Dual-association of gnotobiotic IL-10-/- mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis

Inflamm Bowel Dis. 2007 Dec;13(12):1457-66. doi: 10.1002/ibd.20246.

Abstract

Background: Monoassociating gnotobiotic IL-10-deficient (-/-) mice with either nonpathogenic Enterococcus faecalis or a nonpathogenic Escherichia coli strain induces T-cell-mediated colitis with different kinetics and anatomical location (E. faecalis: late onset, distal colonic; E. coli: early onset, cecal).

Hypothesis: E. faecalis and E. coli act in an additive manner to induce more aggressive colitis than disease induced by each bacterial species independently.

Methods: Germ-free (GF) inbred 129S6/SvEv IL-10-/- and wildtype (WT) mice inoculated with nonpathogenic E. faecalis and/or E. coli were killed 3-7 weeks later. Colonic segments were scored histologically for inflammation (0 to 4) or incubated in media overnight to measure spontaneous IL-12/IL-23p40 secretion. Bacterial species were quantified by serial dilution and plated on culture media. Mesenteric lymph node (MLN) CD4(+) cells were stimulated with antigen-presenting cells pulsed with bacterial lysate (E. faecalis, E. coli, Bacteroides vulgatus) or KLH (unrelated antigen control). IFN-gamma and IL-17 levels were measured in the supernatants.

Results: Dual-associated IL-10-/- (but not WT) mice developed mild-to-moderate pancolitis by 3 weeks that progressed to severe distal colonic-predominant pancolitis with reactive atypia and duodenal inflammation by 7 weeks. NF-kappaB was activated in the duodenum and colon in dual-associated IL-10-/- x NF-kappaB(EGFP) mice. The aggressiveness of intestinal inflammation and the degree of antigen-specific CD4(+) cell activation were greater in dual- versus monoassociated IL-10-/- mice.

Conclusion: Two commensal bacteria that individually induce phenotypically distinct colitis in gnotobiotic IL-10-/- mice act additively to induce aggressive pancolitis and duodenal inflammation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • Colitis / immunology*
  • Colitis / microbiology*
  • Colon / chemistry
  • Colon / pathology
  • Colony Count, Microbial
  • Duodenitis / immunology
  • Duodenitis / microbiology
  • Enterococcus faecalis / growth & development*
  • Escherichia coli / growth & development*
  • Escherichia coli Infections / immunology*
  • Escherichia coli Infections / microbiology
  • Germ-Free Life
  • Gram-Positive Bacterial Infections / immunology*
  • Gram-Positive Bacterial Infections / microbiology
  • Interferon-gamma / analysis
  • Interleukin-10 / deficiency*
  • Interleukin-12 / genetics
  • Interleukin-23 / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / biosynthesis
  • Up-Regulation

Substances

  • Interleukin-23
  • NF-kappa B
  • Interleukin-10
  • Interleukin-12
  • Interferon-gamma