32. Shoichet BK, Baase WA, Kuroki R, Matthews BW. A relationship between protein stability and protein function. Proc Natl Acad Sci USA 1995; 92: 452-456.
33. Thomas VL, McReynolds AC, Shoichet BK. Structural bases for stability-function tradeoffs in antibiotic resistance. J Mol Biol 2010; 396: 47-59.
34. Chen P, Shakhnovich EI. Thermal adaptation of viruses and bacteria. Biophys J 2010; 98: 1109-1118.
35. Zeldovich KB, Chen P, Shakhnovich EI. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc Natl Acad Sci USA 2007; 104: 16152-16157.
36. Isom DG, Cannon BR, Castaneda CA, Robinson A, Garcia-Moreno B. High tolerance for ionizable residues in the hydrophobic interior of proteins. Proc Natl Acad Sci USA 2008; 105: 17784-17788.
37. Karp DA, Stahley MR, Garcia-Moreno B. Conformational consequences of ionization of Lys, Asp, and Glu buried at position 66 in staphylococcal nuclease. Biochemistry 2010; 49: 4138-4146.
38. Isom DG, Castaneda CA, Cannon BR, Velu PD, Garcia-Moreno EB. Charges in the hydrophobic interior of proteins. Proc Natl Acad Sci USA 2010;doi:10.1073/pnas.1004213107.