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Human APOE Isoform-Dependent Effects on Brain β-Amyloid Levels in PDAPP Transgenic Mice
Open accessAbstract
To investigate the role of human apolipoprotein E (apoE) on Abeta deposition in vivo, we crossed PDAPP mice lacking mouse Apoe to targeted replacement mice expressing human apoE (PDAPP/TRE2, PDAPP/TRE3, or PDAPP/TRE4). We then measured the levels of apoE protein and Abeta peptides in plasma, CSF, and brain homogenates in these mice at different ages. We also quantified the amount of brain Abeta and amyloid burden in 18-month-old mice. In young PDAPP/TRE4 mice that were analyzed at an age before brain Abeta deposition, we observed a significant decrease in the levels of apoE in CSF and brain when compared with age-matched mice expressing either human E2 or E3. The brain levels of Abeta42 in PDAPP/TRE4 mice were substantially elevated even at this very early time point. In older PDAPP/TRE4 mice, the levels of insoluble apoE protein increased in parallel to the dramatic rise in brain Abeta burden, and the majority of apoE was associated with Abeta. In TRE4 only mice, we also observed a significant decrease in the level of apoE in brain homogenates. Since the relative level of apoE mRNA was equivalent in PDAPP/TRE and TRE only mice, it appears that post-translational mechanisms influence the levels of apoE protein in brain (E4 < E3 << E2), resulting in early and dramatic apoE isoform-dependent effects on brain Abeta levels (E4 >> E3 > E2) that increase with age. Therapeutic strategies aimed at increasing the soluble levels of apoE protein, regardless of isoform, may effectively prevent and (or) treat Alzheimer's disease.
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In the citing paper
“Plaque deposition is increased with APOE4 compared with APOE2 and APOE3 in humans and transgenic mice expressing familial AD (FAD) mutations (FAD-Tg) (2)(3)(4)(5).”
From APOE4-specific Changes in Aβ Accumulation in a New Transgenic Mouse Model of Alzheimer Disease (2012) · cites this paper as [3]
In the citing paper
“For example, crossing apoE-targeted replacement mice (apoE-TR) (9) with PDAPP mice (10) delays plaque deposition from ϳ10 to 18 months, although once detected, plaque levels are greater with APOE4 than APOE3 (3).”
From APOE4-specific Changes in Aβ Accumulation in a New Transgenic Mouse Model of Alzheimer Disease (2012) · cites this paper as [3]
In the citing paper
“Introduction of human APOE to existing FAD-Tg mice significantly delays plaque deposition, although once detected, plaque levels are generally greater with APOE4 than APOE3 (3, 6 -8).”
From APOE4-specific Changes in Aβ Accumulation in a New Transgenic Mouse Model of Alzheimer Disease (2012) · cites this paper as [3]
In the citing paper
“Crossing a transgenic mouse model of AD that has high levels of human Aβ in the brain with human APOE targeted replacement mice demonstrated age-dependent and APOE isoform-dependent (E4>>E3>E2) Aβ deposition and amyloid burden in the brain in a manner that recapitulates the human condition observed in pre-symptomatic elderly APOE4 carriers as well as AD patients.18–21”
From AAVrh.10-Mediated APOE2 Central Nervous System Gene Therapy for APOE4-Associated Alzheimer's Disease (2018) · cites this paper as [18]
In the citing paper
“Even in homozygous APOE2/2 mice, prior reports have been inconsistent regarding further reductions in amyloid pathology compared with APOE3/3 , re fl ecting ongoing debate 34,48,49 .”
From APOE2 attenuates APOE4-associated amyloid pathology and related toxicity in a mouse model of Alzheimer’s disease (2026) · cites this paper as [49]
In the citing paper
“we and others have reported human apoE isoform-dependent differences in amyloid plaque deposition in APP-transgenic mice (E4 > E3 > E2) (10-14).”
From Human ApoE isoforms differentially regulate brain amyloid-β peptide clearance (2011) · cites this paper as [14]
In the citing paper
“Although there are some conflicting studies (61), several groups have reported that the concentration of apoE in the brains of human apoE knock-in mice varies in an apoE isoform-dependent manner, that is, E2>E3>E4 (14, 62, 63).”
From Human ApoE isoforms differentially regulate brain amyloid-β peptide clearance (2011) · cites this paper as [14]
In the citing paper
“though apoE concentration differences are unlikely to completely account for Aβ metabolism differences in the setting of apoE3 versus apoE4 (14)”
From Human ApoE isoforms differentially regulate brain amyloid-β peptide clearance (2011) · cites this paper as [14]
In the citing paper
“APOE isoform-dependent amyloid deposition has been consistently observed in humans and Aβ depositing mouse models (Holtzman et al., 2000; Bales et al., 2009; Reiman et al., 2009; Morris et al., 2010).”
From Haploinsufficiency of Human APOE Reduces Amyloid Deposition in a Mouse Model of Amyloid-β Amyloidosis (2011) · cites this paper as Bales et al., 2009
In the citing paper
“In fact, we have previously demonstrated that APP/ε4 and PDAPP/ε4 mice have greatly increased content of apoE within Aβ deposits compared to the same Tg mice lines expressing other human APOE alleles [19, 36].”
