The IL-33/ST2 axis augments effector T-cell responses during acute GVHD

Blood. 2015 May 14;125(20):3183-92. doi: 10.1182/blood-2014-10-606830. Epub 2015 Mar 26.

Abstract

Interleukin (IL)-33 binding to the receptor suppression of tumorigenicity 2 (ST2) produces pro-inflammatory and anti-inflammatory effects. Increased levels of soluble ST2 (sST2) are a biomarker for steroid-refractory graft-versus-host disease (GVHD) and mortality. However, whether sST2 has a role as an immune modulator or only as a biomarker during GVHD was unclear. We show increased IL-33 production by nonhematopoietic cells in the gastrointestinal (GI) tract in mice post-conditioning and patients during GVHD. Exogenous IL-33 administration during the peak inflammatory response worsened GVHD. Conversely, GVHD lethality and tumor necrosis factor-α production was significantly reduced in il33(-/-) recipients. ST2 was upregulated on murine and human alloreactive T cells and sST2 increased as experimental GVHD progressed. Concordantly, st2(-/-) vs wild-type (WT) donor T cells had a marked reduction in GVHD lethality and GI histopathology. Alloantigen-induced IL-18 receptor upregulation was lower in st2(-/-) T cells, and linked to reduced interferon-γ production by st2(-/-) vs WT T cells during GVHD. Blockade of IL-33/ST2 interactions during allogeneic-hematopoietic cell transplantation by exogenous ST2-Fc infusions had a marked reduction in GVHD lethality, indicating a role of ST2 as a decoy receptor modulating GVHD. Together, these studies point to the IL-33/ST2 axis as a novel and potent target for GVHD therapy.

Publication types

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

MeSH terms

  • Acute Disease
  • Animals
  • Cluster Analysis
  • Disease Models, Animal
  • Gene Expression
  • Gene Expression Profiling
  • Graft vs Host Disease / diagnosis
  • Graft vs Host Disease / genetics
  • Graft vs Host Disease / immunology*
  • Graft vs Host Disease / metabolism*
  • Graft vs Host Disease / mortality
  • Hematopoietic Stem Cell Transplantation / adverse effects
  • Humans
  • Interferon-gamma / biosynthesis
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Intestinal Mucosa / metabolism
  • Intestines / pathology
  • Intestines / radiation effects
  • Isoantigens / immunology
  • Mice
  • Mice, Knockout
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Severity of Illness Index
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism*
  • Tissue Donors
  • Transplantation Conditioning
  • Transplantation, Homologous

Substances

  • IL1RL1 protein, human
  • IL33 protein, human
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Interleukins
  • Isoantigens
  • Receptors, Cell Surface
  • Interferon-gamma