Escherichia coli glutaminyl-tRNA synthetase is electrostatically optimized for binding of its cognate substrates

Journal of Molecular Biology

Volumn 342, Issue 2, 2004, Pages 435-452

  Green, David F ^a,b   Tidor, Bruce ^a,b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c USA   (United States)

Author keywords

continuum electrostatics; electrostatic optimization; enzyme catalysis; molecular recognition; Poisson Boltzmann

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI PROTEIN; GLUTAMINE TRANSFER RNA LIGASE; LIGAND;

ARTICLE; BINDING SITE; CALCULATION; CATALYSIS; CHEMICAL REACTION; CONTROLLED STUDY; DIELECTRIC CONSTANT; ELECTRICITY; ENZYME BINDING; ESCHERICHIA COLI; LIGAND BINDING; NONHUMAN; PARAMETER; PRIORITY JOURNAL; PROTEIN INTERACTION; SURFACE CHARGE;

ESCHERICHIA COLI;

EID: 4344595498     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.087     Document Type: Article

References (62)

1. C. Chothia Hydrophobic bonding and accessible surface area in proteins Nature 248 1974 338 339
2. C. Chothia, and J. Janin Principles of protein-protein recognition Nature 256 1975 705 708
3. K.A. Sharp, A. Nicholls, R.F. Fine, and B. Honig Reconciling the magnitude of the microscopic and macroscopic hydrophobic effects Science 252 1991 106 109
4. B. Tidor, and M. Karplus The contribution of vibrational entropy to molecular association. The dimerization of insulin J. Mol. Biol. 238 1994 405 411
5. M.A. Gilson, J.A. Given, B.L. Bush, and J.A. McCammon The statistical thermodynamic basis for computation of binding affinities: a critical review Biophys. J. 72 1997 1047 1069
6. L. Lo Conte, C. Chothia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198
7. Z.S. Hendsch, and B. Tidor Electrostatic interactions in the GCN4 leucine zipper: substantial contributions arise from intramolecular interactions enhanced on binding Protein Sci. 8 1999 1381 1392
8. L.-P. Lee, and B. Tidor Optimization of binding electrostatics: charge complementarity in the barnase-barstar protein complex Protein Sci. 10 2001 362 377
9. L.-P. Lee, and B. Tidor Barstar is electrostatically optimized for tight binding to barnase Nature Struct. Biol. 8 2001 73 76
10. W. Freist, D.H. Gauss, M. Ibba, and D. Söll Glutaminyl-tRNA synthetase Biol. Chem. 378 1997 1103 1117
11. J.J. Perona, M.A. Rould, and T.A. Steitz Structural basis for transfer RNA aminoacylation by Escherichia coli glutaminyl-tRNA synthetase Biochemistry 32 1993 8758 8771
12. Gln complexed with glutaminyl-tRNA synthetase and ATP suggests a possible role for pseudo-uridines in stabilization of RNA structure Biochemistry 33 1994 7560 7567
13. Gln and ATP Biol. Chem. 35 1996 14725 14733
14. V.L. Rath, L.F. Silvian, B. Beijer, B.S. Sproat, and T.A. Steitz How glutaminyl-tRNA synthetase selects glutamine Structure 6 1998 439 449
15. W. Freist Mechanisms of aminoacyl-tRNA synthetases: a critical consideration of recent results Biochemistry 28 1989 6787 6795
16. T. Bhattacharyya, A. Bhattacharyya, and S. Roy A fluorescence spectroscopic study of glutaminyl-tRNA synthetase from Escherichia coli and its implications for the enzyme mechanism Eur. J. Biochem. 200 1991 739 745
17. L.-P. Lee, and B. Tidor Optimization of electrostatic binding free energy J. Chem. Phys. 106 1997 8681 8690
18. E. Kangas, and B. Tidor Optimizing electrostatic affinity in ligand-receptor binding: theory, computation, and ligand properties J. Chem. Phys. 109 1998 7522 7545
