1887

Abstract

The genus comprises highly pathogenic as well as opportunistic or apathogenic species exhibiting a great variability with respect to their ability to persist or multiply within monocytic host cells. The impact of the permeability of the mycobacterial outer membrane on intracellular persistence was studied. For this purpose, a mutant with a deletion of the major porin gene and a second mutant lacking and the homologous porin gene were used. Deletion of together with significantly enhanced intracellular persistence in murine bone marrow macrophages, the mouse macrophage cell line J774A.1 and . Complementation of in the porin mutant strains resulted in restoration of the wild-type phenotype with respect to intracellular persistence. This is the first report to show that the deletion of porins of mycobacteria results in improved persistence in eukaryotic cells, demonstrating that the intracellular persistence of depends upon the permeability of the outer membrane.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27969-0
2005-07-01
2019-11-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/7/mic1512403.html?itemId=/content/journal/micro/10.1099/mic.0.27969-0&mimeType=html&fmt=ahah

References

  1. Allen, P. G. & Dawidowicz, E. A. ( 1990a; ). Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast. J Cell Physiol 145, 508–513.[CrossRef]
    [Google Scholar]
  2. Allen, P. G. & Dawidowicz, E. A. ( 1990b; ). Phagocytosis in Acanthamoeba: II. Soluble and insoluble mannose-rich ligands stimulate phosphoinositide metabolism. J Cell Physiol 145, 514–521.[CrossRef]
    [Google Scholar]
  3. Andrews, T. & Sullivan, K. E. ( 2003; ). Infections in patients with inherited defects in phagocytic function. Clin Microbiol Rev 16, 597–621.[CrossRef]
    [Google Scholar]
  4. Barker, K., Fan, H., Carroll, C., Kaplan, G., Barker, J., Hellmann, W. & Cohn, Z. A. ( 1996; ). Nonadherent cultures of human monocytes kill Mycobacterium smegmatis, but adherent cultures do not. Infect Immun 64, 428–433.
    [Google Scholar]
  5. Bashyam, M. D. & Tyagi, A. ( 1994; ). An efficient and high-yielding method for isolation of RNA from mycobacteria. Biotechniques 17, 834–836.
    [Google Scholar]
  6. Brooks, S. E. & Schneider, D. L. ( 1985; ). Oxidative metabolism associated with phagocytosis in Acanthamoeba castellanii. J Protozool 32, 330–333.[CrossRef]
    [Google Scholar]
  7. Brown, M. R. & Barker, J. ( 1999; ). Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol 7, 46–50.[CrossRef]
    [Google Scholar]
  8. Brown-Elliott, B. A. & Wallace, R. J. J. ( 2002; ). Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 15, 716–746.[CrossRef]
    [Google Scholar]
  9. Bruhn, H., Riekens, B., Berninghausen, O. & Leippe, M. ( 2003; ). Amoebapores and NK-lysin, members of a class of structurally distinct antimicrobial and cytolytic peptides from protozoa and mammals: a comparative functional analysis. Biochem J 375, 737–744.[CrossRef]
    [Google Scholar]
  10. Cirillo, J. D., Falkow, S., Tompkins, L. S. & Bermudez, L. E. ( 1997; ). Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 65, 3759–3767.
    [Google Scholar]
  11. Cotter, P. D. & Hill, C. ( 2003; ). Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67, 429–453.[CrossRef]
    [Google Scholar]
  12. Daley, C. L. & Griffith, D. E. ( 2002; ). Pulmonary disease caused by rapidly growing mycobacteria. Clin Chest Med 23, 623–632, vii.[CrossRef]
    [Google Scholar]
  13. Deretic, V. & Fratti, R. A. ( 1999; ). Mycobacterium tuberculosis phagosome. Mol Microbiol 31, 1603–1609.[CrossRef]
    [Google Scholar]
