Molecular basis for the unique deubiquitinating activity of the NF-kappaB inhibitor A20

J Mol Biol. 2008 Feb 15;376(2):526-40. doi: 10.1016/j.jmb.2007.11.092. Epub 2007 Dec 4.

Abstract

Nuclear factor kappaB (NF-kappaB) activation in tumor necrosis factor, interleukin-1, and Toll-like receptor pathways requires Lys63-linked nondegradative polyubiquitination. A20 is a specific feedback inhibitor of NF-kappaB activation in these pathways that possesses dual ubiquitin-editing functions. While the N-terminal domain of A20 is a deubiquitinating enzyme (DUB) for Lys63-linked polyubiquitinated signaling mediators such as TRAF6 and RIP, its C-terminal domain is a ubiquitin ligase (E3) for Lys48-linked degradative polyubiquitination of the same substrates. To elucidate the molecular basis for the DUB activity of A20, we determined its crystal structure and performed a series of biochemical and cell biological studies. The structure reveals the potential catalytic mechanism of A20, which may be significantly different from papain-like cysteine proteases. Ubiquitin can be docked onto a conserved A20 surface; this interaction exhibits charge complementarity and no steric clash. Surprisingly, A20 does not have specificity for Lys63-linked polyubiquitin chains. Instead, it effectively removes Lys63-linked polyubiquitin chains from TRAF6 without dissembling the chains themselves. Our studies suggest that A20 does not act as a general DUB but has the specificity for particular polyubiquitinated substrates to assure its fidelity in regulating NF-kappaB activation in the tumor necrosis factor, interleukin-1, and Toll-like receptor pathways.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alanine / metabolism
  • Amino Acid Sequence
  • Amino Acid Substitution
  • Binding Sites
  • Catalysis
  • Cell Line
  • Conserved Sequence
  • Crystallography, X-Ray
  • DNA-Binding Proteins
  • Escherichia coli / genetics
  • Gene Deletion
  • Glutathione Transferase / metabolism
  • Humans
  • Hydrogen Bonding
  • Intracellular Signaling Peptides and Proteins / chemistry
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / isolation & purification
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Kidney / cytology
  • Models, Molecular
  • Molecular Sequence Data
  • NF-kappa B / antagonists & inhibitors*
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / genetics
  • Nuclear Proteins / isolation & purification
  • Nuclear Proteins / metabolism*
  • Polyubiquitin / chemistry
  • Polyubiquitin / metabolism
  • Precipitin Tests
  • Protein Binding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Sequence Homology, Amino Acid
  • Static Electricity
  • Substrate Specificity
  • TNF Receptor-Associated Factor 6 / metabolism
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Ubiquitin / metabolism
  • Ubiquitin-Protein Ligases / chemistry
  • Ubiquitination*

Substances

  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • NF-kappa B
  • Nuclear Proteins
  • TNF Receptor-Associated Factor 6
  • Ubiquitin
  • Polyubiquitin
  • Ubiquitin-Protein Ligases
  • Glutathione Transferase
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Alanine