Type I IFN induces protein ISGylation to enhance cytokine expression and augments colonic inflammation

Proc Natl Acad Sci U S A. 2015 Nov 17;112(46):14313-8. doi: 10.1073/pnas.1505690112. Epub 2015 Oct 29.

Abstract

Type I IFNs have broad activity in tissue inflammation and malignant progression that depends on the expression of IFN-stimulated genes (ISGs). ISG15, one such ISG, can form covalent conjugates to many cellular proteins, a process termed "protein ISGylation." Although type I IFNs are involved in multiple inflammatory disorders, the role of protein ISGylation during inflammation has not been evaluated. Here we report that protein ISGylation exacerbates intestinal inflammation and colitis-associated colon cancer in mice. Mechanistically, we demonstrate that protein ISGylation negatively regulates the ubiquitin-proteasome system, leading to increased production of IFN-induced reactive oxygen species (ROS). The increased cellular ROS then enhances LPS-induced activation of p38 MAP kinase and the expression of inflammation-related cytokines in macrophages. Thus our studies reveal a regulatory role for protein ISGylation in colonic inflammation and its related malignant progression, indicating that targeting ubiquitin-activating enzyme E1 homolog has therapeutic potential in treating inflammatory diseases.

Keywords: ISGylation; cancer; cytokine; inflammation; ubiquitylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Colitis / chemically induced
  • Colitis / metabolism*
  • Colitis / pathology
  • Colon / metabolism*
  • Colon / pathology
  • Interferon Type I / metabolism*
  • Lipopolysaccharides / toxicity
  • Mice
  • Reactive Oxygen Species / metabolism*
  • Ubiquitin-Activating Enzymes / metabolism*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Interferon Type I
  • Lipopolysaccharides
  • Reactive Oxygen Species
  • p38 Mitogen-Activated Protein Kinases
  • Ubiquitin-Activating Enzymes