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Calcium release mediated by redox-sensitive RyR2 channels has a central role in hippocampal structural plasticity and spatial memory

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2018
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More, Jamileth Y.
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Calcium release mediated by redox-sensitive RyR2 channels has a central role in hippocampal structural plasticity and spatial memory
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Author
  • More, Jamileth Y.;
  • Bruna, Barbara A.;
  • Lobos, Pedro;
  • Galaz, Jose L.;
  • Figueroa, Paula L.;
  • Namias, Silvia;
  • Sánchez, Gina;
  • Barrientos Briones, Genaro;
  • Valdes Guerrero, Jose;
  • Paula Lima, Andrea;
  • Hidalgo Tapia, María Cecilia;
  • Adasme, Tatiana;
Abstract
Aims: Previous studies indicate that hippocampal synaptic plasticity and spatial memory processes entail calcium release from intracellular stores mediated by ryanodine receptor (RyR) channels. In particular, RyR-mediated Ca2+ release is central for the dendritic spine remodeling induced by brain-derived neurotrophic factor (BDNF), a neurotrophin that stimulates complex signaling pathways leading to memory-associated protein synthesis and structural plasticity. To examine if upregulation of ryanodine receptor type-2 (RyR2) channels and the spine remodeling induced by BDNF entail reactive oxygen species (ROS) generation, and to test if RyR2 downregulation affects BDNF-induced spine remodeling and spatial memory. Results: Downregulation of RyR2 expression (short hairpin RNA [shRNA]) in primary hippocampal neurons, or inhibition of nitric oxide synthase (NOS) or NADPH oxidase, prevented agonist-mediated RyR-mediated Ca2+ release, whereas BDNF promoted cytoplasmic ROS generation. RyR2 downregulation or inhibitors of N-methyl-d-aspartate (NMDA) receptors, or NOS or of NADPH oxidase type-2 (NOX2) prevented RyR2 upregulation and the spine remodeling induced by BDNF, as did incubation with the antioxidant agent N-acetyl l-cysteine. In addition, intrahippocampal injection of RyR2-directed antisense oligodeoxynucleotides, which caused significant RyR2 downregulation, caused conspicuous defects in a memorized spatial memory task. Innovation: The present novel results emphasize the key role of redox-sensitive Ca2+ release mediated by RyR2 channels for hippocampal structural plasticity and spatial memory. Conclusion: Based on these combined results, we propose (i) that BDNF-induced RyR2-mediated Ca2+ release and ROS generation via NOS/NOX2 are strictly required for the dendritic spine remodeling and the RyR2 upregulation induced by BDNF, and (ii) that RyR2 channel expression is crucial for spatial memory processes.
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FONDECYT 3120093 11140580 1140545 1150736 1170053 BNI P-09-015
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URI: https://repositorio.uchile.cl/handle/2250/150623
DOI: 10.1089/ars.2017.7277
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Antioxidants & Redox Signaling, Mar 2018
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