Correction: Uncovering the determinants of a highly perturbed tyrosine p K a in the active site of ketosteroid isomerase (Biochemistry (2013) 52:44 (7840-7855) DOI: 10.1021/bi401083b);Uncovering the determinants of a highly perturbed tyrosine pKa in the active site of ketosteroid isomerase

Biochemistry

Volumn 52, Issue 44, 2013, Pages 7840-7855

  Schwans, Jason P ^a   Sunden, Fanny ^a   Gonzalez, Ana ^b   Tsai, Yingssu ^a,b   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; CHAINS; ENZYMES; HYDROGEN BONDS; METAL IONS; METALS; MOLECULES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SOLUTIONS; STATISTICAL TESTS;

ABSORBANCE SPECTROSCOPY; COMPREHENSIVE COMPARISONS; COMPUTATIONAL APPROACH; DOMINANT CONTRIBUTIONS; SITE DIRECTED MUTAGENESIS; STABILIZING INTERACTIONS; STRUCTURAL PERTURBATION; STRUCTURAL REARRANGEMENT;

X RAY CRYSTALLOGRAPHY;

BACTERIAL ENZYME; STEROID DELTA ISOMERASE; TYROSINE; WATER;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ASSAY; ENZYME KINETICS; ENZYME STRUCTURE; FEEDBACK SYSTEM; HYDROGEN BOND; MUTAGENESIS; NONHUMAN; PEPTIDE SYNTHESIS; PKA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS PUTIDA; SITE DIRECTED MUTAGENESIS; ULTRAVIOLET SPECTROSCOPY; X RAY CRYSTALLOGRAPHY;

PSEUDOMONAS PUTIDA;

EID: 84887711854     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.8b00246     Document Type: Erratum

References (99)

1. a values of catalytic groups in enzyme active sites IUBMB Life 53, 85-98
2. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy Proc. Natl. Acad. Sci. U.S.A. 96, 5498-5503
3. 5-steroid isomerase Biochemistry 37, 10499-10506
4. a values of active site residues Biochemistry 35, 814-823
5. Karp, D. A., Stahley, M. R., and Garcia-Moreno, B. (2010) Conformational consequences of ionization of Lys, Asp, and Glu buried at position 66 in staphylococcal nuclease Biochemistry 49, 4138-4146
6. a for Cys282 in the active site of human muscle creatine kinase Biochemistry 40, 11698-11705
7. Dyson, H. J., Jeng, M. F., Tennant, L. L., Slaby, I., Lindell, M., Cui, D. S., Kuprin, S., and Holmgren, A. (1997) Effects of buried charged groups on cysteine thiol ionization and reactivity in Escherichia coli thioredoxin: Structural and functional characterization of mutants of Asp 26 and Lys 57 Biochemistry 36, 2622-2636
8. Oda, Y., Yamazaki, T., Nagayama, K., Kanaya, S., Kuroda, Y., and Nakamura, H. (1994) Individual ionization constants of all the carboxyl groups in ribonuclease HI from Escherichia coli determined by NMR Biochemistry 33, 5275-5284
9. 13C-NMR study of bacillus circulans xylanase Biochemistry 35, 9958-9966
10. a of the essential Cys-12 residue of the ArsC arsenate reductase of plasmid R773 J. Biol. Chem. 271, 33256-33260
11. a of the catalytic base in 4-oxalocrotonate tautomerase: kinetic and structural effects of mutations of Phe-50 Biochemistry 40, 1984-1995
12. Sun, S. and Toney, M. D. (1999) Evidence for a two-base mechanism involving tyrosine-265 from arginine-219 mutants of alanine racemase Biochemistry 38, 4058-4065
13. a of the retinal Schiff base during the photocycle of bacteriorhodopsin Proc. Natl. Acad. Sci. U.S.A. 93, 1731-1734
14. a of active-site lysine 115 Biochemistry 35, 41-46
15. Kokesh, F. C. and Westheimer, F. H. (1971) A reporter group at the active site of acetoacetate decarboxylase. II. Ionization constant of the amino group J. Am. Chem. Soc. 93, 7270-7274
16. Lodi, P. J. and Knowles, J. R. (1991) Neutral imidazole is the electrophile in the reaction catalyzed by triosephosphate isomerase: Structural origins and catalytic implications Biochemistry 30, 6948-6956
17. Fafarman, A. T., Sigala, P. A., Schwans, J. P., Fenn, T. D., Herschlag, D., and Boxer, S. G. (2012) Quantitative, directional measurement of electric field heterogeneity in the active site of ketosteroid isomerase Proc. Natl. Acad. Sci. U.S.A. 109, 299-308
18. Sigala, P. A., Fafarman, A. T., Schwans, J. P., Fried, S. D., Fenn, T. D., Caaveiro, J. M., Pybus, B., Ringe, D., Petsko, G. A., Boxer, S. G., and Herschlag, D. (2013) Quantitative dissection of hydrogen bond-mediated proton transfer in the ketosteroid isomerase active site Proc. Natl. Acad. Sci. U.S.A. 110, 2552-2561
19. Elcock, A. H. (2001) Prediction of functionally important residues based solely on the computed energetics of protein structure J. Mol. Biol. 312, 885-896
20. a, redox reactions and solvation free energies J. Phys. Chem. B 113, 1253-1272
21. Russell, S. T. and Warshel, A. (1985) Calculations of electrostatic energies in proteins. The energetics of ionized groups in bovine pancreatic trypsin inhibitor J. Mol. Biol. 185, 389-404
22. a, proton transfer reactions, and general acid catalysis reactions in enzymes Biochemistry 20, 3167-3177
23. Sandberg, L. and Edholm, O. (1999) A fast and simple method to calculate protonation states in proteins Proteins 36, 474-483
24. a values in enzyme active sites Protein Sci. 12, 1894-1901
25. a calculations Protein Sci. 12, 313-326
26. a calculations Proteins 43, 403-412
27. Mehler, E. L. and Guarnieri, F. (1999) A self-consistent, microenvironment modulated screened coulomb potential approximation to calculate pH-dependent electrostatic effects in proteins Biophys. J. 77, 3-22
28. Vizcarra, C. L. and Mayo, S. L. (2005) Electrostatics in computational protein design Curr. Opin. Chem. Biol. 9, 622-626
29. Juffer, A. H. (1998) Theoretical calculations of acid-dissociation constants of proteins Biochem. Cell Biol. 76, 198-209
30. as in proteins Biochemistry 35, 7819-7833
31. a values in proteins Proteins 48, 388-403
