ABIN3 Negatively Regulates Necroptosis-induced Intestinal Inflammation Through Recruiting A20 and Restricting the Ubiquitination of RIPK3 in Inflammatory Bowel Disease

J Crohns Colitis. 2021 Jan 13;15(1):99-114. doi: 10.1093/ecco-jcc/jjaa131.

Abstract

Background and aims: There is evidence for a disturbed necroptosis function in many inflammatory diseases, but its role in inflammatory bowel diseases [IBD] and the underlying mechanisms are unclear. Here, we studied the functional significance and molecular mechanisms of ABIN3, a ubiquitin-binding protein, in regulating the ubiquitination and activation of necroptosis in IBD.

Methods: The expression of necroptosis hallmarks and ABIN3 were assessed in inflamed samples of IBD patients, dextran sodium sulphate [DSS]-induced colitis models, and azoxymethane [AOM]/DSS models in mice. ABIN3 was overexpressed and silenced to explore its function in regulating necroptosis, inflammation, and intestinal barrier function. Immuoprecipitiation [IP] and co-IP assays were performed to investigate the cross-talk between ABIN3 and deubiquitinating enzyme A20, and the mechanisms of coordinating ubiquitination modification to regulate necroptosis.

Results: Excessive necroptosis is an important contributory factor towards the uncontrolled inflammation and intestinal barrier defects in IBD and experimental colitis. Blocking necroptosis by Nec-1s or GSK'872 significantly prevented cell death and alleviated DSS-induced colitis in vivo, whereas in the AOM/DSS model, necroptosis inhibitors aggravated the severity of colitis-associated colon carcinogenesis [CAC]. Mechanistically, ABIN3 is rapidly recruited to the TNF-RSC complex, which interacts and coordinates with deubiquitinating enzyme A20 to control the K63 deubiquitination modification and subsequent activation of the critical necroptosis kinase, RIPK3, to suppress necroptosis.

Conclusions: ABIN3 regulates inflammatory response and intestinal barrier function by interacting with A20 and coordinating the K63 deubiquitination modification of necroptosis in IBD.

Keywords: A20; ABIN3; RIPK3; inflammation; intestinal barrier; necroptosis; ubiquitination.

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Benzothiazoles / pharmacology*
  • Enzyme Inhibitors / pharmacology
  • Imidazoles / pharmacology*
  • Indoles / pharmacology*
  • Inflammation / metabolism
  • Inflammatory Bowel Diseases* / immunology
  • Inflammatory Bowel Diseases* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Necroptosis / drug effects
  • Quinolines / pharmacology*
  • Receptor-Interacting Protein Serine-Threonine Kinases* / antagonists & inhibitors
  • Receptor-Interacting Protein Serine-Threonine Kinases* / metabolism
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor alpha-Induced Protein 3 / metabolism*
  • Ubiquitination / drug effects

Substances

  • Adaptor Proteins, Signal Transducing
  • Benzothiazoles
  • Enzyme Inhibitors
  • GSK872
  • Imidazoles
  • Indoles
  • Quinolines
  • Tnip2 protein, mouse
  • necrostatin-1
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Ripk3 protein, mouse
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Tnfaip3 protein, mouse