Clinical value of whole-genome sequencing of Mycobacterium tuberculosis

The Lancet Infectious Diseases

Volumn 15, Issue 9, 2015, Pages 1077-1090

  Takiff, Howard E ^a,b   Feo, Oscar ^a  

^a Instituto Venezolano de Investigaciones Cientificas Centro de Microbiologia y Biologia Celular   (Venezuela)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ETHAMBUTOL; ETHIONAMIDE; PYRAZINAMIDE; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; BACTERIAL GENOME; BACTERIAL TRANSMISSION; CONTACT EXAMINATION; DATA BASE; DNA REPLICATION; DRUG IDENTIFICATION; DRUG SENSITIVITY; DRUG TARGETING; EPIDEMIC; GENETIC MANIPULATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HUMAN; MITOCHONDRIAL GENOME; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MULTIDRUG RESISTANCE; MULTILOCUS SEQUENCE TYPING; MUTATION RATE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TUBERCULOSIS; WHOLE GENOME SEQUENCE; GENETICS; MICROBIOLOGY; MULTIDRUG RESISTANT TUBERCULOSIS; PHYLOGENY; TUBERCULOSIS, PULMONARY;

DISEASE OUTBREAKS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HUMANS; MUTATION RATE; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; TUBERCULOSIS, MULTIDRUG-RESISTANT; TUBERCULOSIS, PULMONARY;

EID: 84940730637     PISSN: 14733099     EISSN: 14744457     Source Type: Journal    
DOI: 10.1016/S1473-3099(15)00071-7     Document Type: Review

References (197)

1. Boritsch EC, Supply P, Honoré N, Seemann T, Stinear TP, Brosch R A glimpse into the past and predictions for the future: the molecular evolution of the tuberculosis agent. Mol Microbiol 2014, 93:835-852.
2. Le Chevalier F, Cascioferro A, Majlessi L, Herrmann JL, Brosch R Mycobacterium tuberculosis evolutionary pathogenesis and its putative impact on drug development. Future Microbiol 2014, 9:969-985.
3. Bos KI, Harkins KM, Herbig A, et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 2014, 514:494-497.
4. Trauner A, Borrell S, Reither K, Gagneux S Evolution of drug resistance in tuberculosis: recent progress and implications for diagnosis and therapy. Drugs 2014, 74:1063-1072.
5. Niemann S, Supply P Diversity and evolution of Mycobacterium tuberculosis: moving to whole-genome-based approaches. Cold Spring Harb Perspect Med 2014, 4:a021188.
6. Behr MA Comparative genomics of mycobacteria: some answers, yet more new questions. Cold Spring Harb Perspect Med 2014, 5:a021204.
7. Warner DF, Koch A, Mizrahi V Diversity and disease pathogenesis in Mycobacterium tuberculosis. Trends Microbiol 2015, 23:14-21.
8. Warner DF, Mizrahi V Translating genomics research into control of tuberculosis: lessons learned and future prospects. Genome Biol 2014, 15:514.
9. Hasnain SE, O'Toole RF, Grover S, Ehtesham NZ Whole genome sequencing: a new paradigm in the surveillance and control of human tuberculosis. Tuberculosis (Edinb) 2015, 95:91-94.
10. Gonzalo-Asensio J, Malaga W, Pawlik A, et al. Evolutionary history of tuberculosis shaped by conserved mutations in the PhoPR virulence regulator. Proc Natl Acad Sci USA 2014, 111:11491-11496.
11. Wlodarska M, Johnston JC, Gardy JL, Tang P A microbiological revolution meets an ancient disease: improving the management of tuberculosis with genomics. Clin Microbiol Rev 2015, 28:523-539.
12. Verver S, Warren RM, Beyers N, et al. Rate of reinfection tuberculosis after successful treatment is higher than rate of new tuberculosis. Am J Respir Crit Care Med 2005, 171:1430-1435.
13. Marx FM, Dunbar R, Enarson DA, et al. The temporal dynamics of relapse and reinfection tuberculosis after successful treatment: a retrospective cohort study. Clin Infect Dis 2014, 58:1676-1683.
14. Bryant JM, Harris SR, Parkhill J, et al. Whole-genome sequencing to establish relapse or re-infection with Mycobacterium tuberculosis: a retrospective observational study. Lancet Respir Med 2013, 1:786-792.
15. Guerra-Assuncao JA, Houben RM, Crampin AC, et al. Recurrence due to relapse or reinfection with Mycobacterium tuberculosis: a whole-genome sequencing approach in a large, population-based cohort with a high HIV infection prevalence and active follow-up. J Infect Dis 2015, 211:1154-1163.
16. Menzies D Molecular methods for tuberculosis trials: time for whole-genome sequencing?. Lancet Respir Med 2013, 1:759-761.
17. McCartney C The genomics of tuberculosis (accessed April 18, 2015). https://publichealthmatters.blog.gov.uk/2014/06/16/the-genomics-of-tuberculosis/.
