USP7 Is a Tumor-Specific WNT Activator for APC-Mutated Colorectal Cancer by Mediating β-Catenin Deubiquitination

Cell Rep. 2017 Oct 17;21(3):612-627. doi: 10.1016/j.celrep.2017.09.072.

Abstract

The tumor suppressor gene adenomatous polyposis coli (APC) is mutated in most colorectal cancers (CRCs), resulting in constitutive Wnt activation. To understand the Wnt-activating mechanism of the APC mutation, we applied CRISPR/Cas9 technology to engineer various APC-truncated isogenic lines. We find that the β-catenin inhibitory domain (CID) in APC represents the threshold for pathological levels of Wnt activation and tumor transformation. Mechanistically, CID-deleted APC truncation promotes β-catenin deubiquitination through reverse binding of β-TrCP and USP7 to the destruction complex. USP7 depletion in APC-mutated CRC inhibits Wnt activation by restoring β-catenin ubiquitination, drives differentiation, and suppresses xenograft tumor growth. Finally, the Wnt-activating role of USP7 is specific to APC mutations; thus, it can be used as a tumor-specific therapeutic target for most CRCs.

Keywords: APC; USP7; Wnt signaling; colorectal cancer; ubiquitination; β-catenin.

MeSH terms

  • Adenomatous Polyposis Coli Protein / genetics*
  • Amino Acid Sequence
  • Animals
  • Cell Differentiation / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / pathology
  • HEK293 Cells
  • Humans
  • Mice
  • Mutation / genetics*
  • Organoids / metabolism
  • Protein Binding / drug effects
  • Protein Domains
  • Small Molecule Libraries / pharmacology
  • Ubiquitin-Specific Peptidase 7 / chemistry
  • Ubiquitin-Specific Peptidase 7 / metabolism*
  • Ubiquitination* / drug effects
  • Wnt Signaling Pathway / drug effects
  • beta Catenin / chemistry
  • beta Catenin / metabolism*
  • beta-Transducin Repeat-Containing Proteins / metabolism

Substances

  • Adenomatous Polyposis Coli Protein
  • Small Molecule Libraries
  • beta Catenin
  • beta-Transducin Repeat-Containing Proteins
  • USP7 protein, human
  • Ubiquitin-Specific Peptidase 7