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Host Response and Inflammation

Citrobacter rodentium Infection in Mice Elicits a Mucosal Th1 Cytokine Response and Lesions Similar to Those in Murine Inflammatory Bowel Disease

Lisa M. Higgins, Gad Frankel, Gill Douce, Gordon Dougan, Thomas T. MacDonald
Lisa M. Higgins
Department of Paediatric Gastroenterology, St. Bartholomew’s and the Royal London School of Medicine and Dentistry, St. Bartholomew’s Hospital, London EC1A 7BE, and
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Gad Frankel
Department of Biochemistry, Imperial College of Science, Technology and Medicine, London SW7 2AZ, United Kingdom
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Gill Douce
Department of Biochemistry, Imperial College of Science, Technology and Medicine, London SW7 2AZ, United Kingdom
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Gordon Dougan
Department of Biochemistry, Imperial College of Science, Technology and Medicine, London SW7 2AZ, United Kingdom
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Thomas T. MacDonald
Department of Paediatric Gastroenterology, St. Bartholomew’s and the Royal London School of Medicine and Dentistry, St. Bartholomew’s Hospital, London EC1A 7BE, and
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DOI: 10.1128/IAI.67.6.3031-3039.1999
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    Fig. 1.

    Swiss NIH mice infected with wild-type C. rodentium showed severe colonic hyperplasia compared to mice infected with an intimin mutant strain. Crypt lengths were measured on days 2, 6, and 12 postinfection. Mean crypt lengths in the colons of mice infected with wild-type C. rodentium (open bars) were significantly greater than those of mice infected with the control mutant strain (closed bars). Error bars represent standard errors. Each group contained five mice. ∗, P < 0.05).

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    Fig. 2.

    Bacteria were visualized on the epithelial surface (a) and in the mucosa and submucosa (b) of C. rodentium-infected Swiss NIH mice. The clear area between the muscularis mucosa and the external muscle layer is the submucosa, which becomes edematous duringCitrobacter infection. The arrows indicate bacteria. Immunoperoxidase immunohistochemistry was performed with anti-intimin antibody. Magnification, ×400.

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    Fig. 3.

    Mean cell counts for peroxidase-containing cells in the mucosa and submucosa (A) and for CD3+ (B), CD4+(C), and CD8+ (D) cells infiltrating the lamina propria of Swiss NIH mice were determined on days 2, 6, and 12 postinfection. In addition to the massive increase in numbers of CD3+ and CD4+ cells in the mucosa of C. rodentium-infected mice, there was also a slight increase in numbers of these cells in control mice. This probably reflected the increase which is seen in normal mice around this time (21). Closed bars represent mice infected with an intimin mutant strain; open bars represent mice infected with wild-type C. rodentium. Error bars indicate standard errors. Each group contained five mice. ∗, P < 0.05).

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    Fig. 4.

    Immunoperoxidase immunohistochemistry of colon tissue of infected Swiss NIH mice. (a and b) CD4+ cells in mice infected with an intimin mutant strain (a) or wild-type C. rodentium (b). In colon tissues of control mice, only a few CD4+ cells are visible in the lamina propria (arrows). InCitrobacter-infected mice, there is a massive accumulation of CD4+ cells at the crypt bases and in the lamina propria (arrows). (c and d) MHC class II-positive cells in the lamina propria of intimin-mutant-infected mice (c) and wild-type-C. rodentium-infected mice (d). In control mice, MHC class II-positive cells can be seen in the lamina propria, and the surface epithelium is also positive (arrows). InCitrobacter-infected mice, every surface and crypt epithelial cell is strongly class II positive, as are all cells in the lamina propria. Serial sections stained with control antibodies showed only a few cells expressing endogenous peroxidase in the mucosa, although these cells were more abundant in the submucosa (see Fig. 3A). Original magnification, ×100.

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    Fig. 5.

    Quantitation of intraepithelial cells. Counts are expressed as the number of positive intraepithelial lymphocytes per 100 epithelial cells. Each group contained five Swiss NIH mice. Closed bars represent mice infected with the intimin mutant strain; open bars represent mice infected with wild-type C. rodentium. Values are means ± standard errors. (A) CD3+ cells; (B) CD4+ cells; (C) CD8+ cells. ∗, P < 0.05.

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    Fig. 6.

    Cytokine and KGF mRNA transcripts in distal colonic tissue as measured by RT-PCR on days 6 and 12 postinfection. Closed bars represent mice infected with the intimin mutant strain; open bars represent mice infected with wild-type C. rodentium. Each group contained five Swiss NIH mice. Values are means ± standard errors. (A) IL-1; (B) TNF-α; (C) IL-12; (D) IFN-γ; (E) IL-4; (F) KGF. ∗, P < 0.05.

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    Fig. 7.

    (A) Cell counts on day 12 postinfection of C3H mice with wild-type intimin-β-expressing C. rodentium (open bars), intimin-α-expressing DBS255(pCVD438) (hatched bars), and intimin mutant (closed bars) strains. (B) Crypt lengths (day 12) in the colons of wild-type-C. rodentium-infected mice (open bars) or mice infected with C. rodentium expressing human intimin α were significantly greater than those of mice infected with the control mutant strain (closed bars). Each group contained five mice. Values are means ± standard errors. ∗, P < 0.05.

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  • Table 1.

    Bacterial strains used in this study

    StrainDescriptionIntimin derivative expressed
    C. rodentium biotype 4280Wild-type C. rodentiumβ
    DBS255C. rodentium eae mutantNone
    E2348/69Wild-type EPEC (O127ab:H6)α
    DBS255(pCVD438)DBS255 complemented with eae from E2348/69α
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Citrobacter rodentium Infection in Mice Elicits a Mucosal Th1 Cytokine Response and Lesions Similar to Those in Murine Inflammatory Bowel Disease
Lisa M. Higgins, Gad Frankel, Gill Douce, Gordon Dougan, Thomas T. MacDonald
Infection and Immunity Jun 1999, 67 (6) 3031-3039; DOI: 10.1128/IAI.67.6.3031-3039.1999

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Citrobacter rodentium Infection in Mice Elicits a Mucosal Th1 Cytokine Response and Lesions Similar to Those in Murine Inflammatory Bowel Disease
Lisa M. Higgins, Gad Frankel, Gill Douce, Gordon Dougan, Thomas T. MacDonald
Infection and Immunity Jun 1999, 67 (6) 3031-3039; DOI: 10.1128/IAI.67.6.3031-3039.1999
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KEYWORDS

Adhesins, Bacterial
Carrier Proteins
Citrobacter
cytokines
Enterobacteriaceae Infections
Escherichia coli Proteins
Fibroblast Growth Factors
Inflammatory Bowel Diseases
Th1 Cells

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