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Astrocytic ApoE reprograms neuronal cholesterol metabolism and histone-acetylation-mediated memory
Open accessAbstract
Astrocytes metabolically interact with neighboring neurons by providing multiple substances to neurons. How astrocytes regulate neural functions via altering the neuronal metabolic state remains elusive. Here, we demonstrate that astrocytic ApoE vectors a variety of microRNAs (miRNAs), and these miRNAs specifically silence genes involved in neuronal cholesterol biosynthesis, ultimately accounting for accumulation of the pathway-initiating substrate acetyl-CoA. Consequently, histone acetylation is promoted, and transcription is activated in neurons. Functionally, we demonstrate that ApoE-mediated neuronal histone acetylation leads to increased H3K27ac enrichment in the promoters of multiple neuronal immediate early genes and subsequently to enhanced memory consolidation in mice. Importantly, human ApoE4 vectors lower levels of miRNAs than ApoE3 and therefore is less capable of metabolic and epigenetic regulation in neurons. Collectively, our findings define an astrocytic ApoE-mediated neuronal epigenetic mechanism as a novel means through which astrocytes modulate brain connectivity and function.
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“Of note, sApoE has been found to influence the transcriptome by modulating histone acetylation (68, 69).”
From Secreted Apoe rewires melanoma cell state vulnerability to ferroptosis (2024) · cites this paper as [68]
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Prakash, N., Matos, H. Y., Sebaoui, S., Tsai, L., Tran, T., Aromolaran, A., Atrachji, I., Campbell, N., Goodrich, M., Hernandez‐Pineda, D., et al. (2023) · The Journal of Comparative Neurology · doi:10.1002/cne.25545 · Cited by 4
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BackgroundKin17 promotes rDNA transcription, ribosomal biogenesis, and cortical lamination
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“67 Notably, ApoE4 particles were less effective in promoting histone acetylation and memory consolidation—suggesting that the epigenetic response to lipid cues is altered in ε 4 carriers and may contribute to lineage-specific inheritance of AD risk.”
Miftakhov, R., Fortygina, P., Zuzina, A. B., Balaban, P. M., & Borodinova, A. A. (2026) · Scientific Reports · doi:10.1038/s41598-026-56373-0
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Recent advances in brain aging and epigenetics
Hong-Da, L. I. U., ZHANG, J., & Qiang, L. I. U. (2026) · Shengming kexue · doi:10.3724/cbls.2026086
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“Apolipoprotein E (APOE), a 34-kDa glycoprotein primarily known for its role in lipid metabolism and Alzheimer’s disease 10,11 has emerged as a promising candidate.”
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“The resulting excess acetyl-CoA alters histone acetylation and epigenetically promotes transcription of immediate early genes, such as Fos , Arc , and Egr1 , which are associated with neuronal memory [32].”
Roland, N. J., Zigmond, J. W., Manganaro, J. E., Estrella, L. D., & Stauch, K. L. (2026) · Neurochemistry International · doi:10.1016/j.neuint.2026.106125 · Cited by 1
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“Additionally, astrocyte-derived APOE may modulate neuronal lipid metabolism by acting through carrier miRNAs, thereby reducing cholesterol synthesis [38].”
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“Apart from cholesterol, ApoE particles carry a variety of microRNAs that actively repress cholesterol biosynthesis in neurons (22).”
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“Especially considering that other groups claimed molecular mechanisms by direct apoE4 action to neurons (Huang et al., 2017; Lee et al., 2021; Li et al., 2021; Ramakrishna et al., 2021; Shi et al., 2017), apoE4 and apoE4 particles themselves may also underlie neuronal impairment together with astrocyticderived toxic f…”
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“Neuronal activity induced acetylation of histone H3 at lysine 27 (H3K27ac) at the enhancers of IEGs regulates their transcription (L.-F. Chen et al., 2019; Xiaohui Li et al., 2021; Malik et al., 2014), and a previous study showed that DEK chromatin binding pattern overlaps with H3K27ac (Sandén et al., 2014).”
BackgroundMaladaptive aging trajectory in late-onset Alzheimer's disease
Lv, T., Sun, H., Xia, T., Zhu, M. L., & Li, Y. (2026) · The Innovation Life · doi:10.59717/j.xinn-life.2026.100206
Progress of DNA Methylation and Histone Acetylation in the Pathogenesis of Cerebral Hemorrhage
Liu, X.-J. (2025) · Advances in Clinical Medicine · doi:10.12677/acm.2025.1541324
Metadata
- Authors
- Li, X., Zhang, J., Li, D., He, C., He, K., Xue, T., Wan, L., Zhang, C., & Liu, Q.
- Affiliations
- University of Science and Technology of China (CN)
- University of Pennsylvania (US)
- Harvard University (US)
- Corresponding author
- Zhang, Juan
- Liu, Qiang
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2021-03
- Volume
- 109
- Issue
- 6
- Pages
- 957-970.e8
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W3124009158
- Cited by
- 165
- References
- 0
- Citations by year
- 2026: 28 · 2025: 32 · 2024: 35 · 2023: 29 · 2022: 30 · 2021: 11
- FWCI
- 12.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 381 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Key Research and Development Program of China (2020YFA0509300)
- Fundamental Research Funds for the Central Universities
- Innovative Program of Development Foundation of Hefei Center for Physical Science and Technology (2018CXFX005)
- National Natural Science Foundation of China (31871082, 82071185, 91849101)
- Natural Science Foundation of Anhui Province (2008085QC117)
- Chinese Academy of Sciences (QYZDB-SSW-SMC035, XDB39000000)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Keywords
- astrocytes, apolipoprotein E, microRNA transfer, histone acetylation, H3K27ac, memory consolidation, epigenetic regulation, acetyl-CoA, APOE ε4, APOE3, immediate early genes, astrocyte-neuron metabolic coupling
- MeSH terms
- Memory Consolidation, Acetylation, Animals, Apolipoproteins E, Astrocytes, Cell Line, Cholesterol, Gene Expression Regulation, Histones, Humans, Mice, Inbred C57BL, Neurons, Epigenesis, Genetic, Mice
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