Mycolic Acid Cyclopropanation is Essential for Viability, Drug Resistance, and Cell Wall Integrity of Mycobacterium tuberculosis

Chemistry and Biology

Volumn 16, Issue 5, 2009, Pages 499-509

  Barkan, Daniel ^a   Liu, Zhen ^b   Sacchettini, James C ^b   Glickman, Michael S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

CHEMBIO; MICROBIO

Indexed keywords

AMINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CMAA2 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; CYCLOPROPANE DERIVATIVE; METHYLTRANSFERASE; MYCOLIC ACID; OCTYLAMINE;

ANTIBIOTIC RESISTANCE; ARTICLE; CELL WALL; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; STRUCTURE ACTIVITY RELATION;

AMINES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL WALL; CYCLOPROPANES; DRUG RESISTANCE, BACTERIAL; METHYLTRANSFERASES; MYCOBACTERIUM TUBERCULOSIS; MYCOLIC ACIDS; PHENOTYPE; STRUCTURE-ACTIVITY RELATIONSHIP;

MYCOBACTERIUM TUBERCULOSIS;

EID: 65749086909     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2009.04.001     Document Type: Article

References (41)

1. Alahari A., Trivelli X., Guerardel Y., Dover L.G., Besra G.S., Sacchettini J.C., Reynolds R.C., Coxon G.D., and Kremer L. Thiacetazone, an antitubercular drug that inhibits cyclopropanation of cell wall mycolic acids in mycobacteria. PLoS ONE 2 (2007) e1343
2. Alahari A., Alibaud L., Trivelli X., Gupta R., Lamichhane G., Reynolds R.C., Bishai W.R., Guerardel Y., and Kremer L. Mycolic acid methyltransferase, MmaA4, is necessary for thiacetazone susceptibility in Mycobacterium tuberculosis. Mol. Microbiol. 71 (2009) 1263-1277
3. Arora P., Goyal A., Natarajan V.T., Rajakumara E., Verma P., Gupta R., Yousuf M., Trivedi O.A., Mohanty D., Tyagi A., et al. Mechanistic and functional insights into fatty acid activation in Mycobacterium tuberculosis. Nat. Chem. Biol. 5 (2009) 166-173
4. Bao X., Katz S., Pollard M., and Ohlrogge J. Carbocyclic fatty acids in plants: biochemical and molecular genetic characterization of cyclopropane fatty acid synthesis of Sterculiafoetida. Proc. Natl. Acad. Sci. USA 99 (2002) 7172-7177
5. Barry III C.E., Lee R.E., Mdluli K., Sampson A.E., Schroeder B.G., Slayden R.A., and Yuan Y. Mycolic acids: structure, biosynthesis and physiological functions. Prog. Lipid Res. 37 (1998) 143-179
6. Behr M.A., Schroeder B.G., Brinkman J.N., Slayden R.A., and Barry III C.E. A point mutation in the mma3 gene is responsible for impaired methoxymycolic acid production in Mycobacterium bovis BCG strains obtained after 1927. J. Bacteriol. 182 (2000) 3394-3399
7. Belley A., Alexander D., Di Pietrantonio T., Girard M., Jones J., Schurr E., Liu J., Sherman D.R., and Behr M.A. Impact of methoxymycolic acid production by Mycobacterium bovis BCG vaccines. Infect. Immun. 72 (2004) 2803-2809
8. Bhatt A., Fujiwara N., Bhatt K., Gurcha S.S., Kremer L., Chen B., Chan J., Porcelli S.A., Kobayashi K., Besra G.S., et al. Deletion of kasB in Mycobacterium tuberculosis causes loss of acid-fastness and subclinical latent tuberculosis in immunocompetent mice. Proc. Natl. Acad. Sci. USA 104 (2007) 5157-5162
9. Chevalier J., Mallea M., and Pages J.M. Comparative aspects of the diffusion of norfloxacin, cefepime and spermine through the F porin channel of Enterobacter cloacae. Biochem. J. 348 (2000) 223-227
10. Dao D.N., Sweeney K., Hsu T., Gurcha S.S., Nascimento I.P., Roshevsky D., Besra G.S., Chan J., Porcelli S.A., and Jacobs W.R. Mycolic acid modification by the mmaA4 gene of M. tuberculosis modulates IL-12 production. PLoS Pathog. 4 (2008) e1000081
11. Dubnau E., Marrakchi H., Smith I., Daffe M., and Quemard A. Mutations in the cmaB gene are responsible for the absence of methoxymycolic acid in Mycobacterium bovis BCG Pasteur. Mol. Microbiol. 29 (1998) 1526-1528
12. Dubnau E., Chan J., Raynaud C., Mohan V.P., Laneelle M.A., Yu K., Quemard A., Smith I., and Daffe M. Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol. Microbiol. 36 (2000) 630-637
13. Dye C. Global epidemiology of tuberculosis. Lancet 367 (2006) 938-940
14. Gandhi N.R., Moll A., Sturm A.W., Pawinski R., Govender T., Lalloo U., Zeller K., Andrews J., and Friedland G. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368 (2006) 1575-1580
15. George K.M., Yuan Y., Sherman D.R., and Barry III C.E. The biosynthesis of cyclopropanated mycolic acids in Mycobacterium tuberculosis. Identification and functional analysis of CMAS-2. J. Biol. Chem. 270 (1995) 27292-27298
