Evolution of enzymatic activity in the tautomerase superfamily: Mechanistic and structural consequences of the L8R mutation in 4-oxalocrotonate tautomerase

Biochemistry

Volumn 45, Issue 25, 2006, Pages 7700-7708

  Poelarends, Gerrit J ^a,b   Almrud, Jeffrey J ^a   Serrano, Hector ^a   Darty, Joseph E ^a   Johnson Jr , William H ^a   Hackert, Marvin L ^a   Whitman, Christian P ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBONS; CATALYSIS; CRYSTAL STRUCTURE; DEHALOGENATION; PROTEINS; STABILIZATION;

ACTIVE-SITE MUTATIONS; CAAD ACTIVITY; DICHLOROPROPENE DEGRADATION; MUTANTS;

ENZYMES;

2 HYDROXYMUCONATE; 2 OXO 3 HEXENEDIOATE; 2 OXO 4 HEXENEDIOATE; 3 CHLOROACRYLIC ACID DEHALOGENASE; 4 OXALOCROTONATE TAUTOMERASE; ARGININE; AROMATIC HYDROCARBON; ISOLEUCINE; LEUCINE; PROLINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DEHALOGENATION; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN FOLDING; PSEUDOMONAS PUTIDA; REACTION ANALYSIS;

BINDING SITES; CRYSTALLIZATION; EVOLUTION, MOLECULAR; HYDROLASES; ISOMERASES; KINETICS; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PSEUDOMONAS PUTIDA; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

PSEUDOMONAS PAVONACEAE; PSEUDOMONAS PUTIDA;

EID: 33746914768     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0600603     Document Type: Article

References (50)

