1887

Abstract

It has been shown that phagocyte mannose receptors play an important role in phagocytosis of virulent tubercle bacilli, but not of avirulent strains. Accordingly, we investigated the occurrence and structure of the outermost mannoconjugates of the capsule of five strains of the tubercle bacillus differing in their degrees of virulence. The extracellular and surface-exposed arabinomannan-containing polysaccharides were chemically characterized as being composed mainly of neutral fatty-acyl-free arabinomannans (AMs) possessing a reducing end consisting of mannose. Although no lipoarabinomannan (LAM) was detected, small amounts of acidic polysaccharides, exhibiting the same electrophoretic mobility as LAM, were identified as succinylated AMs (two to three residues per molecule) lacking the phosphatidylinositol anchor of LAM. AMs from the different strains shared the same structural features, notably the capping of a large portion of the arabinan segments with mannosyl residues. However, no correlation was observed between either the percentage of capping or the amount of AMs and the degrees of virulence of the strains. The occurrence and amounts of other mannoconjugates (phosphatidylinositol mannosides and the mannoseassociated 19 and 38 kDa lipoproteins) in the various tubercle bacilli were also examined. Although both classes of compounds were identified in all the examined strains, a correlation between the amounts of the glycoconjugates and the degrees of virulence of the strains could not be established. These data do not support the implication of these promising mannosylated molecules in the selective phagocytosis of virulent tubercle bacilli and indicate that the involvement of mannose receptors in phagocytosis of virulent needs to be re-investigated.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-142-4-927
1996-04-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/142/4/mic-142-4-927.html?itemId=/content/journal/micro/10.1099/00221287-142-4-927&mimeType=html&fmt=ahah

References

  1. Andersen A.B., Yuan Z.L., Haslov K., Vergmann B., Bennedsen J. Interspecies reactivity of five monoclonal antibodies to Mycobacterium tuberculosis as examined by immuno-blotting and enzyme-linked immunosorbent assay. Infect Immun 1986; 23:446–451
    [Google Scholar]
  2. Asselineau J. Branched-chain fatty acids of mycobacteria. Indian J Chest Dis 1982; 24:143–157
    [Google Scholar]
  3. Bermudez L.E., Young L.S., Enkel H. Interaction of Mycobacterium avium complex with human macrophages: roles of membrane receptors and serum proteins. Infect Immun 1991; 59:1697–1702
    [Google Scholar]
  4. Bloom B.R., Murray J.L. Tuberculosis: commentary on a reemergent killer. Science 1992; 257:1055–1064
    [Google Scholar]
  5. Bradbury J.H., Jenkins G.A. Determination of the structures of trisaccharides by 13C-NMR spectroscopy. Carbohydr Res 1984; 126:125–156
    [Google Scholar]
  6. Chatterjee D., Bozic C., McNeil M., Brennan P.J. Structural features of the arabinan component of the lipo-arabinomannan of Mycobacterium tuberculosis. J Biol Chem 1991; 266:9652–9660
    [Google Scholar]
  7. Chatterjee D., Hunter S.W., McNeil M., Brennan P.J. Lipoarabinomannan. Multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J Biol Chem 1992a; 267:6228–6233
    [Google Scholar]
  8. Chatterjee D., Lowell K., Rivoire B., McNeil M.R., Brennan P.J. Lipoarabinomannan of Mycobacterium tuberculosis: capping with mannosyl residues in some strains. Biol Chem 1992b; 267:6234–6239
    [Google Scholar]
