Testing Electrostatic Complementarity in Enzyme Catalysis: Hydrogen Bonding in the Ketosteroid Isomerase Oxyanion Hole

Kraut, Daniel A.; Sigala, Paul A.; Pybus, Brandon; Liu, Corey W.; Ringe, Dagmar; Petsko, Gregory A.; Herschlag, Daniel

doi:10.1371/journal.pbio.0040099

Title: Testing Electrostatic Complementarity in Enzyme Catalysis: Hydrogen Bonding in the Ketosteroid Isomerase Oxyanion Hole

Journal Article · Tue Mar 28 00:00:00 EST 2006 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.0040099· OSTI ID:1627145

Kraut, Daniel A. ^[1]; Sigala, Paul A. ^[1]; Pybus, Brandon ^[2]; Liu, Corey W. ^[3]; Ringe, Dagmar ^[2]; Petsko, Gregory A. ^[2]; Herschlag, Daniel ^[1]

Stanford Univ., CA (United States). Dept. of Biochemistry
Brandeis Univ., Waltham, MA (United States). Dept. of Biochemistry
SLAC National Accelerator Lab., Menlo Park, CA (United States). Magnetic Resonance Lab.

A longstanding proposal in enzymology is that enzymes are electrostatically and geometrically complementary to the transition states of the reactions they catalyze and that this complementarity contributes to catalysis. Experimental evaluation of this contribution, however, has been difficult. We have systematically dissected the potential contribution to catalysis from electrostatic complementarity in ketosteroid isomerase. Phenolates, analogs of the transition state and reaction intermediate, bind and accept two hydrogen bonds in an active site oxyanion hole. The binding of substituted phenolates of constant molecular shape but increasing pK_a models the charge accumulation in the oxyanion hole during the enzymatic reaction. As charge localization increases, the NMR chemical shifts of protons involved in oxyanion hole hydrogen bonds increase by 0.50–0.76 ppm/pK_a unit, suggesting a bond shortening of ~0.02 Å/pK_a unit. Nevertheless, there is little change in binding affinity across a series of substituted phenolates (ΔΔG = –0.2 kcal/mol/pK_a unit). The small effect of increased charge localization on affinity occurs despite the shortening of the hydrogen bonds and a large favorable change in binding enthalpy (ΔΔH = –2.0 kcal/mol/pK_a unit). This shallow dependence of binding affinity suggests that electrostatic complementarity in the oxyanion hole makes at most a modest contribution to catalysis of ~300-fold. We propose that geometrical complementarity between the oxyanion hole hydrogen-bond donors and the transition state oxyanion provides a significant catalytic contribution, and suggest that KSI, like other enzymes, achieves its catalytic prowess through a combination of modest contributions from several mechanisms rather than from a single dominant contribution.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-76SF00515; W-31-109-Eng-38

OSTI ID:: 1627145

Journal Information:: PLoS Biology (Online), Vol. 4, Issue 4; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (127)

Hydrogen bonding between solutes in aqueous solution Stahl, Neil.; Jencks, William P. Journal of the American Chemical Society, Vol. 108, Issue 14 https://doi.org/10.1021/ja00274a058	journal	July 1986
Hydrogen bonding and biological specificity analysed by protein engineering Fersht, Alan R.; Shi, Jian-Ping; Knill-Jones, Jack Nature, Vol. 314, Issue 6008 https://doi.org/10.1038/314235a0	journal	March 1985
High-Resolution Crystal Structures of Δ⁵-3-Ketosteroid Isomerase with and without a Reaction Intermediate Analogue Kim, Suhng Wook; Cha, Sun-Shin; Cho, Hyun-Soo Biochemistry, Vol. 36, Issue 46 https://doi.org/10.1021/bi971546+	journal	November 1997
Structural origins of efficient proton abstraction from carbon by a catalytic antibody Debler, E. W.; Ito, S.; Seebeck, F. P. Proceedings of the National Academy of Sciences, Vol. 102, Issue 14 https://doi.org/10.1073/pnas.0409207102	journal	March 2005
How do enzymes work? Kraut, J. Science, Vol. 242, Issue 4878 https://doi.org/10.1126/science.3051385	journal	October 1988
