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. 1984 Jul;45(1):160–165. doi: 10.1128/iai.45.1.160-165.1984

Interaction of group A streptococcal peptidoglycan polysaccharide with human polymorphonuclear leukocytes: implications for pathogenesis of chronic inflammation.

P A Leong, J H Schwab, M S Cohen
PMCID: PMC263294  PMID: 6329955

Abstract

Injection of sterile aqueous preparations of the peptidoglycan polysaccharide of group A streptococci produces chronic inflammation in several animal models. Accordingly, the effect of peptidoglycan and group A-specific polysaccharide (PG-APS) polymers on human polymorphonuclear neutrophil oxidative metabolism was studied with the supposition that this interaction may contribute to the inflammation observed. PG-APS in concentrations of 1.0 to 100 micrograms/ml stimulated oxygen consumption and hexose monophosphate shunt activity in the presence of 10% normal serum in a dose-related manner. Stimulation did not occur in serum-free media and was reduced in media with heat-treated serum. The stimulation of hexose monophosphate shunt activity by PG-APS opsonized with normal serum (bound complement components) and the activated supernatant from which PG-APS had been removed by centrifugation (presumably containing the soluble complement component, C5a) demonstrated 79 and 75%, respectively, of the stimulation with PG-APS in the presence of 10% normal serum. PG-APS triggered release of O2- (3.4 +/- 2.0 nmol by 10(6) human polymorphonuclear neutrophils over 30 min), which was significantly enhanced (9.6 +/- 2.9 nmol O2-) by treatment of cells with cytochalasin B. These results show that PG-APS interacts with serum in such a fashion as to activate human polymorphonuclear neutrophil metabolism and increase secretion of O2-.

