Structural insights into the quinolone resistance mechanism of Mycobacterium tuberculosis DNA gyrase

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Piton, Jérémie ^a,b,c   Petrella, Stéphanie ^c   Delarue, Marc ^a,b   André Leroux, Gwénaëlle ^a,b   Jarlier, Vincent ^c   Aubry, Alexandra ^c   Mayer, Claudine ^a,b,d  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); QUINOLINE DERIVED ANTIINFECTIVE AGENT; BACTERIAL DNA; METAL; QUINOLONE DERIVATIVE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BIOPHYSICS; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG DNA BINDING; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME STRUCTURE; MOLECULAR MODEL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PROTEIN DOMAIN; STRUCTURE ANALYSIS; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ENZYME ACTIVE SITE; ENZYMOLOGY; METABOLISM; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

MYCOBACTERIUM TUBERCULOSIS;

AMINO ACID MOTIFS; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA GYRASE; DNA, BACTERIAL; DRUG DESIGN; DRUG RESISTANCE, BACTERIAL; METALS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PROTEIN STRUCTURE, SECONDARY; QUINOLONES;

EID: 77957908236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012245     Document Type: Article

References (56)

1. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369-413.
2. Buhler C, Gadelle D, Forterre P, Wang JC, Bergerat A (1998) Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res 26: 5157-5162.
3. Gadelle D, Filee J, Buhler C, Forterre P (2003) Phylogenomics of type II DNA topoisomerases. Bioessays 25: 232-242.
4. Schoeffler AJ, Berger JM (2005) Recent advances in understanding structurefunction relationships in the type II topoisomerase mechanism. Biochem Soc Trans 33: 1465-1470.
5. Levine C, Hiasa H, Marians KJ (1998) DNA gyrase and topoisomerase IV: biochemical activities, physiological roles during chromosome replication, and drug sensitivities. Biochim Biophys Acta 1400: 29-43.
6. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
7. Aubry A, Fisher LM, Jarlier V, Cambau E (2006) First functional characterization of a singly expressed bacterial type II topoisomerase: the enzyme from Mycobacterium tuberculosis. Biochem Biophys Res Commun 348: 158-165.
8. Schoeffler AJ, Berger JM (2008) DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys 41: 41-101.
9. Hooper CD, Rubinstein E (2003) Quinolone Antimicrobial Agents: ASM Press.
10. Blumberg HM, Burman WJ, Chaisson RE, Daley CL, Etkind SC, et al. (2003) American Thoracic Society/Centers for Disease Control and Prevention/ Infectious Diseases Society of America: treatment of tuberculosis. Am J Respir Crit Care Med 167: 603-662.
11. Conde MB, Efron A, Loredo C, De Souza GR, Graca NP, et al. (2009) Moxifloxacin versus ethambutol in the initial treatment of tuberculosis: a doubleblind, randomised, controlled phase II trial. Lancet 373: 1183-1189.
12. World Health Organization (2008) Global tuberculosis control-epidemiology, strategy, financing. WHO report 2009 WHO/HTM/TB/2009. 411 p.
13. Matrat S, Aubry A, Mayer C, Jarlier V, Cambau E (2008) Mutagenesis in the alpha3alpha4 GyrA helix and in the Toprim domain of GyrB refines the contribution of Mycobacterium tuberculosis DNA gyrase to intrinsic resistance to quinolones. Antimicrob Agents Chemother 52: 2909-2914.
14. Guillemin I, Jarlier V, Cambau E (1998) Correlation between quinolone susceptibility patterns and sequences in the A and B subunits of DNA gyrase in mycobacteria. Antimicrob Agents Chemother 42: 2084-2088.
15. Duong DA, Nguyen TH, Nguyen TN, Dai VH, Dang TM, et al. (2009) Beijing genotype of Mycobacterium tuberculosis is significantly associated with high-level fluoroquinolone resistance in Vietnam. Antimicrob Agents Chemother 53: 4835-4839.
16. Sun Z, Zhang J, Zhang X, Wang S, Zhang Y, et al. (2008) Comparison of gyrA gene mutations between laboratory-selected ofloxacin-resistant Mycobacterium tuberculosis strains and clinical isolates. Int J Antimicrob Agents 31: 115-121.
17. van Doorn HR, An DD, de Jong MD, Lan NT, Hoa DV, et al. (2008) Fluoroquinolone resistance detection in Mycobacterium tuberculosis with locked nucleic acid probe real-time PCR. Int J Tuberc Lung Dis 12: 736-742.
18. Hooper DC (1999) Mechanisms of fluoroquinolone resistance. Drug Resist Updat 2: 38-55.
19. Mdluli K, Ma Z (2007) Mycobacterium tuberculosis DNA gyrase as a target for drug discovery. Infect Disord Drug Targets 7: 159-168.
20. Takiff HE, Salazar L, Guerrero C, Philipp W, Huang WM, 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.
21. Aubry A, Veziris N, Cambau E, Truffot-Pernot C, Jarlier V, et al. (2006) Novel gyrase mutations in quinolone-resistant and -hypersusceptible clinical isolates of Mycobacterium tuberculosis: functional analysis of mutant enzymes. Antimicrob Agents Chemother 50: 104-112.
22. Veziris N, Martin C, Brossier F, Bonnaud F, Denis F, et al. (2007) Treatment failure in a case of extensively drug-resistant tuberculosis associated with selection of a GyrB mutant causing fluoroquinolone resistance. Eur J Clin Microbiol Infect Dis 26: 423-425.
