1887

Abstract

Adhesion of to extracellular matrix proteins is mediated by antennae-like surface structures composed of EmaA oligomers. EmaA is an outer-membrane protein orthologous to the autotransporter YadA, a virulence determinant of . was present in the 27 strains examined, covering the six serotypes of . Ten individual genotypes and three different forms of the protein (full-length, intermediate and truncated) were predicted. The prototypic, full-length EmaA (202 kDa) was only associated with serotypes b and c, which displayed antennae-like surface structures. These strains bound to collagen embedded in a 3D matrix. The intermediate form of EmaA (173 kDa) was exclusively associated with serotypes d and a, which contained a 279 aa in-frame deletion, as well as a different N-terminal head domain sequence. These differences modified the appearance of the EmaA structures on the cell surface but maintained collagen-binding activity. Strains containing the truncated form of EmaA had single or multiple substitutions, deletions or insertions in the sequences, which resulted in the absence of EmaA molecules on the outer membrane and loss of collagen-binding activity. Population structure analyses of this organism, based on , indicated that serotypes b and c belonged to one subpopulation, which was independent of the other serotypes. The main divergence was found in the functional head domain. The conserved genotype within serotypes suggests a stable clonal linkage between this autotransporter protein and other virulence determinants.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/005892-0
2007-08-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2447.html?itemId=/content/journal/micro/10.1099/mic.0.2007/005892-0&mimeType=html&fmt=ahah

References

  1. Albandar, J. M., Muranga, M. B. & Rams, T. E. ( 2002; ). Prevalence of aggressive periodontitis in school attendees in Uganda. J Clin Periodontol 29, 823–831.[CrossRef]
    [Google Scholar]
  2. Asakawa, R., Komatsuzawa, H., Kawai, T., Yamada, S., Goncalves, R. B., Izumi, S., Fujiwara, T., Nakano, Y., Suzuki, N. & other authors ( 2003; ). Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50, 1125–1139.[CrossRef]
    [Google Scholar]
  3. Becker, J., Schuppan, D., Rabanus, J., Rauch, R., Niechoy, U. & Gelderblom, H. ( 1991; ). Immunoelectron microscopic localization of collagens type I, V, VI and of procollagen type III in human periodontal ligament and cementum. J Histochem Cytochem 39, 103–110.[CrossRef]
    [Google Scholar]
  4. Bornstein, P. & Traub, W. ( 1979; ). The chemistry and biology of collagen. In The Proteins, 3rd edn, vol. 4, pp. 411–632. Edited by H. Neurath & R. L. Orlando, FL: Hill Academic Press.
  5. Caroff, M. & Karibian, D. ( 2003; ). Structure of bacterial lipopolysaccharides. Carbohydr Res 338, 2431–2447.[CrossRef]
    [Google Scholar]
  6. Cotter, S. E., Surana, N. K., Grass, S. & St. Geme, J. W. ( 2006; ). Trimeric autotransporters require trimerization of the passenger domain for stability and adhesive activity. J Bacteriol 188, 5400–5407.[CrossRef]
    [Google Scholar]
  7. Dingemans, K. P., Teeling, P., Lagendijk, J. H. & Becker, A. E. ( 2000; ). Extracellular matrix of the human aortic media: an ultrastructural histochemical and immunohistochemical study of the adult aortic media. Anat Rec 258, 1–14.[CrossRef]
    [Google Scholar]
  8. Dixon, D. R. & Darveau, R. P. ( 2005; ). Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid A structure. J Dent Res 84, 584–595.[CrossRef]
    [Google Scholar]
  9. Dogan, B., Saarela, M., Jousimies-Somer, H., Alaluusua, S. & Asikainen, S. ( 1999; ). Actinobacillus actinomycetemcomitans serotype e – biotypes, genetic diversity and distribution in relation to periodontal status. Oral Microbiol Immunol 14, 98–103.[CrossRef]
    [Google Scholar]
  10. Edgar, R. C. ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.[CrossRef]
    [Google Scholar]
  11. Felsenstein, J. ( 2005; ). phylip (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
  12. Fine, D. H., Velliyagounder, K., Furgang, D. & Kaplan, J. ( 2005; ). The Actinobacillus actinomycetemcomitans autotransporter adhesin Aae exhibits specificity for buccal epithelial cells from humans and old world primates. Infect Immun 73, 1947–1953.[CrossRef]
    [Google Scholar]
  13. Haubek, D., Poulsen, K., Asikainen, S. & Kilian, M. ( 1995; ). Evidence for absence in northern Europe of especially virulent clonal types of Actinobacillus actinomycetemcomitans. J Clin Microbiol 33, 395–401.
