Substrate specificity of the deazaflavin-dependent nitroreductase from Mycobacterium tuberculosis responsible for the bioreductive activation of bicyclic nitroimidazoles

FEBS Journal

Volumn 279, Issue 1, 2012, Pages 113-125

  Gurumurthy, Meera ^a   Mukherjee, Tathagata ^b   Dowd, Cynthia S ^b,d   Singh, Ramandeep ^b,e   Niyomrattanakit, Pornwaratt ^a   Tay, Jo Ann ^a,f   Nayyar, Amit ^b   Lee, Yong Sok ^c   Cherian, Joseph ^a,g   Boshoff, Helena I ^b   Dick, Thomas ^a,h   Barry III, Clifton E ^b   Manjunatha, Ujjini H ^a  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

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

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

^e THSTI   (India)

^f AGENCY FOR SCIENCE   (Singapore)

^g ETC   (Singapore)

^h NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

F420; mycobacterium; nitroimidazole; PA 824; tuberculosis

Indexed keywords

6,7 DIHYDRO 2 NITRO 6 (4 TRIFLUOROMETHOXYBENZYLOXY) 5H IMIDAZO[2,1 B][1,3]OXAZINE; CGI 17341; DEAZAFLAVIN DEPENDENT NITROREDUCTASE; DELAMANID; NITRIC OXIDE; NITROIMIDAZOLE DERIVATIVE; NITROREDUCTASE; REACTIVE NITROGEN SPECIES; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CHEMOLUMINESCENCE; DRUG ACTIVATION; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CHEMISTRY; ENZYME KINETICS; ENZYME METABOLISM; ENZYME SPECIFICITY; LIGAND BINDING; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DOCKING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; REDUCTION; STEADY STATE; STEREOCHEMISTRY; STEREOISOMERISM; STEREOSPECIFICITY;

ANTITUBERCULAR AGENTS; CLONING, MOLECULAR; FLAVINS; KINETICS; MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE; NITROIMIDAZOLES; NITROREDUCTASES; OXAZOLES; PROTEIN CONFORMATION; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 83655167068     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08404.x     Document Type: Article

References (41)