  14. Dorner, B. G., Scheffold, A., Rolph, M. S., Huser, M. B., Kaufmann, S. H., Radbruch, A., Flesch, I. E. & Kroczek, R. A. ( 2002; ). MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc Natl Acad Sci U S A 99, 6181–6186.[CrossRef]
    [Google Scholar]
  15. Engelhardt, H., Heinz, C. & Niederweis, M. ( 2002; ). A tetrameric porin limits the cell wall permeability of Mycobacterium smegmatis. J Biol Chem 277, 37567–37572.[CrossRef]
    [Google Scholar]
  16. Faller, M., Niederweis, M. & Schulz, G. E. ( 2004; ). The structure of a mycobacterial outer-membrane channel. Science 303, 1189–1192.[CrossRef]
    [Google Scholar]
  17. Fratti, R. A., Chua, J., Vergne, I. & Deretic, V. ( 2003; ). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100, 5437–5442.[CrossRef]
    [Google Scholar]
  18. Gao, L. Y., Laval, F., Lawson, E. H., Groger, R. K., Woodruff, A., Morisaki, J. H., Cox, J. S., Daffe, M. & Brown, E. J. ( 2003; ). Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol Microbiol 49, 1547–1563.[CrossRef]
    [Google Scholar]
  19. Greub, G. & Raoult, D. ( 2004; ). Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17, 413–433.[CrossRef]
    [Google Scholar]
  20. Heinz, C., Engelhardt, H. & Niederweis, M. ( 2003; ). The core of the tetrameric mycobacterial porin MspA is an extremely stable beta-sheet domain. J Biol Chem 278, 8678–8685.[CrossRef]
    [Google Scholar]
  21. Howard, S. T. & Byrd, T. F. ( 2000; ). The rapidly growing mycobacteria: saprophytes and parasites. Microbes Infect 2, 1845–1853.[CrossRef]
    [Google Scholar]
  22. Jouanguy, E., Lamhamedi-Cherradi, S., Lammas, D. & 19 other authors ( 1999; ). A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection. Nat Genet 21, 370–378.[CrossRef]
    [Google Scholar]
  23. Kaps, I., Ehrt, S., Seeber, S., Schnappinger, D., Martin, C., Riley, L. W. & Niederweis, M. ( 2001; ). Energy transfer between fluorescent proteins using a co-expression system in Mycobacterium smegmatis. Gene 278, 115–124.[CrossRef]
    [Google Scholar]
  24. Kumar, D., Srivastava, B. S. & Srivastava, R. ( 1998; ). Genetic rearrangements leading to disruption of heterologous gene expression in mycobacteria: an observation with Escherichia coli beta-galactosidase in Mycobacterium smegmatis and its implication in vaccine development. Vaccine 16, 1212–1215.[CrossRef]
    [Google Scholar]
  25. Lewin, A., Freytag, B., Meister, B., Sharbati-Tehrani, S., Schafer, H. & Appel, B. ( 2003; ). Use of a quantitative TaqMan-PCR for the fast quantification of mycobacteria in broth culture, eukaryotic cell culture and tissue. J Vet Med B Infect Dis Vet Public Health 50, 505–509.[CrossRef]
    [Google Scholar]
  26. Mailaender, C., Reiling, N., Engelhardt, H., Bossmann, S., Ehlers, S. & Niederweis, M. ( 2004; ). The MspA porin promotes growth and increases antibiotic susceptibility of both Mycobacterium bovis BCG and Mycobacterium tuberculosis. Microbiology 150, 853–864.[CrossRef]
    [Google Scholar]
  27. McNeil, P. L., Tanasugarn, L., Meigs, J. B. & Taylor, D. L. ( 1983; ). Acidification of phagosomes is initiated before lysosomal enzyme activity is detected. J Cell Biol 97, 692–702.[CrossRef]
    [Google Scholar]
  28. Miltner, E. C. & Bermudez, L. E. ( 2000; ). Mycobacterium avium grown in Acanthamoeba castellanii is protected from the effects of antimicrobials. Antimicrob Agents Chemother 44, 1990–1994.[CrossRef]
    [Google Scholar]
  29. Moffat, J. F. & Tompkins, L. S. ( 1992; ). A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellanii. Infect Immun 60, 296–301.
    [Google Scholar]
