Mechanisms of GTN-induced migraine: Role of NOS isoforms, sGC and peroxynitrite in a migraine relevant mouse model

Cephalalgia. 2024 Sep;44(9):3331024241277542. doi: 10.1177/03331024241277542.

Abstract

Background: Migraine research has highlighted the pivotal role of nitric oxide (NO) in migraine pathophysiology. Nitric oxide donors such as glyceryl trinitrate (GTN) induce migraine attacks in humans, whereas spontaneous migraine attacks can be aborted by inhibiting NO production. The present study aimed to investigate how GTN triggers migraine through its three nitric oxide synthase (NOS) isoforms (neuronal NOS (nNOS), endothelial NOS (eNOS) and inducible NOS (iNOS)) via a suspected feed-forward phenomenon.

Methods: Migraine-relevant hypersensitivity was induced by repeated injection of GTN in an in vivo mouse model. Cutaneous tactile sensitivity was assessed using von Frey filaments. Signaling pathways involved in this model were dissected using non-selective and selective NOS inhibitors, knockout mice lacking eNOS or nNOS and their wild-type control mice. Also, we tested a soluble guanylate cyclase inhibitor and a peroxynitrite decomposition catalyst (Ntotal = 312).

Results: Non-selective NOS inhibition blocked GTN-induced hypersensitivity. This response was partially associated with iNOS, and potentially nNOS and eNOS conjointly. Furthermore, we found that the GTN response was largely dependent on the generation of peroxynitrite and partly soluble guanylate cyclase.

Conclusions: Migraine-relevant hypersensitivity induced by GTN is mediated by a possible feed-forward phenomenon of NO driven mainly by iNOS but with contributions from other isoforms. The involvement of peroxynitrite adds to the notion that oxidative stress reactions are also involved.

Keywords: GTN; NOS; migraine signaling; mouse model; nitric oxide; peroxynitrate; von Frey.

MeSH terms

  • Animals
  • Disease Models, Animal*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Migraine Disorders* / chemically induced
  • Migraine Disorders* / metabolism
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Nitric Oxide Synthase Type I / metabolism
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Nitroglycerin* / pharmacology
  • Nitroglycerin* / toxicity
  • Peroxynitrous Acid* / metabolism
  • Soluble Guanylyl Cyclase / metabolism

Substances

  • Nitroglycerin
  • Peroxynitrous Acid
  • Soluble Guanylyl Cyclase
  • Nitric Oxide Synthase Type I
  • Nitric Oxide Synthase Type III
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II