Advertisement

Mycobacterial Genomes

  • David C. Alexander
  • Jun Liu

Abstract

Tuberculosis (TB), caused by Mycobacterium tuberculosis, remains a major cause of death around the world. Diseases caused by nontuberculous mycobacteria are increasingly associated with immunocompromised individuals. The availability of whole-genome sequences of mycobacterial species in the past several years has revolutionized TB research. This chapter provides an overview of the biology of mycobacteria and the diseases that they cause, with emphasis on how recent advances in genomics have improved our knowledge of the lifestyle and phylogeny of these organisms.

Key Words

Mycobacterial genomes Mycobacterium tuberculosis Mycobacteria 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Cornet, G. (1904) Tuberculosis and Acute General Miliary Tuberculosis. W.B. Sauders and Co., Philadelphia.Google Scholar
  2. 2.
    World Health Organization. Stop TB Annual Report. (2001) World Health Organization, Geneva, Switzerland.Google Scholar
  3. 3.
    World Health Organization (2002) Leprosy. Global situation. Wkly. Epidemiol. Rec. 77, 1–8.Google Scholar
  4. 4.
    Cocito, C., Gilot, P., Coene, M., de Kesel, M., Poupart, P., and Vannuffel, P. (1994) Paratuberculosis. Clin. Microbiol. Rev. 7, 328–345.PubMedGoogle Scholar
  5. 5.
    Cole, S. T., Brosch, R., Parkhill, J., et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537–544.PubMedCrossRefGoogle Scholar
  6. 6.
    Garnier, T., Eiglmeier, K., Camus, J. C., et al. (2003) The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. USA 100, 7877–7882.PubMedCrossRefGoogle Scholar
  7. 7.
    Cole, S. T., Eiglmeier, K., Parkhill, J., et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409, 1007–1011.PubMedCrossRefGoogle Scholar
  8. 8.
    Fleischmann, R. D., Alland, D., Eisen, J. A., et al. (2002) Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J. Bacteriol. 184, 5479–5490.PubMedCrossRefGoogle Scholar
  9. 9.
    Harmsen, D., Dostal, S., Roth, A., et al. (2003) RIDOM: comprehensive and public sequence database for identification of Mycobacterium species. BMC. Infect. Dis. 3, 26.PubMedCrossRefGoogle Scholar
  10. 10.
    Primm, T. P., Lucero, C. A., and Falkinham, J. O. (2004) Health impacts of environmental mycobacteria. Clin. Microbiol. Rev. 17, 98–106.PubMedCrossRefGoogle Scholar
  11. 11.
    Wayne, L. G. and Sramek, H. A. (1992) Agents of newly recognized or infrequently encountered mycobacterial diseases. Clin. Microbiol. Rev. 5, 1–25.PubMedGoogle Scholar
  12. 12.
    Wolinsky, E. (1992) Mycobacterial diseases other than tuberculosis. Clin. Infect. Dis. 15, 1–10.PubMedGoogle Scholar
  13. 13.
    Tortoli, E. (2003) Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin. Microbiol. Rev. 16, 319–354.PubMedCrossRefGoogle Scholar
  14. 14.
    Roth, A., Fischer, M., Hamid, M. E., Michalke, S., Ludwig, W., and Mauch, H. (1998) Differentiation of phylogenetically related slowly growing mycobacteria based on 16S-23S rRNA gene internal transcribed spacer sequences. J. Clin. Microbiol. 36, 139–147.PubMedGoogle Scholar
  15. 15.
    Cloud, J. L., Neal, H., Rosenberry, R., et al. (2002) Identification of Mycobacterium spp. by using a commercial 16S ribosomal DNA sequencing kit and additional sequencing libraries. J. Clin. Microbiol. 40, 400–406.PubMedCrossRefGoogle Scholar
  16. 16.
    Koch, R. (1882) Die Aetiologie der Tuberkulose. Berliner Klinischen Wochenschrift. 15, 221–230.Google Scholar
  17. 17.
    Salo, W. L., Aufderheide, A. C., Buikstra, J., and Holcomb, T. A. (1994) Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. Proc. Natl. Acad. Sci. USA 91, 2091–2094.PubMedCrossRefGoogle Scholar
  18. 18.
    Zink, A. R., Sola, C., Reischl, U., et al. (2003) Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J. Clin. Microbiol. 41, 359–367.PubMedCrossRefGoogle Scholar
  19. 19.
    Dye, C., Scheele, S., Dolin, P., Pathania, V., and Raviglione, M. C. (1999) Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282, 677–686.PubMedCrossRefGoogle Scholar
  20. 20.
    World Health Organization. Global Tuberculosis Control: Surveillance, Planning, Financing. WHO Report 2004. (2004) World Health Organization, Geneva, Switzerland.Google Scholar
  21. 21.
    Gazzard, B. (2001) Tuberculosis, HIV and the developing world. Clin. Med. 1, 62–68.PubMedGoogle Scholar
  22. 22.
    Porter, J. D. (1996) Mycobacteriosis and HIV infection: the new public health challenge. J. Antimicrob. Chemother. 37, 113–120.PubMedGoogle Scholar
  23. 23.
    Cosma, C. L., Sherman, D. R., and Ramakrishnan, L. (2003) The secret lives of the pathogenic mycobacteria. Annu. Rev. Microbiol. 57, 641–676.PubMedCrossRefGoogle Scholar
  24. 24.
    Smith, I. (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin. Microbiol. Rev. 16, 463–496.PubMedCrossRefGoogle Scholar
  25. 25.
    Amer, A. O. and Swanson, M. S. (2002) A phagosome of one’s own: a microbial guide to life in the macrophage. Curr. Opin. Microbiol. 5, 56–61.PubMedCrossRefGoogle Scholar
  26. 26.
    Deretic, V. and Fratti, R. A. (1999) Mycobacterium tuberculosis phagosome. Mol. Microbiol. 31, 1603–1609.PubMedCrossRefGoogle Scholar
  27. 27.
    Stewart, G. R., Robertson, B. D., and Young, D. B. (2003) Tuberculosis: a problem with persistence. Nat. Rev. Microbiol. 1, 97–105.PubMedCrossRefGoogle Scholar
  28. 28.
    Wayne, L. G. (1994) Dormancy of Mycobacterium tuberculosis and latency of disease. Eur. J. Clin. Microbiol. Infect. Dis. 13, 908–914.PubMedCrossRefGoogle Scholar
  29. 29.
    Lawn, S. D., Butera, S. T., and Shinnick, T. M. (2002) Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes. Infect. 4, 635–646.PubMedCrossRefGoogle Scholar
  30. 30.
    Espinal, M. A. (2003) The global situation of MDR-TB. Tuberculosis 83, 44–51.PubMedCrossRefGoogle Scholar
  31. 31.
    Mukherjee, J. S., Rich, M. L., Socci, A. R., et al. (2004) Programmes and principles in treatment of multidrug-resistant tuberculosis. Lancet 363, 474–481.PubMedCrossRefGoogle Scholar
  32. 32.
    Nachega, J. B. and Chaisson, R. E. (2003) Tuberculosis drug resistance: a global threat. Clin. Infect. Dis. 36, S24–S30.PubMedCrossRefGoogle Scholar
  33. 33.
    Valway, S. E., Sanchez, M. P., Shinnick, T. F., et al. (1998) An outbreak involving extensive transmission of a virulent strain of Mycobacterium tuberculosis. N. Engl. J. Med. 338, 633–639.PubMedCrossRefGoogle Scholar
  34. 34.
    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.PubMedGoogle Scholar
  35. 35.
    van Soolingen, D., Qian, L., de Haas, P. E., et al. (1995) Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J. Clin. Microbiol. 33, 3234–3238.PubMedGoogle Scholar
  36. 36.
    Tsolaki, A. G., Hirsh, A. E., DeRiemer, K., et al. (2004) Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc. Natl. Acad. Sci. USA 101, 4865–4870.PubMedCrossRefGoogle Scholar
  37. 37.
    Perna, N. T., Plunkett, G., Burland, V., et al. (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409, 529–533.PubMedCrossRefGoogle Scholar
  38. 38.
    Sreevatsan, S., Pan, X., Stockbauer, K. E., et al. (1997) Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionary recent global dissemination. Proc. Natl. Acad. Sci. USA 94, 9869–9874.PubMedCrossRefGoogle Scholar
  39. 39.
    Barnes, P. F. and Cave, M. D. (2003) Molecular epidemiology of tuberculosis. N. Engl. J. Med. 349, 1149–1156.PubMedCrossRefGoogle Scholar
  40. 40.
    van Soolingen, D. (2001) Molecular epidemiology of tuberculosis and other mycobacterial infections: main methodologies and achievements. J. Intern. Med. 249, 1–26.PubMedCrossRefGoogle Scholar
  41. 41.
    Mostrom, P., Gordon, M., Sola, C., Ridell, M., and Rastogi, N. (2002) Methods used in the molecular epidemiology of tuberculosis. Clin. Microbiol. Infect. 8, 694–704.PubMedCrossRefGoogle Scholar
  42. 42.
    Brosch, R., Gordon, S. V., Marmiesse, M., et al. (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl. Acad. Sci. USA 99, 3684–3689.PubMedCrossRefGoogle Scholar
  43. 43.
    Gutacker, M. M., Smoot, J. C., Migliaccio, C. A., et al. (2002) Genome-wide analysis of synonymous single nucleotide polymorphisms in Mycobacterium tuberculosis complex organisms: resolution of genetic relationships among closely related microbial strains. Genetics 162, 1533–1543.PubMedGoogle Scholar
  44. 44.
    Mostowy, S., Cousins, D., Brinkman, J., Aranaz, A., and Behr, M. A. (2002) Genomic deletions suggest a phylogeny for the Mycobacterium tuberculosis complex. J. Infect. Dis. 186, 74–80.PubMedCrossRefGoogle Scholar
  45. 45.
