Lipid transport in Mycobacterium tuberculosis and its implications in virulence and drug development

Biochemical Pharmacology

Volumn 96, Issue 3, 2015, Pages 159-167

  Bailo, Rebeca ^a   Bhatt, Apoorva ^b   Aínsa, José A ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Drug resistance; Lipid transport; MmpL S proteins; Transport proteins; Tuberculosis

Indexed keywords

AMIKACIN; AMINOGLYCOSIDE; AMINOSALICYLIC ACID; BACTERIAL PROTEIN; BENZIMIDAZOLE; CAPREOMYCIN; CIPROFLOXACIN; CYCLOSERINE; ETHAMBUTOL; ETHIONAMIDE; GATIFLOXACIN; IRON; ISONIAZID PLUS PYRAZINAMIDE PLUS RIFAMPICIN; KANAMYCIN; LEVOFLOXACIN; MOXIFLOXACIN; MYCOBACTERIAL MEMBRANE PROTEIN LARGE; MYCOBACTERIAL MEMBRANE PROTEIN LARGE INHIBITOR; MYCOBACTERIAL MEMBRANE PROTEIN SMALL; N (2 ADAMANTYL) N' GERANYLETHYLENEDIAMINE; OFLOXACIN; PROTEIN INHIBITOR; PROTIONAMIDE; RIFABUTIN; RIFAPENTINE; STREPTOMYCIN; TERIZIDONE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIOMYCIN; CARRIER PROTEIN; CORD FACTOR; GLYCOLIPID; HEME; MMPL3 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; MMPL7 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; SULFOLIPID I; TREHALOSE MONOMYCOLATE; VIRULENCE FACTOR;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; HUMAN; LIPID TRANSPORT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TUBERCULOSIS; ANTAGONISTS AND INHIBITORS; CELL WALL; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; EXTENSIVELY DRUG-RESISTANT TUBERCULOSIS; GENE EXPRESSION; GENETICS; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL; VIRULENCE;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL WALL; CORD FACTORS; DRUG DESIGN; EXTENSIVELY DRUG-RESISTANT TUBERCULOSIS; GENE EXPRESSION; GLYCOLIPIDS; HEME; HUMANS; LIPID METABOLISM; MEMBRANE TRANSPORT PROTEINS; MYCOBACTERIUM TUBERCULOSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 84934872269     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.05.001     Document Type: Note

References (71)

