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.

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2007-08-01
2020-08-08
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References

  1. Albandar J. M., Muranga M. B., Rams T. E.. 2002; Prevalence of aggressive periodontitis in school attendees in Uganda. J Clin Periodontol29:823–831
    [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 Microbiol50:1125–1139
    [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 Cytochem39:103–110
    [Google Scholar]
  4. Bornstein P., Traub W.. 1979; The chemistry and biology of collagen. In The Proteins , 3rd edn.vol 4 pp411–632 Edited by Neurath H., L R.. Orlando, FL: Hill Academic Press;
    [Google Scholar]
  5. Caroff M., Karibian D.. 2003; Structure of bacterial lipopolysaccharides. Carbohydr Res338:2431–2447
    [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 Bacteriol188:5400–5407
    [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 Rec258:1–14
    [Google Scholar]
  8. Dixon D. R., Darveau R. P.. 2005; Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid A structure. J Dent Res84:584–595
    [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 Immunol14:98–103
    [Google Scholar]
  10. Edgar R. C.. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32:1792–1797
    [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:
    [Google Scholar]
  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 Immun73:1947–1953
    [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 Microbiol33:395–401
    [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 Periodontol29:657–660
    [Google Scholar]
  15. Hillmann G., Dogan S., Geurtsen W.. 1998; Histopathological investigation of gingival tissue from patients with rapidly progressive periodontitis. J Periodontol69:195–208
    [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 J19:5989–5999
    [Google Scholar]
  17. Huelsenbeck J. P., Ronquist F.. 2001; MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics17:754–755
    [Google Scholar]
  18. Inouye T., Ohta H., Kokeguchi S., Fukui K., Kato K.. 1990; Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans . FEMS Microbiol Lett57:13–17
    [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 Bacteriol188:4841–4850
    [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 Microbiol9:429–437
    [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 Immun69:5375–5384
    [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 Microbiol40:1181–1187
    [Google Scholar]
  23. Kolodrubetz D., Dailey T., Ebersole J., Kraig E.. 1989; Cloning and expression of the leukotoxin gene from Actinobacillus actinomycetemcomitans . Infect Immun57:1465–1469
    [Google Scholar]
  24. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685
    [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 Chem269:31289–31295
    [Google Scholar]
  26. Mintz K. P.. 2004; Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology150:2677–2688
    [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 Acta1442:409–414
    [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 Acta1493:259–263
    [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 Microbiol56:2135–2146
    [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 Biol302:205–217
    [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 Microbiol38:79–84
    [Google Scholar]
  32. Paturel L., Casalta J. P., Habib G., Nezri M., Raoult D.. 2004; Actinobacillus actinomycetemcomitans endocarditis. Clin Microbiol Infect10:98–118
    [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. Microbiology140:2049–2060
    [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 Biol25:833–838
    [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 Bacteriol185:3735–3744
    [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 Immun71:2384–2393
    [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 Immun74:6163–6170
    [Google Scholar]
  38. Skurnik M., Wolf-Watz H.. 1989; Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol3:517–529
    [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 Med166:554–559
    [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 pp143–160 Edited by Baumberg S., Young J. P. W., Wellington E. M. H., Saunders J. R. Cambridge, UK: Press Syndicate of University of Cambridge;
    [Google Scholar]
  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 Bacteriol182:6005–6013
    [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;1517135–138
    [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 Microbiol52:182–188
    [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 Periodontol75:592–599
    [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 Immun66:107–114
    [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
    [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 Immunol18:135–139
    [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 Immun41:19–27
    [Google Scholar]
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