18. Davies A, Scott S, Badger S, Török ME, Peacock SJ Public perceptions of bacterial whole-genome sequencing for tuberculosis. Trends Genet 2015, 31:58-60.
19. Otal I, Martín C, Vincent-Lévy-Frebault V, Thierry D, Gicquel B Restriction fragment length polymorphism analysis using IS6110 as an epidemiological marker in tuberculosis. J Clin Microbiol 1991, 29:1252-1254.
20. Kamerbeek J, Schouls L, Kolk A, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 1997, 35:907-914.
21. Supply P, Lesjean S, Savine E, Kremer K, van Soolingen D, Locht C Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units. J Clin Microbiol 2001, 39:3563-3571.
22. Jagielski T, van Ingen J, Rastogi N, Dziadek J, Mazur PK, Bielecki J Current methods in the molecular typing of Mycobacterium tuberculosis and other mycobacteria. Biomed Res Int 2014, 2014:645802.
23. Lee RS, Radomski N, Proulx JF, et al. Re-emergence and amplification of tuberculosis in the Canadian Arctic. J Infect Dis 2015, 211:1905-1914.
24. Mehaffy C, Guthrie JL, Alexander DC, Stuart R, Rea E, Jamieson FB Marked microevolution of a unique Mycobacterium tuberculosis strain in 17 years of ongoing transmission in a high risk population. PLoS One 2014, 9:e112928.
25. Luo T, Yang C, Peng Y, et al. Whole-genome sequencing to detect recent transmission of Mycobacterium tuberculosis in settings with a high burden of tuberculosis. Tuberculosis (Edinb) 2014, 94:434-440.
26. Jamieson FB, Teatero S, Guthrie JL, Neemuchwala A, Fittipaldi N, Mehaffy C Whole-genome sequencing of the Mycobacterium tuberculosis Manila sublineage results in less clustering and better resolution than mycobacterial interspersed repetitive-unit-variable-number tandem-repeat (MIRU-VNTR) typing and spoligotyping. J Clin Microbiol 2014, 52:3795-3798.
27. Roetzer A, Diel R, Kohl TA, et al. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 2013, 10:e1001387.
28. Coll F, Mallard K, Preston MD, et al. SpolPred: rapid and accurate prediction of Mycobacterium tuberculosis spoligotypes from short genomic sequences. Bioinformatics 2012, 28:2991-2993.
29. Buermans HP, den Dunnen JT Next generation sequencing technology: advances and applications. Biochim Biophys Acta 2014, 1842:1932-1941.
30. Ragheb MN, Ford CB, Chase MR, Lin PL, Flynn JL, Fortune SM The mutation rate of mycobacterial repetitive unit loci in strains of M. tuberculosis from cynomolgus macaque infection. BMC Genomics 2013, 14:145.
31. Cole ST, Brosch R, Parkhill J, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
32. McEvoy CR, Cloete R, Müller B, et al. Comparative analysis of Mycobacterium tuberculosis pe and ppe genes reveals high sequence variation and an apparent absence of selective constraints. PLoS One 2012, 7:e30593.
33. Schürch AC, Kremer K, Daviena O, et al. High-resolution typing by integration of genome sequencing data in a large tuberculosis cluster. J Clin Microbiol 2010, 48:3403-3406.
34. Sanger F, Nicklen S, Coulson AR DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977, 74:5463-5467.
35. Gardy JL, Johnston JC, Ho Sui SJ, et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 2011, 364:730-739.
36. Stucki D, Ballif M, Bodmer T, et al. Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis 2015, 2011:1306-1316.
37. Walker TM, Ip CL, Harrell RH, et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 2013, 13:137-146.
38. Pérez-Lago L, Comas I, Navarro Y, et al. Whole genome sequencing analysis of intrapatient microevolution in Mycobacterium tuberculosis: potential impact on the inference of tuberculosis transmission. J Infect Dis 2014, 209:98-108.
39. Walker TM, Lalor MK, Broda A, et al. Assessment of Mycobacterium tuberculosis transmission in Oxfordshire, UK, 2007-12, with whole pathogen genome sequences: an observational study. Lancet Respir Med 2014, 2:285-292.
40. Glynn JR, Guerra-Assunção JA, Houben RM, et al. Whole genome sequencing shows a low proportion of tuberculosis disease is attributable to known close contacts in Rural Malawi. PLoS One 2015, 10:e0132840.
41. Bryant JM, Schürch AC, van Deutekom H, et al. Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis 2013, 13:110.
42. Kremer K, van Soolingen D, Frothingham R, et al. Comparison of methods based on different molecular epidemiological markers for typing of Mycobacterium tuberculosis complex strains: interlaboratory study of discriminatory power and reproducibility. J Clin Microbiol 1999, 37:2607-2618.
43. Demay C, Liens B, Burguière T, et al. SITVITWEB - a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol 2012, 12:755-766.