Theoretical studies of enzymic reactions: Dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme Warshel, A.; Levitt, M. Journal of Molecular Biology, Vol. 103, Issue 2 https://doi.org/10.1016/0022-2836(76)90311-9	journal	May 1976
Lengthening of the covalent O–H bond in O–H ^... O hydrogen bonds re-examined from low-temperature neutron diffraction data of organic compounds Steiner, T.; Saenger, W. Acta Crystallographica Section B Structural Science, Vol. 50, Issue 3 https://doi.org/10.1107/S0108768193011966	journal	June 1994
Importance of Hydrogen-Bond Formation in Stabilizing the Transition State of Subtilisin Wells, J. A.; Cunningham, B. C.; Graycar, T. P. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 317, Issue 1540, p. 415-423 https://doi.org/10.1098/rsta.1986.0051	journal	April 1986
Electrophilic Assistance by Asp-99 of 3-Oxo-Δ ⁵ -steroid Isomerase Thornburg, Lora D.; Hénot, Frédéric; Bash, Diarmad P. Biochemistry, Vol. 37, Issue 29 https://doi.org/10.1021/bi980099a	journal	June 1998
Proton chemical shift tensors in hydrogen‐bonded dimers of RCOOH and ROH Rohlfing, Celeste McMichael; Allen, Leland C.; Ditchfield, Robert The Journal of Chemical Physics, Vol. 79, Issue 10 https://doi.org/10.1063/1.445589	journal	November 1983
The correlation between hydrogen-bond lengths and proton chemical shifts in crystals Jeffrey, G. A.; Yeon, Y. Acta Crystallographica Section B Structural Science, Vol. 42, Issue 4 https://doi.org/10.1107/S0108768186098038	journal	August 1986
Enzyme catalysis: not different, just better Knowles, Jeremy R. Nature, Vol. 350, Issue 6314 https://doi.org/10.1038/350121a0	journal	March 1991
Energetic cost and structural consequences of burying a hydroxyl group within the core of a protein determined from Ala .fwdarw. Ser and Val .fwdarw. Thr substitutions in T4 lysozyme Blaber, Michael; Lindstrom, Joel D.; Gassner, Nadine Biochemistry, Vol. 32, Issue 42 https://doi.org/10.1021/bi00093a013	journal	October 1993
NMR evidence for the participation of a low-barrier hydrogen bond in the mechanism of delta 5-3-ketosteroid isomerase. Zhao, Q.; Abeygunawardana, C.; Talalay, P. Proceedings of the National Academy of Sciences, Vol. 93, Issue 16 https://doi.org/10.1073/pnas.93.16.8220	journal	August 1996
Enzymes work by solvation substitution rather than by desolvation. Warshel, A.; Aqvist, J.; Creighton, S. Proceedings of the National Academy of Sciences, Vol. 86, Issue 15 https://doi.org/10.1073/pnas.86.15.5820	journal	August 1989
1H, 13C and 15N chemical shift referencing in biomolecular NMR Wishart, David S.; Bigam, Colin G.; Yao, Jian Journal of Biomolecular NMR, Vol. 6, Issue 2 https://doi.org/10.1007/BF00211777	journal	September 1995
Do salt bridges stabilize proteins? A continuum electrostatic analysis: Salt-bridge effects on protein stability Hendsch, Zachary S.; Tidor, Bruce Protein Science, Vol. 3, Issue 2 https://doi.org/10.1002/pro.5560030206	journal	February 1994
Kinetic and ultraviolet spectroscopic studies of active-site mutants of .DELTA.5-3-ketosteroid isomerase Kuliopulos, Athan; Mildvan, Albert S.; Shortle, David Biochemistry, Vol. 28, Issue 1 https://doi.org/10.1021/bi00427a022	journal	January 1989
Walden-Inversion-Enforced Transition-State Stabilization in a Protein Tyrosine Phosphatase Alhambra, Cristobal; Wu, Li; Zhang, Zhong-Yin Journal of the American Chemical Society, Vol. 120, Issue 16 https://doi.org/10.1021/ja972578n	journal	April 1998
Geometry of the imino-carbonyl (N-H...O:C) hydrogen bond. 1. Lone-pair directionality Taylor, Robin; Kennard, Olga; Versichel, Werner Journal of the American Chemical Society, Vol. 105, Issue 18 https://doi.org/10.1021/ja00356a010	journal	September 1983
Low-barrier hydrogen bonds and enzymic catalysis Cleland, W.; Kreevoy, M. Science, Vol. 264, Issue 5167 https://doi.org/10.1126/science.8009219	journal	June 1994
Dependence of Calculated NMR Proton Chemical Shifts on Electron Density Properties in Proton-Transfer Processes on Short Strong Hydrogen Bonds Pacios, Luis F.; Gómez, Pedro C. The Journal of Physical Chemistry A, Vol. 108, Issue 52 https://doi.org/10.1021/jp0466892	journal	December 2004
Crystal structure of a lysozyme-tetrasaccharide lactone complex Ford, L. O.; Johnson, L. N.; Machin, P. A. Journal of Molecular Biology, Vol. 88, Issue 2 https://doi.org/10.1016/0022-2836(74)90487-2	journal	September 1974
Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride Fukada, Harumi; Takahashi, Katsutada Proteins: Structure, Function, and Genetics, Vol. 33, Issue 2 https://doi.org/10.1002/(SICI)1097-0134(19981101)33:2<159::AID-PROT2>3.0.CO;2-E	journal	November 1998
Why Enzymes Are Proficient Catalysts: Beyond the Pauling Paradigm Zhang, Xiyun; Houk, K. N. Accounts of Chemical Research, Vol. 38, Issue 5 https://doi.org/10.1021/ar040257s	journal	March 2005
Development of a Knowledge-Based Potential for Crystals of Small Organic Molecules: Calculation of Energy Surfaces for C=0···H−N Hydrogen Bonds Grzybowski, Bartosz A.; Ishchenko, Alexey V.; DeWitte, Robert S. The Journal of Physical Chemistry B, Vol. 104, Issue 31 https://doi.org/10.1021/jp000644t	journal	August 2000
On the calculation of electrostatic interactions in proteins Gilson, Michael K.; Rashin, Alexander; Fine, Richard Journal of Molecular Biology, Vol. 184, Issue 3 https://doi.org/10.1016/0022-2836(85)90297-9	journal	August 1985
Electrostatic Origin of the Catalytic Power of Enzymes and the Role of Preorganized Active Sites Warshel, Arieh Journal of Biological Chemistry, Vol. 273, Issue 42 https://doi.org/10.1074/jbc.273.42.27035	journal	October 1998
New Ideas about Enzyme Reactions Dewar, M. J. S. Enzyme, Vol. 36, Issue 1-2 https://doi.org/10.1159/000469274	journal	January 1986
Evaluation of the Internal Equilibrium Constant for 3-Oxo-.DELTA.5-steroid Isomerase Using the D38E and D38N Mutants: The Energetic Basis for Catalysis Hawkinson, David C.; Pollack, Ralph M.; Ambulos, Nicholas P. Biochemistry, Vol. 33, Issue 40 https://doi.org/10.1021/bi00206a021	journal	October 1994
Fluorescence spectrometry. A review Parker, C. A.; Rees, W. T. The Analyst, Vol. 87, Issue 1031 https://doi.org/10.1039/an9628700083	journal	January 1962
Analog approaches to the structure of the transition state in enzyme reactions Wolfenden, Richard Accounts of Chemical Research, Vol. 5, Issue 1 https://doi.org/10.1021/ar50049a002	journal	January 1972
Linear solvation energy relationships: standard molar Gibbs free energies and enthalpies of transfer of ions from water into nonaqueous solvents Marcus, Y.; Kamlet, M. J.; Taft, R. W. The Journal of Physical Chemistry, Vol. 92, Issue 12 https://doi.org/10.1021/j100323a057	journal	June 1988
Exact Analysis of Competition Ligand Binding by Displacement Isothermal Titration Calorimetry Sigurskjold, Bent W. Analytical Biochemistry, Vol. 277, Issue 2 https://doi.org/10.1006/abio.1999.4402	journal	January 2000
Understanding enzymic catalysis: the importance of short, strong hydrogen bonds Gerlt, John A.; Kreevoy, Maurice M.; Cleland, W. W. Chemistry & Biology, Vol. 4, Issue 4 https://doi.org/10.1016/S1074-5521(97)90069-7	journal	April 1997
Solvent isotope effects on the ionization of hydrofluoric acid Kresge, A. J.; Chiang, Y. The Journal of Physical Chemistry, Vol. 77, Issue 6 https://doi.org/10.1021/j100625a018	journal	March 1973
The Catalytic Power of Ketosteroid Isomerase Investigated by Computer Simulation ^† Feierberg, Isabella; Åqvist, Johan Biochemistry, Vol. 41, Issue 52 https://doi.org/10.1021/bi026873i	journal	December 2002
On the magnitude of the electrostatic contribution to ligand-DNA interactions. Misra, V. K.; Honig, B. Proceedings of the National Academy of Sciences, Vol. 92, Issue 10 https://doi.org/10.1073/pnas.92.10.4691	journal	May 1995
Leaving group specificity in the chymotrypsin-catalyzed hydrolysis of peptides. Stereochemical interpretation Fersht, Alan R.; Blow, D. M.; Fastrez, Jacques Biochemistry, Vol. 12, Issue 11 https://doi.org/10.1021/bi00735a002	journal	May 1973
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
“Strong” Hydrogen Bonds in Chemistry and Biology Perrin, Charles L.; Nielson, Jennifer B. Annual Review of Physical Chemistry, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.physchem.48.1.511	journal	October 1997