    Mostowy, S., Onipede, A., Gagneux, S., et al. (2004) Genomic analysis distinguishes Mycobacterium africanum. J. Clin. Microbiol. 42, 3594–3599.PubMedCrossRefGoogle Scholar
  46. 46.
    Mostowy, S., Cousins, D., and Behr, M. A. (2004) Genomic interrogation of the dassie bacillus reveals it as a unique RD1 mutant within the Mycobacterium tuberculosis complex. J. Bacteriol. 186, 104–109.PubMedCrossRefGoogle Scholar
  47. 47.
    Chen, J. M., Alexander, D. C., Behr, M. A., and Liu, J. (2003) Mycobacterium bovis BCG vaccines exhibit defects in alanine and serine catabolism. Infect. Immun. 71, 708–716.PubMedCrossRefGoogle Scholar
  48. 48.
    Behr, M. A. and Small, P. M. (1999) A historical and molecular phylogeny of BCG strains. Vaccine 17, 915–922.PubMedCrossRefGoogle Scholar
  49. 49.
    Crispen, R. (1989) History of BCG and its substrains. Prog. Clin. Biol. Res. 310, 35–50PubMedGoogle Scholar
  50. 50.
    Behr, M. A. and Small, P. M. (1997) Has BCG attenuated to impotence? Nature 389, 133–134.PubMedCrossRefGoogle Scholar
  51. 51.
    Brewer, T. F. and Colditz, G. A. (1995) Relationship between bacille Calmette-Guerin (BCG) strains and the efficacy of BCG vaccine in the prevention of tuberculosis. Clin. Infect. Dis. 20, 126–135.PubMedGoogle Scholar
  52. 52.
    Brandt, L., Feino, C. J., Weinreich, O. A., et al. (2002) Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infect. Immun. 70, 672–678.PubMedCrossRefGoogle Scholar
  53. 53.
    Buddle, B. M., Wards, B. J., Aldwell, F. E., Collins, D. M., and de Lisle, G. W. (2002) Influence of sensitisation to environmental mycobacteria on subsequent vaccination against bovine tuberculosis. Vaccine 20, 1126–1133.PubMedCrossRefGoogle Scholar
  54. 54.
    Behr, M. A., Wilson, M. A., Gill, W. P., et al. (1999) Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520–1523.PubMedCrossRefGoogle Scholar
  55. 55.
    Mahairas, G. G., Sabo, P. J., Hickey, M. J., Singh, D. C., and Stover, C. K. (1996) Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J. Bacteriol. 178, 1274–1282.PubMedGoogle Scholar
  56. 56.
    Lewis, K. N., Liao, R., Guinn, K. M., et al. (2003) Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J. Infect. Dis. 187, 117–123.PubMedCrossRefGoogle Scholar
  57. 57.
    Pym, A. S., Brodin, P., Brosch, R., Huerre, M., and Cole, S. T. (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol. Microbiol. 46, 709–717.PubMedCrossRefGoogle Scholar
  58. 58.
    Mostowy, S., Tsolaki, A. G., Small, P. M., and Behr, M. A. (2003) The in vitro evolution of BCG vaccines. Vaccine 21, 4270–4274.PubMedCrossRefGoogle Scholar
  59. 59.
    Doherty, T. M. and Andersen, P. (2002) Tuberculosis vaccine development. Curr. Opin. Pulm. Med. 8, 183–187.PubMedCrossRefGoogle Scholar
  60. 60.
    Kumar, H., Malhotra, D., Goswami, S., and Bamezai, R. N. (2003) How far have we reached in tuberculosis vaccine development? Crit. Rev. Microbiol. 29, 297–312.PubMedCrossRefGoogle Scholar
  61. 61.
    Young, D. B. and Stewart, G. R. (2002) Tuberculosis vaccines. Br. Med. Bull. 62, 73–86.PubMedCrossRefGoogle Scholar
  62. 62.
    Horwitz, M. A. and Harth, G. (2003) A new vaccine against tuberculosis affords greater survival after challenge than the current vaccine in the guinea pig model of pulmonary tuberculosis. Infect. Immun. 71, 1672–1679.PubMedCrossRefGoogle Scholar
  63. 63.
    Pym, A. S., Brodin, P., Majlessi, L., et al. (2003) Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9, 533–539.PubMedCrossRefGoogle Scholar
  64. 64.
    Stover, C. K., Bansal, G. P., Hanson, M. S., et al. (1993) Protective immunity elicited by recombinant bacille Calmette-Guerin (BCG) expressing outer surface protein A (OspA) lipoprotein: a candidate Lyme disease vaccine. J. Exp. Med. 178, 197–209.PubMedCrossRefGoogle Scholar
  65. 65.
    Stover, C. K., de la Cruz, V. F., Fuerst, T. R., et al. (1991) New use of BCG for recombinant vaccines. Nature 351, 456–460.PubMedCrossRefGoogle Scholar
  66. 66.
