The role of transport mechanisms in Mycobacterium Tuberculosis drug resistance and tolerance

Pharmaceuticals

Volumn 5, Issue 11, 2012, Pages 1210-1235

  Sarathy, Jansy Passiflora ^a   Dartois, Véronique ^a,b,d   Lee, Edmund Jon Deoon ^c  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Drug transport; Efflux; Mycobacterium tuberculosis; Persistence; Porins; Resistance

Indexed keywords

AMPICILLIN; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CEFALORIDINE; CHLORAMPHENICOL; DOXORUBICIN; ERYTHROMYCIN; ETHAMBUTOL; ISONIAZID; MACROLIDE; NORFLOXACIN; NOVOBIOCIN; PORIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RESERPINE; RIFAMYCIN; STREPTOMYCIN; THIORIDAZINE; VANCOMYCIN; VERAPAMIL;

ACTIVE TRANSPORT; BACTERIAL CELL WALL; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM ISOLATE; CELL MEMBRANE PERMEABILITY; DISK DIFFUSION; DRUG RESISTANT TUBERCULOSIS; DRUG TOLERANCE; DRUG TRANSPORT; ESCHERICHIA COLI; HYDROPHOBICITY; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NON REPLICATING PERSISTENCE; NONHUMAN; PHENOTYPE; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA TYPHIMURIUM;

EID: 84869215863     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph5111210     Document Type: Review

References (140)

1. World Health Organization. Global Tuberculosis Control; WHO Press: Geneva, Switzerland, 2011.
2. World Health Organization. Tuberculosis MDR-TB & XDR-TB Progress report. WHO Press: Geneva, Switzerland, 2011.
3. Mitchison, D.A. The action of antituberculosis drugs in short-course chemotherapy. Tubercle. 1985, 66, 219-225.
4. Sacchettini, J.C.; Rubin, E.J.; Freundlich, J.S. Drugs versus bugs: in pursuit of the persistent predator Mycobacterium tuberculosis. Nat. Rev. Microbiol. 2008, 6, 41-52.
5. Chao, M.C.; Rubin, E.J. Letting sleeping dos lie: does dormancy play a role in tuberculosis? Annu. Rev. Microbiol. 2010, 64, 293-311.
6. Wayne, L.G.; Hayes, L.G. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 1996, 64, 2062-9.
7. Wayne, L.G., Sohaskey, C.D. Nonreplicating persistence of mycobacterium tuberculosis. Annu. Rev. Microbiol. 2001, 55, 139-163.
8. Kjellsson, M.C.; Via, L.E.; Goh, A.; Weiner, D.; Low, K.M.; Kern, S.; Pillai, G.; Barry, C.E. III.; Dartois, V. Penetration of anti-tuberculosis agents in rabbit pulmonary lesions: a pharmacokinetic evaluation. Antimicrob. Agents Chemother. 2011, 56, 446-457.
9. Coates, A.; Hu, Y.; Bax, R.; Page, C. The future challenges facing the development of new antimicrobial drugs. Nat. Rev. Drug Discov. 2002, 1, 895-910.
10. Lomovskaya, O.; Bostian, K.A. Practical applications and feasibility of efflux pump inhibitors in the clinic--a vision for applied use. Biochem. Pharmacol. 2006, 71, 910-918.
11. Jarlier, V.; Nikaido, H. Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol. Lett. 1994, 123, 11-18.
12. Brennan, P.J. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb). 2003, 83, 91-97.
13. Daffe, M.; Draper, P. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 1998, 39, 131-203.
14. Barry, C.E.; Crick, D.C.; McNeil, M.R. Targeting the formation of the cell wall core of M. tuberculosis. Infect. Disord. Drug Targets. 2007, 7, 182-202.
15. Barry, C.E. 3rd. Interpreting cell wall 'virulence factors' of Mycobacterium tuberculosis. Trends Microbiol. 2001, 9, 237-241.
16. Mishra, A.K.; Driessen, N.N.; Appelmelk, B.J.; Besra, G.S. Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol. Rev. 2011, 35, 1126-1157.
17. Jarlier, V.; Nikaido, H. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J. Bacteriol. 1990, 172, 1418-23.
18. Connell, N.D.; Nikaido, H. In Tuberculosis: Pathogenesis, Protection, and Control; Bloom, B. R., Ed.; ASM Press: Washington, DC, USA, 1994; Chapter 22, pp. 333-352.
