Mechanism underlying apolipoprotein E (ApoE) isoform‐dependent lipid efflux from neural cells in culture

Minagawa, Hirohisa; Gong, Jiang‐Sheng; Jung, Cha‐Gyun; Watanabe, Atsushi; Lund‐Katz, Sissel; Phillips, Michael C.; Saito, Hiroyuki; Michikawa, Makoto

doi:10.1002/jnr.22073

Cited by 90Cholesterol and Lipid MetabolismAlzheimer's disease research and treatmentsLipoproteins and Cardiovascular Health

Mechanism underlying apolipoprotein E (ApoE) isoform‐dependent lipid efflux from neural cells in culture

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Minagawa, Hirohisa, Gong, Jiang‐Sheng, Jung, Cha‐Gyun, Watanabe, Atsushi, Lund‐Katz, Sissel, Phillips, Michael C., Saito, Hiroyuki, Michikawa, Makoto·2009·Journal of Neuroscience Research

DOI 10.1002/jnr.22073PMC PMC3065888

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Abstract

We determined the molecular mechanisms underlying apolipoprotein E (ApoE)‐isoform‐dependent lipid efflux from neurons and ApoE‐deficient astrocytes in culture. The ability of ApoE3 to induce lipid efflux was 2.5‐ to 3.9‐fold greater than ApoE4. To explore the contributions of the amino‐ and carboxyl‐terminal tertiary structure domains of ApoE to cellular lipid efflux, each domain was studied separately. The amino‐terminal fragment of ApoE3 (22‐kDa‐ApoE3) induced lipid efflux greater than 22‐kDa‐ApoE4, whereas the common carboxyl‐terminal fragment of ApoE induced very low levels of lipid efflux. Addition of segments of the carboxyl‐terminal domain to 22‐kDa‐ApoE3 additively induced lipid efflux in a length‐dependent manner; in contrast, this effect did not occur with ApoE4. This observation, coupled with the fact that introduction of the E255A mutation (which disrupts domain–domain interaction) into ApoE4 increases lipid efflux, indicates that interaction between the amino‐ and carboxyl‐terminal domains in ApoE4 reduces the ability of this isoform to mediate lipid efflux from neural cells. Dimeric 22‐kDa or intact ApoE3 induced higher lipid efflux than monomeric 22‐kDa or intact ApoE3, respectively, indicating that dimerization of ApoE3 enhances the ability to release lipids. The adenosine triphosphate–binding cassette protein A1 (ABCA1) is involved in ApoE‐induced lipid efflux. In conclusion, there are two major factors, intramolecular domain interaction and intermolecular dimerization, that cause ApoE‐isoform‐dependent lipid efflux from neural cells in culture. © 2009 Wiley‐Liss, Inc.

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APOE2 is the most efficient at promoting cholesterol efflux, and APOE4 is the least efficient, correlating inversely with AD risk.
“While APOE2 is the most efficient at promoting cholesterol efflux, APOE4 is the least efficient, correlating inversely with AD risk.”
From Deletion of neuronal Idol ameliorates Alzheimer's disease–related pathologies via APOE receptors (2025) · cites this paper as [65]
The Results report greater cholesterol efflux with ApoE3 than ApoE4 in cultured neural cells, and the introductory passage describes ApoE4 as an AD risk factor. The paper does not establish that ApoE2 is the most efficient or compare efflux across all three isoforms; its proposed connection between cholesterol handling and AD risk is also hedged. (LLM, conf=0.88)
Experimental — accuracy not yet measured
APOE isoforms differ in their ability to regulate lipid metabolism and cholesterol efflux.
“One key difference among APOE isoforms is their ability to regulate lipid metabolism and cholesterol efflux.”
From Deletion of neuronal Idol ameliorates Alzheimer's disease–related pathologies via APOE receptors (2025) · cites this paper as [65]

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Apolipoprotein E exhibits isoform‐specific promotion of lipid efflux from astrocytes and neurons in culture
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P2‐152: Mechanism underlying apolipoprotein E (ApoE) isoform‐dependent HDL generation and impairment of ApoE3‐mediated HDL generation by homocysteine
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Novel action of apolipoprotein E (ApoE): ApoE isoform specifically inhibits lipid-particle-mediated cholesterol release from neurons
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Influence of ApoA-I Structure on the ABCA1-mediated Efflux of Cellular Lipids
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Cell Biology Of ApoE In Cortical Cultured Neurons: Possible Roles In Alzheimer's Disease
Barsukova, A. G. (2003) · Journal of Collective Bargaining in the Academy

Authors: Minagawa, H., Gong, J., Jung, C., Watanabe, A., Lund‐Katz, S., Phillips, M. C., Saito, H., & Michikawa, M.
Affiliations: National Center for Geriatrics and Gerontology (JP)
Children's Hospital of Philadelphia (US)
Kobe Pharmaceutical University (JP)
Corresponding author: Michikawa, Makoto
ORCID: Jung, Cha‐Gyun
Watanabe, Atsushi
Phillips, Michael C.
Saito, Hiroyuki
Michikawa, Makoto
Venue: Journal of Neuroscience Research
Publisher: Wiley
Published: 2009-03-26
Volume: 87
Issue: 11
Pages: 2498-2508
ISSN: 0360-4012 (ISSN-L)
1097-4547
DOI: 10.1002/jnr.22073
PMC: PMC3065888
OpenAlex: W2092006044
Cited by: 90
References: 50
Citations by year: 2026: 5 · 2025: 10 · 2024: 3 · 2023: 6 · 2022: 15 · 2021: 8 · 2020: 10 · 2019: 5 · 2018: 1 · 2017: 6 · 2016: 4 · 2015: 2 · 2014: 2 · 2013: 2 · 2012: 3
FWCI: 3.72
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Neuroscience Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Heart, Lung, and Blood Institute (R01HL056083, HL-56083)
Topics: Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Keywords: apolipoprotein E, APOE isoforms, lipid efflux, APOE3, APOE ε4, N-terminal domain, C-terminal domain, domain-domain interactions, protein dimerization, ABCA1, ABC transporters, neurons, astrocytes, cholesterol efflux
MeSH terms: Animals, Astrocytes, Brain, Cells, Cultured, Central Nervous System Agents, Cholesterol, Glyburide, Humans, Hydroxycholesterols, Mutation, Neurons, Phosphatidylcholines, Time Factors, ATP-Binding Cassette Transporters, Rats, Apolipoprotein E3, Apolipoprotein E4, Protein Multimerization, ATP Binding Cassette Transporter 1

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Mechanism underlying apolipoprotein E (ApoE) isoform‐dependent lipid efflux from neural cells in culture

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