A proficient enzyme Radzicka, A.; Wolfenden, R. Science, Vol. 267, Issue 5194 https://doi.org/10.1126/science.7809611	journal	January 1995
Entropic Contributions to Rate Accelerations in Enzymic and Intramolecular Reactions and the Chelate Effect Page, M. I.; Jencks, W. P. Proceedings of the National Academy of Sciences, Vol. 68, Issue 8 https://doi.org/10.1073/pnas.68.8.1678	journal	August 1971
Probing the limits of protein-amino acid side chain recognition with the aminoacyl-tRNA synthetases. Discrimination against phenylalanine by tyrosyl-tRNA synthetases Fersht, Alan R.; Shindler, Julian S.; Tsui, Wing-Cheong Biochemistry, Vol. 19, Issue 24 https://doi.org/10.1021/bi00565a009	journal	November 1980
Calibration of methanol and ethylene glycol nuclear magnetic resonance thermometers Raiford, David S.; Fisk, Cherie L.; Becker, Edwin D. Analytical Chemistry, Vol. 51, Issue 12 https://doi.org/10.1021/ac50048a040	journal	October 1979
Molecular Architecture and Biological Reactions: Answers to many basic problems of biology—nature of growth, mechanism of duplication of viruses and genes, action of enzymes, mechanism, of physiological activity of drugs, hormones, and vitamins, structure and action of nerve and brain tissue—may lie in knowledge of molecular structure and intermolecular reactions Pauling, Linus Chemical & Engineering News, Vol. 24, Issue 10 https://doi.org/10.1021/cen-v024n010.p1375	journal	May 1946
The Low Barrier Hydrogen Bond in Enzymatic Catalysis Cleland, W. Wallace; Frey, Perry A.; Gerlt, John A. Journal of Biological Chemistry, Vol. 273, Issue 40 https://doi.org/10.1074/jbc.273.40.25529	journal	October 1998
Purification and mechanism of action of proline racemase Cardinale, George J.; Abeles, Robert H. Biochemistry, Vol. 7, Issue 11 https://doi.org/10.1021/bi00851a026	journal	November 1968
Challenges in Enzyme Mechanism and Energetics Kraut, Daniel A.; Carroll, Kate S.; Herschlag, Daniel Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161617	journal	June 2003
Catalysis, binding and enzyme-substrate complementarity Fersht, Alan Roy Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 187, Issue 1089, p. 397-407 https://doi.org/10.1098/rspb.1974.0084	journal	November 1974
Substituent Effects on the Binding of Phenols to the D38N Mutant of 3-Oxo-Δ ⁵ -steroid Isomerase. A Probe for the Nature of Hydrogen Bonding to the Intermediate ^† Petrounia, Ioanna P.; Pollack, Ralph M. Biochemistry, Vol. 37, Issue 2 https://doi.org/10.1021/bi972262s	journal	January 1998
Binding energy and catalysis: a lesson from protein engineering of the tyrosyl-tRNA synthetase Fersht, Alan R.; Leatherbarrow, Robin J.; Wells, Tim N. C. Trends in Biochemical Sciences, Vol. 11, Issue 8 https://doi.org/10.1016/0968-0004(86)90289-6	journal	August 1986
The importance of a distal hydrogen bonding group in stabilizing the transition state in subtilisin BPN' Braxton, S.; Wells, J. A. Journal of Biological Chemistry, Vol. 266, Issue 18 https://doi.org/10.1016/S0021-9258(18)99027-7	journal	June 1991
Electrostatic Interactions in Membranes and Proteins Honig, B. H.; Hubbell, W. L.; Flewelling, R. F. Annual Review of Biophysics and Biophysical Chemistry, Vol. 15, Issue 1 https://doi.org/10.1146/annurev.bb.15.060186.001115	journal	June 1986
Calculation of protein extinction coefficients from amino acid sequence data Gill, Stanley C.; von Hippel, Peter H. Analytical Biochemistry, Vol. 182, Issue 2 https://doi.org/10.1016/0003-2697(89)90602-7	journal	November 1989
Site-directed mutagenesis and the role of the oxyanion hole in subtilisin. Bryan, P.; Pantoliano, M. W.; Quill, S. G. Proceedings of the National Academy of Sciences, Vol. 83, Issue 11 https://doi.org/10.1073/pnas.83.11.3743	journal	June 1986
Probing the Ser-Ser-Lys Catalytic Triad Mechanism of Peptide Amidase: Computational Studies of the Ground State, Transition State, and Intermediate ^† Valiña, Anna Liza B.; Mazumder-Shivakumar, Devleena; Bruice, Thomas C. Biochemistry, Vol. 43, Issue 50 https://doi.org/10.1021/bi049025r	journal	December 2004
