Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling

J Biol Chem. 2004 Feb 20;279(8):7055-63. doi: 10.1074/jbc.M309184200. Epub 2003 Nov 25.

Abstract

Diverse cellular events are regulated by post-translational modification of substrate proteins via covalent attachment of one or a chain of ubiquitin molecules. The outcome of (poly)ubiquitination depends upon the specific lysine residues involved in the formation of polyubiquitin chains. Lys48-linked chains act as a universal signal for proteasomal degradation, whereas Lys63-linked chains act as a specific signal in several non-degradative processes. Although it has been anticipated that functional diversity between alternatively linked polyubiquitin chains relies on linkage-dependent differences in chain conformation/topology, direct structural evidence in support of this model has been lacking. Here we use NMR methods to determine the structure of a Lys63-linked di-ubiquitin chain. The structure is characterized by an extended conformation, with no direct contact between the hydrophobic residues Leu8, Ile44, and Val70 on the ubiquitin units. This structure contrasts with the closed conformation observed for Lys48-linked di-ubiquitin wherein these residues form the interdomain interface (Cook, W. J., Jeffrey, L. C., Carson, M., Zhijian, C., and Pickart, C. M. (1992) J. Biol. Chem. 267, 16467-16471; Varadan, R., Walker, O., Pickart, C., and Fushman, D. (2002) J. Mol. Biol. 324, 637-647). Consistent with the open conformation of the Lys(63)-linked di-ubiquitin, our binding studies show that both ubiquitin domains in this chain can bind a ubiquitin-associated domain from HHR23A independently and in a mode similar to that for mono-ubiquitin. In contrast, Lys48-linked di-ubiquitin binds in a different, higher affinity mode that has yet to be determined. This is the first experimental evidence that alternatively linked polyubiquitin chains adopt distinct conformations.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Cysteine Endopeptidases / metabolism
  • DNA-Binding Proteins / chemistry
  • Fungal Proteins / chemistry
  • Ligands
  • Lysine / chemistry*
  • Magnetic Resonance Spectroscopy
  • Models, Molecular
  • Molecular Sequence Data
  • Multienzyme Complexes / metabolism
  • Mutagenesis, Site-Directed
  • Polyubiquitin / chemistry*
  • Proteasome Endopeptidase Complex
  • Protein Binding
  • Protein Conformation
  • Protein Processing, Post-Translational
  • Protein Structure, Tertiary
  • Saccharomyces cerevisiae Proteins / chemistry
  • Signal Transduction
  • Ubiquitin / chemistry*
  • Ubiquitin-Conjugating Enzymes / chemistry

Substances

  • DNA-Binding Proteins
  • Fungal Proteins
  • Ligands
  • Multienzyme Complexes
  • RAD23 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Ubiquitin
  • Polyubiquitin
  • UBC13 protein, S cerevisiae
  • Ubiquitin-Conjugating Enzymes
  • Cysteine Endopeptidases
  • Proteasome Endopeptidase Complex
  • Lysine