Wnt signaling promotes oncogenic transformation by inhibiting c-Myc-induced apoptosis

J Cell Biol. 2002 Apr 29;157(3):429-40. doi: 10.1083/jcb.200201110. Epub 2002 Apr 29.

Abstract

Aberrant activation of the Wnt/beta-catenin signaling pathway is associated with numerous human cancers and often correlates with the overexpression or amplification of the c-myc oncogene. Paradoxical to the cellular transformation potential of c-Myc is its ability to also induce apoptosis. Using an inducible c-MycER expression system, we found that Wnt/beta-catenin signaling suppressed apoptosis by inhibiting c-Myc-induced release of cytochrome c and caspase activation. Both cyclooxygenase 2 and WISP-1 were identified as effectors of the Wnt-mediated antiapoptotic signal. Soft agar assays showed that neither c-Myc nor Wnt-1 alone was sufficient to induce cellular transformation, but that Wnt and c-Myc coordinated in inducing transformation. Furthermore, coexpression of Wnt-1 and c-Myc induced high-frequency and rapid tumor growth in nude mice. Extensive apoptotic bodies were characteristic of c-Myc-induced tumors, but not tumors induced by coactivation of c-Myc and Wnt-1, indicating that the antiapoptotic function of Wnt-1 plays a critical role in the synergetic action between c-Myc and Wnt-1. These results elucidate the molecular mechanisms by which Wnt/beta-catenin inhibits apoptosis and provide new insight into Wnt signaling-mediated oncogenesis.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis* / genetics
  • CCN Intercellular Signaling Proteins
  • Caspase Inhibitors
  • Caspases / metabolism
  • Cell Line
  • Cell Transformation, Neoplastic*
  • Cyclooxygenase 2
  • Cytochrome c Group / metabolism
  • Enzyme Activation
  • Gene Expression Regulation, Neoplastic
  • Growth Substances
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes / metabolism
  • Membrane Proteins
  • Oncogene Proteins
  • Prostaglandin-Endoperoxide Synthases / metabolism
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-myc / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-myc / metabolism
  • Rats
  • Signal Transduction*
  • Wnt Proteins
  • Wnt1 Protein
  • Zebrafish Proteins*

Substances

  • CCN Intercellular Signaling Proteins
  • CCN4 protein, human
  • CCN4 protein, rat
  • Caspase Inhibitors
  • Cytochrome c Group
  • Growth Substances
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes
  • Membrane Proteins
  • Oncogene Proteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-myc
  • WNT1 protein, human
  • Wnt Proteins
  • Wnt1 Protein
  • Wnt1 protein, rat
  • Zebrafish Proteins
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Prostaglandin-Endoperoxide Synthases
  • Caspases