    Varaldo, P. B., Leite, L. C., Dias, W. O., et al. (2004) Recombinant Mycobacterium bovis BCG expressing the Sm14 antigen of Schistosoma mansoni protects mice from cercarial challenge. Infect. Immun. 72, 3336–3343.PubMedCrossRefGoogle Scholar
  67. 67.
    Shelley, M. D., Court, J. B., Kynaston, H., et al. (2004) Intravesical Bacillus Calmette-Guerin in Ta and T1 Bladder Cancer. In: The Cochrane Library 4, John Wiley and Sons, Ltd, Chichester, UK.Google Scholar
  68. 68.
    Hansen, G. H. A. (1875) On the etiology of leprosy. Br. J. Foreign Med. Chir. Rev. 55, 459–489.Google Scholar
  69. 69.
    Brennan, P. J. and Vissa, V. D. (2001) Genomic evidence for the retention of the essential mycobacterial cell wall in the otherwise defective Mycobacterium leprae. Lepr. Rev. 72, 415–428.PubMedGoogle Scholar
  70. 70.
    Behr, M. A., Schroeder, B. G., Brinkman, J. N., Slayden, R. A., and Barry, C. E. (2000) A point mutation in the mma3 gene is responsible for impaired methoxymycolic acid production in Mycobacterium bovis BCG strains obtained after 1927. J. Bacteriol. 182, 3394–3399.PubMedCrossRefGoogle Scholar
  71. 71.
    Groathouse, N. A., Rivoire, B., Kim, H., et al. (2004) Multiple polymorphic loci for molecular typing of strains of Mycobacterium leprae. J. Clin. Microbiol. 42, 1666–1672.PubMedCrossRefGoogle Scholar
  72. 72.
    Shin, Y. C., Lee, H., Walsh, G. P., Kim, J. D., and Cho, S. N. (2000) Variable numbers of TTC repeats in Mycobacterium leprae DNA from leprosy patients and use in strain differentiation. J. Clin. Microbiol. 38, 4535–4538.PubMedGoogle Scholar
  73. 73.
    Chacon, O., Bermudez, L. E., and Barletta, R. G. (2004) Johne’s disease, inflammatory bowel disease, and Mycobacterium paratuberculosis. Annu. Rev. Microbiol. 58, 329–363.PubMedCrossRefGoogle Scholar
  74. 74.
    Greenstein, R. J. (2003) Is Crohn’s disease caused by a mycobacterium? Comparisons with leprosy, tuberculosis, and Johne’s disease. Lancet Infect. Dis. 3, 507–514.PubMedCrossRefGoogle Scholar
  75. 75.
    Hermon-Taylor, J. and Bull, T. (2002) Crohn’s disease caused by Mycobacterium avium subspecies paratuberculosis: a public health tragedy whose resolution is long overdue. J. Med. Microbiol. 51, 3–6.PubMedGoogle Scholar
  76. 76.
    Novi, C., Rindi, L., Lari, N., and Garzelli, C. (2000) Molecular typing of Mycobacterium avium isolates by sequencing of the 16S-23S rDNA internal transcribed spacer and comparison with IS1245-based fingerprinting. J. Med. Microbiol. 49, 1091–1095.PubMedGoogle Scholar
  77. 77.
    Krzywinska, E., Krzywinski, J., and Schorey, J. S. (2004) Naturally occurring horizontal gene transfer and homologous recombination in Mycobacterium. Microbiology 150, 1707–1712.PubMedCrossRefGoogle Scholar
  78. 78.
    Whittington, R. J., Marshall, D. J., Nicholls, P. J., Marsh, I. B., and Reddacliff, L. A. (2004) Survival and dormancy of Mycobacterium avium subsp. paratuberculosis in the environment. Appl. Environ. Microbiol. 70, 2989–3004.PubMedCrossRefGoogle Scholar
  79. 79.
    Falkinham, J. O., Norton, C. D., and LeChevallier, M. W. (2001) Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other Mycobacteria in drinking water distribution systems. Appl. Environ. Microbiol. 67, 1225–1231.PubMedCrossRefGoogle Scholar
  80. 80.
    Skriwan, C., Fajardo, M., Hagele, S., et al. (2002) Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int. J. Med. Microbiol. 291, 615–624.PubMedCrossRefGoogle Scholar
  81. 81.
    Semret, M., Zhai, G., Mostowy, S., et al. (2004) Extensive genomic polymorphism within Mycobacterium avium. J. Bacteriol. 186, 6332–6334.PubMedCrossRefGoogle Scholar
  82. 82.
    Bull, T. J., Hermon-Taylor, J., Pavlik, I., El-Zaatari, F., and Tizard, M. (2000) Characterization of IS900 loci in Mycobacterium avium subsp. paratuberculosis and development of multiplex PCR typing. Microbiology 146, 2185–2197.PubMedGoogle Scholar
  83. 83.
    Amonsin, A., Li, L. L., Zhang, Q., et al. (2004) Multilocus short sequence repeat sequencing approach for differentiating among Mycobacterium avium subsp. paratuberculosis strains. J. Clin. Microbiol. 42, 1694–1702.PubMedCrossRefGoogle Scholar
  84. 84.