1. A.G. Nerlich, and S. Losch Paleopathology of human tuberculosis and the potential role of climate Interdiscip. Perspect. Infect. Dis. 2009 2009 437187
2. I. Comas, M. Coscolla, T. Luo, S. Borrell, K.E. Holt, and M. Kato-Maeda Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans Nat. Genet. 45 2013 1176 1182
3. P. Supply, M. Marceau, S. Mangenot, D. Roche, C. Rouanet, and V. Khanna Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis Nat. Genet. 45 2013 172 179
4. S. Gagneux Host-pathogen coevolution in human tuberculosis Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 850 859
5. WHO. Global tuberculosis report 2014. World Health Organization, 2014.
6. A. Zumla, P. Nahid, and S.T. Cole Advances in the development of new tuberculosis drugs and treatment regimens Nat. Rev. Drug Discov. 12 2013 388 404
7. WHO/IUATLD. Anti-tuberculosis drug resistance in the world. Report no. 2. Prevalence and Trends, 2000.
8. N.R. Gandhi, A. Moll, A.W. Sturm, R. Pawinski, T. Govender, and U. Lalloo 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
9. K. Dheda, T. Gumbo, N.R. Gandhi, M. Murray, G. Theron, and Z. Udwadia Global control of tuberculosis: from extensively drug-resistant to untreatable tuberculosis Lancet Respir. Med. 2 2014 321 338
10. K.A. Cohen, W.R. Bishai, and A.S. Pym Molecular basis of drug resistance in Mycobacterium tuberculosis Microbiol. Spect. 2014 2
11. Almeida Da Silva PE, Palomino JC. Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. J. Antimicrob. Chemother. 2011;66:1417-1430.
12. H. Ouellet, J.B. Johnston, and P.R. de Montellano Cholesterol catabolism as a therapeutic target in Mycobacterium tuberculosis Trends Microbiol. 19 2011 530 539
13. M. Sani, E.N. Houben, J. Geurtsen, J. Pierson, K. de Punder, and M. van Zon Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins PLoS Pathog. 6 2010 e1000794
14. C. Hoffmann, A. Leis, M. Niederweis, J.M. Plitzko, and H. Engelhardt 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 2008 3963 3967
15. B. Zuber, M. Chami, C. Houssin, J. Dubochet, G. Griffiths, and M. Daffe Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state J. Bacteriol. 190 2008 5672 5680
16. W. Groenewald, M.S. Baird, J.A. Verschoor, D.E. Minnikin, and A.K. Croft Differential spontaneous folding of mycolic acids from Mycobacterium tuberculosis Chem. Phys. Lipids 180 2014 15 22
17. A. Lemassu, A. Ortalo-Magne, F. Bardou, G. Silve, M.A. Laneelle, and M. Daffe Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria Microbiology 142 Pt 6 1996 1513 1520
18. L.M. Lopez-Marin Nonprotein structures from mycobacteria: emerging actors for tuberculosis control Clin. Dev. Immunol. 2012 2012 917860
19. M.A. Forrellad, L.I. Klepp, A. Gioffre, Sabio, J. Garcia, H.R. Morbidoni, and M. de la Paz Santangelo Virulence factors of the Mycobacterium tuberculosis complex Virulence 4 2012 3 66
20. L.R. Camacho, D. Ensergueix, E. Perez, B. Gicquel, and C. Guilhot Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis Mol. Microbiol. 34 1999 257 267
21. A.K. Mishra, N.N. Driessen, B.J. Appelmelk, and G.S. Besra Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction FEMS Microbiol. Rev. 35 2011 1126 1157
22. X.Z. Li, and H. Nikaido Efflux-mediated drug resistance in bacteria: an update Drugs 69 2009 1555 1623
23. A.K. Pandey, and C.M. Sassetti Mycobacterial persistence requires the utilization of host cholesterol Proc. Natl. Acad. Sci. U.S.A. 105 2008 4376 4380
24. M.D. Miner, J.C. Chang, A.K. Pandey, C.M. Sassetti, and D.R. Sherman Role of cholesterol in Mycobacterium tuberculosis infection Indian J. Exp. Biol. 47 2009 407 411
25. M.A. Forrellad, M. McNeil, L. Santangelo Mde, F.C. Blanco, E. Garcia, and L.I. Klepp Role of the Mce1 transporter in the lipid homeostasis of Mycobacterium tuberculosis Tuberculosis (Edinb) 94 2014 170 177
26. O. Marjanovic, A.T. Iavarone, and L.W. Riley Sulfolipid accumulation in Mycobacterium tuberculosis disrupted in the mce2 operon J. Microbiol. 49 2011 441 447
27. I.T. Paulsen TransportDB 2002 http://www.membranetransport.org/
28. G. Lamichhane, S. Tyagi, and W.R. Bishai Designer arrays for defined mutant analysis to detect genes essential for survival of Mycobacterium tuberculosis in mouse lungs Infect. Immun. 73 2005 2533 2540
29. S.E. Converse, J.D. Mougous, M.D. Leavell, J.A. Leary, C.R. Bertozzi, and J.S. Cox MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence Proc. Natl. Acad. Sci. U.S.A. 100 2003 6121 6126
