Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1987 Sep;169(9):4223–4227. doi: 10.1128/jb.169.9.4223-4227.1987

Structure of Bordetella pertussis peptidoglycan.

W J Folkening, W Nogami, S A Martin, R S Rosenthal
PMCID: PMC213733  PMID: 2887547

Abstract

Bordetella pertussis Tohama phases I and III were grown to the late-exponential phase in liquid medium containing [3H]diaminopimelic acid and treated by a hot (96 degrees C) sodium dodecyl sulfate extraction procedure. Washed sodium dodecyl sulfate-insoluble residue from phases I and III consisted of complexes containing protein (ca. 40%) and peptidoglycan (60%). Subsequent treatment with proteinase K yielded purified peptidoglycan which contained N-acetylglucosamine, N-acetylmuramic acid, alanine, glutamic acid, and diaminopimelic acid in molar ratios of 1:1:2:1:1 and less than 2% protein. Radiochemical analyses indicated that 3H added in diaminopimelic acid was present in peptidoglycan-protein complexes and purified peptidoglycan as diaminopimelic acid exclusively and that pertussis peptidoglycan was not O acetylated, consistent with it being degraded completely by hen egg white lysozyme. Muramidase-derived disaccharide peptide monomers and peptide-cross-linked dimers and higher oligomers were isolated by molecular-sieve chromatography; from the distribution of these peptidoglycan fragments, the extent of peptide cross-linking of both phase I and III peptidoglycan was calculated to be ca. 48%. Unambiguous determination of the structure of muramidase-derived peptidoglycan fragments by fast atom bombardment-mass spectrometry and tandem mass spectrometry indicated that the pertussis peptidoglycan monomer fraction was surprisingly homogeneous, consisting of greater than 95% N-acetylglucosaminyl-N-acetylmuramyl-alanyl-glutamyl-diaminopimelyl++ +-alanine.

Full text

PDF
4223

Selected References

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

  1. Abehsira-Amar O., Damais C., Parant M., Chedid L. Strain dependence of muramyl dipeptide-induced LAF(IL 1) release by murine-adherent peritoneal cells. J Immunol. 1985 Jan;134(1):365–368. [PubMed] [Google Scholar]
  2. Adam A., Ciorbaru R., Ellouz F., Petit J. F., Lederer E. Adjuvant activity of monomeric bacterial cell wall peptidoglycans. Biochem Biophys Res Commun. 1974 Feb 4;56(3):561–567. doi: 10.1016/0006-291x(74)90640-8. [DOI] [PubMed] [Google Scholar]
  3. Chedid L., Audibert F., Johnson A. G. Biological activities of muramyl dipeptide, a synthetic glycopeptide analogous to bacterial immunoregulating agents. Prog Allergy. 1978;25:63–105. [PubMed] [Google Scholar]
  4. Dougherty T. J. Analysis of Neisseria gonorrhoeae peptidoglycan by reverse-phase, high-pressure liquid chromatography. J Bacteriol. 1985 Jul;163(1):69–74. doi: 10.1128/jb.163.1.69-74.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fleming T. J., Wallsmith D. E., Rosenthal R. S. Arthropathic properties of gonococcal peptidoglycan fragments: implications for the pathogenesis of disseminated gonococcal disease. Infect Immun. 1986 May;52(2):600–608. doi: 10.1128/iai.52.2.600-608.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fraser-Smith E. B., Waters R. V., Matthews T. R. Correlation between in vivo anti-Pseudomonas and anti-Candida activities and clearance of carbon by the reticuloendothelial system for various muramyl dipeptide analogs, using normal and immunosuppressed mice. Infect Immun. 1982 Jan;35(1):105–110. doi: 10.1128/iai.35.1.105-110.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gmeiner J., Kroll H. P. Murein biosynthesis and O-acetylation of N-acetylmuramic acid during the cell-division cycle of Proteus mirabilis. Eur J Biochem. 1981 Jun;117(1):171–177. doi: 10.1111/j.1432-1033.1981.tb06317.x. [DOI] [PubMed] [Google Scholar]
  8. Goldman W. E., Klapper D. G., Baseman J. B. Detection, isolation, and analysis of a released Bordetella pertussis product toxic to cultured tracheal cells. Infect Immun. 1982 May;36(2):782–794. doi: 10.1128/iai.36.2.782-794.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Juy D., Chedid L. Comparison between macrophage activation and enhancement of nonspecific resistance to tumors by mycobacterial immunoadjuvants. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4105–4109. doi: 10.1073/pnas.72.10.4105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kohashi O., Pearson C. M., Watanabe Y., Kotani S., Koga T. Structural requirements for arthritogenicity of peptidoglycans from Staphylococcus aureus and Lactobacillus plant arum and analogous synthetic compounds. J Immunol. 1976 Jun;116(6):1635–1639. [PubMed] [Google Scholar]
  11. Krueger J. M., Pappenheimer J. R., Karnovsky M. L. The composition of sleep-promoting factor isolated from human urine. J Biol Chem. 1982 Feb 25;257(4):1664–1669. [PubMed] [Google Scholar]
  12. Martin S. A., Karnovsky M. L., Krueger J. M., Pappenheimer J. R., Biemann K. Peptidoglycans as promoters of slow-wave sleep. I. Structure of the sleep-promoting factor isolated from human urine. J Biol Chem. 1984 Oct 25;259(20):12652–12658. [PubMed] [Google Scholar]
  13. Martin S. A., Rosenthal R. S., Biemann K. Fast atom bombardment mass spectrometry and tandem mass spectrometry of biologically active peptidoglycan monomers from Neisseria gonorrhoeae. J Biol Chem. 1987 Jun 5;262(16):7514–7522. [PubMed] [Google Scholar]
  14. Melly M. A., McGee Z. A., Rosenthal R. S. Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis. 1984 Mar;149(3):378–386. doi: 10.1093/infdis/149.3.378. [DOI] [PubMed] [Google Scholar]
  15. Petersen B. H., Rosenthal R. S. Complement consumption gonococcal peptidoglycan. Infect Immun. 1982 Feb;35(2):442–448. doi: 10.1128/iai.35.2.442-448.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pisabarro A. G., de Pedro M. A., Vázquez D. Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J Bacteriol. 1985 Jan;161(1):238–242. doi: 10.1128/jb.161.1.238-242.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rosenthal R. S., Folkening W. J., Miller D. R., Swim S. C. Resistance of O-acetylated gonococcal peptidoglycan to human peptidoglycan-degrading enzymes. Infect Immun. 1983 Jun;40(3):903–911. doi: 10.1128/iai.40.3.903-911.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rosenthal R. S., Gfell M. A., Folkening W. J. Influence of protein synthesis inhibitors on regulation of extent of O-acetylation of gonococcal peptidoglycan. Infect Immun. 1985 Jul;49(1):7–13. doi: 10.1128/iai.49.1.7-13.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rosenthal R. S. Release of soluble peptidoglycan from growing gonococci: hexaminidase and amidase activities. Infect Immun. 1979 Jun;24(3):869–878. doi: 10.1128/iai.24.3.869-878.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rosenthal R. S., Wright R. M., Sinha R. K. Extent of peptide cross-linking in the peptidoglycan of Neisseria gonorrhoeae. Infect Immun. 1980 Jun;28(3):867–875. doi: 10.1128/iai.28.3.867-875.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sinha R. K., Rosenthal R. S. Release of soluble peptidoglycan from growing conococci: demonstration of anhydro-muramyl-containing fragments. Infect Immun. 1980 Sep;29(3):914–925. doi: 10.1128/iai.29.3.914-925.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stainer D. W., Scholte M. J. A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol. 1970 Oct;63(2):211–220. doi: 10.1099/00221287-63-2-211. [DOI] [PubMed] [Google Scholar]
  23. Swim S. C., Gfell M. A., Wilde C. E., 3rd, Rosenthal R. S. Strain distribution in extents of lysozyme resistance and O-acetylation of gonococcal peptidoglycan determined by high-performance liquid chromatography. Infect Immun. 1983 Nov;42(2):446–452. doi: 10.1128/iai.42.2.446-452.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Takada H., Tsujimoto M., Kato K., Kotani S., Kusumoto S., Inage M., Shiba T., Yano I., Kawata S., Yokogawa K. Macrophage activation by bacterial cell walls and related synthetic compounds. Infect Immun. 1979 Jul;25(1):48–53. doi: 10.1128/iai.25.1.48-53.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES