SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of mycobacterium tuberculosis

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 4, 2012, Pages 1797-1809

  Tahlan, Kapil ^a   Wilson, Regina ^b   Kastrinsky, David B ^a   Arora, Kriti ^a   Nair, Vinod ^c   Fischer, Elizabeth ^c   Whitney Barnes, S ^d   Walker, John R ^d   Alland, David ^b   Barry III, Clifton E ^a   Boshoff, Helena I ^a,e  

^a National Institute for Allergy and Infectious Disease   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

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

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

^e MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOGALACTAN; CORD FACTOR; ENZYME; MEMBRANE PROTEIN; MMPL3 PROTEIN; MYCOLIC ACID; N (2 ADAMANTYL) N' GERANYLETHYLENEDIAMINE; TREHALOSE MONOMYCOLATE; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; CELL DISRUPTION; CONTROLLED STUDY; DRUG TARGETING; ENZYME INHIBITION; ENZYME RELEASE; GENE MUTATION; GENE SEQUENCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT;

ACYLTRANSFERASES; ADAMANTANE; AEROBIOSIS; ANTIGENS, BACTERIAL; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CELL WALL; CHROMATOGRAPHY, THIN LAYER; CORD FACTORS; DRUG RESISTANCE, BACTERIAL; ETHYLENEDIAMINES; LIPID METABOLISM; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON; MUTATION; MYCOBACTERIUM TUBERCULOSIS; MYCOLIC ACIDS;

EID: 84863404695     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05708-11     Document Type: Article

References (75)