16. Glickman M.S. The mmaA2 gene of Mycobacterium tuberculosis encodes the distal cyclopropane synthase of the alpha-mycolic acid. J. Biol. Chem. 278 (2003) 7844-7849
17. Glickman M.S., Cox J.S., and Jacobs Jr. W.R. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 5 (2000) 717-727
18. Glickman M.S., Cahill S.M., and Jacobs Jr. W.R. The Mycobacterium tuberculosis cmaA2 gene encodes a mycolic acid trans-cyclopropane synthetase. J. Biol. Chem. 276 (2001) 2228-2233
19. Grogan D.W., and Cronan Jr. J.E. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61 (1997) 429-441
20. Guianvarc'h D., Drujon T., Leang T.E., Courtois F., and Ploux O. Identification of new inhibitors of E. coli cyclopropane fatty acid synthase using a colorimetric assay. Biochim. Biophys. Acta 1764 (2006) 1381-1388
21. Huang C.C., Smith C.V., Glickman M.S., Jacobs Jr. W.R., and Sacchettini J.C. Crystal structures of mycolic acid cyclopropane synthases from Mycobacterium tuberculosis. J. Biol. Chem. 277 (2002) 11559-11569
22. Liu J., Takiff H.E., and Nikaido H. Active efflux of fluoroquinolones in Mycobacterium smegmatis mediated by LfrA, a multidrug efflux pump. J. Bacteriol. 178 (1996) 3791-3795
23. Lozada-Ramirez J.D., Martinez-Martinez I., Sanchez-Ferrer A., and Garcia-Carmona F. A colorimetric assay for S-adenosylhomocysteine hydrolase. J. Biochem. Biophys. Methods 67 (2006) 131-140
24. Makinoshima H., and Glickman M.S. Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature 436 (2005) 406-409
25. McGarrity J.T., and Armstrong J.B. Phase transition behaviour of artificial liposomes composed of phosphatidylcholines acylated with cyclopropane fatty acids. Biochim. Biophys. Acta 640 (1981) 544-548
26. McRee D.E. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
27. Mdluli K., and Spigelman M. Novel targets for tuberculosis drug discovery. Curr. Opin. Pharmacol. 6 (2006) 459-467
28. Otwinowski Z., and Minor W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
29. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
30. Nagamachi E., Shibuya S., Hirai Y., Matsushita O., Tomochika K., and Kanemasa Y. Adaptational changes of fatty acid composition and the physical state of membrane lipids following the change of growth temperature in Yersinia enterocolitica. Microbiol. Immunol. 35 (1991) 1085-1093
31. Pashley C.A., and Parish T. Efficient switching of mycobacteriophage L5-based integrating plasmids in Mycobacterium tuberculosis. FEMS Microbiol. Lett. 229 (2003) 211-215
32. Payne D.J., Gwynn M.N., Holmes D.J., and Pompliano D.L. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 6 (2007) 29-40
33. Quemard A., Laneelle M.-A., Marrakchi H., Prome D., Dubnau E., and Daffe M. Structure of a hydroxymycolic acid potentially involved in the synthesis of oxygenated mycolic acids of the Mycobacterium tuberculosis complex. Eur. J. Biochem. 250 (1997) 758-763
34. Rao V., Fujiwara N., Porcelli S.A., and Glickman M.S. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J. Exp. Med. 201 (2005) 535-543
35. Rao V., Gao F., Chen B., Jacobs Jr. W.R., and Glickman M.S. Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J. Clin. Invest. 116 (2006) 1660-1667
36. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
37. Watanabe M., Aoyagi Y., Ridell M., and Minnikin D.E. Separation and characterization of individual mycolic acids in representative mycobacteria. Microbiology 147 (2001) 1825-1837
38. Watanabe M., Aoyagi Y., Mitome H., Fujita T., Naoki H., Ridell M., and Minnikin D.E. Location of functional groups in mycobacterial meromycolate chains; the recognition of new structural principles in mycolic acids. Microbiology 148 (2002) 1881-1902
39. World Health Organization. Anti-Tuberculosis Drug Resistance in the World. Fourth Global Report (2008), WHO Press, Geneva, Switzerland
40. Yuan Y., Zhu Y., Crane D.D., and Barry III C.E. The effect of oxygenated mycolic acid composition on cell wall function and macrophage growth in Mycobacterium tuberculosis. Mol. Microbiol. 29 (1998) 1449-1458
41. Zwart P.H., Afonine P.V., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., McKee E., Moriarty N.W., Read R.J., Sacchettini J.C., et al. Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426 (2008) 419-435