    Dohmann, K., Strommenger, B., Stevenson, K., et al. (2003) Characterization of genetic differences between Mycobacterium avium subsp. paratuberculosis type I and type II isolates. J. Clin. Microbiol. 41, 5215–5223.PubMedCrossRefGoogle Scholar
  85. 85.
    Motiwala, A. S., Strother, M., Amonsin, A., et al. (2003) Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: evidence for limited strain diversity, strain sharing, and identification of unique targets for diagnosis. J. Clin. Microbiol. 41, 2015–2026.PubMedCrossRefGoogle Scholar
  86. 86.
    Bannantine, J. P., Hansen, J. K., Paustian, M. L., et al. (2004) Expression and immunogenicity of proteins encoded by sequences specific to Mycobacterium avium subsp. paratuberculosis. J. Clin. Microbiol. 42, 106–114.PubMedCrossRefGoogle Scholar
  87. 87.
    van der Werf, T. S., Stinear, T., Stienstra, Y., van der Graaf, W. T., and Small, P. L. (2003) Mycolactones and Mycobacterium ulcerans disease. Lancet 362, 1062–1064.PubMedCrossRefGoogle Scholar
  88. 88.
    MacCallum, P., Tolhurst, J. C., Buckle, G., and Sissons, H. A. (1948) A new mycobacterial infection in man. J. Pathol. Bacteriol. 60, 93–122.CrossRefPubMedGoogle Scholar
  89. 89.
    Clancey, J. K. (1964) Mycobacterial skin ulcers in Uganda: description of a new mycobacterium (Mycobacterium Buruli). J. Pathol. Bacteriol. 88, 175–187.PubMedCrossRefGoogle Scholar
  90. 90.
    Decostere, A., Hermans, K., and Haesebrouck, F. (2004) Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet. Microbiol. 99, 159–166.PubMedCrossRefGoogle Scholar
  91. 91.
    Stinear, T. P., Mve-Obiang, A., Small, P. L., et al. (2004) Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc. Natl. Acad. Sci. USA 101, 1345–1349.PubMedCrossRefGoogle Scholar
  92. 92.
    Gao, L. Y., Guo, S., McLaughlin, B., Morisaki, H., Engel, J. N., and Brown, E. J. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol. Microbiol. 53, 1677–1693.PubMedCrossRefGoogle Scholar
  93. 93.
    Chan, K., Knaak, T., Satkamp, L., Humbert, O., Falkow, S., and Ramakrishnan, L. (2002) Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc. Natl. Acad. Sci. USA 99, 3920–3925.PubMedCrossRefGoogle Scholar
  94. 94.
    Ramakrishnan, L. and Falkow, S. (1994) Mycobacterium marinum persists in cultured mammalian cells in a temperature-restricted fashion. Infect. Immun. 62, 3222–3229.PubMedGoogle Scholar
  95. 95.
    Ramakrishnan, L., Federspiel, N. A., and Falkow, S. (2000) Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288, 1436–1439.PubMedCrossRefGoogle Scholar
  96. 96.
    Ramakrishnan, L., Valdivia, R. H., McKerrow, J. H., and Falkow, S. (1997) Mycobacterium marinum causes both long-term subclinical infection and acute disease in the leopard frog (Rana pipiens). Infect. Immun. 65, 767–773.PubMedGoogle Scholar
  97. 97.
    Andrew, P. W. and Roberts, I. S. (1993) Construction of a bioluminescent mycobacterium and its use for assay of antimycobacterial agents. J. Clin. Microbiol. 31, 2251–2254.PubMedGoogle Scholar
  98. 98.
    Mayuri, Bagchi, G., Das, T. K., and Tyagi, J. S. (2002) Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR-DevS two-component system, Rv3134c and chaperone alpha-crystallin homologues. FEMS Microbiol. Lett. 211, 231–237.PubMedGoogle Scholar
  99. 99.
    Triccas, J. A., Parish, T., Britton, W. J., and Gicquel, B. (1998) An inducible expression system permitting the efficient purification of a recombinant antigen from Mycobacterium smegmatis. FEMS Microbiol. Lett. 167, 151–156.PubMedCrossRefGoogle Scholar
  100. 100.
    Wei, J., Dahl, J. L., Moulder, J. W., et al. (2000) Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J. Bacteriol. 182, 377–384.PubMedCrossRefGoogle Scholar
  101. 101.
    Gardner, G. M. and Weiser, R. S. (1947) A bacteriophage for Mycobacterium smegmatis. Proc. Soc. Exp. Biol. Med. 66, 205–206.Google Scholar
  102. 102.
    Bardarov, S. J., Dou, H., Eisenach, K., et al. (2003) Detection and drug-susceptibility testing of M. tuberculosis from sputum samples using luciferase reporter phage: comparison with the Mycobacteria Growth Indicator Tube (MGIT) system. Diagn. Microbiol. Infect. Dis. 45, 53–61.PubMedCrossRefGoogle Scholar
  103. 103.
