1887

Abstract

is enteropathogenic for man and rodents. Previous studies provided evidence that invades the lymphoid follicles of the Peyer’s patches (PP) of the small intestine. In this study -induced tissue alterations of the follicle-associated epithelium (FAE) and the underlying PP tissue were analysed by scanning (SEM) and transmission electron microscopy (TEM) as well as by conventional histological examination. For this purpose, an experimental mouse infection model including orogastric infections as well as ileal loop experiments were used. A rapid and selective colonisation of the FAE after orogastric yersinia infection was observed by SEM. TEM studies confirmed that adhered closely to the FAE including M cells and enterocytes. Histological studies and TEM revealed that selectively invaded the PP M cells but not other cells of the FAE. One day after infection the FAE as altered and small micro-abscesses comprising yersiniae expressing the major outer-membrane protein YadA were observed immediately beneath the FAE. Adjacent villi were dilated from lymphangiectasis and transmigrating polymorphonuclear leucocytes (PMNL) were found within the epithelium. At 5–7 days after infection the FAE and parts of PP were destroyed. Profound alterations of the cyto-architecture of the PP were due to the enormous recruitment of PMNL. By day 5 after infection, abscesses were found in the mesenteric lymph nodes. However, TEM studies revealed evidence that may disseminate from the PP not only the lymphatics but also by invasion of blood vessels. Taken together, the results of this study demonstrate that the FAE is the primary site of host-pathogen interaction in infection and that this pathogen penetrates M cells and subsequently induces destruction of the PP.

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1996-04-01
2024-04-19
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References

