A pre-steady state kinetic analysis of the αy60W mutant of trans-3-chloroacrylic acid dehalogenase: Implications for the mechanism of the wild-type enzyme

Biochemistry

Volumn 51, Issue 46, 2012, Pages 9420-9435

  Huddleston, Jamison P ^a   Schroeder, Gottfried K ^a   Johnson, Kenneth A ^a   Whitman, Christian P ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ,3-DICHLOROPROPENE; ACTIVE SITE; BACTERIAL DEGRADATION; CATALYTIC MECHANISMS; CATALYTIC RESIDUE; CONFORMATIONAL CHANGE; DEHALOGENASE; ENZYME-CATALYZED REACTIONS; ISOMERIC MIXTURES; KINETIC ANALYSIS; KINETIC MECHANISM; KINETIC MODELS; MALONATES; PRE-STEADY STATE; PRODUCT RELEASE; STOPPED FLOW; SUBSTRATE BINDING; TAUTOMERASE; WILD-TYPE ENZYMES;

BROMINE COMPOUNDS; CATALYSIS; CONFORMATIONS; DEGRADATION; ENZYMES; RATE CONSTANTS;

KINETICS;

ACRYLIC ACID; BROMIDE; CIS 3 CHLOROACRYLIC ACID DEHALOGENASE; FLUORESCENT DYE; MALONATE SEMIALDEHYDE DEHYDROGENASE (ACETYLATING); TRANS 3 CHLOROACRYLIC ACID DEHALOGENASE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; DEHALOGENATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SUBSTRATE; KINETICS; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; STEADY STATE; WILD TYPE;

BASE SEQUENCE; CATALYTIC DOMAIN; DNA PRIMERS; HYDROLASES; KINETICS; MUTATION; POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS);

EID: 84869439957     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3010686     Document Type: Article

References (41)