1. Alland D, Steyn AJ, Weisbrod T, Aldrich K, Jacobs WR, Jr. 2000. Characterization of the Mycobacterium tuberculosis iniBAC promoter, a promoter that responds to cell wall biosynthesis inhibition. J. Bacteriol. 182:1802-1811. (Pubitemid 30165365)
2. Backus KM, et al. 2011. Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis. Nat. Chem. Biol. 7:228-235.
3. Barry CE. 2011. Lessons from seven decades of antituberculosis drug discovery. Curr. Top. Med. Chem. 11:1216-1225.
4. Barry CE III, Blanchard JS. 2010. The chemical biology of new drugs in the development for tuberculosis. Curr. Opin. Chem. Biol. 14:456-466.
5. Barry CE III, et al. 1998. Mycolic acids: structure, biosynthesis and physiological functions. Prog. Lipid Res. 37:143-179.
6. Barry CE, Crick DC, McNeil MR. 2007. Targeting the formation of the cell wall core of M. tuberculosis. Infect. Disord. Drug Targets 7:182-202. (Pubitemid 47099127)
7. Belisle JT, et al. 1997. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276:1420-1422. (Pubitemid 27235411)
8. Bergval IL, Schuitema AR, Klatser PR, Anthony RM. 2009. Resistant mutants of Mycobacterium tuberculosis selected in vitro do not reflect the in vivo mechanism of isoniazid resistance. J. Antimicrob. Chemother. 64:515-523.
9. Besra GS, et al. 1994. Identification of the apparent carrier in mycolic acid synthesis. Proc. Natl. Acad. Sci. U. S. A. 91:12735-12739.
10. Bhatt A, Brown AK, Singh A, Minnikin DE, Besra GS. 2008. Loss of a mycobacterial gene encoding a reductase leads to an altered cell wall containing beta-oxo-mycolic acid analogs and accumulation of ketones. Chem. Biol. 15:930-939.
11. Boshoff HI, et al. 2004. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem. 279:40174-40184. (Pubitemid 39258293)
12. Brennan PJ. 2003. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 83:91-97. (Pubitemid 36683556)
13. Brennan PJ, Nikaido H. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64:29-63.
14. Camacho LR, et al. 2001. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 276:19845-19854.
15. Colangeli R, et al. 2005. The Mycobacterium tuberculosis iniA gene is essential for activity of an efflux pump that confers drug tolerance to both isoniazid and ethambutol. Mol. Microbiol. 55:1829-1840. (Pubitemid 40445216)
16. Converse SE, et al. 2003. MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc. Natl. Acad. Sci. U. S. A. 100:6121-6126. (Pubitemid 36576941)
17. Crick DC, Mahapatra S, Brennan PJ. 2001. Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology 11:107R-118R. (Pubitemid 32976343)
18. Daffe M, Draper P. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131-203. (Pubitemid 29077883)
19. De Sousa-D'Auria C, et al. 2003. New insights into the biogenesis of the cell envelope of corynebacteria: identification and functional characterization of five new mycoloyltransferase genes in Corynebacterium glutamicum. FEMS Microbiol. Lett. 224:35-44. (Pubitemid 36830820)
20. Domenech P, Reed MB, Barry CE III. 2005. Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect. Immun. 73:3492-3501. (Pubitemid 40745893)
21. Domenech P, et al. 2004. The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J. Biol. Chem. 279:21257-21265. (Pubitemid 38656531)
22. Doster B, Murray FJ, Newman R, Woolpert SF. 1973. Ethambutol in the initial treatment of pulmonary tuberculosis. U.S. Public Health Service tuberculosis therapy trials. Am. Rev. Respir. Dis. 107:177-190.
23. Draper P. 1998. The outer parts of the mycobacterial envelope as permeability barriers. Front. Biosci. 3:D1253-D1261.
24. Elkins CA, Nikaido H. 2002. Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominantly by two large periplasmic loops. J. Bacteriol. 184:6490-6498. (Pubitemid 35332552)
25. Goldman RC, et al. 2007. Programs to facilitate tuberculosis drug discovery: the tuberculosis antimicrobial acquisition and coordinating facility. Infect. Disord. Drug Targets. 7:92-104. (Pubitemid 47099122)
26. Hancock IC, Carman S, Besra GS, Brennan PJ, Waite E. 2002. Ligation of arabinogalactan to peptidoglycan in the cell wall of Mycobacterium smegmatis requires concomitant synthesis of the two wall polymers. Microbiology 148:3059-3067. (Pubitemid 35243705)
27. Heifets LB, Lindholm-Levy PJ, Flory M. 1991. Comparison of bacteriostatic and bactericidal activity of isoniazid and ethionamide against Mycobacterium avium and Mycobacterium tuberculosis. Am. Rev. Respir. Dis. 143:268-270.
28. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. 2008. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U. S. A. 105:3963-3967. (Pubitemid 351723507)
29. Hugonnet JE, Tremblay LW, Boshoff HI, Barry CE III, Blanchard JS. 2009. Meropenem-clavulanate is effective against extensively drugresistant Mycobacterium tuberculosis. Science 323:1215-1218.
30. Jackson M, et al. 1999. Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Mol. Microbiol. 31:1573-1587. (Pubitemid 29110112)
31. Jain M, Cox JS. 2005. Interaction between polyketide synthase and transporter suggests coupled synthesis and export of virulence lipid in M. tuberculosis. PLoS Pathog. 1:e2.
32. Jia L, Coward L, Gorman GS, Noker PE, Tomaszewski JE. 2005. Pharmacoproteomic effects of isoniazid, ethambutol, and N-geranyl-N′-(2- adamantyl)ethane-1,2-diamine (SQ109) on Mycobacterium tuberculosis H37Rv. J. Pharmacol. Exp. Ther. 315:905-911. (Pubitemid 41500757)
33. Jia L, et al. 2006. Interspecies pharmacokinetics and in vitro metabolism of SQ109. Br. J. Pharmacol. 147:476-485. (Pubitemid 43355045)
34. Jia L, et al. 2005. Pharmacodynamics and pharmacokinetics of SQ109, a new diamine-based antitubercular drug. Br. J. Pharmacol. 144:80-87. (Pubitemid 40192564)
35. Kastrinsky DB, McBride NS, Backus KM, LeBlanc JJ, Barry CE III. 2010. Mycolic acid/cyclopropane fatty acid/fatty acid biosynthesis and health relations, p 65-145. In Mander L, Liu H-W (ed.), Comprehensive natural products II, vol I. Elsevier Science, Amsterdam, Netherlands.
36. Kaur D, Guerin ME, Skovierova H, Brennan PJ, Jackson M. 2009. Chapter 2: biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv. Appl. Microbiol. 69:23-78.