19. Bhamidi, S.; Scherman, M.S.; Jones, V.; Crick, D.C.; Belisle, J.T.; Brennan, P.J.; McNeil, M.R. Detailed structural and quantitative analysis reveals the spatial organization of the cell walls of in vivo grown Mycobacterium leprae and in vitro grown Mycobacterium tuberculosis. J. Biol. Chem. 2011, 286, 23168-23177.
20. Brennan, P.J.; Nikaido, H. The envelope of mycobacteria. Annu. Rev. Biochem. 1995, 64, 29-63.
21. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67, 593-656.
22. Daffe, M.; Etienne, G. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tuber. Lung Dis. 1999, 79, 153-169.
23. Mailaender, C.; Reiling, N.; Engelhardt, H.; Bossmann, S.; Ehlers, S.; Niederweis, M. The MspA porin promotes growth and increases antibiotic susceptibility of both Mycobacterium bovis BCG and Mycobacterium tuberculosis. Microbiology. 2004, 150, 853-864.
24. rd; Besra, G.S.; Nikaido, H. Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J. Biol. Chem. 1996, 271, 29545-29551.
25. Danilchanka, O.; Pavlenok, M.; Niederweis, M. Role of porins for uptake of antibiotics by Mycobacterium smegmatis. Antimicrob. Agents Chemother. 2008, 52, 3127-3134.
26. Trias, J.; Jarlier, V.; Benz, R. Porins in the cell wall of mycobacteria. Science. 1992, 258, 1479-1481.
27. Nikaido, H.; Rosenberg, E.Y. Effect on solute size on diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J. Gen. Physiol. 1981, 77, 121-135.
28. Nikaido, H.; Vaara, M. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 1985, 49, 1-32.
29. Niederweis, M.; Ehrt, S.; Heinz, C.; Klocker, U.; Karosi, S.; Swiderek, K.M.; Riley, L.W.; Benz, R. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol. Microbiol. 1999, 33, 933-945.
30. Stahl, C.; Kubetzko, S.; Kaps, I.; Seeber, S.; Engelhardt, H.; Niederweis, M. MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 2001, 40, 451-464.
31. Stephan, J.; Mailaender, C.; Etienne, G.; Daffe, M.; Niederweis, M. Multidrug resistance of a porin deletion mutant of Mycobacterium smegmatis. Antimicrob. Agents Chemother. 2004, 48, 4163-4170.
32. Niederweis, M. Mycobacterial porins--new channel proteins in unique outer membranes. Mol. Microbiol. 2003, 49, 1167-1177.
33. Mahfoud, M.; Sukumaran, S.; Hulsmann, P.; Grieger, K.; Niederweis, M. Topology of the porin MspA in the outer membrane of Mycobacterium smegmatis. J. Biol. Chem. 2006, 281, 5908-5915.
34. Niederweis, M. In The Mycobacterial Cell Envelope; Daffe, M., Reyrat, J. M., Eds.; ASM Press: Washington, DC, U.S.A., 2008; Chapter 9, pp. 153-166.
35. Senaratne, R.H.; Mobasheri, H.; Papavinasasundaram, K.G.; Jenner, P.; Lea, E.J.; Draper, P. Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J. Bacteriol. 1998, 180, 3541-3547.
36. Teriete, P.; Yao, Y.; Kolodzik, A.; Yu, J.; Song, H.; Niederweis, M.; Marassi, F.M. Mycobacterium tuberculosis Rv0899 adopts a mixed alpha/beta-structure and does not form a transmembrane beta-barrel. Biochemistry. 2010, 49, 2768-2777.
37. Yang, Y.; Auguin, D.; Delbecq, S.; Dumas, E.; Molle, G.; Molle, V.; Roumestand, C.; Saint, N. Structure of the Mycobacterium tuberculosis OmpATb protein: a model of an oligomeric channel in the mycobacterial cell wall. Proteins 2011, 79, 645-661.
38. Song, H.; Huff, J.; Janik, K.; Walter, K.; Keller, C.; Ehlers, S.; Bossmann, S.H.; Niederweis, M. Expression of the ompATb operon accelerates ammonia secretion and adaptation of Mycobacterium tuberculosis to acidic environments. Mol. Microbiol. 2011, 80, 900-918.
