Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1980 Feb;27(2):335–343. doi: 10.1128/iai.27.2.335-343.1980

Sialidase-Enhanced Lectin-Like Mechanism for Actinomyces viscosus and Actinomyces naeslundii Hemagglutination

R P Ellen 1, E D Fillery 1, K H Chan 1, D A Grove 1
PMCID: PMC550769  PMID: 6769798

Abstract

Laboratory strains representing six numerical taxonomy clusters and fresh isolates of human Actinomyces viscosus and Actinomyces naeslundii were studied by standard flocculation slide tests for the ability to hemagglutinate erythrocytes (RBC) from various animal species. Human AB and horse RBC were agglutinated more frequently and rapidly than others; guinea pig RBC were agglutinated by only a few strains. Human AB RBC were selected for studies of hemagglutination mechanisms. Treatment of RBC with clostridial neuraminidase (NTRBC) greatly enhanced hemagglutination for almost all strains. In hapten inhibition experiments in which various concentrations of sugars were used, β-galactosides were the most effective inhibitors of hemagglutination for both RBC and NTRBC; inhibition of NTRBC agglutination required higher concentrations. Soybean lectin agglutinated both RBC and NTRBC but not Actinomyces cells. NTRBC agglutinated at a 125-fold-lower concentration. Hemagglutination was sensitive to ethylenediaminetetraacetate for one strain tested. Hemagglutination reactions were reversible by addition of β-galactosides. The ability of Actinomyces strains to “prime” RBC for hemagglutination by removing sialic acid to expose more penultimate β-galactoside sites was studied by recycling Actinomyces-agglutinated RBC which were dispersed with a lactose solution and washed free of bacteria (primed RBC). Priming in this manner augmented subsequent hemagglutination by indicator Actinomyces strains and made the RBC more sensitive to agglutination by soybean lectin. The priming ability of Actinomyces strains generally correlated with the amount of sialic acid removed from primed RBC. Strains representing the numerical taxonomy clusters differed in both their hemagglutinating and priming activities. Cluster 5 strains (typical A. naeslundii) were good agglutinators of RBC, NTRBC, and primed RBC but were poor primers. Cluster 3 strains (atypical A. naeslundii) were the weakest hemagglutinators but could prime RBC adequately for subsequent agglutination by other strains. Together, these data indicate that Actinomyces hemagglutination proceeds via a two-step mechanism: (i) neuraminidase removal of terminal sialic acid and (ii) lectin-like binding to exposed β-galactoside-associated sites on the RBC. Strains differ in the extent to which they can perform the two functions, and this specificity may relate to their taxonomic classification.

