G protein-coupled receptor-mediated mitogen-activated protein kinase activation through cooperation of Galpha(q) and Galpha(i) signals

Mol Cell Biol. 2000 Sep;20(18):6837-48. doi: 10.1128/MCB.20.18.6837-6848.2000.

Abstract

G protein-coupled receptors (GPCRs) have been shown to stimulate extracellular regulated kinases (ERKs) through a number of linear pathways that are initiated by G(q/11) or G(i) proteins. We studied signaling to the ERK cascade by receptors that simultaneously activate both G protein subfamilies. In HEK293T cells, bradykinin B(2) receptor (B(2)R)-induced stimulation of ERK2 and transcriptional activity of Elk1 are dependent on Galpha(q)-mediated protein kinase C (PKC) and on Galpha(i)-induced Ras activation, while they are independent of Gbetagamma subunits, phosphatidylinositol 3-kinase, and tyrosine kinases. Similar results were obtained with m(1) and m(3) muscarinic receptors in HEK293T cells and with the B(2)R in human and mouse fibroblasts, indicating a general mechanism in signaling toward the ERK cascade. Furthermore, the bradykinin-induced activation of ERK is strongly reduced in Galpha(q/11)-deficient fibroblasts. In addition, we found that constitutively active mutants of Galpha(q/11) or Galpha(i) proteins alone poorly stimulate ERK2, whereas a combination of both led to synergistic effects. We conclude that dually coupled GPCRs require a cooperation of Galpha(i)- and G(q/11)-mediated pathways for efficient stimulation of the ERK cascade. Cooperative signaling by multiple G proteins thus might represent a novel concept implicated in the regulation of cellular responses by GPCRs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cell Line, Transformed
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • DNA-Binding Proteins*
  • Enzyme Activation
  • GTP-Binding Protein alpha Subunits, Gi-Go / genetics
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism*
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • GTP-Binding Protein beta Subunits*
  • GTP-Binding Protein gamma Subunits*
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism*
  • Heterotrimeric GTP-Binding Proteins*
  • Humans
  • MAP Kinase Signaling System*
  • Mice
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinases / genetics
  • Mitogen-Activated Protein Kinases / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Potassium Channels / genetics
  • Protein Kinase C / metabolism
  • Proto-Oncogene Proteins c-raf / metabolism
  • Proto-Oncogene Proteins*
  • Receptor, Bradykinin B2
  • Receptor, Muscarinic M1
  • Receptor, Muscarinic M3
  • Receptors, Bradykinin / metabolism
  • Receptors, Cell Surface / metabolism
  • Receptors, Muscarinic / metabolism
  • Transcription Factors*
  • Transcriptional Activation
  • Virulence Factors, Bordetella / pharmacology
  • beta-Adrenergic Receptor Kinases
  • ets-Domain Protein Elk-1
  • ras Proteins / metabolism

Substances

  • DNA-Binding Proteins
  • ELK1 protein, human
  • Elk1 protein, mouse
  • G-protein Beta gamma
  • GTP-Binding Protein beta Subunits
  • GTP-Binding Protein gamma Subunits
  • Potassium Channels
  • Proto-Oncogene Proteins
  • Receptor, Bradykinin B2
  • Receptor, Muscarinic M1
  • Receptor, Muscarinic M3
  • Receptors, Bradykinin
  • Receptors, Cell Surface
  • Receptors, Muscarinic
  • Transcription Factors
  • Virulence Factors, Bordetella
  • ets-Domain Protein Elk-1
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-raf
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C
  • beta-Adrenergic Receptor Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinases
  • GTP-Binding Proteins
  • GTP-Binding Protein alpha Subunits, Gi-Go
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • Heterotrimeric GTP-Binding Proteins
  • ras Proteins