Recruitment of A20 by the C-terminal domain of NEMO suppresses NF-κB activation and autoinflammatory disease

Proc Natl Acad Sci U S A. 2016 Feb 9;113(6):1612-7. doi: 10.1073/pnas.1518163113. Epub 2016 Jan 22.

Abstract

Receptor-induced NF-κB activation is controlled by NEMO, the NF-κB essential modulator. Hypomorphic NEMO mutations result in X-linked ectodermal dysplasia with anhidrosis and immunodeficiency, also referred to as NEMO syndrome. Here we describe a distinct group of patients with NEMO C-terminal deletion (ΔCT-NEMO) mutations. Individuals harboring these mutations develop inflammatory skin and intestinal disease in addition to ectodermal dysplasia with anhidrosis and immunodeficiency. Both primary cells from these patients, as well as reconstituted cell lines with this deletion, exhibited increased IκB kinase (IKK) activity and production of proinflammatory cytokines. Unlike previously described loss-of-function mutations, ΔCT-NEMO mutants promoted increased NF-κB activation in response to TNF and Toll-like receptor stimulation. Investigation of the underlying mechanisms revealed impaired interactions with A20, a negative regulator of NF-κB activation, leading to prolonged accumulation of K63-ubiquitinated RIP within the TNFR1 signaling complex. Recruitment of A20 to the C-terminal domain of NEMO represents a novel mechanism limiting NF-κB activation by NEMO, and its absence results in autoinflammatory disease.

Keywords: A20; HED-ID; NF-κB; TLR; autoinflammatory disease.

MeSH terms

  • Case-Control Studies
  • Cell Line
  • Cell Nucleus / metabolism
  • Cytokines / biosynthesis
  • DNA-Binding Proteins / metabolism*
  • Deubiquitinating Enzyme CYLD
  • Female
  • Gene Expression Regulation
  • Humans
  • I-kappa B Kinase / chemistry*
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / metabolism*
  • Immunity, Innate
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Male
  • Monocytes / metabolism
  • Mutant Proteins / metabolism
  • Mutation / genetics
  • NF-kappa B / metabolism*
  • Nuclear Proteins / metabolism*
  • Pedigree
  • Phenotype
  • Polyubiquitin / metabolism
  • Protein Structure, Tertiary
  • Protein Transport
  • Receptors, Tumor Necrosis Factor / metabolism
  • T-Lymphocytes / metabolism
  • Toll-Like Receptors / metabolism
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Tumor Suppressor Proteins / metabolism
  • Ubiquitination

Substances

  • Cytokines
  • DNA-Binding Proteins
  • IKBKG protein, human
  • Intracellular Signaling Peptides and Proteins
  • Mutant Proteins
  • NF-kappa B
  • Nuclear Proteins
  • Receptors, Tumor Necrosis Factor
  • Toll-Like Receptors
  • Tumor Suppressor Proteins
  • Polyubiquitin
  • I-kappa B Kinase
  • CYLD protein, human
  • Deubiquitinating Enzyme CYLD
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3