Cited by 499Alzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration MechanismsNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 52 of the 52 references it cites were found in a registry or an index; 32 of the 43 sources its claims cite were checked for support.

APOE4 impairs myelination via cholesterol dysregulation in oligodendrocytes

Open access

Abstract

APOE4 is the strongest genetic risk factor for Alzheimer's disease 1-3. However, the effects of APOE4 on the human brain are not fully understood, limiting opportunities to develop targeted therapeutics for individuals carrying APOE4 and other risk factors for Alzheimer's disease 4-8. Here, to gain more comprehensive insights into the impact of APOE4 on the human brain, we performed single-cell transcriptomics profiling of post-mortem human brains from APOE4 carriers compared with non-carriers. This revealed that APOE4 is associated with widespread gene expression changes across all cell types of the human brain. Consistent with the biological function of APOE 2-6, APOE4 significantly altered signalling pathways associated with cholesterol homeostasis and transport. Confirming these findings with histological and lipidomic analysis of the post-mortem human brain, induced pluripotent stem-cell-derived cells and targeted-replacement mice, we show that cholesterol is aberrantly deposited in oligodendrocytes-myelinating cells that are responsible for insulating and promoting the electrical activity of neurons. We show that altered cholesterol localization in the APOE4 brain coincides with reduced myelination. Pharmacologically facilitating cholesterol transport increases axonal myelination and improves learning and memory in APOE4 mice. We provide a single-cell atlas describing the transcriptional effects of APOE4 on the aging human brain and establish a functional link between APOE4, cholesterol, myelination and memory, offering therapeutic opportunities for Alzheimer's disease.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

APOE4 is associated with widespread transcriptomic changes in the aged human brain, including cholesterol dysregulation in oligodendrocytes and reduced myelination. Facilitating cholesterol transport with cyclodextrin increases myelination and improves learning and memory in APOE4/4 targeted-replacement mice.

Key findings

  • Single-nucleus RNA-sequencing of post-mortem prefrontal cortex from 32 subjects (12 APOE3/3, 12 APOE3/4, 8 APOE4/4) yielded 178,789 nuclei (164,741 after QC); APOE4 was associated with 486 candidate perturbed GO Biological Processes, including 404 cell-type-specific and 82 broadly dysregulated pathways.
  • APOE4 oligodendrocytes showed dose-dependent increases in cholesterol-related gene expression (4/4 > 3/4 > 3/3, p = 0.01) and altered cholesterol localization: in APOE4-carriers, Bodipy-cholesterol along neurofilaments decreased from 58% to 19% (p = 0.0106), with higher mean Bodipy-cholesterol intensity (p = 0.0220).
  • APOE4 was associated with reduced myelination: post-mortem APOE3/4 PFC had reduced Black Gold II area (p = 0.0031) and reduced MBP immunoreactivity (p = 0.0027 and p = 0.0294); APOE4/4 corpus callosum had higher g-ratios (p < 0.0001); APOE4/4-TR mice had fewer myelinated axons (p = 0.0265) and higher g-ratios (p < 0.0001).
  • Cyclodextrin treatment increased MBP colocalization with neurofilament in APOE4/4 iPSC co-cultures by 43% ± 5% (p = 0.0274), reduced g-ratio in APOE4/4-TR mice (p < 0.0001), increased MBP immunoreactivity (p = 0.0008), increased novel object preference (p = 0.0466), and decreased Puzzle Box latency (p = 0.02).

Methods

  • Post-mortem human prefrontal cortex from ROSMAP was profiled by 10x Genomics snRNA-seq; nuclei were clustered with ACTIONet, differential expression was modeled with NEBULA negative binomial mixed models, and pathway activity was analyzed with GSVA and Limma.
  • Lipidomic profiling used mass spectrometry on post-mortem corpus callosum (APOE4/4 n = 3, all female; APOE3/3 n = 3, all female) and a separate prefrontal cortex dataset of 314 individuals; isogenic APOE3/3 and APOE4/4 iPSC-derived oligodendroglia and iNeuron co-cultures, plus APOE targeted-replacement mice, were used for functional and histological validation.
  • Pharmacological experiments treated APOE4/4 iPSC-derived oligodendroglia with simvastatin, atorvastatin, or cyclodextrin, and treated APOE4/4-TR mice with subcutaneous cyclodextrin (2 g/kg twice weekly for eight weeks) or saline; myelination was assessed by imaging and TEM, and cognition by novel object recognition and Puzzle Box tasks.

Limitations

  • The paper states that additional well-powered lipidomic analyses designed to quantify cholesteryl esters in post-mortem tissue are needed; the corpus callosum lipidomic comparison had n = 3 per genotype and showed only a trend toward higher cholesteryl esters (p ≥ 0.7).
  • The paper states that genetic diversity may confound APOE4 effects observed in post-mortem human brain tissue, motivating the use of isogenic iPSC lines and APOE-TR mice; it also notes that covariates inherent to post-mortem human samples were controlled by quantifying myelin in inbred APOE-TR mice.
  • The paper states that power analysis to determine sample size was not performed and that experimenters were not blinded to drug injections or behavioral trials (TEM analysis was blinded); evident from the text, several human and mouse experiments used small samples, such as n = 3 per genotype for human TEM and Black Gold II staining and n = 4–5 mice per group for in vivo cyclodextrin histology/TEM.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1038/s41586-022-05439-w

Cites

52 of 52 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

108 Own result · 54 Own interpretation · 26 Own method · 12 Partly supported · 5 Supported · 4 No full text of the sources · 2 Supported so far · 1 No basis given · accuracy not yet measured

Show all 122 claims

  • Probably not a substantial claim. 40
  • It may state two separate claims as one. 59
  • The quote only partly states this claim. 1
90 of 90
  • The paper relies on this without support.