39. Rohde, K.; Yates, R.M.; Purdy, G.E.; Russell, D.G. Mycobacterium tuberculosis and the environment within the phagosome. Immunol. Rev. 2007, 219, 37-54.
40. Marassi, F.M. Mycobacterium tuberculosis Rv0899 defines a family of membrane proteins widespread in nitrogen-fixing bacteria. Proteins 2011, 79, 2946-2955.
41. Song, H.; Sandie, R.; Wang, Y.; Andrade-Navarro, M.A.; Niederweis, M. Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis (Edinb) 2008, 88, 526-544.
42. Siroy, A.; Mailaender, C.; Harder, D.; Koerber, S.; Wolschendorf, F.; Danilchanka, O.; Wang, Y.; Heinz, C.; Niederweis, M. Rv1698 of Mycobacterium tuberculosis represents a new class of channel-forming outer membrane proteins. J. Biol. Chem. 2008, 283, 17827-17837.
43. Sharbati, S.; Schramm, K.; Rempel, S.; Wang, H.; Andrich, R.; Tykiel, V.; Kunisch, R.; Lewin, A. Characterisation of porin genes from Mycobacterium fortuitum and their impact on growth. BMC Microbiol. 2009, 9, 31.
44. Heinz, C.; Niederweis, M. Selective extraction and purification of a mycobacterial outer membrane protein. Anal. Biochem. 2000, 285, 113-120.
45. Engelhardt, H.; Heinz, C.; Niederweis, M. A tetrameric porin limits the cell wall permeability of Mycobacterium smegmatis. J. Biol. Chem. 2002, 277, 37567-37572.
46. Nakae, T. Identification of the outer membrane protein of E. coli that produces transmembrane channels in reconstituted vesicle membranes. Biochem. Biophys. Res. Commun. 1976, 71, 877-84.
47. Benz, R.; Orlik, F. In Bacterial and Eukaryotic Porins: Structure, Function, Mechanism; Benz, R., Ed.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2005; Chapter 8, pp. 183-212.
48. Saint, N.; Lou, K.L.; Widmer, C.; Luckey, M.; Schirmer, T.; Rosenbusch, J.P. Structural and functional characterization of OmpF porin mutants selected for larger pore size. II. Functional characterization. J. Biol. Chem. 1996, 271, 20676-20680.
49. Hancock, R.E.; Decad, G.M.; Nikaido, H. Identification of the protein producing transmembrane diffusion pores in the outer membrane of Pseudomonas aeruginosa PA01. Biochim. Biophys. Acta. 1979, 554, 323-331.
50. Benz, R.; Hancock, R.E. Properties of the large ion-permeable pores formed from protein F of Pseudomonas aeruginosa in lipid bilayer membranes. Biochim. Biophys. Acta. 1981, 646, 298-308.
51. Benz, R.; Ishii, J.; Nakae, T. Determination of ion permeability through the channels made of porins from the outer membrane of Salmonella typhimurium in lipid bilayer membranes. The J. Membr. Biol. 1980, 56, 19-29.
52. Naenna, P.; Noisumdaeng, P.; Pongpech, P.; Tribuddharat, C. Detection of outer membrane porin protein, an imipenem influx channel, in Pseudomonas aeruginosa clinical isolates. Southeast Asian J. Trop. Med. Public Health. 2010, 41, 614-624.
53. Kishii, R.; Takei, M. Relationship between the expression of ompF and quinolone resistance in Escherichia coli. J. Infect. Chemother. 2009, 15, 361-366.
54. Tavio, M.M.; Vila, J.; Ruiz, J.; Martin-Sanchez, A.M.; Jimenez de Anta, M.T. Mechanisms involved in the development of resistance to fluoroquinolones in Escherichia coli isolates. J. Antimicrob. Chemother. 1999, 44, 735-742.
55. Davin-Regli, A.; Bolla, J.M.; James, C.E.; Lavigne, J.P.; Chevalier, J.; Garnotel, E.; Molitor, A.; Pages, J.M. Membrane permeability and regulation of drug influx and efflux in enterobacterial pathogens. Curr. Drug Targets. 2008, 9, 750-759.
56. Braibant, M.; Gilot, P.; Content, J. The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol. Rev. 2000, 24, 449-467.
