Profile and Regulation of Apolipoprotein E (ApoE) Expression in the CNS in Mice with Targeting of Green Fluorescent Protein Gene to the ApoE Locus

Xu, Qin; Bernardo, Aubrey; Walker, David; Kanegawa, Tiffany; Mahley, Robert W.; Huang, Yadong

doi:10.1523/jneurosci.5476-05.2006

Cited by 524Alzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration MechanismsBarrier Structure and Function Studies

Profile and Regulation of Apolipoprotein E (ApoE) Expression in the CNS in Mice with Targeting of Green Fluorescent Protein Gene to the ApoE Locus

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Xu, Qin, Bernardo, Aubrey, Walker, David, Kanegawa, Tiffany, Mahley, Robert W., Huang, Yadong·2006·The Journal of Neuroscience

DOI 10.1523/jneurosci.5476-05.2006PMC PMC6674234

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Abstract

To study the profile and regulation of apolipoprotein E (apoE) expression in the CNS, we generated mice in which apoE expression can be detected in vivo with unprecedented sensitivity and resolution. cDNA encoding enhanced green fluorescent protein (EGFP) with a stop codon was inserted by gene targeting into the apoE gene locus (EGFP apoE ) immediately after the translation initiation site. Insertion of EGFP into one apoE allele provides a real-time location marker of apoE expression in vivo ; the remaining allele is sufficient to maintain normal cellular physiology. In heterozygous EGFP apoE mice, EGFP was highly expressed in hepatocytes and peritoneal macrophages. EGFP was also expressed in brain astrocytes; however some astrocytes (∼25%) expressed no EGFP, suggesting that a subset of these cells does not express apoE. EGFP was expressed in <10% of microglia after kainic acid treatment, suggesting that microglia are not a major source of brain apoE. Although hippocampal neurons did not express EGFP under normal conditions, kainic acid treatment induced intense expression of EGFP in injured neurons, demonstrating apoE expression in neurons in response to excitotoxic injury. The neuronal expression was confirmed by in situ hybridization of mouse apoE mRNA and by anti-apoE immunostaining. Smooth muscle cells of large blood vessels and cells surrounding small vessels in the CNS also strongly expressed EGFP, as did cells in the choroid plexus. EGFP apoE reporter mice will be useful for studying the regulation of apoE expression in the CNS and might provide insights into the diverse mechanisms of apoE4-related neurodegeneration.

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APOE is a soluble factor expressed by many cell types.
“Insight into APOE4-mediated pathogenesis is complicated by the fact that APOE is a soluble factor expressed by many cell types12,13.”
From APOE4 impairs myelination via cholesterol dysregulation in oligodendrocytes (2022) · cites this paper as [13]
Astrocytes synthesize most of CNS ApoE.
“Because astrocytes synthesize most of CNS ApoE and were the cell type most affected by the global E4 to E2 transition, we generated APOE4s2loxP/loxP/Aldh1l1-CreERT2 APOE switch mice (APOE4s2A) that would express APOE4 in all CNS cell types except for astrocytes, which would selectively transition to APOE2 upon TAM injection29,30 (Fig. 4a).”
From APOE4 to APOE2 allelic switching in mice improves Alzheimer’s disease-related metabolic signatures, neuropathology and cognition (2025) · cites this paper as [29]
APOE is mainly secreted by astrocytes but is also expressed in microglia, neurons, and oligodendrocytes, particularly under injury and degenerative conditions.
“Although mainly secreted by astrocytes, APOE is also expressed in microglia, neurons, and oligodendrocytes, particularly under injury and degenerative conditions. 2 , 13”
From Deletion of neuronal Idol ameliorates Alzheimer's disease–related pathologies via APOE receptors (2025) · cites this paper as [13]
In the central nervous system, APOE is produced predominantly by astrocytes, although it can also be produced by reactive microglia and, to a lesser extent, stressed neurons and other glial cells.
“In the CNS, APOE is produced predominantly by astrocytes, although it can also be produced by reactive microglia and, to a lesser extent, stressed neurons and other glial cells96,97.”
From Multifaceted roles of APOE in Alzheimer disease (2024) · cites this paper as [96]
APOE expression is markedly upregulated by reactive microglia in the brains of individuals with AD.
“its expression is markedly upregulated by reactive microglia in the brains of individuals with AD96,150.”
From Multifaceted roles of APOE in Alzheimer disease (2024) · cites this paper as [96]