19. E. Kangas, and B. Tidor Electrostatic complementarity at ligand binding sites: application to chorismate mutase J. Phys. Chem. ser. B 105 2001 880 888
20. T.N.C. Wells, C.K. Ho, and A.R. Fersht Free energy of hydrolysis of tyrosyl adenylate and its binding to wild-type and engineered mutant tyrosyl-tRNA synthetases Biochemistry 25 1986 6603 6608
21. P. Brick, T.N. Bhat, and D.M. Blow Structure of tyrosyl-tRNA synthetase refined at 2.3 Å resolution: Interaction of the enzyme with the tyrosyl adenylate intermediate J. Mol. Biol. 208 1988 83 98
22. M. Baltzinger, S.X. Lin, and P. Remy Yeast phenylalanyl-tRNA synthetase: symmetric behavior of the enzyme during activation of phenylalanine as shown by a rapid kinetic investigation Biochemistry 22 1983 675 681
23. I.H. Sigel Isomeric equilibria in complexes of adenosine 5′-triphosphate with divalent metal ions Eur. J. Biochem. 165 1987 65 72
24. P. Retailleau, X. Huang, Y. Yin, M. Hu, V. Weinreb, and P. Vachette Interconversion of ATP binding and conformational free energies by tryptophanyl-tRNA synthetase: structures of ATP bound to open and closed, pre-transition state conformations J. Mol. Biol. 325 2003 39 63
25. L. Turi, and L.L. Dannenberg Molecular orbital study of acetic acid aggregation. 1. Monomers and dimers J. Phys. Chem. 97 1993 12197 12204
26. Voet, D. & Voet, J.G. (1995). Biochemistry 2nd edit., Wiley, New York.
27. G. Archontis, S. Thomas, D. Moras, and M. Karplus Specific amino acid recognition by aspartyl-tRNA synthetase studied by free energy simulations J. Mol. Biol. 275 1998 823 846
28. T. Simonson, G. Archontis, and M. Karplus A Poisson-Boltzmann study of charge insertion in an enzyme active site: the effect of dielectric relaxation J. Phys. Chem. ser. B 103 1999 6142 6156
29. G. Archontis, T. Simonson, and M. Karplus Binding free energies and free energy components from molecular dynamics and Poisson-Boltzmann calculations. Application to amino acid recognition by aspartyl-tRNA synthetase J. Mol. Biol. 306 2001 307 327
30. W.P. Jencks Binding energy, specificity, and enzymic catalysis: the Circe effect Advan. Enzymol. 43 1975 219 410
31. Fersht, A.R. (1985). Enzyme Structure and Mechanism, 2nd edit., W. H. Freeman, New York.
32. M.K. Gilson, and B.H. Honig Calculation of electrostatic potentials in an enzyme active site Nature 330 1987 84 86
33. M.K. Gilson, and B. Honig Calculation of the total electrostatic energy of a macro-molecular system: solvation energies, binding energies, and conformational analysis Proteins: Struct. Funct. Genet. 4 1988 7 18
34. V. Mohan, M.E. Davis, J.A. McCammon, and B.M. Pettitt Continuum model calculations of solvation free energies: accurate evaluation of electrostatic contributions J. Phys. Chem. 96 1992 6428 6431
35. Z.S. Hendsch, and B. Tidor Do salt bridges stabilize proteins? A continuum electrostatics analysis Protein Sci. 3 1994 211 226
36. D. Sitkoff, K.A. Sharp, and B. Honig Accurate calculation of hydration free energies using macroscopic solvent models J. Phys. Chem. 98 1994 1978 1988
37. J. Antosiewicz, J.A. McCammon, and M.K. Gilson Prediction of pH-dependent properties of proteins J. Mol. Biol. 238 1994 415 436
38. J. Antosiewicz, J.A. McCammon, and M.K. Gilson The determination of pK(a)s in proteins Biochemistry 35 1996 7819 7833
39. M. Schaefer, M. Sommer, and M. Karplus pH-dependence of protein stability: absolute electrostatic free energy differences between conformations J. Phys. Chem. ser. B 101 1997 1663 1683
40. a calculations: conformational averaging versus the average structure Proteins: Struct. Funct. Genet. 33 1998 145 158
41. B. Kuhn, and P.A. Kollman A ligand that is predicted to bind better to avidin than biotin: insights from computational fluorine scanning J. Am. Chem. Soc. 122 2000 3909 3916
42. D. Murray, S. McLaughlin, and B. Honig The role of electrostatic interactions in the regulation of the membrane association of G protein βγ heterodimers J. Biol. Chem. 276 2001 45153 45159
43. T. Sulea, and E.O. Purisima Optimizing ligand charges for maximum binding affinity. A solvated interaction energy approach J. Phys. Chem. ser. B 105 2001 889 899
44. A.T. Brünger, and M. Karplus Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison Proteins: Struct. Funct. Genet. 4 1988 148 156
45. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
46. A.D. MacKerell, J. Wiorkiewicz-Kuczera, and M.M. Karplus An all-atom empirical energy function for the simulation of nucleic acids J. Am. Chem. Soc. 117 1995 11946 11975
47. C.I. Bayly, P. Cieplak, W.D. Cornell, and P.A. Kollman A well-behaved electro static potential based method using charge restraints for determining atom-centered charges: the RESP model J. Phys. Chem. 97 1993 10269 10280
48. W.D. Cornell, P. Cieplak, C.I. Bayly, and P.A. Kollman Application of RESP charges to calculate conformational energies, hydrogen bond energies, and free energies of solvation J. Am. Chem. Soc. 115 1993 9620
49. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Gill, P. M. W., Johnson, B. G., Robb, M. A. et al. (1995). Gaussian 94, Revision D.1, Gaussian, Inc., Pittsburgh, PA.
50. D.F. Green, and B. Tidor A comprehensive evaluation of ab initio charge determination methods for use in continuum electrostatic calculations J. Phys. Chem. ser. B 107 2003 10261 10273
51. Bockris, J.O'M. & Reddy,A.K.N. (1973). Modern Electrochemistry, Plenum Press, New York.
52. M.K. Gilson, K.A. Sharp, and B.H. Honig Calculating the electrostatic potential of molecules in solution: method and error assessment J. Comput. Chem. 9 1988 327 335
53. K.A. Sharp, and B. Honig Electrostatic interactions in macromolecules: theory and applications Annu. Rev. Biophys. Biophys. Chem. 19 1990 301 332
54. K.A. Sharp, and B. Honig Calculating total electrostatic energies with the nonlinear Poisson-Boltzmann equation J. Phys. Chem. 94 1990 7684 7692
55. L.T. Chong, S.E. Dempster, Z.S. Hendsch, L.-P. Lee, and B. Tidor Computation of electrostatic complements to proteins: a case of charge stabilized binding Protein Sci. 7 1998 206 210
56. E. Kangas, and B. Tidor Charge optimization leads to favorable electrostatic binding free energy Phys. Rev. ser. E 59 1999 5958 5961
57. E. Kangas, and B. Tidor Electrostatic specificity in molecular ligand design J. Chem. Phys. 112 2000 9120 9131
58. Shanno, D. & Vanderbei, R.J. (1999). An interior-point method for nonconvex nonlinear programming, Computat. Optimization Appl., 12.
59. R.J. Vanderbei LOQO: an interior-point code for quadratic programing Optimization Methods Software 12 1999 451 454
60. R.J. Vanderbei LOQO user's manual-version 3.10 Optimization Methods Software 12 1999 485 514
61. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallog. 24 1991 946 950
62. E.A. Merritt, and D.J. Bacon Raster3D: photorealistic molecular graphics Methods Enzymol. 277 1997 505 524