New superfamily members identified for Schiff-Base enzymes based on verification of catalytically essential residues

Biochemistry

Volumn 45, Issue 28, 2006, Pages 8546-8555

  Choi, Kyung H ^a,b   Lai, Vicky ^a   Foster, Christine E ^a   Morris, Aaron J ^a   Tolan, Dean R ^a   Allen, Karen N ^a,b  

^a Boston University   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYSIS; DEHYDRATION; ENZYME KINETICS; FRUCTOSE; MUTAGENESIS; PHOSPHATES; SUBSTRATES;

ALDOLASES FRUCTOSE-1,6-(BIS)PHOSPHATE (FBP) ALDOLASE; CATALYTIC DYAD; PRE-STEADY-STATE KINETICS; SCHIFF-BASE FORMATION;

ENZYMES;

2 KETO 3 DEOXY 6 PHOSPHOGLUCONATE ALDOLASE; ENZYME; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUTAMIC ACID; HISTIDINE; LYASE; LYSINE; N ACETYLNEURAMINATE LYASE; SCHIFF BASE; TRANSALDOLASE; TYROSINE; UNCLASSIFIED DRUG;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; BETA CHAIN; CATALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; PRIORITY JOURNAL; PROTEIN FAMILY; PROTON TRANSPORT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; STEADY STATE;

ALDEHYDE-LYASES; AMINO ACID SEQUENCE; CATALYSIS; EVOLUTION, MOLECULAR; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SCHIFF BASES; SEQUENCE ALIGNMENT;

EID: 33746078101     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060239d     Document Type: Article

References (52)

