Apolipoprotein E, gender, and Alzheimer’s disease: an overlooked, but potent and promising interaction

Ungar, Leo; Altmann, Andre; Greicius, Michael D.

doi:10.1007/s11682-013-9272-x

Cited by 259Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsMedicinal Plants and Neuroprotection

Apolipoprotein E, gender, and Alzheimer’s disease: an overlooked, but potent and promising interaction

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Ungar, Leo, Altmann, Andre, Greicius, Michael D.·2014·Brain Imaging and Behavior

DOI 10.1007/s11682-013-9272-xPMC PMC4282773

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Abstract

Alzheimer's disease (AD) is an increasingly prevalent, fatal neurodegenerative disease that has proven resistant, thus far, to all attempts to prevent it, forestall it, or slow its progression. The ε4 allele of the Apolipoprotein E gene (APOE4) is a potent genetic risk factor for sporadic and late-onset familial AD. While the link between APOE4 and AD is strong, many expected effects, like increasing the risk of conversion from MCI to AD, have not been widely replicable. One critical, and commonly overlooked, feature of the APOE4 link to AD is that several lines of evidence suggest it is far more pronounced in women than in men. Here we review previous literature on the APOE4 by gender interaction with a particular focus on imaging-related studies.

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The APOE-e4 genotype may have a stronger association with Alzheimer's dementia and neurodegeneration in women than in men.
“the APOE-e4 genotype, the best known common genetic risk factor for Alzheimer's dementia, may have a stronger association with Alzheimer's dementia 285,286 and neurodegeneration 287 in women than in men.”
From 2023 Alzheimer's disease facts and figures (2023) · cites this paper as [286]
The link between Alzheimer's disease and APOE4 is more prominent in women than in men.
“At molecular levels, the link between AD and a genetic risk factor, APOE4 is much more prominent in women than men [7, 8].”
From Sex specific molecular networks and key drivers of Alzheimer’s disease (2023) · cites this paper as [8]

