MEK1-RSK2 contributes to Hedgehog signaling by stabilizing GLI2 transcription factor and inhibiting ubiquitination

Oncogene. 2014 Jan 2;33(1):65-73. doi: 10.1038/onc.2012.544. Epub 2012 Dec 3.

Abstract

The transcription factor GLI2 has an important role in the transduction of Hedgehog signaling and thereby regulates tumorigenesis in a wide variety of human tumors. However, the mechanisms controlling GLI2 protein expression and stabilization are incompletely understood. In this study, we show that the mitogen-activated protein kinase MEK1 modulates GLI2 both at the mRNA and protein level. Constitutively activated MEK1 prolonged the half-life of GLI2 and increased its nuclear translocation, accompanied by attenuated ubiquitination of GLI2 protein. RSK2, a protein kinase lying downstream of MEK-ERK cascade, mimicked the effect of MEK on GLI2 stabilization. MEK1 and RSK2 failed to augment the half-life of GLI2 lacking GSK-3β phosphorylation sites, indicating that MEK-RSK stabilizes GLI2 by controlling targeting GSK-3β-mediated phosphorylation and ubiquitination of GLI2. The significance of MEK-RSK stabilization was demonstrated in experiments showing that activation of MEK-RSK paralleled higher protein level of GLI2 in several multiple myelomas (MM) cells relative to normal B cells. Moreover, combined treatment with RSK and GLI inhibitors led to an enhanced apoptosis of MM cells. Thus, our results indicate that MEK-RSK cascade positively regulates GLI2 stabilization and represses its degradation via inhibiting GSK-3β-dependent phosphorylation and ubiquitination of GLI2.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Apoptosis
  • Cell Line, Tumor
  • Gene Expression
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • HEK293 Cells
  • Half-Life
  • Hedgehog Proteins / metabolism*
  • Humans
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism*
  • MAP Kinase Kinase 1 / metabolism*
  • MAP Kinase Signaling System
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphorylation
  • Protein Stability
  • Proteolysis
  • Ribosomal Protein S6 Kinases, 90-kDa / metabolism*
  • Ubiquitination*
  • Up-Regulation
  • Zinc Finger Protein Gli2

Substances

  • GLI2 protein, human
  • Hedgehog Proteins
  • Kruppel-Like Transcription Factors
  • Nuclear Proteins
  • Zinc Finger Protein Gli2
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Ribosomal Protein S6 Kinases, 90-kDa
  • ribosomal protein S6 kinase, 90kDa, polypeptide 3
  • Glycogen Synthase Kinase 3
  • MAP Kinase Kinase 1
  • MAP2K1 protein, human