Bond Dissociation Energies of F2- and HF2-. A Gas-Phase Experimental and G2 Theoretical Study Wenthold, Paul G.; Squires, Robert R. The Journal of Physical Chemistry, Vol. 99, Issue 7 https://doi.org/10.1021/j100007a034	journal	February 1995
Thermodynamics and mechanism of the PO ₃ [phosphoester dianion] transfer process in the phosphoglucomutase reaction Ray, William J.; Long, James W. Biochemistry, Vol. 15, Issue 18 https://doi.org/10.1021/bi00663a014	journal	September 1976
Mechanistic Insights from the Three-Dimensional Structure of 3-Oxo-Δ5-steroid Isomerase Pollack, Ralph M.; Thornburg, Lora D.; Wu, Zheng Rong Archives of Biochemistry and Biophysics, Vol. 370, Issue 1 https://doi.org/10.1006/abbi.1999.1384	journal	October 1999
Directional hydrogen bonding to sp2- and sp3-hybridized oxygen atoms and its relevance to ligand-macromolecule interactions Murray-Rust, Peter; Glusker, Jenny P. Journal of the American Chemical Society, Vol. 106, Issue 4 https://doi.org/10.1021/ja00316a034	journal	February 1984
Short, Strong Hydrogen Bonds in the Gas Phase and in Solution: Theoretical Exploration of p K _a Matching and Environmental Effects on the Strengths of Hydrogen Bonds and Their Potential Roles in Enzymatic Catalysis Chen, Jiangang; McAllister, Michael A.; Lee, Jeehiun K. The Journal of Organic Chemistry, Vol. 63, Issue 14 https://doi.org/10.1021/jo972262y	journal	July 1998
Hydrogen bonding of carbonyl, ether, and ester oxygen atoms with alkanol hydroxyl groups Lommerse, Jos P. M.; Price, Sarah L.; Taylor, Robin Journal of Computational Chemistry, Vol. 18, Issue 6 https://doi.org/10.1002/(SICI)1096-987X(19970430)18:6<757::AID-JCC3>3.0.CO;2-R	journal	April 1997
Forces, bond lengths, and reactivity: fundamental insight into the mechanism of enzyme catalysis Tonge, Peter J.; Carey, Paul R. Biochemistry, Vol. 31, Issue 38 https://doi.org/10.1021/bi00153a002	journal	September 1992
X-ray and Thermodynamic Studies of Staphylococcal Nuclease Variants I92E and I92K: Insights into Polarity of the Protein Interior Nguyen, Duc M.; Leila Reynald, R.; Gittis, Apostolos G. Journal of Molecular Biology, Vol. 341, Issue 2 https://doi.org/10.1016/j.jmb.2004.05.066	journal	August 2004
Rapid measurement of binding constants and heats of binding using a new titration calorimeter Wiseman, Thomas; Williston, Samuel; Brandts, John F. Analytical Biochemistry, Vol. 179, Issue 1 https://doi.org/10.1016/0003-2697(89)90213-3	journal	May 1989
Inhibition of Elastase by N -Sulfonylaryl β-Lactams: Anatomy of a Stable Acyl−Enzyme Complex ^, Wilmouth, Rupert C.; Westwood, Nicholas J.; Anderson, Kerry Biochemistry, Vol. 37, Issue 50 https://doi.org/10.1021/bi9816249	journal	November 1998
High-Precision Measurement of Hydrogen Bond Lengths in Proteins by Nuclear Magnetic Resonance Methods Harris, Thomas K.; Mildvan, Albert S. Proteins: Structure, Function, and Genetics, Vol. 35, Issue 3 https://doi.org/10.1002/(SICI)1097-0134(19990515)35:3<275::AID-PROT1>3.0.CO;2-V	journal	May 1999
The hydrogen bond in molecular recognition Fersht, Alan R. Trends in Biochemical Sciences, Vol. 12 https://doi.org/10.1016/0968-0004(87)90146-0	journal	January 1987
Dissecting the catalytic triad of a serine protease Carter, Paul; Wells, James A. Nature, Vol. 332, Issue 6164 https://doi.org/10.1038/332564a0	journal	April 1988
Solution Structure of 3-Oxo-5-Steroid Isomerase Wu, Z. R. Science, Vol. 276, Issue 5311 https://doi.org/10.1126/science.276.5311.415	journal	April 1997
Environments and mechanistic roles of the tyrosine residues of .DELTA.5-3-ketosteroid isomerase Li, Yaw Kuen; Kuliopulos, Athan; Mildvan, Albert S. Biochemistry, Vol. 32, Issue 7 https://doi.org/10.1021/bi00058a016	journal	February 1993
Reevaluation of the Born model of ion hydration Rashin, Alexander A.; Honig, Barry The Journal of Physical Chemistry, Vol. 89, Issue 26 https://doi.org/10.1021/j100272a006	journal	December 1985
