The effect of non-steroidal anti-inflammatory agents on behavioural changes and cytokine production following systemic inflammation: Implications for a role of COX-1

Brain Behav Immun. 2010 Mar;24(3):409-19. doi: 10.1016/j.bbi.2009.11.006. Epub 2009 Dec 4.

Abstract

Systemic inflammation gives rise to metabolic and behavioural changes, largely mediated by pro-inflammatory cytokines and prostaglandin production (PGE(2)) at the blood-brain barrier. Despite numerous studies, the exact biological pathways that give rise to these changes remains elusive. This study investigated the mechanisms underlying immune-to-brain communication following systemic inflammation using various anti-inflammatory agents. Mice were pre-treated with selective cyclo-oxygenase (COX) inhibitors, thromboxane synthase inhibitors or dexamethasone, followed by intra-peritoneal injection of lipopolysaccharide (LPS). Changes in body temperature, open-field activity, and burrowing were assessed and mRNA and/or protein levels of inflammatory mediators measured in serum and brain. LPS-induced systemic inflammation resulted in behavioural changes and increased production of IL-6, IL-1beta and TNF-alpha, as well as PGE(2) in serum and brain. Indomethacin and ibuprofen reversed the effect of LPS on behaviour without changing peripheral or central IL-6, IL-1beta and TNF-alpha mRNA levels. In contrast, dexamethasone did not alter LPS-induced behavioural changes, despite complete inhibition of cytokine production. A selective COX-1 inhibitor, piroxicam, but not the selective COX-2 inhibitor, nimesulide, reversed the LPS-induced behavioural changes without affecting IL-6, IL-1beta and TNF-alpha protein expression levels in the periphery or mRNA levels in the hippocampus. Our results suggest that the acute LPS-induced changes in burrowing and open-field activity depend on COX-1. We further show that COX-1 is not responsible for the induction of brain IL-6, IL-1beta and TNF-alpha synthesis or LPS-induced hypothermia. Our results may have implications for novel therapeutic strategies to treat or prevent neurological diseases with an inflammatory component.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology*
  • Behavior, Animal / drug effects*
  • Body Temperature / drug effects
  • Brain Chemistry / drug effects
  • Cyclooxygenase 1 / physiology*
  • Cyclooxygenase 2 / physiology
  • Cyclooxygenase Inhibitors / pharmacology
  • Cytokines / biosynthesis*
  • Cytokines / blood
  • Dinoprostone / biosynthesis
  • Dinoprostone / physiology
  • Female
  • Inflammation / drug therapy*
  • Inflammation / enzymology
  • Inflammation / psychology*
  • Kinetics
  • Lipopolysaccharides / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Motor Activity / drug effects
  • RNA / biosynthesis
  • RNA / isolation & purification
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • Cyclooxygenase Inhibitors
  • Cytokines
  • Lipopolysaccharides
  • RNA
  • Cyclooxygenase 1
  • Cyclooxygenase 2
  • Dinoprostone