Development, validation, and application of adapted PEOE charges to estimate pKa values of functional groups in protein-ligand complexes

Proteins: Structure, Function and Genetics

Volumn 65, Issue 2, 2006, Pages 424-437

  Czodrowski, Paul ^a   Dramburg, Ingo ^a   Sotriffer, Christoph A ^a   Klebe, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Drug design; Electrostatics; pKa values; Protein ligand complexes; Protonation states

Indexed keywords

AMINO ACID; FUNCTIONAL GROUP; LYSOZYME; XYLAN ENDO 1,3 BETA XYLOSIDASE;

ARTICLE; COMPLEX FORMATION; CORRELATION COEFFICIENT; DRUG DESIGN; ELECTRICITY; ENERGY TRANSFER; ENTHALPY; ENTROPY; ENZYME ACTIVE SITE; LIGAND BINDING; MOLECULAR DYNAMICS; PARTIAL EQUALIZATION OF ORBITAL ELECTRONEGATIVITIES; PKA; PRIORITY JOURNAL; PROTEIN BINDING; PROTON TRANSPORT; SOLVATION; STRUCTURE ANALYSIS;

AMINO ACIDS; ELECTRONS; ELECTROSTATICS; IONS; LIGANDS; ORGANIC CHEMICALS; PROTEIN BINDING; PROTEINS; STATIC ELECTRICITY;

EID: 33749021099     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21110     Document Type: Article

References (70)

1. Yamazaki T. NMR and X-ray evidence that the HIV protease catalytic aspartyl groups are protonated in the complex formed by the protease and a non-peptide cyclic urea-based inhibitor. J Am Chem Soc 1994;116:10791-10792.
2. Wang YX, Freedberg DI, Yamazaki T, Wingfield PT, Stahl SJ, Kaufman JD, Kiso Y, Torchia DA. Solution NMR evidence that the HIV-1 protease catalytic aspartyl groups have different ionization states in the complex formed with the asymmetric drug KNI-272. Biochemistry 1996;35:9945-9950.
3. Singer AU, Forman-Kay JD. pH titration studies of an SH2 domain-phosphopeptide complex: unusual histidine and phosphate pKa values. Protein Sci 1997;6:1910-1919.
4. Dullweber F, Stubbs MT, Musil D, Sturzebecher J, Klebe G. Factorising ligand affinity: a combined thermodynamic and crystallographic study of trypsin and thrombin inhibition. J Mol Biol 2001;313:593-614.
5. Linderstrom-Lang K. Om Proteinstoffernes Ionisation. Lab Carlsberg 1924;15:1-29.
6. Tanford C, Kirkwood JG. Theory of protein titration curves. I. General equations for impenetrable spheres. J Am Chem Soc 1957; 79:5333-5339.
7. Tanford C, Roxford R. Interpretation of protein titration curves. Application to lysozyme. Biochemistry 1972;11:2192-2198.
8. Warshel A, Levitt M. Theoretical studies of enzymatic reactions: dielectric electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 1976;103:227-249.
9. Warshel A. Calculations of enzymic reactions: calculations of pKa, proton transfer reactions, and general acid catalysis reactions in enzymes. Biochemistry 1981;20:3167-3177.
10. Warshel A, Russell ST. Calculations of electrostatic interactions in biological systems and in solutions. Quart Rev Biophys 1984;17:283-422.
11. Sham YY, Chu ZT, Warshel A. Consistent calculations of pKa's of ionizable residues in proteins: semi-microscopic and macroscopic approaches. J Phys Chem B 1997;101:4458-4472.
12. Warshel A, Sussman F, King G. Free energy of charges in solvated proteins: microscopic calculations using a reversible charging process. Biochemistry 1986;25:8368-8372.
13. Schutz CN, Warshel A. What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 2001; 44:400-417.
14. Wisz MS, Hellinga HW. An empirical model for electrostatic interactions in proteins incorporating multiple geometry-dependent dielectric constants. Proteins 2003;51:360-377.
15. Li H, Robertson AD, Jensen JH. Very fast empirical prediction and rationalization of protein pKa values. Proteins 2005;61: 704-721.
16. Mehler EL, Guarnieri F. A self-consistent, microenvironment modulated screened Coulomb potential approximation to calculate pH-dependent electrostatic effects in proteins. Biophys J 1999;77:3-22.
17. Bashford D, Karplus M. pKa's of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry 1990;29:10219-10225.
18. Börjesson U, Hünenberger PH. Explicit-solvent molecular dynamics simulation at constant pH: methodology and application to simple amines. J Chem Phys 2001;114:9706-9719.
19. Baptista AM, Martel PJ, Petersen SB. Simulation of protein conformational freedom as a function of pH: constant-pH molecular dynamics using implicit titration. Proteins 1997;27:523-544.
20. Klingen AR, Ullman GM. Negatively-charged aminoacids and hydrogen bond pattern tune the pKa values of the Rieske-type iron-sulfur proteins. Biochemistry 2004;43:12383-12389.
21. Verwey EJW, Overbeek JTG. Theory of the stability of lyophobic colloids. The interaction of sol particles having an electric double layer. New York: Elsevier; 1948.
22. Gilson MK. Multiple-site titration and molecular modeling: two rapid methods for computing energies and forces for ionizable groups in proteins. Proteins 1993;15:266-282.
23. Yang AS, Gunner MR, Sampogna R, Sharp K, Honig B. On the calculation of pKas in proteins. Proteins 1993;15:252-265.
24. Antosiewicz J, McCammon JA, Gilson MK. Prediction of pH-dependent properties of proteins. J Mol Biol 1994;238:415-436.
25. Demchuk E, Wade RC. Improving the continuum dielectric approach to calculating pKas of ionizable groups in proteins. J Phys Chem 1996;100:17373-17387.
26. Nielsen JE, Vriend G. Optimizing the hydrogen-bond network in Poisson-Boltzmann equation-based pK(a) calculations. Proteins 2001;43:403-412.
27. Nielsen JE, McCammon JA. Calculating pKa values in enzyme active sites. Protein Sci 2003;12:1894-1901.
28. Brooks C, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comp Chem 1983;4: 187-212.
29. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KMJ, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc 1995;117: 5179-5197.
30. Jorgensen WL, Tirado-Rives J. The OPLS potential function for proteins. Energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc 1988;110:1657-1666.
31. Bashford D, Case DA, Dalvit C, Tennant L, Wright PE. Electrostatic calculations of side chain pKa values in myoglobin and comparison with NMR data for histidines. Biochemistry 1993;32: 8045-8056.
32. Russell ST, Warshel A. Calculations of electrostatic energies in proteins. The energetics of ionized groups in bovine pancreatic trypsin inhibitor. J Mol Biol 1985;185:389-404.
33. Warshel A, Chu ZT. Calculations of solvation free energies in chemistry and biology. In: Cramer CJ, Truhlar DG, editors. ACS Symposium Series: Structure and Reactivity in Aqueous Solution: Characterization of Chemical and Biological Systems, 1994.
34. Sitkoff D, Ben-Tal N, Honig B. Calculation of alkane to water solvation free energies using continuum solvent models. J Phys Chem 1996;100:2744-2752.
35. Cannon WR, Garrison BJ, Benkovic SJ. Consideration of the pH-dependent inhibition of dihydrofolate reductase by methotrexate. J Mol Biol 1997;271:656-668.
