Prevention of experimental colitis by parenteral administration of a pathogen-derived immunomodulatory molecule

Gut. 2007 Mar;56(3):351-7. doi: 10.1136/gut.2006.099861. Epub 2006 Sep 4.

Abstract

Background: Filamentous haemagglutinin (FHA) of Bordetella pertussis subverts host immune responses by inhibiting interleukin (IL)12 and enhancing IL10 production by macrophages and dendritic cells, and promoting the induction of regulatory T cells.

Hypothesis: Injection of FHA would ameliorate disease in a T cell-dependent model of colitis via the induction of anti-inflammatory cytokines and regulatory T cells.

Methods: Colitis was induced by injection of CD4CD45RB(high) naive T cells into severe combined immunodeficient (SCID) mice. Mice were treated with four subcutaneous injections of FHA or buffer alone.

Results: Parenteral injection of FHA stimulated IL10 and/or transforming growth factor beta production in local and mesenteric lymph nodes and Peyer's patches of mice 2-6 h after administration. Compared with phosphate-buffered saline-treated mice, FHA-treated SCID mice had significantly (p<0.01) less weight loss, lower colon weight, less colon shrinkage and reduced inflammatory lesions. The therapeutic effect of FHA was associated with enhanced IL10 and reduced type 1 and type 2 T helper cytokine production by spleen cells. Finally, FHA also attenuated the symptoms of colitis in SCID mice transferred with CD4CD45RB(high) T cells from IL10-deficient mice.

Conclusions: Our finding shows that FHA suppresses type 1 T helper and pro-inflammatory cytokines, and ameliorates disease activity in a chronic T cell-dependent model of colitis, an effect that was not dependent on IL10 production by T cells, but was associated with induction of anti-inflammatory cytokines in vivo. Having already been used as a pertussis vaccine component in children, FHA is a promising candidate for clinical testing in patients with Crohn's disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / therapeutic use*
  • Animals
  • Bordetella pertussis / immunology
  • Colitis / immunology
  • Colitis / pathology
  • Colitis / prevention & control*
  • Cytokines / biosynthesis
  • Disease Models, Animal
  • Interleukin-10 / biosynthesis
  • Leukocyte Common Antigens / analysis
  • Lymph Nodes / immunology
  • Lymphocyte Transfusion
  • Mice
  • Mice, Inbred BALB C
  • Mice, SCID
  • Peyer's Patches / immunology
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1
  • Th1 Cells / immunology
  • Th2 Cells / immunology
  • Transforming Growth Factor beta / biosynthesis
  • Virulence Factors, Bordetella / therapeutic use*

Substances

  • Adhesins, Bacterial
  • Cytokines
  • Transforming Growth Factor beta
  • Virulence Factors, Bordetella
  • filamentous hemagglutinin adhesin, Bordetella pertussis
  • Interleukin-10
  • Leukocyte Common Antigens
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1