Disclosure of selective advantages in the "modern" sublineage of the Mycobacterium tuberculosis Beijing genotype family by quantitative proteomics

Molecular and Cellular Proteomics

Volumn 13, Issue 10, 2014, Pages 2632-2645

  De Keijzer, Jeroen ^a   De Haas, Petra E ^b   De Ru, Arnoud H ^a   Van Veelen, Peter A ^a   Van Soolingen, Dick ^b,c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ETHAMBUTOL; ISONIAZID; MEMBRANE PROTEIN; PROTEOME; RIFAMPICIN; RV0450C MMPL4 PROTEIN; RV1269C PROTEIN; RV3137 PROTEIN; RV3283 SSEA PROTEIN; THIOSULFATE SULFURTRANSFERASE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ALGORITHM; AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM ISOLATE; CELL LYSATE; ENZYME ACTIVITY; GENE INSERTION SEQUENCE; GENETIC CONSERVATION; GENOTYPE; HYDROPHOBICITY; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS BEIJING STRAIN; NONHUMAN; NONSYNONYMOUS SINGLE NUCLEOTIDE POLYMORPHISM; PHYSICAL CHEMISTRY; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN STABILITY; PROTEOMICS; QUANTITATIVE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; VARIABLE NUMBER OF TANDEM REPEAT; WILD TYPE; ADAPTATION; CLASSIFICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PATHOGENICITY; PHYSIOLOGY; PROCEDURES;

MYCOBACTERIUM TUBERCULOSIS;

ADAPTATION, PHYSIOLOGICAL; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENOTYPE; MYCOBACTERIUM TUBERCULOSIS; PROTEOMICS; VIRULENCE FACTORS;

EID: 84931094609     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.038380     Document Type: Article

References (93)

1. Organisation, W. H. (2013) Global Tuberculosis Report 2013. 306
2. Schurch, A. C., and van Soolingen, D. (2012) DNA fingerprinting of Mycobacterium tuberculosis: from phage typing to whole-genome sequencing. Infect. Genet. Evol. 12, 602-609
3. Brosch, R., Gordon, S. V., Marmiesse, M., Brodin, P., Buchrieser, C., Eiglmeier, K., Garnier, T., Gutierrez, C., Hewinson, G., Kremer, K., Parsons, L. M., Pym, A. S., Samper, S., van Soolingen, D., and Cole, S. T. (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl. Acad. Sci. U. S. A. 99, 3684-3689
4. Hershberg, R., Lipatov, M., Small, P. M., Sheffer, H., Niemann, S., Homolka, S., Roach, J. C., Kremer, K., Petrov, D. A., Feldman, M. W., and Gagneux, S. (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6, e311
5. van Soolingen, D., Qian, L., de Haas, P. E., Douglas, J. T., Traore, H., Portaels, F., Qing, H. Z., Enkhsaikan, D., Nymadawa, P., and van Embden, J. D. (1995) Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J. Clin. Microbiol. 33, 3234-3238
6. Glynn, J. R., Whiteley, J., Bifani, P. J., Kremer, K., and van Soolingen, D. (2002) Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg. Infect. Dis. 8, 843-849
7. Parwati, I., Alisjahbana, B., Apriani, L., Soetikno, R. D., Ottenhoff, T. H., van der Zanden, A. G., van der Meer, J., van Soolingen, D., and van Crevel, R. (2010) Mycobacterium tuberculosis Beijing genotype is an independent risk factor for tuberculosis treatment failure in Indonesia. J. Infect. Dis. 201, 553-557
8. Kremer, K., Glynn, J. R., Lillebaek, T., Niemann, S., Kurepina, N. E., Kreiswirth, B. N., Bifani, P. J., and van Soolingen, D. (2004) Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J. Clin. Microbiol. 42, 4040-4049
