Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1991 Aug;59(8):2719–2726. doi: 10.1128/iai.59.8.2719-2726.1991

Evidence for invasion of a human oral cell line by Actinobacillus actinomycetemcomitans.

D H Meyer 1, P K Sreenivasan 1, P M Fives-Taylor 1
PMCID: PMC258078  PMID: 1855989

Abstract

Actinobacillus actinomycetemcomitans, an oral bacterial species associated with periodontal disease, was found to invade human cell lines. Invasion was demonstrated by recovery of viable organisms from gentamicin-treated KB cell monolayers and by light and electron microscopy. Internalization occurred through a cytochalasin D-sensitive process. Invasion efficiencies of some A. actinomycetemcomitans strains were comparable to those of invasive members of the family Enterobacteriaceae. Differences in invasiveness were correlated with bacterial colonial morphology. Smooth variants invaded more proficiently than rough variants. A. actinomycetemcomitans can undergo a smooth-to-rough colonial morphology shift which results in the loss of invasiveness. Coordinated regulation of genes involved in the rough-to-smooth phenotypic transitions may play a role in the episodic nature of periodontal disease.

Full text

PDF
2719

Images in this article

2722Image
on p.2722
2723Image
on p.2723

Selected References

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

  1. Detilleux P. G., Deyoe B. L., Cheville N. F. Penetration and intracellular growth of Brucella abortus in nonphagocytic cells in vitro. Infect Immun. 1990 Jul;58(7):2320–2328. doi: 10.1128/iai.58.7.2320-2328.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ewanowich C. A., Melton A. R., Weiss A. A., Sherburne R. K., Peppler M. S. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. doi: 10.1128/iai.57.9.2698-2704.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ewanowich C. A., Sherburne R. K., Man S. F., Peppler M. S. Bordetella parapertussis invasion of HeLa 229 cells and human respiratory epithelial cells in primary culture. Infect Immun. 1989 Apr;57(4):1240–1247. doi: 10.1128/iai.57.4.1240-1247.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Finlay B. B., Falkow S. Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie. 1988 Aug;70(8):1089–1099. doi: 10.1016/0300-9084(88)90271-4. [DOI] [PubMed] [Google Scholar]
  5. Frank R. M. Bacterial penetration in the apical pocket wall of advanced human periodontitis. J Periodontal Res. 1980 Nov;15(6):563–573. doi: 10.1111/j.1600-0765.1980.tb00315.x. [DOI] [PubMed] [Google Scholar]
  6. Gahring L. C., Heffron F., Finlay B. B., Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun. 1990 Feb;58(2):443–448. doi: 10.1128/iai.58.2.443-448.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Genco R. J., Slots J. Host responses in periodontal diseases. J Dent Res. 1984 Mar;63(3):441–451. doi: 10.1177/00220345840630031601. [DOI] [PubMed] [Google Scholar]
  9. Giannella R. A., Washington O., Gemski P., Formal S. B. Invasion of HeLa cells by Salmonella typhimurium: a model for study of invasiveness of Salmonella. J Infect Dis. 1973 Jul;128(1):69–75. doi: 10.1093/infdis/128.1.69. [DOI] [PubMed] [Google Scholar]
  10. Haffajee A. D., Socransky S. S., Dzink J. L., Taubman M. A., Ebersole J. L., Smith D. J. Clinical, microbiological and immunological features of subjects with destructive periodontal diseases. J Clin Periodontol. 1988 Apr;15(4):240–246. doi: 10.1111/j.1600-051x.1988.tb01577.x. [DOI] [PubMed] [Google Scholar]
  11. Holt S. C., Ebersole J., Felton J., Brunsvold M., Kornman K. S. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science. 1988 Jan 1;239(4835):55–57. doi: 10.1126/science.3336774. [DOI] [PubMed] [Google Scholar]