    The mechanisms by which APOE4 mediates its effects on amyloid-β deposition, tau pathology, and cognitive decline are not fully understood.

    “However, the mechanisms by which APOE4 mediates these effects are not fully understood.”
  • The paper relies on this without support.

    How cholesterol and lipid abnormalities impair learning and memory in the APOE4 brain, and whether such effects can be mitigated, remains unclear.

    “Despite these longstanding associations, how cholesterol and lipid abnormalities impair learning and memory in the APOE4 brain, and whether such effects can be mitigated, remains unclear.”
  • The paper relies on this without support.

    APOE is a lipid and cholesterol transporter.

    “APOE is a lipid and cholesterol transporter.”
  • The paper relies on this without support.

    Genetic diversity may confound the effects of APOE4 observed on human post-mortem brain tissue.

    “Genetic diversity may confound the effects of APOE4 observed on human post-mortem brain tissue.”
  • The paper relies on this without support.

    APOE-TR mice recapitulate human APOE4 effects on myelination sufficiently for conclusions about human APOE4.

    “To control for covariates inherent to post-mortem human samples, we also quantified myelin levels in inbred APOE-TR mice (9 months old, male and female mice; n = 4 per genotype).”
  • The paper relies on this without support.

    Isogenic iPSC-derived oligodendroglia and iNeuron co-cultures model human oligodendrocyte myelination sufficiently for conclusions about human APOE4.

    “To investigate this, we employed an in vitro myelination assay using isogenic iPSC-derived oligodendroglia co-cultured with NGN2-induced neurons derived from the same iPSCs (iNeurons) in a three-dimensional extracellular matrix that allows cells to interact with each other and self-assemble into tissue-like structures (Extended Data Fig. 9a).”
  • The paper relies on this without support.

    MBP immunoreactivity and g-ratio are valid measures of myelin levels.

    “To quantify relative myelin levels per axon, we calculated the g-ratio (the inner axonal diameter divided by the outer diameter with myelin sheath) for 150 neurons per condition.”
  • The paper relies on this without support.

    Bodipy-cholesterol and filipin staining reflect intracellular cholesterol localization and storage.

    “To further characterize APOE4-mediated differences in cholesterol storage, we stained isogenic APOE3/3 and APOE4/4 oligodendroglia with the cholesterol dye filipin, Bodipy-cholesterol, and lipid-droplet associated PLIN1.”
  • The paper relies on this without support.

    Cyclodextrin’s beneficial effects on myelination and cognition in APOE4 mice are mediated by facilitating cholesterol transport.

    “Collectively, these data demonstrate that pharmacological enhancement of cholesterol transport can improve APOE4 myelination in vitro and in vivo.”
9 of 9

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

1 of 1

Citations

Cites

Show all 48 references

Cited by

Sorted by citations

Metadata

Authors
Blanchard, J. W., Akay, L. A., Davila-Velderrain, J., von Maydell, D., Mathys, H., Davidson, S. M., Effenberger, A., Chen, C.-Y., Maner-Smith, K., Hajjar, I., Ortlund, E. A., Bula, M., Agbas, E., Ng, A., Jiang, X., Kahn, M., Blanco-Duque, C., Lavoie, N., Liu, L., Reyes, R., Lin, Y.-T., Ko, T., R’Bibo, L., Ralvenius, W. T., Bennett, D. A., Cam, H. P., Kellis, M., & Tsai, L.-H.
Affiliations
  • Massachusetts Institute of Technology (US)
  • MIT Computer Science and Artificial Intelligence Laboratory (US)
  • University of Pittsburgh (US)
  • Princeton University (US)
  • Emory University (US)
  • Icahn School of Medicine at Mount Sinai (US)
  • Rush University Medical Center (US)
  • Broad Institute (US)
Corresponding author
  • Kellis, Manolis
  • Tsai, Li-Huei
Venue
Nature
Published
2022-11-16
Volume
611
Issue
7937
Pages
769-779
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W4309507742
Cited by
496
References
48
Citations by year
2026: 105 · 2025: 161 · 2024: 118 · 2023: 102 · 2022: 7
FWCI
33.92
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
Funders
  • National Institute on Aging (R01AG017917, K24AG062786, R01AG058002, RF1AG057470, RF1AG054012, U01AG046152, R01AG015819, P30AG010161, RF1AG062377, U01AG061356, RF1AG051633, P30AG072975)
  • National Human Genome Research Institute (U54HG008097)
  • National Institute of Neurological Disorders and Stroke (U01NS110453, UH3NS115064, UG3NS115064, R01NS114239)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
APOE ε4, Alzheimer's disease, myelination, oligodendrocytes, cholesterol homeostasis, cholesterol transport, single-cell transcriptomics, postmortem brain, brain aging, learning and memory, axonal myelination, lipidomics, induced pluripotent stem cell-derived cells, targeted replacement mice
MeSH terms
Aging, Alzheimer Disease, Animals, Autopsy, Biological Transport, Brain, Cholesterol, Heterozygote, Homeostasis, Humans, Memory, Myelin Sheath, Nerve Fibers, Myelinated, Neurons, Oligodendroglia, Gene Expression Profiling, Mice, Apolipoprotein E4, Induced Pluripotent Stem Cells, Single-Cell Analysis

About these checks

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.

A language model drew the claims from the paper on 2026-10-11, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).

A second model labelled each claim on 2026-10-11 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).

Cited sources are checked with a language model’s help (gpt-6-sol).

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review