9. Kremer, K., van-der-Werf, M. J., Au, B. K., Anh, D. D., Kam, K. M., van-Doorn, H. R., Borgdorff, M. W., and van-Soolingen, D. (2009) Vaccine-induced immunity circumvented by typical Mycobacterium tuberculosis Beijing strains. Emerg. Infect. Dis. 15, 335-339
10. Devaux, I., Kremer, K., Heersma, H., and Van Soolingen, D. (2009) Clusters of multidrug-resistant Mycobacterium tuberculosis cases, Europe. Emerg. Infect. Dis. 15, 1052-1060
11. Buu, T. N., van Soolingen, D., Huyen, M. N., Lan, N. T., Quy, H. T., Tiemersma, E. W., Kremer, K., Borgdorff, M. W., and Cobelens, F. G. (2012) Increased transmission of Mycobacterium tuberculosis Beijing genotype strains associated with resistance to streptomycin: a population-based study. PloS One 7, e42323
12. Buu, T. N., Huyen, M. N., Lan, N. T., Quy, H. T., Hen, N. V., Zignol, M., Borgdorff, M. W., Cobelens, F. G., and van Soolingen, D. (2009) The Beijing genotype is associated with young age and multidrug-resistant tuberculosis in rural Vietnam. Int. J. Tuberc. Lung Dis. 13, 900-906
13. Lopez, B., Aguilar, D., Orozco, H., Burger, M., Espitia, C., Ritacco, V., Barrera, L., Kremer, K., Hernandez-Pando, R., Huygen, K., and van Soolingen, D. (2003) A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin. Exp. Immunol. 133, 30-37
14. Abebe, F., and Bjune, G. (2006) The emergence of Beijing family genotypes of Mycobacterium tuberculosis and low-level protection by bacille Calmette-Guerin (BCG) vaccines: is there a link? Clin. Exp. Immunol. 145, 389-397
15. Grode, L., Seiler, P., Baumann, S., Hess, J., Brinkmann, V., Nasser Eddine, A., Mann, P., Goosmann, C., Bandermann, S., Smith, D., Bancroft, G. J., Reyrat, J. M., van Soolingen, D., Raupach, B., and Kaufmann, S. H. (2005) Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J. Clin. Invest. 115, 2472-2479
16. Anh, D. D., Borgdorff, M. W., Van, L. N., Lan, N. T., van Gorkom, T., Kremer, K., and van Soolingen, D. (2000) Mycobacterium tuberculosis Beijing genotype emerging in Vietnam. Emerg. Infect. Dis. 6, 302-305
17. van der Spuy, G. D., Kremer, K., Ndabambi, S. L., Beyers, N., Dunbar, R., Marais, B. J., van Helden, P. D., and Warren, R. M. (2009) Changing Mycobacterium tuberculosis population highlights clade-specific pathogenic characteristics. Tuberculosis 89, 120-125
18. van Crevel, R., Parwati, I., Sahiratmadja, E., Marzuki, S., Ottenhoff, T. H., Netea, M. G., van der Ven, A., Nelwan, R. H., van der Meer, J. W., Alisjahbana, B., and van de Vosse, E. (2009) Infection with Mycobacterium tuberculosis Beijing genotype strains is associated with polymorphisms in SLC11A1/NRAMP1 in Indonesian patients with tuberculosis. J. Infect. Dis. 200, 1671-1674
19. Ebrahimi-Rad, M., Bifani, P., Martin, C., Kremer, K., Samper, S., Rauzier, J., Kreiswirth, B., Blazquez, J., Jouan, M., van Soolingen, D., and Gicquel, B. (2003) Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family. Emerg. Infect. Dis. 9, 838-845
20. de Steenwinkel, J. E., ten Kate, M. T., de Knegt, G. J., Kremer, K., Aarnoutse, R. E., Boeree, M. J., Verbrugh, H. A., van Soolingen, D., and Bakker-Woudenberg, I. A. (2012) Drug susceptibility of Mycobacterium tuberculosis Beijing genotype and association with MDR TB. Emerg. Infect. Dis. 18, 660-663
