1887

Abstract

In a search for novel bioactive cell surface structures of periodontal pathogens, it was found that sera from two patients with -associated infections reacted strongly at 17 kDa on immunoblots of outer-membrane protein (OMP) preparations. The 17 kDa antigen was also recognized by anti-CsgA ( curli major subunit) antibody. The 17 kDa protein was identified as peptidoglycan-associated lipoprotein (PAL; AaPAL) by two-dimensional immunoblotting and subsequent sequence analysis by mass spectrometry and bioinformatics tools. AaPAL was an OMP and a lipoprotein, and it had an OmpA-like domain. In a group of middle-aged subjects (=26), serum reactivity to AaPAL was associated with the presence of periodontitis but not with the oral detection of . Both human sera and rabbit antisera against three different types of antigens, the gel-purified AaPAL, whole-cell antigens, and CsgA, recognized putative PALs of oral haemophili in addition to AaPAL. The results demonstrated that the novel AaPAL is a conserved bacterial lipoprotein. It is expressed and is strongly immunoreactive. The antigenic cross-reactivity found between AaPAL and oral haemophili may enhance local and systemic immuno-inflammatory reactions in periodontitis.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.46470-0
2006-07-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/55/7/931.html?itemId=/content/journal/jmm/10.1099/jmm.0.46470-0&mimeType=html&fmt=ahah

References

  1. Adu-Bobie, J., Lupetti, P., Brunelli, B., Granoff, D., Norais, N., Ferrari, G., Grandi, G., Rappuoli, R. & Pizza, M. ( 2004; ). GNA33 of Neisseria meningitidis is a lipoprotein required for cell separation, membrane architecture, and virulence. Infect Immun 72, 1914–1919.[CrossRef]
    [Google Scholar]
  2. Aliprantis, A. O., Yang, R. B., Mark, M. R., Suggett, S., Devaux, B., Radolf, J. D., Klimpel, G. R., Godowski, P. & Zychlinsky, A. ( 1999; ). Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 285, 736–739.[CrossRef]
    [Google Scholar]
  3. Armitage, G. C. ( 1999; ). Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4, 1–6.[CrossRef]
    [Google Scholar]
  4. Asakawa, R., Komatsuzawa, H., Kawai, T. & 12 other authors ( 2003; ). Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50, 1125–1139.[CrossRef]
    [Google Scholar]
  5. Asikainen, S. & Chen, C. ( 1999; ). Oral ecology and person-to-person transmission of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Periodontol 2000 20, 65–81.[CrossRef]
    [Google Scholar]
  6. Asikainen, S., Jousimies-Somer, H., Kanervo, A. & Saxen, L. ( 1990; ). The immediate efficacy of adjunctive doxycycline in treatment of localized juvenile periodontitis. Arch Oral Biol 35, 231S–234S.[CrossRef]
    [Google Scholar]
  7. Asikainen, S., Lai, C. H., Alaluusua, S. & Slots, J. ( 1991; ). Distribution of Actinobacillus actinomycetemcomitans serotypes in periodontal health and disease. Oral Microbiol Immunol 6, 115–118.[CrossRef]
    [Google Scholar]
  8. Bogdan, J. A., Jr & Apicella, M. A. ( 1995; ). Mapping of a surface-exposed, conformational epitope of the P6 protein of Haemophilus influenzae. Infect Immun 63, 4395–4401.
    [Google Scholar]
  9. Bolstad, A. I., Kristoffersen, T., Olsen, I., Preus, H. R., Jesen, H. B., Vasstrand, E. N. & Bakken, V. ( 1990; ). Outer membrane proteins of Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus studied by SDS-PAGE and immunoblotting. Oral Microbiol Immunol 5, 155–161.[CrossRef]
    [Google Scholar]
  10. Brightbill, H. D., Libraty, D. H., Krutzik, S. R. & 11 other authors ( 1999; ). Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732–736.[CrossRef]
    [Google Scholar]
  11. Burnens, A., Stucki, U., Nicolet, J. & Frey, J. ( 1995; ). Identification and characterization of an immunogenic outer membrane protein of Campylobacter jejuni. J Clin Microbiol 33, 2826–2832.
