1887

Abstract

is an increasingly important cause of human disease; however, virulence determinants are largely uncharacterized. Previously, it was demonstrated that a rough, wild-type human clinical isolate (390R) causes persistent, invasive infection, while a smooth isogenic mutant (390S) has lost this capability. During serial passage of 390S, a spontaneous rough revertant was obtained, which was named 390V. This revertant regained the ability to cause persistent, invasive infection in human monocytes and the lungs of mice. Glycopeptidolipid (GPL), which plays a role in environmental colonization, was present in abundance in the cell wall of 390S, and was associated with sliding motility and biofilm formation. In contrast, a marked reduction in the amount of GPL in the cell wall of 390R and 390V was correlated with cord formation, a property associated with mycobacterial virulence. These results indicate that the ability to switch between smooth and rough morphologies may allow to transition between a colonizing phenotype and a more virulent, invasive form.

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2006-06-01
2019-08-24
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References

  1. Attorri, S., Dunbar, S. & Clarridge, J. E. ( 2000; ). Assessment of morphology for rapid presumptive identification of Mycobacterium tuberculosis and Mycobacterium kansasii. J Clin Microbiol 38, 1426–1429.
    [Google Scholar]
  2. Barrow, W. W. & Brennan, P. J. ( 1982; ). Isolation in high frequency of rough variants of Mycobacterium intracellulare lacking C-mycoside glycopeptidolipids antigens. J Bacteriol 150, 381–384.
    [Google Scholar]
  3. Barrow, W. W., Ullom, B. P. & Brennan, P. J. ( 1980; ). Peptidoglycolipid nature of the superficial cell wall sheath of smooth-colony-forming mycobacteria. J Bacteriol 144, 814–822.
    [Google Scholar]
  4. Belisle, J. T. & Brennan, P. J. ( 1989; ). Chemical basis of rough and smooth variation in mycobacteria. J Bacteriol 171, 3465–3470.
    [Google Scholar]
  5. Billman-Jacobe, H., McConville, M. J., Haites, R. E., Kovacevic, S. & Coppel, R. L. ( 1999; ). Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol Microbiol 33, 1244–1253.
    [Google Scholar]
  6. Boucher, R. C. ( 2004; ). New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23, 146–158.[CrossRef]
    [Google Scholar]
  7. Brennan, P. J. & Goren, M. B. ( 1979; ). Structural studies on the type-specific antigens and lipids of the Mycobacterium avium–Mycobacterium intracellulare–Mycobacterium scrofulaceum complex. J Biol Chem 254, 4205–4211.
    [Google Scholar]
  8. Brennan, P. J. & Nikaido, H. ( 1995; ). The envelope of mycobacteria. Annu Rev Biochem 64, 29–63.[CrossRef]
    [Google Scholar]
  9. Brown-Elliott, B. A. & Wallace, R. J., Jr ( 2002; ). Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 15, 716–746.[CrossRef]
    [Google Scholar]
  10. Brown-Elliott, B. A. & Wallace, R. J. ( 2005; ). Infections caused by nontuberculous mycobacteria. In Principles and Practice of Infectious Diseases, 6th edn, vol. 2, pp. 2910–2911. Edited by G. L. Mandell, J. E. Bennett & R. Dolin. Philadelphia, PA: Elsevier.
  11. Byrd, T. F. ( 1997; ). TNF promotes growth of virulent M. tuberculosis in human monocytes: iron-mediated growth suppression is correlated with decreased release of TNF from iron-treated, infected monocytes. J Clin Invest 99, 2518–2529.[CrossRef]
    [Google Scholar]
  12. Byrd, T. F. & Lyons, C. R. ( 1999; ). Preliminary characterization of a Mycobacterium abscessus mutant in human and murine models of infection. Infect Immun 67, 4700–4707.