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Selected References

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

  1. Abdulla E. M., Schwab J. H. Biological properties of streptococcal cell-wall particles. 3. Dermonecrotic reaction to cell-wall mucopeptides. J Bacteriol. 1966 Jan;91(1):374–383. doi: 10.1128/jb.91.1.374-383.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ayoub E. M., McCarty M. Intraphagocytic beta-N-acetylglucosaminidase. Properties of the enzyme and its activity on group A streptococcal carbohydrate in comparison with a soil bacillus enzyme. J Exp Med. 1968 Apr 1;127(4):833–851. doi: 10.1084/jem.127.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ayoub E. M., Wannamaker L. W. The fate of group A streptococci following phagocytosis. In vitro phagocytic studies of isotope-labeled streptococci. J Immunol. 1967 Dec;99(6):1099–1105. [PubMed] [Google Scholar]
  4. Babior B. M., Kipnes R. S., Curnutte J. T. Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest. 1973 Mar;52(3):741–744. doi: 10.1172/JCI107236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chetty C., Klapper D. G., Schwab J. H. Soluble peptidoglycan-polysaccharide fragments of the bacterial cell wall induce acute inflammation. Infect Immun. 1982 Dec;38(3):1010–1019. doi: 10.1128/iai.38.3.1010-1019.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen M. S., Metcalf J. A., Root R. K. Regulation of oxygen metabolism in human granulocytes: relationship between stimulus binding and oxidative response using plant lectins as probes. Blood. 1980 Jun;55(6):1003–1010. [PubMed] [Google Scholar]
  7. Cromartie W. J., Craddock J. G. Rheumatic-like cardiac lesions in mice. Science. 1966 Oct 14;154(3746):285–287. doi: 10.1126/science.154.3746.285. [DOI] [PubMed] [Google Scholar]
  8. Cromartie W. J., Craddock J. G., Schwab J. H., Anderle S. K., Yang C. H. Arthritis in rats after systemic injection of streptococcal cells or cell walls. J Exp Med. 1977 Dec 1;146(6):1585–1602. doi: 10.1084/jem.146.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dalldorf F. G., Cromartie W. J., Anderle S. K., Clark R. L., Schwab J. H. The relation of experimental arthritis to the distribution of streptococcal cell wall fragments. Am J Pathol. 1980 Aug;100(2):383–402. [PMC free article] [PubMed] [Google Scholar]
  10. Eisenberg R., Fox A., Greenblatt J. J., Anderle S. K., Cromartie W. J., Schwab J. H. Measurement of bacterial cell wall in tissues by solid-phase radioimmunoassay: correlation of distribution and persistence with experimental arthritis in rats. Infect Immun. 1982 Oct;38(1):127–135. doi: 10.1128/iai.38.1.127-135.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fox A., Brown R. R., Anderle S. K., Chetty C., Cromartie W. J., Gooder H., Schwab J. H. Arthropathic properties related to the molecular weight of peptidoglycan-polysaccharide polymers of streptococcal cell walls. Infect Immun. 1982 Mar;35(3):1003–1010. doi: 10.1128/iai.35.3.1003-1010.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Glick A. D., Ranhand J. M., Cole R. M. Degradation of group A streptococcal cell walls by egg-white lysozyme and human lysosomal enzymes. Infect Immun. 1972 Sep;6(3):403–413. doi: 10.1128/iai.6.3.403-413.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldstein I. M., Roos D., Kaplan H. B., Weissmann G. Complement and immunoglobulins stimulate superoxide production by human leukocytes independently of phagocytosis. J Clin Invest. 1975 Nov;56(5):1155–1163. doi: 10.1172/JCI108191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Greenblatt J., Boackle R. J., Schwab J. H. Activation of the alternate complement pathway by peptidoglycan from streptococcal cell wall. Infect Immun. 1978 Jan;19(1):296–303. doi: 10.1128/iai.19.1.296-303.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hunter N., Schwab J. H., Simpson D. M. Experimental periodontitis induced in rats by streptococcal cell wall fragments. J Periodontal Res. 1979 Nov;14(6):453–466. doi: 10.1111/j.1600-0765.1979.tb00245.x. [DOI] [PubMed] [Google Scholar]
  16. Janoff A., Carp H. Proteases, antiproteases, and oxidants: pathways of tissue injury during inflammation. Monogr Pathol. 1982;(23):62–82. [PubMed] [Google Scholar]
  17. Jones J. M., Schwab J. H. Effects of streptococcal cell wall fragments on phagocytosis and tissue culture cells. Infect Immun. 1970 Mar;1(3):232–242. doi: 10.1128/iai.1.3.232-242.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Klebanoff S. J. Oxygen metabolism and the toxic properties of phagocytes. Ann Intern Med. 1980 Sep;93(3):480–489. doi: 10.7326/0003-4819-93-3-480. [DOI] [PubMed] [Google Scholar]
  19. Lehmeyer J. E., Snyderman R., Johnston R. B., Jr Stimulation of neutrophil oxidative metabolism by chemotactic peptides: influence of calcium ion concentration and cytochalasin B and comparison with stimulation by phorbol myristate acetate. Blood. 1979 Jul;54(1):35–45. [PubMed] [Google Scholar]
  20. Nathan C. F., Brukner L. H., Silverstein S. C., Cohn Z. A. Extracellular cytolysis by activated macrophages and granulocytes. I. Pharmacologic triggering of effector cells and the release of hydrogen peroxide. J Exp Med. 1979 Jan 1;149(1):84–99. doi: 10.1084/jem.149.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oliver J. M. Cell biology of leukocyte abnormalities--membrane and cytoskeletal function in normal and defective cells. A review. Am J Pathol. 1978 Oct;93(1):221–270. [PMC free article] [PubMed] [Google Scholar]
  22. Page R. C., Davies P., Allison A. C. Pathogenesis of the chronic inflammatory lesion induced by group A streptococcal cell walls. Lab Invest. 1974 May;30(5):568–581. [PubMed] [Google Scholar]
  23. Pryzwansky K. B., MacRae E. K., Lambris J. D. Capping of complement receptors on human neutrophils induced by group A streptococcal cell walls. J Immunol. 1983 Apr;130(4):1674–1677. [PubMed] [Google Scholar]
  24. Roos D., Homan-Müller J. W., Weening R. S. Effect of cytochalasin B on the oxidative metabolism of human peripheral blood granulocytes. Biochem Biophys Res Commun. 1976 Jan 12;68(1):43–50. doi: 10.1016/0006-291x(76)90007-3. [DOI] [PubMed] [Google Scholar]
  25. Root R. K., Metcalf J. A. H2O2 release from human granulocytes during phagocytosis. Relationship to superoxide anion formation and cellular catabolism of H2O2: studies with normal and cytochalasin B-treated cells. J Clin Invest. 1977 Dec;60(6):1266–1279. doi: 10.1172/JCI108886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Root R. K., Metcalf J., Oshino N., Chance B. H2O2 release from human granulocytes during phagocytosis. I. Documentation, quantitation, and some regulating factors. J Clin Invest. 1975 May;55(5):945–955. doi: 10.1172/JCI108024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SALTON M. R. The properties of lysozyme and its action on microorganisms. Bacteriol Rev. 1957 Jun;21(2):82–100. doi: 10.1128/br.21.2.82-100.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SCHWAB J. H., CROMARTIE W. J. Studies on a toxic cellular component of group A streptococci. J Bacteriol. 1957 Nov;74(5):673–679. doi: 10.1128/jb.74.5.673-679.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwab J. H., Ohanian S. H. Degradation of streptococcal cell wall antigens in vivo. J Bacteriol. 1967 Nov;94(5):1346–1352. doi: 10.1128/jb.94.5.1346-1352.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Smialowicz R. J., Schwab J. H. Cytotoxicity of rat macrophages activated by persistent or biodegradable bacterial cell walls. Infect Immun. 1977 Sep;17(3):599–606. doi: 10.1128/iai.17.3.599-606.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smialowicz R. J., Schwab J. H. Inhibition of macrophage phagocytic activity by group A streptococcal cell walls. Infect Immun. 1978 Apr;20(1):258–261. doi: 10.1128/iai.20.1.258-261.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smialowicz R. J., Schwab J. H. Processing of streptococcal cell walls by rat macrophages and human monocytes in vitro. Infect Immun. 1977 Sep;17(3):591–598. doi: 10.1128/iai.17.3.591-598.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

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