    [Google Scholar]
  12. Cascales, E. & Lloubes, R. ( 2004; ). Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51, 873–885.
    [Google Scholar]
  13. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J. C. & Lloubes, R. ( 2002; ). Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184, 754–759.[CrossRef]
    [Google Scholar]
  14. Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., Normark, S. & Hultgren, S. J. ( 2002; ). Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295, 851–855.[CrossRef]
    [Google Scholar]
  15. Clavel, T., Germon, P., Vianney, A., Portalier, R. & Lazzaroni, J. C. ( 1998; ). TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29, 359–367.[CrossRef]
    [Google Scholar]
  16. Collinson, S. K., Emody, L., Muller, K. H., Trust, T. J. & Kay, W. W. ( 1991; ). Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol 173, 4773–4781.
    [Google Scholar]
  17. D'Aiuto, F., Nibali, L., Parkar, M., Suvan, J. & Tonetti, M. S. ( 2005; ). Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res 84, 269–273.[CrossRef]
    [Google Scholar]
  18. Deich, R. A., Metcalf, B. J., Finn, C. W., Farley, J. E. & Green, B. A. ( 1988; ). Cloning of genes encoding a 15,000-dalton `peptidoglycan-associated outer membrane lipoprotein and an antigenically related 15,000-dalton protein from Haemophilus influenzae. J Bacteriol 170, 489–498.
    [Google Scholar]
  19. Ebersole, J. L., Steffen, M. J. & Cappelli, D. ( 1999; ). Longitudinal human serum antibody responses to outer membrane antigens of Actinobacillus actinomycetemcomitans. J Clin Periodontol 26, 732–741.[CrossRef]
    [Google Scholar]
  20. Epstein, S. E. ( 2002; ). The multiple mechanisms by which infection may contribute to atherosclerosis development and course. Circ Res 90, 2–4.
    [Google Scholar]
  21. Evans, D. G., Evans, D. J., Jr & Tjoa, W. ( 1977; ). Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun 18, 330–337.
    [Google Scholar]
  22. Fadl, A. A., Sha, J., Klimpel, G. R., Olano, J. P., Niesel, D. W. & Chopra, A. K. ( 2005; ). Murein lipoprotein is a critical outer membrane component involved in Salmonella enterica serovar Typhimurium systemic infection. Infect Immun 73, 1081–1096.[CrossRef]
    [Google Scholar]
  23. Fisette, P. L., Ram, S., Andersen, J. M., Guo, W. & Ingalls, R. R. ( 2003; ). The Lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF-κB activation in epithelial cells in a Toll-like receptor 2-dependent manner. J Biol Chem 278, 46252–46260.[CrossRef]
    [Google Scholar]
  24. Fives-Taylor, P. M., Meyer, D. H., Mintz, K. P. & Brissette, C. ( 1999; ). Virulence factors of Actinobacillus actinomycetemcomitans. Periodontol 2000 20, 136–167.[CrossRef]
    [Google Scholar]
  25. Fortney, K. R., Young, R. S., Bauer, M. E., Katz, B. P., Hood, A. F., Munson, R. S., Jr & Spinola, S. M. ( 2000; ). Expression of peptidoglycan-associated lipoprotein is required for virulence in the human model of Haemophilus ducreyi infection. Infect Immun 68, 6441–6448.[CrossRef]
    [Google Scholar]
  26. Fredriksson, M. I., Figueredo, C. M., Gustafsson, A., Bergstrom, K. G. & Asman, B. E. ( 1999; ). Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol 70, 1355–1360.[CrossRef]
    [Google Scholar]
  27. Frey, J., Kuhnert, P., Villiger, L. & Nicolet, J. ( 1996; ). Cloning and characterization of an Actinobacillus pleuropneumoniae outer membrane protein belonging to the family of PAL lipoproteins. Res Microbiol 147, 351–361.[CrossRef]
    [Google Scholar]
  28. Hammar, M., Arnqvist, A., Bian, Z., Olsen, A. & Normark, S. ( 1995; ). Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18, 661–670.[CrossRef]
    [Google Scholar]
  29. Hammar, M., Bian, Z. & Normark, S. ( 1996; ). Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci U S A 93, 6562–6566.[CrossRef]
    [Google Scholar]
  30. Hasebe, A., Yoshimura, A., Into, T. & 10 other authors ( 2004; ). Biological activities of Bacteroides forsythus lipoproteins and their possible pathological roles in periodontal disease. Infect Immun 72, 1318–1325.[CrossRef]
    [Google Scholar]
  31. Hellman, J., Roberts, J. D., Jr, Tehan, M. M., Allaire, J. E. & Warren, H. S. ( 2002; ). Bacterial peptidoglycan-associated lipoprotein is released into the bloodstream in Gram-negative sepsis and causes inflammation and death in mice. J Biol Chem 277, 14274–14280.[CrossRef]
    [Google Scholar]
  32. Hirschfeld, M., Kirschning, C. J., Schwandner, R., Wesche, H., Weis, J. H., Wooten, R. M. & Weis, J. J. ( 1999; ). Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 163, 2382–2386.
