Targeting dormant bacilli to fight tuberculosis

Mediterranean Journal of Hematology and Infectious Diseases

Volumn 5, Issue 1, 2013, Pages

  Fattorini, Lanfranco ^a   Piccaro, Giovanni ^a   Mustazzolu, Alessandro ^a   Giannoni, Federico ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ETHAMBUTOL; ISONIAZID; PYRAZINAMIDE; RIFAMPICIN;

ANTIBIOTIC THERAPY; BACILLI; BACTERIAL CLEARANCE; CLINICAL TRIAL (TOPIC); DISEASE CARRIER; DRUG RESISTANT TUBERCULOSIS; HUMAN; IN VITRO STUDY; LATENT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; REVIEW; TARGET ORGANISM; TREATMENT DURATION; TUBERCULOSIS;

EID: 85042807866     PISSN: None     EISSN: 20353006     Source Type: Journal    
DOI: 10.4084/MJHID.2013.072     Document Type: Review

References (54)

1. World Health Organization. Global tuberculosis report 2012. WHO/HTM/TB/2012.6
2. Zumla A, Raviglione M, Hafner R, von Reyn CF. Tuberculosis. N Engl J Med. 2013; 368:745-55. http://dx.doi.org/10.1056/NEJMra1200894 PMid:23425167
3. Zumla A, Nahid P, Cole ST. Advances in the development of new tuberculosis drugs and treatment regimens. Nat Rev Drug Discov. 2013;12:388-404. http://dx.doi.org/10.1038/nrd4001 PMid:23629506
4. Ahuja SD, Ashkin D, Avendano M, Banerjee R, Bauer M, Bayona JN, Becerra MC, Benedetti A, Burgos M, Centis R, Chan ED, Chiang CY, Cox H, D'Ambrosio L, DeRiemer K, Dung NH, Enarson D, Falzon D, Flanagan K, Flood J, Garcia-Garcia ML, Gandhi N, Granich RM, Hollm-Delgado MG, Holtz TH, Iseman MD, Jarlsberg LG, Keshavjee S, Kim HR, Koh WJ, Lancaster J, Lange C, de Lange WC, Leimane V, Leung CC, Li J, Menzies D, Migliori GB, Mishustin SP, Mitnick CD, Narita M, O'Riordan P, Pai M, Palmero D, Park SK, Pasvol G, Pe-a J, Pérez-Guzmán C, Quelapio MI, Ponce-de-Leon A, Riekstina V, Robert J, Royce S, Schaaf HS, Seung KJ, Shah L, Shim TS, Shin SS, Shiraishi Y, Sifuentes-Osornio J, Sotgiu G, Strand MJ, Tabarsi P, Tupasi TE, van Altena R, Van der Walt M, Van der Werf TS, Vargas MH, Viiklepp P, Westenhouse J, Yew WW, Yim JJ; Collaborative Group for Meta-Analysis of Individual Patient Data in MDR-TB. Multidrug resistant pulmonary tuberculosis treatment regimens and patient outcomes: an individual patient data meta-analysis of 9, 153 patients. PLoS Med. 2012;9(8):e1001300. PMid:22952439 PMCid:PMC3429397
5. Fattorini L, Mustazzolu A, Piccaro G, Pardini M, Filippini P, Giannoni F, Migliori GB, Sotgiu G, Borroni E, Cirillo DM; Italian Multicentre Study on Resistance to Antituberculosis Drugs Group.Drug-resistant tuberculosis among foreign-born persons in Italy. Eur Respir J. 2012;40:497-500. http://dx.doi.org/10.1183/09031936.00021012 PMid:22855470
6. Ottenhoff TH, Kaufmann SH.Vaccines against tuberculosis: where are we and where do we need to go? PLoS Pathog. 2012;8(5):e1002607. http://dx.doi.org/10.1371/journal.ppat.1002607 PMid:22589713 PMCid:PMC3349743
7. Locht C, Rouanet C, Hougardy JM, Mascart F. How a different look at latency can help to develop novel diagnostics and vaccines against tuberculosis. Expert Opin Biol Ther. 2007;7:1665-77. http://dx.doi.org/10.1517/14712598.7.11.1665 PMid:17961090
8. Barry CE 3rd, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, Schnappinger D, Wilkinson RJ, Young D.The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol. 2009;7:845-55. PMid:19855401
9. Fox GJ, Barry SE, Britton WJ, Marks GB. Contact investigation for tuberculosis: a systematic review and meta-analysis. Eur Respir J. 2013;41:140-56. http://dx.doi.org/10.1183/09031936.00070812 PMid:22936710 PMCid:PMC3533588
