β-adrenergic receptors activate exchange protein directly activated by camp (epac), translocate munc13-1, and enhance the rab3a-rim1α interaction to potentiate glutamate release at cerebrocortical nerve terminals

The adenylyl cyclase activator forskolin facilitates synaptic transmission presynaptically via cAMP-dependent protein kinase (PKA). In addition, cAMP also increases glutamate release via PKA-independent mechanisms, although the downstream presynaptic targets remain largely unknown. Here, we describe...

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Detalles Bibliográficos
Autores: Ferrero, José Javier, Alvarez, Ana Maria, Ramírez-Franco, Jorge, Godino, Maria del Carmen, Bartolomé-Martín, David, Aguado, Carolina, Torres Molina, Magdalena Isabel, Luján, Rafael, Ciruela, Francisco, Sánchez-Prieto Borja, José
Tipo de recurso: artículo
Fecha de publicación:2013
País:España
Institución:Universidad Complutense de Madrid (UCM)
Repositorio:Docta Complutense
Idioma:inglés
OAI Identifier:oai:docta.ucm.es:20.500.14352/129940
Acceso en línea:https://hdl.handle.net/20.500.14352/129940
Access Level:acceso abierto
Palabra clave:612.8.015
Cyclic AMP (cAMP)
G Protein-coupled Receptors (GPCR)
Neurotransmitter Release
Phospholipase C
Synaptosomes
Epac Proteins
Munc13–1
RIM1α
Rab3A
Neurociencias (Biológicas)
2490.02 Neuroquímica
Descripción
Sumario:The adenylyl cyclase activator forskolin facilitates synaptic transmission presynaptically via cAMP-dependent protein kinase (PKA). In addition, cAMP also increases glutamate release via PKA-independent mechanisms, although the downstream presynaptic targets remain largely unknown. Here, we describe the isolation of a PKA-independent component of glutamate release in cerebrocortical nerve terminals after blocking Na+ channels with tetrodotoxin. We found that 8-pCPT-2′-O-Me-cAMP, a specific activator of the exchange protein directly activated by cAMP (Epac), mimicked and occluded forskolin-induced potentiation of glutamate release. This Epac-mediated increase in glutamate release was dependent on phospholipase C, and it increased the hydrolysis of phosphatidylinositol 4,5-bisphosphate. Moreover, the potentiation of glutamate release by Epac was independent of protein kinase C, although it was attenuated by the diacylglycerol-binding site antagonist calphostin C. Epac activation translocated the active zone protein Munc13-1 from soluble to particulate fractions; it increased the association between Rab3A and RIM1α and redistributed synaptic vesicles closer to the presynaptic membrane. Furthermore, these responses were mimicked by the β-adrenergic receptor (βAR) agonist isoproterenol, consistent with the immunoelectron microscopy and immunocytochemical data demonstrating presynaptic expression of βARs in a subset of glutamatergic synapses in the cerebral cortex. Based on these findings, we conclude that βARs couple to a cAMP/Epac/PLC/Munc13/Rab3/RIM-dependent pathway to enhance glutamate release at cerebrocortical nerve terminals. Background: G protein-coupled receptors generating cAMP at nerve terminals modulate neurotransmitter release. Results: β-Adrenergic receptor enhances glutamate release via Epac protein activation and Munc13-1 translocation at cerebrocortical nerve terminals. Conclusion: Protein kinase A-independent signaling pathways triggered by β-adrenergic receptors control presynaptic function. Significance: β-Adrenergic receptors target presynaptic release machinery.