    [Google Scholar]
  33. 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]
  34. Komatsuzawa, H., Asakawa, R., Kawai, T., Ochiai, K., Fujiwara, T., Taubman, M. A., Ohara, M., Kurihara, H. & Sugai, M. ( 2002; ). Identification of six major outer membrane proteins from Actinobacillus actinomycetemcomitans. Gene 288, 195–201.[CrossRef]
    [Google Scholar]
  35. Lazzaroni, J. C. & Portalier, R. ( 1992; ). The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol Microbiol 6, 735–742.[CrossRef]
    [Google Scholar]
  36. Llamas, M. A., Rodriguez-Herva, J. J., Hancock, R. E., Bitter, W., Tommassen, J. & Ramos, J. L. ( 2003; ). Role of Pseudomonas putida tol-oprL gene products in uptake of solutes through the cytoplasmic membrane. J Bacteriol 185, 4707–4716.[CrossRef]
    [Google Scholar]
  37. Lloubes, R., Cascales, E., Walburger, A., Bouveret, E., Lazdunski, C., Bernadac, A. & Journet, L. ( 2001; ). The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152, 523–529.[CrossRef]
    [Google Scholar]
  38. Loos, B. G., Craandijk, J., Hoek, F. J., Wertheim-van Dillen, P. M. & van der Velden, U. ( 2000; ). Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 71, 1528–1534.[CrossRef]
    [Google Scholar]
  39. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. ( 1951; ). Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265–275.
    [Google Scholar]
  40. Mattila, K., Vesanen, M., Valtonen, V., Nieminen, M., Palosuo, T., Rasi, V. & Asikainen, S. ( 2002; ). Effect of treating periodontitis on C-reactive protein levels: a pilot study. BMC Infect Dis 2, 30.[CrossRef]
    [Google Scholar]
  41. Moore, W. E. & Moore, L. V. ( 1994; ). The bacteria of periodontal diseases. Periodontol 2000 5, 66–77.[CrossRef]
    [Google Scholar]
  42. Neu, H. C. & Heppel, L. A. ( 1965; ). The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J Biol Chem 240, 3685–3692.
    [Google Scholar]
  43. Olsén, A., Arnqvist, A., Hammar, M. & Normark, S. ( 1993; ). Environmental regulation of curli production in Escherichia coli. Infect Agents Dis 2, 272–274.
    [Google Scholar]
  44. Paju, S., Carlson, P., Jousimies-Somer, H. & Asikainen, S. ( 2003; ). Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus in systemic and nonoral infections in Finland. APMIS 111, 653–657.[CrossRef]
    [Google Scholar]
  45. Paturel, L., Casalta, J. P., Habib, G., Nezri, M. & Raoult, D. ( 2004; ). Actinobacillus actinomycetemcomitans endocarditis. Clin Microbiol Infect 10, 98–118.[CrossRef]
    [Google Scholar]
  46. Pussinen, P. J., Vilkuna-Rautiainen, T., Alfthan, G., Mattila, K. & Asikainen, S. ( 2002; ). Multiserotype enzyme-linked immunosorbent assay as a diagnostic aid for periodontitis in large-scale studies. J Clin Microbiol 40, 512–518.[CrossRef]
    [Google Scholar]
  47. Pussinen, P. J., Jauhiainen, M., Vilkuna-Rautiainen, T., Sundvall, J., Vesanen, M., Mattila, K., Palosuo, T., Alfthan, G. & Asikainen, S. ( 2004; ). Periodontitis decreases the antiatherogenic potency of high density lipoprotein. J Lipid Res 45, 139–147.
