S-nitrosoglutathione inhibits cerebrovascular angiotensin II-dependent and -independent AT1 receptor responses: A possible role of S-nitrosation

Br J Pharmacol. 2019 Jun;176(12):2049-2062. doi: 10.1111/bph.14644. Epub 2019 May 7.

Abstract

Background and purpose: Angiotensin II (AngII) and NO regulate the cerebral circulation. AngII AT1 receptors exert ligand-dependent and ligand-independent (myogenic tone [MT]) vasoconstriction of cerebral vessels. NO induces post-translational modifications of proteins such as S-nitrosation (redox modification of cysteine residues). In cultured cells, S-nitrosation decreases AngII's affinity for the AT1 receptor. The present work evaluated the functional consequences of S-nitrosation on both AngII-dependent and AngII-independent cerebrovascular responses.

Experimental approach: S-Nitrosation was induced in rat isolated middle cerebral arteries by pretreatment with the NO donors, S-nitrosoglutathione (GSNO) or sodium nitroprusside (SNP). Agonist-dependent activation of AT1 receptors was evaluated by obtaining concentration-response curves to AngII. Ligand-independent activation of AT1 receptors was evaluated by calculating MT (active vs. passive diameter) at pressures ranging from 20 to 200 mmHg in the presence or not of a selective AT1 receptor inverse agonist.

Key results: GSNO or SNP completely abolished the AngII-dependent AT1 receptor-mediated vasoconstriction of cerebral arteries. GSNO had no impact on responses to other vasoconstrictors sharing (phenylephrine, U46619) or not (5-HT) the same signalling pathway. MT was reduced by GSNO, and the addition of losartan did not further decrease MT, suggesting that GSNO blocks AT1 receptor-dependent MT. Ascorbate (which reduces S-nitrosated compounds) restored the response to AngII but not the soluble GC inhibitor ODQ, suggesting that these effects are mediated by S-nitrosation rather than by S-nitrosylation.

Conclusions and implications: In rat middle cerebral arteries, GSNO pretreatment specifically affects the AT1 receptor and reduces both AngII-dependent and AngII-independent activation, most likely through AT1 receptor S-nitrosation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • Cerebral Arteries / drug effects*
  • Dose-Response Relationship, Drug
  • HEK293 Cells
  • Humans
  • Ligands
  • Male
  • Nitric Oxide / metabolism
  • Nitrosation / drug effects
  • Rats
  • Rats, Wistar
  • Receptor, Angiotensin, Type 1 / metabolism*
  • S-Nitrosoglutathione / administration & dosage
  • S-Nitrosoglutathione / pharmacology*
  • Signal Transduction / drug effects
  • Structure-Activity Relationship

Substances

  • Ligands
  • Receptor, Angiotensin, Type 1
  • Angiotensin II
  • Nitric Oxide
  • S-Nitrosoglutathione