ApoE4 induces Aβ42, tau, and neuronal pathology in the hippocampus of young targeted replacement apoE4 mice

Liraz, Ori; Boehm-Cagan, Anat; Michaelson, Daniel M

doi:10.1186/1750-1326-8-16

Cited by 118Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

ApoE4 induces Aβ42, tau, and neuronal pathology in the hippocampus of young targeted replacement apoE4 mice

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Liraz, Ori, Boehm-Cagan, Anat, Michaelson, Daniel M·2013·Molecular Neurodegeneration

DOI 10.1186/1750-1326-8-16PMC PMC3659080

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Abstract

Background: Recent findings suggest that the pathological effects of apoE4, the most prevalent genetic risk factor for Alzheimer’s disease (AD), start many years before the onset of the disease and are already detectable at a young age. In the present study we investigated the extent to which such pathological and cognitive impairments also occur in young apoE4 mice. Results: This study revealed that the levels of the presynaptic glutamatergic vesicular transporter, VGlut, in the CA3, CA1, and DG hippocampal subfields were lower in hippocampal neurons of young (4-month-old) apoE4-targeted replacement mice than in those of the apoE3 mice. In contrast, the corresponding inhibitory GABAergic nerve terminals and perikarya were not affected by apoE4. This synaptic effect was associated with hyperphosphorylation of tau in these neurons. In addition, apoE4 increased the accumulation of neuronal Aβ42 and induced mitochondrial changes, both of which were specifically pronounced in CA3 neurons. Spatial navigation behavioral studies revealed that these hippocampal pathological effects of apoE4 are associated with corresponding behavioral impairments. Time-course studies revealed that the effects of apoE4 on tau hyperphosphorylation and the mitochondria were already apparent at the age of 1 month and that the apoE4-driven accumulation of neuronal Aβ and reduced VGlut levels evolve later and are apparent at the age of 2–4 months. Furthermore, the levels of tau phosphorylation decrease in apoE3 mice and increase in apoE4 mice between 1 and 4 months, whereas the levels of Aβ42 decrease in apoE3 mice and are not affected in apoE4 mice over the same time period. Conclusions: These findings show that apoE4 stimulates the accumulation of Aβ42 and hyperphosphorylated tau and reduces the levels of VGlut in hippocampal neurons of young apoE4-targeted replacement mice and that these neurochemical effects are associated with cognitive impairments. This model is not associated with hypothesis-driven mechanistic manipulations and is thus most suitable for unbiased studies of the mechanisms underlying the pathological effects of apoE4.

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Previous studies have reported LTP deficits in APOE4-carrying mice compared to APOE3-carrying mice, in addition to morphological alterations in CA1 hippocampal neurons such as shortened dendritic length, reduced spine density, decreased levels of the presynaptic glutamatergic transporter vGLUT and GABAergic interneuron loss.
“Previous studies have reported LTP deficits in APOE4-carrying mice compared to APOE3-carrying mice, in addition to morphological alterations in CA1 hippocampal neurons such as shortened dendritic length, reduced spine density, decreased levels of the presynaptic glutamatergic transporter vGLUT and GABAergic interneuron loss [79–81].”
From Analysis of early effects of human APOE isoforms on Alzheimer’s disease and type III hyperlipoproteinemia pathways using knock-in rat models with humanized APP and APOE (2024) · cites this paper as [80]
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Both the receptor-binding and lipid-binding regions are critical for ApoE4 fragment-related neurotoxicity and mitochondrial impairment, rather than full-length protein.
“Both regions are thought to be critical for ApoE4 fragment-related neurotoxicity and mitochondrial impairment, rather than full-length protein [29,31].”
From Apoe4 and Alzheimer’s Disease Pathogenesis—Mitochondrial Deregulation and Targeted Therapeutic Strategies (2023) · cites this paper as [31]
The Introduction (page unavailable) associates apoE4 with mitochondrial pathology, and the Results (page unavailable) report altered mitochondrial markers in apoE4 mice. But the paper does not establish that both receptor-binding and lipid-binding regions are critical, or that fragments rather than full-length apoE4 cause neurotoxicity and mitochondrial impairment; the Discussion says the mechanism of the observed effects is unknown. (LLM, conf=0.84)
Experimental — accuracy not yet measured
ApoE4 promotes the accumulation of P-tau especially in CA3 hippocampal neurons of ApoE4-TR mice, accompanied by cognitive deficits.
“previous studies revealed that ApoE4 promotes the accumulation of P-tau especially in CA3 hippocampal neurons of ApoE4-TR mice, which was accompanied by cognitive deficits [31]”
From Apoe4 and Alzheimer’s Disease Pathogenesis—Mitochondrial Deregulation and Targeted Therapeutic Strategies (2023) · cites this paper as [31]