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Amyloid β40/42 clearance across the blood-brain barrier following intra-ventricular injections in wild-type, apoE knock-out and human apoE3 or E4 expressing transgenic mice
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Hypomorphic Apolipoprotein E Mice
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APOE ε3/ε4 heterozygotes have an elevated proportion of apolipoprotein E4 in cerebrospinal fluid relative to plasma, independent of Alzheimer’s disease diagnosis
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Expression of apolipoprotein E by cultured vascular smooth muscle cells is controlled by growth state.
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Transcription Factor AP-2 Regulates Human Apolipoprotein E Gene Expression in Astrocytoma Cells
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Sialylated Human Apolipoprotein E (apoEs) Is Preferentially Associated with Neuron-Enriched Cultures from APOE Transgenic Mice
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Identification of a novel enhancer of brain expression near the apoE gene cluster by comparative genomics
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l-Serine-mediated release of apolipoprotein E and lipids from microglial cells
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Neuronal apolipoprotein E is not synthesized in neuron after focal ischemia in rat brain
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The TREM2-APOE Pathway Drives the Transcriptional Phenotype of Dysfunctional Microglia in Neurodegenerative Diseases
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979 · see citing works
Blood-Brain Barrier: From Physiology to Disease and Back
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The glymphatic system: a beginner's guide
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The role of apolipoprotein E in Alzheimer's disease
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Apolipoprotein E and Alzheimer disease: pathobiology and targeting strategies
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APOE4 Causes Widespread Molecular and Cellular Alterations Associated with Alzheimer’s Disease Phenotypes in Human iPSC-Derived Brain Cell Types
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ApoE Promotes the Proteolytic Degradation of Aβ
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Apolipoprotein E: Structure and function in lipid metabolism, neurobiology, and Alzheimer’s diseases
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Apolipoprotein E: from cardiovascular disease to neurodegenerative disorders
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Apolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease
Holtzman, D. M., Herz, J., & Bu, G. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006312 · Cited by 782 · see citing works
Neuron-Astrocyte Metabolic Coupling Protects against Activity-Induced Fatty Acid Toxicity
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ApoE in Alzheimer’s disease: pathophysiology and therapeutic strategies
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Age, APOE and sex: triad of risk of Alzheimer’s disease.
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Apolipoprotein E Is a Ligand for Triggering Receptor Expressed on Myeloid Cells 2 (TREM2)
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CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration
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ApoE and Aβ in Alzheimer’s Disease: Accidental Encounters or Partners?
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Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS
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A Quarter Century of APOE and Alzheimer’s Disease: Progress to Date and the Path Forward
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Central Nervous System Lipoproteins: ApoE and Regulation of Cholesterol Metabolism
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Cholesterol metabolism in neurons and astrocytes
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APOE4 impairs myelination via cholesterol dysregulation in oligodendrocytes
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“Insight into APOE4-mediated pathogenesis is complicated by the fact that APOE is a soluble factor expressed by many cell types 12,13 .”
Background
An Efficient Platform for Astrocyte Differentiation from Human Induced Pluripotent Stem Cells
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Gain of toxic apolipoprotein E4 effects in human iPSC-derived neurons is ameliorated by a small-molecule structure corrector
Wang, C., Najm, R., Xu, Q., Jeong, D.-E., Walker, D., Balestra, M. E., Yoon, S. Y., Yuan, H., Li, G., Miller, Z. A., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0004-z · Cited by 428 · see citing works
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Apolipoprotein e sets the stage: response to injury triggers neuropathology
Mahley, R. W., & Huang, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.11.020 · Cited by 412 · see citing works
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Cholesterol and matrisome pathways dysregulated in astrocytes and microglia
TCW, J., Qian, L., Pipalia, N. H., Chao, M. J., Liang, S. A., Shi, Y., Jain, B. R., Bertelsen, S. E., Kapoor, M., Marcora, E., et al. (2022) · Cell · doi:10.1016/j.cell.2022.05.017 · Cited by 411 · see citing works
Apolipoprotein E in Alzheimer's Disease: An Update
Yu, J.-T., Tan, L., & Hardy, J. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014300 · Cited by 394 · see citing works
ApoE4 Impairs Neuron-Astrocyte Coupling of Fatty Acid Metabolism
Qi, G., Mi, Y., Shi, X., Gu, H., Brinton, R. D., & Yin, F. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108572 · Cited by 379 · see citing works
Lipid accumulation induced by APOE4 impairs microglial surveillance of neuronal-network activity
Victor, M. B., Leary, N., Luna, X., Meharena, H. S., Scannail, A. N., Bozzelli, P. L., Samaan, G., Murdock, M. H., von Maydell, D., Effenberger, A. H., et al. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.07.005 · Cited by 316 · see citing works
Apolipoprotein E4 Impairs Neuronal Insulin Signaling by Trapping Insulin Receptor in the Endosomes
Zhao, N., Liu, C.-C., Van Ingelgom, A. J., Martens, Y. A., Linares, C., Knight, J. A., Painter, M. M., Sullivan, P. M., & Bu, G. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.003 · Cited by 289 · see citing works
GABAergic Interneuron Dysfunction Impairs Hippocampal Neurogenesis in Adult Apolipoprotein E4 Knockin Mice
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Lipid droplets in the nervous system
Ralhan, I., Chang, C.-L., Lippincott-Schwartz, J., & Ioannou, M. S. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202102136 · Cited by 281 · see citing works
The Role of APOE4 in Disrupting the Homeostatic Functions of Astrocytes and Microglia in Aging and Alzheimer’s Disease
Fernandez, C. G., Hamby, M. E., McReynolds, M. L., & Ray, W. J. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00014 · Cited by 277 · see citing works
Lipid and Lipoprotein Metabolism in Microglia
Loving, B. A., & Bruce, K. D. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00393 · Cited by 255 · see citing works
Apolipoprotein E and Alzheimer’s disease: Findings, hypotheses, and potential mechanisms
Koutsodendris, N., Nelson, M. R., Rao, A., & Huang, Y. (2022) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-030421-112756 · Cited by 231 · see citing works
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Cholesterol and Alzheimer’s Disease; From Risk Genes to Pathological Effects
Feringa, F. M., & van der Kant, R. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.690372 · Cited by 226 · see citing works
APOE genotype alters glial activation and loss of synaptic markers in mice
Zhu, Y., Nwabuisi‐Heath, E., Dumanis, S. B., Tai, L. M., Yu, C., Rebeck, G. W., & Ladu, M. J. (2012) · Glia · doi:10.1002/glia.22289 · Cited by 224 · see citing works
Apolipoprotein E4 domain interaction mediates detrimental effects on mitochondria and is a potential therapeutic target for Alzheimer disease
Chen, H.-K., Ji, Z.-S., Dodson, S. E., Miranda, R. D., Rosenblum, C. I., Reynolds, I. J., Freedman, S. B., Weisgraber, K. H., Huang, Y., & Mahley, R. W. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.151084 · Cited by 209 · see citing works
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Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease
Najm, R., Jones, E. A., & Huang, Y. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0324-6 · Cited by 183 · see citing works
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Multifaceted roles of APOE in Alzheimer disease
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Background
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“2,13 APOE binds to cell surface receptors, such as low-density lipoprotein receptor (LDLR), LDLR-related protein 1 (LRP1), very low-density lipoprotein receptor (VLDLR), and apolipoprotein E receptor 2 (APOER2 or LRP8).”