1. Palmer, D. R. J., Garrett, J. B., Sharma, V., Meganathan, R., Babbitt, P. C., and Gerlt, J. A. (1999) Unexpected divergence of enzyme function and sequence: "N-Acylamino acid racemase" is o-succinylbenzoate synthase, Biochemistry 38, 4252-4258.
2. James, L. C., and Tawfik, D. S. (2001) Catalytic and binding polyreactivities shared by two unrelated proteins: The potential role of promiscuity in enzyme evolution, Protein Sci. 10, 2600-2607.
3. O'Brien, P. J., and Herschlag, D. (2001) Functional interrelationships in the alkaline phosphatase superfamily: Phosphodiesterase activity of Escherichia coli alkaline phosphatase, Biochemistry 40, 5691-5699.
4. Wang, S. C., Johnson, W. H., Jr., and Whitman, C. P. (2003) The 4-oxalocrotonate tautomerase- and YwhB-catalyzed hydration of 3E-haloacrylates: Implications for evolution of new enzymatic activities, J. Am. Chem. Soc. 125, 14282-14283.
5. Poelarends, G. J., Serrano, H., Johnson, W. H., Jr., Hoffman, D. W., and Whitman, C. P. (2004) The hydratase activity of malonate semialdehyde decarboxylase: Mechanistic and evolutionary implications, J. Am. Chem. Soc. 126, 15658-15659.
6. Yew, W. S., Akana, J., Wise, E. L., Rayment, I., and Gerlt, J. A. (2005) Evolution of enzymatic activities in the orotidine 5′-monophosphate decarboxylase suprafamily: Enhancing the promiscuous D-arabino-hex-3-ulose 6-phosphate synthase reaction catalyzed by 3-keto-L-gulonate 6-phosphate decarboxylase, Biochemistry 44, 1807-1815.
7. Roodveldt, C., and Tawfik, D. S. (2005) Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily, Biochemistry 44, 12728-12736.
8. Jensen, R. A. (1976) Enzyme recruitment in evolution of new function, Ann. Rev. Microbiol. 30, 409-425.
9. Hughes, A. L. (1994) The evolution of functionally novel proteins after gene duplication, Proc. R. Soc. London, Ser. B 256, 119-124.
10. O'Brien, P. J., and Herschlag, D. (1999) Catalytic promiscuity and the evolution of new enzymatic activities, Chem. Biol. 6, R91-R105.
11. 8-barrels: Functional promiscuity produced by single substitutions in the enolase superfamily, Biochemistry 42, 8387-8393.
12. Aharoni, A., Gaidukov, L., Khersonsky, O., McQ Gould, S., Roodveldt, C., and Tawfik, D. S. (2005) The "evolvability" of promiscuous protein functions, Nat. Genet. 37, 73-76.
13. Whitman, C. P. (2002) The 4-oxalocrotonate tautomerase family of enzymes: How nature makes new enzymes using a β-α-β structural motif, Arch. Biochem. Biophys. 402, 1-13.
14. Poelarends, G. J., and Whitman, C. P. (2004) Evolution of enzymatic activity in the tautomerase superfamily: Mechanistic and structural studies of the 1,3-dichloropropene catabolic enzymes, Bioorg. Chem. 32, 376-392.
15. Almrud, J. J., Kern, A. D., Wang, S. C., Czerwinski, R. M., Johnson, W. H., Jr., Murzin, A. G., Hackert, M. L., and Whitman, C. P. (2002) The crystal structure of YdcE, a 4-oxalocrotonate tautomerase homologue from Escherichia coli, confirms the structural basis for oligomer diversity, Biochemistry 41, 12010-12024.
16. Poelarends, G. J., Serrano, H., Person, M. D., Johnson, W. H., Jr., Murzin, A. G., and Whitman, C. P. (2004) Cloning, expression, and characterization of a cis-3-chloroacrylic acid dehalogenase: Insights into the mechanistic, structural, and evolutionary relationship between isomer-specific 3-chloroacrylic acid dehalogenases, Biochemistry 43, 759-772.
17. Harayama, S., Rekik, M., Ngai, K.-L., and Ornston, L. N. (1989) Physically associated enzymes produce and metabolize 2-hydroxy-2,4-dienoate, a chemically unstable intermediate formed in catechol metabolism via meta cleavage in Pseudomonas putida, J. Bacteriol. 171, 6251-6258.
18. Chen L. H., Kenyon G. L., Curtin F., Harayama S., Bembenek M. E., Hajipour G., and Whitman C. P. (1992) 4-Oxalocrotonate tautomerase, an enzyme composed of 62 amino acid residues per monomer, J. Biol. Chem. 267, 17716-17721.
19. Whitman, C. P., Aird, B. A., Gillespie, W. R., and Stolowich, N. J. (1991) Chemical and enzymatic ketonization of 2-hydroxymuconate, a conjugated enol, J. Am. Chem. Soc. 113, 3154-3162.
20. Poelarends, G. J., Wilkens, M., Larkin, M. J., van Elsas, J. D., and Janssen, D. B. (1998) Degradation of 1,3-dichloropropene by Pseudomonas cichorii 170, Appl. Environ. Microbiol. 64, 2931-2936.
21. Poelarends, G. J., Saunier, R., and Janssen, D. B. (2001) trans-3-Chloroacrylic acid dehalogenase from Pseudomonas pavonaceae 170 shares structural and mechanistic similarities with 4-oxalocrotonate tautomerase, J. Bacteriol. 183, 4269-4277.
22. Wang, S. C., Person, M. D., Johnson, W. H., Jr., and Whitman, C. P. (2003) Reactions of trans-3-chloroacrylic acid dehalogenase with acetylene substrates: Consequences of and evidence for a hydration reaction, Biochemistry 42, 8762-8773.
