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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28625-0
2006-06-01
2020-05-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/6/1581.html?itemId=/content/journal/micro/10.1099/mic.0.28625-0&mimeType=html&fmt=ahah

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 Microbiol38:1426–1429
    [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 Bacteriol150:381–384
    [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 Bacteriol144:814–822
    [Google Scholar]
  4. Belisle J. T, Brennan P. J. 1989; Chemical basis of rough and smooth variation in mycobacteria. J Bacteriol171:3465–3470
    [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 Microbiol33:1244–1253
    [Google Scholar]
  6. Boucher R. C. 2004; New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J23:146–158[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 Chem254:4205–4211
    [Google Scholar]
  8. Brennan P. J, Nikaido H. 1995; The envelope of mycobacteria. Annu Rev Biochem64:29–63[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 Rev15:716–746[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 Mandell G. L., Bennett J. E., Dolin R.. Philadelphia, PA: Elsevier;
    [Google Scholar]
  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 Invest99:2518–2529[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 Immun67:4700–4707
    [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 A82:3068–3072[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 Microbiol52:747–752[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 Microbiol37:1771–1776
    [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 Immunol23:5–27[CrossRef]
    [Google Scholar]
  17. Collins F. M, Cunningham D. S. 1981; Systemic Mycobacterium kansasii infection and regulation of the alloantigenic response. Infect Immun32:614–624
    [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 Dis190:957–966[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 Med161:641–645[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 Bacteriol182:6177–6182[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 J16:354–358[CrossRef]
    [Google Scholar]
  22. Fregnan G. B, Smith D. W. 1962; Description of various colony forms of mycobacteria. J Bacteriol83:819–826
    [Google Scholar]
  23. Furuchi A, Tokunaga T. 1972; Nature of the receptor substance of Mycobacterium smegmatis for D4 bacteriophage adsorption. J Bacteriol111:404–411
    [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 Cell5:717–727[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 Virol9:999–1003
    [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 Dis147:1271–1278[CrossRef]
    [Google Scholar]
  27. Howard S. T, Byrd T. F. 2000; The rapidly growing mycobacteria: saprophytes and parasites. Microbes Infect2:1845–1853[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. Microbiology148:2987–2996
    [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 Pathog25:203–214[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. Microbiology140:1109–1118[CrossRef]
    [Google Scholar]
  31. Lorian V. 1966; Direct cord reading medium for isolation of mycobacteria. Appl Microbiol14:603–607
    [Google Scholar]
  32. Martinez A, Torella S, Kolter R. 1999; Sliding motility in mycobacteria. J Bacteriol181:7331–7338
    [Google Scholar]
  33. McNeil M, Chatterjee D, Hunter W, Brennan P. 1989; Mycobacterial glycolipids: isolation, structures, antigenicity, and synthesis of neoantigens. Methods Enzymol179:215–242
    [Google Scholar]
  34. Middlebrook G, Dubos R. J, Pierce C. 1947; Virulence and morphological characteristics of mammalian tubercle bacilli. J Exp Med175–189
    [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 Med167:828–834[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 Bacteriol178:456–461
    [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 Med201:535–543[CrossRef]
    [Google Scholar]
  38. Recht J, Kolter R. 2001; Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis . J Bacteriol183:5718–5724[CrossRef]
    [Google Scholar]
  39. Recht J, Martinez A, Torello S, Kolter R. 2000; Genetic analysis of sliding motility in Mycobacterium smegmatis . J Bacteriol182:4348–4351[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 Pathog16:121–130[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 Microbiol48:875–888[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;
    [Google Scholar]
  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 Microbiol39:816–819[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 Dis102:499–506
    [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 Dis9:1587–1591[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. Tuberculosis82:293–300[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28625-0
Loading
/content/journal/micro/10.1099/mic.0.28625-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error