44. Sola C, Filliol I, Gutierrez MC, Mokrousov I, Vincent V, Rastogi N Spoligotype database of Mycobacterium tuberculosis: biogeographic distribution of shared types and epidemiologic and phylogenetic perspectives. Emerg Infect Dis 2001, 7:390-396.
45. Supply P, Allix C, Lesjean S, et al. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 2006, 44:4498-4510.
46. Weniger T, Krawczyk J, Supply P, Niemann S, Harmsen D MIRU-VNTRplus: a web tool for polyphasic genotyping of Mycobacterium tuberculosis complex bacteria. Nucleic Acids Res 2010, 38:W326-W331.
47. Comas I, Coscolla M, Luo T, et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 2013, 45:1176-1182.
48. Blouin Y, Hauck Y, Soler C, et al. Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One 2012, 7:e52841.
49. Koren S, Treangen TJ, Hill CM, Pop M, Phillippy AM Automated ensemble assembly and validation of microbial genomes. BMC Bioinformatics 2014, 15:126.
50. Dark MJ Whole-genome sequencing in bacteriology: state of the art. Infect Drug Resist 2013, 6:115-123.
51. Jolley KA, Maiden MC BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010, 11:595.
52. Pérez-Losada M, Cabezas P, Castro-Nallar E, Crandall KA Pathogen typing in the genomics era: MLST and the future of molecular epidemiology. Infect Genet Evol 2013, 16:38-53.
53. Baker L, Brown T, Maiden MC, Drobniewski F Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis 2004, 10:1568-1577.
54. Kohl TA, Diel R, Harmsen D, et al. Whole-genome-based Mycobacterium tuberculosis surveillance: a standardized, portable, and expandable approach. J Clin Microbiol 2014, 52:2479-2486.
55. Guerra-Assunção JA, Crampin AC, Houben RM, et al. Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife 2015, 4:4.
56. Ford CB, Lin PL, Chase MR, et al. Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 2011, 43:482-486.
57. Colangeli R, Arcus VL, Cursons RT, et al. Whole genome sequencing of Mycobacterium tuberculosis reveals slow growth and low mutation rates during latent infections in humans. PLoS One 2014, 9:e91024.
58. Werngren J, Hoffner SE Drug-susceptible Mycobacterium tuberculosis Beijing genotype does not develop mutation-conferred resistance to rifampin at an elevated rate. J Clin Microbiol 2003, 41:1520-1524.
59. Ford CB, Shah RR, Maeda MK, et al. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat Genet 2013, 45:784-790.
60. Casali N, Nikolayevskyy V, Balabanova Y, et al. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat Genet 2014, 46:279-286.
61. Pietersen E, Ignatius E, Streicher EM, et al. Long-term outcomes of patients with extensively drug-resistant tuberculosis in South Africa: a cohort study. Lancet 2014, 383:1230-1239.
62. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 2012, 13:601-612.
63. McGrath M, Gey van Pittius NC, van Helden PD, Warren RM, Warner DF Mutation rate and the emergence of drug resistance in Mycobacterium tuberculosis. J Antimicrob Chemother 2014, 69:292-302.
64. Warner DF, Tønjum T, Mizrahi V DNA metabolism in mycobacterial pathogenesis. Curr Top Microbiol Immunol 2013, 374:27-51.
65. Rock JM, Lang UF, Chase MR, et al. DNA replication fidelity in Mycobacterium tuberculosis is mediated by an ancestral prokaryotic proofreader. Nat Genet 2015, 47:677-681.
66. Cousins DV, Bastida R, Cataldi A, et al. tuberculosis in seals caused by a novel member of the Mycobacterium tuberculosis complex: Mycobacterium pinnipedii sp. nov. Int J Syst Evol Microbiol 2003, 53:1305-1314.
67. Alexander KA, Laver PN, Michel AL, et al. Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerg Infect Dis 2010, 16:1296-1299.
68. Mostowy S, Cousins D, Behr MA Genomic interrogation of the dassie bacillus reveals it as a unique RD1 mutant within the Mycobacterium tuberculosis complex. J Bacteriol 2004, 186:104-109.
69. Parsons SD, Drewe JA, Gey van Pittius NC, Warren RM, van Helden PD Novel cause of tuberculosis in meerkats, South Africa. Emerg Infect Dis 2013, 19:2004-2007.
70. Coscolla M, Lewin A, Metzger S, et al. Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 2013, 19:969-976.
71. van Ingen J, Rahim Z, Mulder A, et al. Characterization of Mycobacterium orygis as M. tuberculosis complex subspecies. Emerg Infect Dis 2012, 18:653-655.
72. Brosch R, Gordon SV, Marmiesse M, et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 2002, 99:3684-3689.
73. Pfyffer GE, Auckenthaler R, van Embden JD, van Soolingen D Mycobacterium canettii, the smooth variant of M. tuberculosis, isolated from a Swiss patient exposed in Africa. Emerg Infect Dis 1998, 4:631-634.
