Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice

Infect Immun. 2005 Sep;73(9):5468-81. doi: 10.1128/IAI.73.9.5468-5481.2005.

Abstract

Infections with intestinal helminth and bacterial pathogens, such as enteropathogenic Escherichia coli, continue to be a major global health threat for children. To test the hypothesis that intestinal helminth infection may be a risk factor for enteric bacterial infection, a murine model was established by using the intestinal helminth Heligomosomoides polygyrus. To analyze the modulatory effect of a Th2-inducing helminth on the outcome of enteric bacterium Citrobacter rodentium infection, BALB/c and STAT 6 knockout (KO) mice were infected with H. polygyrus, C. rodentium, or both. We found that only BALB/c mice coinfected with H. polygyrus and C. rodentium displayed a marked morbidity and mortality. The enhanced susceptibility to C. rodentium and intestinal injury of coinfected BALB/c mice were shown to be associated with a significant increase in helminth-driven Th2 responses, mucosally and systemically, and correlated with a significant downregulation of protective gamma interferon and with a dramatic upregulation of the proinflammatory tumor necrosis factor alpha response. In addition, C. rodentium-associated colonic pathology in coinfected BALB/c mice was significantly enhanced, whereas bacterial burden was increased and clearance was delayed. In contrast, coinfection in STAT 6 KO mice failed to promote C. rodentium infection or to induce a more severe intestinal inflammation and tissue injury, demonstrating a mechanism by which helminth influences the development of host protective immunity and susceptibility to bacterial infections. We conclude that H. polygyrus coinfection can promote C. rodentium-associated disease and colitis through a STAT 6-mediated immune mechanism.

Publication types

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

MeSH terms

  • Animals
  • Citrobacter rodentium / immunology*
  • Colitis / immunology*
  • Colitis / microbiology
  • Colitis / parasitology
  • Colitis / pathology
  • Cytokines / metabolism
  • Enterobacteriaceae Infections / immunology*
  • Enterobacteriaceae Infections / microbiology
  • Enterobacteriaceae Infections / parasitology
  • Enterobacteriaceae Infections / pathology
  • Feces / microbiology
  • Female
  • Immunity, Mucosal / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Nematospiroides dubius / immunology*
  • STAT6 Transcription Factor
  • Strongylida Infections / immunology*
  • Strongylida Infections / mortality
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Trans-Activators / deficiency
  • Trans-Activators / genetics

Substances

  • Cytokines
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • Trans-Activators