Effects of the α-helix dipole upon the functioning and structure of proteins and peptides Hol, W. Advances in Biophysics, Vol. 19 https://doi.org/10.1016/0065-227X(85)90053-X	journal	January 1985
What about protein polarity? Warshel, Arieh Nature, Vol. 330, Issue 6143 https://doi.org/10.1038/330015a0	journal	November 1987
Theoretical Investigation of the Relationship between Proton NMR Chemical Shift and Hydrogen Bond Strength Kumar, Ganesh A.; McAllister, Michael A. The Journal of Organic Chemistry, Vol. 63, Issue 20 https://doi.org/10.1021/jo980759h	journal	October 1998
Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate Vocadlo, David J.; Davies, Gideon J.; Laine, Roger Nature, Vol. 412, Issue 6849 https://doi.org/10.1038/35090602	journal	August 2001
Waterlogged molecules Wolfenden, R. Science, Vol. 222, Issue 4628 https://doi.org/10.1126/science.6359416	journal	December 1983
Dielectric properties of trypsin inhibitor and lysozyme calculated from molecular dynamics simulations Smith, Paul E.; Brunne, Roger M.; Mark, Alan E. The Journal of Physical Chemistry, Vol. 97, Issue 9 https://doi.org/10.1021/j100111a046	journal	March 1993
Directionality of Hydrogen Bonds to Sulfur and Oxygen Platts, J. A.; Howard, S. T.; Bracke, B. R. F. Journal of the American Chemical Society, Vol. 118, Issue 11 https://doi.org/10.1021/ja952871s	journal	January 1996
Electrostatic Complementarity at Ligand Binding Sites: Application to Chorismate Mutase Kangas, Erik; Tidor, Bruce The Journal of Physical Chemistry B, Vol. 105, Issue 4 https://doi.org/10.1021/jp003449n	journal	January 2001
Microscopic rate constants for the acetate ion catalyzed isomerization of 5-androstene-3,17-dione to 4-androstene-3,17-dione: a model for steroid isomerase Zeng, Baifei; Pollack, Ralph M. Journal of the American Chemical Society, Vol. 113, Issue 10 https://doi.org/10.1021/ja00010a028	journal	May 1991
Direct Structural Observation of an Acyl-Enzyme Intermediate in the Hydrolysis of an Ester Substrate by Elastase Ding, Xiaochun; Rasmussen, Bjarne F.; Petsko, Gregory A. Biochemistry, Vol. 33, Issue 31 https://doi.org/10.1021/bi00197a032	journal	August 1994
Unlocking the Secrets of Enzyme Power Using Raman Spectroscopy Carey, Paul R.; Tonge, Peter J. Accounts of Chemical Research, Vol. 28, Issue 1 https://doi.org/10.1021/ar00049a002	journal	January 1995
Short, strong hydrogen bonds on enzymes: NMR and mechanistic studies Mildvan, A. S.; Massiah, M. A.; Harris, T. K. Journal of Molecular Structure, Vol. 615, Issue 1-3 https://doi.org/10.1016/S0022-2860(02)00212-0	journal	September 2002
Enzymatic Catalysis and Transition-State Theory Lienhard, G. E. Science, Vol. 180, Issue 4082 https://doi.org/10.1126/science.180.4082.149	journal	April 1973
The Activated Complex and the Absolute Rate of Chemical Reactions. Eyring, Henry. Chemical Reviews, Vol. 17, Issue 1 https://doi.org/10.1021/cr60056a006	journal	August 1935
Correlations between proton chemical shift tensors, deuterium quadrupole couplings, and bond distances for hydrogen bonds in solids Berglund, Bo; Vaughan, Robert W. The Journal of Chemical Physics, Vol. 73, Issue 5 https://doi.org/10.1063/1.440423	journal	September 1980
Low-barrier hydrogen bonds and low fractionation factor bases in enzymic reactions Cleland, W. W. Biochemistry, Vol. 31, Issue 2 https://doi.org/10.1021/bi00117a001	journal	January 1992
Experimental evaluation of the effective dielectric constant of proteins Rees, Douglas C. Journal of Molecular Biology, Vol. 141, Issue 3 https://doi.org/10.1016/0022-2836(80)90184-9	journal	August 1980
Serine Proteases: Structure and Mechanism of Catalysis Kraut, J. Annual Review of Biochemistry, Vol. 46, Issue 1 https://doi.org/10.1146/annurev.bi.46.070177.001555	journal	June 1977
Binding of 2-Naphthols to D38E Mutants of 3-Oxo-Δ ⁵ -steroid Isomerase: Variation of Ligand Ionization State with the Nature of the Electrophilic Component Petrounia, Ioanna P.; Blotny, Grzegorz; Pollack, Ralph M. Biochemistry, Vol. 39, Issue 1 https://doi.org/10.1021/bi9917838	journal	December 1999