  1. Cover T. L., Aber R. C. Yersinia enterocolitica. N Engl J Med 1989; 321:16–24
    [Google Scholar]
  2. Hoogkamp-Korstanje J. A. A., de Koning J., Samsom J. R. Incidence of human infection with Yersinia enterocolitica serotypes O3, O8, and O9 and the use of indirect immunofluorescence in diagnosis. J Infect Dis 1986; 153:138–141
    [Google Scholar]
  3. Rabson A. R., Hallett A. F., Koornhof H. J. Generalized Yersinia enterocolitica infection. J Infect Dis 1975; 131:447–451
    [Google Scholar]
  4. Bouza E., Dominguez A., Meseguer M. Yersinia enterocolitica septicemia. Am J Clin Pathol 1980; 74:404–409
    [Google Scholar]
  5. Ahvonen P., Sievers K., Aho K. Arthritis associated with Yersinia enterocolitica infection. Acta Rheumatol Scand 1969; 15:232–253
    [Google Scholar]
  6. Granfors K., Viljanen M., Tiilikainen A., Toivanen A. Persistence of IgM, IgG, and IgA antibodies to Yersinia in yersinia arthritis. J Infect Dis 1980; 141:424–429
    [Google Scholar]
  7. Carter P. B. Animal model of human disease. Yersinia enteritis. Animal model: oral Yersinia enterocolitica infection of mice. Am J Pathol 1975; 81:703–706
    [Google Scholar]
  8. Heesemann J., Gaede K., Autenrieth I. B. Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis. APMIS 1993; 101:417–429
    [Google Scholar]
  9. Carter P. B. Pathogenicity of Yersińia enterocolitica for mice. Infect Immun 1975; 11:164–170
    [Google Scholar]
  10. Autenrieth I. B., Hantschmann P., Heymer B., Heesemann J. Immunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes. Immunobiology 1993; 187:1–16
    [Google Scholar]
  11. Beuscher H. U., Rausch, U-P., Ottemess I G., Rollinghoff M. Transition from interleukin 1 beta (IL-1 beta) to IL-1 alpha production during maturation of inflammatory macrophages in vivo. J Exp Med 1992; 175:1793–1797
    [Google Scholar]
  12. Pospischil A. [Structure and function of Peyer’s patches in the intestines of different animal species.]. Schweiz Arch Tierheilkd 1989; 131:595–603
    [Google Scholar]
  13. Bienenstock J., Befus A. D. Review: mucosal immunology. Immunology 1980; 41:249–270
    [Google Scholar]
  14. Autenrieth I. B., Tingle A., Reske-Kunz A., Heesemann J. T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect Immun 1992; 60:1140–1149
    [Google Scholar]
  15. Autenrieth I. B., Vogel U., Preger S., Heymer B., Heesemann J. Experimental Yersinia enterocolitica infection in euthymic and T-cell-deficient athymic nude C57BL/6 mice: comparison of time course, histomorphology, and immune response. Infect Immun 1993; 61:2585–2595
    [Google Scholar]
  16. Autenrieth I. B., Beer M., Bohn E., Kaufmann S. H. E., Heesemann J. Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun 1994; 62:2590–2599
    [Google Scholar]
  17. Hanski C., Kutschka U., Schmoranzer H. P. Immunohisto-chemical and electron microscopic study of interaction of Yersinia enterocolitica serotype O8 with intestinal mucosa during experimental enteritis. Infect Immun 1989; 57:673–678
    [Google Scholar]
  18. Grützkau A., Hanski C., Hahn H., Riecken E. O. Involvement of M cells in the bacterial invasion of Peyer’s patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 1990; 31:1011–1015
    [Google Scholar]
  19. Bye W. A., Allan C. H., Trier J. S. Structure, distribution, and origin of M cells in Peyer’s patches of mouse ileum. Gastroenterology 1984; 86:789–801
    [Google Scholar]
  20. Neutra M. R., Kraehenbuhl J.-P. Transepithelial transport and mucosal defence I: the role of M cells. Trends Cell Biol 1992; 2:134–138
    [Google Scholar]
  21. Giannasca P. J., Neutra M. R. Interactions of microorganisms with intestinal M cells: mucosal invasion and induction of secretory immunity. Infect Agents Dis 1994; 2:242–248
    [Google Scholar]
  22. Miller V. L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 1988; 56:1242–1248
    [Google Scholar]
  23. Miller V. L., Finlay B. B., Falkow S. Factors essential for the penetration of mammalian cells by Yersinia. Curr Top Microbiol Immunol 1988; 138:15–39
    [Google Scholar]
  24. Miller V. L. Tissue-culture invasion: fact or artefact?. Trends Microbiol 1995; 3:69–71
    [Google Scholar]
  25. Jones B. D., Ghori N., Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J Exp Med 1994; 180:15–23
    [Google Scholar]
  26. Kohbata S., Yokoyama H., Yabuuchi E. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer’s patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol 1986; 30:1225–1237
    [Google Scholar]
  27. Hsu H. S. Pathogenesis and immunity in murine salmonellosis. Microbiol Rev 1989; 53:390–409
    [Google Scholar]
  28. Finlay B. B. Molecular and cellular mechanisms of Salmonella pathogenesis. Curr Top Microbiol Immunol 1994; 192:163–185
    [Google Scholar]
  29. Sansonetti P. J. Molecular mechanisms of cell and tissue invasion by Shigella flexneri. Infect Agents Dis 1993; 2:201–206
    [Google Scholar]
  30. Perdomo J. J., Gounon P., Sansonetti P. J. Polymorphonuclear leukocytes transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J Clin Invest 1994; 93:633–643
    [Google Scholar]
  31. Heesemann J., Laufs R. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol 1983; 155:761–767
    [Google Scholar]
  32. Vogel U., Autenrieth I. B., Bemer R., Heesemann J. Role of plasmid-encoded antigens of Yersinia enterocolitica in humoral immunity against secondary Y. enterocolitica infection in mice. Microb Pathog 1993; 15:23–36
    [Google Scholar]
  33. Kamovsky M. J. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 1965; 27:137A (Abstract)
    [Google Scholar]
  34. Davis C. P., Savage D. C. Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect Immun 1974; 10:948–956
    [Google Scholar]
  35. Klaasen H. L. B. M., Koopman J. P., Poelma F. G. J., Beynen A. C. Intestinal, segmented, filamentous bacteria. FEMS Microbiol Rev 1992; 88:165–180
    [Google Scholar]
  36. Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 1974; 66:189–203
    [Google Scholar]
  37. Staats H. F., Jackson R. J., Marinaro M., Takahashi I., Kiyono H., McGhee J. R. Mucosal immunity to infection with implications for vaccine development. Curr Opin Immunol 1994; 6:572–583
    [Google Scholar]
  38. Kraehenbuhl J.-P., Neutra M. R. Transepithelial transport and mucosal defence II. secretion of IgA. Trends Cell Biol 1992; 2:170–174
    [Google Scholar]
  39. Neutra M. R., Phillips T. L., Mayer E. L., Fishkind D. J. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer’s patch. Cell Tissue Res 1987; 247:537–546
    [Google Scholar]
  40. Pappo J., Ermak T. H. Uptake and translocation of fluorescent latex particles by rabbit Peyer’s patches follicle epithelium: a quantitative model for M cell uptake. Clin Exp Immunol 1989; 76:144–148
    [Google Scholar]
  41. Savidge T. C., Smith M. W., James P. S., Aldred P. Salmonella-induced M-cell formation in germ-free mouse Peyer’s patch tissue. Am J Pathol 1991; 139:177–184
    [Google Scholar]
  42. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropino-cytosis of bacteria. Nature 1993; 364:639–642
    [Google Scholar]
  43. Rosqvist R., Magnusson, K-E., Wolf-Watz H. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 1994; 13:964–972
    [Google Scholar]
  44. Rosqvist R., Forsberg A., Wolf Watz H. Microinjection of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Biochem Soc Trans 1991; 19:1131–1132
    [Google Scholar]
  45. Klebanoff S. J. Phagocytic cells: products of oxygen metabolism. In Gallin J. I., Goldstein I. M., Snyderman R. (eds) Inflammation: basic principles and clinical correlates New York: Raven-Press Ltd; 1988391–444
    [Google Scholar]
  46. Henson P. M., Henson J. E., Fittschen C., Kimani G., Bratton D. L., Riches D. W. H. Phagocytic cells: degranulation and secretion. In Gallin J. I., Goldstein I. M., Snyderman R. (eds) Inflammation: basic principles and clinical correlates New York: Raven Press; 1988363–390
    [Google Scholar]
  47. Ewald J. H., Heesemann J., Rudiger H., Autenrieth I. B. Interaction of polymorphonuclear leukocytes with Yersinia enterocolitica-. role of the Yersinia virulence plasmid and modulation by the iron-chelator desferrioxamine B. J Infect Dis 1994; 170:140–150
    [Google Scholar]
  48. Stambach M. N., Bevan M. J. Cells infected with Yersinia present an epitope to class I MHC-restricted CTL. J Immunol 1994; 153:1603–1612
    [Google Scholar]
  49. Lian C.-J., Hwang W. S., Pai C. H. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect Immun 1987; 55:1176–1183
    [Google Scholar]
  50. Hessemann J., Gruter L. Genetic evidence that the outer membrane protein Yopl of Yersinia enterocolitica mediates adherence and phagocytosis resistance to human epithelial cells. FEMS Microbiol Lett 1987; 40:37–41
    [Google Scholar]
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