Deletion of IL-6 Exacerbates Colitis and Induces Systemic Inflammation in IL-10-Deficient Mice

J Crohns Colitis. 2020 Jul 9;14(6):831-840. doi: 10.1093/ecco-jcc/jjz176.

Abstract

Background and aims: Interleukin 6 [IL-6] or its receptor is currently a candidate for targeted biological therapy of inflammatory bowel disease [IBD]. Thus, a comprehensive understanding of the consequences of blocking IL-6 is imperative. We investigated this by evaluating the effects of IL-6 deletion on the spontaneous colitis of IL-10-deficient mice [IL-10-/-].

Methods: IL-6/IL-10 double-deficient mice [IL-6-/-/IL-10-/-] were generated and analysed for intestinal inflammation, general phenotypes and molecular/biochemical changes in the colonic mucosa compared with wild-type and IL-10-/- mice.

Results: Unexpectedly, the IL-6-/-/IL-10-/- mice showed more pronounced gut inflammation and earlier disease onset than IL-10-/- mice, both locally [colon and small bowel] and systemically [splenomegaly, ulcerative dermatitis, leukocytosis, neutrophilia and monocytosis]. IL-6-/-/IL-10-/- mice exhibited elevations of multiple cytokines [IL-1β, IL-4, IL-12, TNFα] and chemokines [MCP-1 and MIG], but not IFN-γ [Th1], IL-17A and IL-17G [Th17], or IL-22 [Th22]. FOXP3 and TGF-β, two key factors for regulatory T [Treg] cell differentiation, were significantly down-regulated in the colonic mucosa, but not in the thymus or mesenteric lymph nodes, of IL-6-/-/IL-10-/- mice. CTLA-4 was diminished while iNOS was up-regulated in the colonic mucosa of IL-6-/-/IL-10-/- mice.

Conclusion: In IL-10-/- mice, complete IL-6 blockade significantly aggravates gut inflammation, at least in part by suppressing Treg/CTLA-4 and promoting the IL-1β/Th2 pathway. In addition, the double mutant exhibits signs of severe systemic inflammation. Our data define a new function of IL-6 and suggest that caution should be exercised when targeting IL-6 in IBD patients, particularly those with defects in IL-10 signalling.

Keywords: Inflammatory bowel disease [IBD]; Crohn’s disease [CD]; extraintestinal manifestation; interleukin 10 [IL-10]; interleukin 6 [IL-6].

MeSH terms

  • Animals
  • CTLA-4 Antigen / immunology*
  • Cell Differentiation
  • Crohn Disease* / immunology
  • Crohn Disease* / therapy
  • Disease Models, Animal
  • Inflammation / immunology
  • Inflammatory Bowel Diseases* / immunology
  • Inflammatory Bowel Diseases* / therapy
  • Interleukin-10 / immunology*
  • Interleukin-6 / immunology*
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / pathology
  • Mice
  • Mice, Knockout
  • Molecular Targeted Therapy / adverse effects
  • Molecular Targeted Therapy / methods
  • Receptors, Interleukin-6 / immunology
  • T-Lymphocytes, Regulatory / immunology

Substances

  • CTLA-4 Antigen
  • IL10 protein, mouse
  • Interleukin-6
  • Receptors, Interleukin-6
  • Interleukin-10