High persister mutants in mycobacterium tuberculosis

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Torrey, Heather L ^a   Keren, Iris ^a   Via, Laura E ^b   Lee, Jong Seok ^c   Lewis, Kim ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c International Tuberculosis Research Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

KANAMYCIN; MOXIFLOXACIN; RIFAMPICIN; ANTIINFECTIVE AGENT;

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM ISOLATE; CARBON METABOLISM; CONTROLLED STUDY; GENE IDENTIFICATION; GENE MUTATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HIP GENE; LIPOGENESIS; MOLECULAR GENETICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; SURVIVAL RATE; TRANSCRIPTION REGULATION; TUBERCULOSIS; UPREGULATION; ANIMAL; BACTERIAL GENOME; BIOLOGICAL MODEL; DNA SEQUENCE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOUSE; MUTATION; PATHOLOGY; PHENOTYPE;

ANIMALS; ANTI-BACTERIAL AGENTS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDIES; GENOME, BACTERIAL; MICE; MODELS, BIOLOGICAL; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; SEQUENCE ANALYSIS, DNA; TUBERCULOSIS;

EID: 84969753024     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155127     Document Type: Article

References (66)

1. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA. 1999; 282: 677-686. PMID: 10517722
2. van Crevel R, Ottenhoff TH, van der Meer JW. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev. 2002; 15: 294-309. PMID: 11932234
3. Parrish NM, Dick JD, Bishai WR. Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol. 1998; 6: 107-112. PMID: 9582936
4. Wayne L. Dormancy of Mycobacterium tuberculosis and latency of disease. Eur J Clin Microbiol Infect Dis. 1994; 13: 908-914. PMID: 7698116
5. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett. 2004; 230: 13-18. PMID: 14734160
6. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial Persistence as a Phenotypic Switch. Science. 2004; 305: 1622-1625. PMID: 15308767
7. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol. 2004; 186: 8172-8180. PMID: 15576765
8. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. Persisters: A distinct physiological state of E. coli. BMC Microbiol. 2006; 6: 53-61. PMID: 16768798
9. Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K. Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci USA. 2011; 108: 13206-13211. doi: 10.1073/pnas.1100186108 PMID: 21788497
10. Falla TJ, Chopra I. Joint tolerance to beta-lactam and fluoroquinolone antibiotics in Escherichia coli results from overexpression of hipA. Antimicrob Agents Chemother. 1998; 42: 3282-3284. PMID: 9835528
11. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. Molecular mechanisms of HipAmediated multidrug tolerance and its neutralization by HipB. Science. 2009; 323: 396-401. doi: 10. 1126/science.1163806 PMID: 19150849
12. Correia FF, D'Onofrio A, Rejtar T, Li L, Karger BL, Makarova K, et al. Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J Bacteriol. 2006; 188: 8360-8367. PMID: 17041039
13. Harrison JJ, Wade WD, Akierman S, Vacchi-Suzzi C, Stremick CA, Turner RJ, et al. The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing in a biofilm. Antimicrob Agents Chemother. 2009; 53: 2253-2258. doi: 10.1128/AAC.00043-09 PMID: 19307375
14. Maisonneuve E, Castro-Camargo M, Gerdes K. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell. 2013; 154: 1140-1150. doi: 10.1016/j.cell.2013.07.048 PMID: 23993101
15. Dorr T, Vulic M, Lewis K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 2010; 8: e1000317. doi: 10.1371/journal.pbio.1000317 PMID: 20186264
16. Unoson C, Wagner E. A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol Microbiol. 2008; 70: 258-270. doi: 10.1111/j.1365-2958.2008.06416.x PMID: 18761622
17. Gurnev PA, Ortenberg R, Dorr T, Lewis K, Bezrukov SM. Persister-promoting bacterial toxin TisB produces anion-selective pores in planar lipid bilayers. FEBS Lett. 2012; 586: 2529-2534. doi: 10.1016/j. febslet.2012.06.021 PMID: 22728134
18. Spoering A, Vulic M, Lewis K. GlpD and PlsB participate in persister cell formation in Escherichia coli. J Bacteriol. 2006; 188: 5136-5144. PMID: 16816185
19. Hansen S, Lewis K, Vulic M. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob Agents Chemother. 2008; 52(8): 2718-26. doi: 10.1128/AAC.00144-08 PMID: 18519731
20. Girgis HS, Harris K, Tavazoie S. Large mutational target size for rapid emergence of bacterial persistence. PNAS. 2012; 109: 12740-12745. doi: 10.1073/pnas.1205124109 PMID: 22802628