Low-Affinity Binding Determined by Titration Calorimetry Using a High-Affinity Coupling Ligand: A Thermodynamic Study of Ligand Binding to Protein Tyrosine Phosphatase 1B Zhang, Yan-Ling; Zhang, Zhong-Yin Analytical Biochemistry, Vol. 261, Issue 2 https://doi.org/10.1006/abio.1998.2738	journal	August 1998
Site-directed mutagenesis: A tool for studying enzyme catalysis Plapp, Bryce V. Methods in Enzymology, Vol. 249, 91-119 https://doi.org/10.1016/0076-6879(95)49032-9	book	January 1995
Short strong hydrogen bonds: can they explain enzymic catalysis? Peter Guthrie, J. Chemistry & Biology, Vol. 3, Issue 3 https://doi.org/10.1016/S1074-5521(96)90258-6	journal	March 1996
Critical Analysis of Antibody Catalysis Hilvert, Donald Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.751	journal	June 2000
Preparation of .beta.-substituted tryptophan derivatives: comparison of the reactivity of N-methylindole toward aziridine-2-lactones and aziridine-2-carboxylic esters and interpretation of results using MNDO calculations Dubois, Laurent; Mehta, Anita; Tourette, Emmanuelle The Journal of Organic Chemistry, Vol. 59, Issue 2 https://doi.org/10.1021/jo00081a025	journal	January 1994
Understanding the rates of certain enzyme-catalyzed reactions: Proton abstraction from carbon acids, acyl transfer reactions, and displacement reactions of phosphodiesters Gerlt, John A.; Gassman, Paul G. Biochemistry, Vol. 32, Issue 45 https://doi.org/10.1021/bi00096a001	journal	November 1993
Enzymatic mechanisms for catalysis of enolization: ketosteroid isomerase Pollack, Ralph M. Bioorganic Chemistry, Vol. 32, Issue 5 https://doi.org/10.1016/j.bioorg.2004.06.005	journal	October 2004
Subtilisin. Stereochemical mechanism involving transition-state stabilization Robertus, Jon D.; Kraut, Joseph; Alden, Richard A. Biochemistry, Vol. 11, Issue 23 https://doi.org/10.1021/bi00773a016	journal	November 1972
Internal stark effect measurement of the electric field at the amino terminus of an alpha helix Lockhart, D.; Kim, P. Science, Vol. 257, Issue 5072 https://doi.org/10.1126/science.1502559	journal	August 1992
A Transition State Analog for Lysozyme Secemski, Isaac I.; Lehrer, Sherwin S.; Lienhard, Gustav E. Journal of Biological Chemistry, Vol. 247, Issue 15 https://doi.org/10.1016/S0021-9258(19)44974-0	journal	August 1972
Energetics of 3-oxo-.DELTA.5-steroid isomerase: source of the catalytic power of the enzyme Hawkinson, David C.; Eames, Teresa C. M.; Pollack, Ralph M. Biochemistry, Vol. 30, Issue 45 https://doi.org/10.1021/bi00109a007	journal	November 1991
Stability of "salt bridges" in membrane proteins. Honig, B. H.; Hubbell, W. L. Proceedings of the National Academy of Sciences, Vol. 81, Issue 17 https://doi.org/10.1073/pnas.81.17.5412	journal	September 1984
Structural effects on rates and equilibriums. XV. Hydrogen-bonded intermediates and stepwise mechanisms for proton-exchange reactions between oxygen atoms in hydroxylic solvents Hine, Jack Journal of the American Chemical Society, Vol. 94, Issue 16 https://doi.org/10.1021/ja00771a038	journal	August 1972
A View at the Millennium: the Efficiency of Enzymatic Catalysis Bruice, Thomas C. Accounts of Chemical Research, Vol. 35, Issue 3 https://doi.org/10.1021/ar0001665	journal	March 2002
Concluding remarks Perutz, Max Ferdinand Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 167, Issue 1009, p. 448-448 https://doi.org/10.1098/rspb.1967.0046	journal	April 1967
Identification of active site residues by site-directed mutagenesis of delta 5-3-ketosteroid isomerase from Pseudomonas putida biotype B. Kim, S. W.; Choi, K. Y. Journal of bacteriology, Vol. 177, Issue 9 https://doi.org/10.1128/JB.177.9.2602-2605.1995	journal	January 1995
Selective chemical catalysis by an antibody Pollack, S.; Jacobs, J.; Schultz, P. Science, Vol. 234, Issue 4783 https://doi.org/10.1126/science.3787262	journal	December 1986
Strong hydrogen bonding in gas-phase anions. An ion cyclotron resonance determination of fluoride binding energetics to Broensted acids from gas-phase fluoride exchange equilibrium measurements Larson, J. W.; McMahon, T. B. Journal of the American Chemical Society, Vol. 105, Issue 10 https://doi.org/10.1021/ja00348a003	journal	May 1983
