Signal integration and coincidence detection in the mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) cascade: concomitant activation of receptor tyrosine kinases and of LRP-1 leads to sustained ERK phosphorylation via down-regulation of dual specificity phosphatases (DUSP1 and -6)

J Biol Chem. 2011 Jul 22;286(29):25663-74. doi: 10.1074/jbc.M111.221903. Epub 2011 May 24.

Abstract

Diverse stimuli can feed into the MAPK/ERK cascade; this includes receptor tyrosine kinases, G protein-coupled receptors, integrins, and scavenger receptors (LDL receptor-related protein (LRP)). Here, we investigated the consequence of concomitant occupancy of the receptor tyrosine kinases (by EGF, basic FGF, VEGF, etc.) and of LRP family members (by LDL or lactoferrin). The simultaneous stimulation of a receptor tyrosine kinase by its cognate ligand and of LRP-1 (by lactoferrin or LDL) resulted in sustained activation of ERK, which was redirected to the cytoplasm. Accordingly, elevated levels of active cytosolic ERK were translated into accelerated adhesion to vitronectin. The sustained ERK response was seen in several cell types, but it was absent in cells deficient in LRP-1 (but not in cells lacking the LDL receptor). This response was also contingent on the presence of urokinase (uPA) and its receptor (uPAR), because it was absent in uPA(-/-) and uPAR(-/-) fibroblasts. Combined stimulation of the EGF receptor and of LRP-1 delayed nuclear accumulation of phosphorylated ERK. This shift in favor of cytosolic accumulation of phospho-ERK was accounted for by enhanced proteasomal degradation of dual specificity phosphatases DUSP1 and DUSP6, which precluded dephosphorylation of cytosolic ERK. These observations demonstrate that the ERK cascade can act as a coincidence detector to decode the simultaneous engagement of a receptor tyrosine kinase and of LRP-1 and as a signal integrator that encodes this information in a spatially and temporally distinct biological signal. In addition, the findings provide an explanation of why chronic elevation of LRP-1 ligands (e.g. PAI-1) can predispose to cancer.

Publication types

  • Research Support, Non-U.S. Gov't
  • Retracted Publication

MeSH terms

  • Animals
  • Cell Adhesion / drug effects
  • Cell Line, Tumor
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism
  • Down-Regulation* / drug effects
  • Dual Specificity Phosphatase 1 / metabolism*
  • Dual Specificity Phosphatase 6 / metabolism*
  • Enzyme Activation / drug effects
  • Epidermal Growth Factor / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / enzymology
  • Fibroblasts / metabolism
  • Humans
  • Lactoferrin / pharmacology
  • Ligands
  • Low Density Lipoprotein Receptor-Related Protein-1
  • MAP Kinase Signaling System* / drug effects
  • Mice
  • Phosphorylation / drug effects
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Structure, Tertiary
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Receptors, LDL / metabolism*
  • Receptors, Urokinase Plasminogen Activator / chemistry
  • Receptors, Urokinase Plasminogen Activator / metabolism
  • Time Factors
  • Tumor Suppressor Proteins / metabolism*
  • Vitronectin / metabolism

Substances

  • Ligands
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Lrp1 protein, mouse
  • Receptors, LDL
  • Receptors, Urokinase Plasminogen Activator
  • Tumor Suppressor Proteins
  • Vitronectin
  • Epidermal Growth Factor
  • Receptor Protein-Tyrosine Kinases
  • Extracellular Signal-Regulated MAP Kinases
  • Dual Specificity Phosphatase 1
  • Dual Specificity Phosphatase 6
  • Dusp1 protein, mouse
  • Dusp6 protein, mouse
  • Lactoferrin
  • Proteasome Endopeptidase Complex