Dissecting the paradoxical effects of hydrogen bond mutations in the ketosteroid isomerase oxyanion hole

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 5, 2010, Pages 1960-1965

  Kraut, Daniel A ^a   Sigala, Paul A ^a   Fenn, Timothy D ^a   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Active site environment; Enzymatic catalysis; Protein cavities; Site directed mutagenesis

Indexed keywords

ALANINE; EQUILENIN; FLUORINE; GLYCINE; HYDROXYL GROUP; OXYGEN; SERINE; STEROID DELTA ISOMERASE; THREONINE; TYROSINE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; GENE MUTATION; HYDROGEN BOND; MOLECULAR INTERACTION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SOLVATION; SPECTROSCOPY; X RAY;

AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; COMAMONAS TESTOSTERONI; CRYSTALLOGRAPHY, X-RAY; EQUILENIN; HYDROGEN BONDING; KETOSTEROIDS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PSEUDOMONAS PUTIDA; RECOMBINANT PROTEINS; STATIC ELECTRICITY; STEROID ISOMERASES;

BACTERIA (MICROORGANISMS);

EID: 76649126435     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911168107     Document Type: Article

References (38)

1. Fersht AR (1999) Structure and Mechanism in Protein Science (W.H. Freeman and Company, New York).
2. Radzicka A, Wolfenden R (1995) A proficient enzyme. Science, 267:90-93.
3. Jiang L, et al. (2008) De novo computational design of retro-aldol enzymes. Science, 319:1387-1391.
4. Kaplan J, DeGrado WF (2004) De novo design of catalytic proteins. Proc Natl Acad Sci USA, 101:11566-11570.
5. Gerlt JA, Babbitt PC (2009) Enzyme (re)design: Lessons from natural evolution and computation. Curr Opin Chem Biol, 13:10-18.
6. Lad C, Williams NH, Wolfenden R (2003) The rate of hydrolysis of phosphomonoester dianions and the exceptional catalytic proficiencies of protein and inositol phosphatases. Proc Natl Acad Sci USA, 100:5607-5610.
7. Kuliopulos A, Mildvan AS, Shortle D, Talalay P (1989) Kinetic and ultraviolet spectroscopic studies of active-site mutants of delta 5-3-ketosteroid isomerase. Biochemistry, 28:149-159.
8. Kim DH, et al. (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.
9. Cleland WW, Frey PA, Gerlt JA (1998) The low barrier hydrogen bond in enzymatic catalysis. J Biol Chem, 273:25529-25532.
10. Kim SW, et al. (1997) High-resolution crystal structures of delta 5-3-ketosteroid isomerase with and without a reaction intermediate analogue. Biochemistry, 36:14030-14036.
11. Zhao Q, Abeygunawardana C, Talalay P, Mildvan AS (1996) NMR evidence for the participation of a low-barrier hydrogen bond in the mechanism of delta 5-3-ketosteroid isomerase. Proc Natl Acad Sci USA, 93:8220-8224.
12. Feierberg I, Aqvist J (2002) The catalytic power of ketosteroid isomerase investigated by computer simulation. Biochemistry, 41:15728-15735.
13. Nam GH, et al. (2001) Maintenance of alpha-helical structures by phenyl rings in the active-site tyrosine triad contributes to catalysis and stability of ketosteroid isomerase from Pseudomonas putida biotype b. Biochemistry, 40:13529-13537.
14. Hawkinson DC, Eames TC, Pollack RM (1991) Energetics of 3-oxo-delta 5-steroid isomerase: Source of the catalytic power of the enzyme. Biochemistry, 30:10849-10858.
15. Pollack RM, Bantia S, Bounds PL, Koffman BM (1986) pH dependence of the kinetic parameters for 3-oxo-delta 5-steroid isomerase. Substrate catalysis and inhibition by (3s)-spiro[5 alpha- androstane-3,2′-oxiran]-17-one. Biochemistry, 25:1905-1911.
16. Schwans JP, Kraut DA, Herschlag DA (2009) Determining the catalytic role of remote substrate binding interactions in ketosteroid isomerase. Proc Natl Acad Sci USA, 106:14271-14275.