32. Nakamura, H. (1996) Roles of electrostatic interaction in proteins Q. Rev. Biophys. 29, 1-90
33. a values of lysine residues buried inside a protein Proc. Natl. Acad. Sci. U.S.A. 108, 5260-5265
34. a values for protein-ligand complexes Proteins 73, 765-783
35. a values Proteins 61, 704-721
36. a shifts in proteins Proteins 48, 283-292
37. a of glutamic acid-35 Biochemistry 31, 5545-5553
38. Joshi, M. D., Sidhu, G., Nielsen, J. E., Brayer, G. D., Withers, S. G., and McIntosh, L. P. (2001) Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase Biochemistry 40, 10115-10139
39. Thurlkill, R. L., Grimsley, G. R., Scholtz, J. M., and Pace, C. N. (2006) Hydrogen bonding markedly reduces the p K of buried carboxyl groups in proteins J. Mol. Biol. 362, 594-604
40. Laurents, D. V., Huyghues-Despointes, B. M., Bruix, M., Thurlkill, R. L., Schell, D., Newsom, S., Grimsley, G. R., Shaw, K. L., Trevino, S., Rico, M., Briggs, J. M., Antosiewicz, J. M., Scholtz, J. M., and Pace, C. N. (2003) Charge-charge interactions are key determinants of the p K values of ionizable groups in ribonuclease Sa (pI=3.5) and a basic variant (pI=10.2) J. Mol. Biol. 325, 1077-1092
41. Adams, J., Johnson, K., Matthews, R., and Benkovic, S. J. (1989) Effects of distal point-site mutations on the binding and catalysis of dihydrofolate reductase from Escherichia coli Biochemistry 28, 6611-6618
42. Pey, A. L., Rodriguez-Larrea, D., Gavira, J. A., Garcia-Moreno, B., and Sanchez-Ruiz, J. M. (2010) Modulation of buried ionizable groups in proteins with engineered surface charge J. Am. Chem. Soc. 132, 1218-1219
43. Kraut, D. A., Carroll, K. S., and Herschlag, D. (2003) Challenges in enzyme mechanism and energetics Annu. Rev. Biochem. 72, 517-571
44. Kraut, D. A., Sigala, P. A., Fenn, T. D., and Herschlag, D. (2010) Dissecting the paradoxical effects of hydrogen bond mutations in the ketosteroid isomerase oxyanion hole Proc. Natl. Acad. Sci. U.S.A. 107, 1960-1965
45. Schwans, J. P., Sunden, F., Gonzalez, A., Tsai, Y., and Herschlag, D. (2011) Evaluating the catalytic contribution from the oxyanion hole in ketosteroid isomerase J. Am. Chem. Soc. 133, 20052-20055
46. Knowles, J. R. (1987) Tinkering with enzymes: What are we learning? Science 236, 1252-1258
47. Lim, W. A., Farruggio, D. C., and Sauer, R. T. (1992) Structural and energetic consequences of disruptive mutations in a protein core Biochemistry 31, 4324-4333
48. Lim, W. A. and Sauer, R. T. (1989) Alternative packing arrangements in the hydrophobic core of lambda repressor Nature 339, 31-36
49. Baase, W. A., Liu, L., Tronrud, D. E., and Matthews, B. W. (2010) Lessons from the lysozyme of phage T4 Protein Sci. 19, 631-641
50. Dao-pin, S., Anderson, D. E., Baase, W. A., Dahlquist, F. W., and Matthews, B. W. (1991) Structural and thermodynamic consequences of burying a charged residue within the hydrophobic core of T4 lysozyme Biochemistry 30, 11521-11529
51. Mooers, B. H., Baase, W. A., Wray, J. W., and Matthews, B. W. (2009) Contributions of all 20 amino acids at site 96 to the stability and structure of T4 lysozyme Protein Sci. 18, 871-880
52. Zhang, X. J., Wozniak, J. A., and Matthews, B. W. (1995) Protein flexibility and adaptability seen in 25 crystal forms of T4 lysozyme J. Mol. Biol. 250, 527-552
53. Kraut, D. A., Sigala, P. A., Pybus, B., Liu, C. W., Ringe, D., Petsko, G. A., and Herschlag, D. (2006) Testing electrostatic complementarity in enzyme catalysis: hydrogen bonding in the ketosteroid isomerase oxyanion hole PLoS Biol. 4, 501-519
54. Kent, S. B. (1988) Chemical synthesis of peptides and proteins Annu. Rev. Biochem. 57, 957-989
55. Hackeng, T. M., Griffin, J. H., and Dawson, P. E. (1999) Protein synthesis by native chemical ligation: Expanded scope by using straightforward methodology Proc. Natl. Acad. Sci. U.S.A. 96, 10068-10073
56. Johnson, E. C. and Kent, S. B. (2006) Insights into the mechanism and catalysis of the native chemical ligation reaction J. Am. Chem. Soc. 128, 6640-6646
57. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 6, 1948-1954
58. Nagel, R. L., Ranney, H. M., and Kucinskis, L. L. (1966) Tyrosine ionization in human carbon monoxide and deoxyhemoglobins Biochemistry 5, 1934-1942
