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Cited by 118Alzheimer's disease research and treatmentsNeuroscience and Neuropharmacology ResearchCalcium signaling and nucleotide metabolism

Early presynaptic and postsynaptic calcium signaling abnormalities mask underlying synaptic depression in presymptomatic Alzheimer’s disease mice

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Chakroborty, S., Kim, J., Schneider, C., Jacobson, C., Molgo, J., Stutzmann, G. E.·2012·Journal of Neuroscience
DOI 10.1523/jneurosci.0936-12.2012PMC PMC3417348
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Abstract

Alzheimer's disease (AD)-linked presenilin (PS) mutations result in pronounced endoplasmic reticulum calcium disruptions that occur before detectable histopathology and cognitive deficits. More subtly, these early AD-linked calcium alterations also reset neurophysiological homeostasis, such that calcium-dependent presynaptic and postsynaptic signaling appear functionally normal yet are actually operating under aberrant calcium signaling systems. In these 3xTg-AD mouse brains, upregulated ryanodine receptor (RyR) activity is associated with a shift toward synaptic depression, likely through a reduction in presynaptic vesicle stores and increased postsynaptic outward currents through small-conductance calcium-activated potassium SK2 channels. The deviant RyR-calcium involvement in the 3xTg-AD mice also compensates for an intrinsic predisposition for hippocampal long-term depression (LTD) and reduced long-term potentiation (LTP). In this study, we detail the impact of disrupted RyR-mediated calcium stores on synaptic transmission properties, LTD, and calcium-activated membrane channels of hippocampal CA1 pyramidal neurons in presymptomatic 3xTg-AD mice. Using electrophysiological recordings in young 3xTg-AD and nontransgenic (NonTg) hippocampal slices, we show that increased RyR-evoked calcium release in 3xTg-AD mice "normalizes" an altered synaptic transmission system operating under a shifted homeostatic state that is not present in NonTg mice. In the process, we uncover compensatory signaling mechanisms recruited early in the disease process that counterbalance the disrupted RyR-calcium dynamics, namely increases in presynaptic spontaneous vesicle release, altered probability of vesicle release, and upregulated postsynaptic SK channel activity. Because AD is increasingly recognized as a "synaptic disease," calcium-mediated signaling alterations may serve as a proximal trigger for the synaptic degradation driving the cognitive loss in AD.

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Authors
Chakroborty, S., Kim, J., Schneider, C., Jacobson, C., Molgo, J., & Stutzmann, G. E.
Affiliations
Rosalind Franklin University of Medicine and Science (US)
ORCID
Stutzmann, G. E.
Venue
Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2012-06-13
Volume
32
Issue
24
Pages
8341-8353
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.0936-12.2012
PMC
PMC3417348
OpenAlex
W2079952612
Cited by
118
References
5
Citations by year
2025: 2 · 2024: 5 · 2023: 6 · 2022: 8 · 2021: 6 · 2020: 12 · 2019: 12 · 2018: 7 · 2017: 11 · 2016: 8 · 2015: 10 · 2014: 15 · 2013: 13 · 2012: 3
FWCI
8.79
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
Funders
National Institute on Aging (R01AG030205, R56AG055497)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords
Alzheimer's disease, ryanodine receptor, endoplasmic reticulum calcium stores, synaptic depression, preclinical Alzheimer's disease, 3xTg-AD mice, presenilin mutations, synaptic homeostasis, synaptic vesicle release, small conductance calcium-activated potassium channels, SK2 channel, long-term depression, long-term potentiation, CA1 pyramidal neurons, synaptic transmission
MeSH terms
Alzheimer Disease, Animals, Calcium, Female, Male, Membrane Potentials, Mice, Inbred C57BL, Mice, Transgenic, Synaptic Transmission, Synaptic Vesicles, Pyramidal Cells, Ryanodine Receptor Calcium Release Channel, Calcium Signaling, Long-Term Synaptic Depression, Mice, Small-Conductance Calcium-Activated Potassium Channels, Inositol 1,4,5-Trisphosphate Receptors, CA1 Region, Hippocampal

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