Targeting persisters for tuberculosis control

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 5, 2012, Pages 2223-2230

  Zhang, Ying ^a   Yew, Wing Wai ^b   Barer, Michael R ^c  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

6,7 DIHYDRO 2 NITRO 6 (4 TRIFLUOROMETHOXYBENZYLOXY) 5H IMIDAZO[2,1 B][1,3]OXAZINE; BEDAQUILINE; CYCLOSERINE; DIETHYLDITHIOCARBAMIC ACID; ETHAMBUTOL; GATIFLOXACIN; HEAT SHOCK PROTEIN; ISONIAZID; MOXIFLOXACIN; NICLOSAMIDE; NITAZOXANIDE; OPC 68673; PYRAZINAMIDE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; RIFAMYCIN; RIFAPENTINE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; COMBINATION CHEMOTHERAPY; ENERGY YIELD; GENE EXPRESSION; HUMAN; IMMUNOTHERAPY; MOLECULARLY TARGETED THERAPY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SHORT SURVEY; TREATMENT OUTCOME; TUBERCULOSIS; TUBERCULOSIS CONTROL;

ANTITUBERCULAR AGENTS; BIOLOGICAL TRANSPORT; DRUG RESISTANCE, BACTERIAL; ENERGY METABOLISM; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR TARGETED THERAPY; MYCOBACTERIUM TUBERCULOSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; TUBERCULOSIS, PULMONARY;

EID: 84860211277     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.06288-11     Document Type: Short Survey

References (88)

1. Adams KN, et al. 2011. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145:39-53.
2. Andries K, et al. 2005. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307:223-227. (Pubitemid 40116230)
3. Barer MR. 1997. Viable but non-culturable and dormant bacteria: time to resolve an oxymoron and a misnomer? J. Med. Microbiol. 46:629-631.
4. Barer MR, Harwood CR. 1999. Bacterial viability and culturability. Adv. Microb. Physiol. 41:93-137. (Pubitemid 32756224)
5. Barry CE, III, et al. 2009. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat. Rev. Microbiol. 7:845-855.
6. Bartek IL, et al. 2009. The DosR regulon of M. tuberculosis and antibacterial tolerance. Tuberculosis (Edinb.) 89:310-316.
7. Betts J, Lukey P, Robb L, McAdam R, Duncan K. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43:717-731. (Pubitemid 34597265)
8. Bigger JW. 1944. Treatment of staphylococcal infections with penicillin. Lancet 244:497-500.
9. Bryk R, et al. 2008. Selective killing of nonreplicating mycobacteria. Cell Host Microbe 3:137-145. (Pubitemid 351325759)
10. Burman WJ, et al. 2006. Moxifloxacin versus ethambutol in the first 2 months of treatment for pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 174:331-338. (Pubitemid 44156613)
11. Byrne ST, et al. 2007. Pyrrolidine dithiocarbamate and diethyldithiocarbamate are active against growing and nongrowing persister Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 51:4495-4497. (Pubitemid 350209912)
12. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. 1999. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34:257-267. (Pubitemid 29486244)
13. Cho SH, et al. 2007. Low-oxygen-recovery assay for high-throughput screening of compounds against nonreplicating Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 51:1380-1385. (Pubitemid 46586820)
14. Cogan NG. 2006. Effects of persister formation on bacterial response to dosing. J. Theor. Biol. 238:694-703. (Pubitemid 43075584)
15. Conde MB, et al. 2009. Moxifloxacin versus ethambutol in the initial treatment of tuberculosis: a double-blind, randomised, controlled phase II trial. Lancet 373:1183-1189.
16. Connolly LE, Edelstein PH, Ramakrishnan L. 2007. Why is long-term therapy required to cure tuberculosis? PLoS Med. 4:e120.
17. Dahl JL, et al. 2003. The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc. Natl. Acad. Sci. U. S. A. 100:10026-10031. (Pubitemid 37087062)
18. Darby CM, Nathan CF. 2010. Killing of non-replicating Mycobacterium tuberculosis by 8-hydroxyquinoline. J. Antimicrob. Chemother. 65:1424-1427.
19. de Carvalho LP, Lin G, Jiang X, Nathan C. 2009. Nitazoxanide kills replicating and nonreplicating Mycobacterium tuberculosis and evades resistance. J. Med. Chem. 52:5789-5792.
20. Deb C, et al. 2009. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4:e6077.
21. Dhar N, McKinney JD. 2010. Mycobacterium tuberculosis persistence mutants identified by screening in isoniazid-treated mice. Proc. Natl. Acad. Sci. U. S. A. 107:12275-12280.
22. Dhiman RK, et al. 2009. Menaquinone synthesis is critical for maintaining mycobacterial viability during exponential growth and recovery from non-replicating persistence. Mol. Microbiol. 72:85-97.
23. Dorman SE, et al. 2009. Substitution of moxifloxacin for isoniazid during intensive phase treatment of pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 180:273-280.
24. Dorr T, Lewis K, Vulic M. 2009. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 5:e1000760.
25. Drusano GL, et al. 2010. The combination of rifampin plus moxifloxacin is synergistic for suppression of resistance but antagonistic for cell kill of Mycobacterium tuberculosis as determined in a hollow-fiber infection model. mBio 1(3):e00139-10. doi:10.1128/mBio.00139-10.
26. Fox W, Ellard GA, Mitchison DA. 1999. Studies on the treatment of tuberculosis undertaken by the British Medical Research Council tuberculosis units, 1946-1986, with relevant subsequent publications. Int. J. Tuberc. Lung Dis. 3:S231-279. (Pubitemid 29481843)
27. Gandotra S, Lebron MB, Ehrt S. 2010. The Mycobacterium tuberculosis proteasome active site threonine is essential for persistence yet dispensable for replication and resistance to nitric oxide. PLoS Pathog. 6:e1001040.
28. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S. 2007. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 13:1515-1520. (Pubitemid 350224249)
29. Garton NJ, et al. 2008. Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med. 5:e75.