21. Ford, C. B., Shah, R. R., Maeda, M. K., Gagneux, S., Murray, M. B., Cohen, T., Johnston, J. C., Gardy, J., Lipsitch, M., and Fortune, S. M. (2013) Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat. Genet. 45, 784-790
22. Dong, H., Shi, L., Zhao, X., Sang, B., Lv, B., Liu, Z., and Wan, K. (2012) Genetic diversity of Mycobacterium tuberculosis isolates from Tibetans in Tibet, China. PloS One 7, e33904
23. Yu, Q., Su, Y., Lu, B., Ma, Y., Zhao, X., Yang, X., Dong, H., Liu, Y., Lian, L., Wan, L., Wu, Y., and Wan, K. (2013) Genetic diversity of Mycobacterium tuberculosis isolates from Inner Mongolia, China. PloS One 8, e57660
24. Casali, N., Nikolayevskyy, V., Balabanova, Y., Ignatyeva, O., Kontsevaya, I., Harris, S. R., Bentley, S. D., Parkhill, J., Nejentsev, S., Hoffner, S. E., Horstmann, R. D., Brown, T., and Drobniewski, F. (2012) Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res. 22, 735-745
25. Johnson, R., Warren, R. M., van der Spuy, G. D., Gey van Pittius, N. C., Theron, D., Streicher, E. M., Bosman, M., Coetzee, G. J., van Helden, P. D., and Victor, T. C. (2010) Drug-resistant tuberculosis epidemic in the Western Cape driven by a virulent Beijing genotype strain. Int. J. Tuberc. Lung Dis. 14, 119-121
26. European Concerted Action on New Generation Genetic, M., Techniques for the, E., and Control of, T. (2006) Beijing/W genotype Mycobacterium tuberculosis and drug resistance. Emerg. Infect. Dis. 12, 736-743
27. Mokrousov, I., Narvskaya, O., Otten, T., Vyazovaya, A., Limeschenko, E., Steklova, L., and Vyshnevskyi, B. (2002) Phylogenetic reconstruction within Mycobacterium tuberculosis Beijing genotype in northwestern Russia. Res. Microbiol. 153, 629-637
28. Iwamoto, T. (2009) Population structure analysis of Mycobacterium tuberculosis Beijing family in Japan. Kekkaku : Tuberculosis 84, 755-759
29. Tsolaki, A. G., Gagneux, S., Pym, A. S., Goguet de la Salmoniere, Y. O., Kreiswirth, B. N., Van Soolingen, D., and Small, P. M. (2005) Genomic deletions classify the Beijing/W strains as a distinct genetic lineage of Mycobacterium tuberculosis. J. Clin. Microbiol. 43, 3185-3191
30. Schurch, A. C., Kremer, K., Warren, R. M., Hung, N. V., Zhao, Y., Wan, K., Boeree, M. J., Siezen, R. J., Smith, N. H., and van Soolingen, D. (2011) Mutations in the regulatory network underlie the recent clonal expansion of a dominant subclone of the Mycobacterium tuberculosis Beijing genotype. Infect. Genet. Evol.. 11, 587-597
31. Hanekom, M., van der Spuy, G. D., Streicher, E., Ndabambi, S. L., McEvoy, C. R., Kidd, M., Beyers, N., Victor, T. C., van Helden, P. D., and Warren, R. M. (2007) A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family is associated with an increased ability to spread and cause disease. J. Clin. Microbiol. 45, 1483-1490
32. van Laarhoven, A., Mandemakers, J. J., Kleinnijenhuis, J., Enaimi, M., Lachmandas, E., Joosten, L. A., Ottenhoff, T. H., Netea, M. G., van Soolingen, D., and van Crevel, R. (2013) Low induction of proinflammatory cytokines parallels evolutionary success of modern strains within the Mycobacterium tuberculosis Beijing genotype. Infect. Immun. 81, 3750-3756
33. Jungblut, P. R., Schaible, U. E., Mollenkopf, H. J., Zimny-Arndt, U., Raupach, B., Mattow, J., Halada, P., Lamer, S., Hagens, K., and Kaufmann, S. H. (1999) Comparative proteome analysis of Mycobacterium tuberculosis and Mycobacterium bovis BCG strains: towards functional genomics of microbial pathogens. Mol. Microbiol. 33, 1103-1117
