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. 1995 Dec;63(12):4589–4594. doi: 10.1128/iai.63.12.4589-4594.1995

Role of the capsular polysaccharide-like serotype-specific antigen in resistance of Actinobacillus actinomycetemcomitans to phagocytosis by human polymorphonuclear leukocytes.

N Yamaguchi 1, M Kawasaki 1, Y Yamashita 1, K Nakashima 1, T Koga 1
PMCID: PMC173659  PMID: 7591110

Abstract

Serotype b-specific polysaccharide antigen (SPA) of Actinobacillus actinomycetemcomitans Y4 consists of D-fucose and L-rhamnose. To clarify the role of SPA in phagocytosis of the organism by human polymorphonuclear leukocytes (PMNs), monoclonal antibodies (MAbs) against SPA and SPA-defective mutants, which were constructed by inserting the transposon Tn916 into strain Y4, were used in a chemiluminescence (CL) assay and a phagocytic killing assay. The CL responses of human PMNs to strain Y4 were very low, and the organism was not killed by PMNs. In contrast, SPA-defective mutants induced strong CL responses. The addition of immunoglobulin G MAbs against Y4 SPA enhanced significantly both the CL responses to strain Y4 and the killing of the organism in the presence of complement. The CL responses to SPA-defective mutants were little affected by the addition of these MAbs. We conclude that SPA of A. actinomycetemcomitans plays an important role in the resistance to host defenses by PMNs.

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Selected References

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  1. Absolom D. R. The role of bacterial hydrophobicity in infection: bacterial adhesion and phagocytic ingestion. Can J Microbiol. 1988 Mar;34(3):287–298. doi: 10.1139/m88-054. [DOI] [PubMed] [Google Scholar]
  2. Agarwal S., Suzuki J. B., Piesco N. P., Aichelmann-Reidy M. B. Neutrophil function in juvenile periodontitis: induction of adherence. Oral Microbiol Immunol. 1994 Oct;9(5):262–271. doi: 10.1111/j.1399-302x.1994.tb00069.x. [DOI] [PubMed] [Google Scholar]
  3. Amano K., Nishihara T., Shibuya N., Noguchi T., Koga T. Immunochemical and structural characterization of a serotype-specific polysaccharide antigen from Actinobacillus actinomycetemcomitans Y4 (serotype b). Infect Immun. 1989 Oct;57(10):2942–2946. doi: 10.1128/iai.57.10.2942-2946.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Amir J., Scott M. G., Nahm M. H., Granoff D. M. Bactericidal and opsonic activity of IgG1 and IgG2 anticapsular antibodies to Haemophilus influenzae type b. J Infect Dis. 1990 Jul;162(1):163–171. doi: 10.1093/infdis/162.1.163. [DOI] [PubMed] [Google Scholar]
  5. Asikainen S., Lai C. H., Alaluusua S., Slots J. Distribution of Actinobacillus actinomycetemcomitans serotypes in periodontal health and disease. Oral Microbiol Immunol. 1991 Apr;6(2):115–118. doi: 10.1111/j.1399-302x.1991.tb00462.x. [DOI] [PubMed] [Google Scholar]
  6. Baker P. J., Wilson M. E. Opsonic IgG antibody against Actinobacillus actinomycetemcomitans in localized juvenile periodontitis. Oral Microbiol Immunol. 1989 Jun;4(2):98–105. doi: 10.1111/j.1399-302x.1989.tb00106.x. [DOI] [PubMed] [Google Scholar]
  7. Baltimore R. S., Kasper D. L., Baker C. J., Goroff D. K. Antigenic specificity of opsonophagocytic antibodies in rabbit anti-sera to group B streptococci. J Immunol. 1977 Feb;118(2):673–678. [PubMed] [Google Scholar]
  8. Becker R. S. Conjugate vaccines: practice and theory. Springer Semin Immunopathol. 1993;15(2-3):217–226. doi: 10.1007/BF00201102. [DOI] [PubMed] [Google Scholar]
  9. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  10. Califano J. V., Schenkein H. A., Tew J. G. Immunodominant antigen of Actinobacillus actinomycetemcomitans Y4 in high-responder patients. Infect Immun. 1989 May;57(5):1582–1589. doi: 10.1128/iai.57.5.1582-1589.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. China B., N'Guyen B. T., de Bruyere M., Cornelis G. R. Role of YadA in resistance of Yersinia enterocolitica to phagocytosis by human polymorphonuclear leukocytes. Infect Immun. 1994 Apr;62(4):1275–1281. doi: 10.1128/iai.62.4.1275-1281.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Christersson L. A., Zambon J. J., Genco R. J. Dental bacterial plaques. Nature and role in periodontal disease. J Clin Periodontol. 1991 Jul;18(6):441–446. doi: 10.1111/j.1600-051x.1991.tb02314.x. [DOI] [PubMed] [Google Scholar]
  13. Cooper N. R. Complement evasion strategies of microorganisms. Immunol Today. 1991 Sep;12(9):327–331. doi: 10.1016/0167-5699(91)90010-Q. [DOI] [PubMed] [Google Scholar]
  14. Dahlgren C., Follin P., Johansson A., Lock R., Orselius K. Localization of the luminol-dependent chemiluminescence reaction in human granulocytes. J Biolumin Chemilumin. 1989 Jul;4(1):263–266. doi: 10.1002/bio.1170040137. [DOI] [PubMed] [Google Scholar]
  15. Ebersole J. L., Taubman M. A., Smith D. J., Hammond B. F., Frey D. E. Human immune responses to oral microorganisms. II. Serum antibody responses to antigens from Actinobacillus actinomycetemcomitans and the correlation with localized juvenile periodontitis. J Clin Immunol. 1983 Oct;3(4):321–331. doi: 10.1007/BF00915793. [DOI] [PubMed] [Google Scholar]
  16. Genco C. A., Schifferle R. E., Njoroge T., Forng R. Y., Cutler C. W. Resistance of a Tn4351-generated polysaccharide mutant of Porphyromonas gingivalis to polymorphonuclear leukocyte killing. Infect Immun. 1995 Feb;63(2):393–401. doi: 10.1128/iai.63.2.393-401.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gmür R., McNabb H., van Steenbergen T. J., Baehni P., Mombelli A., van Winkelhoff A. J., Guggenheim B. Seroclassification of hitherto nontypeable Actinobacillus actinomycetemcomitans strains: evidence for a new serotype e. Oral Microbiol Immunol. 1993 Apr;8(2):116–120. doi: 10.1111/j.1399-302x.1993.tb00556.x. [DOI] [PubMed] [Google Scholar]
  18. Hosker H. S., Kelly C., Corris P. A. Assessment of phagocytic function using chemiluminescence. Blood Rev. 1989 Jun;3(2):88–93. doi: 10.1016/0268-960x(89)90003-9. [DOI] [PubMed] [Google Scholar]
  19. Kaplan A. H., Weber D. J., Oddone E. Z., Perfect J. R. Infection due to Actinobacillus actinomycetemcomitans: 15 cases and review. Rev Infect Dis. 1989 Jan-Feb;11(1):46–63. doi: 10.1093/clinids/11.1.46. [DOI] [PubMed] [Google Scholar]
  20. Koga T., Senpuku H., Nakashima K., Ishihara Y., Nishihara T. Monoclonal antibody-coated latex agglutination assay for identification of Actinobacillus actinomycetemcomitans. Zentralbl Bakteriol. 1990 Oct;274(1):91–99. doi: 10.1016/s0934-8840(11)80978-3. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Miyasaki K. T. The neutrophil: mechanisms of controlling periodontal bacteria. J Periodontol. 1991 Dec;62(12):761–774. doi: 10.1902/jop.1991.62.12.761. [DOI] [PubMed] [Google Scholar]
  23. Miyasaki K. T., Wilson M. E., Genco R. J. Killing of Actinobacillus actinomycetemcomitans by the human neutrophil myeloperoxidase-hydrogen peroxide-chloride system. Infect Immun. 1986 Jul;53(1):161–165. doi: 10.1128/iai.53.1.161-165.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mundi H., Björkstén B., Svanborg C., Ohman L., Dahlgren C. Extracellular release of reactive oxygen species from human neutrophils upon interaction with Escherichia coli strains causing renal scarring. Infect Immun. 1991 Nov;59(11):4168–4172. doi: 10.1128/iai.59.11.4168-4172.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nakano Y., Inai Y., Yamashita Y., Nagaoka S., Kusuzaki-Nagira T., Nishihara T., Okahashi N., Koga T. Molecular and immunological characterization of a 64-kDa protein of Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol. 1995 Jun;10(3):151–159. doi: 10.1111/j.1399-302x.1995.tb00136.x. [DOI] [PubMed] [Google Scholar]
  26. Page R. C., Sims T. J., Engel L. D., Moncla B. J., Bainbridge B., Stray J., Darveau R. P. The immunodominant outer membrane antigen of Actinobacillus actinomycetemcomitans is located in the serotype-specific high-molecular-mass carbohydrate moiety of lipopolysaccharide. Infect Immun. 1991 Oct;59(10):3451–3462. doi: 10.1128/iai.59.10.3451-3462.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Saarela M., Asikainen S., Alaluusua S., Pyhälä L., Lai C. H., Jousimies-Somer H. Frequency and stability of mono- or poly-infection by Actinobacillus actinomycetemcomitans serotypes a, b, c, d or e. Oral Microbiol Immunol. 1992 Oct;7(5):277–279. doi: 10.1111/j.1399-302x.1992.tb00588.x. [DOI] [PubMed] [Google Scholar]
  28. Sanders L. A., Feldman R. G., Voorhorst-Ogink M. M., de Haas M., Rijkers G. T., Capel P. J., Zegers B. J., van de Winkel J. G. Human immunoglobulin G (IgG) Fc receptor IIA (CD32) polymorphism and IgG2-mediated bacterial phagocytosis by neutrophils. Infect Immun. 1995 Jan;63(1):73–81. doi: 10.1128/iai.63.1.73-81.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sato S., Takamatsu N., Okahashi N., Matsunoshita N., Inoue M., Takehara T., Koga T. Construction of mutants of Actinobacillus actinomycetemcomitans defective in serotype b-specific polysaccharide antigen by insertion of transposon Tn916. J Gen Microbiol. 1992 Jun;138(6):1203–1209. doi: 10.1099/00221287-138-6-1203. [DOI] [PubMed] [Google Scholar]
  30. Sims T. J., Moncla B. J., Darveau R. P., Page R. C. Antigens of Actinobacillus actinomycetemcomitans recognized by patients with juvenile periodontitis and periodontally normal subjects. Infect Immun. 1991 Mar;59(3):913–924. doi: 10.1128/iai.59.3.913-924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Takahashi T., Nishihara T., Ishihara Y., Amano K., Shibuya N., Moro I., Koga T. Murine macrophage interleukin-1 release by capsularlike serotype-specific polysaccharide antigens of Actinobacillus actinomycetemcomitans. Infect Immun. 1991 Jan;59(1):18–23. doi: 10.1128/iai.59.1.18-23.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Underwood K., Sjöström K., Darveau R., Lamont R., Schenkein H., Gunsolley J., Page R., Engel D. Serum antibody opsonic activity against Actinobacillus actinomycetemcomitans in human periodontal diseases. J Infect Dis. 1993 Dec;168(6):1436–1443. doi: 10.1093/infdis/168.6.1436. [DOI] [PubMed] [Google Scholar]
  33. Van Dyke T. E., Lester M. A., Shapira L. The role of the host response in periodontal disease progression: implications for future treatment strategies. J Periodontol. 1993 Aug;64(8 Suppl):792–806. doi: 10.1902/jop.1993.64.8s.792. [DOI] [PubMed] [Google Scholar]
  34. Wilson M. E., Bronson P. M., Hamilton R. G. Immunoglobulin G2 antibodies promote neutrophil killing of Actinobacillus actinomycetemcomitans. Infect Immun. 1995 Mar;63(3):1070–1075. doi: 10.1128/iai.63.3.1070-1075.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wilson M. E., Genco R. J. The role of antibody, complement and neutrophils in host defense against Actinobacillus actinomycetemcomitans. Immunol Invest. 1989 Jan-May;18(1-4):187–209. doi: 10.3109/08820138909112237. [DOI] [PubMed] [Google Scholar]
  36. Wilson M. E., Schifferle R. E. Evidence that the serotype b antigenic determinant of Actinobacillus actinomycetemcomitans Y4 resides in the polysaccharide moiety of lipopolysaccharide. Infect Immun. 1991 Apr;59(4):1544–1551. doi: 10.1128/iai.59.4.1544-1551.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zambon J. J. Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol. 1985 Jan;12(1):1–20. doi: 10.1111/j.1600-051x.1985.tb01348.x. [DOI] [PubMed] [Google Scholar]
  38. Zambon J. J., Slots J., Genco R. J. Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun. 1983 Jul;41(1):19–27. doi: 10.1128/iai.41.1.19-27.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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