36. Trylska J, Antosiewicz J, Geller M, Hodge CN, Klabe RM, Head MS, Gilson MK. Thermodynamic linkage between the binding of protons and inhibitors to HIV-1 protease. Protein Sci 1999;8:180-195.
37. Hansson T, Äqvist J. Estimation of binding free energies for HIV proteinase inhibitors by molecular dynamics simulations. Protein Eng 1995;8:1137-1144.
38. Marelius J, Graffner-Nordberg M, Hansson T, Hallberg A, Åqvist J. Computation of affinity and selectivity: binding of 2,4-diaminopteridine and 2,4-diaminoquinazoline inhibitors to dihydrofolate reductases. J Comput-Aid Mol Des 1998;12:119-131.
39. Storer JW, Giesen DJ, Cramer CJ, Truhlar DG. Class IV charge models: a new semiempirical approach in quantum chemistry. J Comput-Aid Mol Des 1995;9:87-110.
40. Bayly C, Cieplak P, Cornell WD, Kollman PA. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J Phys Chem 1993;97: 10269-10280.
41. Gasteiger J, Marsili M. Iterative partial equalization of orbital electronegativity-a rapid access to atomic charges. Tetrahedron 1980;36:3219-3228.
42. Del Re G. A simple MO-LCAO method for the calculation of charge distributions in saturated organic molecules. J Chem Soc 1958:4031-4040.
43. Mulliken RS. A new electroaffinity scale; together with data on valence states and on valence ionization potentials and electron affinities. J Chem Phys 1934;2:782-793.
44. Hinze J, Jaffe HH. Electronegativity. I. Orbital electronegativity of neutral atoms. J Am Chem Soc 1962;84:540-546.
45. Hinze J, Jaffe HH. Electronegativity. IV. Orbital electronegativities of the neutral atoms of the periods three a and four a and of positive ions of periods one and two. J Phys Chem 1963;67: 1501-1506.
46. Gasteiger J. Empirical methods for the calculation of physicochemical data of organic compounds. In: Jochum C, Hicks MG, Sunkel J, editors. Physical Property Prediction in Organic Chemistry. Heidelberg: Springer Verlag; 1988.
47. Wolfenden R. Interaction of the peptide bond with solvent water: a vapor phase analysis. Biochemistry 1978;17:201-204.
48. Bashford D. An object-oriented programming suite for electrostatic effects in biological molecules. In: Ishikawa Y, Oldehoeft RR, Reynders JVW, Tholburn M, editors. Lecture Notes in Computer Science. Berlin: Springer; 1997. pp 233-240. ISCOPE97.
49. Sitkoff D, Ben-Tal N, Honig B. Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem 1994;98:1978-1988.
50. Pedretti A, Villa L, Vistoli G. VEGA-an open platform to develop chemi-bio-informatics applications, using plug-in architecture and script-programming. J Comput-Aid Mol Des 2004;18: 167-173.
51. Viswanadhan VN, Ghose AK, Singh UC, Wendoloski JJ. Prediction of solvation free energies of small organic molecules: additive-constitutive models based on molecular fingerprints and atomic constants. J Chem Inf Comput Sci 1999;39:405-412.
52. GALAXY 2.3. Molecular modeling software package. San Antonio, TX: AM Technologies; 1997.
53. Smith BJ. Solvation parameters for amino acids. J Comp Chem 1999;20:428-442.
54. Bashford D, Karplus M. Multiple-site titration curves of proteins: an analysis of exact and approximate methods for their calculation. J Phys Chem 1991;95:9556-9561.
55. Gasteiger J, Rudolph C, Sadowski J. Automatic generation of 3D-atomic coordinates for organic molecules. Tetrahedron Comput Method 1990;3:537-547.
56. Molecular Operating Environment (MOE 1999.05). Montreal, Quebec, Canada: Chemical Computing Group Inc.; 1998.
57. Sanner MF, Spehner JC, Olson AJ. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 1996;38:305-320.
58. Bondi A. van der Waals volumes and radii. J Phys Chem 1964; 68:441-451.
59. Word JM, Lovell SC, Richardson JS, Richardson DC. Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J Mol Biol 1999;285:1735-1747.
60. Fokkens J. Microcalorimetric studies to correlate thermodynamic and structural properties of inhibitors of the blood clotting cascade. PhD Thesis. Marburg: Philipps University Marburg; 2005.
61. MacKerell JAD, Bashford D, Bellott M, Dunbrack RL, Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wirkiewicz-Kuczera D, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
62. Warshel A, Åqvist J. Electrostatic energy and macromolecular function. Ann Rev Biophys Biophys Chem 1991;20:267-298.
63. King G, Lee FS, Warshel A. Microscopic simulations of macroscopic dielectric constants of solvated proteins. J Chem Phys 1991;95:4366-4377.
64. Warshel A, Russell ST, Churg AK. Macroscopic models for studies of electrostatic interactions in proteins: limitations and applicability. Proc Natl Acad Sci USA 1984;81:4785-4789.
65. Joshi MD, Sidhu G, Nielsen JE, Brayer GD, Withers SG, McIntosh LP. Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidases. Biochemistry 2001; 40:10115-10139.
66. Cocco L, Groff JP, Temple C, Jr, Montgomery JA, London RE, Matwiyoff NA, Blakely RL. Carbon-13 nuclear magnetic resonance study of protonation of methotrexate and aminopterin bound to dihydrofolate reductase. Biochemistry 1981;20:3972-3978.
67. Stone SR, Morrison JF. The pH-dependence of the binding of dihydrofolate and substrate analogues to dihydrofolate reductase from Escherichia coli. Biophys Acta 1983;745:247-258.
68. Cocco L, Roth B, Temple C, Jr, Montgomery JA, London RE, Blakely RL. Protonated state of methotrexate, trimethoprim, and pyrimthamine bound to dihydrofolate reductase. Arch Biochem Biophys Acta 1983;226:567-577.
69. London RE, Howell EE, Warren MS, Kraut J, Blakely RL. Nuclear magnetic resonance study of the state of protonation of inhibitors bound to mutant dihydrofolate reductase lacking the active-site carboxyl. Biochemistry 1986;25:7229-7235.
70. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. PDB2PQR: an automated pipeline for the setup, execution, and analysis of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 2004;32:665-667.