Direct GPCR-EGFR interaction enables synergistic membrane-to-nucleus information transfer

Cell Mol Life Sci. 2024 Jun 20;81(1):272. doi: 10.1007/s00018-024-05281-5.

Abstract

We addressed the heteromerization of the epidermal growth factor receptor (EGFR) with G-protein coupled receptors (GPCR) on the basis of angiotensin-II-receptor-subtype-1(AT1R)-EGFR interaction as proof-of-concept and show its functional relevance during synergistic nuclear information transfer, beyond ligand-dependent EGFR transactivation. Following in silico modelling, we generated EGFR-interaction deficient AT1R-mutants and compared them to AT1R-wildtype. Receptor interaction was assessed by co-immunoprecipitation (CoIP), Förster resonance energy transfer (FRET) and fluorescence-lifetime imaging microscopy (FLIM). Changes in cell morphology, ERK1/2-phosphorylation (ppERK1/2), serum response factor (SRF)-activation and cFOS protein expression were determined by digital high content microscopy at the single cell level. FRET, FLIM and CoIP confirmed the physical interaction of AT1R-wildtype with EGFR that was strongly reduced for the AT1R-mutants. Responsiveness of cells transfected with AT1R-WT or -mutants to angiotensin II or EGF was similar regarding changes in cell circularity, ppERK1/2 (direct and by ligand-dependent EGFR-transactivation), cFOS-expression and SRF-activity. By contrast, the EGFR-AT1R-synergism regarding these parameters was completely absent for in the interaction-deficient AT1R mutants. The results show that AT1R-EGFR heteromerisation enables AT1R-EGFR-synergism on downstream gene expression regulation, modulating the intensity and the temporal pattern of nuclear AT1R/EGFR-information transfer. Furthermore, remote EGFR transactivation, via ligand release or cytosolic tyrosine kinases, is not sufficient for the complete synergistic control of gene expression.

Keywords: AT1R; Angiotensin II receptor type 1; EGFR; Epidermal growth factor receptor; Heteromerizsation; Serum response factor.

MeSH terms

  • Angiotensin II / metabolism
  • Angiotensin II / pharmacology
  • Cell Membrane / metabolism
  • Cell Nucleus* / metabolism
  • Epidermal Growth Factor / metabolism
  • ErbB Receptors* / metabolism
  • Fluorescence Resonance Energy Transfer
  • HEK293 Cells
  • Humans
  • Phosphorylation
  • Protein Binding
  • Receptor, Angiotensin, Type 1* / genetics
  • Receptor, Angiotensin, Type 1* / metabolism
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism
  • Serum Response Factor / genetics
  • Serum Response Factor / metabolism

Substances

  • ErbB Receptors
  • Receptor, Angiotensin, Type 1
  • EGFR protein, human
  • Receptors, G-Protein-Coupled
  • Angiotensin II
  • Epidermal Growth Factor
  • Serum Response Factor