74. van Soolingen D, Hoogenboezem T, de Haas PE, et al. A novel pathogenic taxon of the Mycobacterium tuberculosis complex, Canetti: characterization of an exceptional isolate from Africa. Int J Syst Bacteriol 1997, 47:1236-1245.
75. Supply P, Marceau M, Mangenot S, et al. Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat Genet 2013, 45:172-179.
76. Hill V, Zozio T, Sadikalay S, et al. MLVA based classification of Mycobacterium tuberculosis complex lineages for a robust phylogeographic snapshot of its worldwide molecular diversity. PLoS One 2012, 7:e41991.
77. Zhang J, Abadia E, Refregier G, et al. Mycobacterium tuberculosis complex CRISPR genotyping: improving efficiency, throughput and discriminative power of 'spoligotyping' with new spacers and a microbead-based hybridization assay. J Med Microbiol 2010, 59:285-294.
78. Brites D, Gagneux S Co-evolution of Mycobacterium tuberculosis and Homo sapiens. Immunol Rev 2015, 264:6-24.
79. Bottai D, Stinear TP, Supply P, Brosch R Mycobacterial pathogenomicas and evolution. Microbiol Spectrum 2014, 2. MGM2-0025-2013.
80. Firdessa R, Berg S, Hailu E, et al. Mycobacterial lineages causing pulmonary and extrapulmonary tuberculosis, Ethiopia. Emerg Infect Dis 2013, 19:460-463.
81. Coscolla M, Gagneux S Consequences of genomic diversity in Mycobacterium tuberculosis. Semin Immunol 2014, 26:431-444.
82. Merker M, Blin C, Mona S, et al. Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage. Nat Genet 2015, 47:242-249.
83. Hanekom M, van der Spuy GD, Streicher E, et al. A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family is associated with an increased ability to spread and cause disease. J Clin Micro 2007, 45:1483-1490.
84. Ribeiro SC, Gomes LL, Amaral EP, et al. Mycobacterium tuberculosis strains of the modern sublineage of the Beijing family are more likely to display increased virulence than strains of the ancient sublineage. J Clin Microbiol 2014, 52:2615-2624.
85. Faksri K, Chaiprasert A, Pardieu C, et al. Heterogeneity of phenotypic characteristics of the modern and ancestral Beijing strains of Mycobacterium tuberculosis. Asian Pac J Allergy Immunol 2014, 32:124-132.
86. van Laarhoven A, Mandemakers JJ, Kleinnijenhuis J, et al. Low induction of proinflammatory cytokines parallels evolutionary success of modern strains within the Mycobacterium tuberculosis Beijing genotype. Infect Immun 2013, 81:3750-3756.
87. Chen Y-Y, Chang J-R, Huang W-F, et al. The pattern of cytokine production in vitro induced by ancient and modern Beijing Mycobacterium tuberculosis strains. PLoS One 2014, 9:e94296.
88. Luo T, Comasc I, Luo D, et al. Southern east Asian origin and coexpansion of Mycobacterium tuberculosis Beijing family with Han Chinese. PNAS 2015, 112:8136-8141.
89. Mokrousov I Insights into the origin, emergence, and current spread of a successful Russian clone of Mycobacterium tuberculosis. Clin Microbiol Rev 2013, 26:342-360.
90. Ahidjo BA, Kuhnert D, McKenzie JL, et al. VapC toxins from Mycobacterium tuberculosis are ribonucleases that differentially inhibit growth and are neutralized by cognate VapB antitoxins. PLoS One 2011, 6:e21738.
91. Gioffré A, Infante E, Aguilar D, et al. Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect 2005, 7:325-334.
92. Stavrum R, Stavrum AK, Valvatne H, et al. Modulation of transcriptional and inflammatory responses in murine macrophages by the Mycobacterium tuberculosis mammalian cell entry (Mce) 1 complex. PLoS One 2011, 6:e26295.
93. Parish T, Smith DA, Kendall S, Casali N, Bancroft GJ, Stoker NG Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect Immun 2003, 71:1134-1140.
94. Shilova MV, Dye C The resurgence of tuberculosis in Russia. Philos Trans R Soc Lond B Biol Sci 2001, 356:1069-1075.
95. Kiers A, Klarenbeek A, Mendelts B, Van Soolingen D, Koëter G Transmission of Mycobacterium pinnipedii to humans in a zoo with marine mammals. Int J Tuberc Lung Dis 2008, 12:1469-1473.
96. Kay GL, Sergeant MJ1, Zhou Z, et al. Eighteenth-century genomes show that mixed infections were common at time of peak tuberculosis in Europe. Nat Commun 2015, 6:6717.
97. Arriaza BT, Salo W, Aufderheide AC, Holcomb TA Pre-Columbian tuberculosis in northern Chile: molecular and skeletal evidence. Am J Phys Anthropol 1995, 98:37-45.
98. Gómez i Prat J, de Souza SM Prehistoric tuberculosis in America: adding comments to a literature review. Mem Inst Oswaldo Cruz 2003, 98(suppl 1):151-159.
