Attenuated desensitization of β-adrenergic receptor by water-soluble N-nitrosamines that induce S-nitrosylation without NO release

Circ Res. 2013 Jan 18;112(2):327-34. doi: 10.1161/CIRCRESAHA.112.277665. Epub 2012 Dec 4.

Abstract

Rationale: The clinical problem of loss of β-adrenergic receptor (β-AR) response, both in the pathogenesis of heart failure and during therapeutic application of β-agonists, is attributable, at least in part, to desensitization, internalization, and downregulation of the receptors. In the regulation of β-AR signaling, G protein-coupled receptor kinase 2 (GRK2) primarily phosphorylates agonist-occupied β-ARs, and this modification promotes desensitization, internalization, and downregulation of β-ARs. It has been demonstrated that GRK2 is inhibited by its S-nitrosylation. However, compounds that induce S-nitrosylation, such as S-nitrosoglutathione, simultaneously generate NO, which has been demonstrated to operate for cardiovascular protection.

Objective: We examine whether S-nitrosylation without NO generation inhibits desensitization of β(2)-AR by GRK2. We thus aim to synthesize compounds that specifically induce S-nitrosylation.

Methods and results: We have developed water-soluble N-nitrosamines that have S-nitrosylating activity but lack NO-generating activity. These compounds, at least partly, rescue β-AR from desensitization in HEK 293 cells expressing FLAG-tagged human β(2)-AR and in rat cardiac myocytes. They inhibit isoproterenol-dependent phosphorylation and internalization of β(2)-AR. Indeed, they nitrosylate GRK2 in vitro and in cells, and their S-nitrosylation of GRK2 likely underlies their inhibition of β(2)-AR desensitization.

Conclusions: Compounds that induce S-nitrosylation without NO release inhibit GRK2 and attenuate β(2)-AR desensitization. Developing water-soluble drugs that specifically induce S-nitrosylation may be a promising therapeutic strategy for heart failure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • HEK293 Cells
  • Humans
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Nitric Oxide* / metabolism
  • Nitrosamines / chemistry
  • Nitrosamines / metabolism*
  • Nitrosamines / pharmacology*
  • Rats
  • Receptors, Adrenergic, beta-2 / metabolism*
  • Solubility / drug effects
  • Water / chemistry
  • Water / physiology*

Substances

  • Nitrosamines
  • Receptors, Adrenergic, beta-2
  • Water
  • Nitric Oxide