23. Subramanya, H. S., Roper, D. I., Dauter, Z., Dodson, E. J., Davies, G. J., Wilson, K. S., and Wigley, D. B. (1996) Enzymatic ketonization of 2-hydroxymuconate: Specificity and mechanism investigated by the crystal structures of two isomerases, Biochemistry 35, 792-802.
24. Taylor, A. B., Czerwinski, R. M., Johnson, W. H., Jr., Whitman, C. P., and Hackert M. L. (1998) Crystal structure of 4-oxalocrotonate tautomerase inactivated by 2-oxo-3-pentynoate at 2.4 Å resolution: Analysis and implications for the mechanism of inactivation and catalysis, Biochemistry 37, 14692-14700.
25. de Jong, R. M., Brugman, W., Poelarends, G. J., Whitman, C. P., and Dijkstra, B. W. (2004) The X-ray structure of trans-3-chloroacrylic acid dehalogenase reveals a novel hydration mechanism in the tautomerase superfamily, J. Biol. Chem. 279, 11546-11552.
26. Stivers, J. T., Abeygunawardana, C., Mildvan, A. S., Hajipour, G., Whitman, C. P., and Chen, L. H. (1996) Catalytic role of the amino-terminal proline in 4-oxalocrotonate tautomerase: Affinity labeling and heteronuclear NMR studies, Biochemistry 35, 803-813.
27. a values of active site residues, Biochemistry 35, 814-823.
28. Azurmendi, H. F., Wang, S. C., Massiah, M. A., Poelarends, G. J., Whitman, C. P., and Mildvan, A. S. (2004) The roles of active-site residues in the catalytic mechanism of trans-3-chloroacrylic acid dehalogenase: A kinetic, NMR, and mutational analysis, Biochemistry 43, 4082-4091.
29. Keuning, S., Janssen, D. B., and Whitholt, B. (1985) Purification and characterization of hydrolytic haloalkane dehalogenase from Xanthobacter autotrophicus GJ10, J. Bacteriol. 163, 635-639.
30. Weber, D. J., Abeygunawardana, C., Bessman, M. J., and Mildvan, A. S. (1993) Secondary structure of the MutT enzyme as determined by NMR, Biochemistry 32, 13081-13088.
31. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
32. Matthews, B. W. (1968) Solvent content of protein crystals, J. Mol. Biol. 33, 491-497.
33. Vagin, A., and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement, J. Appl. Crystallogr. 30, 1022-1025.
34. Collaborative Computational Project, Number 4. (1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
35. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255.
36. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
37. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
38. Kraulis, P. J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
39. Merritt, E. A., and Murphy, M. E. (1994) Raster3D version 2.0. A program for photorealistic molecular graphics, Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 869-873.
40. a of the catalytic base in 4-oxalocrotonate tautomerase: Kinetic and structural effects of mutations of Phe-50, Biochemistry 40, 1984-1995.
41. Harris, T. K., Czerwinski, R. M., Johnson, W. H., Jr., Legler, P. M., Abeygunawardana, C., Massiah, M. A., Stivers, J. T., Whitman, C. P., and Mildvan, A. S. (1999) Kinetic, stereochemical, and structural effects of mutations of the active site arginine residues in 4-oxalocrotonate tautomerase, Biochemistry 38, 12343-12357.
42. Murzin, A. G. (1996) Structural classification of proteins: New superfamilies, Curr. Opin. Struct. Biol. 6, 386-394.
43. Poelarends, G. J., Johnson, W. H., Jr., Murzin, A. G., and Whitman, C. P. (2003) Mechanistic characterization of a bacterial malonate semialdehyde decarboxylase: Identification of a new activity in the tautomerase superfamily, J. Biol. Chem. 278, 48674-48683.
44. Rosengren, E., Aman, P., Thelin, S., Hansson, C., Ahlfors, S., Bjork, P., Jacobsson, L., and Rorsman, H. (1997) The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase, FEBS Lett. 417, 85-88.
45. Sparnins, V. L., Chapman, P. J., and Dagley, S. (1974) Bacterial degradation of 4-hydroxyphenylacetic acid and homoprotocatechuic acid, J. Bacteriol. 120, 159-167.
46. Almrud, J. J., Poelarends, G. J., Johnson, W. H., Jr., Serrano, H., Hackert, M. L., and Whitman, C. P. (2005) Crystal structures of the wild-type, P1A mutant, and inactivated malonate semialdehyde decarboxylase: A structural basis for the decarboxylase and hydratase activities, Biochemistry 44, 14818-14827.
47. Suzuki, M., Sugimoto, H., Nakagawa, A., Tanaka, I., Nishihira, J., and Sakai, M. (1996) Crystal structure of the macrophage migration inhibitory factor from rat liver, Nat. Struct. Biol. 3, 259-266.
48. Horvat, C. M., and Wolfenden, R. V. (2005) A persistent pesticide residue and the unusual catalytic proficiency of a dehalogenating enzyme, Proc. Natl. Acad. Sci. U.S.A. 102, 16199-16202.
49. 8-barrels: In vitro enhancement of a "new" reaction in the enolase superfamily, Biochemistry 44, 11722-11729.
50. Gould, S. M., and Tawfik D. S. (2005) Directed evolution of the promiscuous esterase activity of carbonic anhydrase II, Biochemistry 44, 5444-5452.