99. de Jong BC, Antonio M, Gagneux S Mycobacterium africanum - review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 2010, 4:e744.
100. Groenheit R, Ghebremichael S, Svensson J, et al. The Guinea-Bissau family of Mycobacterium tuberculosis complex revisited. PLoS One 2011, 6:e18601.
101. Godreuil S, Torrea G, Terru D, et al. First molecular epidemiology study of Mycobacterium tuberculosis in Burkina Faso. J Clin Microbiol 2007, 45:921-927.
102. Niobe-Eyangoh SN, Kuaban C, Sorlin P, et al. Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon. J Clin Microbiol 2003, 41:2547-2553.
103. Gehre F, Otu J, DeRiemer K, et al. Deciphering the growth behaviour of Mycobacterium africanum. PLoS Negl Trop Dis 2013, 7:e2220.
104. Sassetti CM, Boyd DH, Rubin EJ Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 2003, 48:77-84.
105. Behr MA, Gordon SV Why doesn't Mycobacterium tuberculosis spread in animals?. Trends Microbiol 2015, 23:1-2.
106. Zhang Y, Heym B, Allen B, Young D, Cole S The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 1992, 358:591-593.
107. Takiff HE, Cimino M, Musso MC, et al. Efflux pump of the proton antiporter family confers low-level fluoroquinolone resistance in Mycobacterium smegmatis. Proc Natl Acad Sci USA 1996, 93:362-366.
108. Lechartier B, Rybniker J, Zumla A, Cole ST Tuberculosis drug discovery in the post-post-genomic era. EMBO Mol Med 2014, 6:158-168.
109. Ioerger TR, O'Malley T, Liao R, et al. Identification of new drug targets and resistance mechanisms in Mycobacterium tuberculosis. PLoS One 2013, 8:e75245.
110. Andries K, Verhasselt P, Guillemont J, et al. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 2005, 307:223-227.
111. Goldman RC Why are membrane targets discovered by phenotypic screens and genome sequencing in Mycobacterium tuberculosis?. Tuberculosis (Edinb) 2013, 93:569-588.
112. Li K, Schurig-Briccio LA, Feng X, et al. Multitarget drug discovery for tuberculosis and other infectious diseases. J Med Chem 2014, 57:3126-3139.
113. Li W, Upadhyay A, Fontes FL, et al. Novel insights into the mechanism of inhibition of MmpL3, a target of multiple pharmacophores in Mycobacterium tuberculosis. Antimicrob Agents Chemother 2014, 58:6413-6423.
114. Trauner A, Sassetti CM, Rubin EJ Genetic strategies for identifying new drug targets. Microbiol Spectrum 2014, 2. MGM2-0030-2013.
115. Lanzas F, Karakousis PC, Sacchettini JC, Ioerger TR Multidrug-resistant tuberculosis in panama is driven by clonal expansion of a multidrug-resistant Mycobacterium tuberculosis strain related to the KZN extensively drug-resistant M. tuberculosis strain from South Africa. J Clin Microbiol 2013, 51:3277-3285.
116. Eldholm V, Monteserin J, Rieux A, et al. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat Commun 2015, 6:7119.
117. Wozniak M, Tiuryn J, Wong L GWAMAR: genome-wide assessment of mutations associated with drug resistance in bacteria. BMC Genomics 2014, 15(suppl 10):S10.
118. Pym AS, Saint-Joanis B, Cole ST Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect Immun 2002, 70:4955-4960.
119. Wang F, Langley R, Gulten G, et al. Mechanism of thioamide drug action against tuberculosis and leprosy. J Exp Med 2007, 204:73-78.
120. Sherman DR, Mdluli K, Hickey MJ, et al. Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 1996, 272:1641-1643.
121. Ramaswamy S, Musser JM Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. Tuber Lung Dis 1998, 79:3-29.
122. Mariam DH, Mengistu Y, Hoffner SE, Andersson DI Effect of rpoB mutations conferring rifampin resistance on fitness of Mycobacterium tuberculosis. Antimicrob Agents Chemother 2004, 48:1289-1294.
123. Gagneux S, Long CD, Small PM, Van T, Schoolnik GK, Bohannan BJ The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 2006, 312:1944-1946.
124. Comas I, Borrell S, Roetzer A, et al. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet 2012, 44:106-110.
125. Koch A, Mizrahi V, Warner DF The impact of drug resistance on Mycobacterium tuberculosis physiology: what can we learn from rifampicin?. Emerg Microbes Infect 2014, 3:e17.
126. Trindade S, Sousa A, Xavier KB, Dionisio F, Ferreira MG, Gordo I Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet 2009, 5:e1000578.
127. de Vos M, Müller B, Borrell S, et al. Putative compensatory mutations in the rpoC gene of rifampin-resistant Mycobacterium tuberculosis are associated with ongoing transmission. Antimicrob Agents Chemother 2013, 57:827-832.
128. Brandis G, Hughes D Genetic characterization of compensatory evolution in strains carrying rpoB Ser531Leu, the rifampicin resistance mutation most frequently found in clinical isolates. J Antimicrob Chemother 2013, 68:2493-2497.
