1887

Abstract

is a common cause of serious diarrhoeal disease in humans, in contrast to the avian population, where exposure results in prolonged colonization at high density without disease. Colonized poultry present a significant source of infection to humans worldwide. The aim of this work was to compare the interaction of with primary intestinal cells from humans and poultry to identify factors that account for the divergent outcome following exposure. A primary intestinal cell model of infection was developed using cells grown from human and chicken intestinal biopsies. The cultured cells were infected with a number of strains of . Invasion by and the influence of intestinal mucus on internalization were studied by fluorescence microscopy and gentamicin protection assays. invaded primary human intestinal cells in a microtubule-, microfilament- and caveolin-dependent manner. Entry of into primary chicken intestinal cells also occurred. Chicken mucus, but not intestinal mucus of human origin, significantly reduced infection of primary human intestinal cells. Avian mucus appears to inhibit from interacting with epithelial cell surfaces.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/000711-0
2007-02-01
2019-11-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/561.html?itemId=/content/journal/micro/10.1099/mic.0.2006/000711-0&mimeType=html&fmt=ahah

References

  1. Beery, J. T., Hugdahl, M. B. & Doyle, M. P. ( 1988; ). Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54, 2365–2370.
    [Google Scholar]
  2. Biswas, D., Itoh, K. & Sasakawa, C. ( 2000; ). Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol 29, 203–211.[CrossRef]
    [Google Scholar]
  3. Blaser, M. J. ( 1997; ). Epidemiologic and clinical features of Campylobacter jejuni infections. J Infect Dis 176, Suppl. 2, S103–S105.
    [Google Scholar]
  4. Bourlioux, P., Koletzko, B., Guarner, F. & Braesco, V. ( 2003; ). The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium “The Intelligent Intestine”, held in Paris, June 14, 2002. Am J Clin Nutr 78, 675–683.
    [Google Scholar]
  5. Byrne, C., Doherty, D., Mooney, A., Byrne, M., Woodward, D., Johnson, W., Rodgers, F. & Bourke, B. ( 2001; ). Basis of the superiority of cefoperazone amphotericin teicoplanin for isolating Campylobacter upsaliensis from stools. J Clin Microbiol 39, 2713–2716.[CrossRef]
    [Google Scholar]
  6. Clyne, M. & Drumm, B. ( 1993; ). Adherence of Helicobacter pylori to primary human gastrointestinal cells. Infect Immun 61, 4051–4057.
    [Google Scholar]
  7. Clyne, M. & Drumm, B. ( 1997; ). Adherence of Helicobacter pylori to the gastric mucosa. Can J Gastroenterol 11, 243–248.
    [Google Scholar]
  8. Clyne, M., Dillon, P., Daly, S., O'Kennedy, R., May, F. E., Westley, B. R. & Drumm, B. ( 2004; ). Helicobacter pylori interacts with the human single-domain trefoil protein TFF1. Proc Natl Acad Sci U S A 101, 7409–7414.[CrossRef]
    [Google Scholar]
  9. Cossart, P. & Sansonetti, P. J. ( 2004; ). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242–248.[CrossRef]
    [Google Scholar]
  10. Crushell, E., Harty, S., Sharif, F. & Bourke, B. ( 2004; ). Enteric campylobacter: purging its secrets? Pediatr Res 55, 3–12.[CrossRef]
    [Google Scholar]
  11. Denbow, D. ( 2000; ). Gastrointestinal anatomy and physiology. In Sturkie's Avian Physiology, 5th edn, pp. 299–324. Edited by G. Causey Whittow. San Diego: Academic Press.
  12. Falk, P. G., Hooper, L. V., Midtvedt, T. & Gordon, J. I. ( 1998; ). Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62, 1157–1170.
    [Google Scholar]
  13. Farthing, M. J. ( 2004; ). Bugs and the gut: an unstable marriage. Best Pract Res Clin Gastroenterol 18, 233–239.
    [Google Scholar]
  14. Frost, J. A. ( 2001; ). Current epidemiological issues in human campylobacteriosis. Symp Ser Soc Appl Microbiol 30, 85S–95S.
    [Google Scholar]
  15. Guarner, F. & Malagelada, J. R. ( 2003; ). Gut flora in health and disease. Lancet 361, 512–519.[CrossRef]
    [Google Scholar]
  16. Hanninen, M. L., Perko-Makela, P., Pitkala, A. & Rautelin, H. ( 2000; ). A three-year study of Campylobacter jejuni genotypes in humans with domestically acquired infections and in chicken samples from the Helsinki area. J Clin Microbiol 38, 1998–2000.
