Sigma 1 receptor activation regulates brain-derived neurotrophic factor through NR2A-CaMKIV-TORC1 pathway to rescue the impairment of learning and memory induced by brain ischaemia/reperfusion

Psychopharmacology (Berl). 2015 May;232(10):1779-91. doi: 10.1007/s00213-014-3809-6. Epub 2014 Nov 26.

Abstract

Rationale: Sigma-1 receptor (Sig-1R) agonists showed anti-amnesic properties in Alzheimer's disease models and anti-inflammatory properties in cerebrum ischaemia models. The agonist of Sig-1R was reported to up-regulate brain-derived neurotrophic factor (BDNF) levels in the hippocampus of mice. Here, we investigate whether the activation of Sig-1R attenuates the learning and memory impairment induced by ischaemia/reperfusion and how it affects the expression of BDNF.

Objectives: Bilateral common carotid artery occlusion (BCCAO) was induced for 20 min in C57BL/6 mice.

Materials and methods: Sig-1R agonist, PRE084, sigma 1/2 non-selective agonist, DTG, Sig-1R antagonist and BD1047 were injected once daily throughout the experiment. Behavioural tests were performed from day 8. On day 22 after BCCAO, mice were sacrificed for biochemical analysis.

Results: PRE084 and DTG ameliorated learning and memory impairments in the Y maze, novel object recognition, and water maze tasks and prevented the decline of synaptic proteins and BDNF expression in the hippocampus of BCCAO mice. Furthermore, PRE084 and DTG up-regulated the level of NMDA receptor 2A (NR2A), calcium/calmodulin-dependent protein kinase type IV (CaMKIV) and CREB-specific co-activator transducer of regulated CREB activity 1 (TORC1). Additionally, the effects of PRE084 and DTG were antagonised by the co-administration of BD1047.

Conclusions: Sig-1R activation showed an attenuation in the ischaemia/reperfusion model and the activation of Sig-1R increased the expression of BDNF, possibly through the NR2A-CaMKIV-TORC1 pathway, and Sig-1R agonists might function as neuroprotectant agents in vascular dementia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Ischemia / complications
  • Brain Ischemia / metabolism*
  • Brain-Derived Neurotrophic Factor / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 4 / metabolism*
  • Female
  • Male
  • Mechanistic Target of Rapamycin Complex 1
  • Memory / drug effects
  • Memory / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Morpholines / pharmacology
  • Multiprotein Complexes / metabolism*
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Receptors, sigma / agonists
  • Receptors, sigma / metabolism*
  • Reperfusion Injury / complications
  • Reperfusion Injury / metabolism
  • Sigma-1 Receptor
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Brain-Derived Neurotrophic Factor
  • Morpholines
  • Multiprotein Complexes
  • Receptors, N-Methyl-D-Aspartate
  • Receptors, sigma
  • 2-(4-morpholino)ethyl-1-phenylcyclohexane-1-carboxylate
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 4
  • Camk4 protein, mouse
  • N-methyl D-aspartate receptor subtype 2A