MEK-ERK signaling controls Hdm2 oncoprotein expression by regulating hdm2 mRNA export to the cytoplasm

J Biol Chem. 2005 Apr 29;280(17):16651-8. doi: 10.1074/jbc.M412334200. Epub 2005 Feb 21.

Abstract

The physical and functional interaction between the transcription factor p53 and its negative regulatory partner protein Hdm2 (Mdm2 in mouse) is a key point of convergence of multiple signaling pathways that regulates cell proliferation and survival. hdm2 mRNA transcription is induced by p53, forming the basis of an auto-regulatory feedback loop. Growth and survival factor-activated Ras-Raf-MEK-ERK signaling can also regulate Hdm2 expression independently of p53, contributing to the pro-survival effect of these factors. In murine fibroblasts, this occurs through the regulation of mdm2 mRNA transcription. Here we show that, in human breast cancer epithelial cells, MEK-dependent regulation of Hdm2 expression also occurs at a post-transcriptional level. Pharmacological blockade of MEK activity in T47D cells inhibits Hdm2 protein synthesis by 80-90%. This occurs in the absence of changes in the expression of the major hdm2-P1 mRNA transcript and only an approximately 40% reduction in hdm2-P2 transcript levels. The amounts of both transcripts that are associated with polyribosomes and are, hence, being actively translated are reduced by >80% by the MEK inhibitor, U0126. We show here that this is due to the inhibition of hdm2 mRNA export from the nucleus when MEK activity is inhibited. In MCF-7 breast cancer cells that express wild-type p53, Hdm2 is required to suppress p53-dependent transcription when MEK kinase is active. Regulation of the nuclear export of hdm2 mRNA provides, therefore, a mechanism whereby mitogen-stimulated cells avoid p53-dependent cell cycle arrest or apoptosis by maintaining the dynamic equilibrium of the Hdm2-p53 feedback loop.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • Butadienes / pharmacology
  • Cell Cycle
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Cell Proliferation
  • Cell Survival
  • Cytoplasm / metabolism
  • Enzyme Inhibitors / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Gene Expression Regulation, Neoplastic*
  • Genes, Reporter
  • Humans
  • In Situ Hybridization
  • Mitogen-Activated Protein Kinase Kinases / metabolism*
  • Mitogen-Activated Protein Kinase Kinases / physiology*
  • Models, Biological
  • Nitriles / pharmacology
  • Nuclear Proteins / biosynthesis*
  • Nuclear Proteins / metabolism*
  • Nuclear Proteins / physiology*
  • Plasmids / metabolism
  • Protein Binding
  • Protein Transport
  • Proto-Oncogene Proteins / biosynthesis*
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins / physiology*
  • Proto-Oncogene Proteins c-mdm2
  • RNA / metabolism
  • RNA Processing, Post-Transcriptional
  • RNA, Messenger / metabolism
  • Time Factors
  • Transcription, Genetic
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Butadienes
  • Enzyme Inhibitors
  • Nitriles
  • Nuclear Proteins
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Tumor Suppressor Protein p53
  • U 0126
  • RNA
  • MDM2 protein, human
  • Proto-Oncogene Proteins c-mdm2
  • Extracellular Signal-Regulated MAP Kinases
  • Mitogen-Activated Protein Kinase Kinases