Elucidating population-wide mycobacterial replication dynamics at the single-cell level

Microbiology (United Kingdom)

Volumn 162, Issue 6, 2016, Pages 966-978

  Mouton, Jacoba M ^a   Helaine, Sophie ^b   Holden, David W ^b   Sampson, Samantha L ^a,b  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL; CYCLOSERINE; PANTOTHENIC ACID; THEOPHYLLINE; TYLOXAPOL; ANTIINFECTIVE AGENT;

ANIMAL CELL; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM IDENTIFICATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE; FLUORESCENCE DILUTION; INTRACELLULAR BACTERIUM; MACROPHAGE; MICROBIAL POPULATION DYNAMICS; MURINE; MYCOBACTERIAL REPLICATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; TUBERCULOSIS; ANIMAL; ANTIBIOTIC RESISTANCE; CELL LINE; DNA REPLICATION; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOUSE; PROCEDURES; RAW 264.7 CELL LINE;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL LINE; DNA REPLICATION; DRUG RESISTANCE, BACTERIAL; MACROPHAGES; MICE; MYCOBACTERIUM TUBERCULOSIS; RAW 264.7 CELLS; SINGLE-CELL ANALYSIS; TUBERCULOSIS;

EID: 84977156597     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000288     Document Type: Article

References (44)

1. Adams, K. N., Takaki, K., Connolly, L. E., Wiedenhoft, H., Winglee, K., Humbert, O., Edelstein, P. H., Cosma, C. L. & Ramakrishnan, L. (2011). Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145, 39–53.
2. Aldridge, B. B., Fernandez-Suarez, M., Heller, D., Ambravaneswaran, V., Irimia, D., Toner, M. & Fortune, S. M. (2012). Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 335, 100–104.
3. Anes, E., Peyron, P., Staali, L., Jordao, L., Gutierrez, M. G., Kress, H., Hagedorn, M., Maridonneau-Parini, I. & Skinner, M. A. (2006). Dynamic life and death interactions between Mycobacterium smegmatis and J774 macrophages. Cell Microbiol 8, 939–960.
4. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science 305, 1622–1625.
5. Betts, J. C., Lukey, P. T., Robb, L. C., McAdam, R. A. & Duncan, K. (2002). Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43, 717–731.
6. Bhaskar, A., Chawla, M., Mehta, M., Parikh, P., Chandra, P., Bhave, D., Kumar, D., Carroll, K. S. & Singh, A. (2014). Reengineering redox sensitive GFP to measure mycothiol redox potential of Mycobacterium tuberculosis during infection. PLoS Pathog 10, e1003902.
7. Bigger, J. W. (1944). Treatment of staphylococcal infections with penicillin. Lancet 244, 497–500.
8. Carroll, P., Schreuder, L. J., Muwanguzi-Karugaba, J., Wiles, S., Robertson, B. D., Ripoll, J., Ward, T. H., Bancroft, G. J., Schaible, U. E. & Parish, T. (2010). Sensitive detection of gene expression in mycobacteria under replicating and non-replicating conditions using optimized far-red reporters. PLoS One 5, e9823.
9. Cañas-Duarte, S. J., Restrepo, S. & Pedraza, J. M. (2014). Novel protocol for persister cells isolation. PLoS One 9, e88660.
10. Cohen, N. R., Lobritz, M. A. & Collins, J. J. (2013). Microbial persistence and the road to drug resistance. Cell Host Microbe 13, 632–642.
11. Colangeli, R., Arcus, V. L., Cursons, R. T., Ruthe, A., Karalus, N., Coley, K., Manning, S. D., Kim, S., Marchiano, E. & Alland, D. (2014). Whole genome sequencing of Mycobacterium tuberculosis reveals slow growth and low mutation rates during latent infections in humans. PLoS One 9, e91024.
12. Deb, C., Lee, C. M., Dubey, V. S., Daniel, J., Abomoelak, B., Sirakova, T. D., Pawar, S., Rogers, L. & Kolattukudy, P. E. (2009). A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4, e6077.
13. Dhar, N. & McKinney, J. D. (2010). Mycobacterium tuberculosis persistence mutants identified by screening in isoniazid-treated mice. Proc Natl Acad Sci U S A 107, 12275–12280.
14. Ford, C. B., Lin, P. L., Chase, M. R., Shah, R. R., Iartchouk, O., Galagan, J., Mohaideen, N., Ioerger, T. R. & Sacchettini, J. C. (2011). Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43, 482–486.
15. Garton, N. J., Waddell, S. J., Sherratt, A. L., Lee, S. M., Smith, R. J., Senner, C., Hinds, J., Rajakumar, K. & Adegbola, R. A. (2008). Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med 5, e75.
16. Gengenbacher, M., Rao, S. P., Pethe, K. & Dick, T. (2010). Nutrientstarved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 156, 81–87.
17. Gill, W. P., Harik, N. S., Whiddon, M. R., Liao, R. P., Mittler, J. E. & Sherman, D. R. (2009). A replication clock for Mycobacterium tuberculosis. Nat Med 15, 211–214.
18. Hartman-Adams, H., Clark, K. & Juckett, G. (2014). Update on latent tuberculosis infection. Am Fam Physician 89, 889–896.
19. Helaine, S. & Kugelberg, E. (2014). Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol 22, 417–424.
20. Helaine, S., Cheverton, A. M., Watson, K. G., Faure, L. M., Matthews, S. A. & Holden, D. W. (2014). Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343, 204–208.
21. Helaine, S., Thompson, J. A., Watson, K. G., Liu, M., Boyle, C. & Holden, D. W. (2010). Dynamics of intracellular bacterial replication at the single cell level. Proc Natl Acad Sci U S A 107, 3746–3751.
22. Inouye, S. & Tsuji, F. I. (1994). Aequorea green fluorescent protein. Expression of the gene and fluorescence characteristics of the recombinant protein. FEBS Lett 341, 277–280.
23. Keren, I., Minami, S., Rubin, E. & Lewis, K. (2011). Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. MBio 2, e00100–11.
24. Luthuli, B. B., Purdy, G. E. & Balagadd_e, F. K. (2015). Confinementinduced drug-tolerance in mycobacteria mediated by an efflux mechanism. PLoS One 10, e0136231.
25. Maglica, Ž., Özdemir, E. & McKinney, J. D. (2015). Single-cell tracking reveals antibiotic-induced changes in mycobacterial energy metabolism. MBio 6, e02236–14.
26. Maisonneuve, E., Shakespeare, L. J., Jørgensen, M. G. & Gerdes, K. (2011). Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 108, 13206–13211.
27. Mak, P. A., Rao, S. P., Ping Tan, M., Lin, X., Chyba, J., Tay, J., Ng, S. H., Tan, B. H. & Cherian, J. (2012). A high-throughput screen to identify inhibitors of ATP homeostasis in non-replicating Mycobacterium tuberculosis. ACS Chem Biol 7, 1190–1197.
28. Manina, G., Dhar, N. & McKinney, J. D. (2015). Stress and host immunity amplify Mycobacterium tuberculosis phenotypic heterogeneity and induce nongrowing metabolically active forms. Cell Host Microbe 17, 32–46.
29. Mitchison, D. A. & Coates, A. R. (2004). Predictive in vitro models of the sterilizing activity of anti-tuberculosis drugs. Curr Pharm Des 10, 3285–3295.
30. Parker, A. E. & Bermudez, L. E. (1997). Expression of the green fluorescent protein (GFP) in mycobacterium avium as a tool to study the interaction between mycobacteria and host cells. Microb Pathog 22, 193–198.
31. Prakash, H., Lüth, A., Grinkina, N., Holzer, D., Wadgaonkar, R., Gonzalez, A. P., Anes, E. & Kleuser, B. (2010). Sphingosine kinase-1 (SphK-1) regulates Mycobacterium smegmatis infection in macrophages. PLoS One 5, e10657.
32. Raffetseder, J., Pienaar, E., Blomgran, R., Eklund, D., Patcha Brodin, V., Andersson, H., Welin, A. & Lerm, M. & Brodin, P. V. (2014). Replication rates of Mycobacterium tuberculosis in human macrophages do not correlate with mycobacterial antibiotic susceptibility. PLoS One 9:e112426.
33. Rodríguez, J. G., Hern_andez, A. C., Helguera-Repetto, C., Aguilar Ayala, D., Guadarrama-Medina, R., Anzóla, J. M., Bustos, J. R., Zambrano, M. M., Gonz_alez-Y-Merchand, J. & Gonzalez, Y. M. J. (2014). Global adaptation to a lipid environment triggers the dormancy- related phenotype of Mycobacterium tuberculosis. MBio 5, e01125–14.
34. Roostalu, J., Jõers, A., Luidalepp, H., Kaldalu, N. & Tenson, T. (2008). Cell division in Escherichia coli cultures monitored at single cell resolution. BMC Microbiol 8, 68.
35. Sampson, S. L., Dascher, C. C., Sambandamurthy, V. K., Russell, R. G., Jacobs, W. R., Bloom, B. R. & Hondalus, M. K. (2004). Protection elicited by a double leucine and pantothenate auxotroph of Mycobacterium tuberculosis in guinea pigs. Infect Immun 72, 3031–3037.
36. Seeliger, J. C., Topp, S., Sogi, K. M., Previti, M. L., Gallivan, J. P. & Bertozzi, C. R. (2012). A riboswitch-based inducible gene expression system for mycobacteria. PLoS One 7, e29266.
37. Shcherbo, D., Shemiakina, I. I., Ryabova, A. V., Luker, K. E., Schmidt, B. T., Souslova, E. A., Gorodnicheva, T. V., Strukova, L. & Shidlovskiy, K. M. (2010). Near-infrared fluorescent proteins. Nat Methods 7, 827–829.
38. Snapper, S. B., Melton, R. E., Mustafa, S., Kieser, T. & Jacobs, W. R. (1990). Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4, 1911–1919.
39. Tan, S., Sukumar, N., Abramovitch, R. B., Parish, T. & Russell, D. G. (2013). Mycobacterium tuberculosis responds to chloride and pH as synergistic cues to the immune status of its host cell. PLoS Pathog 9, e1003282.
40. Wakamoto, Y., Dhar, N., Chait, R., Schneider, K., Signorino-Gelo, F., Leibler, S. & McKinney, J. D. (2013). Dynamic persistence of antibiotic- stressed mycobacteria. Science 339, 91–95.
41. Walter, N. D., Dolganov, G. M., Garcia, B. J., Worodria, W., Andama, A., Musisi, E., Ayakaka, I., Van, T. T. & Voskuil, M. I. (2015). Transcriptional adaptation of drug-tolerant Mycobacterium tuberculosis during treatment of human tuberculosis. J Infect Dis 212, 990–998.
42. WHO (2015). Global Tuberculosis Report 2014. Geneva: World Health Organization.
43. Zelmer, A., Carroll, P., Andreu, N., Hagens, K., Mahlo, J., Redinger, N., Robertson, B. D., Wiles, S. & Ward, T. H. (2012). A new in vivo model to test anti-tuberculosis drugs using fluorescence imaging. J Antimicrob Chemother 67, 1948–1960.
44. Zhang, Y., Yew, W. W. & Barer, M. R. (2012). Targeting persisters for tuberculosis control. Antimicrob Agents Chemother 56, 2223–2230.