Disruption of 5-HT2A receptor-PDZ protein interactions alleviates mechanical hypersensitivity in carrageenan-induced inflammation in rats

PLoS One. 2013 Sep 18;8(9):e74661. doi: 10.1371/journal.pone.0074661. eCollection 2013.

Abstract

Despite common pathophysiological mechanisms, inflammatory and neuropathic pain do not respond equally to the analgesic effect of antidepressants, except for selective serotonin reuptake inhibitors (SSRIs), which show a limited efficacy in both conditions. We previously demonstrated that an interfering peptide (TAT-2ASCV) disrupting the interaction between 5-HT2A receptors and its associated PDZ proteins (e.g. PSD-95) reveals a 5-HT2A receptor-mediated anti-hyperalgesic effect and enhances the efficacy of fluoxetine (a SSRI) in diabetic neuropathic pain conditions in rats. Here, we have examined whether the same strategy would be useful to treat inflammatory pain. Sub-chronic inflammatory pain was induced by injecting λ-carrageenan (100 µl, 2%) into the left hind paw of the rat. Mechanical hyperalgesia was assessed after acute treatment with TAT-2ASCV or/and fluoxetine (SSRI) 2.5 h after λ-carrageenan injection. Possible changes in the level of 5-HT2A receptors and its associated PDZ protein PSD-95 upon inflammation induction were quantified by Western blotting in dorsal horn spinal cord. Administration of TAT-2ASCV peptide (100 ng/rat, intrathecally) but not fluoxetine (10 mg/kg, intraperitoneally) relieves mechanical hyperalgesia (paw pressure test) in inflamed rats. This anti-hyperalgesic effect involves spinal 5-HT2A receptors and GABAergic interneurons as it is abolished by a 5-HT2A antagonist (M100907, 150 ng/rat, intrathecally) and a GABAA antagonist, (bicuculline, 3 µg/rat, intrathecally). We also found a decreased expression of 5-HT2A receptors in the dorsal spinal cord of inflamed animals which could not be rescued by TAT-2ASCV injection, while the amount of PSD-95 was not affected by inflammatory pain. Finally, the coadministration of fluoxetine does not further enhance the anti-hyperalgesic effect of TAT-2ASCV peptide. This study reveals a role of the interactions between 5-HT2A receptors and PDZ proteins in the pathophysiological pathways of inflammatory pain and opens new perspectives in its control thanks to molecules disrupting 5-HT2A receptor/PDZ protein interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bicuculline / pharmacology
  • Carrageenan
  • Disks Large Homolog 4 Protein
  • Fluorobenzenes / pharmacology
  • Fluoxetine / administration & dosage
  • Fluoxetine / pharmacology
  • Hyperalgesia / complications
  • Hyperalgesia / drug therapy
  • Hyperalgesia / metabolism*
  • Hyperalgesia / pathology
  • Inflammation / chemically induced*
  • Inflammation / complications
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Injections
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Male
  • Membrane Proteins / metabolism*
  • Pain / complications
  • Pain / drug therapy
  • Pain / metabolism
  • Pain / pathology
  • Peptides / administration & dosage
  • Peptides / pharmacology
  • Peptides / therapeutic use
  • Piperidines / pharmacology
  • Posterior Horn Cells / drug effects
  • Posterior Horn Cells / metabolism
  • Posterior Horn Cells / pathology
  • Protein Binding / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Serotonin, 5-HT2A / metabolism*
  • Serotonin 5-HT2 Receptor Antagonists / administration & dosage
  • Serotonin 5-HT2 Receptor Antagonists / pharmacology
  • Serotonin 5-HT2 Receptor Antagonists / therapeutic use

Substances

  • Disks Large Homolog 4 Protein
  • Dlg4 protein, rat
  • Fluorobenzenes
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Peptides
  • Piperidines
  • Receptor, Serotonin, 5-HT2A
  • Serotonin 5-HT2 Receptor Antagonists
  • Fluoxetine
  • Carrageenan
  • volinanserin
  • Bicuculline

Grants and funding

This work was supported by the French National Agency for Research (n°ANR-08-MNP-026) and Dicyt 2012-AHK, Chile. A.E. and C.C. were supported by the French Ministère de l’Enseignement Supérieur et de la Recherche, the Université d’Auvergne and INSERM. A.S.W. was supported by grant from the Région Auvergne-FEDER. X.P. was a recipient of a doctoral fellowship from Inserm-Région Auvergne. P.M. was also supported by grants from la Fondation pour la Recherche Médicale (Contracts Equipe FRM 2005, 2009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.