1. 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.
2. Babbitt, P. C., and Gerlt, J. A. (1997) Understanding enzyme superfamilies. Chemistry as the fundamental determinant in the evolution of new catalytic activities, J. Biol. Chem. 272, 30591-30594.
3. Gerlt, J. A., and Babbitt, P. C. (2000) Can sequence determine function? Genome Biol. 1, REVIEWS0005.1-REVIEWS0005.9.
4. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: A structural classification of proteins database for the investigation of sequences and structures, J. Mol. Biol. 247, 536-540.
5. Rutter, W. J. (1960) Aldolase, Enzymes 5, 341-372.
6. Horecker, B. L., Tsolas, O., and Lai, C. Y. (1975) Aldolases, in The Enzymes (Boyer, P. D., Ed.) pp 213-258, Academic Press, New York.
7. Marsh, J. J., and Lebherz, H. G. (1992) Fructose-bisphosphate aldolases: An evolutionary history, Trends Biochem. Sci. 17, 110-113.
8. Cooper, S. J., Leonard, G. A., McSweeney, S. M., Thompson, A. W., Naismith, J. H., Qamar, S., Plater, A., Berry, A., and Hunter, W. N. (1996) The crystal structure of a class II fructose-1,6-bisphosphate aldolase shows a novel binuclear metal-binding active site embedded in a familiar fold, Structure 4, 1303-1315.
9. Sygusch, J., Beaudry, D., and Allaire, M. (1987) Molecular architecture of rabbit skeletal muscle aldolase at 2.7-Å resolution, Proc. Natl. Acad. Sci. U.S.A. 84, 7846-7850.
10. Lawrence, M. C., Barbosa, J. A., Smith, B. J., Hall, N. E., Pilling, P. A., Ooi, H. C., and Marcuccio, S. M. (1997) Structure and mechanism of a sub-family of enzymes related to N-acetylneuraminate lyase, J. Mol. Biol. 266, 381-399.
11. Barbosa, J. A., Smith, B. J., DeGori, R., Ooi, H. C., Marcuccio, S. M., Campi, E. M., Jackson, W. R., Brossmer, R., Sommer, M., and Lawrence, M. C. (2000) Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme, J. Mol. Biol. 303, 405-421.
12. Grazi, E., Rowley, P. T., Chang, T., Tchola, O., and Horecker, B. L. (1962) The mechanisms of action of aldolases III: Schiff base formation with lysine, Biochem. Biophys. Res. Commun. 9, 38-43.
13. Midelfort, C. F., Gupta, R. K., and Rose, I. A. (1976) Fructose 1,6-bisphosphate: Isomeric composition, kinetics, and substrate specificity for the aldolases, Biochemistry 15, 2178-2185.
14. Rose, I. A., O'Connell, E. L., and Mehler, A. H. (1965) Mechanism of the aldolase reaction, J. Biol. Chem. 240, 1758-1765.
15. Rose, I. A., and Warms, J. V. B. (1985) Complexes of muscle aldolase in equilibrium with fructose 1,6-bisphosphate, Biochemistry 24, 3952-3957.
16. Choi, K.-H., and Tolan, D. R. (2004) Presteady-state kinetic evidence for a ring-opening activity in fructose-1,6-(bis)phosphate aldolase, J. Am. Chem. Soc. 126, 3402-3403.
17. Rose, I. A., Warms, J. V. B., and Kuo, D. J. (1987) Concentration and partitioning of intermediates in the fructose bisphosphate aldolase reaction. Comparison of the muscle and liver enzymes, J. Biol. Chem. 262, 692-701.
18. Morris, A. J., and Tolan, D. R. (1994) Lysine-146 of rabbit muscle aldolase is essential for cleavage and condensation of the C3-C4 bond of fructose 1,6-bis(phosphate), Biochemistry 33, 12291-12297.
19. Matthews, B. W., Remington, S. J., Grutter, M. G., and Anderson, W. F. (1981) Relation between hen egg white lysozyme and bacteriophage T4 lysozyme: Evolutionary implications, J. Mol. Biol. 147, 545-558.
20. Choi, K. H., Shi, J., Hopkins, C. E., Tolan, D. R., and Allen, K. N. (2001) Snapshots of catalysis: The structure of fructose-1,6-(bis)phosphate aldolase covalently bound to the substrate dihydroxyacetone phosphate, Biochemistry 40, 13868-13875.
21. Choi, K. H., Mazurkie, A. S., Morris, A. J., Utheza, D., Tolan, D. R., and Allen, K. N. (1999) Structure of a fructose-1,6-bis-(phosphate) aldolase liganded to its natural substrate in a cleavage-defective mutant at 2.3 Å, Biochemistry 38, 12655-12664.
22. Morris, A. J., and Tolan, D. R. (1993) Site-directed mutagenesis identifies aspartate 33 as a previously unidentified critical residue in the catalytic mechanism of rabbit aldolase A, J. Biol. Chem. 268, 1095-1100.
23. Morris, A. J., Davenport, R. C., and Tolan, D. R. (1996) A lysine to arginine substitution at position 146 of rabbit aldolase A shifts the rate-determining step to Schiff base formation, Protein Eng. 9, 61-67.
24. Blom, N., and Sygusch, J. (1997) Product binding and role of the C-terminal region in class I D-fructose 1,6-bisphosphate aldolase, Nat. Struct. Biol. 4, 36-39.
25. St-Jean, M., Lafrance-Vanasse, J., Liotard, B., and Sygusch, J. (2005) High-resolution reaction intermediates of rabbit muscle fructose-1,6- bisphosphate aldolase: Substrate cleavage and induced fit, J. Biol. Chem. 280, 27262-27270.
26. 8 barrel proteins, J. Biol. Chem. 278, 47253-47260.
