Apolipoprotein E4 Causes Age- and Sex-Dependent Impairments of Hilar GABAergic Interneurons and Learning and Memory Deficits in Mice
Open accessAbstract
Apolipoprotein (apo) E4 is the major genetic risk factor for Alzheimer's disease (AD). ApoE4 has sex-dependent effects, whereby the risk of developing AD is higher in apoE4-expressing females than males. However, the mechanism underlying the sex difference, in relation to apoE4, is unknown. Previous findings indicate that apoE4 causes age-dependent impairments of hilar GABAergic interneurons in female mice, leading to learning and memory deficits. Here, we investigate whether the detrimental effects of apoE4 on hilar GABAergic interneurons are sex-dependent using apoE knock-in (KI) mice across different ages. We found that in female apoE-KI mice, there was an age-dependent depletion of hilar GABAergic interneurons, whereby GAD67- or somatostatin-positive--but not NPY- or parvalbumin-positive-interneuron loss was exacerbated by apoE4. Loss of these neuronal populations was correlated with the severity of spatial learning deficits at 16 months of age in female apoE4-KI mice; however, this effect was not observed in female apoE3-KI mice. In contrast, we found an increase in the numbers of hilar GABAergic interneurons with advancing age in male apoE-KI mice, regardless of apoE genotype. Moreover, male apoE-KI mice showed a consistent ratio of hilar inhibitory GABAergic interneurons to excitatory mossy cells approximating 1.5 that is independent of apoE genotype and age, whereas female apoE-KI mice exhibited an age-dependent decrease in this ratio, which was exacerbated by apoE4. Interestingly, there are no apoE genotype effects on GABAergic interneurons in the CA1 and CA3 subregions of the hippocampus as well as the entorhinal and auditory cortexes. These findings suggest that the sex-dependent effects of apoE4 on developing AD is in part attributable to inherent sex-based differences in the numbers of hilar GABAergic interneurons, which is further modulated by apoE genotype.
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No neurodegeneration was found in our hAPOE4 model at 12 months, unlike other studies reporting neuronal pathology in humanized APOE4 mice at 6 months.
“Unlike other studies reporting neuronal pathology in humanized APOE4 mice at 6 months (Leung et al. 2012;Tong et al. 2016), no neurodegeneration was found in our hAPOE4 model at 12 months.”
From Apolipoprotein E ε4 disrupts oligodendrocyte differentiation by interfering with astrocyte‐derived lipid transport (2023) · cites this paper as Leung et al. 2012
ApoE4 transgenic and apoE4-knock-in mice show age- and sex-dependent learning and memory deficits in the absence of amyloid-β accumulation, as compared to apoE3 transgenic and apoE3-knock-in mice.
“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 [70]
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Li, Y., Hao, Y., Serras, C. P., Yao, L., Liang, Z., Almonte-Loya, A., Blumenfeld, J. R., Suan, K., Yoon, S. Y., Grone, B. P., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.03.691944
Self-citation
- Authors
- Leung, L., Andrews-Zwilling, Y., Yoon, S. Y., Jain, S., Ring, K., Dai, J., Wang, M. M., Tong, L., Walker, D., & Huang, Y.
- Affiliations
- Gladstone Institutes (US)
- Corresponding author
- Huang, Yadong
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-12-31
- Volume
- 7
- Issue
- 12
- Pages
- e53569
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3534053
- OpenAlex
- W2094912260
- Cited by
- 109
- References
- 97
- Citations by year
- 2026: 11 · 2025: 11 · 2024: 9 · 2023: 7 · 2022: 10 · 2021: 14 · 2020: 6 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 7 · 2014: 9 · 2013: 1
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Gladstone Institutes (AG022074)
- National Institutes of Health (1c06rr018928-01, AG‐022074)
- National Institute on Aging (P01AG022074)
- National Institute of Neurological Disorders and Stroke (P30NS065780)
- National Center for Research Resources (C06RR18928, C06-RR-018928)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007470)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- APOE ε4, sex differences, Alzheimer's disease, interneuron loss, GAD67, somatostatin, mossy cells, spatial learning deficits, age-related neurodegeneration, hippocampus, APOE3
- MeSH terms
- Age Factors, Animals, Hippocampus, Interneurons, Memory Disorders, Mice, Transgenic, Sex Factors, Maze Learning, Mice, Apolipoprotein E4, Gene Knock-In Techniques, GABAergic Neurons
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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