30. P. Domenech, M.B. Reed, and C.E. Barry 3rd. Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance Infect. Immun. 73 2005 3492 3501
31. J.S. Cox, B. Chen, M. McNeil, and W.R. Jacobs Jr. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice Nature 402 1999 79 83
32. P. Domenech, M.B. Reed, C.S. Dowd, C. Manca, G. Kaplan, and C.E. Barry 3rd. The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis J. Biol. Chem. 279 2004 21257 21265
33. J.M. Belardinelli, G. Larrouy-Maumus, V. Jones, L.P. Sorio de Carvalho, M.R. McNeil, and M. Jackson Biosynthesis and translocation of unsulfated acyltrehaloses in Mycobacterium tuberculosis J. Biol. Chem. 289 2014 27952 27965
34. A.E. Grzegorzewicz, H. Pham, V.A. Gundi, M.S. Scherman, E.J. North, and T. Hess Inhibition of mycolic acid transport across the Mycobacterium tuberculosis plasma membrane Nat. Chem. Biol. 8 2012 334 341
35. C. Varela, D. Rittmann, A. Singh, K. Krumbach, K. Bhatt, and L. Eggeling MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria Chem. Biol. 19 2012 498 506
36. S.A. Pacheco, F.F. Hsu, K.M. Powers, and G.E. Purdy MmpL11 protein transports mycolic acid-containing lipids to the mycobacterial cell wall and contributes to biofilm formation in Mycobacterium smegmatis J. Biol. Chem. 288 2013 24213 24222
37. C. Deshayes, H. Bach, D. Euphrasie, R. Attarian, M. Coureuil, and W. Sougakoff MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis Mol. Microbiol. 78 2010 989 1003
38. M. Jain, and J.S. Cox Interaction between polyketide synthase and transporter suggests coupled synthesis and export of virulence lipid in M. tuberculosis PLoS Pathog. 1 2005 e2
39. C. Carel, K. Nukdee, S. Cantaloube, M. Bonne, C.T. Diagne, and F. Laval Mycobacterium tuberculosis proteins involved in mycolic acid synthesis and transport localize dynamically to the old growing pole and septum PLoS One 9 2014 e97148
40. R.M. Wells, C.M. Jones, Z. Xi, A. Speer, O. Danilchanka, and K.S. Doornbos Discovery of a siderophore export system essential for virulence of Mycobacterium tuberculosis PLoS Pathog 9 2013 e1003120
41. C.P. Owens, N. Chim, A.B. Graves, C.A. Harmston, A. Iniguez, and H. Contreras The Mycobacterium tuberculosis secreted protein Rv0203 transfers heme to membrane proteins MmpL3 and MmpL11 J. Biol. Chem. 288 2013 21714 21728
42. M.V. Tullius, C.A. Harmston, C.P. Owens, N. Chim, R.P. Morse, and L.M. McMath Discovery and characterization of a unique mycobacterial heme acquisition system Proc. Natl. Acad. Sci. U.S.A. 108 2011 5051 5056
43. A. Milano, M.R. Pasca, R. Provvedi, A.P. Lucarelli, G. Manina, and A.L. Ribeiro Azole resistance in Mycobacterium tuberculosis is mediated by the MmpS5-MmpL5 efflux system Tuberculosis (Edinb) 89 2009 84 90
44. K. Andries, C. Villellas, N. Coeck, K. Thys, T. Gevers, and L. Vranckx Acquired resistance of Mycobacterium tuberculosis to bedaquiline PLoS One 9 2014 e102135
45. R.C. Hartkoorn, S. Uplekar, and S.T. Cole Cross-resistance between clofazimine and bedaquiline through upregulation of MmpL5 in Mycobacterium tuberculosis Antimicrob. Agents Chemother. 58 2014 2979 2981
46. A. Radhakrishnan, N. Kumar, C.C. Wright, T.H. Chou, M.L. Tringides, and J.R. Bolla Crystal structure of the transcriptional regulator Rv0678 of Mycobacterium tuberculosis J. Biol. Chem. 289 2014 16526 16540
47. L. Rodrigues, D. Machado, I. Couto, L. Amaral, and M. Viveiros Contribution of efflux activity to isoniazid resistance in the Mycobacterium tuberculosis complex Infect. Genet. Evol. 12 2011 695 700
48. M.R. Pasca, P. Guglierame, E. De Rossi, F. Zara, and G. Riccardi mmpL7 gene of Mycobacterium tuberculosis is responsible for isoniazid efflux in Mycobacterium smegmatis Antimicrob. Agents Chemother. 49 2005 4775 4777
49. W.X. Xu, L. Zhang, J.T. Mai, R.C. Peng, E.Z. Yang, and C. Peng The Wag31 protein interacts with AccA3 and coordinates cell wall lipid permeability and lipophilic drug resistance in Mycobacterium smegmatis Biochem. Biophys. Res. Commun. 448 2014 255 260
50. C.M. Jones, R.M. Wells, A.V. Madduri, M.B. Renfrow, C. Ratledge, and D.B. Moody Self-poisoning of Mycobacterium tuberculosis by interrupting siderophore recycling Proc. Natl. Acad. Sci. U.S.A. 111 2014 1945 1950