17. Tsai J, Taylor R, Chothia C, GersteinM(1999) The packing density in proteins: Standard radii and volumes. J Mol Biol, 290:253-266.
18. Williams MA, Goodfellow JM, Thornton JM (1994) Buried waters and internal cavities in monomeric proteins. Protein Sci, 3:1224-1235.
19. Hubbard SJ, Gross KH, Argos P (1994) Intramolecular cavities in globular proteins. Protein Eng, 7:613-626.
20. Liu L, Quillin ML, Matthews BW (2008) Use of experimental crystallographic phases to examine the hydration of polar and nonpolar cavities in T4 lysozyme. Proc Natl Acad Sci USA, 105:14406-14411.
21. Choi G, et al. (2001) Pseudoreversion of the catalytic activity of Y14F by the additional substitution(s) of tyrosine with phenylalanine in the hydrogen bond network of delta 5-3-ketosteroid isomerase from Pseudomonas putida biotype b. Biochemistry, 40:6828-6835.
22. Oh KS, et al. (2000) Role of catalytic residues in enzymatic mechanisms of homologous ketosteroid isomerases. Biochemistry, 39:13891-13896.
23. Gerig JT (1989) Fluorine nuclear magnetic resonance of fluorinated ligands. Methods Enzymol, 177:3-23.
24. Petrounia IP, Pollack RM (1998) Substituent effects on the binding of phenols to the D38N mutant of 3-oxo-delta5-steroid isomerase. A probe for the nature of hydrogen bonding to the intermediate. Biochemistry, 37:700-705.
25. Kraut DA, et al. (2006) Testing electrostatic complementarity in enzyme catalysis: Hydrogen bonding in the ketosteroid isomerase oxyanion hole. PLoS Biol, 4:501-519.
26. Sigala PA, et al. (2008) Testing geometrical discriminationwithin an enzyme active site: Constrained hydrogen bonding in the ketosteroid isomerase oxyanion hole. J Am Chem Soc, 130:13696-13708.
27. DerHovanessian A, Rablen PR, Jain A (2000) Ab initio and density functional calculations of 19F NMR chemical shifts for models of carbonic anhydrase inhibitors. J Phys Chem A, 104:6056-6061.
28. Kraut DA, Carroll KS, Herschlag D (2003) Challenges in enzyme mechanism and energetics. Annu Rev Biochem, 72:517-571.
29. Knowles JR (1987) Tinkering with enzymes: What are we learning?. Science, 236:1252-1258.
30. Fersht AR (1988) Relationships between apparent binding energies measured in site-directed mutagenesis experiments and energetics of binding and catalysis. Biochemistry, 27:1577-1580.
31. Plapp BV (1995) Site-directed mutagenesis: A tool for studying enzyme catalysis. Method Enzymol, 249:91-119.
32. Harpham MR, Levinger NE, Ladanyi BM (2008) An investigation of water dynamics in binary mixtures of water and dimethyl sulfoxide. J Phys Chem B, 112:283-293.
33. Perera PN, et al. (2009) Observation of water dangling OH bonds around dissolved nonpolar groups. Proc Natl Acad Sci USA, 106:12230-12234.
34. Laage D, Stirnemann G, Hynes JT (2009) Why water reorientation slows without iceberg formation around hydrophobic solutes. J Phys Chem B, 113:2428-2435.
35. Timmer RL, Bakker HJ (2009) Hydrogen bond fluctuations of the hydration shell of the bromide anion. J Phys Chem A, 113:6104-6110.
36. DeLano WL (2007) MacPyMOL: A PyMOL-based molecular graphics application for MacOS X (DeLano Scientific LLC, Palo Alto, CA).
37. Zhao Q, Abeygunawardana C, Gittis AG, Mildvan AS (1997) Hydrogen bonding at the active site of delta 5-3-ketosteroid isomerase. Biochemistry, 36:14616-14626.
38. Kraut DA, Churchill MJ, Dawson PE, Herschlag D (2009) Evaluating the potential for halogen bonding in the oxyanion hole of ketosteroid isomerase using unnatural amino acid mutagenesis. ACS Chem Biol, 4:269-273.