Potentiation of transient receptor potential V1 functions by the activation of metabotropic 5-HT receptors in rat primary sensory neurons

J Physiol. 2006 Nov 1;576(Pt 3):809-22. doi: 10.1113/jphysiol.2006.112250. Epub 2006 Aug 10.

Abstract

5-Hydroxytryptamine (5-HT) is one of the major chemical mediators released in injured and inflamed tissue and is capable of inducing hyperalgesia in vivo. However, the cellular mechanisms of 5-HT-induced hyperalgesia remain unclear. Transient receptor potential V1 (TRPV1) plays a pivotal role in nociceptive receptors. In the present study, we determined whether 5-HT changes TRPV1 functions in cultured dorsal root ganglion (DRG) neurons isolated from neonatal rats, using Ca(2+) imaging and whole-cell patch-clamp techniques. In more than 70% of DRG neurons, 5-HT potentiated the increases of [Ca(2+)](i) induced by capsaicin, protons and noxious heat. Capsaicin-induced current and depolarizing responses, and proton-induced currents were also augmented by 5-HT. RT-PCR analysis revealed the expression of 5-HT(2A) and 5-HT(7) receptors in rat DRG neurons. Agonists for 5-HT(2A) and 5-HT(7) receptors mimicked the potentiating effect of 5-HT, and their antagonists decreased it. In DRG ipsilateral to the complete Freund's adjuvant-injected inflammation side, expression levels of 5-HT(2A) and 5-HT(7) mRNAs increased, and the potentiating effect of 5-HT was more prominent than in the contralateral control side. These results suggest that the PKC- and PKA-mediated signalling pathways are involved in the potentiating effect of 5-HT on TRPV1 functions through the activation of 5-HT(2A) and 5-HT(7) receptors, respectively. Under inflammatory conditions, the increases of the biosynthesis of these 5-HT receptors may lead to further potentiation of TRPV1 functions, resulting in the generation of inflammatory hyperalgesia in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics, Non-Narcotic / pharmacology
  • Animals
  • Capsaicin / pharmacology
  • Cells, Cultured
  • Female
  • Gene Expression Regulation
  • Hyperalgesia / physiopathology
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Neurons, Afferent / cytology
  • Neurons, Afferent / physiology*
  • Patch-Clamp Techniques
  • Protein Kinases / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Wistar
  • Receptor, Serotonin, 5-HT2A / genetics
  • Receptor, Serotonin, 5-HT2A / physiology*
  • Receptors, Serotonin / genetics
  • Receptors, Serotonin / physiology*
  • Second Messenger Systems / physiology*
  • Serotonin / pharmacology
  • Serotonin Agents / pharmacology
  • Synapses / physiology
  • TRPV Cation Channels / drug effects
  • TRPV Cation Channels / physiology*

Substances

  • Analgesics, Non-Narcotic
  • RNA, Messenger
  • Receptor, Serotonin, 5-HT2A
  • Receptors, Serotonin
  • Serotonin Agents
  • TRPV Cation Channels
  • Trpv1 protein, rat
  • serotonin 7 receptor
  • Serotonin
  • Protein Kinases
  • Capsaicin