The chemical versatility of the β-α-β fold: Catalytic promiscuity and divergent evolution in the tautomerase superfamily

Cellular and Molecular Life Sciences

Volumn 65, Issue 22, 2008, Pages 3606-3618

  Poelarends, G J ^a   Veetil, V Puthan ^a   Whitman, C P ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Catalytic promiscuity; Divergent evolution; Tautomerase superfamily

Indexed keywords

3 CHLOROACRYLIC ACID DEHALOGENASE; 4 OXALOCROTONATE TAUTOMERASE; 5 (CARBOXYMETHYL) 2 HYDROXYMUCONATE ISOMERASE; HYDROLYASE; ISOMERASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MALONATE SEMIALDEHYDE DECARBOXYLASE; PHENYLPYRUVATE TAUTOMERASE; PROLINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CATALYSIS; CORYNEBACTERIUM GLUTAMICUM; CRYSTAL STRUCTURE; DECARBOXYLATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; EVOLUTION; GENE EXPRESSION; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN MOTIF; REVIEW;

CARBON-CARBON DOUBLE BOND ISOMERASES; CARBOXY-LYASES; CATALYSIS; EVOLUTION, MOLECULAR; HYDROLASES; ISOMERASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY;

EID: 56549088539     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8285-x     Document Type: Review

References (57)