    [Google Scholar]
  17. Hannu, T., Mattila, L., Rautelin, H., Pelkonen, P., Lahdenne, P., Siitonen, A. & Leirisalo-Repo, M. ( 2002; ). Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology 41, 312–318.[CrossRef]
    [Google Scholar]
  18. Hashim, A., Clyne, M., Mulcahy, G., Akiyoshi, D., Chalmers, R. & Bourke, B. ( 2004; ). Host cell tropism underlies species restriction of human and bovine Cryptosporidium parvum genotypes. Infect Immun 72, 6125–6131.[CrossRef]
    [Google Scholar]
  19. Hendrixson, D. R. & DiRita, V. J. ( 2004; ). Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52, 471–484.[CrossRef]
    [Google Scholar]
  20. Hu, L. & Kopecko, D. J. ( 1999; ). Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect Immun 67, 4171–4182.
    [Google Scholar]
  21. Hugdahl, M. B., Beery, J. T. & Doyle, M. P. ( 1988; ). Chemotactic behavior of Campylobacter jejuni. Infect Immun 56, 1560–1566.
    [Google Scholar]
  22. Jacobs-Reitsma, W. ( 2000; ). Campylobacter in the food supply. In Campylobacter, 2nd edn, pp. 467–481. Edited by I. Nachamkin & M. J. Blaser. Washington, DC: American Society for Microbiology.
  23. Jones, M. A., Marston, K. L., Woodall, C. A., Maskell, D. J., Linton, D., Karlyshev, A. V., Dorrell, N., Wren, B. W. & Barrow, P. A. ( 2004; ). Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 72, 3769–3776.[CrossRef]
    [Google Scholar]
  24. Karlyshev, A. V., Everest, P., Linton, D., Cawthraw, S., Newell, D. G. & Wren, B. W. ( 2004; ). The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150, 1957–1964.[CrossRef]
    [Google Scholar]
  25. Konkel, M. E., Mead, D. J., Hayes, S. F. & Cieplak, W., Jr ( 1992; ). Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J Infect Dis 166, 308–315.[CrossRef]
    [Google Scholar]
  26. Kopecko, D. J., Hu, L. & Zaal, K. J. ( 2001; ). Campylobacter jejuni–microtubule-dependent invasion. Trends Microbiol 9, 389–396.[CrossRef]
    [Google Scholar]
  27. Madden, R. H., Moran, L. & Scates, P. ( 1998; ). Frequency of occurrence of Campylobacter spp. in red meats and poultry in Northern Ireland and their subsequent subtyping using polymerase chain reaction-restriction fragment length polymorphism and the random amplified polymorphic DNA method. J Appl Microbiol 84, 703–708.[CrossRef]
    [Google Scholar]
  28. McSweegan, E., Burr, D. H. & Walker, R. I. ( 1987; ). Intestinal mucus gel and secretory antibody are barriers to Campylobacter jejuni adherence to INT 407 cells. Infect Immun 55, 1431–1435.
    [Google Scholar]
  29. Meinersmann, R. J., Rigsby, W. E., Stern, N. J., Kelley, L. C., Hill, J. E. & Doyle, M. P. ( 1991; ). Comparative study of colonizing and noncolonizing Campylobacter jejuni. Am J Vet Res 52, 1518–1522.
    [Google Scholar]
  30. Monteville, M. R., Yoon, J. E. & Konkel, M. E. ( 2003; ). Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149, 153–165.[CrossRef]
    [Google Scholar]
  31. Mooney, A., Byrne, C., Clyne, M., Johnson-Henry, K., Sherman, P. & Bourke, B. ( 2003; ). Invasion of human epithelial cells by Campylobacter upsaliensis. Cell Microbiol 5, 835–847.[CrossRef]
    [Google Scholar]
  32. Moxley, R. A. ( 2004; ). Escherichia coli O157 : H7: an update on intestinal colonization and virulence mechanisms. Anim Health Res Rev 5, 15–33.[CrossRef]
    [Google Scholar]
  33. Nachamkin, I., Yang, X. H. & Stern, N. J. ( 1993; ). Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl Environ Microbiol 59, 1269–1273.
    [Google Scholar]
  34. Nadeau, E., Messier, S. & Quessy, S. ( 2003; ). Comparison of Campylobacter isolates from poultry and humans: association between in vitro virulence properties, biotypes, and pulsed-field gel electrophoresis clusters. Appl Environ Microbiol 69, 6316–6320.[CrossRef]
    [Google Scholar]
  35. Newell, D. G. & Wagenaar, J. A. ( 2000; ). Poultry infections and their control at the farm level. In Campylobacter, 2nd edn, pp. 497–510. Edited by I. Nachamkin & M. J. Blaser. Washington, DC: American Society for Microbiology.