    Carriere, C., Riska, P. F., Zimhony, O., et al. (1997) Conditionally replicating luciferase reporter phages: improved sensitivity for rapid detection and assessment of drug susceptibility of Mycobacterium tuberculosis. J. Clin. Microbiol. 35, 3232–3239.PubMedGoogle Scholar
  104. 104.
    Hazbon, M. H., Guarin, N., Ferro, B. E., et al. (2003) Photographic and luminometric detection of luciferase reporter phages for drug susceptibility testing of clinical Mycobacterium tuberculosis isolates. J. Clin. Microbiol. 41, 4865–4869.PubMedCrossRefGoogle Scholar
  105. 105.
    Riska, P. F. and Jacobs, W. R. Jr. (1998) The use of luciferase-reporter phage for antibiotic-susceptibility testing of mycobacteria. Methods Mol. Biol. 101, 431–455.PubMedGoogle Scholar
  106. 106.
    Riska, P. F., Su, Y., Bardarov, S., et al. (1999) Rapid film-based determination of antibiotic susceptibilities of Mycobacterium tuberculosis strains by using a luciferase reporter phage and the Bronx Box. J. Clin. Microbiol. 37, 1144–1149.PubMedGoogle Scholar
  107. 107.
    Bardarov, S., Bardarov, J. S. J., Pavelka, J. M. J., et al. (2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007–3017.PubMedGoogle Scholar
  108. 108.
    Bardarov, S., Kriakov, J., Carriere, C., et al. (1997) Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 94, 10,961–10,966.PubMedCrossRefGoogle Scholar
  109. 109.
    Jacobs, W. R. Jr., Snapper, S. B., Tuckman, M., and Bloom, B. R. (1989) Mycobacteriophage vector systems. Rev. Infect. Dis. 11, S404–S410.PubMedGoogle Scholar
  110. 110.
    Pearson, R. E., Jurgensen, S., Sarkis, G. J., Hatfull, G. F., and Jacobs, W. R. J. (1996) Construction of D29 shuttle phasmids and luciferase reporter phages for detection of mycobacteria. Gene 183, 129–136.PubMedCrossRefGoogle Scholar
  111. 111.
    Jacobs, W. R. J., Tuckman, M., and Bloom, B. R. (1987) Introduction of foreign DNA into mycobacteria using a shuttle phasmid. Nature 327, 532–535.PubMedCrossRefGoogle Scholar
  112. 112.
    Pedulla, M. L., Ford, M. E., Houtz, J. M., et al. (2003) Origins of highly mosaic mycobacteriophage genomes. Cell 113, 171–182.PubMedCrossRefGoogle Scholar
  113. 113.
    Hendrix, R. W., Smith, M. C., Burns, R. N., Ford, M. E., and Hatfull, G. F. (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc. Natl. Acad. Sci. USA 96, 2192–2197.PubMedCrossRefGoogle Scholar
  114. 114.
    Hatfull, G. F. and Sarkis, G. J. (1993) DNA sequence, structure and gene expression of mycobacteriophage L5: a phage system for mycobacterial genetics. Mol. Microbiol. 7, 395–405.PubMedCrossRefGoogle Scholar
  115. 115.
    Ford, M. E., Sarkis, G. J., Belanger, A. E., Hendrix, R. W., and Hatfull, G. F. (1998) Genome structure of mycobacteriophage D29: implications for phage evolution. J. Mol. Biol. 279, 143–164.PubMedCrossRefGoogle Scholar
  116. 116.
    Ford, M. E., Stenstrom, C., Hendrix, R. W., and Hatfull, G. F. (1998) Mycobacteriophage TM4: genome structure and gene expression. Tuber. Lung Dis. 79, 63–73.PubMedCrossRefGoogle Scholar
  117. 117.
    Mediavilla, J., Jain, S., Kriakov, J., et al. (2000) Genome organization and characterization of mycobacteriophage Bxb1. Mol. Microbiol. 38, 955–970.PubMedCrossRefGoogle Scholar
  118. 118.
    Marmiesse, M., Brodin, P., Buchrieser, C., et al. (2004) Macro-array and bioinformatic analyses reveal mycobacterial ‘core’ genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150, 483–496.PubMedCrossRefGoogle Scholar
  119. 119.
    Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83, 91–97.PubMedCrossRefGoogle Scholar
  120. 120.
    Brennan, P. J. and Nikaido, H. (1995) The envelope of mycobacteria. Ann. Rev. Biochem. 64, 29–63.PubMedCrossRefGoogle Scholar
  121. 121.
    Liu, J. and Nikaido, H. (1999) A mutant in Mycobacterium smegmatis defective in the biosynthesis of mycolic acids accumulates meromycolates. Proc. Natl. Acad. Sci. USA 96, 4011–4016.PubMedCrossRefGoogle Scholar
  122. 122.
    Kolattukudy, P. E., Fernandes, N. D., Azad, A. K., Fitzmaurice, A. M., and Sirakova, T. D. (1997) Biochemistry and molecular genetics of cell-wall lipid biosynthesis in mycobacteria. Mol. Microbiol. 24, 263–270.PubMedCrossRefGoogle Scholar
  123. 123.
    Liu, J., Barry, C. E., Besra, G. S., and Nikaido, H. (1996) Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J. Biol. Chem. 271, 29,545–29,551.PubMedCrossRefGoogle Scholar
  124. 124.
    Liu, J., Rosenberg, E. Y., and Nikaido, H. (1995) Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc. Natl. Acad. Sci. USA 92, 11,254–11,258.PubMedCrossRefGoogle Scholar
  125. 125.
    Minnikin, D. E., Kremer, L., Dover, L. G., and Besra, G. S. (2002) The methyl-branched fortifications of Mycobacterium tuberculosis. Chem. Biol. 9, 545–553.PubMedCrossRefGoogle Scholar
  126. 126.
    Cox, J. S., Chen, B., McNeil, M., and Jacobs, W. R. J. (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402, 79–83.PubMedCrossRefGoogle Scholar
  127. 127.
    Nigou, J., Gilleron, M., and Puzo, G. (2003) Lipoarabinomannans: from structure to biosynthesis. Biochimie 85, 153–166.PubMedCrossRefGoogle Scholar
  128. 128.
    Adindla, S. and Guruprasad, L. (2003) Sequence analysis corresponding to the PPE and PE proteins in Mycobacterium tuberculosis and other genomes. J. Biosci. 28, 169–179.PubMedCrossRefGoogle Scholar
  129. 129.
    Sampson, S. L., Lukey, P., Warren, R. M., van Helden, P. D., Richardson, M., and Everett, M. J. (2001) Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis 81, 305–317.PubMedCrossRefGoogle Scholar
  130. 130.
    Choudhary, R. K., Mukhopadhyay, S., Chakhaiyar, P., et al. (2003) PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect. Immun. 71, 6338–6343.PubMedCrossRefGoogle Scholar
  131. 131.
    Okkels, L. M., Brock, I., Follmann, F., et al. (2003) PPE protein (Rv3873) from DNA segment RD1 of Mycobacterium tuberculosis: strong recognition of both specific T-cell epitopes and epitopes conserved within the PPE family. Infect. Immun. 71, 6116–6123.PubMedCrossRefGoogle Scholar
  132. 132.
    Zubrzycki, I. Z. (2004) Analysis of the products of genes encompassed by the theoretically predicted pathogenicity islands of Mycobacterium tuberculosis and Mycobacterium bovis. Proteins 54, 563–568.PubMedCrossRefGoogle Scholar
  133. 133.
    Sassetti, C. M. and Rubin, E. J. (2003) Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. USA 100, 12,989–12,994.PubMedCrossRefGoogle Scholar
  134. 134.
    Andersen, P., Andersen, A. B., Sorensen, A. L., and Nagai, S. (1995) Recall of longlived immunity to Mycobacterium tuberculosis infection in mice. J. Immunol. 154, 3359–3372.PubMedGoogle Scholar
  135. 135.
    Berthet, F. X., Rasmussen, P. B., Rosenkrands, I., Andersen, P., and Gicquel, B. (1998) A Mycobacterium tuberculosis operon encoding ESAT-6 and a novel low-molecularmass culture filtrate protein (CFP-10). Microbiology 144, 3195–3203.PubMedCrossRefGoogle Scholar
  136. 136.
    Hsu, T., Hingley-Wilson, S. M., Chen, B., et al. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl. Acad. Sci. USA 100, 12,420–12,425.PubMedCrossRefGoogle Scholar
  137. 137.
    Sorensen, A. L., Nagai, S., Houen, G., Andersen, P., and Andersen, A. B. (1995) Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect. Immun. 63, 1710–1717.PubMedGoogle Scholar
  138. 138.
    Okkels, L. M. and Andersen, P. (2004) Protein-protein interactions of proteins from the ESAT-6 family of Mycobacterium tuberculosis. J. Bacteriol. 186, 2487–2491.PubMedCrossRefGoogle Scholar
  139. 139.
    Gey, V. P. N., Gamieldien, J., Hide, W., Brown, G. D., Siezen, R. J., and Beyers, A. D. (2001) The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Grampositive bacteria. Genome Biol. 2, 1–18.Google Scholar
  140. 140.
    van Pinxteren, L. A., Ravn, P., Agger, E. M., Pollock, J., and Andersen, P. (2000) Diagnosis of tuberculosis based on the two specific antigens ESAT-6 and CFP10. Clin. Diagn. Lab. Immunol. 7, 155–160.PubMedCrossRefGoogle Scholar
  141. 141.
    Collins, D. M., Kawakami, R. P., Wards, B. J., Campbell, S., and de Lisle, G. W. (2003) Vaccine and skin testing properties of two avirulent Mycobacterium bovis mutants with and without an additional esat-6 mutation. Tuberculosis 83, 361–366.PubMedCrossRefGoogle Scholar
  142. 142.
