Phosphorylation regulates Myc expression via prolonged activation of the mitogen-activated protein kinase pathway

J Cell Physiol. 2006 Jul;208(1):133-40. doi: 10.1002/jcp.20649.

Abstract

We previously showed that prolonged and strong ERK phosphorylation induced by Compound 5 (Cpd 5), a Cdc25A protein phosphatase inhibitor, was involved in its mechanism of cell growth inhibition. To study the relationship between ERK phosphorylation and cell growth inhibition, we used Cpd 5 as a tool to investigate ERK-regulated c-Myc expression in Hep3B hepatoma cells. We found that ERK phosphorylation caused by Cpd 5 induced c-Myc phosphorylation, but suppressed c-Myc expression at the mRNA and protein levels. Furthermore, Cpd 5 inhibited c-Myc transcriptional activity and DNA binding ability, and this inhibition was antagonized by ERK kinase (MEK) inhibitor U-0126, implying that the ERK pathway was involved in regulating c-Myc expression. Since the participation of c-Myc protein in transcription requires its dimerization with Max protein, we examined the Myc-Max association in Cpd 5-treated cells and found that Cpd 5 suppressed Myc-Max dimerization. Transfection of Hep3B cells with mutated ERK (T188A/Y190F), which has lost its dual-phosphorylation sites, attenuated the actions of Cpd 5 on Myc-Max association. To further demonstrate whether Myc phosphorylation by Cpd 5-induced ERK activation was able to directly regulate c-myc gene expression, a chromatin immunoprecipitation (ChIP) assay was used to examine the binding of phospho-Myc to the c-myc promoter region. We found that phospho-Myc induced by Cpd 5 had lost its ability to bind to the c-myc promoter, whereas MEK inhibitor U-0126 antagonized this inhibitory effect. These data suggest that an increase in c-Myc phosphorylation in response to prolonged ERK phosphorylation negatively auto-regulates c-Myc gene expression, leading to the suppression of its target gene expression and cell cycle block.

Publication types

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

MeSH terms

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / physiology
  • Blotting, Western
  • Butadienes / pharmacology
  • Carcinoma, Hepatocellular / pathology
  • Cell Cycle / genetics
  • Cell Cycle / physiology
  • Cell Cycle Proteins / analysis
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / physiology
  • Cell Line, Tumor
  • Electrophoretic Mobility Shift Assay
  • Enzyme Activation / drug effects
  • Enzyme Activation / physiology
  • Enzyme Inhibitors / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / drug effects
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / physiology*
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Expression Regulation, Neoplastic / physiology*
  • Humans
  • Immunoprecipitation
  • Liver Neoplasms / pathology
  • Nitriles / pharmacology
  • Oligonucleotide Array Sequence Analysis
  • Phosphorylation / drug effects
  • Promoter Regions, Genetic / genetics
  • Promoter Regions, Genetic / physiology
  • Protein Binding / drug effects
  • Protein Binding / physiology
  • Proto-Oncogene Proteins c-myc / genetics*
  • Proto-Oncogene Proteins c-myc / physiology*
  • RNA, Messenger / analysis
  • RNA, Messenger / genetics
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / physiology
  • Transfection
  • Vitamin K / analogs & derivatives
  • Vitamin K / pharmacology
  • cdc25 Phosphatases / analysis
  • cdc25 Phosphatases / genetics
  • cdc25 Phosphatases / physiology

Substances

  • 2-(2-hydroxyethylsulfanyl)-3-methyl-1,4-naphthoquinone
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Butadienes
  • Cell Cycle Proteins
  • Enzyme Inhibitors
  • MAX protein, human
  • Nitriles
  • Proto-Oncogene Proteins c-myc
  • RNA, Messenger
  • U 0126
  • Vitamin K
  • Extracellular Signal-Regulated MAP Kinases
  • CDC25C protein, human
  • cdc25 Phosphatases