57. Louw, G.E.; Warren, R.M.; Gey van Pittius, N.C.; McEvoy, C.R.; van Helden, P.D.; Victor, T.C. A balancing act: efflux/influx in mycobacterial drug resistance. Antimicrobial. Agents Chemother. 2009, 53, 3181-3189.
58. Davidson, A.L.; Chen, J. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 2004, 73, 241-268.
59. Cole, S.T.; Brosch, R.; Parkhill, J.; Garnier, T.; Churcher, C.; Harris, D.; Gordon, S. V.; Eiglmeier, K.; Gas, S.; Barry, C.E., 3rd; et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998, 393, 537-544.
60. Linton, K.J.; Higgins, C.F. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 1998, 28, 5-13.
61. Li, X.Z.; Nikaido, H. Efflux-mediated drug resistance in bacteria: an update. Drugs. 2009, 69, 1555-1623.
62. Li, X.Z.; Nikaido, H. Efflux-mediated drug resistance in bacteria. Drugs. 2004, 64, 159-204.
63. Higgins, C.F. Multiple molecular mechanisms for multidrug resistance transporters. Nature. 2007, 446, 749-757.
64. Hollenstein, K.; Dawson, R.J.; Locher, K.P. Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 2007, 17, 412-418.
65. Mazurkiewicz, P.; Driessen, A.J.; Konings, W.N. What do proton motive force driven multidrug resistance transporters have in common? Curr. Issues Mol. Biol. 2005, 7, 7-21.
66. Paulsen, I.T.; Nguyen, L.; Sliwinski, M.K.; Rabus, R.; Saier, M.H. Jr. Microbial genome analyses: comparative transport capabilities in eighteen prokaryotes. J. Mol. Biol. 2000, 301, 75-100.
67. De Rossi, E.; Ainsa, J.A.; Riccardi, G. Role of mycobacterial efflux transporters in drug resistance: an unresolved question. FEMS Microbiol. Rev. 2006, 30, 36-52.
68. Zimic, M.; Fuentes, P.; Gilman, R.H.; Gutierrez, A.H.; Kirwan, D.; Sheen, P. Pyrazinoic acid efflux rate in Mycobacterium tuberculosis is a better proxy of pyrazinamide resistance. Tuberculosis (Edinb). 2012, 92, 84-91.
69. Pasca, M.R.; Guglierame, P.; Arcesi, F.; Bellinzoni, M.; De Rossi, E.; Riccardi, G. Rv2686c-Rv2687c-Rv2688c, an ABC fluoroquinolone efflux pump in Mycobacterium tuberculosis. Antimicro.b Agents Chemother. 2004, 48, 3175-3178.
70. Balganesh, M.; Kuruppath, S.; Marcel, N.; Sharma, S.; Nair, A.; Sharma, U. Rv1218c, an ABC transporter of Mycobacterium tuberculosis with implications in drug discovery. Antimicrob. Agents Chemother. 2010, 54, 5167-5172.
71. Choudhuri, B.S.; Bhakta, S.; Barik, R.; Basu, J.; Kundu, M.; Chakrabarti, P. Overexpression and functional characterization of an ABC (ATP-binding cassette) transporter encoded by the genes drrA and drrB of Mycobacterium tuberculosis. Biochem. J. 2002, 367, 279-285.
72. Pasca, M.R.; Guglierame, P.; De Rossi, E.; Zara, F.; Riccardi, G. mmpL7 gene of Mycobacterium tuberculosis is responsible for isoniazid efflux in Mycobacterium smegmatis. Antimicrob. Agents Chemother. 2005, 49, 4775-4777.
73. Ainsa, J.A.; Blokpoel, M.C.; Otal, I.; Young, D.B.; De Smet, K.A.; Martin, C. Molecular cloning and characterization of Tap, a putative multidrug efflux pump present in Mycobacterium fortuitum and Mycobacterium tuberculosis. J. Bacteriol. 1998, 180, 5836-5843.
74. Ramon-Garcia, S.; Martin, C.; Ainsa, J.A.; De Rossi, E. Characterization of tetracycline resistance mediated by the efflux pump Tap from Mycobacterium fortuitum. J. Antimicrob. Chemother. 2006, 57, 252-259.
75. Sharma, S.; Kumar, M.; Nargotra, A.; Koul, S.; Khan, I.A. Piperine as an inhibitor of Rv1258c, a putative multidrug efflux pump of Mycobacterium tuberculosis. J. Antimicrob. Chemother. 2010, 65, 1694-1701.