59. Donovan, J. W., Laskowski, M. J., and Scheraga, H. A. (1961) The effects of charged groups on the chromophores of lysozyme and of amino acids J. Am. Chem. Soc. 83, 2686-2694
60. Soltis, S. M., Cohen, A. E., Deacon, A., Eriksson, T., Gonzalez, A., McPhillips, S., Chui, H., Dunten, P., Hollenbeck, M., Mathews, I., Miller, M., Moorhead, P., Phizackerley, R. P., Smith, C., Song, J., van dem Bedem, H., Ellis, P., Kuhn, P., McPhillips, T., Sauter, N., Sharp, K., Tsyba, I., and Wolf, G. (2008) New paradigm for macromolecular crystallography experiments at SSRL: Automated crystal screening and remote data collection Acta Crystallogr., Sect. D. 64, 1210-1221
61. Kabsch, W. (2010) XDS Acta Crystallogr., Sect. D 66, 125-132
62. Collaborative Computational Project, Number 4. (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr., Sect. D 50, 760-763
63. Krissinel, E. B., Winn, M. D., Ballard, C. C., Ashton, A. W., Patel, P., Potterton, E. A., McNicholas, S. J., Cowtan, K. D., and Emsley, P. (2004) The new CCP4 Coordinate Library as a toolkit for the design of coordinate-related applications in protein crystallography Acta Crystallogr., Sect. D 60, 2250-2255
64. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D 53, 240-255
65. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr., Sect. D 60, 2126-2132
66. Pollack, R. M. (2004) Enzymatic mechanisms for catalysis of enolization: Ketosteroid isomerase Bioorg. Chem. 32, 341-353
67. 5-steroid isomerase Arch. Biochem. Biophys. 370, 9-15
68. 5-3-ketosteroid isomerase Curr. Opin. Struct. Biol. 11, 674-678
69. Liu, Y., Thoden, J. B., Kim, J., Berger, E., Gulick, A. M., Ruzicka, F. J., Holden, H. M., and Frey, P. A. (1997) Mechanistic roles of tyrosine 149 and serine 124 in UDP-galactose 4-epimerase from Escherichia coli Biochemistry 36, 10675-10684
70. a values in the ovomucoid third domain to charge replacement at a neighboring residue Biochemistry 39, 8067-8072
71. a values for turkey ovomucoid third domain using a polarizable force field J. Phys. Chem. B 113, 7844-7850
72. a determination of the Asp(102) side chain in a serine protease J. Am. Chem. Soc. 134, 2348-2354
73. 5-3-ketosteroid isomerase with and without a reaction intermediate analogue Biochemistry 36, 14030-14036
74. Sigala, P. A., Caaveiro, J. M., Ringe, D., Petsko, G. A., and Herschlag, D. (2009) Hydrogen bond coupling in the ketosteroid isomerase active site Biochemistry 48, 6932-6939
75. Crammer, J. L. and Neuberger, A. (1943) The state of tyrosine in egg albumin and in insulin as determined by spectrophotometric titration Biochem. J. 37, 302-310
76. Grimsley, G. R., Scholtz, J. M., and Pace, C. N. (2009) A summary of the measured p K values of the ionizable groups in folded proteins Protein Sci. 18, 247-251
77. Richarz, R. and Wuthrich, K. (1978) Carbon-13 NMR chemical shifts of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH Biopolymers 17, 2133-2141
78. Jang, D. S., Cha, H. J., Cha, S. S., Hong, B. H., Ha, N. C., Lee, J. Y., Oh, B. H., Lee, H. S., and Choi, K. Y. (2004) Structural double-mutant cycle analysis of a hydrogen bond network in ketosteroid isomerase from Pseudomonas putida biotype B Biochem. J. 382, 967-973
79. Schwans, J. P., Sunden, F., Lassila, J. K., Gonzalez, A., Tsai, Y., and Herschlag, D. (2013) Use of anion-aromatic interactions to position the general base in the ketosteroid isomerase active site Proc. Natl. Acad. Sci. U.S.A. 110, 11308-11313
80. 5-3-ketosteroid isomerase from Pseudomonas putida biotype B J. Bacteriol. 177, 2602-2605
81. 5-3-ketosteroid isomerase from Pseudomonas testosteroni Biochemistry 37, 8325-8330
82. Gerratana, B., Cleland, W. W., and Frey, P. A. (2001) Mechanistic roles of Thr134, Tyr160, and Lys 164 in the reaction catalyzed by dTDP-glucose 4,6-dehydratase Biochemistry 40, 9187-9195
83. Pundak, S. and Roche, R. S. (1984) Tyrosine and tyrosinate fluorescence of bovine testes calmodulin: Calcium and pH dependence Biochemistry 23, 1549-1555
84. Kim, D. H., Jang, D. S., Nam, G. H., Choi, G., Kim, J. S., Ha, N. C., Kim, M. S., Oh, B. H., and Choi, K. Y. (2000) Contribution of the hydrogen-bond network involving a tyrosine triad in the active site to the structure and function of a highly proficient ketosteroid isomerase from Pseudomonas putida biotype B Biochemistry 39, 4581-4589