  9. Daffé M., Lanéelle M.-A., Asselineau C., Lévy-Frébault V., David H.L. Intérêt taxonomique des acides gras des mycobactéries: proposition d’une méthode d’analyse. Ann Microbiol Inst Pasteur 1983; 134:367–377
    [Google Scholar]
  10. Daffé M., Brennan P.J., McNeil M. Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H- and 13C-NMR analyses. J Biol Chem 1990; 265:6734–6743
    [Google Scholar]
  11. Daffé M., Brennan P.J., McNeil M. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodo-coccus, and Nocardia spp. Carbohydr Res 1993; 249:383–398
    [Google Scholar]
  12. Dittmer J.C.F., Lester R.L. A simple specific spray for the detection of phospholipids on thin layer chromatograms. J Eipid Res 1964; 5:126–127
    [Google Scholar]
  13. Ellner J.J., Daniel T.M. Immunosuppression by mycobacterial arabinomannan. Clin Exp Immunol 1979; 35:250–257
    [Google Scholar]
  14. Espitia C., Mancilla R. Identification, isolation and partial characterization of Mycobacterium tuberculosis glycoprotein antigens. Clin Exp Immunol 1989; 77:378–383
    [Google Scholar]
  15. Espitia C., Onate A., Zhang Y., Young D., Moreno C. Biochemical characterization of native and recombinant Con-A binding proteins of Mycobacterium tuberculosis. Abstr Second Int Conf Pathog Mycobact Infect (Stockholm) 199352
    [Google Scholar]
  16. Espitia C., Espinosa R., Saavedra R., Mancilla R., Romain F., Laqueyrerie A., Moreno C. Antigenic and structural similarities between Mycobacterium tuberculosis 50- to 55-kilodalton and Mycobacterium bovis BCG 45- to 47-kilodalton antigens. Infect Immun 1995; 63:580–584
    [Google Scholar]
  17. Fournié J.-J., Mullins R.J., Basten A. Isolation and structural characteristics of a monoclonal antibody-defined crossreactive phospholipid antigen from Mycobacterium tuberculosis and Mycobacterium leprae. J Biol Chem 1991; 266:1211–1219
    [Google Scholar]
  18. Garbe T., Harris D., Vordermeier M., Lathigra R., Ivanyi J., Young D. Expression of the Mycobacterium tuberculosis 19-kilodalton antigen in Mycobacterium smegmatis\ immunological analysis and evidence of glycosylation. Inject Immun 1993; 61:260–267
    [Google Scholar]
  19. Goren M.B., Brennan P.J. Mycobacterial lipids. In Tuberculosis 1979 Edited by Youmans G.P. Philadelphia: W. B. Saunders; pp 69–193
    [Google Scholar]
  20. Gorin A.J., Mazurek M. Further studies on the assignment of signals in 13C magnetic resonance spectra of aldoses and derived methyl glycosides. Can J Chem 1975; 53:1212–1223
    [Google Scholar]
  21. Hetland G., Wiker H.G. Antigen 85C on Mycobacterium bovis BCG and M. tuberculosis promotes monocyte-CR3-mediated uptake of microbeads coated with mycobacterial products. Immunology 1994; 82:445–449
    [Google Scholar]
  22. Hirsch C.S., Ellner J.J., Russell D.G., Rich E.A. Complement receptor-mediated uptake and tumor necrosis factor-a-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J Immunol 1994; 152:743–753
    [Google Scholar]
  23. Hunter S.W., Brennan P.J. Evidence for the presence of a phosphatidylinositol anchor on the lipoarabinomannan and lipomannan of Mycobacterium tuberculosis. J Biol Chem 1990; 265:9272–9279
    [Google Scholar]
  24. Khoo K.-H., Dell A., Morris H.R., Brennan P.J., Chatterjee D. Inositol phosphate capping of the nonreducing termini of lipoarabinomannan from rapidly growing strains of Mycobacterium. J Biol Chem 1995; 270:12380–12389
    [Google Scholar]
  25. Kochi A. The global tuberculosis situation and the new control strategy of the World Health Organization. Tubercle 1991; 72:1–6
    [Google Scholar]
  26. Lemassu A., Daffé M. tructural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem J 1994; 297:351–357
    [Google Scholar]
  27. Ljungqvist L., Worsaae A., Heron I. Antibody responses against Mycobacterium tuberculosis in 11 strains of inbred mice: novel monoclonal antibody specificities generated by fusions, using spleens from BALB. 10 and CBA/J mice. Infect Immun 1988; 56:1994–1998
    [Google Scholar]
  28. Misaki A., Azuma I., Yamamura Y. Structural and immunochemical studies on D-arabino-D-mannans and D-mannans of Mycobacterium tuberculosis and other Mycobacterium species. J Biochem 1977; 82:1759–1770
    [Google Scholar]
  29. Moreno C., Mehlert A., Lamb J. The inhibitory effects of mycobacterial lipoarabinomannan and polysaccharides upon polyclonal and monoclonal human T cell proliferation. Clin Exp 1988; ImmunollA:206–210
    [Google Scholar]
  30. Ortalo-Magné A., Dupont M.-A., Lemassu A., Andersen A.B., Gounon P., Daffé M. Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 1995; 141:1605–1620
    [Google Scholar]
  31. Prinzis S., Chatterjee D., Brennan P.J. Structure and antigenicity of lipoarabinomannan from Mycobacterium bovis BCG. J Gen Microbiol 1994; 139:2649–2658
    [Google Scholar]
  32. Sauton B. Sur la nutrition minérale du bacille tuberculeux. C R Acad Sei Ser III Sei Vie 1912; 155:860–863
    [Google Scholar]
  33. Schlesinger L.S. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 1993; 150:2920–2930
    [Google Scholar]
  34. Schlesinger L.S., Horwitz M.A. Phagocytosis of leprosy bacilli is mediated by complement receptors CR1 and CR3 on human monocytes and complement component C3 in serum. J Clin Invest 1990; 85:1304–1314
    [Google Scholar]
  35. Schlesinger L.S., Horwitz M.A. Phagocytosis of Mycobacterium leprae by human monocyte-derived macrophages is mediated by complement receptors CRI (CD35), CR3 (CDllb/CD18), CR4 (CDllc/CD18) and IFN-y activation inhibits complement receptor function and phagocytosis of this bacterium. J Immunol 1991; 147:1983–1994
    [Google Scholar]
  36. Schlesinger L.S., Bellinger-Kawahara C.G., Payne N.R., Horwitz M.A. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 1990; 144:2771–2780
    [Google Scholar]
  37. Schlesinger L.S., Hull S.R., Kaufman T.M. Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 1994; 152:4070–4079
    [Google Scholar]
  38. Steenken W., Gardner L.U. R1 strain of tubercle bacillus. Am Rev Tuberc 1946a; 54:51–61
    [Google Scholar]
  39. Steenken W., Gardner L.U. History of H37 strain of tubercle bacillus. Am Rev Tuberc 1946b; 54:62–66
    [Google Scholar]
  40. Stokes R.W., Haidl I.D., Jefferies W.A., Speert D.P. Mycobacteria-macrophage interactions. Macrophage phenotype determines the nonopsonic binding of Mycobacterium tuberculosis to murine macrophages. J Immunol 1993; 151:7067–7076
    [Google Scholar]
  41. Venisse A., Berjeaud J.-M., Chaurand P., Gilleron M., Puzo G. Structural features of lipoarabinomannan from Mycobacterium bovis BCG. J Biol Chem 1993; 268:12401–12411
    [Google Scholar]
  42. Weber P.L., Gray G.R. Structural and immunochemical characterization of the acidic arabinomannan of Mycobacterium smegmatis. Carbohydr Res 1979; 74:259–278
    [Google Scholar]
  43. Young D.B., Kaufmann S.H.E., Hermans P.W.M., Thole J.E.R. Mycobacterial protein antigens: a compilation. Mol Microbiol 1992; 6:133–145
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-142-4-927
Loading
/content/journal/micro/10.1099/00221287-142-4-927
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