Ectopic expression of OX1R in ulcerative colitis mediates anti-inflammatory effect of orexin-A

Biochim Biophys Acta Mol Basis Dis. 2018 Nov;1864(11):3618-3628. doi: 10.1016/j.bbadis.2018.08.023. Epub 2018 Aug 18.

Abstract

Orexins (orexin-A and orexin-B) are hypothalamic peptides that are produced by the same precursor and are involved in sleep/wake control, which is mediated by two G protein-coupled receptor subtypes, OX1R and OX2R. Ulcerative colitis (UC) is an inflammatory bowel disease, (IBD) which is characterized by long-lasting inflammation and ulcers that affect the colon and rectum mucosa and is known to be a significant risk factor for colon cancer development. Based on our recent studies showing that OX1R is aberrantly expressed in colon cancer, we wondered whether orexin-A could play a role in UC. Immunohistochemistry studies revealed that OX1R is highly expressed in the affected colonic epithelium of most UC patients, but not in the non-affected colonic mucosa. Injection of exogenous orexin-A specifically improved the inflammatory symptoms in the two colitis murine models. Conversely, injection of inactive orexin-A analog, OxB7-28 or OX1R specific antagonist SB-408124 did not have anti-inflammatory effect. Moreover, treatment with orexin-A in DSS-colitis induced OX1R-/- knockout mice did not have any protective effect. The orexin-A anti-inflammatory effect was due to the decreased expression of pro-inflammatory cytokines in immune cells and specifically in T-cells isolated from colonic mucosa. Moreover, orexin-A inhibited canonical NFκB activation in an immune cell line and in intestinal epithelial cell line. These results suggest that orexin-A might represent a promising alternative to current UC therapies.

Keywords: GPCR; Inflammation; Inflammatory bowel disease; Neuropeptide; Orexins; Ulcerative colitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Cell Line
  • Colitis, Ulcerative / chemically induced
  • Colitis, Ulcerative / drug therapy
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / pathology*
  • Cytokines / immunology
  • Cytokines / metabolism
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Down-Regulation
  • Ectopic Gene Expression
  • Epithelial Cells / drug effects
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Female
  • Humans
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / pathology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Orexin Receptor Antagonists / pharmacology
  • Orexin Receptors / genetics
  • Orexin Receptors / metabolism*
  • Orexins / pharmacology*
  • Orexins / therapeutic use
  • Phenylurea Compounds / pharmacology
  • Retrospective Studies
  • Signal Transduction / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Young Adult

Substances

  • Cytokines
  • HCRTR1 protein, human
  • Hcrtr1 protein, mouse
  • NF-kappa B
  • Orexin Receptor Antagonists
  • Orexin Receptors
  • Orexins
  • Phenylurea Compounds
  • SB 408124
  • Dextran Sulfate