Cloning, biochemical properties, and distribution of mycobacterial haloalkane dehalogenases

Applied and Environmental Microbiology

Volumn 71, Issue 11, 2005, Pages 6736-6745

  Jesenská, Andrea ^a   Pavlová, Martina ^a   Strouhal, Michal ^a   Chaloupková, Radka ^a   Těšínská, Iva ^a   Monincová, Marta ^a   Prokop, Zbyněk ^a   Bartoš, Milan ^b   Pavlík, Ivo ^b   Rychlík, Ivan ^b   Möbius, Petra ^c   Nagata, Yuji ^d   Damborský, Jiři ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

^b VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^c FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CLONING; PH EFFECTS; POLYPEPTIDES; PROTEINS;

DEHALOGENASE ACTIVITY; PCR SCREENING; THIOREDOXIN;

ENZYMES;

BACTERIAL ENZYME; MYCOBACTERIAL HALOALKANE DEHALOGENASE; POLYPEPTIDE; PROTEIN; PROTEIN DMBA; PROTEIN DMBB; UNCLASSIFIED DRUG;

ENZYME;

ARTICLE; CATALYSIS; CIRCULAR DICHROISM; COMPARATIVE GENOMIC HYBRIDIZATION; ENZYME ACTIVITY; GENE EXPRESSION; GENOMICS; HYDROLYSIS; MOLECULAR CLONING; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION;

ANIMALS; BACTERIAL PROTEINS; CATTLE; CLONING, MOLECULAR; ENZYME STABILITY; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROLASES; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; SEQUENCE ANALYSIS, DNA; TEMPERATURE;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; ESCHERICHIA COLI; MYCOBACTERIUM; MYCOBACTERIUM AFRICANUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM BOVIS BCG; MYCOBACTERIUM CAPRAE; MYCOBACTERIUM MICROTI; MYCOBACTERIUM PINNIPEDII; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX;

EID: 32044445515     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.11.6736-6745.2005     Document Type: Article

References (45)

1. Allan, D., P. Thomas, and S. Gatt. 1980. 1,2-Diacylglycerol kinase of human erythrocyte membranes: assay with endogenously generated substrate. Biochem. J. 191:669-672.
2. Barth, S., M. Fischer, R. D. Schmid, and J. Pleiss. 2004. The database of epoxide hydrolases and haloalkane dehalogenases: one structure, many functions. Bioinformatics 20:2845-2847.
3. Chaloupkova, R., J. Sykorova, Z. Prokop, A. Jesenska, M. Monincova, M. Pavlova, M. Tsuda, Y. Nagata, and J. Damborsky. 2003. Modification of activity and specificity of haloalkane dehalogenase from Sphingomonas paucimobilis UT26 by engineering of its entrance tunnel. J. Biol. Chem. 278:52622-52628.
4. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M.-A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
5. Cole, S. T., K. Eiglmeier, J. Parkhill, K. D. James, N. R. Thomson, P. R. Wheeler, N. Honore, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M. A. Quail, M. A. Rajandream, K. M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J. R. Woodward, and B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1011.
6. Copley, S. D. 1998. Microbial dehalogenases: enzymes recruited to convert xenobiotic substrates. Curr. Opin. Chem. Biol. 2:613-617.
7. Damborsky, J., and J. Koca. 1999. Analysis of the reaction mechanism and substrate specificity of haloalkane dehalogenases by sequential and structural comparisons. Protein Eng. 12:989-998.
8. Damborsky, J., M. G. Nyandoroh, M. Nemec, I. Holoubek, A. T. Bull, and D. J. Hardman. 1997. Some biochemical properties and classification of a range of bacterial haloalkane dehalogenases. Biotechnol. Appl. Biochem. 26:19-25.
9. Damborsky, J., E. Rorije, A. Jesenska, Y. Nagata, G. Klopman, and W. J. G. M. Peijnenburg. 2001. Structure-specificity relationships for haloalkane dehalogenases. Environ. Toxicol. Chem. 20:2681-2689.
10. de Kreij, A., B. van den Burg, G. Venema, G. Vriend, V. G. Eijsink, and J. E. Nielsen. 2002. Effects of modifying the surface charge on the catalytic activity of a thermolysin-like protease. J. Biol. Chem. 277:15432-15438.
11. Fujiyoshi, T., J. Nakayama, and M. Anai. 1982. Two pH optima of adenosine 5′-triphosphate dependent deoxyribonuclease from Bacillus laterosporus. Biochemistry 21:4159-4164.
12. Garnier, T., K. Eiglmeier, J. C. Camus, N. Medina, H. Mansoor, M. Pryor, S. Duthoy, S. Grondin, C. Lacroix, C. Monsempe, S. Simon, B. Harris, R. Atkin, J. Doggett, R. Mayes, L. Keating, P. R. Wheeler, J. Parkhill, B. G. Barrell, S. T. Cole, S. V. Gordon, and R. G. Hewinson. 2003. The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. USA 100: 7877-7882.
13. Green, E. P., M. T. Moss, J. Hermon-Taylor, and J. J. McFadden. 1989. Insertion elements in mycobacteria. Acta Leprol. 7:239-242.
14. Iwasaki, I., S. Utsumi, and T. Ozawa. 1952. New colorimetric determination of chloride using mercuric thiocyanate and ferric ion. Bull. Chem. Soc. Japan 25:226.
15. Janssen, D. B. 2004. Evolving haloalkane dehalogenases. Curr. Opin. Chem. Biol. 8:150-159.
16. Janssen, D. B., J. Gerritse, J. Brackman, C. Kalk, D. Jager, and B. Witholt. 1988. Purification and characterization of a bacterial dehalogenase with activity toward halogenated alkanes, alcohols, and ethers. Eur. J. Biochem. 171:67-92.
17. Janssen, D. B., F. Pries, J. Ploeg, B. Kazemier, P. Terpstra, and B. Witholt. 1989. Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhlA gene. J. Bacteriol. 171:6791-6799.
18. Jesenska, A., M. Bartos, V. Czernekova, I. Rychlik, I. Pavlik, and J. Damborsky. 2002. Cloning and expression of the haloalkane dehalogenase gene dhmA from Mycobacterium avium N85 and preliminary characterization of DhmA. Appl. Environ. Microbiol. 68:3724-3730.
19. Jesenska, A., I. Sedlacek, and J. Damborsky. 2000. Dehalogenation of haloalkanes by Mycobacterium tuberculosis H37Rv and other mycobacteria. Appl. Environ. Microbiol. 66:219-222.
20. Keuning, S., D. B. Janssen, and B. Witholt. 1985. Purification and characterization of hydrolytic haloalkane dehalogenase from Xanthobacter autotrophicus GJ10. J. Bacteriol. 163:635-639.
21. Kirschner, P., and E. C. Bottger. 1998. Species identification of mycobacteria using rDNA sequencing. Methods Mol. Biol. 101:349-361.
22. Krooshof, G. H., E. M. Kwant, J. Damborsky, J. Koca, and D. B. Janssen. 1997. Repositioning the catalytic triad acid of haloalkane dehalogenase: effects on activity and kinetics. Biochemistry 36:9571-9580.
23. Kunze, Z. M., F. Portaels, and J. J. McFadden. 1992. Biologically distinct subtypes of Mycobacterium avium differ in possession of insertion sequence IS901. J. Clin. Microbiol. 30:2366-2372.
24. Mahairas, G. G., P. J. Sabo, M. J. Hickey, D. C. Singh, and C. K. Stover. 1996. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J. Bacteriol. 178:1274-1282.
25. Marek, J., J. Vevodova, I. Kuta-Smatanova, Y. Nagata, L. A. Svensson, J. Newman, M. Takagi, and J. Damborsky. 2000. Crystal structure of the haloalkane dehalogenase from Sphingomonas paucimobilis UT26. Biochemistry 39:14082-14086.
26. Marvanova, S., Y. Nagata, M. Wimmerova, J. Sykorova, K. Hynkova, and J. Damborsky. 2001. Biochemical characterization of broad-specificity enzymes using multivariate experimental design and a colorimetric microplate assay: characterization of the haloalkane dehalogenase mutants. J. Microbiol. Methods 44:149-157.
27. Mattow, J., P. R. Jungblut, U. E. Schaible, H. J. Mollenkopf, S. Lamer, U. Zimny-Arndt, K. Hagens, E. C. Muller, and S. H. Kaufmann. 2001. Identification of proteins from Mycobacterium tuberculosis missing in attenuated Mycobacterium bovis BCG strains. Electrophoresis 22:2936-2946.
28. Nagai, R., S. Takewaki, A. Wada, K. Okuzumi, A. Tobita, and A. Ohkubo. 1990. Rapid detection and identification of mycobacterial DNA by PCR. Rinsho Byori 38:1247-1253. (In Japanese.)
29. Nagata, Y., K. Hynkova, J. Damborsky, and M. Takagi. 1999. Construction and characterization of histidine-tagged haloalkane dehalogenase (LinB) of a new substrate class from a γ-hexachlorocyclohexane-degrading bacterium, Sphingomonas paucimobilis UT26. Protein Expr. Purif. 17:299-304.
30. Nagata, Y., K. Miyauchi, J. Damborsky, K. Manova, A. Ansorgova, and M. Takagi. 1997. Purification and characterization of haloalkane dehalogenase of a new substrate class from a γ-hexachlorocyclohexane-degrading bacterium, Sphingomonas paucimobilis UT26. Appl. Environ. Microbiol. 63: 3707-3710.
31. Nagata, Y., T. Nariya, R. Ohtomo, M. Fukuda, K. Yano, and M. Takagi. 1993. Cloning and sequencing of a dehalogenase gene encoding an enzyme with hydrolase activity involved in the degradation of hexachlorocyclohexane in Pseudomonas paucimobilis. J. Bacteriol. 175:6403-6410.
32. Nagata, Y., Z. Prokop, S. Marvanova, J. Sykorova, M. Monincova, M. Tsuda, and J. Damborsky. 2003. Reconstruction of mycobacterial dehalogenase Rv2579 by cumulative mutagenesis of haloalkane dehalogenase LinB. Appl. Environ. Microbiol. 69:2349-2355.
33. Newman, J., T. S. Peat, R. Richard, L. Kan, P. E. Swanson, J. A. Affholter, I. H. Holmes, J. F. Schindler, C. J. Unkefer, and T. C. Terwilliger. 1999. Haloalkane dehalogenase: structure of a Rhodococcus enzyme. Biochemistry 38:16105-16114.
34. Pavlik, I., P. Svastova, J. Bartl, L. Dvorska, and I. Rychlik. 2000. Relationship between IS901 in the Mycobacterium avium complex strains isolated from birds, animals, humans, and environment and virulence for poultry. Clin. Diagn. Lab. Immunol. 7:212-217.
35. Poelarends, G., M. Zandstra, T. Bosma, L. A. Kulakov, M. J. Larkin, J. R. Marchesi, A. J. Weightman, and D. B. Janssen. 2000. Haloalkane-utilizing Rhodococcus strains isolated from geographically distinct locations possess a highly conserved gene cluster encoding haloalkane catabolism. J. Bacteriol. 182:2725-2731.
36. Poelarends, G. J., L. A. Kulakov, M. J. Larkin, J. E. T. van Hylckama Vlieg, and D. B. Janssen. 2000. Roles of horizontal transfer and gene integration in evolution of 1,3-dichloropropene- and 1,2-dibromoethane- degradative pathways. J. Bacteriol. 182:2191-2199.
37. Poelarends, G. J., J. E. T. van Hylckama Vlieg, J. R. Marchesi, L. M. Freitas dos Santos, and D. B. Janssen. 1999. Degradation of 1,2-dibromoethane by Mycobacterium sp. strain GP1. J. Bacteriol. 181:2050-2058.
38. Poelarends, G. J., M. Wilkens, M. J. Larkin, J. D. vanElsas, and D. B. Janssen. 1998. Degradation of 1,3-dichloropropene by Pseudomonas cichorii 170. Appl. Environ. Microbiol. 64:2931-2936.
39. Reen, R. K., D. S. Jamwal, S. C. Taneja, J. L. Koul, R. K. Dubey, F. J. Wiebel, and J. Singh. 1993. Impairment of UDP-glucose dehydrogenase and glucuronidation activities in liver and small intestine of rat and guinea pig in vitro by piperine. Biochem. Pharmacol. 46:229-238.
40. Rorem, E. S., and S. Schwimmer. 1963. Double pH optima of potato invertase. Experientia 19:150-151.
41. Sallis, P. J., S. J. Armfield, A. T. Bull, and D. J. Hardman. 1990. Isolation and characterization of a haloalkane halidohydrolase from Rhodococcus erythropolis Y2. J. Gen. Microbiol. 136:115-120.
42. Scholtz, R., T. Leisinger, F. Suter, and A. M. Cook. 1987. Characterization of 1-chlorohexane halidohydrolase, a dehalogenase of wide substrate range from an Arthrobacter sp. J. Bacteriol. 169:5016-5021.
43. Thierry, D., A. Brisson-Noel, V. Vincent-Levy-Frebault, S. Nguyen, J. L. Guesdon, and B. Gicquel. 1990. Characterization of a Mycobacterium tuberculosis insertion sequence, IS6110, and its application in diagnosis. J. Clin. Microbiol. 28:2668-2673.
44. Verschueren, K. H. G., F. Seljee, H. J. Rozeboom, K. H. Kalk, and B. W. Dijkstra. 1993. Crystallographic analysis of the catalytic mechanism of haloalkane dehalogenase. Nature 363:693-698.
45. Yokota, T., T. Omori, and T. Kodama. 1987. Purification and properties of haloalkane dehalogenase from Corynebacterium sp. strain m15-3. J. Bacteriol. 169:4049-4054.