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In Vivo Effects of ApoE and Clusterin on Amyloid-β Metabolism and Neuropathology
Holtzman, D. M. (2004) · Journal of Molecular Neuroscience · doi:10.1385/jmn:23:3:247 · Cited by 138 · see citing works
Apolipoprotein E4 (1–272) fragment is associated with mitochondrial proteins and affects mitochondrial function in neuronal cells
Nakamura, T., Watanabe, A., Fujino, T., Hosono, T., & Michikawa, M. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-35 · Cited by 124 · see citing works
ApoE isoform affects LTP in human targeted replacement mice
Trommer, B. L., Shah, C., Yun, S. H., Gamkrelidze, G., Pasternak, E. S., Ye, G. L., Sotak, M., Sullivan, P. M., Pasternak, J. F., & LaDu, M. J. (2004) · NeuroReport · doi:10.1097/00001756-200412030-00020 · Cited by 124 · see citing works
Lipoprotein receptors and cholesterol in APP trafficking and proteolytic processing, implications for Alzheimer's disease
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Reduced levels of human apoE4 protein in an animal model of cognitive impairment
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Changes in PKC gamma immunoreactivity in mouse hippocampus induced by spatial discrimination learning
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Genetic variation at a single locus and age of onset for Alzheimer's disease
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Activation of the amyloid cascade in apolipoprotein E4 transgenic mice induces lysosomal activation and neurodegeneration resulting in marked cognitive deficits
Belinson, H., Lev, D., Masliah, E., & Michaelson, D. M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5633-07.2008 · Cited by 101 · see citing works
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Functional analysis of APOE locus genetic variation implicates regional enhancers in the regulation of both TOMM40 and APOE
Bekris, L. M., Lutz, F., & Yu, C. (2011) · Journal of Human Genetics · doi:10.1038/jhg.2011.123 · Cited by 98 · see citing works
Dominant negative effects of apolipoprotein E4 revealed in transgenic models of neurodegenerative disease
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APOE related alterations in cerebral activation even at college age
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Apolipoprotein E and β‐amyloid (1–42) regulation of glycogen synthase kinase‐3β
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Positive Effects of Cholinergic Stimulation Favor Young APOE ɛ4 Carriers
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Molecular dissection of the paired helical filament
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Accelerated hippocampal atrophy in Alzheimer's disease with apolipoprotein E ε4 allele
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Spectroscopic Studies of GSK3β Phosphorylation of the Neuronal Tau Protein and Its Interaction with the N-Terminal Domain of Apolipoprotein E
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Preferential accumulation of amyloid-beta in presynaptic glutamatergic terminals (VGluT1 and VGluT2) in Alzheimer's disease cortex
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Differences in apolipoprotein E3/3 and E4/4 allele-specific gene expression in hippocampus in Alzheimer disease
Xu, P., Li, Y., Qin, X., Scherzer, C. R., Xu, H., Schmechel, D. E., Hulette, C. M., Ervin, J. F., Gullans, S. R., Haines, J. L., et al. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.07.004 · Cited by 76 · see citing works
Aβ42 neurotoxicity in primary co-cultures: effect of apoE isoform and Aβ conformation
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ApoE ε4 is associated with eIF2α phosphorylation and impaired learning in young mice
Segev, Y., Michaelson, D. M., & Rosenblum, K. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.06.020 · Cited by 69 · see citing works
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Progressive loss of synaptic integrity in human apolipoprotein E4 targeted replacement mice and attenuation by apolipoprotein E2
Klein, R. C., Mace, B. E., Moore, S. D., & Sullivan, P. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.027 · Cited by 67 · see citing works