1. Hartmans, S., Jansen, M. W., Van der Werf, M. J., and De Bont, J. A. M. (1991) Bacterial metabolism of 3-chloroacrylic acid J. Gen. Microbiol. 137, 2025-2032
2. van Hylckama Vlieg, J. E. and Janssen, D. B. (1991) Bacterial degradation of 3-chloroacrylic acid and the characterization of cis-and trans-specific dehalogenases Biodegradation 2, 139-150
3. 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 (Pubitemid 28363164)
4. 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 (Pubitemid 32568079)
5. 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 (Pubitemid 36899820)
6. 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 (Pubitemid 38114064)
7. 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 (Pubitemid 41079507)
8. Murzin, A. G. (1996) Structural classification of proteins: New superfamilies Curr. Opin. Struct. Biol. 6, 386-394 (Pubitemid 26197440)
9. Poelarends, G. J., Veetil, V. P., and Whitman, C. P. (2008) The chemical versatility of the β-α-β fold: Catalytic promiscuity and divergent evolution in the tautomerase superfamily Cell. Mol. Life Sci. 65, 3606-3618
10. 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 (Pubitemid 38401655)
11. 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 (Pubitemid 38445627)
12. De Jong, R. M., Bazzacco, P., Poelarends, G. J., Johnson, W. H., Jr., Kim, Y. J., Burks, E. A., Serrano, H., Thunnissen, A.-M. W. H., Whitman, C. P., and Dijkstra, B. W. (2007) Crystal structures of native and inactivated cis-3-chloroacrylic acid dehalogenase. Structural basis for substrate specificity and inactivation by (R)-oxirane-2-carboxylate J. Biol. Chem. 282, 2440-2449 (Pubitemid 47076762)
13. Robertson, B. A., Schroeder, G. K., Jin, Z., Johnson, K. A., and Whitman, C. P. (2009) Pre-steady state kinetic analysis of cis-3-chloroacrylic acid dehalogenase: Analysis and implications Biochemistry 48, 11737-11744
14. Schroeder, G. K., Johnson, W. H., Jr., Huddleston, J. P., Serrano, H., Johnson, K. A., and Whitman, C. P. (2012) Reaction of cis-3-chloroacrylic acid dehalogenase with an allene substrate, 2,3-butadienoate: Hydration via an enamine J. Am. Chem. Soc. 134, 293-304
15. Poelarends, G. J., Johnson, W. H., Jr., Serrano, H., and Whitman, C. P. (2007) Phenylpyruvate tautomerase activity of trans-3-chloroacrylic acid dehalogenase: Evidence for an enol intermediate in the dehalogenase reaction Biochemistry 46, 9596-9604 (Pubitemid 47291966)
16. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular cloning: A laboratory manual, 2nd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
17. Waddell, W. J. (1956) A simple ultraviolet spectrophotometric method for the determination of protein J. Lab. Clin. Med. 48, 311-314
18. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680-685
19. Trott, O. and Olson, A. J. (2010) AutoDock vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31, 455-461
20. DeLano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.
21. Dixon, M. (1953) Determination of enzyme-inhibitor constants Biochem. J. 55, 170-171
22. Cornish-Bowden, A. (1974) Simple graphical method for determining the inhibition constants of mixed, uncompetitive, and noncompetitive inhibitors Biochem. J. 137, 143-144
23. Johnson, K. A. (1992) Transient-state kinetic analysis of enzyme reaction pathways. In The Enzymes (Sigman, D. S., Ed.) 3rd ed., pp 1-61, Academic Press, San Diego.
24. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global kinetic explorer: A new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
25. Burks, E. A., Fleming, C. D., Mesecar, A. D., Whitman, C. P., and Pegan, S. D. (2010) Kinetic and structural characterization of a heterohexamer 4-oxalocrotonate tautomerase from Chloroflexus aurantiacus J-10-fl: Implications for functional and structural diversity in the tautomerase superfamily Biochemistry 49, 5016-5027
26. Burks, E. A., Yan, W., Johnson, W. H., Jr., Li, W., Schroeder, G. K., Min, C., Gerratana, B., Zhang, Y., and Whitman, C. P. (2011) Kinetic, crystallographic, and mechanistic characterization of TomN: Elucidation of a function for a 4-oxalocrotonate tautomerase homologues in the tomaymycin biosynthetic pathway Biochemistry 50, 7600-7611
27. Robertson, B. A. (2007) Evolution and divergence in the tautomerase superfamily: A pre-steady state kinetic analysis of cis-3-chloroacrylic acid dehalogenase and an inhibition study of its homologue, Cg10062, in Corynebacterium glutamicum. Ph.D. Dissertation, The University of Texas at Austin, Austin, TX.
28. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) FitSpace explorer: An algorithm to evaluate multidimensional parameter space in fitting kinetic data Anal. Biochem. 387, 30-41
29. Copley, S. D. (1999) Microbial dehalogenases. In Comprehensive Natural Products Chemistry (Barton, D. and Nakanishi, K., Eds.) pp 401-422, Elsevier, Amsterdam.
30. Janssen, D. B. (2004) Evolving haloalkane dehalogenases Curr. Opin. Chem. Biol. 8, 150-159 (Pubitemid 38452429)
31. Verschueren, K. H. G., Kingma, J., Rozeboom, H. J., Kalk, K. H., Janssen, D. B., and Dijkstra, B. W. (1993) Crystallographic and fluorescence studies of the interaction of haloalkane dehalogenase with halide ions. Studies with halide compounds reveal a halide binding site in the active site Biochemistry 32, 9031-9037 (Pubitemid 24186224)
32. Schanstra, J. P., Kingma, J., and Janssen, D. B. (1996) Specificity and kinetics of haloalkane dehalogenase J. Biol. Chem. 271, 14747-14753 (Pubitemid 26194953)
33. Schanstra, J. P. and Janssen, D. B. (1996) Kinetics of halide release of haloalkane dehalogenase: Evidence for a slow conformational change Biochemistry 35, 5624-5632 (Pubitemid 26143657)
34. Benning, M. M., Taylor, K. L., Liu, R.-Q., Yang, G., Xiang, H., Wesenberg, G., Dunaway-Mariano, D., and Holden, H. M. (1996) Structure of 4-chlorobenzoyl coenzyme A dehalogenase determined to 1.8 Å resolution: An enzyme catalyst generated via adaptive mutation Biochemistry 35, 8103-8109 (Pubitemid 26234908)
35. Zhang, W., Wei, Y., Luo, L., Taylor, K. L., Yang, G., Dunaway-Mariano, D., Benning, M. M., and Holden, H. M. (2001) Histidine 90 function in 4-chlorobenzoyl-coenzyme A dehalogenase catalysis Biochemistry 40, 13474-13482 (Pubitemid 33130775)
36. Liu, R.-Q., Liang, P.-H., Scholten, J., and Dunaway-Mariano, D. (1995) Transient state kinetic analysis of the chemical intermediates formed in the enzymic dehalogenation of 4-chlorobenzoyl coenzyme A J. Am. Chem. Soc. 117, 5003-5004
37. Xu, D., Wei, Y., Wu, J., Dunaway-Mariano, D., Guo, H., Cui, Q., and Gao, J. (2004) QM/MM studies of the enzyme-catalyzed dechlorination of 4-chlorobenzoyl-CoA provide insight into reaction energetics J. Am. Chem. Soc. 126, 13649-13658 (Pubitemid 39407244)
38. Wu, J., Xu, D., Lu, X., Wang, C., Guo, H., and Dunaway-Mariano, D. (2006) Contributions of long-range electrostatic interactions to 4-chlorobenzoyl-CoA dehalogenase catalysis: A combined theoretical and experimental study Biochemistry 45, 102-112 (Pubitemid 43054087)
39. Segel, I. H. (1993) Enzyme kinetics: Behavior and analysis of rapid equilibrium and steady state enzyme systems, Wiley, New York.
40. 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 (Pubitemid 41688891)
41. Johnson, K. A. (2008) Role of induced-fit in enzyme specificity: A molecular forward/reverse switch J. Biol. Chem. 283, 26297-26301