A Ca2+-dependent mechanism boosting glycolysis and OXPHOS by activating aralar-malate-aspartate shuttle, upon neuronal stimulation

Calcium is an important second messenger regulating a bioenergetic response to the workloads triggered by neuronal activation. In embryonic mouse cortical neurons using glucose as only fuel, activation by NMDA elicits a strong workload (ATP demand)-dependent on Na+ and Ca2+ entry, and stimulates glu...

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Detalhes bibliográficos
Autores: Pérez Liébana, Irene, Juaristi, Inés, González Sánchez, Paloma, González Moreno, Luis, Rial, Eduardo, Podunavac, Maša, Zakarian, Armen, Molgó, Jordi, Vallejo-Illarramendi, Ainara, Mosqueira-Martín, Laura, Lopez de Munain, Adolfo, Pardo Merino, Beatriz, Satrustegui Gil Delgado, Jorgina, Arco, Araceli del
Formato: artículo
Fecha de publicación:2022
País:España
Recursos:Universidad Autónoma de Madrid
Repositorio:Biblos-e Archivo. Repositorio Institucional de la UAM
Idioma:inglés
OAI Identifier:oai:repositorio.uam.es:10486/726900
Acesso em linha:https://hdl.handle.net/10486/726900
https://dx.doi.org/10.1523/JNEUROSCI.1463-21.2022
Access Level:acceso abierto
Palavra-chave:Aralar/AGC1/Slc25a12
calcium regulation
glycolysis
malate aspartate shuttle
mitochondrial calcium uniporter
neuronal metabolism
Biología y Biomedicina / Biología
Descrição
Resumo:Calcium is an important second messenger regulating a bioenergetic response to the workloads triggered by neuronal activation. In embryonic mouse cortical neurons using glucose as only fuel, activation by NMDA elicits a strong workload (ATP demand)-dependent on Na+ and Ca2+ entry, and stimulates glucose uptake, glycolysis, pyruvate and lactate production, and oxidative phosphorylation (OXPHOS) in a Ca2+-dependent way. We find that Ca2+ upregulation of glycolysis, pyruvate levels, and respiration, but not glucose uptake, all depend on Aralar/AGC1/Slc25a12, the mitochondrial aspartate-glutamate carrier, component of the malate-aspartate shuttle (MAS). MAS activation increases glycolysis, pyruvate production, and respiration, a process inhibited in the presence of BAPTA-AM, suggesting that the Ca2+ binding motifs in Aralar may be involved in the activation. Mitochondrial calcium uniporter (MCU) silencing had no effect, indicating that none of these processes required MCU-dependent mitochondrial Ca2+ uptake. The neuronal respiratory response to carbachol was also dependent on Aralar, but not on MCU. We find that mouse cortical neurons are endowed with a constitutive ER-to-mitochondria Ca2+ flow maintaining basal cell bioenergetics in which ryanodine receptors, RyR2, rather than InsP3R, are responsible for Ca2+ release, and in which MCU does not participate. The results reveal that, in neurons using glucose, MCU does not participate in OXPHOS regulation under basal or stimulated conditions, while Aralar-MAS appears as the major Ca2+-dependent pathway tuning simultaneously glycolysis and OXPHOS to neuronal activation