76. Ramon-Garcia, S.; Martin, C.; Thompson, C.J.; Ainsa, J.A. Role of the Mycobacterium tuberculosis P55 efflux pump in intrinsic drug resistance, oxidative stress responses, and growth. Antimicrob. Agents Chemother. 2009, 53, 3675-3682.
77. Silva, P.E.; Bigi, F.; Santangelo, M.P.; Romano, M.I.; Martin, C.; Cataldi, A.; Ainsa, J.A. Characterization of P55, a multidrug efflux pump in Mycobacterium bovis and Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2001, 45, 800-804.
78. Gupta, A.K.; Katoch, V.M.; Chauhan, D.S.; Sharma, R.; Singh, M.; Venkatesan, K.; Sharma, V.D. Microarray analysis of efflux pump genes in multidrug-resistant Mycobacterium tuberculosis during stress induced by common anti-tuberculous drugs. Microb. Drug Resist. 2010, 16, 21-28.
79. Doran, J.L.; Pang, Y.; Mdluli, K.E.; Moran, A.J.; Victor, T.C.; Stokes, R.W.; Mahenthiralingam, E.; Kreiswirth, B.N.; Butt, J.L.; Baron, G.S.; Treit, J.D.; Kerr, V.J.; Van Helden, P.D.; Roberts, M.C.; Nano, F.E. Mycobacterium tuberculosis efpA encodes an efflux protein of the QacA transporter family. Clin. Diagn. Lab. Immunol. 1997, 4, 23-32.
80. Colangeli, R.; Helb, D.; Sridharan, S.; Sun, J.; Varma-Basil, M.; Hazbon, M.H.; Harbacheuski, R.; Megjugorac, N.J.; Jacobs, W.R. Jr.; Holzenburg, A.; Sacchettini, J.C.; Alland, D. The Mycobacterium tuberculosis iniA gene is essential for activity of an efflux pump that confers drug tolerance to both isoniazid and ethambutol. Mol. Microbiol. 2005, 55, 1829-1840.
81. De Rossi, E.; Branzoni, M.; Cantoni, R.; Milano, A.; Riccardi, G.; Ciferri, O. mmr, a Mycobacterium tuberculosis gene conferring resistance to small cationic dyes and inhibitors. J. Bacteriol. 1998, 180, 6068-6071.
82. Dutta, N.K.; Mehra, S.; Kaushal, D.A. Mycobacterium tuberculosis sigma factor network responds to cell-envelope damage by the promising anti-mycobacterial thioridazine. PLoS ONE. 2010, 5, e10069.
83. Liu, J.; Takiff, H.E.; Nikaido, H. Active efflux of fluoroquinolones in Mycobacterium smegmatis mediated by LfrA, a multidrug efflux pump. J.Bbacteriol. 1996, 178, 3791-3795.
84. Drage, M.G.; Tsai, H.C.; Pecora, N.D.; Cheng, T.Y.; Arida, A.R.; Shukla, S.; Rojas, R.E.; Seshadri, C.; Moody, D.B.; Boom, W. H.; Sacchettini, J.C.; Harding, C.V. Mycobacterium tuberculosis lipoprotein LprG (Rv1411c) binds triacylated glycolipid agonists of Toll-like receptor 2. Nat. Struct. Mol. Biol. 2010, 17, 1088-1095.
85. Bianco, M.V.; Blanco, F.C.; Imperiale, B.; Forrellad, M.A.; Rocha, R.V.; Klepp, L.I.; Cataldi, A.A.; Morcillo, N.; Bigi, F. Role of P27 -P55 operon from Mycobacterium tuberculosis in the resistance to toxic compounds. BMC Infect. Dis. 2011, 11, 195.
86. Nguyen, L.; Thompson, C.J. Foundations of antibiotic resistance in bacterial physiology: the mycobacterial paradigm. Trends Microbiol. 2006, 14, 304-312.
87. de Steenwinkel, J.E.; de Knegt, G.J.; ten Kate, M.T.; van Belkum, A.; Verbrugh, H.A.; Kremer, K., van Soolingen, D.; Bakker-Woudenberg, I.A. Time-kill kinetics of anti-tuberculosis drugs, and emergence of resistance, in relation to metabolic activity of Mycobacterium tuberculosis. J. Antimicrob. Chemother. 2010, 65, 2582-2589.