    [Google Scholar]
  13. Camphausen, R. T., Jones, R. L. & Brennan, P. J. ( 1985; ). A glycolipid antigen specific to Mycobacterium paratuberculosis: structure and antigenicity. Proc Natl Acad Sci U S A 82, 3068–3072.[CrossRef]
    [Google Scholar]
  14. Carter, G., Wu, M., Drummond, D. C. & Bermudez, L. E. ( 2003; ). Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol 52, 747–752.[CrossRef]
    [Google Scholar]
  15. Ceri, H., Olson, M. E., Stremick, C., Read, R. R., Morck, D. & Buret, A. ( 1999; ). The Calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37, 1771–1776.
    [Google Scholar]
  16. Chmiel, J. F., Berger, M. & Konstan, M. W. ( 2002; ). The role of inflammation in the pathophysiology of CF lung disease. Clin Rev Allergy Immunol 23, 5–27.[CrossRef]
    [Google Scholar]
  17. Collins, F. M. & Cunningham, D. S. ( 1981; ). Systemic Mycobacterium kansasii infection and regulation of the alloantigenic response. Infect Immun 32, 614–624.
    [Google Scholar]
  18. Conway, B. D., Chu, K. K., Bylund, J., Altman, E. & Speert, D. P. ( 2004; ). Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice. J Infect Dis 190, 957–966.[CrossRef]
    [Google Scholar]
  19. Cullen, A. R., Cannon, C. L., Mark, E. J. & Colin, A. A. ( 2000; ). Mycobacterium abscessus infection in cystic fibrosis. Colonization or infection? Am J Respir Crit Care Med 161, 641–645.[CrossRef]
    [Google Scholar]
  20. Eckstein, T. M., Inamine, J. M., Lambert, M. L. & Belisle, J. T. ( 2000; ). A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium. J Bacteriol 182, 6177–6182.[CrossRef]
    [Google Scholar]
  21. Fauroux, B., Delaisi, B., Clement, A., Saizou, C. & Moissenet, D. ( 1997; ). Mycobacterial lung disease in cystic fibrosis: a prospective study. Pediatr Infect Dis J 16, 354–358.[CrossRef]
    [Google Scholar]
  22. Fregnan, G. B. & Smith, D. W. ( 1962; ). Description of various colony forms of mycobacteria. J Bacteriol 83, 819–826.
    [Google Scholar]
  23. Furuchi, A. & Tokunaga, T. ( 1972; ). Nature of the receptor substance of Mycobacterium smegmatis for D4 bacteriophage adsorption. J Bacteriol 111, 404–411.
    [Google Scholar]
  24. Glickman, M. S., Cox, J. S. & Jacobs, W. R. ( 2000; ). A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5, 717–727.[CrossRef]
    [Google Scholar]
  25. Goren, M. B., McClatchy, J. K., Martens, B. & Brokl, O. ( 1972; ). Mycosides C: behavior as receptor site substance for mycobacteriophage D4. J Virol 9, 999–1003.
    [Google Scholar]
  26. Griffith, D. E., Girard, W. & Wallace, R. J. ( 1993; ). Clinical features of pulmonary disease caused by rapidly growing mycobacteria. An analysis of 154 patients. Am Rev Respir Dis 147, 1271–1278.[CrossRef]
    [Google Scholar]
  27. Howard, S. T. & Byrd, T. F. ( 2000; ). The rapidly growing mycobacteria: saprophytes and parasites. Microbes Infect 2, 1845–1853.[CrossRef]
    [Google Scholar]
  28. Howard, S. T., Byrd, T. F. & Lyons, C. R. ( 2002; ). A polymorphic region in Mycobacterium abscessus contains a novel insertion sequence element. Microbiology 148, 2987–2996.