Full text

PDF
335

Images in this article

Selected References

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

  1. Bar-Shavit Z., Ofek I., Goldman R., Mirelman D., Sharon N. Mannose residues on phagocytes as receptors for the attachment of Escherichia coli and Salmonella typhi. Biochem Biophys Res Commun. 1977 Sep 9;78(1):455–460. doi: 10.1016/0006-291x(77)91276-1. [DOI] [PubMed] [Google Scholar]
  2. Burckhardt J. J., Guggenheim B., Hefti A. Are Actinomyces viscosus antigens B cell mitogens? J Immunol. 1977 Apr;118(4):1460–1465. [PubMed] [Google Scholar]
  3. Cisar J. O., Kolenbrander P. E., McIntire F. C. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun. 1979 Jun;24(3):742–752. doi: 10.1128/iai.24.3.742-752.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellen R. P. Establishment and distribution of Actinomyces viscosus and Actinomyces naeslundii in the human oral cavity. Infect Immun. 1976 Nov;14(5):1119–1124. doi: 10.1128/iai.14.5.1119-1124.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ellen R. P., Leung W. L., Fillery E. D., Grove D. A. Mannose-contaminating agglutinin for Actinomyces viscosus and Actinomyces naeslundii. Infect Immun. 1979 Nov;26(2):427–434. doi: 10.1128/iai.26.2.427-434.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ellen R. P., Walker D. L., Chan K. H. Association of long surface appendages with adherence-related functions of the gram-positive species Actinomyces naeslundii. J Bacteriol. 1978 Jun;134(3):1171–1175. doi: 10.1128/jb.134.3.1171-1175.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engel D., Schroeder H. E., Page R. C. Morphological features and functional properties of human fibroblasts exposed to Actinomyces viscosus substances. Infect Immun. 1978 Jan;19(1):287–295. doi: 10.1128/iai.19.1.287-295.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fillery E. D., Bowden G. H., Hardie J. M. A comparison of strains of bacteria designated Actinomyces viscosus and Actinomyces naeslundii. Caries Res. 1978;12(6):299–312. doi: 10.1159/000260349. [DOI] [PubMed] [Google Scholar]
  9. Gibbons R. A., Jones G. W., Sellwood R. An attempt to identify the intestinal receptor for the K88 adhesin by means of a haemagglutination inhibition test using glycoproteins and fractions from sow colostrum. J Gen Microbiol. 1975 Feb;86(2):228–240. doi: 10.1099/00221287-86-2-228. [DOI] [PubMed] [Google Scholar]
  10. Gibbons R. J., Qureshi J. V. Selective binding of blood group-reactive salivary mucins by Streptococcus mutans and other oral organisms. Infect Immun. 1978 Dec;22(3):665–671. doi: 10.1128/iai.22.3.665-671.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. McIntire F. C., Vatter A. E., Baros J., Arnold J. Mechanism of coaggregation between Actinomyces viscosus T14V and Streptococcus sanguis 34. Infect Immun. 1978 Sep;21(3):978–988. doi: 10.1128/iai.21.3.978-988.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ofek I., Beachey E. H. Mannose binding and epithelial cell adherence of Escherichia coli. Infect Immun. 1978 Oct;22(1):247–254. doi: 10.1128/iai.22.1.247-254.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Old D. C. Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol. 1972 Jun;71(1):149–157. doi: 10.1099/00221287-71-1-149. [DOI] [PubMed] [Google Scholar]
  14. Pinter J. K., Hayashi J. A., Bahn A. N. Extracellular streptococcal neuraminidase. J Bacteriol. 1968 Apr;95(4):1491–1492. doi: 10.1128/jb.95.4.1491-1492.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Salit I. E., Gotschlich E. C. Hemagglutination by purified type I Escherichia coli pili. J Exp Med. 1977 Nov 1;146(5):1169–1181. doi: 10.1084/jem.146.5.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Salit I. E., Gotschlich E. C. Type I Escherichia coli pili: characterization of binding to monkey kidney cells. J Exp Med. 1977 Nov 1;146(5):1182–1194. doi: 10.1084/jem.146.5.1182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sharon N., Lis H. Lectins: cell-agglutinating and sugar-specific proteins. Science. 1972 Sep 15;177(4053):949–959. doi: 10.1126/science.177.4053.949. [DOI] [PubMed] [Google Scholar]
  18. THONARD J. C., HEFFLIN C. M., STEINBERG A. I. NEURAMINIDASE ACTIVITY IN MIXED CULTURE SUPERNATANT FLUIDS OF HUMAN ORAL BACTERIA. J Bacteriol. 1965 Mar;89:924–925. doi: 10.1128/jb.89.3.924-925.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Taichman N. S., Hammond B. F., Tsai C. C., Baehni P. C., McArthur W. P. Interaction of inflammatory cells and oral microorganisms. VII. In vitro polymorphonuclear responses to viable bacteria and to subcellular components of avirulent and virulent strains of Actinomyces viscosus. Infect Immun. 1978 Aug;21(2):594–604. doi: 10.1128/iai.21.2.594-604.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tuyau J. E., Sims W. Occurrence of haemophili in dental plaque and their association with neuraminidase activity. J Dent Res. 1975 Jul-Aug;54(4):737–739. doi: 10.1177/00220345750540040701. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES