Structure of Ddn, the deazaflavin-dependent nitroreductase from Mycobacterium tuberculosis involved in bioreductive activation of PA-824

Structure

Volumn 20, Issue 1, 2012, Pages 101-112

  Cellitti, Susan E ^a   Shaffer, Jennifer ^a   Jones, David H ^a   Mukherjee, Tathagata ^b   Gurumurthy, Meera ^c   Bursulaya, Badry ^a   Boshoff, Helena I ^b   Choi, Inhee ^b   Nayyar, Amit ^b   Lee, Yong Sok ^d   Cherian, Joseph ^c   Niyomrattanakit, Pornwaratt ^c   Dick, Thomas ^c   Manjunatha, Ujjini H ^c   Barry III, Clifton E ^b   Spraggon, Glen ^a   Geierstanger, Bernhard H ^a  

^a GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 DEAZAFLAVINE DERIVATIVE; 6,7 DIHYDRO 2 NITRO 6 (4 TRIFLUOROMETHOXYBENZYLOXY) 5H IMIDAZO[2,1 B][1,3]OXAZINE; NITROIMIDAZOLE; NITROREDUCTASE; REACTIVE NITROGEN SPECIES;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; DRUG RECEPTOR BINDING; DRUG STRUCTURE; ENZYME CONFORMATION; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NOCARDIA FARCINICA; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; FLAVINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NITROIMIDAZOLES; NITROREDUCTASES; PROTEIN BINDING; PROTEIN CONFORMATION; REACTIVE NITROGEN SPECIES;

MYCOBACTERIUM TUBERCULOSIS; NOCARDIA FARCINICA;

EID: 84862925406     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.11.001     Document Type: Article

References (62)

1. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 58 2002 1948 1954 (Pubitemid 35337293)
2. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
3. R.F. Anderson, S.S. Shinde, A. Maroz, M. Boyd, B.D. Palmer, and W.A. Denny Intermediates in the reduction of the antituberculosis drug PA-824, (6S)-2-nitro-6-[4-(trifluoromethoxy)benzyl]oxy-6,7-dihydro-5H-imidazo[2,1-b][1, 3]oxazine, in aqueous solution Org. Biomol. Chem. 6 2008 1973 1980 (Pubitemid 351693244)
4. 420-dependent secondary alcohol dehydrogenase, a member of the bacterial luciferase family Structure 12 2004 361 370 (Pubitemid 38353057)
5. 420/FMN binding site of enzymes within the nonprolyl cis-peptide containing bacterial luciferase family Protein Sci. 14 2005 1840 1849 (Pubitemid 40994154)
6. 420) in Mycobacterium species Arch. Microbiol. 176 2001 37 43 (Pubitemid 32692642)
7. Baker, W.R., Shaopei, C., and Keeler, E.L. (September 1997). Nitroimidazole antibacterial compounds and methods of use thereof. U.S. patent 5,668,127.
8. C.E. Barry III, H.I.M. Boshoff, and C.S. Dowd Prospects for clinical introduction of nitroimidazole antibiotics for the treatment of tuberculosis Curr. Pharm. Des. 10 2004 3239 3262 (Pubitemid 39276613)
9. C.E. Barry III, H.I. Boshoff, V. Dartois, T. Dick, S. Ehrt, J. Flynn, D. Schnappinger, R.J. Wilkinson, and D. Young The spectrum of latent tuberculosis: rethinking the biology and intervention strategies Nat. Rev. Microbiol. 7 2009 845 855
10. 420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding J. Biol. Chem. 283 2008 17531 17541
11. H.I.M. Boshoff, and C.E. Barry III Tuberculosis - metabolism and respiration in the absence of growth Nat. Rev. Microbiol. 3 2005 70 80 (Pubitemid 40028470)
12. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
13. 420)-dependent methylenetetrahydromethanopterin dehydrogenase Biochemistry 48 2009 10098 10105
14. S.E. Cellitti, D.H. Jones, L. Lagpacan, X.S. Hao, Q. Zhang, H.Y. Hu, S.M. Brittain, A. Brinker, J. Caldwell, and B. Bursulaya In vivo incorporation of unnatural amino acids to probe structure, dynamics, and ligand binding in a large protein by nuclear magnetic resonance spectroscopy J. Am. Chem. Soc. 130 2008 9268 9281 (Pubitemid 352031137)
15. E.L. Corbett, C.J. Watt, N. Walker, D. Maher, B.G. Williams, M.C. Raviglione, and C. Dye The growing burden of tuberculosis: global trends and interactions with the HIV epidemic Arch. Intern. Med. 163 2003 1009 1021 (Pubitemid 36548927)
16. M.L. di Salvo, M.K. Safo, F.N. Musayev, F. Bossa, and V. Schirch Structure and mechanism of Escherichia coli pyridoxine 5′-phosphate oxidase Biochim. Biophys. Acta 1647 2003 76 82 (Pubitemid 38234636)
17. C. Dye, S. Scheele, P. Dolin, V. Pathania, and M.C. Raviglione Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project JAMA 282 1999 677 686
18. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
19. M.W. Fraaije, and A. Mattevi Flavoenzymes: diverse catalysts with recurrent features Trends Biochem. Sci. 25 2000 126 132 (Pubitemid 30122424)
20. 420 biosynthesis Arch. Microbiol. 180 2003 455 464 (Pubitemid 38002314)
21. M. Gurumurthy, T. Mukherjee, C.S. Dowd, R. Singh, P. Niyomrattanakit, J.A. Tay, A. Nayyar, Y.S. Lee, J. Cherian, and H.I. Boshoff Substrate specificity of the deazaflavin-dependent nitroreductase from Mycobacterium tuberculosis responsible for the bioreductive activation of bicyclic nitroimidazoles FEBS J. 279 2012 113 125
22. Y. Hu, A.R.M. Coates, and D.A. Mitchison Comparison of the sterilising activities of the nitroimidazopyran PA-824 and moxifloxacin against persisting Mycobacterium tuberculosis Int. J. Tuberc. Lung Dis. 12 2008 69 73
23. J.G. Hurdle, R.B. Lee, N.R. Budha, E.I. Carson, J.J. Qi, M.S. Scherman, S.H. Cho, M.R. McNeil, A.J. Lenaerts, and S.G. Franzblau A microbiological assessment of novel nitrofuranylamides as anti-tuberculosis agents J. Antimicrob. Chemother. 62 2008 1037 1045