    [Google Scholar]
  29. Kansal, R. G., Gomez-Flores, R. & Mehta, R. T. ( 1998; ). Change in colony morphology influences the virulence as well as the biochemical properties of the Mycobacterium avium complex. Microb Pathog 25, 203–214.[CrossRef]
    [Google Scholar]
  30. Lopez-Marin, L. M., Gautier, N., Laneele, M., Silve, G. & Daffe, M. ( 1994; ). Structures of the glycopeptidolipid antigens of Mycobacterium abscessus and Mycobacterium chelonae and possible chemical basis of the serological cross-reactions in the Mycobacterium fortuitum complex. Microbiology 140, 1109–1118.[CrossRef]
    [Google Scholar]
  31. Lorian, V. ( 1966; ). Direct cord reading medium for isolation of mycobacteria. Appl Microbiol 14, 603–607.
    [Google Scholar]
  32. Martinez, A., Torella, S. & Kolter, R. ( 1999; ). Sliding motility in mycobacteria. J Bacteriol 181, 7331–7338.
    [Google Scholar]
  33. McNeil, M., Chatterjee, D., Hunter, W. & Brennan, P. ( 1989; ). Mycobacterial glycolipids: isolation, structures, antigenicity, and synthesis of neoantigens. Methods Enzymol 179, 215–242.
    [Google Scholar]
  34. Middlebrook, G., Dubos, R. J. & Pierce, C. ( 1947; ). Virulence and morphological characteristics of mammalian tubercle bacilli. J Exp Med 175–189.
    [Google Scholar]
  35. Olivier, K. N., Weber, D. J., Wallace, R. J. & 10 other authors ( 2003; ). Nontuberculous mycobacteria. I: Multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med 167, 828–834.[CrossRef]
    [Google Scholar]
  36. Ortalo-Magné, A., Lemassu, A., Lanéelle, M.-A., Bardou, F., Silve, G., Gounon, P., Marchal, G. & Daffé, M. ( 1996; ). Identification of the surface-exposed lipids on the cell envelope of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178, 456–461.
    [Google Scholar]
  37. Rao, V., Fujiwara, N., Porcelli, S. A. & Glickman, M. S. ( 2005; ). Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J Exp Med 201, 535–543.[CrossRef]
    [Google Scholar]
  38. Recht, J. & Kolter, R. ( 2001; ). Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J Bacteriol 183, 5718–5724.[CrossRef]
    [Google Scholar]
  39. Recht, J., Martinez, A., Torello, S. & Kolter, R. ( 2000; ). Genetic analysis of sliding motility in Mycobacterium smegmatis. J Bacteriol 182, 4348–4351.[CrossRef]
    [Google Scholar]
  40. Reddy, V. M., Parikh, K., Luna-Herrera, J., Falkinham, J. O., Brown, S. & Gangadharam, P. R. ( 1994; ). Comparison of virulence of Mycobacterium avium complex strains (MAC) isolated from AIDS and non-AIDS patients. Microb Pathog 16, 121–130.[CrossRef]
    [Google Scholar]
  41. Rhoades, E., Hsu, F., Torrelles, J. B., Turk, J., Chatterjee, D. & Russell, D. G. ( 2003; ). Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol Microbiol 48, 875–888.[CrossRef]
    [Google Scholar]
  42. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  43. Sanguinetti, M., Ardito, F., Fiscarelli, E., La Sorda, M., D'Argenio, P., Ricciotti, G. & Fadda, G. ( 2001; ). Fatal pulmonary infection due to multidrug-resistant Mycobacterium abscessus in a patient with cystic fibrosis. J Clin Microbiol 39, 816–819.[CrossRef]
    [Google Scholar]
  44. Schaefer, W. R., Davis, C. L. & Cohn, M. L. ( 1970; ). Pathogenicity of transparent, opaque, and rough variants of Mycobacterium avium in chickens and mice. Am Rev Respir Dis 102, 499–506.
    [Google Scholar]
  45. Sermet-Gaudelus, I., Le Bourgeois, M., Pierre-Audigier, C. & 11 other authors ( 2003; ). Mycobacterium abscessus and children with cystic fibrosis. Emerg Infect Dis 9, 1587–1591.[CrossRef]
    [Google Scholar]
  46. Torrelles, J. B., Ellis, D., Osborne, T., Hoefer, A., Orme, I. M., Chatterjee, D., Brennan, P. J. & Cooper, A. M. ( 2002; ). Characterization of virulence, colony morphotype and the glycopeptidolipid of Mycobacterium avium strain 104. Tuberculosis 82, 293–300.[CrossRef]
    [Google Scholar]
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