The Poly(ADP-ribose) Polymerase Enzyme Tankyrase Antagonizes Activity of the β-Catenin Destruction Complex through ADP-ribosylation of Axin and APC2

J Biol Chem. 2016 Jun 10;291(24):12747-12760. doi: 10.1074/jbc.M115.705442. Epub 2016 Apr 11.

Abstract

Most colon cancer cases are initiated by truncating mutations in the tumor suppressor, adenomatous polyposis coli (APC). APC is a critical negative regulator of the Wnt signaling pathway that participates in a multi-protein "destruction complex" to target the key effector protein β-catenin for ubiquitin-mediated proteolysis. Prior work has established that the poly(ADP-ribose) polymerase (PARP) enzyme Tankyrase (TNKS) antagonizes destruction complex activity by promoting degradation of the scaffold protein Axin, and recent work suggests that TNKS inhibition is a promising cancer therapy. We performed a yeast two-hybrid (Y2H) screen and uncovered TNKS as a putative binding partner of Drosophila APC2, suggesting that TNKS may play multiple roles in destruction complex regulation. We find that TNKS binds a C-terminal RPQPSG motif in Drosophila APC2, and that this motif is conserved in human APC2, but not human APC1. In addition, we find that APC2 can recruit TNKS into the β-catenin destruction complex, placing the APC2/TNKS interaction at the correct intracellular location to regulate β-catenin proteolysis. We further show that TNKS directly PARylates both Drosophila Axin and APC2, but that PARylation does not globally regulate APC2 protein levels as it does for Axin. Moreover, TNKS inhibition in colon cancer cells decreases β-catenin signaling, which we find cannot be explained solely through Axin stabilization. Instead, our findings suggest that TNKS regulates destruction complex activity at the level of both Axin and APC2, providing further mechanistic insight into TNKS inhibition as a potential Wnt pathway cancer therapy.

Keywords: ADP-ribosylation; Adenomatous Polyposis Coli; Tankyrase; Wnt signaling; XAV939; axin; beta-catenin (β-catenin); colon cancer; destruction complex.

Publication types

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

MeSH terms

  • Adenosine Diphosphate Ribose / metabolism*
  • Amino Acid Motifs / genetics
  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Axin Protein / genetics
  • Axin Protein / metabolism*
  • Blotting, Western
  • Cell Line, Tumor
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Drosophila / genetics
  • Drosophila / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Female
  • Fluorescent Antibody Technique
  • HCT116 Cells
  • Humans
  • Male
  • Protein Binding
  • Substrate Specificity
  • Tankyrases / genetics
  • Tankyrases / metabolism*
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • Two-Hybrid System Techniques
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • APC2 protein, Drosophila
  • APC2 protein, human
  • Axin Protein
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Tumor Suppressor Proteins
  • beta Catenin
  • Adenosine Diphosphate Ribose
  • Tankyrases
  • TNKS protein, human