88. Machado, D.; Couto, I.; Perdigao, J.; Rodrigues, L.; Portugal, I.; Baptista, P.; Veigas, B.; Amaral, L.; Viveiros, M. Contribution of efflux to the emergence of isoniazid and multidrug resistance in Mycobacterium tuberculosis. PLoS ONE. 2012, 7, e34538.
89. Rodrigues, L.; Machado, D.; Couto, I.; Amaral, L.; Viveiros, M. Contribution of efflux activity to isoniazid resistance in the Mycobacterium tuberculosis complex. Infect. Genet. Evol. 2012, 12, 695-700.
90. Wilson M., DeRisi J., Kristensen H.H., Imboden P., Rane S., Brown P.O., Schoolnik G.K. Exploring drug-induced alterations in gene expression in Mycobacterium tuberculosis by microarray hybridization. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 12833-12838.
91. Jiang, X.; Zhang, W.; Zhang, Y.; Gao, F.; Lu, C.; Zhang, X.; Wang, H. Assessment of efflux pump gene expression in a clinical isolate Mycobacterium tuberculosis by real-time reverse transcription PCR. Microb. Drug Resist. 2008, 14, 7-11.
92. Adams, K.N.; Takaki, K.; Connolly, L.E.; Wiedenhoft, H.; Winglee, K.; Humbert, O.; Edelstein, P.H.; Cosma, C.L.; Ramakrishnan, L. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell. 2011, 145, 39-53.
93. Louw, G.E.; Warren, R.M., Gey van Pittius, N.C., Leon, R.; Jimenez, A.; Hernandez-Pando, R.; McEvoy, C. R.; Grobbelaar, M.; Murray, M.; van Helden, P.D.; Victor, T.C. Rifampicin reduces susceptibility to ofloxacin in rifampicin-resistant Mycobacterium tuberculosis through efflux. Am. J. Respir. Crit. Care Med. 2011, 184, 269-276.
94. Nikaido, E.; Giraud, E.; Baucheron, S.; Yamasaki, S.; Wiedemann, A.; Okamoto, K.; Takagi, T.; Yamaguchi, A.; Cloeckaert, A.; Nishino, K. Effects of indole on drug resistance and virulence of Salmonella enterica serovar Typhimurium revealed by genome-wide analyses. Gut. pathogens. 2012, 4, 5.
95. McPhee, J.B.; Tamber, S.; Brazas, M.D.; Lewenza, S.; Hancock, R.E.W. In Antimicrobial Drug Resistance; Mayers, D. L., Ed.; Humana Press: New York, NY, U.S.A., 2009; Chapter 9, pp. 97-110.
96. Warner, D.M.; Shafer, W.M.; Jerse, A.E. Clinically relevant mutations that cause derepression of the Neisseria gonorrhoeae MtrC-MtrD-MtrE Efflux pump system confer different levels of antimicrobial resistance and in vivo fitness. Mol. Microbiol. 2008, 70, 462-478.
97. Maseda, H.; Hashida, Y.; Shirai, A.; Omasa, T.; Nakae, T. Mutation in the sdeS gene promotes expression of the sdeAB efflux pump genes and multidrug resistance in Serratia marcescens. Antimicrob. Agents Chemother. 2011, 55, 2922-2926.
98. Kehrenberg, C.; Cloeckaert, A.; Klein, G.; Schwarz, S. Decreased fluoroquinolone susceptibility in mutants of Salmonella serovars other than Typhimurium: detection of novel mutations involved in modulated expression of ramA and soxS. J. Antimicrob. Chemother. 2009, 64, 1175-1180.
99. Ramaswamy, S.V.; Reich, R.; Dou, S.J.; Jasperse, L.; Pan, X.; Wanger, A.; Quitugua, T.; Graviss, E.A. Single nucleotide polymorphisms in genes associated with isoniazid resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2003, 47, 1241-1250.
100. Telenti, A.; Imboden, P.; Marchesi, F.; Lowrie, D.; Cole, S.; Colston, M.J.; Matter, L.; Schopfer, K.; Bodmer, T. Detection of rifampicin-resistance mutations in Mycobacterium tuberculosis. Lancet. 1993, 341, 647-650.