  30. Niederweis, M. ( 2003; ). Mycobacterial porins – new channel proteins in unique outer membranes. Mol Microbiol 49, 1167–1177.[CrossRef]
    [Google Scholar]
  31. Niederweis, M., Ehrt, S., Heinz, C., Klocker, U., Karosi, S., Swiderek, K. M., Riley, L. W. & Benz, R. ( 1999; ). Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol Microbiol 33, 933–945.[CrossRef]
    [Google Scholar]
  32. Pierre-Audigier, C., Jouanguy, E., Lamhamedi, S. & 9 other authors ( 1997; ). Fatal disseminated Mycobacterium smegmatis infection in a child with inherited interferon gamma receptor deficiency. Clin Infect Dis 24, 982–984.[CrossRef]
    [Google Scholar]
  33. Sander, P., Meier, A. & Bottger, E. C. ( 1995; ). rpsL+: a dominant selectable marker for gene replacement in mycobacteria. Mol Microbiol 16, 991–1000.[CrossRef]
    [Google Scholar]
  34. Schnappinger, D., Ehrt, S., Voskuil, M. I. & 8 other authors ( 2003; ). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198, 693–704.[CrossRef]
    [Google Scholar]
  35. Schreiber, J., Burkhardt, U., Rusch-Gerdes, S., Amthor, M., Richter, E., Zugehor, M., Rosahl, W. & Ernst, M. ( 2001; ). Non-tubercular mycobacterial infection of the lungs due to Mycobacterium smegmatis (in German). Pneumologie 55, 238–243.[CrossRef]
    [Google Scholar]
  36. Sharbati-Tehrani, S., Meister, B., Appel, B. & Lewin, A. ( 2004; ). The porin MspA from Mycobacterium smegmatis improves growth of Mycobacterium bovis BCG. Int J Med Microbiol 294, 235–245.[CrossRef]
    [Google Scholar]
  37. Stahl, C., Kubetzko, S., Kaps, I., Seeber, S., Engelhardt, H. & Niederweis, M. ( 2001; ). MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol Microbiol 40, 451–464.[CrossRef]
    [Google Scholar]
  38. Steinert, M., Birkness, K., White, E., Fields, B. & Quinn, F. ( 1998; ). Mycobacterium avium bacilli grow saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Appl Environ Microbiol 64, 2256–2261.
    [Google Scholar]
  39. Stephan, J., Mailaender, C., Etienne, G., Daffe, M. & Niederweis, M. ( 2004a; ). Multidrug resistance of a porin deletion mutant of Mycobacterium smegmatis. Antimicrob Agents Chemother 48, 4163–4170.[CrossRef]
    [Google Scholar]
  40. Stephan, J., Stemmer, V. & Niederweis, M. ( 2004b; ). Consecutive gene deletions in Mycobacterium smegmatis using the yeast FLP recombinase. Gene 343, 181–190.[CrossRef]
    [Google Scholar]
  41. Taylor, S. J., Ahonen, L. J., de Leij, F. A. & Dale, J. W. ( 2003; ). Infection of Acanthamoeba castellanii with Mycobacterium bovis and M. bovis BCG and survival of M. bovis within the amoebae. Appl Environ Microbiol 69, 4316–4319.[CrossRef]
    [Google Scholar]
  42. Vergne, I., Chua, J., Singh, S. B. & Deretic, V. ( 2004; ). Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20, 367–394.[CrossRef]
    [Google Scholar]
  43. Vonmoos, S., Leuenberger, P., Beer, V. & de Haller, R. ( 1986; ). Pleuropulmonary infection caused by Mycobacterium smegmatis. Case description and literature review (in German). Schweiz Med Wochenschr 116, 1852–1856.
    [Google Scholar]
  44. Walochnik, J., Obwaller, A. & Aspock, H. ( 2000; ). Correlations between morphological, molecular biological, and physiological characteristics in clinical and nonclinical isolates of Acanthamoeba spp. Appl Environ Microbiol 66, 4408–4413.[CrossRef]
    [Google Scholar]
  45. Winiecka-Krusnell, J. & Linder, E. ( 2001; ). Bacterial infections of free-living amoebae. Res Microbiol 152, 613–619.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27969-0
Loading
/content/journal/micro/10.1099/mic.0.27969-0
Loading

Data & Media loading...

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