A molecular mechanism for angiotensin II receptor blocker-mediated slit membrane protection: Angiotensin II increases nephrin endocytosis via AT1-receptor-dependent ERK 1/2 activation

FASEB J. 2024 Sep 15;38(17):e70018. doi: 10.1096/fj.202400369R.

Abstract

Albuminuria is characterized by a disruption of the glomerular filtration barrier, which is composed of the fenestrated endothelium, the glomerular basement membrane, and the slit diaphragm. Nephrin is a major component of the slit diaphragm. Apart from hemodynamic effects, Ang II enhances albuminuria by β-Arrestin2-mediated nephrin endocytosis. Blocking the AT1 receptor with candesartan and irbesartan reduces the Ang II-mediated nephrin-β-Arrestin2 interaction. The inhibition of MAPK ERK 1/2 blocks Ang II-enhanced nephrin-β-Arrestin2 binding. ERK 1/2 signaling, which follows AT1 receptor activation, is mediated by G-protein signaling, EGFR transactivation, and β-Arrestin2 recruitment. A mutant AT1 receptor defective in EGFR transactivation and β-Arrestin2 recruitment reduces the Ang II-mediated increase in nephrin β-Arrestin2 binding. The mutation of β-Arrestin2K11,K12, critical for AT1 receptor binding, completely abrogates the interaction with nephrin, independent of Ang II stimulation. β-Arrestin2K11R,K12R does not influence nephrin cell surface expression. The data presented here deepen our molecular understanding of a blood-pressure-independent molecular mechanism of AT-1 receptor blockers (ARBs) in reducing albuminuria.

Keywords: angiotensin; arrestin; endocytosis; extracellular‐signal‐regulated kinase (ERK); nephrin; podocyte.

MeSH terms

  • Albuminuria / metabolism
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Angiotensin II* / metabolism
  • Angiotensin II* / pharmacology
  • Animals
  • Benzimidazoles
  • Biphenyl Compounds / pharmacology
  • Endocytosis* / drug effects
  • Endocytosis* / physiology
  • HEK293 Cells
  • Humans
  • Irbesartan / pharmacology
  • MAP Kinase Signaling System / drug effects
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Mice
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Podocytes / drug effects
  • Podocytes / metabolism
  • Receptor, Angiotensin, Type 1* / genetics
  • Receptor, Angiotensin, Type 1* / metabolism
  • Tetrazoles
  • beta-Arrestin 2 / genetics
  • beta-Arrestin 2 / metabolism

Substances

  • nephrin
  • Membrane Proteins
  • Angiotensin II
  • Receptor, Angiotensin, Type 1
  • Angiotensin II Type 1 Receptor Blockers
  • Mitogen-Activated Protein Kinase 3
  • Biphenyl Compounds
  • Irbesartan
  • candesartan
  • beta-Arrestin 2
  • Benzimidazoles
  • Tetrazoles