From APOE Genotype Differentially Modulates Effects of Anti-Aβ, Passive Immunization in APP Transgenic Mice (2017) · cites this paper as [36]
In the citing paper
“VAβ is detrimental to the function of cerebrovascular circulation through compromising blood–brain-barrier integrity [49], effecting hemodynamic dysfunction [29, 50], and facilitating occurrence of spontaneous hemorrhages [25, 26, 36].”
From APOE Genotype Differentially Modulates Effects of Anti-Aβ, Passive Immunization in APP Transgenic Mice (2017) · cites this paper as [36]
In the citing paper
“Thus far, the differential effect of targeted ApoE isoform replacement on Ab pathology has been reproduced in single APP V717F mice, which had to be at least 18 months of age to observe substantial Ab load.56,57”
From Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration (2013) · cites this paper as [56]
In the citing paper
“there are apoE isoform-dependent effects (E4>E3>E2) on promoting brain Aβ deposition in PDAPP transgenic mice”
From ApoE4 reduction: An emerging and promising therapeutic strategy for Alzheimer's disease (2022) · cites this paper as Bales et al 2009
In the citing paper
“APOE4-targeted replacement mice, expressing the human APOE4 allele instead of the mouse Apoe, crossed with different AD mouse models such as PDAPP, APP/ PS1ΔE9 and 5xFAD, accelerated plaque formation compared to APOE3-targeted replacement mice (Bales et al, 2009; Castellano et al, 2011; Fagan et al, 2002; Holtzman et al, 2000a; Rodriguez et al, 2014; Youmans et al, 2012).”
From APOE from astrocytes restores Alzheimer’s Aβ-pathology and DAM-like responses in APOE deficient microglia (2024) · cites this paper as Bales et al, 2009
In the citing paper
“Nevertheless other studies have also reported that APOE2 expression is associated with similar or even higher plaque load than APOE3 (Rodriguez et al, 2014; Youmans et al, 2012; Bales et al, 2009; Dodart et al, 2005).”
From APOE from astrocytes restores Alzheimer’s Aβ-pathology and DAM-like responses in APOE deficient microglia (2024) · cites this paper as Bales et al, 2009
In the citing paper
“It has also been shown that APOE2 expression leads to increased APOE levels in mouse models and human brain (Riddell et al, 2008; Bales et al, 2009; Conejero-Goldberg et al, 2014), which can influence amyloid pathology.”
From APOE from astrocytes restores Alzheimer’s Aβ-pathology and DAM-like responses in APOE deficient microglia (2024) · cites this paper as Bales et al, 2009
In the citing paper
“Recently, PDAPP mice bred to apoE2, E3, and apoE4 knock-in mice demonstrated a clear isoform-dependent (E4>E3>E2) effect on Aβ accumulation (Bales et al., 2009).”
From The role of apolipoprotein E in Alzheimer's disease (2009) · cites this paper as Bales et al., 2009
In the citing paper
“In agreement with our data, significantly reduced ApoE levels were also observed in hiPSC-derived ApoE4 astrocytes [15,16,24], as well as in brain homogenates from mouse models expressing the human ApoE4 isoform [43,44].”
From ApoE3 vs. ApoE4 Astrocytes: A Detailed Analysis Provides New Insights into Differences in Cholesterol Homeostasis (2022) · cites this paper as [44]
In the citing paper
“This is further complicated by the fact that expression of different isoforms of human ApoE in transgenic mice results in different levels of plaque and CAA burden with apoE4 expression enhancing amyloid deposition compared to apoE3 or apoE2 [3, 21, 40, 59, 86, 178].”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [3]
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Metadata
- Authors
- Bales, K. R., Liu, F., Wu, S., Lin, S., Koger, D., DeLong, C., Hansen, J. C., Sullivan, P. M., & Paul, S. M.
- Affiliations
- Eli Lilly (United States) (US)
- Duke University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-05-27
- Volume
- 29
- Issue
- 21
- Pages
- 6771-6779
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6665579
- OpenAlex
- W2066673859
- Cited by
- 274
- References
- 53
- Citations by year
- 2026: 2 · 2025: 13 · 2024: 16 · 2023: 14 · 2022: 18 · 2021: 12 · 2020: 20 · 2019: 12 · 2018: 13 · 2017: 22 · 2016: 15 · 2015: 12 · 2014: 22 · 2013: 18 · 2012: 24
- FWCI
- 14.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › 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
- apolipoprotein E, APOE isoforms, amyloid-beta deposition, amyloid burden, cerebrospinal fluid, brain amyloid, amyloid-beta 42, post-translational regulation, Alzheimer's disease
- MeSH terms
- Age Factors, Analysis of Variance, Animals, Apolipoproteins E, Brain, Humans, Mice, Inbred C57BL, Mice, Transgenic, Mutation, Peptide Fragments, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Protein Isoforms, Mice
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