27. Maurady, A., Zdanov, A., de Moissac, D., Beaudry, D., and Sygusch, J. (2002) A conserved glutamate residue exhibits multifunctional catalytic roles in D-fructose-1,6-bisphosphate aldolases, J. Biol. Chem. 277, 9474-9483.
28. Gilson, E., Clement, J. M., Brutlag, D., and Hofnung, M. (1984) A family of dispersed repetitive extragenic palindromic DNA sequences in E. coli, EMBO J. 3, 1417-1412.
29. Sayers, J. R., and Eckstein, F. (1989) Site-directed mutagenesis, based on the phosphorothioate approach, in Protein Function (Creigton, T. E., Ed.) pp 279-295, IRL Press, Oxford, England.
30. Beernink, P. T., and Tolan, D. R. (1992) Construction of a high-copy "ATG vector" for expression in Escherichia coli, Protein Expression Purif. 3, 332-336.
31. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids, J. Mol. Biol. 166, 557-580.
32. Racker, E. (1947) Spectrophotometric measurement of hexokinase and phosphohexokinase activity, J. Biol. Chem. 167, 843-854.
33. Cleland, W. W. (1990) Steady-state kinetics, Enzymes 19, 99-158.
34. Baranowski, T., and Niederland, T. R. (1949) Aldolase activity of myogen A, J. Biol. Chem. 180, 543-551.
35. Kuo, D. J., and Rose, I. A. (1985) Chemical trapping of complexes of dihydroxyacetone phosphate with muscle fructose- 1,6-bisphosphate aldolase, Biochemistry 24, 3947-3952.
36. Sali, A., and Blundell, T. L. (1990) Definition of general topological equivalence in protein structures. A procedure involving comparison of properties and relationships through simulated annealing and dynamic programming, J. Mol. Biol. 212, 403-428.
37. Mizuguchi, K., Deane, C. M., Blundell, T. L., Johnson, M. S., and Overington, J. P. (1998) JOY: Protein sequence-structure representation and analysis, Bioinformatics 14, 617-623.
38. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these methods, Acta Crystallogr. A47, 110-119.
39. Sayer, J. M., Pinsky, B., Schonbrunn, A., and Washtien, W. (1974) Mechanism of carbinolamine formation, J. Am. Chem. Soc. 96, 7998-8009.
40. Allard, J., Grochulski, P., and Sygusch, J. (2001) Covalent intermediate trapped in 2-keto-3-deoxy-6-phosphogluconate (KDPG) aldolase structure at 1.95-Å resolution, Proc. Natl. Acad. Sci. U.S.A. 98, 3679-3684.
41. Heine, A., DeSantis, G., Luz, J. G., Mitchell, M., Wong, C. H., and Wilson, I. A. (2001) Observation of covalent intermediates in an enzyme mechanism at atomic resolution, Science 294, 369-374.
42. Hartmann, M., Schneider, T. R., Pfeil, A., Heinrich, G., Lipscomb, W. N., and Braus, G. H. (2003) Evolution of feedback-inhibited β/α. barrel isoenzymes by gene duplication and a single mutation, Proc. Natl. Acad. Sci. U.S.A. 100, 862-867.
43. Schorken, U., Thorell, S., Schurmann, M., Jia, J., Sprenger, G. A., and Schneider, G. (2001) Identification of catalytically important residues in the active site of Escherichia coli transaldolase, Eur. J. Biochem. 268, 2408-2415.
44. Dobson, R. C., Valegard, K., and Gerrard, J. A. (2004) The crystal structure of three site-directed mutants of Escherichia coli dihydrodipicolinate synthase: Further evidence for a catalytic triad, J. Mol. Biol. 338, 329-339.
45. Leech, A. P., James, R., Coggins, J. R., and Kleanthous, C. (1995) Mutagenesis of active site residues in type I dehydroquinase from Escherichia coli. Stalled catalysis in a histidine to alanine mutant, J. Biol. Chem. 270, 25827-25836.
46. Kruger, D., Schauer, R., and Traving, C. (2001) Characterization and mutagenesis of the recombinant N-acetylneuraminate lyase from Clostridium perfringens: Insights into the reaction mechanism, Eur. J. Biochem. 268, 3831-3839.
47. Littlechild, J., and Watson, H. (1993) A data-based reaction mechanism for type I fructose bisphosphate aldolase, Trends Biochem. Sci. 18, 36-39.
48. Gefflaut, T., Blonski, C., Perie, J., and Willson, M. (1995) Class I aldolases: Substrate specificity, mechanism, inhibitors and structural aspects, Prog. Biophys. Mol. Biol. 63, 301-340.
49. Blonski, C., De Moissac, D., Perie, J., and Sygusch, J. (1997) Inhibition of rabbit muscle aldolase by phosphorylated aromatic compounds, Biochem. J. 323, 71-77.
50. Thorell, S., Schurmann, M., Sprenger, G. A., and Schneider, G. (2002) Crystal structure of decameric fructose-6-phosphate aldolase from Escherichia coli reveals inter-subunit helix swapping as a structural basis for assembly differences in the transaldolase family, J. Mol. Biol. 319, 161-171.
51. 4, Biochem. Biophys. Res. Commun. 74, 1297-1301.
52. Jia, J., Huang, W., Schorken, U., Sahm, H., Sprenger, G. A., Lindqvist, Y., and Schneider, G. (1996) Crystal structure of transaldolase B from Escherichia coli suggests a circular permutation of the α/β barrel within the class I aldolase family, Structure 4, 715-724.