The Isoform-Specific Pathological Effects of ApoE4 in vivo are Prevented by a Fish Oil (DHA) Diet and are Modified by Cholesterol
Kariv-Inbal, Z., Yacobson, S., Berkecz, R., Péter, M., Janáky, T., Lütjohann, D., Broersen, L. M., Hartmann, T., & Michaelson, D. M. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-111265 · Cited by 65 · see citing works
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Synaptic loss is accompanied by an increase in synaptic area in the dentate gyrus of aged human apolipoprotein E4 transgenic mice
Cambon, K., Davies, H. A., & Stewart, M. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00065-8 · Cited by 63 · see citing works
Cognitive Function and Apolipoprotein E in Very Old Adults: Findings From the Nun Study
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Molecular signatures in post-mortem brain tissue of younger individuals at high risk for Alzheimer’s disease as based on APOE genotype
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Quantitative analysis of GAD65 and GAD67 immunoreactivities in somata of GABAergic neurons in the mouse hippocampus proper (CA1 and CA3 regions), with special reference to parvalbumin-containing neurons
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A SAGE study of apolipoprotein E3/3, E3/4 and E4/4 allele-specific gene expression in hippocampus in Alzheimer disease
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Mechanisms of synaptic pathology in Alzheimer’s disease
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Spatial navigation in the Morris water maze: working and long lasting reference memories
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ApoE4-dependent Aβ-mediated neurodegeneration is associated with inflammatory activation in the hippocampus but not the septum
Belinson, H., & Michaelson, D. M. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0218-9 · Cited by 38 · see citing works
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Developmental expression of tau proteins in the chicken and rat brain: Rapid down‐regulation of a paired helical filament epitope in the rat cerebral cortex coincides with the transition from immature to adult tau isoforms
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Following Activation of the Amyloid Cascade, Apolipoprotein E4 Drives the in vivo Oligomerization of Amyloid-β Resulting in Neurodegeneration
Belinson, H., Kariv-Inbal, Z., Kayed, R., Masliah, E., & Michaelson, D. M. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101008 · Cited by 24 · see citing works
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ApoE4‐Driven Accumulation of Intraneuronal Oligomerized Aβ42 following Activation of the Amyloid Cascade In Vivo Is Mediated by a Gain of Function
Zepa, L., Frenkel, M., Belinson, H., Kariv-Inbal, Z., Kayed, R., Masliah, E., & Michaelson, D. M. (2011) · International Journal of Alzheimer’s Disease · doi:10.4061/2011/792070 · Cited by 23 · see citing works
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Differential phosphorylation of tau proteins during kitten brain development and Alzheimer's disease
Riederer, B. M., Mourton-Gilles, C., Frey, P., Delacourte, A., & Probst, A. (2001) · Journal of Neurocytology · doi:10.1023/a:1011991207942 · Cited by 22 · see citing works
Phosphorylation state of tau in the hippocampus of apolipoprotein E4 and E3 knock-in mice
Kobayashi, M., Ishiguro, K., Fukui, Y., Yokoyama, M., & Fujita, S. C. (2003) · Neuroreport · doi:10.1097/00001756-200304150-00008 · Cited by 21 · see citing works
Possible Role of Tau in Mediating Pathological Effects of apoE4 in vivo prior to and following Activation of the Amyloid Cascade
Inbar, D., Belinson, H., Rosenmann, H., & Michaelson, D. M. (2010) · Neurodegenerative Diseases · doi:10.1159/000283477 · Cited by 14 · see citing works
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The Effects of Apolipoproteins E3 and E4 on the Transforming Growth Factor-β System in Targeted Replacement Mice
Haas, A., Liraz, O., & Michaelson, D. M. (2012) · Neurodegenerative Diseases · doi:10.1159/000334902 · Cited by 11 · see citing works
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[Amyloid PET in Alzheimer research].
Ishii, K. (2010) · PubMed · Cited by 1 · see citing works