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Authors: Xu, Q., Bernardo, A., Walker, D., Kanegawa, T., Mahley, R. W., & Huang, Y.
Affiliations: Gladstone Institutes (US)
ORCID: Xu, Qin
Walker, David
Mahley, Robert W.
Huang, Yadong
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2006-05-10
Volume: 26
Issue: 19
Pages: 4985-4994
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.5476-05.2006
PMC: PMC6674234
OpenAlex: W1974878596
Cited by: 524
References: 109
Citations by year: 2026: 28 · 2025: 43 · 2024: 40 · 2023: 33 · 2022: 40 · 2021: 43 · 2020: 40 · 2019: 33 · 2018: 21 · 2017: 19 · 2016: 27 · 2015: 21 · 2014: 15 · 2013: 20 · 2012: 16
FWCI: 11.27
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (P01AG022074)
National Heart, Lung, and Blood Institute (R01 HL37063, R01HL037063)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Keywords: apolipoprotein E, green fluorescent protein, astrocytes, microglia, hippocampal neurons, excitotoxic injury, kainic acid, choroid plexus, smooth muscle cells, central nervous system
MeSH terms: Animals, Apolipoproteins E, Brain, Gene Expression Regulation, Microscopy, Fluorescence, Neurons, Gene Targeting, Gene Expression Profiling, Green Fluorescent Proteins, Mice

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Profile and Regulation of Apolipoprotein E (ApoE) Expression in the CNS in Mice with Targeting of Green Fluorescent Protein Gene to the ApoE Locus

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