An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity

Molecular Microbiology

Volumn 58, Issue 5, 2005, Pages 1392-1405

  Jain, Paras ^a   Nagaraja, Valakunja ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; BACTERIAL GENETICS; CATALYSIS; DRUG SENSITIVITY; ESCHERICHIA COLI; GENETIC CODE; GENOMICS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

CIPROFLOXACIN; DNA TOPOISOMERASES, TYPE II; DNA, SUPERHELICAL; ELECTROPHORESIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME INHIBITORS; MYCOBACTERIUM SMEGMATIS; NOVOBIOCIN; PHYLOGENY;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS;

EID: 28244475353     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04908.x     Document Type: Article

References (47)

1. Barnard, F.M., and Maxwell, A. (2001) Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser (83) and Asp (87). Antimicrob Agents Chemother 45: 1994-2000.
2. Bates, A.D., and Maxwell, A. (1993) DNA Topology. Oxford: IRL Press.
3. Bellon, S., Parsons, J.D., Wei, Y., Hayakawa, K., Swenson, L.L., Charifson, P.S., et al. (2004) Crystal structures of Escherichia coli topoisomerase IV ParE subunit (24 and 43 kilodaltons): a single residue dictates differences in novobiocin potency against topoisomerase IV and DNA gyrase. Antimicrob Agents Chemother 48: 1856-1864.
4. Bhaduri, T., Bagui, T.K., Sikder, D., and Nagaraja, V. (1998) DNA topoisomerase I from Mycobacterium smegmatis. An enzyme with distinct features. J Biol Chem 273: 13925-13932.
5. Camus, J.C., Pryor, M.J., Medigue, C., and Cole, S.T. (2002) Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology 148: 2967-2973.
6. Caron, P.R., and Wang, J.C. (1994) Appendix. II: Alignment of primary sequences of DNA topoisomerases. Adv Pharmacol 298:271-297.
7. Champoux, J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369-413.
8. Chatterji, M., Unniraman, S., Mahadevan, S., and Nagaraja, V. (2001) Effect of different classes of inhibitors on DNA gyrase from Mycobacterium smegmatis. J Antimicrob Chemother 48: 479-485.
9. Cole, S.T., Brosch, R., Parkhill, J., Gamier, T., Churcher, C., Harris, D., et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
10. Cole, S.T., Eiglmeier, K., Parkhill, J., James, K.D., Thomson, N.R., Wheeler, P.R., et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007-1011.
11. Corbett, K.D., and Berger, J.M. (2003) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J 22: 151-163.
12. Corbett, K.D., and Berger, J.M. (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu Rev Biophys Biomol Struct 33: 95-118.
13. Espeli, O., Levine, C., Hassing, H., and Marians, K.J. (2003a) Temporal regulation of topoisomerase IV activity in E. coli. Mol Cell 11: 189-201.
14. Espeli, O., Lee, C., and Marians, K.J. (2003b) A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J Biol Chem 278: 44639-44644.
15. Espeli, O., and Marians, K.J. (2004) Untangling intracellular DNA topology. Mol Microbiol 52: 925-931.
16. Fleischmann, R.D., Alland, D., Eisen, J.A., Carpenter, L., White, O., Peterson, J., et al. (2002) Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol 184: 5479-5490.
17. Forterre, P. (2002) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18: 236-237.
18. Forterre, P., Bouthier De La Tour, C., Philippe, H., and Duguet, M. (2000) Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from archaea to bacteria. Trends Genet 16: 152-154.
19. Gamier, T., Eiglmeier, K., Camus, J.C., Medina, N., Mansoor, H., Pryor, M., et al. (2003) The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 100: 7877-7882.
20. Gormley, N.A., Orphanides, G., Meyer, A., Cullis, P.M., and Maxwell, A. (1996) The interaction of coumarin antibiotics with fragments of DNA gyrase B protein. Biochemistry 35: 5083-5092.
21. Guillemin, I., Sougakoff, W., Cambau, E., Revel-Viravau, V., Moreau, N., and Jarlier, V. (1999) Purification and inhibition by quinolones of DNA gyrases from Mycobacterium avium, Mycobacterium smegmatis and Mycobacterium fortuitum bv. peregrinum. Microbiology 145: 2527-2532.
22. Hardy, C.D., and Cozzarelli, N.R. (2003) Alteration of Escherichia coli topoisomerase IV to novobiocin resistance. Antimicrob Agents Chemother 47: 941-947.
