The Deubiquitinase OTULIN Is an Essential Negative Regulator of Inflammation and Autoimmunity

Cell. 2016 Aug 25;166(5):1215-1230.e20. doi: 10.1016/j.cell.2016.07.019. Epub 2016 Aug 11.

Abstract

Methionine-1 (M1)-linked ubiquitin chains regulate the activity of NF-κB, immune homeostasis, and responses to infection. The importance of negative regulators of M1-linked chains in vivo remains poorly understood. Here, we show that the M1-specific deubiquitinase OTULIN is essential for preventing TNF-associated systemic inflammation in humans and mice. A homozygous hypomorphic mutation in human OTULIN causes a potentially fatal autoinflammatory condition termed OTULIN-related autoinflammatory syndrome (ORAS). Four independent OTULIN mouse models reveal that OTULIN deficiency in immune cells results in cell-type-specific effects, ranging from over-production of inflammatory cytokines and autoimmunity due to accumulation of M1-linked polyubiquitin and spontaneous NF-κB activation in myeloid cells to downregulation of M1-polyubiquitin signaling by degradation of LUBAC in B and T cells. Remarkably, treatment with anti-TNF neutralizing antibodies ameliorates inflammation in ORAS patients and rescues mouse phenotypes. Hence, OTULIN is critical for restraining life-threatening spontaneous inflammation and maintaining immune homeostasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Neutralizing / therapeutic use
  • Autoimmune Diseases / genetics*
  • Autoimmune Diseases / immunology
  • Autoimmune Diseases / therapy
  • Autoimmunity / genetics*
  • B-Lymphocytes / immunology
  • Cytokines / metabolism
  • Deubiquitinating Enzymes / genetics
  • Deubiquitinating Enzymes / metabolism*
  • Disease Models, Animal
  • Endopeptidases / genetics
  • Endopeptidases / metabolism*
  • Germ-Line Mutation
  • Humans
  • Inflammation / genetics*
  • Inflammation / immunology
  • Inflammation / therapy
  • Infliximab / therapeutic use
  • Methionine / metabolism
  • Mice
  • Mice, Mutant Strains
  • Myeloid Cells / immunology
  • Polyubiquitin / metabolism
  • Sequence Deletion
  • Syndrome
  • T-Lymphocytes / immunology
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors

Substances

  • Antibodies, Neutralizing
  • Cytokines
  • Tumor Necrosis Factor-alpha
  • Polyubiquitin
  • Methionine
  • Infliximab
  • Endopeptidases
  • OTULIN protein, human
  • Deubiquitinating Enzymes