34. de Souza, G. A., Fortuin, S., Aguilar, D., Pando, R. H., McEvoy, C. R., van Helden, P. D., Koehler, C. J., Thiede, B., Warren, R. M., and Wiker, H. G. (2010) Using a label-free proteomics method to identify differentially abundant proteins in closely related hypo- and hypervirulent clinical Mycobacterium tuberculosis Beijing isolates. Mol. Cell. Proteomics 9, 2414-2423
35. Neubauer, H., Clare, S. E., Kurek, R., Fehm, T., Wallwiener, D., Sotlar, K., Nordheim, A., Wozny, W., Schwall, G. P., Poznanovic, S., Sastri, C., Hunzinger, C., Stegmann, W., Schrattenholz, A., and Cahill, M. A. (2006) Breast cancer proteomics by laser capture microdissection, sample pooling, 54-cm IPG IEF, and differential iodine radioisotope detection. Electrophoresis 27, 1840-1852
36. Diz, A. P., Truebano, M., and Skibinski, D. O. (2009) The consequences of sample pooling in proteomics: an empirical study. Electrophoresis 30, 2967-2975
37. Geiger, T., Cox, J., Ostasiewicz, P., Wisniewski, J. R., and Mann, M. (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods 7, 383-385
38. Deeb, S. J., D'Souza, R. C., Cox, J., Schmidt-Supprian, M., and Mann, M. (2012) Super-SILAC allows classification of diffuse large B-cell lymphoma subtypes by their protein expression profiles. Mol. Cell. Proteomics 11, 77-89
39. Schubert, O. T., Mouritsen, J., Ludwig, C., Rost, H. L., Rosenberger, G., Arthur, P. K., Claassen, M., Campbell, D. S., Sun, Z., Farrah, T., Gengenbacher, M., Maiolica, A., Kaufmann, S. H., Moritz, R. L., and Aebersold, R. (2013) The Mtb proteome library: a resource of assays to quantify the complete proteome of Mycobacterium tuberculosis. Cell Host Microbe 13, 602-612
40. Schurch, A. C., Kremer, K., Hendriks, A. C., Freyee, B., McEvoy, C. R., van Crevel, R., Boeree, M. J., van Helden, P., Warren, R. M., Siezen, R. J., and van Soolingen, D. (2011) SNP/RD typing of Mycobacterium tuberculosis Beijing strains reveals local and worldwide disseminated clonal complexes. PloS One 6, e28365
41. Bifani, P. J., Mathema, B., Kurepina, N. E., and Kreiswirth, B. N. (2002) Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol. 10, 45-52
42. Narvskaya, O. V., Mokrousov, I. V., Otten, T. F., and Vishnevskii, B. I. (1999) Genetic marking of polyresistant Mycobacterium tuberculosis strains isolated in the north-west of Russia. Probl. Tuberk. 39-41
43. Narvskaya, O. M. I. O., T, Vishnevsky, B. (2005) Molecular markers: application for studies of Mycobacterium tuberculosis population in Russia. Trends in DNA fingerprinting research 15
44. Supply, P., Allix, C., Lesjean, S., Cardoso-Oelemann, M., Rusch-Gerdes, S., Willery, E., Savine, E., de Haas, P., van Deutekom, H., Roring, S., Bifani, P., Kurepina, N., Kreiswirth, B., Sola, C., Rastogi, N., Vatin, V., Gutierrez, M. C., Fauville, M., Niemann, S., Skuce, R., Kremer, K., Locht, C., and van Soolingen, D. (2006) Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J. Clin. Microbiol. 44, 4498-4510
45. Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-van Dillen, P. M., and van der Noordaa, J. (1990) Rapid and simple method for purification of nucleic acids. J. Clin. Microbiol. 28, 495-503