37. Kremer L, Maughan WN, Wilson RA, Dover LG, Besra GS. 2002. The M. tuberculosis antigen 85 complex and mycolyltransferase activity. Lett. Appl. Microbiol. 34:233-237. (Pubitemid 34415692)
38. Lamichhane G, et al. 2003. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 100:7213-7218. (Pubitemid 36706418)
39. Laneelle MA, Daffe M. 2009. Transport assays and permeability in pathogenic mycobacteria. Methods Mol. Biol. 465:143-151.
40. Lange RP, Locher HH, Wyss PC, Then RL. 2007. The targets of currently used antibacterial agents: lessons for drug discovery. Curr. Pharm. Des. 13:3140-3154. (Pubitemid 350130963)
41. Lee RE, et al. 2003. Combinatorial lead optimization of [1,2]-diamines based on ethambutol as potential antituberculosis preclinical candidates. J. Comb. Chem. 5:172-187. (Pubitemid 37123511)
42. Lees AW, Tyrrell WF, Smith J, Allan GW. 1970. Ethambutol in the retreatment of chronic pulmonary tuberculosis. Br. J. Dis. Chest 64:85-89.
43. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
44. Li H, et al. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
45. Liu J, Barry CE III, Besra GS, Nikaido H. 1996. Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J. Biol. Chem. 271:29545-29551. (Pubitemid 26389573)
46. Liu J, Rosenberg EY, Nikaido H. 1995. Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc. Natl. Acad. Sci. U. S. A. 92:11254-11258.
47. Makarov V, et al. 2009. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324:801-804.
48. McClatchy JK. 1971. Mechanism of action of isoniazid on Mycobacterium bovis strain BCG. Infect. Immun. 3:530-534.
49. Mdluli K, Swanson J, Fischer E, Lee RE, Barry CE III. 1998. Mechanisms involved in the intrinsic isoniazid resistance of Mycobacterium avium. Mol. Microbiol. 27:1223-1233. (Pubitemid 28137974)
50. Mikusova K, Slayden RA, Besra GS, Brennan PJ. 1995. Biogenesis of the mycobacterial cell wall and the site of action of ethambutol. Antimicrob. Agents Chemother. 39:2484-2489.
51. Minnikin DE, Kremer L, Dover LG, Besra GS. 2002. The methylbranched fortifications of Mycobacterium tuberculosis. Chem. Biol. 9:545-553.
52. Nikaido H, Kim SH, Rosenberg EY. 1993. Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol. Microbiol. 8:1025-1030. (Pubitemid 23187021)
53. Nikaido H, Takatsuka Y. 2009. Mechanisms of RND multidrug efflux pumps. Biochim. Biophys. Acta 1794:769-781.
54. Nikonenko BV, Protopopova M, Samala R, Einck L, Nacy CA. 2007. Drug therapy of experimental tuberculosis (TB): improved outcome by combining SQ109, a new diamine antibiotic, with existing TB drugs. Antimicrob. Agents Chemother. 51:1563-1565. (Pubitemid 46586854)
55. Prideaux B, et al. 2011. High-sensitivity MALDI-MRM-MS imaging of moxifloxacin distribution in tuberculosis-infected rabbit lungs and granulomatous lesions. Anal. Chem. 83:2112-2118.
56. Protopopova M, et al. 2005. Identification of a new antitubercular drug candidate, SQ109, from a combinatorial library of 1,2-ethylenediamines. J. Antimicrob. Chemother. 56:968-974. (Pubitemid 41631930)
57. Puech V, Bayan N, Salim K, Leblon G, Daffe M. 2000. Characterization of the in vivo acceptors of the mycoloyl residues transferred by the corynebacterial PS1 and the related mycobacterial antigens 85. Mol. Microbiol. 35:1026-1041. (Pubitemid 30137773)
58. Sani M, et al. 2010. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog. 6:e1000794.
59. Sassetti CM, Boyd DH, Rubin EJ. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84. (Pubitemid 36411469)
60. Shepherd RG, et al. 1966. Structure-activity studies leading to ethambutol, a new type of antituberculous compound. Ann. N. Y. Acad. Sci. 135:686-710.
61. Slayden RA, Barry CE III. 2001. Analysis of the lipids of Mycobacterium tuberculosis. Methods Mol. Med. 54:229-245.
62. Somogyi PA, Foldes I. 1983. Incorporation of thymine, thymidine, adenine and uracil into nucleic acids of Mycobacterium phlei and its phage. Ann. Microbiol. (Paris) 134A:19-28. (Pubitemid 13184897)
63. Takayama K, Kilburn JO. 1989. Inhibition of synthesis of arabinogalactan by ethambutol in Mycobacterium smegmatis. Antimicrob. Agents Chemother. 33:1493-1499. (Pubitemid 19228001)
64. Takayama K, Wang C, Besra GS. 2005. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18:81-101. (Pubitemid 40170662)
65. Takayama K, Wang L, David HL. 1972. Effect of isoniazid on the in vivo mycolic acid synthesis, cell growth, and viability of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2:29-35.
66. Tropis M, et al. 2005. The crucial role of trehalose and structurally related oligosaccharides in the biosynthesis and transfer of mycolic acids in Corynebacterineae. J. Biol. Chem. 280:26573-26585. (Pubitemid 41022255)
67. Vilcheze C, Jacobs WR, Jr. 2007. The mechanism of isoniazid killing: clarity through the scope of genetics. Annu. Rev. Microbiol. 61:35-50. (Pubitemid 350058198)
68. Wang L, Slayden RA, Barry CE III, Liu J. 2000. Cell wall structure of a mutant of Mycobacterium smegmatis defective in the biosynthesis of mycolic acids. J. Biol. Chem. 275:7224-7229. (Pubitemid 30146273)
69. Wolucka BA. 2008. Biosynthesis of D-arabinose in mycobacteria - a novel bacterial pathway with implications for antimycobacterial therapy. FEBS J. 275:2691-2711. (Pubitemid 351678659)
70. Wong SY, et al. 2011. Mutations in gidB confer low-level streptomycin resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 55:2515-2522.
71. World Health Organization. 2010. Global tuberculosis control 2010.
72. World Health Organization. 2010. Multidrug and extensively drugresistant TB (M/XDR-TB): 2010 global report on surveillance and response. World Health Organization, Geneva, Switzerland.
73. World Health Organization. 2010. Treatment of tuberculosis: guidelines for national programmes, 4th ed. World Health Organization, Geneva, Switzerland.
74. Zhu M, et al. 2004. Pharmacokinetics of ethambutol in children and adults with tuberculosis. Int. J. Tuberc. Lung Dis. 8:1360-1367. (Pubitemid 39611583)
75. Zuber B, et al. 2008. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190:5672-5680.