The nitroxyl donor, Angeli's salt, inhibits inflammatory hyperalgesia in rats

Neuropharmacology. 2013 Aug:71:1-9. doi: 10.1016/j.neuropharm.2013.03.009. Epub 2013 Mar 27.

Abstract

Nitric oxide modulates pain development. However, there is no evidence on the effect of nitroxyl (HNO/NO⁻) in nociception. Therefore, we addressed whether nitroxyl inhibits inflammatory hyperalgesia and its mechanism using the nitroxyl donor Angeli's salt (AS; Na₂N₂O₃). Mechanical hyperalgesia was evaluated using a modified Randall and Selitto method in rats, cytokine production by ELISA and nitroxyl was determined by confocal microscopy in DAF (a cell permeable reagent that is converted into a fluorescent molecule by nitrogen oxides)-treated dorsal root ganglia neurons in culture. Local pre-treatment with AS (17-450 μg/paw, 30 min) inhibited the carrageenin-induced mechanical hyperalgesia in a dose- and time-dependent manner with maximum inhibition of 97%. AS also inhibited carrageenin-induced cytokine production. AS inhibited the hyperalgesia induced by other inflammatory stimuli including lipopolysaccharide, tumor necrosis factor-α, interleukin-1β and prostaglandin E2. Furthermore, the analgesic effect of AS was prevented by treatment with ODQ (a soluble guanylate cyclase inhibitor), KT5823 (a protein kinase G [PKG] inhibitor) or glybenclamide (an ATP-sensitive K⁺ channel blocker), but not with naloxone (an opioid receptor antagonist). AS induced concentration-dependent increase in fluorescence intensity of DAF-treated neurons in a l-cysteine (nitroxyl scavenger) sensitive manner. l-cysteine did not affect the NO⁺ donor S-Nitroso-N-acetyl-DL- penicillamine (SNAP)-induced anti-hyperalgesia or fluorescence of DAF-treated neurons. This is the first study to demonstrate that nitroxyl inhibits inflammatory hyperalgesia by reducing cytokine production and activating the cGMP/PKG/ATP-sensitive K⁺ channel signaling pathway in vivo.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics, Non-Narcotic / administration & dosage
  • Analgesics, Non-Narcotic / antagonists & inhibitors
  • Analgesics, Non-Narcotic / pharmacology
  • Analgesics, Non-Narcotic / therapeutic use*
  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / administration & dosage
  • Anti-Inflammatory Agents, Non-Steroidal / antagonists & inhibitors
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use*
  • Cells, Cultured
  • Cytokines / metabolism
  • Disease Models, Animal*
  • Dose-Response Relationship, Drug
  • Free Radical Scavengers / pharmacology
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / immunology
  • Ganglia, Spinal / metabolism
  • Hyperalgesia / immunology
  • Hyperalgesia / metabolism
  • Hyperalgesia / prevention & control*
  • Male
  • Neurons / cytology
  • Neurons / drug effects*
  • Neurons / immunology
  • Neurons / metabolism
  • Nitric Oxide Donors / pharmacology
  • Nitrites / administration & dosage
  • Nitrites / antagonists & inhibitors
  • Nitrites / pharmacology
  • Nitrites / therapeutic use*
  • Nitrogen Oxides / agonists*
  • Nitrogen Oxides / antagonists & inhibitors
  • Potassium Channel Blockers / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Rats
  • Rats, Wistar
  • Touch

Substances

  • Analgesics, Non-Narcotic
  • Anti-Inflammatory Agents, Non-Steroidal
  • Cytokines
  • Free Radical Scavengers
  • Nitric Oxide Donors
  • Nitrites
  • Nitrogen Oxides
  • Potassium Channel Blockers
  • Protein Kinase Inhibitors
  • oxyhyponitrite
  • nitroxyl