IDO expressing dendritic cells suppress allograft rejection of small bowel transplantation in mice by expansion of Foxp3+ regulatory T cells

Transpl Immunol. 2015 Oct;33(2):69-77. doi: 10.1016/j.trim.2015.05.003. Epub 2015 May 20.

Abstract

Background: Indoleamine 2,3-dioxygenase (IDO), the enzyme that catalyzes the first and rate-limiting step of tryptophan catabolism, suppresses T-cell responses by tryptophan depletion and accumulation of kynurenine metabolites. IDO prevents allograft rejection in various transplantations.

Methods: Dendritic cells (DC) highly expressing IDO (IDO(+) DC) were cultured through transduction of adenovirus vectors carrying the IDO sequence. IDO(+) DC were incubated with CD4(+) CD25(-) T cells to detect T cell proliferation. The effects of IDO(+) DC and 3-Hydroxyanthranilic acid (3-HAA) were verified in an allogeneic murine small bowel transplantation (SBT) model. Foxp3(+) Treg cells of recipient mice were detected by flow cytometry and cytokines in plasma were determined by ELISA.

Results: IDO(+) DC effectively suppressed proliferation of CD4(+) CD25(-) T cells in vitro, and this effect could be enhanced by adding 3-HAA. In the SBT transplantation model, both 3-HAA (P < 0.05) and IDO(+) DC (P < 0.01) prolonged the survival time of transplanted mice. Mice treated with IDO(+) DC achieved longer mean survival time than 3-HAA administrated mice (11.5d vs. 18.5d). Grafts from IDO(+) DC, 3-HAA and combination treatment group showed reduced inflammation and minimal architectural distortion. IFN-γ production was significantly inhibited by IDO(+) DC and 3-HAA (P<0.05). The expression of IL-2 was slightly lower with 3-HAA or IDO(+) DC treatment. However, IL-10 was higher in 3-HAA, IDO(+) DC and combination treatment groups, while TGF-β was elevated in all non-control groups.

Conclusions: IDO(+) DC plus 3-HAA has an immunoprotective role and represents a potential strategy to suppress acute rejection and prolong survival of grafts in SBT.

Keywords: 3-hydroxyanthranilic acid (3-HAA); Immune tolerance; Indoleamine 2,3-dioxygenase (IDO); Regulatory T cells (treg); Small bowel transplantation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxyanthranilic Acid / pharmacology
  • Animals
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / metabolism
  • Dendritic Cells / drug effects
  • Dendritic Cells / physiology*
  • Forkhead Transcription Factors / metabolism
  • Graft Rejection / immunology*
  • Humans
  • Immune Tolerance
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism*
  • Intestine, Small / transplantation
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Organ Transplantation*
  • T-Lymphocytes, Regulatory / immunology*
  • Transgenes / genetics

Substances

  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • 3-Hydroxyanthranilic Acid