21. Keren I, Minami S, Rubin E, Lewis K. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. MBio. 2011; 2(3): e00100-11. doi: 10.1128/mBio.00100-11 PMID: 21673191
22. Shao Y, Harrison EM, Bi D, Tai C, He X, Ou HY, et al. TADB: a web-based resource for Type 2 toxinantitoxin loci in bacteria and archaea. Nucleic Acids Res. 2011; 39: D606-11. doi: 10.1093/nar/gkq908 PMID: 20929871
23. Sala A, Bordes P, Genevaux P. Multiple Toxin-Antitoxin Systems in Mycobacterium tuberculosis. Toxins. 2014; 6(3): 1002-1020. doi: 10.3390/toxins6031002 PMID: 24662523
24. Singh R, Barry CE, Boshoff HI. The three relE homologs of Mycobacterium tuberculosis have individual, drug-specific effects on bacterial antibiotic tolerance. J. Bacteriol. 2010; 192: 1279-1291. doi: 10. 1128/JB.01285-09 PMID: 20061486
25. Aldridge BB, Fernandez-Suarez M, Heller D, Ambravaneswaran V, Irimia D, Toner M, et al. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science. 2012; 335: 100-104. doi: 10.1126/science.1216166 PMID: 22174129
26. Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F, Leibler S, et al. Dynamic persistence of antibiotic-stressed mycobacteria. Science. 2013; 339: 91-95. doi: 10.1126/science.1229858 PMID: 23288538
27. Deb C, Lee C-M, Dubey VS, Daniel J, Abomoelak B, Sirakova TD, et al. A Novel In Vitro Multiple-Stress Dormancy Model for Mycobacterium tuberculosis Generates a Lipid-Loaded, Drug-Tolerant, Dormant Pathogen. PLoS ONE. 2009; 4: e6077. doi: 10.1371/journal.pone.0006077 PMID: 19562030
28. Baek S-H, Li AH, Sassetti CM. Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol. 2011; 9(5): e1001065. doi: 10.1371/journal.pbio.1001065 PMID: 21629732
29. Spoering AL, Lewis K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol. 2001; 183: 6746-6751. PMID: 11698361
30. Moyed HS, Bertrand KP. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol. 1983; 155: 768-775. PMID: 6348026
31. Slattery A, Victorsen AH, Brown A, Hillman K, Phillips G. Isolation of Highly Persistent Mutants of Salmonella enterica Serovar Typhimurium Reveals a New Toxin-Antitoxin Module. J Bacteriol. 2013; 195 (4): 647-657. doi: 10.1128/JB.01397-12 PMID: 23204462
32. LaFleur MD, Qi Q, Lewis K. Patients with long-term oral carriage harbor high- persister mutants of Candida albicans. Antimicrob Agents Chemother. 2010; 54: 39-44. doi: 10.1128/AAC.00860-09 PMID: 19841146
33. Mulcahy LR, Burns JL, Lory S, Lewis K. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol. 2010; 192: 6191-6199. doi: 10. 1128/JB.01651-09 PMID: 20935098
34. Schumacher MA, Balani P, Min J, Chinnam NB, Hansen S, Vulić M, et al. HipBA-promoter structures reveal the basis of heritable multidrug tolerance. Nature. 2015; 524: 59-64. doi: 10.1038/nature14662 PMID: 26222023
35. Sambandamurthy VK, Derrick SC, Jalapathy KV, Chen B, Russell RG, Morris SL, et al. Long-term protection against tuberculosis following vaccination with a severely attenuated double lysine and pantothenate auxotroph of Mycobacterium tuberculosis. Infect Immun. 2005; 73: 1196-1203. PMID: 15664964
36. Cox JS, Chen B, McNeil M, Jacobs WR Jr. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature. 1999; 402: 79-83. PMID: 10573420
37. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol. 1999; 34: 257-267. PMID: 10564470
38. Murry JP, Pandey AK, Sassetti CM, Rubin EJ. Phthiocerol dimycocerosate transport is required for resisting interferon-γ-independent immunity. J Infect Dis. 2009; 200: 774-782. doi: 10.1086/605128 PMID: 19622047
39. Nandakumar M, Nathan C, Rhee K. Isocitrate lyase mediates broad antibiotic tolerance in Mycobacterium tuberculosis. Nature Comms. 2013; 5: 4306. doi: 10.1038/ncomms5306
40. Yokoyama K, Ishijima SA, Clowney L, Koike H, Aramaki H, Tanaka C, et al. Feast/famine regulatory proteins (FFRPs): Escherichia coli Lrp, AsnC and related archaeal transcription factors. FEMS Microbiol Rev. 2006; 30: 89-108. PMID: 16438681
41. Alland D, Steyn AJ, Weisbrod T, Aldrich K, Jacobs WR Jr. Characterization of the Mycobacterium tuberculosis iniBAC promoter, a promoter that responds to cell wall biosynthesis inhibition. J Bacteriol. 2000; 182: 1802-1811. PMID: 10714983
42. Rastogi N, Labrousse V, and Goh KS. In Vitro Activities of Fourteen Antimicrobial Agents Against Drug Susceptible and Resistant Clinical Isolates of Mycobacterium tuberculosis and Comparative Intracellular Activities Against the Virulent H37Rv Strain in Human Macrophages. Curr Microbiol. 1996; 33: 167-175. PMID: 8672093