  12. Labrec E. H., Schneider H., Magnani T. J., Formal S. B. EPITHELIAL CELL PENETRATION AS AN ESSENTIAL STEP IN THE PATHOGENESIS OF BACILLARY DYSENTERY. J Bacteriol. 1964 Nov;88(5):1503–1518. doi: 10.1128/jb.88.5.1503-1518.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Moore W. E., Holdeman L. V., Cato E. P., Smibert R. M., Burmeister J. A., Palcanis K. G., Ranney R. R. Comparative bacteriology of juvenile periodontitis. Infect Immun. 1985 May;48(2):507–519. doi: 10.1128/iai.48.2.507-519.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Moulder J. W. Comparative biology of intracellular parasitism. Microbiol Rev. 1985 Sep;49(3):298–337. doi: 10.1128/mr.49.3.298-337.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Rosan B., Slots J., Lamont R. J., Listgarten M. A., Nelson G. M. Actinobacillus actinomycetemcomitans fimbriae. Oral Microbiol Immunol. 1988 Jun;3(2):58–63. doi: 10.1111/j.1399-302x.1988.tb00082.x. [DOI] [PubMed] [Google Scholar]
  16. Saglie R., Elbaz J. J. Bacterial penetration into the gingival tissue in periodontal disease. J West Soc Periodontol Periodontal Abstr. 1983;31(3):85–93. [PubMed] [Google Scholar]
  17. Scannapieco F. A., Millar S. J., Reynolds H. S., Zambon J. J., Levine M. J. Effect of anaerobiosis on the surface ultrastructure and surface proteins of Actinobacillus actinomycetemcomitans (Haemophilus actinomycetemcomitans). Infect Immun. 1987 Sep;55(9):2320–2323. doi: 10.1128/iai.55.9.2320-2323.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Slots J. Bacterial specificity in adult periodontitis. A summary of recent work. J Clin Periodontol. 1986 Nov;13(10):912–917. doi: 10.1111/j.1600-051x.1986.tb01426.x. [DOI] [PubMed] [Google Scholar]
  19. Slots J., Genco R. J. Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction. J Dent Res. 1984 Mar;63(3):412–421. doi: 10.1177/00220345840630031101. [DOI] [PubMed] [Google Scholar]
  20. Slots J. Salient Biochemical Characters of Actinobacillus actinomycetemcomitans. Arch Microbiol. 1982 Feb;131(1):60–67. doi: 10.1007/BF00451500. [DOI] [PubMed] [Google Scholar]
  21. Small P. L., Isberg R. R., Falkow S. Comparison of the ability of enteroinvasive Escherichia coli, Salmonella typhimurium, Yersinia pseudotuberculosis, and Yersinia enterocolitica to enter and replicate within HEp-2 cells. Infect Immun. 1987 Jul;55(7):1674–1679. doi: 10.1128/iai.55.7.1674-1679.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Socransky S. S. Microbiology of periodontal disease -- present status and future considerations. J Periodontol. 1977 Sep;48(9):497–504. doi: 10.1902/jop.1977.48.9.497. [DOI] [PubMed] [Google Scholar]
  23. Suzuki J. B. Diagnosis and classification of the periodontal diseases. Dent Clin North Am. 1988 Apr;32(2):195–216. [PubMed] [Google Scholar]
  24. Tanner A. C., Haffer C., Bratthall G. T., Visconti R. A., Socransky S. S. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol. 1979 Oct;6(5):278–307. doi: 10.1111/j.1600-051x.1979.tb01931.x. [DOI] [PubMed] [Google Scholar]
  25. Turner J. G., Drew A. H. An Experimental Inquiry into the Bacteriology of Pyorrhoea. Proc R Soc Med. 1919;12(ODONTOL):104–118. [PMC free article] [PubMed] [Google Scholar]
  26. YOUNG C. W., ROBINSON P. F., SACKTOR B. INHIBITION OF THE SYNTHESIS OF PROTEIN IN INTACT ANIMALS BY ACETOXYCYCLOHEXIMIDE AND A METABOLIC DERANGEMENT CONCOMITANT WITH THIS BLOCKADE. Biochem Pharmacol. 1963 Aug;12:855–865. doi: 10.1016/0006-2952(63)90116-3. [DOI] [PubMed] [Google Scholar]
  27. Zambon J. J., Christersson L. A., Genco R. J. Diagnosis and treatment of localized juvenile periodontitis. J Am Dent Assoc. 1986 Aug;113(2):295–299. doi: 10.14219/jada.archive.1986.0152. [DOI] [PubMed] [Google Scholar]
  28. van Winkelhoff A. J., van Steenbergen T. J., de Graaff J. The role of black-pigmented Bacteroides in human oral infections. J Clin Periodontol. 1988 Mar;15(3):145–155. doi: 10.1111/j.1600-051x.1988.tb01561.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES