Identification of substrate binding sites in enzymes by computational solvent mapping

Journal of Molecular Biology

Volumn 332, Issue 5, 2003, Pages 1095-1113

  Silberstein, Michael ^a   Dennis, Sheldon ^b,d   Brown III, Lawrence ^b,e   Kortvelyesi, Tamas ^b,c   Clodfelter, Karl ^a   Vajda, Sandor ^b  

^a BOSTON UNIVERSITY   (United States)

^b Boston University   (United States)

^c UNIVERSITY OF SZEGED   (Hungary)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e Fish and Neave   (United States)

Author keywords

Ligand binding; Organic solvent; Protein solvation; Structural genomics; X ray structure

Indexed keywords

ENZYME; HALOALKANE DEHALOGENASE; THERMOLYSIN; UNCLASSIFIED DRUG;

ALGORITHM; ARTICLE; CALCULATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; LIGAND BINDING; MATHEMATICAL COMPUTING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SOLVATION;

EID: 0042386537     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.019     Document Type: Article

References (69)

1. Bonanno J.B., Edo C., Eswar N., Pieper U., Romanowski M.J., Ilyin V., et al. Structural genomics of enzymes involved in sterol/isoprenoid biosynthesis. Proc. Natl Acad. Sci. USA. 98:2001;12896-12901.
2. Erlandsen H., Abola E.E., Stevens R.C. Combining structural genomics and enzymology: completing the picture in metabolic pathways and enzyme active sites. Curr. Opin. Struct. Biol. 10:2000;719-730.
3. Skolnick J., Fetrow J.S., Kolinski A. Structural genomics and its importance for gene function analysis. Nature Biotechnol. 18:2000;283-287.
4. Mattos C., Ringe D. Locating and characterizing binding sites on proteins. Nature Biotechnol. 14:1996;595-599.
5. Ringe D., Mattos C. Analysis of the binding surfaces of proteins. Med. Res. Rev. 19:1999;321-331.
6. Allen K.N., Bellamacina C.R., Ding X., Jeffery C.J., Mattos C., Petsko G.A., Ringe D. An experimental approach to mapping the binding surfaces of crystalline proteins. J. Phys. Chem. 100:1996;2605-2611.
7. English A.C., Done S.H., Caves L.S., Groom C.R., Hubbard R.E. Locating interaction sites on proteins: the crystal structure of thermolysin soaked in 2% to 100% isopropanol. Proteins: Struct. Funct. Genet. 37:1999;628-640.
8. English A.C., Groom C.R., Hubbard R.E. Experimental and computational mapping of the binding surface of a crystalline protein. Protein Eng. 14:2001;47-59.
9. Liepinsh E., Otting G. Organic solvents identify specific ligand binding sites on protein surfaces. Nature Biotechnol. 15:1997;264-268.
10. Dennis S., Kortvelyesi T., Vajda S. Computational mapping identifies the binding sites of organic solvents on proteins. Proc. Natl Acad. Sci. USA. 99:2002;4290-4295.
11. Kortvelyesi T., Dennis S., Silberstein M., Brown L. III, Vajda S. Algorithms for computational solvent mapping of proteins. Proteins: Struct. Funct. Genet. 51:2003;340-351.
12. Lichtarge O., Bourne H.R., Cohen F.E. The evolutionary trace method defines the binding surfaces common to a protein family. J. Mol. Biol. 257:1996;342-358.
13. Yao H., Kristensen D.M., Mihalek I., Sowa M.E., Shaw C., Kimmel M., et al. An accurate, sensitive, and scalable method to identify functional sites in protein structures. J. Mol. Biol. 326:2003;255-261.
14. del Sol Mesa A., Pazos F., Valencia A. Automatic methods for predicting functionally important residues. J. Mol. Biol. 326:2003;1289-1302.
15. Hendlich M., Rippmann F., Barnickel G. LIGSITE: automatic and efficient detection of potential small molecule-binding sites in enzymes. J. Mol. Graph. Model. 15:1997;359-363.
16. Liang J., Edelsbrunner J., Woodward C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci. 7:1998;1884-1897.
17. Edelsbrunner H., Facello M., Liang J. On the definition and the construction of pockets in macromolecules. Disc. Appl. Math. 88:1998;83-102.
18. Brady G.P. Jr, Stouten P.F.W. Fast prediction and visualization of protein binding pockets with PASS. J. Comput. Aided Mol. Des. 14:2000;383-401.
19. Ondrechen M.J., Clifton J.G., Ringe D. THEMATICS: a simple computational predictor of enzyme function from structure. Proc. Natl Acad. Sci USA. 98:2001;12473-12478.
20. Gutteridge A., Bartlett G.J., Thornton J.M. Using a neural network and sparial clustering to predict the location of active sites in enzymes. J. Mol. Biol. 330:2003;719-734.
21. Laskowski R.A., Luscombe N.M., Swindells M.H., Thornton J.M. Protein clefts in molecular recognition and function. Protein Sci. 5:1996;2438-2452.
22. Matthews B.W. Structural basis of the action of thermolysin and related zinc peptidases. Accts Chem. Res. 21:1988;333-340.
23. Lipscomb W.N., Strater N. Recent advances in zinc enzymology. Chem. Rev. 96:1996;2375-2433.
24. Marie-Claire C., Ruffet E., Antonczak S., Beaumont A., O'Donohue M., Roques B.P., Fournie-Zaluski M.C. Evidence by site-directed mutagenesis that arginine 203 of thermolysin and arginine 717 of neprilysin (neutral endopeptidase) play equivalent critical roles in substrate hydrolysis and inhibitor binding. Biochemistry. 36:1997;13938-13945.
25. Marie-Claire C., Ruffet E., Tiraboschi G., Fournie-Zaluski M.C. Differences in transition state stabilization between thermolysin (EC 3.4.24.27) and neprilysin (EC 3.4.24.11). FEBS Letters. 438:1998;215-219.
26. Reed G.H., Poyner R.R., Larsen T.M., Wedekind J.E., Rayment I. Structural and mechanistic studies of enolase. Curr. Opin. Struct. Biol. 6:1996;736-743.
27. Zhang E., Brewer J.M., Minor W., Carreira L.A., Lebioda L. Mechanism of enolase: the crystal structure of asymmetric dimer enolase - 2-phospho-D-glycerate/enolase - phosphoenolpyruvate at 2.0 Å resolution. Biochemistry. 36:1997;12526-12534.
28. Larsen T.M., Wedekind J.E., Rayment I., Reed G.H. A carboxylate oxygen of the substrate bridges the magnesium ions at the active site of enolase: structure of the yeast enzyme complexed with the equilibrium mixture of 2-phosphoglycerate and phosphoenolpyruvate at 1.8 Å resolution. Biochemistry. 35:1996;4349-4358.
29. Brewer J.M., Glover C.V.C., Holland M.J., Lebioda L. Significance of the enzymatic properties of yeast S39A enolase to the catalytic mechanism. Biochim. Biophys. Acta. 1383:1998;351-355.
30. Vinarov D.A., Nowak T. Role of His159 in yeast enolase catalysis. Biochemistry. 18:1999;12138-12149.
31. Brewer J.M., Holland M.J., Lebioda L. The H159A mutant of yeast enolase has significant activity. Biochem. Biophys. Res. Commun. 276:2000;1199-1202.
32. 1. Atomic dissection of the enzyme-substrate interactions. Eur. J. Biochem. 247:1997;1-11.
33. Hubner B., Haensler M., Hahn U. Modification of ribonuclease T1 specificity by random mutagenesis of the substrate binding segment. Biochemistry. 38:1999;1371-1376.
34. 1 - influence of subsite interactions on the substrate specificity. J. Biomol. Struct. Dynam. 10:1993;891-903.
35. Kumar K., Walz F.G. Probing functional perfection in substructures of ribonuclease T-1: double combinatorial random mutagenesis involving Asn43, Asn44, and Glu46 in the guanine binding loop. Biochemistry. 40:2001;7348-7357.
36. Alber T.C., Davenport R.C. Jr, Giammona D.A., Lolis E., Petsko G.A., Ringe D. Crystallography and site directed mutagenesis of yeast triosephosphate isomerase: what can we learn about catalysis from a "simple" enzyme? Cold Spring Harbor Symp. Quant. Biol. 52:1987;603-613.
37. Joseph D., Petzko G.A., Karplus M. Anatomy of a conformational change: hinged "lid" motion of the triosephosphate isomerase loop. Science. 249:1990;1425-1428.
38. Norledge B.V., Lamber A.M., Abagyan R.A., Rottmann A., Fernandez A.M., Filimonov V.V., et al. Modeling, mutagenesis, and structural studies on the fully conserved phosphate-binding loop (loop 8) of triosephosphate isomerase: toward a new substrate specificity. Proteins: Struct. Funct. Genet. 42:2001;383-389.
39. Perona J.J., Hedstrom L., Rutter W.J., Fletterick R.J. Structural origins of substrate determination in trypsin and chymotrypsin. Biochemistry. 34:1995;1489-1499.
40. Sprang S., Standing T., Fletterick R.J., Stroud R.M., Finer-Moore J., Xuong N.H., et al. The three-dimensional structure of Asn102 mutant of trypsin: role of Asp102 in serine protease catalysis. Science. 237:1987;905-909.
41. Helland R., Leiros I., Berglund G.I., Willassen N.P., Smalas A.O. The crystal structure of anionic salmon trypsin in complex with bovine pancreatic trypsin inhibitor. Eur. J. Biochem. 256:1998;317-324.
42. Choe J., Fromm H.J., Honzatko R.B. Crystal structures of fructose-1,6-bisphosphatase: mechanism of catalysis and allosteric inhibition revealed in product complexes. Biochemistry. 39:2000;8565-8574.
43. Liang J., Huang S., Zhang Y., Ke H., Lipscomb W.N. Crystal structure of the neutral form of fructose-1,6-bisphosphatase complexed with regulatory inhibitor fructose-2,6-bisphosphate at 2.6 Å resolution. Proc. Natl Acad. Sci. USA. 89:1992;2404-2408.
44. Ke H., Zhang Y., Lipscomb W.N. Crystal structure of fructose-1,6-bisphosphatase complexed with fructose 6-phosphate, AMP, and magnesium. Proc. Natl Acad. Sci. USA. 87:1990;5243-5247.
45. Villeret V., Huang S., Fromm H.J., Lipscomb W.N. Crystallographic evidence for the action of potassium, thallium, and lithium ions on fructose-1,6-bisphosphatase. Proc. Natl Acad. Sci. USA. 92:1995;8916-8920.
46. Schanstra J.P., Ridder I.S., Heimeriks G.J., Rink R., Poelarends G.J., Kalk K.H., et al. Kinetic characterization and X-ray structure of a mutant of haloalkane dehalogenase with higher catalytic activity and modified substrate range. Biochemistry. 35:1996;13186-13195.
47. Pikkemaat M.G., Ridder I.S., Rozeboom H.J., Kalk K.H., Dijkstra B.W., Janssen D.B. Crystallographic and kinetic evidence of a collision complex formed during halide import in haloalkane dehalogenase. Biochemistry. 38:1999;12052-12061.
48. Ogury K., Yamada H., Joshimura H. Regiochemitry of cytochrome P450 isozymes. Annu. Rev. Pharmacol. Toxicol. 34:1994;251-279.
49. Goodford P.J. A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J. Med. Chem. 28:1985;849-875.
50. Miranker A., Karplus M. Functionality maps of binding sites: a multiple copy simultaneous search method. Proteins: Struct. Funct. Genet. 11:1991;29-34.
51. Shortle D., Simons K.T., Baker D. Clustering of low-energy conformations near the native structures of small proteins. Proc. Natl Acad. Sci. USA. 95:1998;11158-11162.
52. Comeau S.R., Gatchell D., Vajda S., Camacho C.J. ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics. 2003;. in the press.
53. Gschwend D.A., Good A.C., Kuntz I.D. Molecular docking towards drug discovery. J. Mol. Recognit. 9:1996;175-816.
54. Goodsell D.S., Olson A.J. Automated docking of substrates to proteins by simulated annealing. Proteins: Struct. Funct. Genet. 8:1990;195-202.
55. Yu E.W., Koshland D.E. Jr. Propagating conformational changes over long (and short) distances in proteins. Proc. Natl. Acad. Sci. USA. 98:2001;9517-9520.
56. Kazlauskas R.J. Molecular modeling and biocatalysis: explanations, predictions, limitations, and opportunities. Curr. Opin. Chem. Biol. 4:2000;81-88.
57. DeVoss J.J., Sibbesen O., Zhang Z., Ortiz de Montellano P.R. Substrate docking algorithms and predictions of the substrate specificity of cytochrome P450cam and its L244A mutant. J. Am. Chem. Soc. 119:1997;5489-5498.
58. Wojciechowski M., Skolnick J. Docking of small ligands to low-resolution and theoretically predicted receptor structures. J. Comp. Chem. 23:2002;189-197.
59. Gilson M.K., Honig B. Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis. Proteins: Struct. Funct. Genet. 4:1988;7-18.
60. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science. 268:1995;1144-1149.
61. Bruccoleri R.E. Grid positioning independence and the reduction of self-energy in the solution of the Poisson-Boltzmann equation. J. Comp. Chem. 14:1993;1417-1422.
62. Zhang C., Vasmatzis G., Cornette J.L., DeLisi C. Determination of atomic desolvation energies from the structures of crystallized proteins. J. Mol. Biol. 267:1996;707-726.
63. Miyazava S., Jernigan R. Estimation of effective interresidue contact energies from protein crystal structures: quasi-chemical approximation. Macromolecules. 18:1985;534-552.
64. Vakser I.A. Protein docking for low-resolution structures. Protein Eng. 8:1995;371-377.
65. Vakser I.A., Matar O.G., Lam C.F. A systematic study of low-resolution recognition in protein-protein complexes. Proc. Natl Acad. Sci. USA. 96:1999;8477-8482.
66. Schaefer M., Karplus M.A. A comprehensive analytical treatment of continuum electrostatics. J. Phys. Chem. 100:1996;1578-1599.
67. Brooks B.R., Bruccoleri R.E., Olafson B., States D.J., Swaminathan S., Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem. 4:1983;197-214.
68. Wallace A.C., Laskowski R.A., Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:1995;127-134.
69. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238:1994;777-793.