24. 420-5,6 by using Mycobacterium smegmatis Appl. Environ. Microbiol. 68 2002 5750 5755 (Pubitemid 35265718)
25. F. Jacobson, and C. Walsh Properties of 7,8-didemethyl-8-hydroxy-5- deazaflavins relevant to redox coenzyme function in methanogen metabolism Biochemistry 23 1984 979 988
26. 420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii J. Biol. Chem. 280 2005 38776 38786 (Pubitemid 43853780)
27. P. Kim, S. Kang, H.I. Boshoff, J. Jiricek, M. Collins, R. Singh, U.H. Manjunatha, P. Niyomrattanakit, L. Zhang, and M. Goodwin Structure-activity relationships of antitubercular nitroimidazoles. 2. Determinants of aerobic activity and quantitative structure-activity relationships J. Med. Chem. 52 2009 1329 1344
28. P. Kim, L. Zhang, U.H. Manjunatha, R. Singh, S. Patel, J. Jiricek, T.H. Keller, H.I. Boshoff, C.E. Barry III, and C.S. Dowd Structure-activity relationships of antitubercular nitroimidazoles. 1. Structural features associated with aerobic and anaerobic activities of 4- and 5-nitroimidazoles J. Med. Chem. 52 2009 1317 1328
29. 420-dependent alcohol dehydrogenase from Methanoculleus thermophilicus Eur. J. Biochem. 239 1996 93 97 (Pubitemid 26228144)
30. H.E. Klock, E.J. Koesema, M.W. Knuth, and S.A. Lesley Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts Proteins 71 2008 982 994 (Pubitemid 351430029)
31. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268 (Pubitemid 41742778)
32. J.D. MacMicking, C. Nathan, G. Hom, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, and N. Hutchinson Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase Cell 81 1995 641 650
33. U.H. Manjunatha, H. Boshoff, C.S. Dowd, L. Zhang, T.J. Albert, J.E. Norton, L. Daniels, T. Dick, S.S. Pang, and C.E. Barry III Identification of a nitroimidazo-oxazine-specific protein involved in PA-824 resistance in Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 103 2006 431 436 (Pubitemid 43122418)
34. U.H. Manjunatha, R. Lahiri, B. Randhawa, C.S. Dowd, J.L. Krahenbuhl, and C.E. Barry III Mycobacterium leprae is naturally resistant to PA-824 Antimicrob. Agents Chemother. 50 2006 3350 3354 (Pubitemid 44527509)
35. U. Manjunatha, H.I. Boshoff, and C.E. Barry The mechanism of action of PA-824: novel insights from transcriptional profiling Commun. Integr. Biol. 2 2009 215 218
36. A. Maroz, S.S. Shinde, S.G. Franzblau, Z.K. Ma, W.A. Denny, B.D. Palmer, and R.F. Anderson Release of nitrite from the antitubercular nitroimidazole drug PA-824 and analogues upon one-electron reduction in protic, non-aqueous solvent Org. Biomol. Chem. 8 2010 413 418
37. M. Matsumoto, H. Hashizume, T. Tomishige, M. Kawasaki, H. Tsubouchi, H. Sasaki, Y. Shimokawa, and M. Komatsu OPC-67683, a nitro-dihydro-imidazooxazole derivative with promising action against tuberculosis in vitro and in mice PLoS Med. 3 2006 e466
38. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
39. P. McPhie Circular dichroism studies on proteins in films and in solution: estimation of secondary structure by g-factor analysis Anal. Biochem. 293 2001 109 119 (Pubitemid 32500512)
40. P. McPhie Concentration-independent estimation of protein secondary structure by circular dichroism: a comparison of methods Anal. Biochem. 375 2008 379 381
41. S. Mori, C. Abeygunawardana, M.O. Johnson, and P.C.M. van Zijl Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation J. Magn. Reson. B 108 1995 94 98
42. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326 (Pubitemid 27085611)
43. B.D. Palmer, A.M. Thompson, H.S. Sutherland, A. Blaser, I. Kmentova, S.G. Franzblau, B.J. Wan, Y.H. Wang, Z.K. Ma, and W.A. Denny Synthesis and structure-activity studies of biphenyl analogues of the tuberculosis drug (6S)-2-nitro-6-[4-(trifluoromethoxy)benzyl]oxy-6,7-dihydro-5H-imidazo[2,1-b][1, 3]oxazine (PA-824) J. Med. Chem. 53 2010 282 294