1. Murzin A. G. (1996) Structural classification of proteins: new superfamilies. Curr. Opin. Struct. Biol. 6, 386-394.
2. 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.
3. 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.
4. Jenkins J. R. and Cooper R. A. (1988) Molecular cloning, expression, and analysis of the genes of the homoprotocatechuate catabolic pathway of Escherichia coli C. J. Bacteriol. 170, 5317-5324.
5. Whitman, C. P. (1999) Keto-enol tautomerisation in enzymatic reactions. In: Comprehensive Natural Products Chemistry, Barton, D. & Nakanishi, K. (eds.), vol. 5, pp. 31-50, Poulter, C.D. (ed.), Elsevier, Oxford.
6. 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.
7. Sun H.-W., Bernhagen J., Bucala R. and Lolis E. (1996) Crystal structure at 2.6 Å resolution of human macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. 93, 5191-5196.
8. 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.
9. Lubetsky J. B., Swope M., Dealwis C., Blake P. and Lolis E. (1999) Pro-1 of macrophage migration inhibitory factor functions as a catalytic base in the phenylpyruvate tautomerase activity. Biochemistry 38, 7346-7354.
10. Poelarends G. J., Serrano H., Person M. D., Johnson Jr. W. H., 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.
11. Poelarends G. J., Johnson Jr. W.H., 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.
12. Almrud J. J., Kern A. D., Wang S. C., Czerwinski R.M., Johnson Jr. W. H., 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.
13. Harayama S., Lehrbach P. R. and Timmis K. N. (1984) Transposon mutagenesis analysis of meta-cleavage operon genes of the TOL plasmid of Pseudomonas putida mt-2. J. Bacteriol. 160, 251-255.
14. 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.
15. 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. Microb. 137, 2025-2032.
16. Van Hylckama Vlieg J. E. T. and Janssen D. B. (1992) Bacterial degradation of 3-chloroacrylic acid and the characterization of cis- and trans-specific dehalogenases. Biodegradation 2, 139-150.
17. 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.
18. Whitman C. P., Aird B. A., Gillespie W. R. and Stolowich, N. J. (1991) Chemical and enzymatic ketonization of 2-hydroxy-muconate, a conjugated enol. J. Am. Chem. Soc. 113, 3154-3162.
19. Whitman C. P., Hajipour G., Watson R. J., Johnson Jr. W. H., Bembenek M. E. and Stolowich N. J. (1992) Stereospecific ketonization of 2-hydroxymuconate by 4-oxalocrotonate tautomerase and 5-(carboxymethyl)-2-hydroxymuconate isomerase. J. Am. Chem. Soc. 114, 10104-10110.
20. 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.
21. 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.
22. Stivers J. T., Abeygunawardana C., Mildvan A. S., Hajipour G., Whitman C. P. and Chen L. H. (1996) The catalytic role of the amino-terminal proline in 4-oxalocrotonate tautomerase: affinity labeling and heteronuclear NMR studies. Biochemistry 35, 803-813.
23. a values of active site residues. Biochemistry 35, 814-823.
24. Wang S. C, Johnson Jr. W. H., Czerwinski R. M., Stamps S. L. and Whitman C. P. (2007) Kinetic and stereochemical analysis of YwhB, a 4-oxalocrotonate tautomerase homologue in Bacillus subtilis: mechanistic implications for the YwhB- and 4-oxalocrotonate tautomerase-catalyzed reactions. Biochemistry 46, 11919-11929.
25. 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.
26. Horowitz N. H. (1945) On the evolution of biochemical syntheses. Proc. Natl. Acad. Sci. USA, 31, 153-157.
27. Jensen R. A. (1976) Enzyme recruitment in evolution of new function. Ann. Rev. Microbiol. 30, 409-25.
28. Hughes A. L. (1994) The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. London Ser. B 256, 119-124.
29. Hughes A. L. (2005) Gene duplication and the origin of novel proteins. Proc. Natl. Acad. Sci. USA, 102, 8791-8792.
30. Perona J. J. and Craik C. S. (1997) Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 272, 29987-29990.
31. Babbitt P. C. and Gerlt J. A. (1997) Understanding enzyme superfamilies. J. Biol. Chem. 272, 30591-30594.
32. Neidhart D. J., Kenyon G. L., Gerlt J. A. and Petsko, G. A. (1990) Mandelate racemase and muconate lactonizing enzyme are mechanistically distinct and structurally homologous. Nature 347, 692-694.
33. Babbitt P. C. and Gerlt J. A. (2001) New functions from old scaffolds: how nature reengineers enzymes for new functions. Adv. in Protein Chem. 55, 1-28.
34. Holden H. M., Benning M. M., Haller T. and Gerlt J. A. (2001) The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme A thioesters. Acc. Chem. Res. 34, 145-157.
35. 8-barrel enzymes. Curr. Opin. Chem. Biol. 7, 252-264.
36. Gerlt J. A., Babbitt P. C. and Rayment I. (2005) Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity. Arch. Biochem. Biophys. 433, 59-70.
37. O'Brien P. J. and Herschlag D. (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol. 6, R91-R105.
38. 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.
39. Copley S. D. (2003) Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr. Opin. Chem. Biol. 7, 265-272.
40. Yoshikuni Y., Ferrin T. E. and Keasling J. D. (2006) Designed divergent evolution of enzyme function. Nature 440, 1078-1082.
41. Roodveldt C. and Tawfik D. S. (2005) Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily. Biochemistry 44, 12728-12736.
42. 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.
43. Wang S. C., Person M. D., Johnson Jr. W. H. 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.
44. Johnson Jr. W. H., Czerwinski R. M., Fitzgerald M. C. and Whitman, C. P. (1997) Inactivation of 4-oxalocrotonate tautomerase by 2-oxo-3-pentynoate. Biochemistry 36, 15724-15732.
45. Taylor A. B., Czerwinski R. M., Johnson Jr. W. H., 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.
46. 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.
47. Azurmendi H. F., Wang S. C., Massiah M. A., PoelarendsG. 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.
48. Poelarends G. J., Serrano H., Johnson Jr. W. H. and Whitman C. P. (2004) Stereospecific alkylation of cis-3-chloroacrylic acid dehalogenase by (R)-oxirane-2-carboxylate: analysis and mechanistic implications. Biochemistry 43, 7187-7196.
49. de Jong R. M., Bazzacco P., Poelarends G. J., Johnson Jr. W. H., Kim Y.-J., Burks E. A., Serrano H., Whitman C. P. and Dijkstra B. W. (2007) Crystal structures of wild type and inactivated cis-3-chloroacrylic acid dehalogenase: the structural basis for substrate specificity and inactivation by (R)-oxirane-2-carboxylate. J. Biol. Chem. 282, 2440-2449.
50. Poelarends G. J., Serrano H., Johnson Jr. W. H., 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.
51. Poelarends G. J., Serrano H., Johnson Jr. W. H. and Whitman C. P. (2005) Inactivation of malonate semialdehyde decarboxylase by 3-halopropiolates: evidence for hydratase activity. Biochemistry 44, 9375-9381.
52. Almrud J. J., Poelarends G. J., Johnson Jr. W. H., Serrano H., Hackert M. L. and Whitman C. P. (2005) Crystal structures of the wild-type, P1A mutant, and inactivated malonate semi-aldehyde decarboxylase: a structural basis for the decarboxylase and hydratase activities. Biochemistry 44, 14818-14827.
53. Wang S. C, Johnson Jr. W. H. and Whitman C. P. (2003) The 4-oxalocrotonate tautomerase- and YwhB-catalyzed hydration of 3E-haloacrylates: implications for the evolution of new enzymatic activities. J. Am. Chem. Soc. 125, 14282-14283.
54. Poelarends G. J., Almrud J. J., Serrano H., Darty J. E., Johnson Jr. W. H., Hackert M. L. and Whitman C. P. (2006) Evolution of enzymatic activity in the tautomerase superfamily:mechanistic and structural consequences of the L8R mutation in 4-oxalocrotonate tautomerase. Biochemistry 45, 7700-7708.
55. Poelarends G. J., Serrano H., Johnson Jr. W. H. and Whitman, C. P (2007) The phenylpyruvate tautomerase activity of trans-3-chloroacrylic acid dehalogenase: evidence for an enol intermediate in the dehalogenase reaction? Biochemistry 46, 9596-9604.
56. Poelarends G. J., Serrano H., Person M. D., Johnson Jr. W. H. and Whitman C. P. (2008) Characterization of Cg10062 from Corynebacterium glutamicum: implications for the evolution of cis-3-chloroacrylic acid dehalogenase activity in the tautomerase superfamily. Biochemistry 47, 8139-8147.
57. DeLano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA, USA. (http://www.pymol.org)