1887

Abstract

Surface-layer proteins (SLPs) have been detected in all strains and play a role in adhesion, although an involvement in the inflammatory process may also be supposed, as they cover the bacterial surface and are immunodominant antigens. The aim of this study was to evaluate the immunomodulatory properties of SLPs obtained from hypervirulent and epidemic (H/E) or non-H/E strains, to try to determine whether they contribute to hypervirulence. SLPs were purified from H/E PCR ribotype 027 and 001 and non-H/E PCR ribotype 012 strains, and the ability to modulate these properties was studied in human models of monocytes and monocyte-derived dendritic cells (MDDCs). The results indicated that SLPs were able to induce immunomodulatory cytokines [interleukin (IL)-1β, IL-6 and IL-10] in monocytes. SLPs induced maturation of MDDCs, which acquired enhanced antigen-presenting activity, a crucial function of the mature stage. SLP-primed MDDCs expressed high levels of IL-10, an important regulatory cytokine. No significant differences were found in the activation induced in monocytes and MDDCs by SLP preparations from H/E and non-H/E strains. Overall, these findings show an important role for SLPs in modulation of the immune response to . However, SLPs from H/E strains did not show a specific immunomodulatory pattern compared with SLPs from non-H/E strains, suggesting that SLPs are not involved in the increased severity of infection peculiar to H/E strains.

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2011-08-01
2020-01-26
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References