10. Gengenbacher M, Kaufmann SH. Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev. 2012;36:514-32. http://dx.doi.org/10.1111/j.1574-6976.2012.00331.x PMid:22320122 PMCid:PMC3319523
11. Kim MJ, Wainwright HC, Locketz M, Bekker LG, Walther GB, Dittrich C, Visser A, Wang W, Hsu FF, Wiehart U, Tsenova L, Kaplan G, Russell DG. Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med. 2010;2:258-74. http://dx.doi.org/10.1002/emmm.201000079 PMid:20597103 PMCid:PMC2913288
12. Cardona PJ, Ruiz-Manzano J. On the nature of Mycobacterium tuberculosis-latent bacilli. Eur Respir J. 2004;24:1044-51. http://dx.doi.org/10.1183/09031936.04.00072604 PMid:15572551
13. Ulrichs T, Kosmiadi GA, Trusov V, Jörg S, Pradl L, Titukhina M, Mishenko V, Gushina N, Kaufmann SH. Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung. J Pathol. 2004;204:217-28. http://dx.doi.org/10.1002/path.1628 PMid:15376257
14. Ulrichs T, Kaufmann SH. New insights into the function of granulomas in human tuberculosis. J Pathol. 2006;208:261-9. http://dx.doi.org/10.1002/path.1906 PMid:16362982
15. Dartois V, Barry CE 3rd. A medicinal chemists' guide to the unique difficulties of lead optimization for tuberculosis. Bioorg Med Chem Lett. 2013;23:4741-50. http://dx.doi.org/10.1016/j.bmcl.2013.07.006 PMid:23910985
16. Kumar A, Toledo JC, Patel RP, Lancaster JR Jr, Steyn AJ. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci U S A. 2007;104:11568-73. http://dx.doi.org/10.1073/pnas.0705054104 PMid:17609369 PMCid:PMC1906723
17. Rustad TR, Harrell MI, Liao R, Sherman DR. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One. 2008;30;3(1):e1502
18. Wayne, L.G., and L.G. Hayes. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun. 1996; 64:2062-9. PMid:8675308 PMCid:PMC174037
19. Piccaro G, Giannoni F, Filippini P, Mustazzolu A, Fattorini L. Activities of drug combinations against Mycobacterium tuberculosis grown in aerobic and hypoxic acidic conditions. Antimicrob Agents Chemother. 2013;57:1428-33. http://dx.doi.org/10.1128/AAC.02154-12 PMid:23295931 PMCid:PMC3591868
20. Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, Sirakova TD, Pawar S, Rogers L, Kolattukudy PE. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One. 2009 Jun 29;4(6):e6077. http://dx.doi.org/10.1371/journal.pone.0006077 PMid:19562030 PMCid:PMC2698117
21. Vandiviere HM, Loring WE, Melvin I, Willis S. The treated pulmonary lesion and its tubercle bacillus. II. The death and resurrection. Am J Med Sci. 1956;232:30-7. http://dx.doi.org/10.1097/00000441-195607000-00006 PMid:13326887
22. Ulrichs T, Kosmiadi GA, Jörg S, Pradl L, Titukhina M, Mishenko V, Gushina N, Kaufmann SH. Differential organization of the local immune response in patients with active cavitary tuberculosis or with nonprogressive tuberculoma. J Infect Dis. 2005;192:89-97. http://dx.doi.org/10.1086/430621 PMid:15942898
23. Kana BD, Mizrahi V. Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunol Med Microbiol. 2010;58:39-50. http://dx.doi.org/10.1111/j.1574-695X.2009.00606.x PMid:19799629
24. Gupta RK, Srivastava BS, Srivastava R. Comparative expression analysis of rpf-like genes of Mycobacterium tuberculosis H37Rv under different physiological stress and growth conditions. Microbiology. 2010;156:2714-22. http://dx.doi.org/10.1099/mic.0.037622-0 PMid:20522500
25. Daniel J, Maamar H, Deb C, Sirakova TD, Kolattukudy PE. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog. 2011;7(6):e1002093. http://dx.doi.org/10.1371/journal.ppat.1002093 PMid:21731490 PMCid:PMC3121879
26. Sirakova TD, Deb C, Daniel J, Singh HD, Maamar H, Dubey VS, Kolattukudy PE. Wax ester synthesis is required for Mycobacterium tuberculosis to enter in vitro dormancy. PLoS One. 2012;7(12):e51641. http://dx.doi.org/10.1371/journal.pone.0051641 PMid:23272127 PMCid:PMC3522743