85. Jencks, W. P. (1987) Catalysis in Chemistry and Enzymology, 2 ed., Dover, New York.
86. Blow, D. (2000) So do we understand how enzymes work? Structure 8, 77-81
87. Narlikar, G. J. and Herschlag, D. (1998) Direct demonstration of the catalytic role of binding interactions in an enzymatic reaction Biochemistry 37, 9902-9911
88. Wang, S., Karbstein, K., Peracchi, A., Beigelman, L., and Herschlag, D. (1999) Identification of the hammerhead ribozyme metal ion binding site responsible for rescue of the deleterious effect of a cleavage site phosphorothioate Biochemistry 38, 14363-14378
89. Huang, Z., Wagner, C. R., and Benkovic, S. J. (1994) Nonadditivity of mutational effects at the folate binding site of Escherichia coli dihydrofolate reductase Biochemistry 33, 11576-11585
90. Fersht, A. R. (1999) Structure and Mechanism in Protein Science, 2 ed., W.H. Freeman and Company, New York.
91. Horovitz, A. (1987) Non-additivity in protein-protein interactions J. Mol. Biol. 196, 733-735
92. Horovitz, A. (1996) Double-mutant cycles: A powerful tool for analyzing protein structure and function Folding Des. 1, R121-126
93. as and adding missing hydrogens to macromolecules Nucleic Acids Res. 33, W368-371
94. a computation in proteins with pH adapted conformations Proteins 71, 1335-1348
95. a values and electrostatic effects in proteins Proteins 79, 3249-3259
96. Moretti, R., Fleishman, S. J., Agius, R., Torchala, M., Bates, P. A., Kastritis, P. L., Rodrigues, J. P., Trellet, M., Bonvin, A. M., Cui, M., Rooman, M., Gillis, D., Dehouck, Y., Moal, I., Romero-Durana, M., Perez-Cano, L., Pallara, C., Jimenez, B., Fernandez-Recio, J., Flores, S., Pacella, M., Kilambi, K. P., Gray, J. J., Popov, P., Grudinin, S., Esquivel-Rodriguez, J., Kihara, D., Zhao, N., Korkin, D., Zhu, X., Demerdash, O. N., Mitchell, J. C., Kanamori, E., Tsuchiya, Y., Nakamura, H., Lee, H., Park, H., Seok, C., Sarmiento, J., Liang, S., Teraguchi, S., Standley, D. M., Shimoyama, H., Terashi, G., Takeda-Shitaka, M., Iwadate, M., Umeyama, H., Beglov, D., Hall, D. R., Kozakov, D., Vajda, S., Pierce, B. G., Hwang, H., Vreven, T., Weng, Z., Huang, Y., Li, H., Yang, X., Ji, X., Liu, S., Xiao, Y., Zacharias, M., Qin, S., Zhou, H. X., Huang, S. Y., Zou, X., Velankar, S., Janin, J., Wodak, S. J., and Baker, D. Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions. Proteins [Online early access]. DOI: 10.1002/prot.24356. Published Online: Aug 23, 2013
97. Fleishman, S. J., Whitehead, T. A., Strauch, E. M., Corn, J. E., Qin, S., Zhou, H. X., Mitchell, J. C., Demerdash, O. N., Takeda-Shitaka, M., Terashi, G., Moal, I. H., Li, X., Bates, P. A., Zacharias, M., Park, H., Ko, J. S., Lee, H., Seok, C., Bourquard, T., Bernauer, J., Poupon, A., Aze, J., Soner, S., Ovali, S. K., Ozbek, P., Tal, N. B., Haliloglu, T., Hwang, H., Vreven, T., Pierce, B. G., Weng, Z., Perez-Cano, L., Pons, C., Fernandez-Recio, J., Jiang, F., Yang, F., Gong, X., Cao, L., Xu, X., Liu, B., Wang, P., Li, C., Wang, C., Robert, C. H., Guharoy, M., Liu, S., Huang, Y., Li, L., Guo, D., Chen, Y., Xiao, Y., London, N., Itzhaki, Z., Schueler-Furman, O., Inbar, Y., Potapov, V., Cohen, M., Schreiber, G., Tsuchiya, Y., Kanamori, E., Standley, D. M., Nakamura, H., Kinoshita, K., Driggers, C. M., Hall, R. G., Morgan, J. L., Hsu, V. L., Zhan, J., Yang, Y., Zhou, Y., Kastritis, P. L., Bonvin, A. M., Zhang, W., Camacho, C. J., Kilambi, K. P., Sircar, A., Gray, J. J., Ohue, M., Uchikoga, N., Matsuzaki, Y., Ishida, T., Akiyama, Y., Khashan, R., Bush, S., Fouches, D., Tropsha, A., Esquivel-Rodriguez, J., Kihara, D., Stranges, P. B., Jacak, R., Kuhlman, B., Huang, S. Y., Zou, X., Wodak, S. J., Janin, J., and Baker, D. (2011) Community-wide assessment of protein-interface modeling suggests improvements to design methodology J. Mol. Biol. 414, 289-302
98. Runthala, A. (2012) Protein structure prediction: challenging targets for CASP10 J. Biomol. Struct. Dyn. 30, 607-615
99. Nugent, T., Cozzetto, D., and Jones, D. T. Evaluation of predictions in the CASP10 model refinement category. Proteins [Online early access]. DOI: 10.1002/prot.24377. Published Online: July 31, 2013