    Wards, B. J., de Lisle, G. W., and Collins, D. M. (2000) An esat6 knockout mutant of Mycobacterium bovis produced by homologous recombination will contribute to the development of a live tuberculosis vaccine. Tuber. Lung Dis. 80, 185–189.PubMedCrossRefGoogle Scholar
  143. 143.
    Brandt, L., Elhay, M., Rosenkrands, I., Lindblad, E. B., and Andersen, P. (2000) ESAT-6 subunit vaccination against Mycobacterium tuberculosis. Infect. Immun. 68, 791–795.PubMedCrossRefGoogle Scholar
  144. 144.
    Mollenkopf, H. J., Groine-Triebkorn, D., Andersen, P., Hess, J., and Kaufmann, S. H. (2001) Protective efficacy against tuberculosis of ESAT-6 secreted by a live Salmonella typhimurium vaccine carrier strain and expressed by naked DNA. Vaccine 19, 4028–4035.PubMedCrossRefGoogle Scholar
  145. 145.
    Mustafa, A. S. and Al-Attiyah, R. (2003) Tuberculosis: looking beyond BCG vaccines. J. Postgrad. Med. 49, 134–140.Google Scholar
  146. 146.
    Olsen, A. W., Hansen, P. R., Holm, A., and Andersen, P. (2000) Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur. J. Immunol. 30, 1724–1732.PubMedCrossRefGoogle Scholar
  147. 147.
    Haile, Y., Caugant, D. A., Bjune, G., and Wiker, H. G. (2002) Mycobacterium tuberculosis mammalian cell entry operon (mce) homologs in Mycobacterium other than tuberculosis (MOTT). FEMS Immunol. Med. Microbiol. 33, 125–132.PubMedCrossRefGoogle Scholar
  148. 148.
    Arruda, S., Bomfim, G., Knights, R., Huima-Byron, T., and Riley, L. W. (1993) Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science 261, 1454–1457.PubMedCrossRefGoogle Scholar
  149. 149.
    Kumar, A., Bose, M., and Brahmachari, V. (2003) Analysis of expression profile of mammalian cell entry (mce) operons of Mycobacterium tuberculosis. Infect. Immun. 71, 6083–6087.PubMedCrossRefGoogle Scholar
  150. 150.
    Das, A. K., Mitra, D., Harboe, M., et al. (2003) Predicted molecular structure of the mammalian cell entry protein Mce1A of Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun. 302, 442–447.PubMedCrossRefGoogle Scholar
  151. 151.
    Chitale, S., Ehrt, S., Kawamura, I., et al. (2001) Recombinant Mycobacterium tuberculosis protein associated with mammalian cell entry. Cell Microbiol. 3, 247–254.PubMedCrossRefGoogle Scholar
  152. 152.
    Shimono, N., Morici, L., Casali, N., et al. (2003) Hypervirulent mutant of Mycobacterium tuberculosis resulting from disruption of the mce1 operon. Proc. Natl. Acad. Sci. USA 100, 15,918–15,923.PubMedCrossRefGoogle Scholar
  153. 153.
    Mukamolova, G. V., Kaprelyants, A. S., Young, D. I., Young, M., and Kell, D. B. (1998) A bacterial cytokine. Proc. Natl. Acad. Sci. USA 95, 8916–8921.PubMedCrossRefGoogle Scholar
  154. 154.
    Mukamolova, G. V., Turapov, O. A., Young, D. I., Kaprelyants, A. S., Kell, D. B., and Young, M. (2002) A family of autocrine growth factors in Mycobacterium tuberculosis. Mol. Microbiol. 46, 623–635.PubMedCrossRefGoogle Scholar
  155. 155.
    Shleeva, M., Mukamolova, G. V., Young, M., Williams, H. D., and Kaprelyants, A. S. (2004) Formation of ‘non-culturable’ cells of Mycobacterium smegmatis in stationary phase in response to growth under suboptimal conditions and their Rpf-mediated resuscitation. Microbiology 150, 1687–1697.PubMedCrossRefGoogle Scholar
  156. 156.
    Tufariello, J. M., Jacobs, W. R. Jr., and Chan, J. (2004) Individual Mycobacterium tuberculosis resuscitation-promoting factor homologues are dispensable for growth in vitro and in vivo. Infect. Immun. 72, 515–526.PubMedCrossRefGoogle Scholar
  157. 157.
    Yeremeev, V. V., Kondratieva, T. K., Rubakova, E. I., et al. (2003) Proteins of the Rpf family: immune cell reactivity and vaccination efficacy against tuberculosis in mice. Infect. Immun. 71, 4789–4794.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2006

Authors and Affiliations

  • David C. Alexander
    • 1
  • Jun Liu
    • 2
  1. 1.Montreal General Hospital Research InstituteMcGill University Health CenterMontrealCanada
  2. 2.Department of Medical Genetics and MicrobiologyUniversity of TorontoTorontoCanada

Personalised recommendations