23. Matrat S, Veziris N, Mayer C, Jarlier V, Truffot-Pernot C, et al. (2006) Functional analysis of DNA gyrase mutant enzymes carrying mutations at position 88 in the A subunit found in clinical strains of Mycobacterium tuberculosis resistant to fluoroquinolones. Antimicrob Agents Chemother 50: 4170-4173.
24. Fu G, Wu J, Liu W, Zhu D, Hu Y, et al. (2009) Crystal structure of DNA gyrase B' domain sheds lights on the mechanism for T-segment navigation. Nucleic Acids Res 37: 5908-5916.
25. Tretter EM, Schoeffler AJ, Weisfield SR, Berger JM (2010) Crystal structure of the DNA gyrase GyrA N-terminal domain from Mycobacterium tuberculosis. Proteins 8(2): 492-495.
26. Laponogov I, Sohi MK, Veselkov DA, Pan XS, Sawhney R, et al. (2009) Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat Struct Mol Biol 16: 667-669.
27. Edwards MJ, Flatman RH, Mitchenall LA, Stevenson CE, Le TB, et al. (2009) A crystal structure of the bifunctional antibiotic simocyclinone D8, bound to DNA gyrase. Science 326: 1415-1418.
28. Fu G, Wu J, Zhu D, Hu Y, Bi L, et al. (2009) Crystallization and preliminary crystallographic studies of Mycobacterium tuberculosis DNA gyrase B C-terminal domain, part of the enzyme reaction core. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 350-352.
29. Dong KC, Berger JM (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450: 1201-1205.
30. Aravind L, Leipe DD, Koonin EV (1998) Toprim-a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Res 26: 4205-4213.
31. Berger JM, Gamblin SJ, Harrison SC, Wang JC (1996) Structure and mechanism of DNA topoisomerase II. Nature 379: 225-232.
32. Fass D, Bogden CE, Berger JM (1999) Quaternary changes in topoisomerase II may direct orthogonal movement of two DNA strands. Nat Struct Biol 6: 322-326.
33. Laponogov I, Veselkov DA, Sohi MK, Pan XS, Achari A, et al. (2007) Breakagereunion domain of Streptococcus pneumoniae topoisomerase IV: crystal structure of a gram-positive quinolone target. PLoS One 2: e301.
34. Carr SB, Makris G, Phillips SE, Thomas CD (2006) Crystallization and preliminary X-ray diffraction analysis of two N-terminal fragments of the DNAcleavage domain of topoisomerase IV from Staphylococcus aureus. Acta Crystallogr Sect F Struct Biol Cryst Commun 62: 1164-1167.
35. Gubaev A, Hilbert M, Klostermeier D (2009) The DNA-gate of Bacillus subtilis gyrase is predominantly in the closed conformation during the DNA supercoiling reaction. Proc Natl Acad Sci U S A 106: 13278-13283.
36. Morais Cabral JH, Jackson AP, Smith CV, Shikotra N, Maxwell A, et al. (1997) Crystal structure of the breakage-reunion domain of DNA gyrase. Nature 388: 903-906.
37. Vagner J, Qu H, Hruby VJ (2008) Peptidomimetics, a synthetic tool of drug discovery. Curr Opin Chem Biol 12: 292-296.
38. Costenaro L, Grossmann JG, Ebel C, Maxwell A (2005) Small-angle X-ray scattering reveals the solution structure of the full-length DNA gyrase a subunit. Structure 13: 287-296.
39. Smith CK, Brannigan JA, Moore MH (1996) Factors affecting DNA sequence selectivity of nogalamycin intercalation: the crystal structure of d(TGTACA)2- nogalamycin2. J Mol Biol 263: 237-258.
40. Rohs R, West SM, Sosinsky A, Liu P, Mann RS, et al. (2009) The role of DNA shape in protein-DNA recognition. Nature 461: 1248-1253.
41. Heddle J, Maxwell A (2002) Quinolone-binding pocket of DNA gyrase: role of GyrB. Antimicrob Agents Chemother 46: 1805-1815.
42. Von Groll A, Martin A, Jureen P, Hoffner S, Vandamme P, et al. (2009) Fluoroquinolone resistance in Mycobacterium tuberculosis and mutations in gyrA and gyrB. Antimicrob Agents Chemother 53: 4498-4500.
43. Piton J, Matrat M, Petrella S, Jarlier V, Aubry A, Mayer C (2009) Purification, crystallization and preliminary X-ray diffraction experiments on the breakagereunion domain of the DNA gyrase from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 1182-1186.
44. Kabsch W (1988) Automatic indexing of rotation diffraction patterns. Journal of Applied Crystallography 21: 67-72.
45. Matthews BW (1968) Solvent content of protein crystals. JMol Biol 33: 491-497.
46. Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallographica Section A 50: 157-163.
47. Collaborative Computational Project N (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
48. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, et al. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60: 2210-2221.
49. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
50. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA http://www.pymol.org.
51. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
52. Vagin A, Teplyakov A (1997) MOLREP: an Automated Program for Molecular Replacement. Journal of Applied Crystallography 30: 1022-1025.
53. Brown PH, Schuck P (2006) Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation. Biophysical Journal 90: 4651-4661.
54. García De La Torre J, Huertas ML, Carrasco B (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophysical Journal 78: 719-730.
55. Aubry A, Pan XS, Fisher LM, Jarlier V, Cambau E (2004) Mycobacterium tuberculosis DNA gyrase: interaction with quinolones and correlation with antimycobacterial drug activity. Antimicrob Agents Chemother 48: 1281-1288.
56. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.