43. Domenech P, Reed MB. Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Mirobiol. 2009; 155: 3532-3543.
44. Trivedi OA, Arora P, Vats A, Ansari MZ, Tickoo R, Sridharan V, et al. Dissecting the mechanism and assembly of a complex virulence mycobacterial lipid. Mol Cell. 2005; 17: 631-643. PMID: 15749014
45. Amato SM, Fazen CH, Henry T, Mok WW, Orman MA, Sandvik EL, et al. The role of metabolism in bacterial persistence. Front Microbiol. 2014; 5: 70. doi: 10.3389/fmicb.2014.00070 PMID: 24624123
46. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, Smith I. The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol. 2006; 60(2): 313-330.
47. Matsuura M, Saldanha R, Ma H, Wank H, Yang J, Mohr G, et al. A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: biochemical demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev. 1997; 11: 2910-2924 PMID: 9353259
48. Recchi C, Sclavi B, Rauzier J, Gicquel B, Reyrat JM. Mycobacterium tuberculosis Rv1395 is a class III transcriptional regulator of the AraC family involved in cytochrome P450 regulation. J Biol Chem. 2003; 278(36): 33763-73. PMID: 12826660
49. Guo M, Feng H, Zhang J, Wang W, Wang Y, Li Y, et al. Dissecting transcription regulatory pathways through a new bacterial one-hybrid reporter system. Genome Res. 2009; 9: 1301-1308. doi: 10.1101/ gr.086595.108
50. Wallis RS, Patil S, Cheon SH, Edmonds K, Phillips M, Perkins MD, et al. Drug tolerance in Mycobacterium tuberculosis. Antimicrob Agents Chemother. 1999; 43: 2600-2606. PMID: 10543735
51. Pandy AK, Sassetti CM. Mycobacterial persistence requires the utilization of host cholesterol. PNAS. 2008; 105: 4376-4380. doi: 10.1073/pnas.0711159105 PMID: 18334639
52. Andrews JM. Determination of minimum inhibitory concentrations. J Antimicrob Chemother. 2001; 48: 5-16. PMID: 11420333
53. Miller JH. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Vol 1. New York: Cold Spring Harbor Laboratory Press; 1992.
54. Ehrt S, Guo XV, Hickey CM, Ryou M, Monteleone M, Riley LW, et al. Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res. 2005; 33(2): e21. doi: 10. 1093/nar/gni013 PMID: 15687379
55. Neidhardt FC, Ingraham JL, Schaechter M. Physiology of the bacterial cell: a molecular approach. Sunderland, MA: Sinauer Associates; 1990.
56. Franzblau SG, Witzig RS, McLaughlin JC, Torres P, Madico G, Hernandez A, et al. Rapid, low-technology MIC determination with clinical Mycobacterium tuberculosis isolates by using the microplate Alamar Blue assay. J Clin Microbiol. 1998; 36: 362-366. PMID: 9466742
57. Shell SS, Prestwich EG, Baek S-H, Shah RR, Sassetti CM, Dedon PC, et al. DNA Methylation Impacts Gene Expression and Ensures Hypoxic Survival of Mycobacterium tuberculosis. PLoS Pathog. 2013; 9(7): e1003419. doi: 10.1371/journal.ppat.1003419 PMID: 23853579
58. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, et al. Accurate whole human genome sequencing using reversible termina- tor chemistry. Nature. 2008; 456: 53-59. doi: 10. 1038/nature07517 PMID: 18987734
59. Fisher S, Barry A, Abreu J, Minie B, Nolan J, Delorey TM, et al. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol. 2011; 12: R1. PMID: 21205303
60. Calogero RA. oneChannelGUI: This package extends the capabilities of affyGUI interface. R Package Version 1.18.7. 2011; Available: http://www.bioinformatica.unito.it/oneChannelGUI.
61. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002; 30: 207-210. PMID: 11752295
62. Shishkin AA, Giannoukos G, Kucukural A, Ciulla D, Busby M, Surka C, et al. Simultaneous generation of many RNA-seq libraries in a single reaction. Nature Methods. 2015; 12: 323-325. doi: 10.1038/ nmeth.3313 PMID: 25730492
63. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25: 1754-1760. doi: 10.1093/bioinformatics/btp324 PMID: 19451168
64. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, et al. Rfam: updates to the RNA families database. Nucleic Acids Res. 2009; 37: D136-D140. doi: 10.1093/nar/gkn766 PMID: 18953034
65. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. RNA-Seq-Based Monitoring of Infection-Linked Changes in Vibrio cholerae Gene Expression. Cell Host Microbe. 2011; 10: 165-174. doi: 10.1016/j.chom.2011.07.007 PMID: 21843873
66. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11: R106. doi: 10.1186/gb-2010-11-10-r106 PMID: 20979621