101. Gengenbacher, M.; Kaufmann, S.H. Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol. Rev. 2012, 36, 514-532.
102. Betts, J.C.; Lukey, P.T.; Robb, L.C.; McAdam, R.A.; Duncan, K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 2002, 43, 717-731.
103. Gengenbacher, M.; Rao, S.P.; Pethe, K.; Dick, T. Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology. 2010, 156, 81-87.
104. Zhang, Y. Persistent and dormant tubercle bacilli and latent tuberculosis. Front. Biosci. 2004, 9, 1136-1156.
105. Herbert, D.; Paramasivan, C.N.; Venkatesan, P.; Kubendiran, G.; Prabhakar, R.; Mitchison, D.A. Bactericidal action of ofloxacin, sulbactam-ampicillin, rifampin, and isoniazid on logarithmic-and stationary-phase cultures of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 1996, 40, 2296-2299.
106. Xie, Z.; Siddiqi, N.; Rubin, E.J. Differential antibiotic susceptibilities of starved Mycobacterium tuberculosis isolates. Antimicrob. Agents Chemother. 2005, 49, 4778-4780.
107. Seiler, P.; Ulrichs, T.; Bandermann, S.; Pradl, L.; Jorg, S.; Krenn, V.; Morawietz, L.; Kaufmann, S.H.; Aichele, P. Cell-wall alterations as an attribute of Mycobacterium tuberculosis in latent infection. J. Infect. Dis. 2003, 188, 1326-1331.
108. Boon, C.; Dick, T. Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J. Bacteriol. 2002, 184, 6760-6767.
109. Park, H.D.; Guinn, K.M.; Harrell, M.I.; Liao, R.; Voskuil, M.I.; Tompa, M.; Schoolnik, G.K.; Sherman, D.R. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 2003, 48, 833-843.
110. Boon, C.; Dick, T. How Mycobacterium tuberculosis goes to sleep: the dormancy survival regulator DosR a decade later. Future Microbiol. 2012, 7, 513-518.
111. Muttucumaru, D.G.; Roberts, G.; Hinds, J.; Stabler, R.A.; Parish, T. Gene expression profile of Mycobacterium tuberculosis in a non-replicating state. Tuberculosis (Edinb). 2004, 84, 239-46.
112. Ramon-Garcia, S.; Mick, V.; Dainese, E.; Martin, C.; Thompson, C.J.; De Rossi, E.; Manganelli, R.; Ainsa, J. A. Functional and genetic characterization of the tap efflux pump in Mycobacterium bovis BCG. Antimicrob. Agents Chemother. 2012, 56, 2074-2083.
113. De la Cruz, M.A.; Calva, E. The complexities of porin genetic regulation. J. Mol. Microbiol. Biotechnol. 2010, 18, 24-36.
114. Hoffmann, C.; Leis, A.; Niederweis, M.; Plitzko, J.M.; Engelhardt, H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 3963-3967.
115. Zuber, B.; Chami, M.; Houssin, C.; Dubochet, J.; Griffiths, G.; Daffe, M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 2008, 190, 5672-5680.
116. Cunningham, A.F.; Spreadbury, C. L. Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J. Bacteriol. 1998, 180, 801-808.
117. Velayati, A.A.; Farnia, P.; Masjedi, M.R.; Zhavnerko, G.K.; Merza, M.A.; Ghanavi, J.; Tabarsi, P.; Poleschuyk, N.N.; Ignatyev, G. Sequential adaptation in latent tuberculosis bacilli: observation by atomic force microscopy (AFM). Int. J. Clin. Exp. Med. 2011, 4, 193-199.
118. Walburger, A.; Koul, A.; Ferrari, G.; Nguyen, L.; Prescianotto-Baschong, C.; Huygen, K.; Klebl, B.; Thompson, C.; Bacher, G.; Pieters, J. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science. 2004, 304, 1800-1804.
119. Meena, L. S.; Rajni. Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv. FEBS J. 2010, 277, 2416-2427.
120. Piddock, L.J.; Ricci, V. Accumulation of five fluoroquinolones by Mycobacterium tuberculosis H37Rv. J. Antimicrob. Chemother. 2001, 48, 787-791.
121. Raynaud, C.; Laneelle, M.A.; Senaratne, R.H.; Draper, P.; Laneelle, G.; Daffe, M. Mechanisms of pyrazinamide resistance in mycobacteria: importance of lack of uptake in addition to lack of pyrazinamidase activity. Microbiology. 1999, 145 (Pt 6), 1359-1367.