Catalytic antibodies Tramontano, A.; Janda, K.; Lerner, R. Science, Vol. 234, Issue 4783 https://doi.org/10.1126/science.3787261	journal	December 1986
Structure of Hen Egg-White Lysozyme: A Three-dimensional Fourier Synthesis at 2 Å Resolution Blake, C. C. F.; Koenig, D. F.; Mair, G. A. Nature, Vol. 206, Issue 4986 https://doi.org/10.1038/206757a0	journal	May 1965
The change in hydrogen bond strength accompanying charge rearrangement: Implications for enzymatic catalysis Shan, S. -o.; Herschlag, D. Proceedings of the National Academy of Sciences, Vol. 93, Issue 25 https://doi.org/10.1073/pnas.93.25.14474	journal	December 1996
Nature of the intermediate in the 3-oxo-.DELTA.5-steroid isomerase reaction Zeng, Baifei; Bounds, Patricia L.; Steiner, Robert F. Biochemistry, Vol. 31, Issue 5 https://doi.org/10.1021/bi00120a032	journal	February 1992
Recent Insights into Inhibition, Structure, and Mechanism of Configuration-Retaining Glycosidases Heightman, Tom D.; Vasella, Andrea T. Angewandte Chemie International Edition, Vol. 38, Issue 6 https://doi.org/10.1002/(sici)1521-3773(19990315)38:6<750::aid-anie750>3.0.co;2-6	journal	March 1999
ChemInform Abstract: CORRELATIONS BETWEEN PROTON CHEMICAL SHIFT TENSORS, DEUTERIUM QUADRUPOLE COUPLINGS, AND BOND DISTANCES FOR HYDROGEN BONDS IN SOLIDS Berglund, B.; Vaughan, R. W. Chemischer Informationsdienst, Vol. 11, Issue 52 https://doi.org/10.1002/chin.198052050	journal	December 1980
Why Enzymes Are Proficient Catalysts: Beyond the Pauling Paradigm Zhang, Xiyun; Houk, K. N. ChemInform, Vol. 36, Issue 29 https://doi.org/10.1002/chin.200529293	journal	July 2005
On the inhibition of β-N-acetyl-D-glucosaminidase by 2-acetamido-2-deoxy-D-glucono-(1→5)-lactone Leaback, D. H. Biochemical and Biophysical Research Communications, Vol. 32, Issue 6 https://doi.org/10.1016/0006-291x(68)90132-0	journal	September 1968
Specific activation of a tyrosine → glycine mutant of Δ5-3-ketosteroid isomerase by phenols Brooks, Bob; Benisek, William F. Biochemical and Biophysical Research Communications, Vol. 184, Issue 3 https://doi.org/10.1016/s0006-291x(05)80036-1	journal	May 1992
Nojirimycin and d-glucono-1,5-lactone as inhibitors of carbohydrases Reese, E. T.; Parrish, F. W.; Ettlinger, M. Carbohydrate Research, Vol. 18, Issue 3 https://doi.org/10.1016/s0008-6215(00)80274-8	journal	July 1971
An Orientation-dependent Hydrogen Bonding Potential Improves Prediction of Specificity and Structure for Proteins and Protein–Protein Complexes Kortemme, Tanja; Morozov, Alexandre V.; Baker, David Journal of Molecular Biology, Vol. 326, Issue 4 https://doi.org/10.1016/s0022-2836(03)00021-4	journal	February 2003
Thermodynamic and extrathermodynamic requirements of enzyme catalysis Wolfenden, Richard Biophysical Chemistry, Vol. 105, Issue 2-3 https://doi.org/10.1016/s0301-4622(03)00066-8	journal	September 2003
Structure and enzymology of Î5-3-ketosteroid isomerase Ha, N. Current Opinion in Structural Biology, Vol. 11, Issue 6 https://doi.org/10.1016/s0959-440x(01)00268-8	journal	December 2001
Protein engineering Leatherbarrow, Robin J.; Fersht, Alan R. "Protein Engineering, Design and Selection", Vol. 1, Issue 1 https://doi.org/10.1093/protein/1.1.7	journal	January 1986
Pushing the boundaries of molecular replacement with maximum likelihood Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 10 https://doi.org/10.1107/s0907444901012471	journal	September 2001
On low-barrier hydrogen bonds and enzyme catalysis Warshel, A.; Papazyan, A.; Kollman, P. Science, Vol. 269, Issue 5220 https://doi.org/10.1126/science.7661987	journal	July 1995
Cloning, nucleotide sequence, and overexpression of the gene coding for delta 5-3-ketosteroid isomerase from Pseudomonas putida biotype B. Kim, S. W.; Kim, C. Y.; Benisek, W. F. Journal of Bacteriology, Vol. 176, Issue 21 https://doi.org/10.1128/jb.176.21.6672-6676.1994	journal	January 1994

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