Identification of a novel role of ZMIZ2 protein in regulating the activity of the Wnt/β-catenin signaling pathway

J Biol Chem. 2013 Dec 13;288(50):35913-24. doi: 10.1074/jbc.M113.529727. Epub 2013 Oct 30.

Abstract

ZMIZ2, also named ZIMP7, is a protein inhibitor of activated STAT (PIAS)-like protein and a transcriptional coactivator. In this study, we investigated the interaction between ZMIZ2 and β-catenin, a key regulator of the Wnt signaling pathway. We demonstrated that the expression of exogenous ZMIZ2 augments TCF (T cell factor) and β-catenin-mediated transcription. In contrast, shRNA knockdown of ZMIZ2 expression specifically represses the enhancement of TCF/β-catenin-mediated transcription by ZMIZ2. Using Wnt3a-conditioned medium, we demonstrated that ZMIZ2 can enhance Wnt ligand-induced TCF/β-catenin-mediated transcription. We also showed a promotional role of ZMIZ2 in enhancing β-catenin downstream target gene expression in human cells and in Zmiz2 null (Zmiz2(-/-)) mouse embryonic fibroblasts (MEFs). The regulatory role of Zmiz2 in Wnt-induced TCF/β-catenin-mediated transcription can be restored in Zmiz2(-/-) MEFs that were infected with adenoviral expression vectors for Zmiz2. Moreover, enhancement of Zmiz2 on TCF/β-catenin-mediated transcription was further demonstrated in Zmiz2 knockout and Axin2 reporter compound mice. Furthermore, the protein-protein interaction between ZMIZ2 and β-catenin was identified by co-immunoprecipitation and in vitro protein pulldown assays. We also observed recruitment of endogenous ZMIZ2 onto the promoter region of the Axin 2 gene, a β-catenin downstream target promoter, in a Wnt ligand-inducible manner. Finally, a promotional role of ZMIZ2 on cell growth was demonstrated in human cell lines and Zmiz2 knockout MEFs. Our findings demonstrate a novel interaction between ZMIZ2 and β-catenin and elucidate a novel mechanism for PIAS-like proteins in regulating Wnt signaling pathways.

Keywords: Cell Signaling; PIAS-like Proteins; Protein-Protein Interactions; Transcription Regulation; Wnt Ligand; Wnt Signaling; ZMIZ2; β-Catenin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Axin Protein / genetics
  • Cell Line
  • Cell Proliferation
  • Female
  • Gene Expression Regulation
  • Gene Knockdown Techniques
  • Humans
  • Hyaluronan Receptors / metabolism
  • Intracellular Signaling Peptides and Proteins / deficiency
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Mice
  • Promoter Regions, Genetic / genetics
  • Protein Inhibitors of Activated STAT
  • Signal Transduction*
  • TCF Transcription Factors / metabolism
  • Transcription, Genetic
  • Wnt Proteins / metabolism*
  • beta Catenin / metabolism*

Substances

  • Axin Protein
  • Axin2 protein, mouse
  • Hyaluronan Receptors
  • Intracellular Signaling Peptides and Proteins
  • Protein Inhibitors of Activated STAT
  • TCF Transcription Factors
  • Wnt Proteins
  • Zimp7 protein, mouse
  • beta Catenin
  • JNK Mitogen-Activated Protein Kinases