    [Google Scholar]
  14. Haubek, D., Ennibi, O., Abdellaoui, L., Benzarti, N. & Poulsen, S. ( 2002; ). Attachment loss in Moroccan early onset periodontitis patients and infection with the JP2-type of Actinobacillus actinomycetemcomitans. J Clin Periodontol 29, 657–660.[CrossRef]
    [Google Scholar]
  15. Hillmann, G., Dogan, S. & Geurtsen, W. ( 1998; ). Histopathological investigation of gingival tissue from patients with rapidly progressive periodontitis. J Periodontol 69, 195–208.[CrossRef]
    [Google Scholar]
  16. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A. & Heesemann, J. ( 2000; ). Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19, 5989–5999.[CrossRef]
    [Google Scholar]
  17. Huelsenbeck, J. P. & Ronquist, F. ( 2001; ). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.[CrossRef]
    [Google Scholar]
  18. Inouye, T., Ohta, H., Kokeguchi, S., Fukui, K. & Kato, K. ( 1990; ). Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans. FEMS Microbiol Lett 57, 13–17.
    [Google Scholar]
  19. Jain, S., van Ulsen, P., Benz, I., Schmidt, M. A., Fernadez, R., Tommassen, J. & Goldberg, M. B. ( 2006; ). Polar localization of the autotransporter family of large bacterial virulence proteins. J Bacteriol 188, 4841–4850.[CrossRef]
    [Google Scholar]
  20. Kachlany, S. C., Planet, P. J., DeSalle, R., Fine, D. H. & Figurski, D. H. ( 2001; ). Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol 9, 429–437.[CrossRef]
    [Google Scholar]
  21. Kaplan, J. B., Perry, M. B., MacLean, L. L., Furgang, D., Wilson, M. E. & Fine, D. H. ( 2001; ). Structural and genetic analyses of O polysaccharide from Actinobacillus actinomycetemcomitans serotype f. Infect Immun 69, 5375–5384.[CrossRef]
    [Google Scholar]
  22. Kaplan, J. B., Schreiner, H. C., Furgang, D. & Fine, D. H. ( 2002; ). Population structure and genetic diversity of Actinobacillus actinomycetemcomitans strains isolated from localized juvenile periodontitis patients. J Clin Microbiol 40, 1181–1187.[CrossRef]
    [Google Scholar]
  23. Kolodrubetz, D., Dailey, T., Ebersole, J. & Kraig, E. ( 1989; ). Cloning and expression of the leukotoxin gene from Actinobacillus actinomycetemcomitans. Infect Immun 57, 1465–1469.
    [Google Scholar]
  24. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  25. Lally, E. T., Golub, E. E. & Kieba, I. R. ( 1994; ). Identification and immunological characterization of the domain of Actinobacillus actinomycetemcomitans leukotoxin that determines its specificity for human target cells. J Biol Chem 269, 31289–31295.
    [Google Scholar]
  26. Mintz, K. P. ( 2004; ). Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 150, 2677–2688.[CrossRef]
    [Google Scholar]
  27. Nakano, Y., Yoshida, Y., Yamashita, Y. & Koga, T. ( 1998; ). A gene cluster for 6-deoxy-l-talan synthesis in Actinobacillus actinomycetemcomitans. Biochim Biophys Acta 1442, 409–414.[CrossRef]
    [Google Scholar]
  28. Nakano, Y., Yoshida, Y., Suzuki, N., Yamashita, Y. & Koga, T. ( 2000; ). A gene cluster for the synthesis of serotype d-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans. Biochim Biophys Acta 1493, 259–263.[CrossRef]
    [Google Scholar]
  29. Nørskov-Lauritsen, N. & Kilian, M. ( 2006; ). Reclassification of Actinobacillus actinomycetemcomitans, Haemophilus aphrophilus, Haemophilus paraphrophilus and Haemophilus segnis as Aggregatibacter actinomycetemcomitans gen. nov., comb. nov., Aggregatibacter aphrophilus comb. nov. and Aggregatibacter segnis comb. nov., and emended description of Aggregatibacter aphrophilus to include V factor-dependent and V factor-independent isolates. Int J Syst Evol Microbiol 56, 2135–2146.[CrossRef]
    [Google Scholar]
  30. Notredame, C., Higgins, D. G. & Heringa, J. ( 2000; ). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302, 205–217.[CrossRef]
    [Google Scholar]
  31. Paju, S., Carlson, P., Jousimies-Somer, H. & Asikainen, S. ( 2000; ). Heterogeneity of Actinobacillus actinomycetemcomitans strains in various human infections and relationships between serotype, genotype, and antimicrobial susceptibility. J Clin Microbiol 38, 79–84.