51. T.R. Ioerger, T. O'Malley, R. Liao, K.M. Guinn, M.J. Hickey, and N. Mohaideen Identification of new drug targets and resistance mechanisms in Mycobacterium tuberculosis PLoS One 8 2013 e75245
52. E.J. North, M. Jackson, and R.E. Lee New approaches to target the mycolic acid biosynthesis pathway for the development of tuberculosis therapeutics Curr. Pharm. Des. 20 2013 4357 4378
53. G. Riccardi, and M.R. Pasca Trends in discovery of new drugs for tuberculosis therapy J. Antibiot. (Tokyo) 67 2014 655 659
54. K. Tahlan, R. Wilson, D.B. Kastrinsky, K. Arora, V. Nair, and E. Fischer SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis Antimicrob. Agents Chemother. 56 2012 1797 1809
55. V. La Rosa, G. Poce, J.O. Canseco, S. Buroni, M.R. Pasca, and M. Biava MmpL3 is the cellular target of the antitubercular pyrrole derivative BM212 Antimicrob. Agents Chemother. 56 2011 324 331
56. S. Lun, H. Guo, O.K. Onajole, M. Pieroni, H. Gunosewoyo, and G. Chen Indoleamides are active against drug-resistant Mycobacterium tuberculosis Nat. Commun. 4 2013 2907
57. E.J. North, M.S. Scherman, D.F. Bruhn, J.S. Scarborough, M.M. Maddox, and V. Jones Design, synthesis and anti-tuberculosis activity of 1-adamantyl-3-heteroaryl ureas with improved in vitro pharmacokinetic properties Bioorg. Med. Chem. 21 2013 2587 2599
58. G. Poce, R.H. Bates, S. Alfonso, M. Cocozza, G.C. Porretta, and L. Ballell Improved BM212 MmpL3 inhibitor analogue shows efficacy in acute murine model of tuberculosis infection PLoS One 8 2013 e56980
59. S.P. Rao, S.B. Lakshminarayana, R.R. Kondreddi, M. Herve, L.R. Camacho, and P. Bifani Indolcarboxamide is a preclinical candidate for treating multidrug-resistant tuberculosis Sci. Transl. Med. 5 2013 214ra168
60. M.J. Remuinan, E. Perez-Herran, J. Rullas, C. Alemparte, M. Martinez-Hoyos, and D.J. Dow Tetrahydropyrazolo[1,5-a]pyrimidine-3-carboxamide and N-benzyl-6',7'-dihydrospiro[piperidine-4,4'-thieno[3,2-c]pyran] analogues with bactericidal efficacy against Mycobacterium tuberculosis targeting MmpL3 PLoS One 8 2013 e60933
61. M.S. Scherman, E.J. North, V. Jones, T.N. Hess, A.E. Grzegorzewicz, and T. Kasagami Screening a library of 1600 adamantyl ureas for anti-Mycobacterium tuberculosis activity in vitro and for better physical chemical properties for bioavailability Bioorg. Med. Chem. 20 2012 3255 3262
62. S.A. Stanley, S.S. Grant, T. Kawate, N. Iwase, M. Shimizu, and C. Wivagg Identification of novel inhibitors of M. tuberculosis growth using whole cell based high-throughput screening ACS Chem. Biol. 7 2012 1377 1384
63. K. Li, L.A. Schurig-Briccio, X. Feng, A. Upadhyay, V. Pujari, and B. Lechartier Multitarget drug discovery for tuberculosis and other infectious diseases J. Med. Chem. 57 2014 3126 3139
64. W. Li, A. Upadhyay, F.L. Fontes, E.J. North, Y. Wang, and D.C. Crans Novel insights into the mechanism of inhibition of MmpL3, a target of multiple pharmacophores in Mycobacterium tuberculosis Antimicrob. Agents Chemother. 58 2014 6413 6423
65. J.M. Blair, M.A. Webber, A.J. Baylay, D.O. Ogbolu, and L.J. Piddock Molecular mechanisms of antibiotic resistance Nat. Rev. Microbiol. 13 2014 42 51
66. L. Rodrigues, J.A. Ainsa, L. Amaral, and M. Viveiros Inhibition of drug efflux in mycobacteria with phenothiazines and other putative efflux inhibitors Recent Pat. Antiinfect. Drug Discov. 6 2011 118 127
67. N. Dinesh, S. Sharma, and M. Balganesh Involvement of efflux pumps in the resistance to peptidoglycan synthesis inhibitors in Mycobacterium tuberculosis Antimicrob. Agents Chemother. 57 2013 1941 1943
68. M. Balganesh, N. Dinesh, S. Sharma, S. Kuruppath, A.V. Nair, and U. Sharma Efflux pumps of Mycobacterium tuberculosis play a significant role in antituberculosis activity of potential drug candidates Antimicrob. Agents Chemother. 56 2012 2643 2651
69. M. Balganesh, S. Kuruppath, N. Marcel, S. Sharma, A. Nair, and U. Sharma Rv1218c, an ABC transporter of Mycobacterium tuberculosis with implications in drug discovery Antimicrob. Agents Chemother. 54 2010 5167 5172
70. R.E. Lee, J.G. Hurdle, J. Liu, D.F. Bruhn, T. Matt, and M.S. Scherman Spectinamides: a new class of semisynthetic antituberculosis agents that overcome native drug efflux Nat. Med. 20 2014 152 158
71. M. Viveiros, M. Martins, L. Rodrigues, D. Machado, I. Couto, and J. Ainsa Inhibitors of mycobacterial efflux pumps as potential boosters for anti-tubercular drugs Expert. Rev. Anti Infect. Ther. 10 2012 983 998