30. Glickman M, Cox J, Jacobs WJ. 2000. A novel mycolic acid cyclopropane synthetase is required for coding, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 5:717-727.
31. Harper J, et al. 2012. Mouse model of necrotic tuberculosis granulomas develops hypoxic lesions. J. Infect. Dis. 205:595-602.
32. Hobby GL, Auerbach O, Lenert TF, Small MJ, Comer JV. 1954. The late emergence of M. tuberculosis in liquid cultures of pulmonary lesions resected from humans. Am. Rev. Tuberc. 70:191-218.
33. Hobby GL, Meyer K, Chaffee E. 1942. Observations on the mechanism of action of penicillin. Proc. Soc. Exp. Biol. Med. 50:281-285.
34. Hu Y, et al. 2000. Detection of mRNA transcripts and active transcription in persistent Mycobacterium tuberculosis induced by exposure to rifampin or pyrazinamide. J. Bacteriol. 182:6358-6365.
35. Ibrahim M, et al. 2007. Synergistic activity of R207910 combined with pyrazinamide against murine tuberculosis. Antimicrob. Agents Chemother. 51:1011-1015. (Pubitemid 46355288)
36. Jindani A, Dore CJ, Mitchison DA. 2003. Bactericidal and sterilizing activities of antituberculosis drugs during the first 14 days. Am. J. Respir. Crit. Care Med. 167:1348-1354. (Pubitemid 36609718)
37. Keren I, Minami S, Rubin E, Lewis K. 2011. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. mBio 2(3):e00100-11. doi:10.1128/mBio.00100-11.
38. Leung CC, Yew WW, Grosset J. 2011. Harnessing the full sterilising activity of rifamycins. Int. J. Tuberc. Lung Dis. 15:429-430.
39. Lewis K. 2008. Multidrug tolerance of biofilms and persister cells. Curr. Top. Microbiol. Immunol. 322:107-131.
40. Li Y, Zhang Y. 2007. PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob. Agents Chemother. 51:2092-2099. (Pubitemid 46903099)
41. Lin G, et al. 2009. Inhibitors selective for mycobacterial versus human proteasomes. Nature 461:621-626.
42. Lowrie DB, et al. 1999. Therapy of tuberculosis in mice by DNA vaccination. Nature 400:269-271. (Pubitemid 29334142)
43. Luidalepp H, Joers A, Kaldalu N, Tenson T. 2011. Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J. Bacteriol. 193:3598-3605.
44. Ma C, et al. 2010. Energy production genes sucB and ubiF are involved in persister survival and tolerance to multiple antibiotics and stresses in Escherichia coli. FEMS Microbiol. Lett. 303:33-40.
45. McCune RM, Feldmann FM, Lambert HP, McDermott W. 1966. Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J. Exp. Med. 123:445-468.
46. McCune RM, Feldmann FM, McDermott W. 1966. Microbial persistence. II. Characteristics of the sterile state of tubercle bacilli. J. Exp. Med. 123:469-486.
47. McCune RM, Jr, McDermott W, Tompsett R. 1956. The fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. II. The conversion of tuberculous infection to the latent state by the administration of pyrazinamide and a companion drug. J. Exp. Med. 104:763-802.
48. McCune RM, Jr, Tompsett R. 1956. Fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. I. The persistence of drug-susceptible tubercle bacilli in the tissues despite prolonged antimicrobial therapy. J. Exp. Med. 104:737-762.
49. McDermott W. 1958. Microbial persistence. Yale J. Biol. Med. 30:257-291.
50. McDermott W, McCune RM, Jr, Tompsett R. 1956. Dynamics of antituberculous chemotherapy. Am. Rev. Tuberc. 74:100-108.
51. McKinney JD, et al. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735-738.
52. Mitchison DA. 2005. The diagnosis and therapy of tuberculosis during the past 100 years. Am. J. Respir. Crit. Care Med. 171:699-706. (Pubitemid 40471139)
53. Mukamolova GV, Turapov O, Malkin J, Woltmann G, Barer MR. 2010. Resuscitation-promoting factors reveal an occult population of tubercle bacilli in sputum. Am. J. Respir. Crit. Care Med. 181:174-180.
54. Munoz-Elias EJ, McKinney JD. 2005. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11:638-644. (Pubitemid 40868304)
55. Neyrolles O, et al. 2006. Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS One 1:e43.
56. Nuermberger E, et al. 2005. Rifapentine, moxifloxacin, or DNA vaccine improves treatment of latent tuberculosis in a mouse model. Am. J. Respir. Crit. Care Med. 172:1452-1456. (Pubitemid 43069820)
57. Nuermberger E, et al. 2004. Moxifloxacin-containing regimen greatly reduces time to culture conversion in murine tuberculosis. Am. J. Respir. Crit. Care Med. 169:421-426. (Pubitemid 38134824)
58. Nuermberger EL, et al. 2004. Moxifloxacin-containing regimens of reduced duration produce a stable cure in murine tuberculosis. Am. J. Respir. Crit. Care Med. 170:1131-1134. (Pubitemid 39488628)
59. Pandey AK, Sassetti CM. 2008. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U. S. A. 105:4376-4380. (Pubitemid 351754388)