27. Pandey AK, Sassetti CM. Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A. 2008;105:4376-80. http://dx.doi.org/10.1073/pnas.0711159105 PMid:18334639 PMCid:PMC2393810
28. Garton NJ, Waddell SJ, Sherratt AL, Lee SM, Smith RJ, Senner C, Hinds J, Rajakumar K, Adegbola RA, Besra GS, Butcher PD, Barer MR. Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med. 2008;5(4):e75. http://dx.doi.org/10.1371/journal.pmed.0050075 PMid:18384229 PMCid:PMC2276522
29. Neyrolles O, Hernandez-Pando R, Pietri-Rouxel F, et al. Is Adipose Tissue a Place for Mycobacterium tuberculosis Persistence? PLoS ONE. 2006;1:e43. http://dx.doi.org/10.1371/journal.pone.0000043 PMid:17183672 PMCid:PMC1762355
30. Lenaerts AJ, Hoff D, Aly S, et al. Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother. 2007;51:3338-45. http://dx.doi.org/10.1128/AAC.00276-07 PMid:17517834 PMCid:PMC2043239
31. Hoff DR, Ryan GJ, Driver ER, Ssemakulu CC, De Groote MA, Basaraba RJ, Lenaerts AJ. Location of intra-and extracellular Mycobacterium tuberculosis populations in lungs of mice and guinea pigs during disease progression and after drug treatment. PLoS One. 2011; 21;6(3):e17550
32. Via LE, Lin PL, Ray SM, et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun. 2008;76:2333-40. http://dx.doi.org/10.1128/IAI.01515-07 PMid:18347040 PMCid:PMC2423064
33. Kjellsson MC, Via LE, Goh A, Weiner D, Low KM, Kern S, Pillai G, Barry CE 3rd, Dartois V. Pharmacokinetic evaluation of the penetration of antituberculosis agents in rabbit pulmonary lesions. Antimicrob Agents Chemother. 2012;56:446-57. http://dx.doi.org/10.1128/AAC.05208-11 PMid:21986820 PMCid:PMC3256032
34. Prideaux B, Dartois V, Staab D, Weiner DM, Goh A, Via LE, Barry CE 3rd, Stoeckli M. High-sensitivity MALDI-MRM-MS imaging of moxifloxacin distribution in tuberculosis-infected rabbit lungs and granulomatous lesions. Anal Chem. 2011;83:2112-8. http://dx.doi.org/10.1021/ac1029049 PMid:21332183 PMCid:PMC3158846
35. Zhang Y, Yew WW, Barer MR. Targeting persisters for tuberculosis control. Antimicrob Agents Chemother. 2012;56:2223-30. http://dx.doi.org/10.1128/AAC.06288-11 PMid:22391538 PMCid:PMC3346619
36. Keren I, Minami S, Rubin E, Lewis K. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. MBio. 2011;2(3):e00100-11
37. Dörr T, Vulic M, Lewis K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 2010;8(2):e1000317
38. Grant SS, Kaufmann BB, Chand NS, Haseley N, Hung DT. Eradication of bacterial persisters with antibiotic-generated hydroxyl radicals. Proc Natl Acad Sci U S A. 2012;109:12147-52. http://dx.doi.org/10.1073/pnas.1203735109 PMid:22778419 PMCid:PMC3409745
39. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. A common mechanism of cellular death induced by bactericidal antibiotics. Cell. 2007;130:797-810. http://dx.doi.org/10.1016/j.cell.2007.06.049 PMid:17803904
40. Iona E, Giannoni F, Pardini M, Brunori L, Orefici G, Fattorini L. Metronidazole plus Rifampin Sterilizes Long-Term Dormant Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2007; 51:1537-40. http://dx.doi.org/10.1128/AAC.01468-06 PMid:17242153 PMCid:PMC1855463
41. Filippini P, Iona E, Piccaro G, Peyron P, Neyrolles O, Fattorini L. Activity of drug combinations against dormant Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2010;54:2712-5. http://dx.doi.org/10.1128/AAC.01736-09 PMid:20350948 PMCid:PMC2876400
42. Lin PL, Dartois V, Johnston PJ, Janssen C, Via L, Goodwin MB, Klein E, Barry CE 3rd, Flynn JL. Metronidazole prevents reactivation of latent Mycobacterium tuberculosis infection in macaques. Proc Natl Acad Sci U S A. 2012;109:14188-93. http://dx.doi.org/10.1073/pnas.1121497109 PMid:22826237 PMCid:PMC3435210
43. Carroll MW, Jeon D, Mountz JM, Lee JD, Jeong YJ, Zia N, Lee M, Lee J, Via LE, Lee S, Eum SY, Lee SJ, Goldfeder LC, Cai Y, Jin B, Kim Y, Oh T, Chen RY, Dodd LE, Gu W, Dartois V, Park SK, Kim CT, Barry CE 3rd, Cho SN. Efficacy and safety of metronidazole for pulmonary multidrug-resistant tuberculosis. Antimicrob Agents Chemother. 2013;57:3903-9. http://dx.doi.org/10.1128/AAC.00753-13 PMid:23733467
44. Singh R, Manjunatha U, Boshoff HI, Ha YH, Niyomrattanakit P, Ledwidge R, Dowd CS, Lee IY, Kim P, Zhang L, Kang S, Keller TH, Jiricek J, Barry CE 3rd. PA-824 kills nonreplicating Mycobacterium tuberculosis by intracellular NO release. Science. 2008;322:1392-5. http://dx.doi.org/10.1126/science.1164571 PMid:19039139 PMCid:PMC2723733
45. Cohen J. Infectious disease. Approval of novel TB drug celebrated-with restraint. Science. 2013;339:130. http://dx.doi.org/10.1126/science.339.6116.130 PMid:23307714
46. Koul A, Vranckx L, Dendouga N, Balemans W, Van den Wyngaert I, Vergauwen K, Göhlmann HW, Willebrords R, Poncelet A, Guillemont J, Bald D, Andries K. Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem. 2008;283:25273-80. http://dx.doi.org/10.1074/jbc.M803899200 PMid:18625705
47. Rao SP, Alonso S, Rand L, Dick T, Pethe K. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2008;105:11945-50. http://dx.doi.org/10.1073/pnas.0711697105 PMid:18697942 PMCid:PMC2575262
48. Franzblau SG, DeGroote MA, Cho SH, Andries K, Nuermberger E, Orme IM, Mdluli K, Angulo-Barturen I, Dick T, Dartois V, Lenaerts AJ. Comprehensive analysis of methods used for the evaluation of compounds against Mycobacterium tuberculosis. Tuberculosis (Edinb). 2012;92:453-88. http://dx.doi.org/10.1016/j.tube.2012.07.003 PMid:22940006
49. Wayne LG, Sohaskey CD. Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol. 2001;55:139-63. http://dx.doi.org/10.1146/annurev.micro.55.1.139 PMid:11544352
50. Williams K, Minkowski A, Amoabeng O, Peloquin CA, Taylor D, Andries K, Wallis RS, Mdluli KE, Nuermberger EL. Sterilizing activities of novel combinations lacking first-and second-line drugs in a murine model of tuberculosis. Antimicrob Agents Chemother. 2012;56:3114-20. http://dx.doi.org/10.1128/AAC.00384-12 PMid:22470112 PMCid:PMC3370712
51. Tasneen R, Li SY, Peloquin CA, Taylor D, Williams KN, Andries K, Mdluli KE, Nuermberger EL. Sterilizing activity of novel TMC207-and PA-824-containing regimens in a murine model of tuberculosis. Antimicrob Agents Chemother. 2011;55:5485-92. http://dx.doi.org/10.1128/AAC.05293-11 PMid:21930883 PMCid:PMC3232786
52. Driver ER, Ryan GJ, Hoff DR, Irwin SM, Basaraba RJ, Kramnik I, Lenaerts AJ. Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2012;56:3181-95. http://dx.doi.org/10.1128/AAC.00217-12 PMid:22470120 PMCid:PMC3370740
53. Diacon AH, Dawson R, von Groote-Bidlingmaier F, Symons G, Venter A, Donald PR, van Niekerk C, Everitt D, Winter H, Becker P, Mendel CM, Spigelman MK. 14-day bactericidal activity of PA-824, bedaquiline, pyrazinamide, and moxifloxacin combinations: a randomised trial. Lancet. 2012;380:986-93. http://dx.doi.org/10.1016/S0140-6736(12)61080-0
54. Dutta NK, Alsultan A, Gniadek TJ, Belchis DA, Pinn ML, Mdluli KE, Nuermberger EL, Peloquin CA, Karakousis PC. Potent rifamycin-sparing regimen cures Guinea pig tuberculosis as rapidly as the standard regimen. Antimicrob Agents Chemother. 2013;57:3910-6. http://dx.doi.org/10.1128/AAC.00761-13 PMid:23733473