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Apolipoprotein E4 Causes Age- and Tau-Dependent Impairment of GABAergic Interneurons, Leading to Learning and Memory Deficits in Mice
Open accessAbstract
Apolipoprotein E4 (apoE4) is the major genetic risk factor for Alzheimer's disease. However, the underlying mechanisms are unclear. We found that female apoE4 knock-in (KI) mice had an age-dependent decrease in hilar GABAergic interneurons that correlated with the extent of learning and memory deficits, as determined in the Morris water maze, in aged mice. Treating apoE4-KI mice with daily peritoneal injections of the GABA A receptor potentiator pentobarbital at 20 mg/kg for 4 weeks rescued the learning and memory deficits. In neurotoxic apoE4 fragment transgenic mice, hilar GABAergic interneuron loss was even more pronounced and also correlated with the extent of learning and memory deficits. Neurodegeneration and tauopathy occurred earliest in hilar interneurons in apoE4 fragment transgenic mice; eliminating endogenous Tau prevented hilar GABAergic interneuron loss and the learning and memory deficits. The GABA A receptor antagonist picrotoxin abolished this rescue, while pentobarbital rescued learning deficits in the presence of endogenous Tau. Thus, apoE4 causes age- and Tau-dependent impairment of hilar GABAergic interneurons, leading to learning and memory deficits in mice. Consequently, reducing Tau and enhancing GABA signaling are potential strategies to treat or prevent apoE4-related Alzheimer's disease.
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“It exacerbates AD-related pathologies, including amyloid-beta (Aβ) plaques, Tau tangles, neurodegeneration and neuroinflammation4–16.”
From The APOE-R136S mutation protects against APOE4-driven tau pathology, neurodegeneration, and neuroinflammation (2023) · cites this paper as [9]
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“Previous studies with mouse (Andrews-Zwilling et al., 2010) and hiPSC-based (Wang et al., 2018) systems have shown that APOE genotypes might influence GABAergic interneuron generation and survival.”
From Isogenic human stem cell models reveal mutation-dependent protective mechanisms of APOE3 Christchurch (2026) · cites this paper as Andrews-Zwilling et al., 2010
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“apoE4 knock-in (KI) mice exhibit an age-dependent loss of hilar GABAergic interneurons and deficits in learning and memory, which is more profound when the mice express neurotoxic apoE fragments”
From ApoE4 reduction: An emerging and promising therapeutic strategy for Alzheimer's disease (2022) · cites this paper as Andrews-Zwilling et al 2010
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“Tau is believed to play a key role in APOE4-related neuronal alterations during aging, as APOE4 leads to age- and Tau-dependent impairment of hilar GABAergic interneurons, resulting in learning and memory deficits in mice [75].”
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“and is associated with spatial learning and memory impairments [22].”
From Arf4 Determines Dentate Gyrus-Mediated Pattern Separation by Regulating Dendritic Spine Development (2012) · cites this paper as [22]
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“For example, both apoE4 transgenic and apoE4-KI mice show age- and sex-dependent learning and memory deficits in the absence of Aβ accumulation, as compared to apoE3 transgenic and apoE3-KI mice [68–71].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [71]
In the citing paper
“In particular, GABAergic interneurons in the dentate gyrus (DG) are particularly vulnerable to apoE4 fragment-mediated neurotoxicity, and in apoE4 fragment transgenic mice, knocking out tau rescues GABAergic interneuron loss as well as learning and memory deficits, demonstrating the tau-dependent nature of apoE4-induced cognitive impairment [71].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [71]
In the citing paper
“For example, apoE4-KI mice display an age- and tau-dependent decrease in hilar GABAergic somatostatin-positive interneurons in the hippocampus [71].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [71]
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Metadata
- Authors
- Andrews-Zwilling, Y., Bien-Ly, N., Xu, Q., Li, G., Bernardo, A., Yoon, S. Y., Zwilling, D., Yan, T. X., Chen, L., & Huang, Y.
- Affiliations
- University of California, San Francisco (US)
- Gladstone Institutes (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-10-13
- Volume
- 30
- Issue
- 41
- Pages
- 13707-13717
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2988475
- OpenAlex
- W1977434686
- Cited by
- 326
- References
- 66
- Citations by year
- 2026: 20 · 2025: 17 · 2024: 24 · 2023: 22 · 2022: 20 · 2021: 27 · 2020: 26 · 2019: 23 · 2018: 9 · 2017: 20 · 2016: 29 · 2015: 14 · 2014: 24 · 2013: 20 · 2012: 21
- FWCI
- 11.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Gladstone Institutes
- National Institutes of Health (1c06rr018928-01, AG‐022074)
- National Institute on Aging (P01AG022074)
- National Center for Research Resources (C06RR18928, C06-RR-018928)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- APOE ε4, Alzheimer's disease, GABAergic interneurons, hilar interneurons, tauopathy, learning and memory impairment, GABAA receptor, pentobarbital, picrotoxin, neurodegeneration, hippocampus, aging
- MeSH terms
- Age Factors, Analysis of Variance, Animals, Cells, Cultured, Electrophysiology, Female, gamma-Aminobutyric Acid, Immunohistochemistry, Interneurons, Memory Disorders, Mice, Transgenic, Nerve Degeneration, Pentobarbital, tau Proteins, Presynaptic Terminals, Statistics, Nonparametric, Maze Learning, Dentate Gyrus, Mice, Apolipoprotein E4
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