Non-redundant properties of IL-1α and IL-1β during acute colon inflammation in mice

Gut. 2014 Apr;63(4):598-609. doi: 10.1136/gutjnl-2012-303329. Epub 2013 Jun 21.

Abstract

Objective: The differential role of the IL-1 agonists, IL-1α, which is mainly cell-associated versus IL-1β, which is mostly secreted, was studied in colon inflammation.

Design: Dextran sodium sulfate (DSS) colitis was induced in mice globally deficient in either IL-1α or IL-1β, and in wild-type mice, or in mice with conditional deletion of IL-1α in intestinal epithelial cells (IECs). Bone marrow transplantation experiments were performed to assess the role of IL-1α or IL-1β of myeloid versus colon non-hematopoietic cells in inflammation and repair in acute colitis.

Results: IL-1α released from damaged IECs acts as an alarmin by initiating and propagating colon inflammation, as IL-1α deficient mice exhibited mild disease symptoms with improved recovery. IL-1β is involved in repair of IECs and reconstitution of the epithelial barrier during the resolution of colitis; its deficiency correlates with disease exacerbation. Neutralisation of IL-1α in control mice during acute colitis led to alleviation of clinical and histological manifestations, whereas treatment with rIL-1Ra or anti-IL-1β antibodies was not effective. Repair after colitis correlated with accumulation of CD8 and regulatory T cells in damaged crypts.

Conclusions: The role of IL-1α and IL-1β differs in DSS-induced colitis in that IL-1α, mainly of colon epithelial cells is inflammatory, whereas IL-1β, mainly of myeloid cell origin, promotes healing and repair. Given the dissimilar functions of each IL-1 agonistic molecule, an IL-1 receptor blockade would not be as therapeutically effective as specific neutralising of IL-1α, which leaves IL-1β function intact.

Keywords: EXPERIMENTAL COLITIS; GUT INFLAMMATION; INTERLEUKINS; INTESTINAL EPITHELIUM; MUCOSAL IMMUNITY.

Publication types

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

MeSH terms

  • Animals
  • Colitis / chemically induced
  • Colitis / pathology
  • Colitis / physiopathology*
  • Colon / drug effects
  • Colon / pathology
  • Colon / physiopathology
  • Dextran Sulfate / pharmacology
  • Disease Models, Animal
  • Interleukin-1 / agonists
  • Interleukin-1alpha / physiology*
  • Interleukin-1beta / physiology*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / pathology
  • Intestinal Mucosa / physiopathology
  • Leukemic Infiltration / physiopathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • T-Lymphocytes / physiology

Substances

  • Interleukin-1
  • Interleukin-1alpha
  • Interleukin-1beta
  • Dextran Sulfate