Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1994 Jan 15;297(Pt 2):351–357. doi: 10.1042/bj2970351

Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis.

A Lemassu 1, M Daffé 1
PMCID: PMC1137836  PMID: 8297342

Abstract

The cell envelope which surrounds pathogenic mycobacteria is postulated to be a defence barrier against phagocytic cells and its outermost constituents have a tendency to accumulate in the culture medium. The present work demonstrates that the exocellular material of Mycobacterium tuberculosis contains large amounts of polysaccharides with only traces, if any at all, of lipids. Three types of polysaccharides were purified by anion-exchange and gel-filtration chromatography; all were found to be neutral compounds devoid of acyl substituents. They consisted of D-glucan, D-arabino-D-mannan and D-mannan, which were eluted from gel-filtration columns in positions corresponding to molecular masses of 123, 13 and 4 kDa respectively. Their predominant structural features were determined by the characterization of the per-O-methyl derivatives of enzymic, acetolysis and Smith-degradation products and by 1H- and 13C-n.m.r. spectroscopy of the purified polysaccharides, using mono- and two-dimensional homonuclear chemical-shift correlated spectroscopy and two-dimensional heteronuclear (1H/13C) spectroscopy. The glucan which represented up to 90% of the polysaccharides was composed of repeating units of five or six-->4-alpha-D-Glcp-1--> residues and a -->4-alpha-D-Glcp substituted at position 6 with an alpha-D-Glcp, indicating a glycogen-like highly branched structure not related to the so-called polysaccharide-II previously identified in tuberculin. The arabinomannan consisted of a mannan segment composed of a -->6-alpha-D-Man-1--> core substituted at some positions 2 with an alpha-D-Manp. The arabinan termini of the arabinomannan were found to be extensively capped with mannosyl residues. The possibility that these polysaccharides contribute to the persistence of the tubercle bacillus in the macrophage by molecular mimicry is discussed.

Full text

PDF
351

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antoine A. D., Tepper B. S. Characterization of glycogens from mycobacteria. Arch Biochem Biophys. 1969 Oct;134(1):207–213. doi: 10.1016/0003-9861(69)90267-7. [DOI] [PubMed] [Google Scholar]
  2. Barrow W. W. Contributing factors of pathogenesis in the Mycobacterium avium complex. Res Microbiol. 1991 May;142(4):427–433. doi: 10.1016/0923-2508(91)90115-q. [DOI] [PubMed] [Google Scholar]
  3. Bradbury J. H., Jenkins G. A. Determination of the structures of trisaccharides by 13C-n.m.r. spectroscopy. Carbohydr Res. 1984 Mar 1;126(1):125–156. doi: 10.1016/0008-6215(84)85131-9. [DOI] [PubMed] [Google Scholar]
  4. Chatterjee D., Bozic C. M., McNeil M., Brennan P. J. Structural features of the arabinan component of the lipoarabinomannan of Mycobacterium tuberculosis. J Biol Chem. 1991 May 25;266(15):9652–9660. [PubMed] [Google Scholar]
  5. Chatterjee D., Lowell K., Rivoire B., McNeil M. R., Brennan P. J. Lipoarabinomannan of Mycobacterium tuberculosis. Capping with mannosyl residues in some strains. J Biol Chem. 1992 Mar 25;267(9):6234–6239. [PubMed] [Google Scholar]
  6. Daffe 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 Apr 25;265(12):6734–6743. [PubMed] [Google Scholar]
  7. Daffé M., Servin P. Scalar, dipolar-correlated and J-resolved 2D-NMR spectroscopy of the specific phenolic mycoside of Mycobacterium tuberculosis. Eur J Biochem. 1989 Oct 20;185(1):157–162. doi: 10.1111/j.1432-1033.1989.tb15097.x. [DOI] [PubMed] [Google Scholar]
  8. Draper P., Rees R. J. Electron-transparent zone of mycobacteria may be a defence mechanism. Nature. 1970 Nov 28;228(5274):860–861. doi: 10.1038/228860a0. [DOI] [PubMed] [Google Scholar]
  9. Ellner J. J., Daniel T. M. Immunosuppression by mycobacterial arabinomannan. Clin Exp Immunol. 1979 Feb;35(2):250–257. [PMC free article] [PubMed] [Google Scholar]
  10. 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 Jun 5;265(16):9272–9279. [PubMed] [Google Scholar]
  11. Jennings H. J. Capsular polysaccharides as human vaccines. Adv Carbohydr Chem Biochem. 1983;41:155–208. doi: 10.1016/s0065-2318(08)60058-x. [DOI] [PubMed] [Google Scholar]
  12. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  13. Lemassu A., Lévy-Frébault V. V., Lanéelle M. A., Daffé M. Lack of correlation between colony morphology and lipooligosaccharide content in the Mycobacterium tuberculosis complex. J Gen Microbiol. 1992 Jul;138(7):1535–1541. doi: 10.1099/00221287-138-7-1535. [DOI] [PubMed] [Google Scholar]
  14. McNeil M., Daffe M., Brennan P. J. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem. 1991 Jul 15;266(20):13217–13223. [PubMed] [Google Scholar]
  15. 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 Dec;82(6):1759–1770. doi: 10.1093/oxfordjournals.jbchem.a131874. [DOI] [PubMed] [Google Scholar]
  16. Misaki A., Seto N., Azuma I. Structure and immunological properties of D-arabino-D-galactans isolated from cell walls of Mycobacterium species. J Biochem. 1974 Jul;76(1):15–27. doi: 10.1093/oxfordjournals.jbchem.a130540. [DOI] [PubMed] [Google Scholar]
  17. Sugden E. A., Samagh B. S., Bundle D. R., Duncan J. R. Lipoarabinomannan and lipid-free arabinomannan antigens of Mycobacterium paratuberculosis. Infect Immun. 1987 Mar;55(3):762–770. doi: 10.1128/iai.55.3.762-770.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. TSUMITA T., OHASHI M. A SYNTHETIC ACYL POLYSACCHARIDE AND THE HEMAGGLUTINATION ACTIVITY. J Exp Med. 1964 Jan 1;119:1017–1025. doi: 10.1084/jem.119.6.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Weber P. L., Gray G. R. Structural and immunochemical characterization of the acidic arabinomannan of Mycobacterium smegmatis. Carbohydr Res. 1979 Sep;74:259–278. doi: 10.1016/s0008-6215(00)84781-3. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES