Bifidobacterium animalis causes extensive duodenitis and mild colonic inflammation in monoassociated interleukin-10-deficient mice

Inflamm Bowel Dis. 2009 Jul;15(7):1022-31. doi: 10.1002/ibd.20900.

Abstract

Background: We recently showed that Bifidobacterium animalis is more prevalent within the colons of interleukin (IL)-10-deficient (-/-) mice than in wildtype (WT) animals colonized with the same specific pathogen-free (SPF) fecal contents. Here we tested the ability of this organism to cause T-cell-mediated intestinal inflammation by introducing it into germ-free (GF) IL-10-/- mice.

Methods: GF IL-10-/- or WT mice were monoassociated with Bifidobacterium animalis subsp. animalis ATCC (American Type Culture Collection, Manassas, VA) 25527(T) or with B. infantis ATCC 15697(T). Inflammation was measured by blinded histologic scores of the duodenum, cecum, and colon and by spontaneous secretion of IL-12/IL-23 p40 from colonic explants. Bacterial antigen-specific CD4(+) mesenteric lymph node (MLN) T-cell recall responses were measured in response to antigen-presenting cells (APC) pulsed with bacterial lysates.

Results: B. animalis caused marked duodenal inflammation and mild colitis in monoassociated IL-10-/- mice, whereas the intestinal tracts of WT animals remained free of inflammation. B. infantis colonization resulted in mild inflammation in the duodena of IL-10-/- mice. CD4(+) MLN T cells from B. animalis monoassociated IL-10-/- mice secreted high levels of IFN-gamma and IL-17 in response to B. animalis lysate. B. animalis equally colonized the different intestinal regions of WT and IL-10-/- mice.

Conclusions: B. animalis, a traditional probiotic species that is expanded in experimental colitis in this model, induces marked duodenal and mild colonic inflammation and TH1/TH17 immune responses when introduced alone into GF IL-10-/- mice. This suggests a potential pathogenic role for this commensal bacterial species in a susceptible host.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, Bacterial / immunology
  • Bifidobacteriales Infections / complications*
  • Bifidobacteriales Infections / immunology
  • Bifidobacteriales Infections / pathology
  • Bifidobacterium / immunology*
  • Colitis / immunology
  • Colitis / microbiology*
  • Colitis / pathology
  • Dendritic Cells / immunology
  • Dendritic Cells / microbiology
  • Dendritic Cells / pathology
  • Disease Models, Animal
  • Duodenitis / immunology
  • Duodenitis / microbiology*
  • Duodenitis / pathology
  • Epitopes / immunology
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology*
  • Interleukin-12 / immunology
  • Interleukin-23 / immunology
  • Mice
  • Mice, Inbred Strains
  • Mice, Mutant Strains
  • Severity of Illness Index
  • Th1 Cells / immunology
  • Th1 Cells / microbiology
  • Th1 Cells / pathology

Substances

  • Antigens, Bacterial
  • Epitopes
  • Interleukin-23
  • Interleukin-10
  • Interleukin-12