Adenosine receptors are the on‐and‐off switch of astrocytic cannabinoid type 1 (CB1) receptor effect upon synaptic plasticity in the medial prefrontal cortex

Author:

Gonçalves‐Ribeiro Joana12ORCID,Savchak Oksana K.12ORCID,Costa‐Pinto Sara12ORCID,Gomes Joana I.12ORCID,Rivas‐Santisteban Rafael34ORCID,Lillo Alejandro34,Sánchez Romero Javier56ORCID,Sebastião Ana M.12ORCID,Navarrete Marta5ORCID,Navarro Gemma347ORCID,Franco Rafael489ORCID,Vaz Sandra H.12ORCID

Affiliation:

1. Instituto de Farmacologia e Neurociências Faculdade de Medicina, Universidade de Lisboa Lisbon Portugal

2. Instituto de Medicina Molecular João Lobo Antunes Faculdade de Medicina, Universidade de Lisboa Lisbon Portugal

3. Department of Biochemistry and Physiology School of Pharmacy and Food Science, Universitat de Barcelona Barcelona Spain

4. CiberNed, Network Center for Neurodegenerative Diseases National Spanish Health Institute Carlos III Madrid Spain

5. Instituto Cajal CSIC Madrid Spain

6. PhD Program in Neuroscience Universidad Autónoma de Madrid‐Instituto Cajal Madrid Spain

7. Institut de Neurociències Universitat de Barcelona Barcelona Spain

8. Molecular Neurobiology Laboratory, Department of Biochemistry and Molecular Biomedicine Faculty of Biology, Universitat de Barcelona Barcelona Spain

9. School of Chemistry Universitat de Barcelona Barcelona Spain

Abstract

AbstractThe medial prefrontal cortex (mPFC) is involved in cognitive functions such as working memory. Astrocytic cannabinoid type 1 receptor (CB1R) induces cytosolic calcium (Ca2+) concentration changes with an impact on neuronal function. mPFC astrocytes also express adenosine A1 and A2A receptors (A1R, A2AR), being unknown the crosstalk between CB1R and adenosine receptors in these cells. We show here that a further level of regulation of astrocyte Ca2+ signaling occurs through CB1R‐A2AR or CB1R‐A1R heteromers that ultimately impact mPFC synaptic plasticity. CB1R‐mediated Ca2+ transients increased and decreased when A1R and A2AR were activated, respectively, unveiling adenosine receptors as modulators of astrocytic CB1R. CB1R activation leads to an enhancement of long‐term potentiation (LTP) in the mPFC, under the control of A1R but not of A2AR. Notably, in IP3R2KO mice, that do not show astrocytic Ca2+ level elevations, CB1R activation decreases LTP, which is not modified by A1R or A2AR. The present work suggests that CB1R has a homeostatic role on mPFC LTP, under the control of A1R, probably due to physical crosstalk between these receptors in astrocytes that ultimately alters CB1R Ca2+ signaling.

Funder

HORIZON EUROPE Innovative Europe

International Society for Neurochemistry

Publisher

Wiley

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