1. WHO (2010) 2010 Global Tuberculosis Control. WHO, Geneva, Switzerland.
2. Barry CE III, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, Schnappinger D, Wilkinson RJ, &, Young D, (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7, 845-855.
3. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, Eum SY, Taylor K, Klein E, Manjunatha U, Gonzales J, et al. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76, 2333-2340.
4. Young DB, Perkins MD, Duncan K, &, Barry CE III, (2008) Confronting the scientific obstacles to global control of tuberculosis. J Clin Invest 118, 1255-1265. (Pubitemid 351500418)
5. WHO (2010) Multidrug and Extensively Drug-Resistant TB: 2010 Global Report on Surveillance and Response. WHO, Geneva, Switzerland.
6. Sharma SK, &, Mohan A, (2006) Multidrug-resistant tuberculosis: a menace that threatens to destabilize tuberculosis control. Chest 130, 261-272. (Pubitemid 44116869)
7. Lamp KC, Freeman CD, Klutman NE, &, Lacy MK, (1999) Pharmacokinetics and pharmacodynamics of the nitroimidazole antimicrobials. Clin Pharmacokinet 36, 353-373. (Pubitemid 29261511)
8. Samuelson J, (1999) Why metronidazole is active against both bacteria and parasites. Antimicrob Agents Chemother 43, 1533-1541. (Pubitemid 29331224)
9. Kokwaro GO, Ismail S, Glazier AP, Ward SA, &, Edwards G, (1993) Effect of malaria infection and endotoxin-induced fever on the metabolism of antipyrine and metronidazole in the rat. Biochem Pharmacol 45, 1243-1249. (Pubitemid 23098321)
10. Wayne LG, &, Sramek HA, (1994) Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob Agents Chemother 38, 2054-2058. (Pubitemid 24278800)
11. Barry CE, Boshoff HIM, &, Dowd CS, (2004) Prospects for clinical introduction of nitroimidazole antibiotics for the treatment of tuberculosis. Curr Pharm Des 10, 3239-3262. (Pubitemid 39276613)
12. Ashtekar DR, Costa-Perira R, Nagrajan K, Vishvanathan N, Bhatt AD, &, Rittel W, (1993) In vitro and in vivo activities of the nitroimidazole CGI 17341 against Mycobacterium tuberculosis. Antimicrob Agents Chemother 37, 183-186. (Pubitemid 23046551)
13. Nagarajan K, Shankar RG, Rajappa S, Shenoy SJ, &, Costa-Pereira R, (1989) Nitroimidazoles XXI 2,3-dihydro-6-nitroimidazo [2,1-b] oxazoles with antitubercular activity. Eur J Med Chem 24, 631-633. (Pubitemid 20025798)
14. Stover CK, Warrener P, VanDevanter DR, Sherman DR, Arain TM, Langhorne MH, Anderson SW, Towell JA, Yuan Y, McMurray DN, et al. (2000) A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 405, 962-966. (Pubitemid 30435054)
15. Matsumoto M, Hashizume H, Tomishige T, Kawasaki M, Tsubouchi H, Sasaki H, Shimokawa Y, &, Komatsu M, (2006) OPC-67683, a nitro-dihydro-imidazooxazole derivative with promising action against tuberculosis in vitro and in mice. PLoS Med 3, e466.
16. Manjunatha U, Boshoff HI, &, Barry CE, (2009) The mechanism of action of PA-824: novel insights from transcriptional profiling. Commun Integr Biol 2, 215-218.
17. Choi KP, Bair TB, Bae YM, &, Daniels L, (2001) Use of transposon Tn5367 mutagenesis and a nitroimidazopyran-based selection system to demonstrate a requirement for fbiA and fbiB in coenzyme F(420) biosynthesis by Mycobacterium bovis BCG. J Bacteriol 183, 7058-7066. (Pubitemid 33121838)
18. Choi KP, Kendrick N, &, Daniels L, (2002) Demonstration that fbiC is required by Mycobacterium bovis BCG for coenzyme F(420) and FO biosynthesis. J Bacteriol 184, 2420-2428. (Pubitemid 34311134)
19. Manjunatha UH, Boshoff H, Dowd CS, Zhang L, Albert TJ, Norton JE, Daniels L, Dick T, Pang SS, &, Barry CE III, (2006) Identification of a nitroimidazo-oxazine-specific protein involved in PA-824 resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103, 431-436. (Pubitemid 43122418)
20. Walsh C, (1986) Naturally-occurring 5-deazaflavin coenzymes-biological redox roles. Acc Chem Res 19, 216-221.
21. Singh R, Manjunatha U, Boshoff HI, Ha YH, Niyomrattanakit P, Ledwidge R, Dowd CS, Lee IY, Kim P, Zhang L, et al. (2008) PA-824 kills nonreplicating Mycobacterium tuberculosis by intracellular NO release. Science 322, 1392-1395. (Pubitemid 352775253)
