Localized delivery of interferon-β by Lactobacillus exacerbates experimental colitis

PLoS One. 2011 Feb 18;6(2):e16967. doi: 10.1371/journal.pone.0016967.

Abstract

Background: There have been conflicting reports of the role of Type I interferons (IFN) in inflammatory bowel disease (IBD). Clinical trials have shown potent efficacy of systemic interferon-beta (IFN-β) in inducing remission of ulcerative colitis. Likewise, IFNAR1(-/-) mice display an increased sensitivity to dextran sulfate sodium (DSS)-induced colitis, suggesting Type I IFN play a protective role during inflammation of the gut. Curiously, however, there have also been reports detailing the spontaneous development of IBD in patients receiving systemic IFN-β therapy for multiple sclerosis or hepatitis.

Methodology/principal findings: To investigate the effects of local administration of IFN-β on a murine model of colitis, we developed a transgenic Lactobacillus acidophilus strain that constitutively expresses IFN-β (La-IFN-β). While pretreatment of mice with control Lactobacillus (La-EV) provided slight protective benefits, La-IFN-β increased sensitivity to DSS. Analysis showed colitic mice pretreated with La-IFN-β had increased production of TNF-α, IFN-γ, IL-17A and IL-13 by intestinal tissues and decreased regulatory T cells (Tregs) in their small intestine. Examination of CD103(+) dendritic cells (DCs) in the Peyer's patches revealed that IFNAR1 expression was dramatically reduced by La-IFN-β. Similarly, bone marrow-derived DCs matured with La-IFN-β experienced a 3-fold reduction of IFNAR1 and were impaired in their ability to induce Tregs.

Conclusions/significance: Our IFNAR1 expression data identifies a correlation between the loss/downregulation of IFNAR1 on DCs and exacerbation of colitis. Our data show that Lactobacillus secreting IFN-β has an immunological effect that in our model results in the exacerbation of colitis. This study underscores that the selection of therapeutics delivered by a bacterial vehicle must take into consideration the simultaneous effects of the vehicle itself.

Publication types

  • Evaluation Study
  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Cells, Cultured
  • Colitis / chemically induced
  • Colitis / genetics*
  • Colitis / microbiology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Dextran Sulfate
  • Disease Models, Animal
  • Disease Progression
  • Gene Transfer Techniques*
  • Genetic Predisposition to Disease
  • Genetic Vectors
  • Interferon Type I / adverse effects*
  • Interferon Type I / genetics*
  • Interferon Type I / metabolism
  • Lactobacillus acidophilus / genetics*
  • Lactobacillus acidophilus / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Organisms, Genetically Modified
  • Receptor, Interferon alpha-beta / genetics
  • Recombinant Proteins

Substances

  • Interferon Type I
  • Recombinant Proteins
  • Receptor, Interferon alpha-beta
  • Dextran Sulfate