Selective siRNA-mediated suppression of 5-HT1A autoreceptors evokes strong anti-depressant-like effects

Mol Psychiatry. 2012 Jun;17(6):612-23. doi: 10.1038/mp.2011.92. Epub 2011 Aug 2.

Abstract

Depression is a major health problem worldwide. Most prescribed anti-depressants, the selective serotonin reuptake inhibitors (SSRI) show limited efficacy and delayed onset of action, partly due to the activation of somatodendritic 5-HT(1A)-autoreceptors by the excess extracellular serotonin (5-HT) produced by SSRI in the raphe nuclei. Likewise, 5-HT(1A) receptor (5-HT(1A)R) gene polymorphisms leading to high 5-HT(1A)-autoreceptor expression increase depression susceptibility and decrease treatment response. In this study, we report on a new treatment strategy based on the administration of small-interfering RNA (siRNA) to acutely suppress 5-HT(1A)-autoreceptor-mediated negative feedback mechanisms. We developed a conjugated siRNA (C-1A-siRNA) by covalently binding siRNA targeting 5-HT(1A) receptor mRNA with the SSRI sertraline in order to concentrate it in serotonin axons, rich in serotonin transporter (SERT) sites. The intracerebroventricular (i.c.v.) infusion of C-1A-siRNA to mice resulted in its selective accumulation in serotonin neurons. This evoked marked anti-depressant-like effects in the forced swim and tail suspension tests, but did not affect anxiety-like behaviors in the elevated plus-maze. In parallel, C-1A-siRNA administration markedly decreased 5-HT(1A)-autoreceptor expression and suppressed 8-OH-DPAT-induced hypothermia (a pre-synaptic 5-HT(1A)R effect in mice) without affecting post-synaptic 5-HT(1A)R expression in hippocampus and prefrontal cortex. Moreover, i.c.v. C-1A-siRNA infusion augmented the increase in extracellular serotonin evoked by fluoxetine in prefrontal cortex to the level seen in 5-HT(1A)R knockout mice. Interestingly, intranasal C-1A-siRNA administration produced the same effects, thus opening the way to the therapeutic use of C-1A-siRNA. Hence, C-1A-siRNA represents a new approach to treat mood disorders as monotherapy or in combination with SSRI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8-Hydroxy-2-(di-n-propylamino)tetralin / antagonists & inhibitors
  • 8-Hydroxy-2-(di-n-propylamino)tetralin / pharmacology
  • Administration, Intranasal
  • Animals
  • Antidepressive Agents / therapeutic use*
  • Autoreceptors / antagonists & inhibitors*
  • Autoreceptors / biosynthesis
  • Depression / drug therapy*
  • Disease Models, Animal
  • Drug Combinations*
  • Drug Design
  • Fluoxetine / pharmacology
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Hypothermia / chemically induced
  • Hypothermia / drug therapy
  • Infusions, Intraventricular
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Prefrontal Cortex / drug effects
  • Prefrontal Cortex / metabolism
  • RNA, Small Interfering / therapeutic use*
  • Receptor, Serotonin, 5-HT1A / biosynthesis
  • Receptor, Serotonin, 5-HT1A / chemistry
  • Receptor, Serotonin, 5-HT1A / genetics*
  • Serotonergic Neurons / drug effects
  • Serotonergic Neurons / metabolism
  • Sertraline / administration & dosage
  • Sertraline / chemistry

Substances

  • Antidepressive Agents
  • Autoreceptors
  • Drug Combinations
  • RNA, Small Interfering
  • Fluoxetine
  • Receptor, Serotonin, 5-HT1A
  • 8-Hydroxy-2-(di-n-propylamino)tetralin
  • Sertraline