22. Cellitti SE, Shaffer J, Jones DH, Mukherjee T, Gurumurthy M, Bursulaya B, Boshoff HI, Choi I, Lee YS, Cherian J, et al. (in press) Structure of Ddn, the Deazaflavin-dependent nitroreductase from Mycobacterium tuberculosis involved in bioreductive activation of PA-824. Structure, in press.
23. Kim P, Zhang L, Manjunatha UH, Singh R, Patel S, Jiricek J, Keller TH, Boshoff HI, Barry CE III, &, Dowd CS, (2009) Structure-activity relationships of antitubercular nitroimidazoles. 1. Structural features associated with aerobic and anaerobic activities of 4- and 5-nitroimidazoles. J Med Chem 52, 1317-1328.
24. Kim P, Kang S, Boshoff HI, Jiricek J, Collins M, Singh R, Manjunatha UH, Niyomrattanakit P, Patel S, Zhang L, et al. (2009) Structure-activity relationships of antitubercular nitroimidazoles. 2. Determinants of aerobic activity and quantitative structure-activity relationships. J Med Chem 52, 5770.
25. Bair TB, Isabelle DW, &, Daniels L, (2001) Structures of coenzyme F-420 in Mycobacterium species. Arch Microbiol 176, 37-43. (Pubitemid 32692642)
26. Eirich LD, Vogels GD, &, Wolfe RS, (1978) Proposed structure for coenzyme F420 from Methanobacterium. Biochemistry 17, 4583-4593. (Pubitemid 9063583)
27. Palmer BD, Thompson AM, Sutherland HS, Blaser A, Kmentova I, Franzblau SG, Wan B, Wang Y, Ma Z, &, Denny WA, (2010) 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, 282-294.
28. Kmentova I, Sutherland HS, Palmer BD, Blaser A, Franzblau SG, Wan B, Wang Y, Ma Z, Denny WA, &, Thompson AM, (2010) Synthesis and structure-activity relationships of aza- and diazabiphenyl analogues of the antitubercular 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, 8421-8439.
29. Toogood HS, Gardiner JM, &, Scrutton NS, (2010) Biocatalytic reductions and chemical versatility of the old yellow enzyme family of flavoprotein oxidoreductases. Chemcatchem 2, 892-914.
30. Ju KS, &, Parales RE, (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74, 250-272.
31. Purwantini E, &, Mukhopadhyay B, (2009) Conversion of NO2 to NO by reduced coenzyme F420 protects mycobacteria from nitrosative damage. Proc Natl Acad Sci USA 106, 6333-6338.
32. Sinha S, Kosalai K, Arora S, Namane A, Sharma P, Gaikwad AN, Brodin P, &, Cole ST, (2005) Immunogenic membrane-associated proteins of Mycobacterium tuberculosis revealed by proteomics. Microbiology 151, 2411-2419. (Pubitemid 40984314)
33. Selengut JD, &, Haft DH, (2010) Unexpected abundance of coenzyme F420-dependent enzymes in the genomes of Mycobacterium tuberculosis and other actinobacteria. J Bacteriol 192, 5788-5798.
34. Taylor MC, Jackson CJ, Tattersall DB, French N, Peat TS, Newman J, Briggs LJ, Lapalikar GV, Campbell PM, Scott C, et al. (2010) Identification and characterization of two families of F420 H2-dependent reductases from Mycobacteria that catalyse aflatoxin degradation. Mol Microbiol 78, 561-575.
35. Graham DE, (2010) A new role for coenzyme F420 in aflatoxin reduction by soil mycobacteria. Mol Microbiol 78, 533-536.
36. Sasaki H, Haraguchi Y, Itotani M, Kuroda H, Hashizume H, Tomishige T, Kawasaki M, Matsumoto M, Komatsu M, &, Tsubouchi H, (2006) Synthesis and antituberculosis activity of a novel series of optically active 6-nitro-2,3-dihydroimidazo[2,1-b]oxazoles. J Med Chem 49, 7854-7860. (Pubitemid 46033674)
37. Isabelle D, Simpson DR, &, Daniels L, (2002) Large-scale production of coenzyme F-420-5,6 by using Mycobacterium smegmatis. Appl Environ Microbiol 68, 5750-5755. (Pubitemid 35265718)
38. Leder L, Freuler F, Forstner M, &, Mayr LM, (2007) New methods for efficient protein production in drug discovery. Curr Opin Drug Discov Develop 10, 193-202. (Pubitemid 46438649)
39. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
40. Li X, Manjunatha UH, Goodwin MB, Knox JE, Lipinski CA, Keller TH, Barry CE III, &, Dowd CS, (2008) Synthesis and antitubercular activity of 7-(R)- and 7-(S)-methyl-2-nitro-6-(S)-(4-(trifluoromethoxy)benzyloxy)-6,7-dihydro-5H- imidazo[2,1-b][1,3]oxazines, analogues of PA-824. Bioorg Med Chem Lett 18, 2256-2262. (Pubitemid 351442913)
41. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Patersson GA, et al. (2009) Gaussian 09, Revision A2. Gaussian Inc., Wallingford, CT.