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Post-translational remodeling of ryanodine receptor induces calcium leak leading to Alzheimer’s disease-like pathologies and cognitive deficits

Lacampagne, Alain, Liu, Xiaoping, Reiken, Steven, Bussiere, Renaud, Meli, Albano C., Lauritzen, Inger, Teich, Andrew F., Zalk, Ran, Saint, Nathalie, Arancio, Ottavio, Bauer, Charlotte, Duprat, Fabrice, Briggs, Clark A., Chakroborty, Shreaya, Stutzmann, Grace E., Shelanski, Michael L., Checler, Frederic, Chami, Mounia, Marks, Andrew R.·2017·Acta Neuropathologica
DOI 10.1007/s00401-017-1733-7
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Abstract

The mechanisms underlying ryanodine receptor (RyR) dysfunction associated with Alzheimer disease (AD) are still not well understood. Here, we show that neuronal RyR2 channels undergo post-translational remodeling (PKA phosphorylation, oxidation, and nitrosylation) in brains of AD patients, and in two murine models of AD (3 × Tg-AD, APP +/- /PS1 +/- ). RyR2 is depleted of calstabin2 (KFBP12.6) in the channel complex, resulting in endoplasmic reticular (ER) calcium (Ca 2+ ) leak. RyR-mediated ER Ca 2+ leak activates Ca 2+ -dependent signaling pathways, contributing to AD pathogenesis. Pharmacological (using a novel RyR stabilizing drug Rycal) or genetic rescue of the RyR2-mediated intracellular Ca 2+ leak improved synaptic plasticity, normalized behavioral and cognitive functions and reduced Aβ load. Genetically altered mice with congenitally leaky RyR2 exhibited premature and severe defects in synaptic plasticity, behavior and cognitive function. These data provide a mechanism underlying leaky RyR2 channels, which could be considered as potential AD therapeutic targets.

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Metadata

Authors
Lacampagne, A., Liu, X., Reiken, S., Bussiere, R., Meli, A. C., Lauritzen, I., Teich, A. F., Zalk, R., Saint, N., Arancio, O., Bauer, C., Duprat, F., Briggs, C. A., Chakroborty, S., Stutzmann, G. E., Shelanski, M. L., Checler, F., Chami, M., & Marks, A. R.
Venue
Acta Neuropathologica
Publisher
Springer Science and Business Media LLC
Published
2017-06-19
Volume
134
Issue
5
Pages
749-767
ISSN
  • 0001-6322
  • 1432-0533
DOI
10.1007/s00401-017-1733-7
Cited by
181
References
5
Language
en
Licence
Funders
  • National Heart, Lung, and Blood Institute (R01HL061503, R01HL102040)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS-R01AR060037)
  • National Institute of Mental Health (NIH T32 HL120826)
  • National Institute of Neurological Disorders and Stroke (R25NS076445)
  • the Fondation Leducq and a generous donation from Carol Stix
  • LABEX (excellence laboratory, program investment for the future) DISTALZ
  • the University Hospital Federation (FHU) OncoAge
  • Fondation Pompidou
  • LECMA (13737)
  • Niagara University (RO1AG030205)
  • Schaefer Award from Columbia University

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Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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