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Michaelson DM Ishai L Ori L Anat B Alex N Counteracting the pathological effects of apoE4 in vivo with anti apoE4 mAbs ApoE, ApoE Receptors & Neurodegeneration Symposium; Mayo Clinic Jacksonville Florida 201223677929

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Amyloid toxicity in Alzheimer’s disease
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Genome-wide association study identifies four novel loci associated with Alzheimer’s endophenotypes and disease modifiers
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Impaired Autophagy in APOE4 Astrocytes
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APOE genotype and stress response - a mini review
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Omega-3 fatty acids, lipids, and apoE lipidation in Alzheimer's disease: a rationale for multi-nutrient dementia prevention
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How Can Insulin Resistance Cause Alzheimer’s Disease?
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Altered ubiquitin signaling induces Alzheimer’s disease-like hallmarks in a three-dimensional human neural cell culture model
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Microglia‐specific <scp>ApoE</scp> knock‐out does not alter Alzheimer's disease plaque pathogenesis or gene expression
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Astrocytic expression of the Alzheimer’s disease risk allele, ApoEε4, potentiates neuronal tau pathology in multiple preclinical models
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Hippocampus-related cognitive impairments in young apoE4 targeted replacement mice
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Chronic exposure to chlorpyrifos triggered body weight increase and memory impairment depending on human apoE polymorphisms in a targeted replacement mouse model
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Associations Between ApoEε4 Carrier Status and Serum BDNF Levels—New Insights into the Molecular Mechanism of ApoEε4 Actions in Alzheimer’s Disease
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Differential effects of apoE4 and activation of ABCA1 on brain and plasma lipoproteins
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Glutamine Antagonist JHU-083 Normalizes Aberrant Hippocampal Glutaminase Activity and Improves Cognition in APOE4 Mice
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Expression of Human Apolipoprotein E4 in Neurons Causes Hyperphosphorylation of Protein Tau in the Brains of Transgenic Mice
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Authors: Liraz, O., Boehm-Cagan, A., & Michaelson, D. M.
Affiliations: Tel Aviv University (IL)
Corresponding author: Michaelson, Daniel M
ORCID: Michaelson, Daniel M
Venue: Molecular Neurodegeneration
Publisher: Springer Science and Business Media LLC
Published: 2013-05-17
Volume: 8
Issue: 1
Pages: 16-16
ISSN: 1750-1326 (ISSN-L)
DOI: 10.1186/1750-1326-8-16
PMC: PMC3659080
OpenAlex: W2096068616
Cited by: 118
References: 103
Citations by year: 2026: 7 · 2025: 14 · 2024: 11 · 2023: 6 · 2022: 5 · 2021: 10 · 2020: 7 · 2019: 12 · 2018: 7 · 2017: 10 · 2016: 9 · 2015: 7 · 2014: 11 · 2013: 2
FWCI: 6.73
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Molecular Neurodegeneration (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: European Commission
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: APOE ε4, Alzheimer's disease, amyloid-beta 42, tau hyperphosphorylation, vesicular glutamate transporter, glutamatergic neurotransmission, hippocampus, CA3 neurons, mitochondrial dysfunction, GABAergic synapses, APOE3, targeted replacement mice
MeSH terms: Aging, Alzheimer Disease, Animals, Behavior, Animal, Cognition Disorders, Enzyme-Linked Immunosorbent Assay, Fluorescent Antibody Technique, Hippocampus, Humans, Immunohistochemistry, Mice, Transgenic, Neurons, Phosphorylation, Immunoblotting, Amyloid beta-Peptides, tau Proteins, Microscopy, Confocal, Genetic Predisposition to Disease, Vesicular Glutamate Transport Proteins, Mice, Apolipoprotein E4

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ApoE4 induces Aβ42, tau, and neuronal pathology in the hippocampus of young targeted replacement apoE4 mice

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