  36. Oelschlaeger, T. A., Guerry, P. & Kopecko, D. J. ( 1993; ). Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc Natl Acad Sci U S A 90, 6884–6888.[CrossRef]
    [Google Scholar]
  37. Pageot, L. P., Perreault, N., Basora, N., Francoeur, C., Magny, P. & Beaulieu, J. F. ( 2000; ). Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microsc Res Tech 49, 394–406.[CrossRef]
    [Google Scholar]
  38. Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T. & other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  39. Pearson, A. D., Greenwood, M. H., Donaldson, J., Healing, T. D., Jones, D. M., Shahamat, M., Feltham, R. K. & Colwell, R. R. ( 2000; ). Continuous source outbreak of campylobacteriosis traced to chicken. J Food Prot 63, 309–314.
    [Google Scholar]
  40. Rabsch, W., Andrews, H. L., Kingsley, R. A., Prager, R., Tschape, H., Adams, L. G. & Baumler, A. J. ( 2002; ). Salmonella enterica serotype typhimurium and its host-adapted variants. Infect Immun 70, 2249–2255.[CrossRef]
    [Google Scholar]
  41. Reed, R. P., Friedland, I. R., Wegerhoff, F. O. & Khoosal, M. ( 1996; ). Campylobacter bacteremia in children. Pediatr Infect Dis J 15, 345–348.[CrossRef]
    [Google Scholar]
  42. Schwartz, D., Perry, R., Dombroski, D. M., Merrick, J. M. & Goldhar, J. ( 1996; ). Invasive ability of C. jejuni/coli isolates from children with diarrhea and the effect of iron-regulated proteins. Zentralbl Bakteriol 283, 485–491.[CrossRef]
    [Google Scholar]
  43. Skirrow, M. B. ( 1994; ). Diseases due to Campylobacter, Helicobacter and related bacteria. J Comp Pathol 111, 113–149.[CrossRef]
    [Google Scholar]
  44. Smirnov, A., Sklan, D. & Uni, Z. ( 2004; ). Mucin dynamics in the chick small intestine are altered by starvation. J Nutr 134, 736–742.
    [Google Scholar]
  45. Smith, C. K., Kaiser, P., Rothwell, L., Humphrey, T., Barrow, P. A. & Jones, M. A. ( 2005; ). Campylobacter jejuni-induced cytokine responses in avian cells. Infect Immun 73, 2094–2100.[CrossRef]
    [Google Scholar]
  46. Stern, N. J., Bailey, J. S., Blankenship, L. C., Cox, N. A. & McHan, F. ( 1988; ). Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Dis 32, 330–334.[CrossRef]
    [Google Scholar]
  47. Stern, N. J., Cox, N. A., Bailey, J. S., Berrang, M. E. & Musgrove, M. T. ( 2001; ). Comparison of mucosal competitive exclusion and competitive exclusion treatment to reduce Salmonella and Campylobacter spp. colonization in broiler chickens. Poult Sci 80, 156–160.[CrossRef]
    [Google Scholar]
  48. Szymanski, C. M., King, M., Haardt, M. & Armstrong, G. D. ( 1995; ). Campylobacter jejuni motility and invasion of Caco-2 cells. Infect Immun 63, 4295–4300.
    [Google Scholar]
  49. Takkinen, J., Ammon, A., Robstad, O. & Breuer, T. ( 2003; ). European survey on Campylobacter surveillance and diagnosis 2001. Euro Surveill 8, 207–213.
    [Google Scholar]
  50. Tay, S. T., Devi, S., Puthucheary, S. & Kautner, I. ( 1996; ). In vitro demonstration of the invasive ability of Campylobacters. Zentralbl Bakteriol 283, 306–313.[CrossRef]
    [Google Scholar]
  51. Verma, M., Madhu, M., Marrota, C., Lakshmi, C. V. & Davidson, E. A. ( 1994; ). Mucin coding sequences are remarkably conserved. Cancer Biochem Biophys 14, 41–51.
    [Google Scholar]
  52. Wolfgang, M. C., Jyot, J., Goodman, A. L., Ramphal, R. & Lory, S. ( 2004; ). Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc Natl Acad Sci U S A 101, 6664–6668.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/000711-0
Loading
/content/journal/micro/10.1099/mic.0.2006/000711-0
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