  1. Acosta-Rodriguez E. V. , Napolitani G. , Lanzavecchia A. , Sallusto F. . ( 2007; ). Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. . Nat Immunol 8:, 942–949. [CrossRef].[PubMed]
    [Google Scholar]
  2. Ausiello C. M. , Fedele G. , Urbani F. , Lande R. , Di Carlo B. , Cassone A. . ( 2002; ). Native and genetically inactivated pertussis toxins induce human dendritic cell maturation and synergize with lipopolysaccharide in promoting T helper type 1 responses. . J Infect Dis 186:, 351–360. [CrossRef].[PubMed]
    [Google Scholar]
  3. Ausiello C. M. , Cerquetti M. , Fedele G. , Spensieri F. , Palazzo R. , Nasso M. , Frezza S. , Mastrantonio P. . ( 2006; ). Surface layer proteins from Clostridium difficile induce inflammatory and regulatory cytokines in human monocytes and dendritic cells. . Microbes Infect 8:, 2640–2646. [CrossRef].[PubMed]
    [Google Scholar]
  4. Barbut F. , Mastrantonio P. , Delmée M. , Brazier J. , Kuijper E. , Poxton I. . on behalf of the European Study Group on Clostridium difficile (ESGCD) ( 2007; ). Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. . Clin Microbiol Infect 13:, 1048–1057. [CrossRef].[PubMed]
    [Google Scholar]
  5. Calabi E. , Ward S. , Wren B. , Paxton T. , Panico M. , Morris H. , Dell A. , Dougan G. , Fairweather N. . ( 2001; ). Molecular characterization of the surface layer proteins from Clostridium difficile . . Mol Microbiol 40:, 1187–1199. [CrossRef].[PubMed]
    [Google Scholar]
  6. Calabi E. , Calabi F. , Phillips A. D. , Fairweather N. F. . ( 2002; ). Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. . Infect Immun 70:, 5770–5778. [CrossRef].[PubMed]
    [Google Scholar]
  7. Cerquetti M. , Molinari A. , Sebastianelli A. , Diociaiuti M. , Petruzzelli R. , Capo C. , Mastrantonio P. . ( 2000; ). Characterization of surface layer proteins from different Clostridium difficile clinical isolates. . Microb Pathog 28:, 363–372. [CrossRef].[PubMed]
    [Google Scholar]
  8. Eidhin D. N. , Ryan A. W. , Doyle R. M. , Walsh J. B. , Kelleher D. . ( 2006; ). Sequence and phylogenetic analysis of the gene for surface layer protein, slpA, from 14 PCR ribotypes of Clostridium difficile . . J Med Microbiol 55:, 69–83. [CrossRef].[PubMed]
    [Google Scholar]
  9. Fedele G. , Stefanelli P. , Spensieri F. , Fazio C. , Mastrantonio P. , Ausiello C. M. . ( 2005; ). Bordetella pertussis-infected human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization and interleukin-23 expression. . Infect Immun 73:, 1590–1597. [CrossRef].[PubMed]
    [Google Scholar]
  10. Hennequin C. , Porcheray F. , Waligora-Dupriet A. , Collignon A. , Barc M. , Bourlioux P. , Karjalainen T. . ( 2001; ). GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. . Microbiology 147:, 87–96.[PubMed]
    [Google Scholar]
  11. Hookman P. , Barkin J. S. . ( 2009; ). Clostridium difficile associated infection, diarrhea and colitis. . World J Gastroenterol 15:, 1554–1580. [CrossRef].[PubMed]
    [Google Scholar]
  12. Karjalainen T. , Waligora-Dupriet A. J. , Cerquetti M. , Spigaglia P. , Maggioni A. , Mauri P. , Mastrantonio P. . ( 2001; ). Molecular and genomic analysis of genes encoding surface-anchored proteins from Clostridium difficile . . Infect Immun 69:, 3442–3446. [CrossRef].[PubMed]
    [Google Scholar]
  13. Kato H. , Yokoyama T. , Arakawa Y. . ( 2005; ). Typing by sequencing the slpA gene of Clostridium difficile strains causing multiple outbreaks in Japan. . J Med Microbiol 54:, 167–171. [CrossRef].[PubMed]
    [Google Scholar]
  14. Killgore G. , Thompson A. , Johnson S. , Brazier J. , Kuijper E. , Pepin J. , Frost E. H. , Savelkoul P. , Nicholson B. et al. ( 2008; ). Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing. . J Clin Microbiol 46:, 431–437. [CrossRef].[PubMed]
    [Google Scholar]
  15. Koboziev I. , Karlsson F. , Grisham M. B. . ( 2010; ). Gut-associated lymphoid tissue, T cell trafficking, and chronic intestinal inflammation. . Ann N Y Acad Sci 1207: Suppl. 1 E86–E93. [CrossRef].[PubMed]
    [Google Scholar]
  16. Kyne L. , Warny M. , Qamar A. , Kelly C. P. . ( 2001; ). Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. . Lancet 357:, 189–193. [CrossRef].[PubMed]
    [Google Scholar]
  17. Lanzavecchia A. , Sallusto F. . ( 2001; ). Regulation of T cell immunity by dendritic cells. . Cell 106:, 263–266. [CrossRef].[PubMed]
    [Google Scholar]
  18. Moore K. W. , de Waal Malefyt R. , Coffman R. L. , O’Garra A. . ( 2001; ). Interleukin-10 and the interleukin-10 receptor. . Annu Rev Immunol 19:, 683–765. [CrossRef].[PubMed]
    [Google Scholar]
  19. Mukherjee K. , Karlsson S. , Burman L. G. , Akerlund T. . ( 2002; ). Proteins released during high toxin production in Clostridium difficile . . Microbiology 148:, 2245–2253.[PubMed]
    [Google Scholar]
  20. O’Brien J. B. , McCabe M. S. , Athié-Morales V. , McDonald G. S. , Ní Eidhin D. B. , Kelleher D. P. . ( 2005; ). Passive immunisation of hamsters against Clostridium difficile infection using antibodies to surface layer proteins. . FEMS Microbiol Lett 246:, 199–205. [CrossRef].[PubMed]
    [Google Scholar]
  21. Pépin J. , Valiquette L. , Alary M. E. , Villemure P. , Pelletier A. , Forget K. , Pépin K. , Chouinard D. . ( 2004; ). Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. . CMAJ 171:, 466–472.[PubMed] [CrossRef]
    [Google Scholar]
  22. Rescigno M. . ( 2002; ). Dendritic cells and the complexity of microbial infection. . Trends Microbiol 10:, 425–431. [CrossRef].[PubMed]
    [Google Scholar]
  23. Serbina N. V. , Jia T. , Hohl T. M. , Pamer E. G. . ( 2008; ). Monocyte-mediated defense against microbial pathogens. . Annu Rev Immunol 26:, 421–452. [CrossRef].[PubMed]
    [Google Scholar]
  24. Sozzani S. , Allavena P. , Vecchi A. , Mantovani A. . ( 2000; ). Chemokines and dendritic cell traffic. . J Clin Immunol 20:, 151–160. [CrossRef].[PubMed]
    [Google Scholar]
  25. Spigaglia P. , Barbanti F. , Mastrantonio P. . ( 2011; ). Surface layer protein A variant of Clostridium difficile PCR-ribotype 027. . Emerg Infect Dis 17:, 317–319.[PubMed] [CrossRef]
    [Google Scholar]
  26. Steinman R. M. , Hemmi H. . ( 2006; ). Dendritic cells: translating innate to adaptive immunity. . Curr Top Microbiol Immunol 311:, 17–58. [CrossRef].[PubMed]
    [Google Scholar]
  27. Tasteyre A. , Barc M. C. , Collignon A. , Boureau H. , Karjalainen T. . ( 2001; ). Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. . Infect Immun 69:, 7937–7940. [CrossRef].[PubMed]
    [Google Scholar]
  28. Taylor P. R. , Martinez-Pomares L. , Stacey M. , Lin H. H. , Brown G. D. , Gordon S. . ( 2005; ). Macrophage receptors and immune recognition. . Annu Rev Immunol 23:, 901–944. [CrossRef].[PubMed]
    [Google Scholar]
  29. Trinchieri G. . ( 2003; ). Interleukin-12 and the regulation of innate resistance and adaptive immunity. . Nat Rev Immunol 3:, 133–146. [CrossRef].[PubMed]
    [Google Scholar]
  30. Waligora A. J. , Hennequin C. , Mullany P. , Bourlioux P. , Collignon A. , Karjalainen T. . ( 2001; ). Characterization of a cell surface protein of Clostridium difficile with adhesive properties. . Infect Immun 69:, 2144–2153. [CrossRef].[PubMed]
    [Google Scholar]
  31. Wüst J. , Sullivan N. M. , Hardegger U. , Wilkins T. D. . ( 1982; ). Investigation of an outbreak of antibiotic-associated colitis by various typing methods. . J Clin Microbiol 16:, 1096–1101.[PubMed]
    [Google Scholar]
  32. Yona S. , Jung S. . ( 2010; ). Monocytes: subsets, origins, fates and functions. . Curr Opin Hematol 17:, 53–59. [CrossRef].[PubMed]
    [Google Scholar]
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