BRET-based assay to monitor EGFR transactivation by the AT1R reveals Gq/11 protein-independent activation and AT1R-EGFR complexes

Biochem Pharmacol. 2018 Dec:158:232-242. doi: 10.1016/j.bcp.2018.10.017. Epub 2018 Oct 19.

Abstract

The type 1 angiotensin II (AngII) receptor (AT1R) transactivates the epidermal growth factor receptor (EGFR), which leads to pathological remodeling of heart, blood vessels and kidney. End-point assays are used as surrogates of EGFR activation, however these downstream readouts are not applicable to live cells, in real-time. Herein, we report the use of a bioluminescence resonance energy transfer (BRET)-based assay to assess recruitment of the EGFR adaptor protein, growth factor receptor-bound protein 2 (Grb2), to the EGFR. In a variety of cell lines, both epidermal growth factor (EGF) and AngII stimulated Grb2 recruitment to EGFR. The BRET assay was used to screen a panel of 9 G protein-coupled receptors (GPCRs) and further developed for other EGFR family members (HER2 and HER3); the AT1R was able to transactivate HER2, but not HER3. Mechanistically, AT1R-mediated ERK1/2 activation was dependent on Gq/11 and EGFR tyrosine kinase activity, whereas the recruitment of Grb2 to the EGFR was independent of Gq/11 and only partially dependent on EGFR tyrosine kinase activity. This Gq/11 independence of EGFR transactivation was confirmed using AT1R mutants and in CRISPR cell lines lacking Gq/11. EGFR transactivation was also apparently independent of β-arrestins. Finally, we used additional BRET-based assays and confocal microscopy to provide evidence that both AngII- and EGF-stimulation promoted AT1R-EGFR heteromerization. In summary, we report an alternative approach to monitoring AT1R-EGFR transactivation in live cells, which provides a more direct and proximal view of this process, including the potential for complexes between the AT1R and EGFR.

Keywords: Angiotensin II; Bioluminescence resonance energy transfer; EGFR transactivation; Epidermal growth factor receptor; G protein-coupled receptor; Receptor heteromerization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bioluminescence Resonance Energy Transfer Techniques / methods*
  • CHO Cells
  • Cricetulus
  • ErbB Receptors / analysis
  • ErbB Receptors / metabolism
  • GTP-Binding Protein alpha Subunits, Gq-G11 / analysis
  • GTP-Binding Protein alpha Subunits, Gq-G11 / metabolism*
  • HEK293 Cells
  • Humans
  • Male
  • Mice
  • NIH 3T3 Cells
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Angiotensin, Type 1 / analysis
  • Receptor, Angiotensin, Type 1 / metabolism*
  • Transcriptional Activation / physiology*

Substances

  • Receptor, Angiotensin, Type 1
  • EGFR protein, human
  • ErbB Receptors
  • GTP-Binding Protein alpha Subunits, Gq-G11