122. Bardou, F.; Raynaud, C.; Ramos, C.; Laneelle, M.A.; Laneelle, G. Mechanism of isoniazid uptake in Mycobacterium tuberculosis. Microbiology. 1998, 144, 2539-2544.
123. Piddock, L.J.; Williams, K. J.; Ricci, V. Accumulation of rifampicin by Mycobacterium aurum, Mycobacterium smegmatis and Mycobacterium tuberculosis. J. Antimicrob. Chemother. 2000, 45, 159-165.
124. Lipinski, C.A. Drug-like properties and the causes of poor solubility and poor permeability. J. Pharmacol. Toxicol.Methods. 2000, 44, 235-249.
125. Franklin, T.J.; Snow, G.A. In Biochemistry and Molecular Biology of Antimicrobial Drug Action; Franklin, T.J., Snow, G.A., Eds.; Springer: New York, NY, USA, 2005; Chapter 7, pp. 121-134.
126. Koul, A.; Arnoult, E.; Lounis, N.; Guillemont, J.; Andries, K. The challenge of new drug discovery for tuberculosis. Nature. 2011, 469, 483-490.
127. Zhang, Y.; Yew, W.W. Mechanisms of drug resistance in Mycobacterium tuberculosis. Int. J. Tuberc. Lung Dis. 2009, 13, 1320-1330.
128. Guillemin, I.; Sougakoff, W.; Cambau, E.; Revel-Viravau, V.; Moreau, N.; Jarlier, V. Purification and inhibition by quinolones of DNA gyrases from Mycobacterium avium, Mycobacterium smegmatis and Mycobacterium fortuitum bv. peregrinum. Microbiology. 1999, 145, 2527-2532.
129. Beggs, W.H.; Auran, N.E. Uptake and binding of 14C-ethambutol by tubercle bacilli and the relation of binding to growth inhibition. Antimicrob. Agents Chemother. 1972, 2, 390-394.
130. Zhang, Y.; Wade, M.M.; Scorpio, A.; Zhang, H.; Sun, Z. Mode of action of pyrazinamide: disruption of Mycobacterium tuberculosis membrane transport and energetics by pyrazinoic acid. J. Antimicrob. Chemother. 2003, 52, 790-795.
131. Muehlbacher, J. InSilico Profile, Version 3.2; Novartis: Basel, Switzerland, 2005.
132. Vega, A.L.D.; Delcour, A.H. Polyamines decrease Escherichia coli outer membrane permeability. J. Bacteriol. 1996, 178, 3715-3721.
133. Iyer, R.; Delcour, A.H. Complex inhibition of OmpF and OmpC bacterial porins by polyamines. J. Biol. Chem. 1997, 272, 18595-18601.
134. Dela Vega, A.L.; Delcour, A.H. Cadaverine induces closing of E. coli porins. EMBO J. 1995, 14, 6058-6065.
135. Allison, K.R.; Brynildsen, M.P.; Collins, J.J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature. 2011, 473, 216-220.
136. Bryan, L.E.; Van den Elzen, H.M. Streptomycin accumulation in susceptible and resistant strains of Escherichia coli and Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1976, 9, 928-938.
137. Bryan, L.E.; Van Den Elzen, H.M. Gentamicin accumulation by sensitive strains of Escherichia coli and Pseudomonas aeruginosa. J. Antibiot. 1975, 28, 696-703.
138. Amaral, L.; Boeree, M.J.; Gillespie, S.H.; Udwadia, Z.F.; van Soolingen, D. Thioridazine cures extensively drug-resistant tuberculosis (XDR-TB) and the need for global trials is now! Int. J. Antimicrob. Agents. 2010, 35, 524-526.
139. Amaral, L.; Martins, M.; Viveiros, M.; Molnar, J.; Kristiansen, J.E. Promising therapy of XDR-TB/MDR-TB with thioridazine an inhibitor of bacterial efflux pumps. Curr. Drug Targets. 2008, 9, 816-819.
140. Amaral, L.; Martins, M.; Viveiros, M. Enhanced killing of intracellular multidrug-resistant Mycobacterium tuberculosis by compounds that affect the activity of efflux pumps. J. Antimicrob. Chemother. 2007, 59, 1237-1246.