Direct binding of the beta1 adrenergic receptor to the cyclic AMP-dependent guanine nucleotide exchange factor CNrasGEF leads to Ras activation

Mol Cell Biol. 2002 Nov;22(22):7942-52. doi: 10.1128/MCB.22.22.7942-7952.2002.

Abstract

G-protein-coupled receptors (GPCRs) can indirectly activate Ras primarily through the betagamma subunits of G proteins, which recruit c-Src, phosphatidylinositol 3-kinase, and Grb2-SOS. However, a direct interaction between a Ras activator (guanine nucleotide exchange factor [GEF]) and GPCRs that leads to Ras activation has never been demonstrated. We report here a novel mechanism for a direct GPCR-mediated Ras activation. The beta1 adrenergic receptor (beta1-AR) binds to the PDZ domain of the cyclic AMP (cAMP)-dependent Ras exchange factor, CNrasGEF, via its C-terminal SkV motif. In cells heterologously expressing beta1-AR and CNrasGEF, Ras is activated by the beta1-AR agonist isoproterenol, and this activation is abolished in beta1-AR mutants that cannot bind CNrasGEF or in CNrasGEF mutants lacking the catalytic CDC25 domain or cAMP-binding domain. Moreover, the activation is transduced via Gsalpha and not via Gbetagamma. In contrast to beta1-AR, the beta2-AR neither binds CNrasGEF nor activates Ras via CNrasGEF after agonist stimulation. These results suggest a model whereby the physical interaction between the beta1-AR and CNrasGEF facilitates the transduction of Gsalpha-induced cAMP signal into the activation of Ras. The present study provides the first demonstration of direct physical association between a Ras activator and a GPCR, leading to agonist-induced Ras activation

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cyclic AMP / metabolism
  • GTP-Binding Protein alpha Subunits, Gs / metabolism
  • Green Fluorescent Proteins
  • Guanine Nucleotide Exchange Factors / metabolism*
  • Humans
  • Ligands
  • Luminescent Proteins / metabolism
  • Models, Biological
  • Nerve Tissue Proteins*
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein Subunits
  • Rats
  • Receptors, Adrenergic, beta-1 / genetics
  • Receptors, Adrenergic, beta-1 / metabolism*
  • Receptors, Adrenergic, beta-2 / genetics
  • Receptors, Adrenergic, beta-2 / metabolism
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Swine
  • ras Proteins / metabolism*

Substances

  • Guanine Nucleotide Exchange Factors
  • Ligands
  • Luminescent Proteins
  • Nerve Tissue Proteins
  • Protein Subunits
  • RAPGEF2 protein, human
  • Receptors, Adrenergic, beta-1
  • Receptors, Adrenergic, beta-2
  • Recombinant Fusion Proteins
  • Green Fluorescent Proteins
  • Cyclic AMP
  • GTP-Binding Protein alpha Subunits, Gs
  • ras Proteins