Treponema denticola cystalysin exhibits significant alanine racemase activity accompanied by transamination: Mechanistic implications

Biochemical Journal

Volumn 371, Issue 2, 2003, Pages 473-483

  Bertoldi, Mariarita ^a   Cellini, Barbara ^a   Paiardini, Alessandro ^b   Di Salvo, Martino ^b   Borri Voltattorni, Carla ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

C S lyase; Pyridoxal 5 phosphate; Side reaction

Indexed keywords

CATALYSIS; COENZYMES; ISOMERS; PH EFFECTS; PHOSPHATES;

ENANTIOMERS;

BIOCHEMISTRY;

ALANINE; ALANINE DEHYDROGENASE; AMINOTRANSFERASE; BACTERIAL ENZYME; CYSTALYSIN; LACTATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PYRIDOXAL 5 PHOSPHATE; RACEMASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ABSORPTION SPECTROPHOTOMETRY; ARTICLE; CATALYSIS; ENANTIOMER; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME KINETICS; MOLECULAR MODEL; NONHUMAN; PH; PRIORITY JOURNAL; SPIROCHETE; STEADY STATE; TRANSAMINATION; TREPONEMA DENTICOLA;

ALANINE; ALANINE RACEMASE; APOENZYMES; CIRCULAR DICHROISM; CLONING, MOLECULAR; CYSTATHIONINE GAMMA-LYASE; ESCHERICHIA COLI; KINETICS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY; TRANSAMINASES; TREPONEMA;

BACTERIA (MICROORGANISMS); SPIROCHAETA; SPIROCHAETALES; TREPONEMA; TREPONEMA DENTICOLA;

EID: 0038302704     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20020875     Document Type: Article

References (39)