44. E.A. Rich, M. Torres, E. Sada, C.K. Finegan, B.D. Hamilton, and Z. Toossi Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB Tuber. Lung Dis. 78 1997 247 255 (Pubitemid 28389094)
45. B.D. Santarsiero, D.T. Yegian, C.C. Lee, G. Spraggon, J. Gu, D. Scheibe, D.C. Uber, E.W. Cornell, R.A. Nordmeyer, and W.F. Kolbe An approach to rapid protein crystallization using nanodroplets J. Appl. Crystallogr. 35 2002 278 281 (Pubitemid 34298337)
46. S.K. Sharma, and A. Mohan Multidrug-resistant tuberculosis: a menace that threatens to destabilize tuberculosis control Chest 130 2006 261 272 (Pubitemid 44116869)
47. R. Singh, U. Manjunatha, H.I.M. Boshoff, Y.H. Ha, P. Niyomrattanakit, R. Ledwidge, C.S. Dowd, I.Y. Lee, P. Kim, and L. Zhang PA-824 kills nonreplicating Mycobacterium tuberculosis by intracellular NO release Science 322 2008 1392 1395 (Pubitemid 352775253)
48. S. Sinha, S. Arora, K. Kosalai, A. Namane, A.S. Pym, and S.T. Cole Proteome analysis of the plasma membrane of Mycobacterium tuberculosis Comp. Funct. Genomics 3 2002 470 483 (Pubitemid 36054268)
49. S. Sinha, K. Kosalai, S. Arora, A. Namane, P. Sharma, A.N. Gaikwad, P. Brodin, and S.T. Cole Immunogenic membrane-associated proteins of Mycobacterium tuberculosis revealed by proteomics Microbiology 151 2005 2411 2419 (Pubitemid 40984314)
50. L. Slabinski, L. Jaroszewski, A.P.C. Rodrigues, L. Rychlewski, I.A. Wilson, S.A. Lesley, and A. Godzik The challenge of protein structure determination - lessons from structural genomics Protein Sci. 16 2007 2472 2482 (Pubitemid 350036752)
51. C.K. Stover, P. Warrener, D.R. VanDevanter, D.R. Sherman, T.M. Arain, M.H. Langhorne, S.W. Anderson, J.A. Towell, Y. Yuan, and D.N. McMurray A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis Nature 405 2000 962 966 (Pubitemid 30435054)
52. K. Suto, K. Kawagoe, N. Shibata, Y. Morimoto, Y. Higuchi, M. Kitamura, T. Nakaya, and N. Yasuoka How do the X-ray structure and the NMR structure of FMN-binding protein differ? Acta Crystallogr. D Biol. Crystallogr. 56 2000 368 371 (Pubitemid 30147194)
53. 2-dependent reductases from Mycobacteria that catalyse aflatoxin degradation Mol. Microbiol. 78 2010 561 575
54. T.C. Terwilliger Maximum-likelihood density modification Acta Crystallogr. D Biol. Crystallogr. 56 2000 965 972 (Pubitemid 30622779)
55. T.C. Terwilliger Automated main-chain model building by template matching and iterative fragment extension Acta Crystallogr. D Biol. Crystallogr. 59 2003 38 44 (Pubitemid 36117204)
56. T.C. Terwilliger, and J. Berendzen Automated MAD and MIR structure solution Acta Crystallogr. D Biol. Crystallogr. 55 1999 849 861 (Pubitemid 29194533)
57. A.M. Thompson, A. Blaser, R.F. Anderson, S.S. Shinde, S.G. Franzblau, Z.K. Ma, W.A. Denny, and B.D. Palmer Synthesis, reduction potentials, and antitubercular activity of ring A/B analogues of the bioreductive drug (6S)-2-nitro-6-[4-(trifluoromethoxy)benzyl]oxy-6,7-dihydro-5H-imidazo[2,1-b][1, 3]oxazine (PA-824) J. Med. Chem. 52 2009 637 645
58. S. Tyagi, E. Nuermberger, T. Yoshimatsu, K. Williams, I. Rosenthal, N. Lounis, W. Bishai, and J. Grosset Bactericidal activity of the nitroimidazopyran PA-824 in a murine model of tuberculosis Antimicrob. Agents Chemother. 49 2005 2289 2293 (Pubitemid 40734456)
59. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8 1995 127 134
60. + oxidoreductase with and without its substrates bound EMBO J. 20 2001 6561 6569 (Pubitemid 33134187)
61. B. Whitehead, C.J. Craven, and J.P. Waltho Double and triple resonance NMR methods for protein assignment Methods Mol. Biol. 60 1997 29 52
62. World Health Organization Global Tuberculosis Control 2011 2011 World Health Organization Geneva WHO/HTM/TB/2011.16