129. Brandis G, Wrande M, Liljas L, Hughes D Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol Microbiol 2012, 85:142-151.
130. Dover LG, Alahari A, Gratraud P, et al. EthA, a common activator of thiocarbamide-containing drugs acting on different mycobacterial targets. Antimicrob Agents Chemother 2007, 51:1055-1063.
131. Ginsburg AS, Woolwine SC, Hooper N, et al. The rapid development of fluoroquinolone resistance in M. tuberculosis. N Engl J Med 2003, 349:1977-1978.
132. Takiff H, Guerrero E Current prospects for the fluoroquinolones as first-line tuberculosis therapy. Antimicrob Agents Chemother 2011, 55:5421-5429.
133. Streicher EM, Bergval I, Dheda K, et al. Mycobacterium tuberculosis population structure determines the outcome of genetics-based second-line drug resistance testing. Antimicrob Agents Chemother 2012, 56:2420-2427.
134. Zhang X, Zhao B, Liu L, Zhu Y, Zhao Y, Jin Q Subpopulation analysis of heteroresistance to fluoroquinolone in Mycobacterium tuberculosis isolates from Beijing, China. J Clin Microbiol 2012, 50:1471-1474.
135. Sun G, Luo T, Yang C, et al. Dynamic population changes in Mycobacterium tuberculosis during acquisition and fixation of drug resistance in patients. J Infect Dis 2012, 206:1724-1733.
136. Merker M, Kohl TA, Roetzer A, et al. Whole genome sequencing reveals complex evolution patterns of multidrug-resistant Mycobacterium tuberculosis Beijing strains in patients. PLoS One 2013, 8:e82551.
137. Eldholm V, Norheim G, von der Lippe B, et al. Evolution of extensively drug-resistant Mycobacterium tuberculosis from a susceptible ancestor in a single patient. Genome Biol 2014, 15:490.
138. Farhat MR, Shapiro BJ, Kieser KJ, et al. Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat Genet 2013, 45:1183-1189.
139. Farhat MR, Shapiro BJ, Sheppard SK, Colijn C, Murray M A phylogeny-based sampling strategy and power calculator informs genome-wide associations study design for microbial pathogens. Genome Med 2014, 6:101.
140. Zhang H, Li D, Zhao L, et al. Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat Genet 2013, 45:1255-1260.
141. Perdigão J, Macedo R, Ribeiro A, Brum L, Portugal I Genetic characterisation of the ethambutol resistance-determining region in Mycobacterium tuberculosis: prevalence and significance of embB306 mutations. Int J Antimicrob Agents 2009, 33:334-338.
142. Guerrero E, Lemus D, Yzquierdo S, et al. Association between embB mutations and ethambutol resistance in Mycobacterium tuberculosis isolates from Cuba and the Dominican Republic: reproducible patterns and problems. Rev Argent Microbiol 2013, 45:21-26.
143. Safi H, Lingaraju S, Amin A, et al. Evolution of high-level ethambutol-resistant tuberculosis through interacting mutations in decaprenylphosphoryl-β-D-arabinose biosynthetic and utilization pathway genes. Nat Genet 2013, 45:1190-1197.
144. Golby P, Nunez J, Witney A, et al. Genome-level analyses of Mycobacterium bovis lineages reveal the role of SNPs and antisense transcription in differential gene expression. BMC Genomics 2013, 14:710.
145. Rose G, Cortes T, Comas I, Coscolla M, Gagneux S, Young DB Mapping of genotype-phenotype diversity among clinical isolates of Mycobacterium tuberculosis by sequence-based transcriptional profiling. Genome Biol Evol 2013, 5:1849-1862.
146. Schürch AC, Kremer K, Warren RM, et al. Mutations in the regulatory network underlie the recent clonal expansion of a dominant subclone of the Mycobacterium tuberculosis Beijing genotype. Infect Genet Evol 2011, 11:587-597.
147. Coll F, Preston M, Guerra-Assunção JA, et al. PolyTB: a genomic variation map for Mycobacterium tuberculosis. Tuberculosis (Edinb) 2014, 94:346-354.
148. Chernyaeva EN, Shulgina MV, Rotkevich MS, et al. Genome-wide Mycobacterium tuberculosis variation (GMTV) database: a new tool for integrating sequence variations and epidemiology. BMC Genomics 2014, 15:308.
149. Joshi KR, Dhiman H, Scaria V tbvar: a comprehensive genome variation resource for Mycobacterium tuberculosis. Database (Oxford) 2014, 2014:bat083.
150. Sandgren A, Strong M, Muthukrishnan P, Weiner BK, Church GM, Murray MB Tuberculosis drug resistance mutation database. PLoS Med 2009, 6:e2.
151. Vishnoi A, Srivastava A, Roy R, Bhattacharya A MGDD: Mycobacterium tuberculosis genome divergence database. BMC Genomics 2008, 9:373.
152. Bharti R, Das R, Sharma P, Katoch K, Bhattacharya A MTCID: a database of genetic polymorphisms in clinical isolates of Mycobacterium tuberculosis. Tuberculosis (Edinb) 2012, 92:166-172.
153. Sherry ST, Ward MH, Kholodov M, et al. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 2001, 29:308-311.
154. Reddy TB, Riley R, Wymore F, et al. TB database: an integrated platform for tuberculosis research. Nucleic Acids Res 2009, 37:D499-D508.
155. Lew JM, Kapopoulou A, Jones LM, Cole ST TubercuList - 10 years after. tuberculosis (Edinb) 2011, 91:1-7.
156. Bhardwaj A, Bhartiya D, Kumar N, Scaria V TBrowse: an integrative genomics map of Mycobacterium tuberculosis. tuberculosis (Edinb) 2009, 89:386-387. the Open Source Drug Discovery Consortium.
157. Lin SY, Rodwell TC, Victor TC, et al. Pyrosequencing for rapid detection of extensively drug-resistant Mycobacterium tuberculosis in clinical isolates and clinical specimens. J Clin Microbiol 2014, 52:475-482.
158. Ajbani K, Lin SY, Rodrigues C, et al. Evaluation of pyrosequencing for detecting extensively drug-resistant Mycobacterium tuberculosis among clinical isolates from four high-burden countries. Antimicrob Agents Chemother 2015, 59:414-420.
159. Outhred AC, Jelfs P, Suliman B, et al. Added value of whole-genome sequencing for management of highly drug-resistant TB. J Antimicrob Chemother 2015, 70:1198-1202.
160. Gordon NC, Price JR, Cole K, et al. Prediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencing. J Clin Microbiol 2014, 52:1182-1191.
161. Price J, Gordon NC, Crook D, Llewelyn M, Paul J The usefulness of whole genome sequencing in the management of Staphylococcus aureus infections. Clin Microbiol Infect 2013, 19:784-789.
162. Steiner A, Stucki D, Coscolla M, Borrell S, Gagneux S KvarQ: targeted and direct variant calling from fastq reads of bacterial genomes. BMC Genomics 2014, 15:881.
163. Feuerriegel S, Schleusener V, Beckert P, et al. PhyResSE: web tool delineating Mycobacterium tuberculosis antibiotic resistance and lineage from whole-genome sequencing data. J Clin Microbiol 2015, 53:1908-1914.
164. Flandrois JP, Lina G, Dumitrescu O MUBII-TB-DB: a database of mutations associated with antibiotic resistance in Mycobacterium tuberculosis. BMC Bioinformatics 2014, 15:107.
165. Walker TM, Kohl TA, Omar SV, et al. Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis 2015, for the Modernizing Medical Microbiology (MMM) Informatics Group, published online June 23. http://dx.doi.org/10.1016/S1473-3099(15)00062-6.
166. Coll F, McNerney R, Preston MD, et al. Rapid determination of anti-tuberculosis drug resistance from whole-genome sequences. Genome Med 2015, 7:51.
167. Ali A, Hasan Z, McNerney R, et al. Whole genome sequencing based characterization of extensively drug-resistant Mycobacterium tuberculosis isolates from Pakistan. PLoS One 2015, 10:e0117771.
168. Li H, Kayani MU, Gu Y, et al. Transmitted extended-spectrum XDR tuberculosis in Beijing with discordant whole-genome sequencing analysis. J Clin Microbiol 2015, 53:2781-2784.
169. Gardy JL Towards genomic prediction of drug resistance in tuberculosis. Lancet Infect Dis 2015, published online June 23. http://dx.doi.org/10.1016/S1473-3099(15)00088-2.
170. Witney AA, Gould KA, Arnold A, et al. Clinical application of whole-genome sequencing to inform treatment for multidrug-resistant tuberculosis cases. J Clin Microbiol 2015, 53:1473-1483.
171. Schürch AC, Kremer K, Hendriks AC, et al. SNP/RD typing of Mycobacterium tuberculosis Beijing strains reveals local and worldwide disseminated clonal complexes. PLoS One 2011, 6:e28365.
172. Plikaytis BB, Marden JL, Crawford JT, Woodley CL, Butler WR, Shinnick TM Multiplex PCR assay specific for the multidrug-resistant strain W of Mycobacterium tuberculosis. J Clin Microbiol 1994, 32:1542-1546.
173. Homolka S, Projahn M, Feuerriegel S, et al. High resolution discrimination of clinical Mycobacterium tuberculosis complex strains based on single nucleotide polymorphisms. PLoS One 2012, 7:e39855.
174. Coll F, McNerney R, Guerra-Assunção JA, et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat Commun 2014, 5:4812.
175. Perez-Lago L, Martinez Lirola M, Herranz M, Comas I, Bouza E, Garcia-de-Viedma D Fast and low-cost decentralized surveillance of transmission of tuberculosis based on strain-specific PCRs tailored from whole genome sequencing data: a pilot study. Clin Microbiol Infect 2015, 21:249.e1-249.e9.
176. Bergval I, Sengstake S, Brankova N, et al. Combined species identification, genotyping, and drug resistance detection of Mycobacterium tuberculosis cultures by MLPA on a bead-based array. PLoS One 2012, 7:e43240.
177. Sengstake S, Bablishvili N, Schuitema A, et al. Optimizing multiplex SNP-based data analysis for genotyping of Mycobacterium tuberculosis isolates. BMC Genomics 2014, 15:572.
178. Cowan LS, Diem L, Brake MC, Crawford JT Transfer of a Mycobacterium tuberculosis genotyping method, Spoligotyping, from a reverse line-blot hybridization, membrane-based assay to the Luminex multianalyte profiling system. J Clin Microbiol 2004, 42:474-477.
179. Abadia E, Zhang J, Ritacco V, et al. The use of microbead-based spoligotyping for Mycobacterium tuberculosis complex to evaluate the quality of the conventional method: providing guidelines for Quality Assurance when working on membranes. BMC Infect Dis 2011, 11:110.
180. Gomgnimbou MK, Hernández-Neuta I, Panaiotov S, et al. Tuberculosis-spoligo-rifampin-isoniazid typing: an all-in-one assay technique for surveillance and control of multidrug-resistant tuberculosis on Luminex devices. J Clin Microbiol 2013, 51:3527-3534.
181. Stucki D, Malla B, Hostettler S, et al. Two new rapid SNP-typing methods for classifying Mycobacterium tuberculosis complex into the main phylogenetic lineages. PLoS One 2012, 7:e41253.
182. Okumura K, Kato M, Kirikae T, Kayano M, Miyoshi-Akiyama T Construction of a virtual Mycobacterium tuberculosis consensus genome and its application to data from a next generation sequencer. BMC Genomics 2015, 16:218.
183. Mattei TA Biomimetic nanopores: a new age of DNA sequencing?. World Neurosurg 2014, 82:252-254.
184. Mikheyev AS, Tin MM A first look at the Oxford Nanopore MinION sequencer. Mol Ecol Resour 2014, 14:1097-1102.
185. Doughty EL, Sergeant MJ, Adetifa I, Antonio M, Pallen MJ Culture-independent detection and characterisation of Mycobacterium tuberculosis and M africanum in sputum samples using shotgun metagenomics on a benchtop sequencer. PeerJ 2014, 2:e585.
186. Seth-Smith HM, Harris SR, Skilton RJ, et al. Whole-genome sequences of Chlamydia trachomatis directly from clinical samples without culture. Genome Res 2013, 23:855-866.
187. Lasken RS Genomic sequencing of uncultured microorganisms from single cells. Nat Rev Microbiol 2012, 10:631-640.
188. Grant IR, Ball HJ, Rowe MT Isolation of Mycobacterium paratuberculosis from milk by immunomagnetic separation. Appl Environ Microbiol 1998, 64:3153-3158.
189. Bergval I, Coll F, Schuitema A, et al. A proportion of mutations fixed in the genomes of in vitro selected isogenic drug-resistant Mycobacterium tuberculosis mutants can be detected as minority variants in the parent culture. FEMS Microbiol Lett 2015, 362:1-7.
190. Votintseva AA, Pankhurst LJ, Anson LW, et al. Mycobacterial DNA extraction for whole-genome sequencing from early positive liquid (MGIT) cultures. J Clin Microbiol 2015, 53:1137-1143.
191. Albert H, Ademun PJ, Lukyamuzi G, et al. Feasibility of magnetic bead technology for concentration of mycobacteria in sputum prior to fluorescence microscopy. BMC Infect Dis 2011, 11:125.
192. Ghodbane R, Drancourt M Magnetic bead protocol for culturing Mycobacterium tuberculosis from sputum specimens. J Clin Microbiol 2013, 51:1578-1579.
193. Liu J, Sun Z-Q, Pei H, et al. Increased case finding of tuberculosis from sputum and sputum deposits after magnetic bead concentration of mycobacteria. J Microbiol Methods 2013, 93:144-147.
194. Brown AC, Bryant JM, Einer-Jensen K, et al. Rapid whole-genome sequencing of Mycobacterium tuberculosis isolates directly from clinical samples. J Clin Microbiol 2015, 53:2230-2237.
195. Vadwai V, Boehme C, Nabeta P, Shetty A, Alland D, Rodrigues C Xpert MTB/RIF: a new pillar in diagnosis of extrapulmonary tuberculosis?. J Clin Microbiol 2011, 49:2540-2545.
196. Underwood A, Green J Call for a quality standard for sequence-based assays in clinical microbiology: necessity for quality assessment of sequences used in microbial identification and typing. J Clin Microbiol 2011, 49:23-26.
197. Gargis AS, Kalman L, Berry MW, et al. Assuring the quality of next-generation sequencing in clinical laboratory practice. Nat Biotechnol 2012, 30:1033-1036.