The β-lactam clavulanic acid mediates glutamate transport-sensitive pain relief in a rat model of neuropathic pain

Eur J Pain. 2018 Feb;22(2):282-294. doi: 10.1002/ejp.1117. Epub 2017 Oct 6.

Abstract

Background: Following nerve injury, down-regulation of astroglial glutamate transporters (GluTs) with subsequent extracellular glutamate accumulation is a key factor contributing to hyperexcitability within the spinal dorsal horn. Some β-lactam antibiotics can up-regulate GluTs, one of which, ceftriaxone, displays analgesic effects in rodent chronic pain models.

Methods: Here, the antinociceptive actions of another β-lactam clavulanic acid, which possesses negligible antibiotic activity, were compared with ceftriaxone in rats with chronic constriction injury (CCI)-induced neuropathic pain. In addition, the protein expression of glutamate transporter-1 (GLT1), its splice variant GLT1b and glutamate-aspartate transporter (GLAST) was measured in the spinal cord of CCI rats. Finally, protein expression of the same GluTs was evaluated in cultured astrocytes obtained from rodents and humans.

Results: Repeated injection of ceftriaxone or clavulanic acid over 10 days alleviated CCI-induced mechanical hypersensitivity, whilst clavulanic acid was additionally able to affect the thermal hypersensitivity. In addition, clavulanic acid up-regulated expression of GLT1b within the spinal cord of CCI rats, whereas ceftriaxone failed to modulate expression of any GluTs in this model. However, both clavulanic acid and ceftriaxone up-regulated GLT1 expression in rat cortical and human spinal astrocyte cultures. Furthermore, clavulanic acid increased expression of GLT1b and GLAST in rat astrocytes in a dose-dependent manner.

Conclusions: Thus, clavulanic acid up-regulates GluTs in cultured rodent- and human astroglia and alleviates CCI-induced hypersensitivity, most likely through up-regulation of GLT1b in spinal dorsal horn.

Significance: Chronic dosing of clavulanic acid alleviates neuropathic pain in rats and up-regulates glutamate transporters both in vitro and in vivo. Crucially, a similar up-regulation of glutamate transporters in human spinal astrocytes by clavulanic acid supports the development of novel β-lactam-based analgesics, devoid of antibacterial activity, for the clinical treatment of chronic pain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics / administration & dosage
  • Analgesics / therapeutic use*
  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Ceftriaxone / administration & dosage
  • Ceftriaxone / therapeutic use*
  • Cells, Cultured
  • Clavulanic Acid / administration & dosage
  • Clavulanic Acid / therapeutic use*
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Excitatory Amino Acid Transporter 2 / metabolism*
  • Glutamic Acid / metabolism*
  • Humans
  • Male
  • Neuralgia / drug therapy*
  • Neuralgia / metabolism
  • Pain Threshold / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism
  • Up-Regulation / drug effects

Substances

  • Analgesics
  • Excitatory Amino Acid Transporter 2
  • Clavulanic Acid
  • Glutamic Acid
  • Ceftriaxone