SLAP2 Adaptor Binding Disrupts c-CBL Autoinhibition to Activate Ubiquitin Ligase Function

J Mol Biol. 2021 Apr 16;433(8):166880. doi: 10.1016/j.jmb.2021.166880. Epub 2021 Feb 20.

Abstract

CBL is a RING type E3 ubiquitin ligase that functions as a negative regulator of tyrosine kinase signaling and loss of CBL E3 function is implicated in several forms of leukemia. The Src-like adaptor proteins (SLAP/SLAP2) bind to CBL and are required for CBL-dependent downregulation of antigen receptor, cytokine receptor, and receptor tyrosine kinase signaling. Despite the established role of SLAP/SLAP2 in regulating CBL activity, the nature of the interaction and the mechanisms involved are not known. To understand the molecular basis of the interaction between SLAP/SLAP2 and CBL, we solved the crystal structure of CBL tyrosine kinase binding domain (TKBD) in complex with SLAP2. The carboxy-terminal region of SLAP2 adopts an α-helical structure which binds in a cleft between the 4H, EF-hand, and SH2 domains of the TKBD. This SLAP2 binding site is remote from the canonical TKBD phospho-tyrosine peptide binding site but overlaps with a region important for stabilizing CBL in its autoinhibited conformation. In addition, binding of SLAP2 to CBL in vitro activates the ubiquitin ligase function of autoinhibited CBL. Disruption of the CBL/SLAP2 interface through mutagenesis demonstrated a role for this protein-protein interaction in regulation of CBL E3 ligase activity in cells. Our results reveal that SLAP2 binding to a regulatory cleft of the TKBD provides an alternative mechanism for activation of CBL ubiquitin ligase function.

Keywords: CBL; Src-like adaptor protein; X-ray crystal structure; activation mechanism; protein-protein interaction; ubiquitin ligase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / chemistry*
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Binding Sites
  • Down-Regulation
  • Humans
  • Molecular Conformation
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein-Tyrosine Kinases / metabolism
  • Proto-Oncogene Proteins c-cbl / chemistry*
  • Proto-Oncogene Proteins c-cbl / genetics
  • Proto-Oncogene Proteins c-cbl / metabolism*
  • Proto-Oncogene Proteins pp60(c-src) / chemistry*
  • Proto-Oncogene Proteins pp60(c-src) / genetics
  • Proto-Oncogene Proteins pp60(c-src) / metabolism*
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Sequence Alignment
  • Signal Transduction
  • Ubiquitin / metabolism*
  • Ubiquitin-Protein Ligases / metabolism
  • src Homology Domains

Substances

  • Adaptor Proteins, Signal Transducing
  • SLA2 protein, human
  • Ubiquitin
  • Proto-Oncogene Proteins c-cbl
  • Ubiquitin-Protein Ligases
  • Protein-Tyrosine Kinases
  • Receptor Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins pp60(c-src)
  • CBL protein, human

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