46. Woods, G. L., Brown-Elliott, B. A., Desmond, E. P., Hall, G. S., Heifets, L., Pfyffer, G. E., Ridderhof, J. C., Wallace, R. J., Warren, N. G., and Witebsky, F. G. (2011) Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes; approved standard, second edition. Clinical and Laboratory Standards Institute
47. Wisniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
48. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A. J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
49. Meiring, H. D., van der Heeft, E., ten Hove, G. J., and de Jong, A. P. J. M. (2002) Nanoscale LC-MS(n): technical design and applications to peptide and protein analysis. J. Sep. Sci. 25, 12
50. de Souza, G. A., Arntzen, M. O., and Wiker, H. G. (2010) MSMSpdbb: providing protein databases of closely related organisms to improve proteomic characterization of prokaryotic microbes. Bioinformatics 26, 698-699
51. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544
52. Narayanan, S., and Deshpande, U. (2013) Whole-Genome Sequences of Four Clinical Isolates of Mycobacterium tuberculosis from Tamil Nadu, South India. Genome Announc. 1
53. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
54. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
55. Yu, N. Y., Wagner, J. R., Laird, M. R., Melli, G., Rey, S., Lo, R., Dao, P., Sahinalp, S. C., Ester, M., Foster, L. J., and Brinkman, F. S. (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26, 1608-1615
56. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
57. Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., and Leunissen, J. A. (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35, W71-74
58. Adzhubei, I. A., Schmidt, S., Peshkin, L., Ramensky, V. E., Gerasimova, A., Bork, P., Kondrashov, A. S., and Sunyaev, S. R. (2010) A method and server for predicting damaging missense mutations. Nat. Methods 7, 248-249
59. Capriotti, E., Fariselli, P., Rossi, I., and Casadio, R. (2008) A three-state prediction of single point mutations on protein stability changes. BMC Bioinformatics 9, S6
60. Brunham, L. R., Singaraja, R. R., Pape, T. D., Kejariwal, A., Thomas, P. D., and Hayden, M. R. (2005) Accurate prediction of the functional significance of single nucleotide polymorphisms and mutations in the ABCA1 gene. PLoS Genet. 1, e83
61. Reddy, T. B., Riley, R., Wymore, F., Montgomery, P., DeCaprio, D., Engels, R., Gellesch, M., Hubble, J., Jen, D., Jin, H., Koehrsen, M., Larson, L., Mao, M., Nitzberg, M., Sisk, P., Stolte, C., Weiner, B., White, J., Zachariah, Z. K., Sherlock, G., Galagan, J. E., Ball, C. A., and Schoolnik, G. K. (2009) TB database: an integrated platform for tuberculosis research. Nucleic Acids Res. 37, D499-508
62. Vandenbergh, P. A., Bawdon, R. E., and Berk, R. S. (1979) Rapid test for determining the intracellullar rhodanese activity of various bacteria Int. J. Syst. Bacteriol. 29, 6
63. Lew, J. M., Kapopoulou, A., Jones, L. M., and Cole, S. T. (2011) TubercuList-10 years after. Tuberculosis 91, 1-7
64. Louw, G. E., Warren, R. M., Gey van Pittius, N. C., McEvoy, C. R., Van Helden, P. D., and Victor, T. C. (2009) A balancing act: efflux/influx in mycobacterial drug resistance. Antimicrob. Agents Chemother. 53, 3181-3189
