PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of iaiPermissionsJournals.ASM.orgJournalIAI ArticleJournal InfoAuthorsReviewers
 
Infect Immun. 1993 April; 61(4): 1239–1245.
PMCID: PMC281353

Requirements for invasion of epithelial cells by Actinobacillus actinomycetemcomitans.

Abstract

Actinobacillus actinomycetemcomitans, an oral bacterium implicated in human periodontal disease, was recently demonstrated to invade cultured epithelial cells (D. H. Meyer, P. K. Sreenivasan, and P. M. Fives-Taylor, Infect. Immun. 59:2719-2726, 1991). This report characterizes the requirements for invasion of KB cells by A. actinomycetemcomitans. The roles of bacterial and host factors were investigated by using selective agents that influence specific bacterial or host cell functions. Inhibition of bacterial protein synthesis decreased invasion, suggesting the absence of a preformed pool of proteins involved in A. actinomycetemcomitans invasion. Inhibition of bacterial and eukaryotic energy synthesis also decreased invasion, confirming that A. actinomycetemcomitans invasion is an active process. Bacterial adherence to KB cells was indicated by scanning electron microscopy of infected KB cells. Further, the addition of A. actinomycetemcomitans-specific serum to the bacterial inoculum reduced invasion substantially, suggesting a role for bacterial attachment in invasion. Many of the adherent bacteria invaded the epithelial cells under optimal conditions. Inhibitors of receptor-mediated endocytosis inhibited invasion by A. actinomycetemcomitans. Like that of many facultatively intracellular bacteria, A. actinomycetemcomitans invasion was not affected by eukaryotic endosomal acidification. These are the first published observations describing the requirements for epithelial cell invasion by a periodontopathogen. They demonstrate that A. actinomycetemcomitans utilizes a mechanism similar to those used by many but not all invasive bacteria to gain entry into eukaryotic cells.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.7M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Brennan MJ, Cisar JO, Vatter AE, Sandberg AL. Lectin-dependent attachment of Actinomyces naeslundii to receptors on epithelial cells. Infect Immun. 1984 Nov;46(2):459–464. [PMC free article] [PubMed]
  • Carrello A, Silburn KA, Budden JR, Chang BJ. Adhesion of clinical and environmental Aeromonas isolates to HEp-2 cells. J Med Microbiol. 1988 May;26(1):19–27. [PubMed]
  • Chen JC, Bavoil P, Clark VL. Enhancement of the invasive ability of Neisseria gonorrhoeae by contact with HecIB, an adenocarcinoma endometrial cell line. Mol Microbiol. 1991 Jun;5(6):1531–1538. [PubMed]
  • Christersson LA, Wikesjö UM, Albini B, Zambon JJ, Genco RJ. Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis. II. Correlation between immunofluorescence and culture techniques. J Periodontol. 1987 Aug;58(8):540–545. [PubMed]
  • Comstock LE, Thomas DD. Characterization of Borrelia burgdorferi invasion of cultured endothelial cells. Microb Pathog. 1991 Feb;10(2):137–148. [PubMed]
  • De Melo MA, Gabbiani G, Pechère JC. Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun. 1989 Jul;57(7):2214–2222. [PMC free article] [PubMed]
  • Detilleux PG, Deyoe BL, Cheville NF. Penetration and intracellular growth of Brucella abortus in nonphagocytic cells in vitro. Infect Immun. 1990 Jul;58(7):2320–2328. [PMC free article] [PubMed]
  • Donnenberg MS, Donohue-Rolfe A, Keusch GT. A comparison of HEp-2 cell invasion by enteropathogenic and enteroinvasive Escherichia coli. FEMS Microbiol Lett. 1990 May;57(1-2):83–86. [PubMed]
  • Elder BL, Boraker DK, Fives-Taylor PM. Whole-bacterial cell enzyme-linked immunosorbent assay for Streptococcus sanguis fimbrial antigens. J Clin Microbiol. 1982 Jul;16(1):141–144. [PMC free article] [PubMed]
  • Ewanowich CA, Melton AR, Weiss AA, Sherburne RK, Peppler MS. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. [PMC free article] [PubMed]
  • Ewanowich CA, Sherburne RK, Man SF, Peppler MS. Bordetella parapertussis invasion of HeLa 229 cells and human respiratory epithelial cells in primary culture. Infect Immun. 1989 Apr;57(4):1240–1247. [PMC free article] [PubMed]
  • Finlay BB. Cell adhesion and invasion mechanisms in microbial pathogenesis. Curr Opin Cell Biol. 1990 Oct;2(5):815–820. [PubMed]
  • Finlay BB, Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. [PMC free article] [PubMed]
  • Gaillard JL, 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. [PMC free article] [PubMed]
  • Hale TL, Bonventre PF. Shigella infection of Henle intestinal epithelial cells: role of the bacterium. Infect Immun. 1979 Jun;24(3):879–886. [PMC free article] [PubMed]
  • Hale TL, Morris RE, Bonventre PF. Shigella infection of henle intestinal epithelial cells: role of the host cell. Infect Immun. 1979 Jun;24(3):887–894. [PMC free article] [PubMed]
  • Hayes NS, Muse KE, Collier AM, Baseman JB. Parasitism by virulent Treponema pallidum of host cell surfaces. Infect Immun. 1977 Jul;17(1):174–186. [PMC free article] [PubMed]
  • Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. [PubMed]
  • Janda JM, Abbott SL, Oshiro LS. Penetration and replication of Edwardsiella spp. in HEp-2 cells. Infect Immun. 1991 Jan;59(1):154–161. [PMC free article] [PubMed]
  • Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem. 1986;55:663–700. [PubMed]
  • Meyer DH, Sreenivasan PK, Fives-Taylor PM. Evidence for invasion of a human oral cell line by Actinobacillus actinomycetemcomitans. Infect Immun. 1991 Aug;59(8):2719–2726. [PMC free article] [PubMed]
  • Miliotis MD, Koornhof HJ, Phillips JI. Invasive potential of noncytotoxic enteropathogenic Escherichia coli in an in vitro Henle 407 cell model. Infect Immun. 1989 Jul;57(7):1928–1935. [PMC free article] [PubMed]
  • Miller VL, Finlay BB, Falkow S. Factors essential for the penetration of mammalian cells by Yersinia. Curr Top Microbiol Immunol. 1988;138:15–39. [PubMed]
  • Moehring JM, Moehring TJ. The spectrum of virus resistance of a KB cell strain resistant to diphtheria toxin. Virology. 1976 Feb;69(2):786–788. [PubMed]
  • Moehring JM, Moehring TJ. Characterization of the diphtheria toxin-resistance system in Chinese hamster ovary cells. Somatic Cell Genet. 1979 Jul;5(4):453–468. [PubMed]
  • Moulder JW. Comparative biology of intracellular parasitism. Microbiol Rev. 1985 Sep;49(3):298–337. [PMC free article] [PubMed]
  • Nowotny A, Behling UH, Hammond B, Lai CH, Listgarten M, Pham PH, Sanavi F. Release of toxic microvesicles by Actinobacillus actinomycetemcomitans. Infect Immun. 1982 Jul;37(1):151–154. [PMC free article] [PubMed]
  • Oldham LJ, Rodgers FG. Adhesion, penetration and intracellular replication of Legionella pneumophila: an in vitro model of pathogenesis. J Gen Microbiol. 1985 Apr;131(4):697–706. [PubMed]
  • Pastan IH, Willingham MC. Receptor-mediated endocytosis of hormones in cultured cells. Annu Rev Physiol. 1981;43:239–250. [PubMed]
  • Robertson PB, Lantz M, Marucha PT, Kornman KS, Trummel CL, Holt SC. Collagenolytic activity associated with Bacteroides species and Actinobacillus actinomycetemcomitans. J Periodontal Res. 1982 May;17(3):275–283. [PubMed]
  • Slots J, Genco RJ. 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. [PubMed]
  • Small PL, Isberg RR, 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. [PMC free article] [PubMed]
  • St Geme JW, 3rd, Falkow S. Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect Immun. 1990 Dec;58(12):4036–4044. [PMC free article] [PubMed]
  • Weinberg A, Holt SC. Interaction of Treponema denticola TD-4, GM-1, and MS25 with human gingival fibroblasts. Infect Immun. 1990 Jun;58(6):1720–1729. [PMC free article] [PubMed]
  • Zambon JJ. Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol. 1985 Jan;12(1):1–20. [PubMed]

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