    [Google Scholar]
  32. Paturel, L., Casalta, J. P., Habib, G., Nezri, M. & Raoult, D. ( 2004; ). Actinobacillus actinomycetemcomitans endocarditis. Clin Microbiol Infect 10, 98–118.[CrossRef]
    [Google Scholar]
  33. Poulsen, K., Theilade, E., Lally, E. T., Demuth, D. R. & Kilian, M. ( 1994; ). Population structure of Actinobacillus actinomycetemcomitans: a framework for studies of disease-associated properties. Microbiology 140, 2049–2060.[CrossRef]
    [Google Scholar]
  34. Pussinen, P. J., Nyyssonen, K., Alfthan, G., Salonen, R., Laukkanen, J. A. & Salonen, J. T. ( 2005; ). Serum antibody levels to Actinobacillus actinomycetemcomitans predict the risk for coronary heart disease. Arterioscler Thromb Vasc Biol 25, 833–838.[CrossRef]
    [Google Scholar]
  35. Roggenkamp, A., Ackermann, N., Jacobi, C., Truelzsch, K., Hoffmann, H. & Heesemann, J. ( 2003; ). Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185, 3735–3744.[CrossRef]
    [Google Scholar]
  36. Rose, J. E., Meyer, D. H. & Fives-Taylor, P. M. ( 2003; ). Aae, an autotransporter involved in adhesion of Actinobacillus actinomycetemcomitans to epithelial cells. Infect Immun 71, 2384–2393.[CrossRef]
    [Google Scholar]
  37. Ruiz, T., Lenox, C., Radermacher, M. & Mintz, K. P. ( 2006; ). Novel surface structures are associated with the adhesion of Actinobacillus actinomycetemcomitans to collagen. Infect Immun 74, 6163–6170.[CrossRef]
    [Google Scholar]
  38. Skurnik, M. & Wolf-Watz, H. ( 1989; ). Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol 3, 517–529.[CrossRef]
    [Google Scholar]
  39. Spahr, A., Klein, E., Khuseyinova, N., Boeckh, C., Muche, R., Kunze, M., Rothenbacher, D., Pezeshki, G., Hoffmeister, A. & Koenig, W. ( 2006; ). Periodontal infections and coronary heart disease: role of periodontal bacteria and importance of total pathogen burden in the Coronary Event and Periodontal Disease (CORODONT) study. Arch Intern Med 166, 554–559.[CrossRef]
    [Google Scholar]
  40. Spratt, B. G., Smith, N. H., Zhou, J., O'Rourke, M. & Feil, E. ( 1995; ). The population genetics of the pathogenic Neisseria. In Population Genetics of Bacteria, pp. 143–160. Edited by S. Baumberg, J. P. W. Young, E. M. H. Wellington & J. R. Saunders. Cambridge, UK: Press Syndicate of University of Cambridge.
  41. St Geme, J. W., III & Cutter, D. ( 2000; ). The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J Bacteriol 182, 6005–6013.[CrossRef]
    [Google Scholar]
  42. Suzuki, N., Nakano, Y., Yoshida, Y., Nakao, H. & Yamashita, Y. ( 2000; ). Genetic analysis of the gene cluster for the synthesis of serotype a-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans. Biochim Biophys Acta 1517, 135–138.[CrossRef]
    [Google Scholar]
  43. Teixeira, R. E., Mendes, E. N., Rogue de Carvalho, M. A., Nicoli, J. R., Farias Lde, M. & Magalhaes, P. P. ( 2006; ). Actinobacillus actinomycetemcomitans serotype-specific genotypes and periodontal status in Brazilian subjects. Can J Microbiol 52, 182–188.[CrossRef]
    [Google Scholar]
  44. Yang, H. W., Asikainen, S., Dogan, B., Suda, R. & Lai, C. H. ( 2004; ). Relationship of Actinobacillus actinomycetemcomitans serotype b to aggressive periodontitis: frequency in pure cultured isolates. J Periodontol 75, 592–599.[CrossRef]
    [Google Scholar]
  45. Yoshida, Y., Nakano, Y., Yamashita, Y. & Koga, T. ( 1998; ). Identification of a genetic locus essential for serotype b-specific antigen synthesis in Actinobacillus actinomycetemcomitans. Infect Immun 66, 107–114.
    [Google Scholar]
  46. Yoshida, Y., Nakano, Y., Suzuki, N., Nakao, H., Yamashita, Y. & Koga, T. ( 1999; ). Genetic analysis of the gene cluster responsible for synthesis of serotype e-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans. Biochim Biophys Acta 1489, 457–461.[CrossRef]
    [Google Scholar]
  47. Yoshida, Y., Suzuki, N., Nakano, Y., Shibuya, K., Ogawa, Y. & Koga, T. ( 2003; ). Distribution of Actinobacillus actinomycetemcomitans serotypes and Porphyromonas gingivalis in Japanese adults. Oral Microbiol Immunol 18, 135–139.[CrossRef]
    [Google Scholar]
  48. Zambon, J. J., Slots, J. & Genco, R. J. ( 1983; ). Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun 41, 19–27.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/005892-0
Loading
/content/journal/micro/10.1099/mic.0.2007/005892-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error