65. Mokrousov, I., Jiao, W. W., Sun, G. Z., Liu, J. W., Valcheva, V., Li, M., Narvskaya, O., and Shen, A. D. (2006) Evolution of drug resistance in different sublineages of Mycobacterium tuberculosis Beijing genotype. Antimicrob. Agents Chemother. 50, 2820-2823
66. Iwamoto, T., Yoshida, S., Suzuki, K., and Wada, T. (2008) Population structure analysis of the Mycobacterium tuberculosis Beijing family indicates an association between certain sublineages and multidrug resistance. Antimicrob. Agents Chemother. 52, 3805-3809
67. Parwati, I., van Crevel, R., and van Soolingen, D. (2010) Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains. Lancet Infect. Dis. 10, 103-111
68. Borgdorff, M. W., and van Soolingen, D. (2013) The re-emergence of tuberculosis: what have we learnt from molecular epidemiology? Clin. Microbiol. Infect. 19, 889-901
69. Faksri, K., Drobniewski, F., Nikolayevskyy, V., Brown, T., Prammananan, T., Palittapongarnpim, P., Prayoonwiwat, N., and Chaiprasert, A. (2011) Genetic diversity of the Mycobacterium tuberculosis Beijing family based on IS6110, SNP, LSP and VNTR profiles from Thailand. Infect. Genet. Evol. 11, 1142-1149
70. Lu, B., Zhao, P., Liu, B., Dong, H., Yu, Q., Zhao, X., and Wan, K. (2012) Genetic diversity of Mycobacterium tuberculosis isolates from Beijing, China assessed by Spoligotyping, LSPs and VNTR profiles. BMC Infect. Dis. 12, 372
71. Bell, C., Smith, G. T., Sweredoski, M. J., and Hess, S. (2012) Characterization of the Mycobacterium tuberculosis proteome by liquid chromatography mass spectrometry-based proteomics techniques: a comprehensive resource for tuberculosis research. J. Proteome Res. 11, 119-130
72. Louw, G. E., Warren, R. M., Gey van Pittius, N. C., Leon, R., Jimenez, A., Hernandez-Pando, R., McEvoy, C. R., Grobbelaar, M., Murray, M., van Helden, P. D., and Victor, T. C. (2011) Rifampicin reduces susceptibility to ofloxacin in rifampicin-resistant Mycobacterium tuberculosis through efflux. Am. J. Respir. Crit. Care Med. 184, 269-276
73. Villellas, C., Aristimuno, L., Vitoria, M. A., Prat, C., Blanco, S., Garcia de Viedma, D., Dominguez, J., Samper, S., and Ainsa, J. A. (2013) Analysis of mutations in streptomycin-resistant strains reveals a simple and reliable genetic marker for identification of the Mycobacterium tuberculosis Beijing genotype. J. Clin, Microbiol. 51, 2124-2130
74. Kelkar, D. S., Kumar, D., Kumar, P., Balakrishnan, L., Muthusamy, B., Yadav, A. K., Shrivastava, P., Marimuthu, A., Anand, S., Sundaram, H., Kingsbury, R., Harsha, H. C., Nair, B., Prasad, T. S., Chauhan, D. S., Katoch, K., Katoch, V. M., Kumar, P., Chaerkady, R., Ramachandran, S., Dash, D., and Pandey, A. (2011) Proteogenomic analysis of Mycobacterium tuberculosis by high resolution mass spectrometry. Mol. Cell. Proteomics 10, M111 011627
75. Jungblut, P. R., Holzhutter, H. G., Apweiler, R., and Schluter, H. (2008) The speciation of the proteome. Chemistry Central Journal 2, 16
76. Schluter, H., Apweiler, R., Holzhutter, H. G., and Jungblut, P. R. (2009) Finding one's way in proteomics: a protein species nomenclature. Chem. Cent. J. 3, 11
77. Low, T. Y., van Heesch, S., van den Toorn, H., Giansanti, P., Cristobal, A., Toonen, P., Schafer, S., Hubner, N., van Breukelen, B., Mohammed, S., Cuppen, E., Heck, A. J., and Guryev, V. (2013) Quantitative and qualitative proteome characteristics extracted from in-depth integrated genomics and proteomics analysis. Cell Rep. 5, 1469-1478
78. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84
79. Griffin, J. E., Gawronski, J. D., Dejesus, M. A., Ioerger, T. R., Akerley, B. J., and Sassetti, C. M. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog. 7, e1002251
80. Camacho, L. R., Ensergueix, D., Perez, E., Gicquel, B., and Guilhot, C. (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34, 257-267
81. Domenech, P., Reed, M. B., and Barry, C. E., 3rd. (2005) Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect. Immun. 73, 3492-3501
82. Wells, R. M., Jones, C. M., Xi, Z., Speer, A., Danilchanka, O., Doornbos, K. S., Sun, P., Wu, F., Tian, C., and Niederweis, M. (2013) Discovery of a siderophore export system essential for virulence of Mycobacterium tuberculosis. PLoS Pathog. 9, e1003120
83. de Knegt, G. J., Bruning, O., ten Kate, M. T., de Jong, M., van Belkum, A., Endtz, H. P., Breit, T. M., Bakker-Woudenberg, I. A., and de Steenwinkel, J. E. (2013) Rifampicin-induced transcriptome response in rifampicin-resistant Mycobacterium tuberculosis. Tuberculosis 93, 96-101
84. Triccas, J. A., Berthet, F. X., Pelicic, V., and Gicquel, B. (1999) Use of fluorescence induction and sucrose counterselection to identify Mycobacterium tuberculosis genes expressed within host cells. Microbiology 145, 2923-2930
85. Rengarajan, J., Bloom, B. R., and Rubin, E. J. (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. U. S. A. 102, 8327-8332
86. Cereda, A., Carpen, A., Picariello, G., Tedeschi, G., and Pagani, S. (2009) The lack of rhodanese RhdA affects the sensitivity of Azotobacter vinelandii to oxidative events. Biochem. J. 418, 135-143
87. Bifani, P. J., Plikavtis, B. B., Kapur, V., Stockbauer, K., Pan, X., Lutfey, M. L., Moghazeh, S. L., Eisner, W., Daniel, T. M., Kaplan, M. H., Crawford, J. T., Musser, B. N., and Kreiswirth, B. N. (1996) Origin and interstate spread of a New York multidrug-resistant Mycobacterium tuberculosis clone family. J. Am. Med. Assoc. 275, 6
88. Constant, P., Perez, E., Malaga, W., Laneelle, M. A., Saurel, O., Daffe, M., and Guilhot, C. (2002) Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. Evidence that all strains synthesize glycosylated p-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J. Biol. Chem. 277, 38148-38158
89. Reed, M. B., Domenech, P., Manca, C., Su, H., Barczak, A. K., Kreiswirth, B. N., Kaplan, G., and Barry, C. E., 3rd. (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431, 84-87
90. Reed, M. B., Gagneux, S., Deriemer, K., Small, P. M., and Barry, C. E., 3rd. (2007) The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J. Bacteriol. 189, 2583-2589
91. Pasca, M. R., Guglierame, P., Arcesi, F., Bellinzoni, M., De Rossi, E., and Riccardi, G. (2004) Rv2686c-Rv2687c-Rv2688c, an ABC fluoroquinolone efflux pump in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 48, 3175-3178
92. Duong, D. A., Nguyen, T. H., Nguyen, T. N., Dai, V. H., Dang, T. M., Vo, S. K., Do, D. A., Nguyen, V. V., Nguyen, H. D., Dinh, N. S., Farrar, J., and Caws, M. (2009) Beijing genotype of Mycobacterium tuberculosis is significantly associated with high-level fluoroquinolone resistance in Vietnam. Antimicrob. Agents Chemother. 53, 4835-4839
93. J.C., O. (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams.