Characterization of DprE1-mediated benzothiazinone resistance in Mycobacterium tuberculosis

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 11, 2016, Pages 6451-6459

  Foo, Caroline Shi Yan ^a   Lechartier, Benoit ^a,b   Kolly, Gaëlle S ^a   Boy Röttger, Stefanie ^a   Neres, João ^a,c   Rybniker, Jan ^a,d   Lupien, Andréanne ^a   Sala, Claudia ^a   Piton, Jérémie ^a   Cole, Stewart T ^a  

^a EPFL   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UCB PHARMA   (Belgium)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BENZOTHIAZINE DERIVATIVE; BENZOTHIAZINONE; CYSTEINE; DECAPRENYLPHOSPHORYL DEXTRO RIBOSE OXIDASE; UNCLASSIFIED DRUG; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEIN; DPRE1 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; ENZYME INHIBITOR; PBTZ169; PIPERAZINE DERIVATIVE; THIAZINE DERIVATIVE; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BIOCHEMICAL ANALYSIS; CATALYTIC EFFICIENCY; CODON; CONTROLLED STUDY; COVALENT BOND; CYTOTOXICITY; ENZYMATIC ASSAY; EX VIVO STUDY; GENE MUTATION; GROWTH RATE; IN VITRO STUDY; MACROPHAGE; MUTANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SOLID; AMINO ACID SUBSTITUTION; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR DOCKING; MULTIDRUG RESISTANCE; MULTIDRUG RESISTANT TUBERCULOSIS; MUTATION; MYCOBACTERIUM SMEGMATIS; STRUCTURE ACTIVITY RELATION;

ALCOHOL OXIDOREDUCTASES; AMINO ACID SUBSTITUTION; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CELL LINE; CYSTEINE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENZYME INHIBITORS; GENE EXPRESSION; HUMANS; MACROPHAGES; MOLECULAR DOCKING SIMULATION; MUTAGENESIS, SITE-DIRECTED; MUTATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PIPERAZINES; STRUCTURE-ACTIVITY RELATIONSHIP; THIAZINES; TUBERCULOSIS, MULTIDRUG-RESISTANT;

EID: 84995404820     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01523-16     Document Type: Article

References (35)