60. Pandey DP, Gerdes K. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 33:966-976. (Pubitemid 41430517)
61. Rosenthal IM, et al. 2007. Daily dosing of rifapentine cures tuberculosis in three months or less in the murine model. PLoS Med. 4:e344.
62. Rustad TR, Harrell MI, Liao R, Sherman DR. 2008. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3:e1502.
63. Rustomjee R, et al. 2008. A phase II study of the sterilising activities of ofloxacin, gatifloxacin and moxifloxacin in pulmonary tuberculosis. Int. J. Tuberc. Lung Dis. 12:128-138. (Pubitemid 351212403)
64. Sala C, et al. 2010. Simple model for testing drugs against non-replicating Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 54:4150-4158.
65. Sassetti CM, Rubin EJ. 2003. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U. S. A. 100:12989-12994. (Pubitemid 37340013)
66. Shi L, et al. 2005. Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc. Natl. Acad. Sci. U. S. A. 102:15629-15634. (Pubitemid 41528107)
67. Shi W, et al. 2011. Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis. Science 333:1630-1632.
68. Shi W, Zhang Y. 2010. PhoY2 but not PhoY1 is the PhoU homologue involved in persisters in Mycobacterium tuberculosis. J. Antimicrob. Chemother. 65:1237-1242.
69. Singh R, Barry CE III, Boshoff HI. 2010. The three RelE homologs of Mycobacterium tuberculosis have individual, drug-specific effects on bacterial antibiotic tolerance. J. Bacterial. 192:1279-1291.
70. Stallings CL, et al. 2009. CarD is an essential regulator of rRNA transcription required for Mycobacterium tuberculosis persistence. Cell 138:146-159.
71. Sun Z, Zhang Y. 1999. Antituberculosis activity of certain antifungal and antihelmintic drugs. Tuber. Lung Dis. 79:319-320. (Pubitemid 29479132)
72. Tasneen R, et al. 2011. Sterilizing activity of novel TMC207-and PA-824-containing regimens in a murine model of tuberculosis. Antimicrob. Agents Chemother. 55:5485-5492.
73. Tasneen R, Tyagi S, Williams K, Grosset J, Nuermberger E. 2008. Enhanced bactericidal activity of rifampin and/or pyrazinamide when combined with PA-824 in a murine model of tuberculosis. Antimicrob. Agents Chemother. 52:3664-3668.
74. Thibonnier M, Thiberge JM, De Reuse H. 2008. Trans-translation in Helicobacter pylori: essentiality of ribosome rescue and requirement of protein tagging for stress resistance and competence. PLoS One 3:e3810.
75. Tuberculosis Research Center Chennai. 2002. Shortening short course chemotherapy: a randomised clinical trial for treatment of smear positive pulmonary tuberculosis with regimens using ofloxacin in the intensive phase. Indian J. Tuberc. 49:27-38.
76. Tufariello JM, Chan J, Flynn JL. 2003. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect. Dis. 3:578-590. (Pubitemid 37064537)
77. Veening JW, Smits WK, Kuipers OP. 2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62:193-210.
78. Voskuil MI, Visconti KC, Schoolnik GK. 2004. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and lowoxygen dormancy. Tuberculosis (Edinb.) 84:218-227. (Pubitemid 38857854)
79. Wallis RS, et al. 1999. Drug tolerance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 43:2600-2666.
80. Wang JY, et al. 2010. Adding moxifloxacin is associated with a shorter time to culture conversion in pulmonary tuberculosis. Int. J. Tuberc. Lung Dis. 14:65-71.
81. Wayne LG, Hayes LG. 1996. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 64:2062-2069. (Pubitemid 26165667)
82. Yew WW, Cynamon M, Zhang Y. 2011. Emerging drugs for the treatment of tuberculosis. Expert Opin. Emerg. Drugs. 16:1-21.
83. Zhang Y. 2007. Advances in the treatment of tuberculosis. Clin. Pharmacol. Ther. 82:595-600. (Pubitemid 47622532)
84. Zhang Y. 2005. The magic bullets and tuberculosis drug targets. Annu. Rev. Pharmacol. Toxicol. 45:529-564. (Pubitemid 40261816)
85. Zhang Y. 2004. Persistent and dormant tubercle bacilli and latent tuberculosis. Front. Biosci. 9:1136-1156. (Pubitemid 39060834)
86. Zhang Y, Mitchison D. 2003. The curious characteristics of pyrazinamide: a review. Int. J. Tuberc. Lung Dis. 7:6-21. (Pubitemid 36427026)
87. Zhang Y, Wade MM, Scorpio A, Zhang H, Sun Z. 2003. Mode of action of pyrazinamide: disruption of Mycobacterium tuberculosis membrane transport and energetics by pyrazinoic acid. J. Antimicrob. Chemother. 52:790-795. (Pubitemid 37407806)
88. Zhang Y, Yang Y, Woods A, Cotter RJ, Sun Z. 2001. Resuscitation of dormant Mycobacterium tuberculosis by phospholipids or specific peptides. Biochem. Biophys. Res. Commun. 284:542-547. (Pubitemid 32918012)