Targeting the dopamine D1 receptor or its downstream signalling by inhibiting phosphodiesterase-1 improves cognitive performance

Br J Pharmacol. 2018 Jul;175(14):3021-3033. doi: 10.1111/bph.14350. Epub 2018 Jun 3.

Abstract

Background and purpose: Insufficient prefrontal dopamine 1 (D1 ) receptor signalling has been linked to cognitive dysfunction in several psychiatric conditions. Because the PDE1 isoform B (PDE1B) is postulated to regulate D1 receptor-dependent signal transduction, in this study we aimed to elucidate the role of PDE1 in cognitive processes reliant on D1 receptor function.

Experimental approach: Cognitive performance of the D1 receptor agonist, SKF38393, was studied in the T-maze continuous alternation task and 5-choice serial reaction time task. D1 receptor/PDE1B double-immunohistochemistry was performed using human and rat prefrontal brain sections. The pharmacological activity of the PDE1 inhibitor, ITI-214, was assessed by measuring the increase in cAMP/cGMP in prefrontal brain tissue and its effect on working memory performance. Mechanistic studies on the modulation of prefrontal neuronal transmission by SKF38393 and ITI-214 were performed using extracellular recordings in brain slices.

Key results: SKF38393 improved working memory and attentional performance in rodents. D1 receptor/PDE1B co-expression was verified in both human and rat prefrontal brain sections. The pharmacological activity of ITI-214 on its target, PDE1, was demonstrated by its ability to increase prefrontal cAMP/cGMP. In addition, ITI-214 improved working memory performance. Both SKF38393 and ITI-214 facilitated neuronal transmission in prefrontal brain slices.

Conclusion and implications: We hypothesize that PDE1 inhibition improves working memory performance by increasing prefrontal synaptic transmission and/or postsynaptic D1 receptor signalling, by modulating prefrontal downstream second messenger levels. These data, therefore, support the use of PDE1 inhibitors as a potential approach for the treatment of cognitive dysfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine / pharmacology*
  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Brain / physiology
  • Cognition / drug effects*
  • Cognitive Dysfunction / drug therapy
  • Cyclic AMP / metabolism
  • Cyclic GMP / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 1 / antagonists & inhibitors*
  • Dopamine Agonists / pharmacology*
  • Heterocyclic Compounds, 4 or More Rings / pharmacology*
  • Male
  • Maze Learning / drug effects
  • Memory, Short-Term / drug effects
  • Mice
  • Rats, Sprague-Dawley
  • Receptors, Dopamine D1 / metabolism*
  • Signal Transduction
  • Synaptic Transmission / drug effects

Substances

  • Dopamine Agonists
  • Heterocyclic Compounds, 4 or More Rings
  • ITI-214
  • Receptors, Dopamine D1
  • 2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine
  • Cyclic AMP
  • Cyclic Nucleotide Phosphodiesterases, Type 1
  • Pde1b protein, mouse
  • Cyclic GMP