    [Google Scholar]
  48. Rolhion, N., Barnich, N., Claret, L. & Darfeuille-Michaud, A. ( 2005; ). Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 187, 2286–2296.[CrossRef]
    [Google Scholar]
  49. Romling, U., Bian, Z., Hammar, M., Sierralta, W. D. & Normark, S. ( 1998; ). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180, 722–731.
    [Google Scholar]
  50. Saarela, M., Asikainen, S., Alaluusua, S., Pyhala, L., Lai, C. H. & Jousimies-Somer, H. ( 1992; ). Frequency and stability of mono- or poly-infection by Actinobacillus actinomycetemcomitans serotypes a, b, c, d or e. Oral Microbiol Immunol 7, 277–279.[CrossRef]
    [Google Scholar]
  51. Sha, J., Fadl, A. A., Klimpel, G. R., Niesel, D. W., Popov, V. L. & Chopra, A. K. ( 2004; ). The two murein lipoproteins of Salmonella enterica serovar Typhimurium contribute to the virulence of the organism. Infect Immun 72, 3987–4003.[CrossRef]
    [Google Scholar]
  52. Slots, J. & Ting, M. ( 1999; ). Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol 2000 20, 82–121.[CrossRef]
    [Google Scholar]
  53. Spinola, S. M., Hiltke, T. J., Fortney, K. & Shanks, K. L. ( 1996; ). The conserved 18,000-molecular-weight outer membrane protein of Haemophilus ducreyi has homology to PAL. Infect Immun 64, 1950–1955.
    [Google Scholar]
  54. Terada, M., Kuroda, T., Matsuyama, S. I. & Tokuda, H. ( 2001; ). Lipoprotein sorting signals evaluated as the LolA-dependent release of lipoproteins from the cytoplasmic membrane of Escherichia coli. J Biol Chem 276, 47690–47694.[CrossRef]
    [Google Scholar]
  55. Von Troil-Linden, B., Torkko, H., Alaluusua, S., Wolf, J., Jousimies-Somer, H. & Asikainen, S. ( 1995; ). Periodontal findings in spouses. A clinical, radiographic and microbiological study. J Clin Periodontol 22, 93–99.
    [Google Scholar]
  56. Walburger, A., Lazdunski, C. & Corda, Y. ( 2002; ). The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol Microbiol 44, 695–708.[CrossRef]
    [Google Scholar]
  57. Wang, Y. & Chen, C. ( 2005; ). Mutation analysis of the flp operon in Actinobacillus actinomycetemcomitans. Gene 351, 61–71.[CrossRef]
    [Google Scholar]
  58. Wang, Y., Shi, W., Chen, W. & Chen, C. ( 2003; ). Type IV pilus gene homologs pilABCD are required for natural transformation in Actinobacillus actinomycetemcomitans. Gene 312, 249–255.[CrossRef]
    [Google Scholar]
  59. Wilson, M. E. ( 1991a; ). IgG antibody response of localized juvenile periodontitis patients to the 29 kiloDalton outer membrane protein of Actinobacillus actinomycetemcomitans. J Periodontol 62, 211–218.[CrossRef]
    [Google Scholar]
  60. Wilson, M. E. ( 1991b; ). The heat-modifiable outer membrane protein of Actinobacillus actinomycetemcomitans: relationship to OmpA proteins. Infect Immun 59, 2505–2507.
    [Google Scholar]
  61. Wilson, M. E. & Hamilton, R. G. ( 1995; ). Immunoglobulin G subclass response of juvenile periodontitis subjects to principal outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect Immun 63, 1062–1069.
    [Google Scholar]
  62. Zambon, J. J. ( 1985; ). Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 12, 1–20.[CrossRef]
    [Google Scholar]
  63. Zambon, J. J., DeLuca, C., Slots, J. & Genco, R. J. ( 1983; ). Studies of leukotoxin from Actinobacillus actinomycetemcomitans using the promyelocytic HL-60 cell line. Infect Immun 40, 205–212.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.46470-0
Loading
/content/journal/jmm/10.1099/jmm.0.46470-0
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