Dimeric switch of Hakai-truncated monomers during substrate recognition: insights from solution studies and NMR structure

J Biol Chem. 2014 Sep 12;289(37):25611-23. doi: 10.1074/jbc.M114.592840. Epub 2014 Jul 29.

Abstract

Hakai, an E3 ubiquitin ligase, disrupts cell-cell contacts in epithelial cells and is up-regulated in human colon and gastric adenocarcinomas. Hakai acts through its phosphotyrosine-binding (HYB) domain, which bears a dimeric fold that recognizes the phosphotyrosine motifs of E-cadherin, cortactin, DOK1, and other Src substrates. Unlike the monomeric nature of the SH2 and phosphotyrosine-binding domains, the architecture of the HYB domain consists of an atypical, zinc-coordinated tight homodimer. Here, we report a C-terminal truncation mutant of the HYB domain (HYB(ΔC)), comprising amino acids 106-194, which exists as a monomer in solution. The NMR structure revealed that this deletion mutant undergoes a dramatic structural change caused by a rearrangement of the atypical zinc-coordinated unit in the C terminus of the HYB domain to a C2H2-like zinc finger in HYB(ΔC). Moreover, using isothermal titration calorimetry, we show that dimerization of HYB(ΔC) can be induced using a phosphotyrosine substrate peptide. This ligand-induced dimerization of HYB(ΔC) is further validated using analytical ultracentrifugation, size-exclusion chromatography, NMR relaxation studies, dynamic light scattering, and circular dichroism experiments. Overall, these observations suggest that the dimeric architecture of the HYB domain is essential for the phosphotyrosine-binding property of Hakai.

Keywords: E3 Ubiquitin Ligase; Nuclear Magnetic Resonance (NMR); Phosphotyrosine; Structural Biology; Zinc Finger.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Cadherins / chemistry*
  • Cadherins / metabolism
  • Crystallography, X-Ray
  • Epithelial Cells / chemistry*
  • Epithelial Cells / metabolism
  • Humans
  • Ligands
  • Magnetic Resonance Spectroscopy
  • Phosphotyrosine / chemistry
  • Protein Binding
  • Protein Conformation
  • Solutions / chemistry
  • Ubiquitin-Protein Ligases / chemistry*
  • Ubiquitin-Protein Ligases / metabolism
  • src Homology Domains*

Substances

  • Cadherins
  • Ligands
  • Solutions
  • Phosphotyrosine
  • CBLL1 protein, human
  • Ubiquitin-Protein Ligases

Associated data

  • PDB/2MQ1