1. WHO. 2015. Global tuberculosis report 2015. WHO, Geneva, Switzerland.
2. Makarov V, Manina G, Mikusova K, Mollmann U, Ryabova O, Saint- Joanis B, Dhar N, Pasca MR, Buroni S, Lucarelli AP, Milano A, De Rossi E, Belanova M, Bobovska A, Dianiskova P, Kordulakova J, Sala C, Fullam E, Schneider P, McKinney JD, Brodin P, Christophe T, Waddell S, Butcher P, Albrethsen J, Rosenkrands I, Brosch R, Nandi V, Bharath S, Gaonkar S, Shandil RK, Balasubramanian V, Balganesh T, Tyagi S, Grosset J, Riccardi G, Cole ST. 2009. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324: 801-804. http://dx.doi.org/10.1126/science.1171583.
3. Pasca MR, Degiacomi G, de Jesus Lopes Ribeiro AL, Zara F, De Mori P, Heym B, Mirrione M, Brerra R, Pagani L, Pucillo L, Troupioti P, Makarov V, Cole ST, Riccardi G. 2010. Clinical isolates of Mycobacterium tuberculosis in four European hospitals are uniformly susceptible to benzothiazinones. Antimicrob Agents Chemother 54: 1616-1618. http://dx.doi.org/10.1128/AAC.01676-09.
4. Makarov V, Lechartier B, Zhang M, Neres J, van der Sar AM, Raadsen SA, Hartkoorn RC, Ryabova OB, Vocat A, Decosterd LA, Widmer N, Buclin T, Bitter W, Andries K, Pojer F, Dyson PJ, Cole ST. 2014. Towards a new combination therapy for tuberculosis with next generation benzothiazinones. EMBO Mol Med 6: 372-383. http://dx.doi.org/10.1002/emmm.201303575.
5. Working Group on New TB Drugs. 2015. Drug pipeline. Stop TB Partnership, Geneva, Switzerland. http://www.newtbdrugs.org/pipeline.php. Accessed 22 November 2015.
6. Mikusova K, Huang H, Yagi T, Holsters M, Vereecke D, D'Haeze W, Scherman MS, Brennan PJ, McNeil MR, Crick DC. 2005. Decaprenylphosphoryl arabinofuranose, the donor of the D-arabinofuranosyl residues of mycobacterial arabinan, is formed via a two-step epimerization of decaprenylphosphoryl ribose. J Bacteriol 187: 8020-8025. http://dx.doi .org/10.1128/JB.187.23.8020-8025.2005.
7. Trefzer C, Rengifo-Gonzalez M, Hinner MJ, Schneider P, Makarov V, Cole ST, Johnsson K. 2010. Benzothiazinones: Prodrugs that covalently modify the decaprenylphosphoryl-D-ribose 2=-epimerase DprE1 of Mycobacterium tuberculosis. JAmChem Soc 132: 13663-13665. http://dx .doi.org/10.1021/ja106357w.
8. Trefzer C, Škovierová H, Buroni S, Bobovská A, Nenci S, Molteni E, Pojer F, Pasca MR, Makarov V, Cole ST, Riccardi G, Mikušová K, Johnsson K. 2012. Benzothiazinones are suicide inhibitors of mycobacterial decaprenylphosphoryl-D-ribofuranose 2=-oxidase DprE1. J Am Chem Soc 134: 912-915. http://dx.doi.org/10.1021/ja211042r.
9. Neres J, Pojer F, Molteni E, Chiarelli LR, Dhar N, Boy-Rottger S, Buroni S, Fullam E, Degiacomi G, Lucarelli AP, Read RJ, Zanoni G, Edmondson DE, De Rossi E, Pasca MR, McKinney JD, Dyson PJ, Riccardi G, Mattevi A, Cole ST, Binda C. 2012. Structural basis for benzothiazinone-mediated killing of Mycobacterium tuberculosis. Sci Transl Med 4: 150ra121. http://dx.doi.org/10.1126/scitranslmed.3004395.
10. Batt SM, Jabeen T, Bhowruth V, Quill L, Lund PA, Eggeling L, Alderwick LJ, Futterer K, Besra GS. 2012. Structural basis of inhibition of Mycobacterium tuberculosis DprE1 by benzothiazinone inhibitors. Proc Natl Acad Sci U S A 109: 11354-11359. http://dx.doi.org/10.1073/pnas .1205735109.
11. Brecik M, Centárová I, Mukherjee R, Kolly GS, Huszár S, Bobovská A, Kilacsková E, Mokošová V, Svetlikova Z, Šarkan M, Neres J, Korduláková J, Cole ST, Mikušová K. 29 April 2015. DprE1 is a vulnerable tuberculosis drug target due to its cell wall localization. ACS Chem Biol http://dx.doi.org/10.1021/acschembio.5b00237.
12. Magnet S, Hartkoorn RC, Székely R, Pató J, Triccas JA, Schneider P, Szántai-Kis C,O? rfi L, Chambon M, Banfi D, Bueno M, Turcatti G, Kéri G, Cole ST. 2010. Leads for antitubercular compounds from kinase inhibitor library screens. Tuberculosis 90: 354-360. http://dx.doi.org/10 .1016/j.tube.2010.09.001.
13. Stanley SA, Grant SS, Kawate T, Iwase N, Shimizu M, Wivagg C, Silvis M, Kazyanskaya E, Aquadro J, Golas A, Fitzgerald M, Dai H, Zhang L, Hung DT. 2012. Identification of novel inhibitors of M. tuberculosis growth using whole cell based high-throughput screening. ACS Chem Biol 7: 1377-1384. http://dx.doi.org/10.1021/cb300151m.
14. Wang F, Sambandan D, Halder R, Wang J, Batt SM, Weinrick B, Ahmad I, Yang P, Zhang Y, Kim J, Hassani M, Huszar S, Trefzer C, Ma Z, Kaneko T, Mdluli KE, Franzblau S, Chatterjee AK, Johnsson K, Mikusova K, Besra GS, Fütterer K, Robbins SH, Barnes SW, Walker JR, Jacobs WR, Schultz PG. 2013. Identification of a small molecule with activity against drug-resistant and persistent tuberculosis. Proc Natl Acad Sci U S A 110: E2510-E2517. http://dx.doi.org/10.1073/pnas.1309171110.
15. Shirude PS, Shandil R, Sadler C, Naik M, Hosagrahara V, Hameed S, Shinde V, Bathula C, Humnabadkar V, Kumar N, Reddy J, Panduga V, Sharma S, Ambady A, Hegde N, Whiteaker J, McLaughlin RE, Gardner H, Madhavapeddi P, Ramachandran V, Kaur P, Narayan A, Guptha S, Awasthy D, Narayan C, Mahadevaswamy J, Vishwas KG, Ahuja V, Srivastava A, Prabhakar K, Bharath S, Kale R, Ramaiah M, Choudhury NR, Sambandamurthy VK, Solapure S, Iyer PS, Narayanan S, Chatterji M. 2013. Azaindoles: Noncovalent DprE1 inhibitors from scaffold morphing efforts, kill Mycobacterium tuberculosis and are efficacious in vivo. J Med Chem 56: 9701-9708. http://dx.doi.org/10.1021/jm401382v.
16. Panda M, Ramachandran S, Ramachandran V, Shirude PS, Humnabadkar V, Nagalapur K, Sharma S, Kaur P, Guptha S, Narayan A, Mahadevaswamy J, Ambady A, Hegde N, Rudrapatna SS, Hosagrahara VP, Sambandamurthy VK, Raichurkar A. 2014. Discovery of pyrazolopyridones as a novel class of non-covalent dpre1 inhibitor with potent anti-mycobacterial activity. J Med Chem 57: 4761-4771. http://dx.doi.org/10.1021/jm5002937.
17. Naik M, Humnabadkar V, Tantry SJ, Panda M, Narayan A, Guptha S, Panduga V, Manjrekar P, Jena LK, Koushik K, Shanbhag G, Jatheendranath S, Manjunatha MR, Gorai G, Bathula C, Rudrapatna S, Achar V, Sharma S, Ambady A, Hegde N, Mahadevaswamy J, Kaur P, Sambandamurthy VK, Awasthy D, Narayan C, Ravishankar S, Madhavapeddi P, Reddy J, Prabhakar K, Saralaya R, Chatterji M, Whiteaker J, McLaughlin B, Chiarelli LR, Riccardi G, Pasca MR, Binda C, Neres J, Dhar N, Signorino-Gelo F, McKinney JD, Ramachandran V, Shandil R, Tommasi R, Iyer PS, Narayanan S, Hosagrahara V, Kavanagh S, Dinesh N, Ghorpade SR. 2014. 4-Aminoquinolone piperidine amides: Noncovalent inhibitors of DprE1 with long residence time and potent antimycobacterial activity. J Med Chem 57: 5419-5434. http://dx.doi.org/10.1021/jm5005978.
18. Neres J, Hartkoorn RC, Chiarelli LR, Gadupudi R, Pasca MR, Mori G, Venturelli A, Savina S, Makarov V, Kolly GS, Molteni E, Binda C, Dhar N, Ferrari S, Brodin P, Delorme V, Landry V, de Jesus Lopes Ribeiro AL, Farina D, Saxena P, Pojer F, Carta A, Luciani R, Porta A, Zanoni G, De Rossi E, Costi MP, Riccardi G, Cole ST. 2015. 2-Carboxyquinoxalines kill Mycobacterium tuberculosis through noncovalent inhibition of DprE1. ACS Chem Biol 10: 705-714. http://dx.doi.org/10.1021/cb5007163.
19. Palomino J-C, Martin A, Camacho M, Guerra H, Swings J, Portaels F. 2002. Resazurin microtiter assay plate: Simple and inexpensive method for detection of drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 46: 2720-2722. http://dx.doi.org/10.1128/AAC.46.8 .2720-2722.2002.
20. van Kessel JC, Marinelli LJ, Hatfull GF. 2008. Recombineering myco- bacteria and their phages. Nat Rev Microbiol 6: 851-857. http://dx.doi.org/10.1038/nrmicro2014.
21. Rybniker J, Vocat A, Sala C, Busso P, Pojer F, Benjak A, Cole ST. 2015. Lansoprazole is an antituberculous prodrug targeting cytochrome bc1. Nat Commun 6: 7659. http://dx.doi.org/10.1038/ncomms8659.
22. Van Durme J, Delgado J, Stricher F, Serrano L, Schymkowitz J, Rousseau F. 2011. A graphical interface for the FoldX forcefield. Bioinformatics 27: 1711-1712. http://dx.doi.org/10.1093/bioinformatics/btr254.
23. Krieger E, Vriend G. 2014. YASARA View-molecular graphics for all devices-from smartphones to workstations. Bioinformatics 30: 2981-2982. http://dx.doi.org/10.1093/bioinformatics/btu426.
24. Schrödinger LLC. 2015. The PyMOL molecular graphics system, version 1.8. Schrödinger, LLC, Cambridge, MA.
25. Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. 2012. Predicting the functional effect of amino acid substitutions and indels. PLoS One 7: E46688. http://dx.doi.org/10.1371/journal.pone.0046688.
26. Choi Y, Chan AP. 2015. PROVEAN Web server: A tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 31: 2745-2747. http://dx.doi.org/10.1093/bioinformatics/btv195.
27. Kolly GS, Mukherjee R, Kilacsková E, Abriata LA, Raccaud M, Blaško J, Sala C, Dal Peraro M, Mikušová K, Cole ST. 2015. GtrA protein Rv3789 is required for arabinosylation of arabinogalactan in Mycobacterium tuberculosis. J Bacteriol 197: 3686-3697. http://dx.doi.org/10.1128/JB.00628-15.
28. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, Morin PM, Marks CB, Padiyar J, Goulding C, Gingery M. 2003. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci U S A 100: 12420-12425. http://dx.doi.org/10.1073/pnas.1635213100.
29. Lechartier B, Hartkoorn RC, Cole ST. 2012. In vitro combination studies of benzothiazinone lead compound BTZ043 against Mycobacterium tuberculosis. Antimicrob Agents Chemother 56: 5790-5793. http://dx.doi .org/10.1128/AAC.01476-12.
30. Riccardi G, Pasca MR, Chiarelli LR, Manina G, Mattevi A, Binda C. 2013. The DprE1 enzyme, one of the most vulnerable targets of Mycobacterium tuberculosis. Appl Microbiol Biotechnol 97: 8841-8848. http://dx .doi.org/10.1007/s00253-013-5218-x.
31. Mikusova K, Makarov V, Neres J. 2013. DprE1-from the discovery to the promising tuberculosis drug target. Curr Pharm Des 20: 4379-4403. http://dx.doi.org/10.2174/138161282027140630122724.
32. Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. 2004. Mycobacterium tuberculosis phagosome maturation arrest: Mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15: 751-760. http://dx.doi.org/10 .1091/mbc.E03-05-0307.
33. Amin AG, Goude R, Shi L, Zhang J, Chatterjee D, Parish T. 2008. EmbA is an essential arabinosyltransferase in Mycobacterium tuberculosis. Microbiology 154: 240-248. http://dx.doi.org/10.1099/mic.0 .2007/012153-0.
34. Chatterji M, Shandil R, Manjunatha MR, Solapure S, Ramachandran V, Kumar N, Saralaya R, Panduga V, Reddy J, Prabhakar KR, Sharma S, Sadler C, Cooper CB, Mdluli K, Iyer PS, Narayanan S, Shirude PS. 2014. 1,4-Azaindole, a potential drug candidate for treatment of tuberculosis. Antimicrob Agents Chemother 58: 5325-5331. http://dx.doi.org/10 .1128/AAC.03233-14.
35. Lambert RJW, Pearson J. 2000. Susceptibility testing: Accurate and reproducible minimum inhibitory concentration (MIC) and noninhibitory concentration (NIC) values. Journal of Applied Microbiology 88: 784-790. http://dx.doi.org/10.1046/j.1365-2672.2000.01017.x .