1. Chu, L., Ebersole, J. L., Kurzban, G. P. and Holt, S. C. (1997) Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect. Immun. 65, 3231-3238
2. Bertoldi, M., Cellini, B., Clausen, T. and Borri Voltattorni, C. (2002) Spectroscopic and kinetic analyses reveal the pyridoxal 5′-phosphate binding mode and the catalytic features of Treponema denticola cystalysin. Biochemistry 41, 9153-9164
3. Metha, P. K. and Christen, P. (2000) The molecular evolution of pyridoxal-5′-phosphate-dependent enzymes. Adv. Enzymol. Relat. Areas Mol. Biol. 74, 129-184
4. Grishin, N. V., Phillips, M. A. and Goldsmith, E. J. (1995) Modeling of the spatial structure of eukaryotic ornithine decarboxylase. Protein Sci. 4, 1291-1304
5. Krupka, H. I., Huber, R., Holt, S. C. and Clausen, T. (2000) Crystal structure from Treponema denticola: a pyridoxal 5′-phosphate-dependent protein acting as a haemolytic enzyme. EMBO J. 19, 3168-3179
6. Shaw, J. P., Petsko, G. A. and Ringe, D. (1997) Determination of the structure of alanine racemase from Bacillus stearothermophilus at 1.9 Å. Biochemistry 36, 1329-1342
7. Jansonius, J. N. (1998) Structure, evolution and action of vitamin B6-dependent enzymes. Curr. Opinion Struct. Biol. 8, 759-769
8. 39 → Ala mutant. J. Biol. Chem. 274, 4189-4194
9. Sun, S. and Toney, M. D. (1999) Evidence for a two-base mechanism involving tyrosine-265 from arginine-219 mutants of alanine racemase. Biochemistry 38, 4058-4065
10. Watanabe, A., Yoshimura, T., Mikami, B. and Esaki, N. (1999) Tyrosine 265 of alanine racemase serves as a substrate abstracting α-hydrogen from L-alanine: the counterpart residue to lysine 39 specific for D-alanine. J. Biochem. (Tokyo) 126, 781-786
11. Watanabe, A., Yoshimura, T., Mikami, B., Hayashi, H., Kagamiyama, H. and Esaki, N. (2002) Reaction of alanine racemase from Bacillus stearothermophilus: X-ray crystallographic studies of the enzyme bound with N-(5′-phosphopyridoxyl)-alanine. J. Biol. Chem. 277, 19166-19172
12. Ondrechen, M. J., Briggs, J. M. and McCammon, J. A. (2001) A model for enzyme-substrate interaction in alanine racemase. J. Am. Chem. Soc. 123, 2830-2834
13. Kurokawa, Y., Watanabe, A., Yoshimura, T., Esaki, N. and Soda, K. (1998) Transamination as a side-reaction catalyzed by alanine racemase of Bacillus stearothermophilus. J. Biochem. (Tokyo) 124, 1163-1169
14. Badet, B., Roise, D. and Wash, C. T. (1984) Inactivation of the dadB Salmonella typhimurium by D and L isomers of β-substituted alanines: kinetics, stoichiometry, active site peptide sequencing, and reaction mechanism. Biochemistry 23, 5188-5194
15. Esaki, N. and Walsh, C. T. (1986) Biosynthetic alanine racemase of Salmonella typhimurium: purification and characterization of the enzyme encoded by the air gene. Biochemistry 25, 3261-3267
16. Di Salvo, M., Yang, E., Zhao, G., Winkler, M. E. and Schirch, V. (1998) Expression, purification, and characterization of recombinant Escherichia coli pyridoxine 5′-phosphate oxidase. Protein Expr. Purif. 13, 249-256
17. Yang, E. S. and Schirch, V. (1998) Tight binding of pyridoxal 5′-phosphate to recombinant Escherichia coli pyridoxine 5′-phosphate oxidase. Arch. Biochem. Biophys. 377, 109-114
18. Bertoldi, M. and Borri Voltattorni, C. (2000) Reaction of dopa decarboxylase with L-aromatic amino acids under aerobic and anaerobic conditions. Biochem. J. 352, 533-538
19. Di Salvo, M. L., Ko, T. P., Musayev, F. N., Raboni, S., Schirch, V. and Safo, M. K. (2002) Active site structure and stereospecificity of Escherichra coli pyridoxine-5′-phosphate oxidase. J. Mol. Biol. 315, 385-397
20. Yoshimura, T., Nishimura, K., Ito, J., Esaki, N., Kagamiyama, H., Manning, J. M. and Soda, K. (1993) Unique stereospecificity of D-amino acid aminotransferase and branched-chain L-amino acid aminotransferase for C-4′ hydrogen transfer of the coenzyme. J. Am. Chem. Soc. 115, 3897-3900
21. Trivedi, V., Gupta, A., Jala, V. R., Saravanan, P., Rao, G. S. J., Rao, N. A., Savithri, H. S. and Subramanja, H. S. (2002) Crystal structure of binary and tertiary complexes of serine hydroxymethyltransferase from B. stearothermophillus: insights into the catalytic mechanism. J. Biol. Chem. 277, 17161-17169
22. Contestabile, R., Paiardini, A., Pascarella, S., di Salvo, M. L., D'Aguanno, S. and Bossa, F. (2001) L-threonine aldolase, serine hydroxymethyltransferase and fungal alanine racemase: a subgroup of strictly related enzymes specialized for different functions. Eur. J. Biochem. 268, 6508-6525
23. Biosym/MSI (1995) InsightII User Guide, Biosym/MSI, San Diego
24. Fersht, A. (1985) The basic equations of enzyme kinetics. In Enzyme Structure and Mechanism, pp. 98-120, W.H. Freeman and Co., New York
25. Feng, L., Geck, M. K., Eliot, A. C. and Kirsch, J. F. (2000) Aminotransferase activity and bioinformatic analysis of 1-aminocyclopropane-1-carboxyrate synthase. Biochemistry 39, 15242-15249
26. Demidkina, T., Myagkikh, I. V. and Azhayev, A. V. (1987) Transamination catalyzed by tyrosine phenol-lyase from Citrobacter intermedius. Eur. J. Biochem. 170, 311-316
27. Gloss, L. M. and Kirsch, J. F. (1995) Decreasing the basicity of the active site, Lys-258, of Escherichia coli of aspartate aminotransferase by replacement with γ-thialysine. Biochemistry 34, 3990-3998
28. Dunathan, H. C. (1971) Stereochemical aspects of pyridoxal phosphate catalysis. Adv. Enzymol. Relat. Areas Mol. Biol. 35, 79-134
29. Lim, H. L., Yoshimura, T., Kurokawa, Y., Esaki, N. and Soda, K. (1998) Nonstereospecific transamination catalyzed by pyridoxal phosphate-dependent amino acid racemases of broad substrate specificity. J. Biol. Chem. 273, 4001-4005
30. Panizzutti, R., De Miranda, J., Ribeiro, C. S., Engelender, S. and Wolosker, H. (2001) A new strategy to decrease N-methyl-D-aspartate (NMDA) receptor coactivation: inhibition of D-serine synthesis by converting serine racemase into an eliminase. Proc. Natl. Acad. Sci. U.S.A. 98, 5294-5299
31. Miles, E. W., Phillips, R. S., Yeh, H. J. C. and Cohen, L A. (1986) Isomerization of (3S)-2,3-dihydro-5-fluoro-L-tryptophan and 5-fluoro-L-tryptophan catalyzed by tryptophan synthase: studies using filorine-19 nuclear magnetic resonance and difference spectroscopy. Biochemistry 25, 4240-4249
32. Shostak, K. and Schirch, V. (1988) Serine hydroxymethyltransferase: mechanism of the racemization and transamination of D- and L-alanine. Biochemistry 27, 8007-8014
33. Kochhar, S. and Christen, P. (1992) Mechanism of racemization of amino acids by aspartate aminotransferase. Eur. J. Biochem. 203, 563-569
34. Chen, H. and Phillips, R. S. (1993) Binding of phenol and analogues to alanine complexes of tyrosine phenol-lyase from Citrobacter freundii: implications for the mechanisms of α,β-elimination and alanine racemization. Biochemistry 32, 11591-11599
35. Watanabe, A., Kurokawa, Y., Yoshimura, T. and Esaki, N. (1999) Role of tyrosine 265 of alanine racemase from Bacillus stearothermophilus. J. Biochem. 125, 987-990
36. Schaler, S. L., Barrett, W. C., Kallarakal, A. T., Mitra, B., Kozarich, J. W., Gerlt, J. A., Clofton, J. G., Petsko, G. A. and Kenyon, G. L. (1996) Mechanism of the reaction catalyzed by mandelate racemase: structure and mechanistic properties of the D270N mutant. Biochemistry 35, 5662-5669
37. Glavas, S. and Tanner, M. E. (1999) Catalytic acid/base residues of glutamate racemase. Biochemistry 38, 4106-4113
38. Cardinale, G. J. and Abeles, R. H. (1968) Purification and mechanism of action of proline racemase. Biochemistry 7, 3970-3978
39. De Lano, W. L. (2002) The pyMOL Molecular Graphics System, DeLano Scientifics, San Carlos, CA