23. Heddle, J.G., Lu, T., Zhao, X., Drlica, K., and Maxwell, A. (2001 ) gyrB-225, a mutation of DNA gyrase that compensates for topoisomerase I deficiency: investigation of its low activity and quinolone hypersensitivity. J Mol Biol 309: 1219-1231.
24. Hiasa, H., and Marians, K.J. (1996) Two distinct modes of strand unlinking during theta-type DNA replication. J Biol Chem 271: 21529-21535.
25. Higgins, P.G., Fluit, A.C., and Schmitz, F.J. (2003) Fluoroquinolones: structure and target sites. Curr Drug Targets 4: 181-190.
26. Kampmann, M., and Stock, D. (2004) Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling. Nucl Acids Res 32: 3537-3545.
27. Kato, J., Nishimura, Y., Imamura, R., Niki, H., Hiraga, S., and Suzuki, H. (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63: 393-404.
28. Kocagoz, T., Hackbarth, C.J., Unsal, I., Rosenberg, E.Y., Nikaido, H., and Chambers, H.F. (1996) Gyrase mutations in laboratory-selected, fluoroquinolone-resistant mutants of Mycobacterium tuberculosis H37Ra. Antimicrob Agents Chemother 40: 1768-1774.
29. Kumar, S., Tamura, K., Jakobsen, I.B., and Nei, M. (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244-1245.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
31. Levine, C., Hiasa, H., and Marians, K.J. (1998) DNA gyrase and topoisomerase IV: biochemical activities, physiological roles during chromosome replication, and drug sensitivities. Biochim Biophys Acta 1400: 29-43.
32. Lewis, R.J., Singh, O.M., Smith, C.V., Skarzynski, T., Maxwell, A., Wonacott, A.J., and Wigley, D.B. (1996) The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J 15: 1412-1420.
33. Liu, L.F., and Wang, J.C. (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84: 7024-7027.
34. Luttinger, A. (1995) The twisted 'life' of DNA in the cell: bacterial topoisomerases. Mol Microbiol 15: 601-606.
35. Manjunatha, U.H., Dalal, M., Chatterji, M., Radha, D.R., Visweswariah, S.S., and Nagaraja, V. (2002) Functional characterisation of mycobacterial DNA gyrase: an efficient decatenase. Nucleic Acids Res 30: 2144-2153.
36. Maxwell, A. (1993) The interaction between coumarin drugs and DNA gyrase. Mol Microbiol 9: 681-686.
37. Maxwell, A. (1997) DNA gyrase as a drug target. Trends Microbiol 5: 102-109.
38. Menzel, R., and Gellert, M. (1983) Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34: 105-113.
39. Napoli, A., Valenti, A., Salerno, V., Nadal, M., Garnier, F., Rossi, M., and Ciaramella, M. (2004) Reverse gyrase recruitment to DNA after UV light irradiation in Sulfolobus solfataricus. J Biol Chem 279: 33192-33198.
40. Nurse, P., Levine, C., Hassing, H., and Marians, K.J. (2003) Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J Biol Chem 278: 8653-8660.
41. Peng, H., and Marians, K.J. (1993) Escherichia coli topoisomerase IV. Purification, characterization, subunit structure, and subunit interactions. J Biol Chem 268: 24481-24490.
42. Philipp, W.J., Poulet, S., Eiglmeier, K., Pascopella, L., Balasubramanian, V., Heym, B., et al. (1996) An integrated map of the genome of the tubercle bacillus, Mycobacterium tuberculosis H37Rv, and comparison with Mycobacterium leprae. Proc Natl Acad Sci USA 93: 3132-3137.
43. Schofield, M.A., Agbunag, R., Michaels, M.L., and Miller, J.H. (1992) Cloning and sequencing of Escherichia coli mutR shows its identity to topB, encoding topoisomerase III. J Bacteriol 174: 5168-5170.
44. Takiff, H.E., Salazar, L., Guerrero, C., Philipp, W., Huang, W.M., Kreiswirth, B., et al. (1994) Cloning and nucleotide sequence of Mycobacterium tuberculosis gyrA and gyrB genes and detection of quinolone resistance mutations. Antimicrob Agents Chemother 38: 773-780.
45. Wang, J.C. (1991) DNA topoisomerases: why so many. J Biol Chem 266: 6659-6662.
46. Wang, Y., Lynch, A.S., Chen, S.J., and Wang, J.C. (2002) On the molecular basis of the thermal sensitivity of an Escherichia coli topA mutant. J Biol Chem 277:1203-1209.
47. Wentzell, L.M., and Maxwell, A. (2000) The complex of DNA gyrase and quinolone drugs on DNA forms a barrier to the T7 DNA polymerase replication complex. J Mol Biol 304: 779-791.