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Treatment outcome of tacrine therapy depends on apolipoprotein genotype and gender of the subjects with Alzheimer's disease
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Differential effects of the APOE genotype on brain function across the lifespan
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Alzheimer's Disease, Apolipoprotein E4, and Gender
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Evidence for an Interaction between Apolipoprotein E Genotype, Gender, and Alzheimer Disease
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Cerebrospinal fluid β-amyloid1–42 and tau in control subjects at risk for Alzheimer’s disease: The effect of APOE ε4 allele
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Serial MRI and CSF biomarkers in normal aging, MCI, and AD
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APOE genotype and cognitive functioning in a large age-stratified population sample.
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Middle-aged human apoE4 targeted-replacement mice show retention deficits on a wide range of spatial memory tasks.
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Postmenopausal hormone therapy and cognitive outcomes: The Women's Health Initiative Memory Study (WHIMS)
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Sex differences in the association of the apolipoprotein E epsilon 4 allele with incidence of dementia, cognitive impairment, and decline
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On Jim Watson's APOE status: genetic information is hard to hide
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Disease Tracking Markers for Alzheimer's Disease at the Prodromal (MCI) Stage
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Age and Apolipoprotein E*4 Allele Effects on Cerebrospinal Fluid β-Amyloid 42 in Adults With Normal Cognition
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The apolipoprotein E ε2 allele is associated with an increased risk of early‐onset alzheimer's disease and a reduced survival
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The effects of APOE on the functional architecture of the resting brain
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The absence of an apolipoprotein ϵ4 allele is associated with a more aggressive form of Alzheimer's disease
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Effects of Age, Sex, and Ethnicity on the Association Between Apolipoprotein E Genotype and Alzheimer Disease: A Meta-analysis
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“In studies with long-lived subjects, the APOE4 effect is detectable in age of onset but is diminished in terms of overall risk, such that beyond age 80 there is little additional risk attributable to APOE4 (Blacker et al. 1997; Dickson et al. 2008; Farrer et al. 1997; Khachaturian et al. 2004).”
Influential
Predictive Utility of Apolipoprotein E Genotype for Alzheimer Disease in Outpatients With Mild Cognitive Impairment
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Gender and age modify the association between APOE and AD-related neuropathology
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Differential Cross-Sectional and Longitudinal Impact of APOE Genotype on Hippocampal Volumes in Nondemented Older Adults
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Reduced size of right hippocampus in 39- to 80-year-old normal subjects carrying the apolipoprotein E ϵ4 allele
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No ɛ4 gene dose effect on hippocampal atrophy in a large MRI database of healthy elderly subjects
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Postmenopausal hormone therapy, timing of initiation, APOE and cognitive decline
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Apolipoprotein E ε4 Allele Is Unrelated to Cognitive or Functional Decline in Alzheimer’s Disease: Retrospective and Prospective Analysis
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Specifically Progressive Deficits of Brain Functional Marker in Amnestic Type Mild Cognitive Impairment
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Apolipoprotein E Phenotypes, Dementia and Mortality in a Prospective Population Sample
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Presence or absence of at least one epsilon 4 allele and gender are not predictive for the response to donepezil treatment in Alzheimer's disease.
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Effects of ApoE-ɛ4 allele load and age on the rates of grey matter and hippocampal volumes loss in a longitudinal cohort of 1186 healthy elderly persons
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Apolipoprotein E Genotype is Associated with Temporal and Hippocampal Atrophy Rates in Healthy Elderly Adults: A Tensor-Based Morphometry Study1
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APOE genotype and survival in men and women with Alzheimer’s disease
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Working memory deficits in healthy APOE epsilon 4 carriers
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Integrating ADNI results into Alzheimer's disease drug development programs
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Apolipoprotein E genotype and progression of Alzheimer's disease: the Rotterdam Study
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Accelerated Memory Decline in Alzheimer's Disease With Apolipoprotein ϵ4 Allele
Hirono, N., Hashimoto, M., Yasuda, M., Kazui, H., & Mori, E. (2003) · Journal of Neuropsychiatry · doi:10.1176/jnp.15.3.354 · Cited by 54 · see citing works
Aging, Estrogens, and Episodic Memory in Women
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Apolipoprotein E 4 and impaired episodic memory in community-dwelling elderly people: a marked sex difference. The Hordaland Health Study
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Predicting memory decline in normal elderly: Genetics, MRI, and cognitive reserve
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Apolipoprotein E ε4 and Change in Cognitive Functioning in Community-Dwelling Older Adults
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Variability of age at onset in siblings with familial Alzheimer disease
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Impairments in spatial memory retention of GFAP-apoE4 female mice
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Medial temporal lobe dysfunction during encoding and retrieval of episodic memory in non-demented APOE epsilon4 carriers.
Kukolja, J., Thiel, C., Eggermann, T., Zerres, K., & Fink, G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.044 · Cited by 39 · see citing works
Behavioral phenotype and BDNF differences related to apoE isoforms and sex in young transgenic mice
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Alzheimer's disease genetics: lessons to improve disease modelling
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Reduced hippocampal activity during encoding in cognitively normal adults carrying the APOE ɛ4 allele
Adamson, M. M., Hutchinson, J. B., Shelton, A. L., Wagner, A. D., & Taylor, J. L. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.04.022 · Cited by 33 · see citing works
Informed choice in direct-to-consumer genetic testing for Alzheimer and other diseases: lessons from two cases
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Do apolipoprotein E genotype and educational attainment predict the rate of cognitive decline in normal aging? A 12-year follow-up of the Maastricht Aging Study.
Gerven, P. W. M. V., van Boxtel, M. P. J., Ausems, E. E. B., Bekers, O., & Jolles, J. (2012) · Neuropsychology · doi:10.1037/a0028685 · Cited by 29 · see citing works
Sex Differences in Presynaptic Density and Neurogenesis in Middle-Aged ApoE4 and ApoE Knockout Mice
Rijpma, A., Jansen, D., Arnoldussen, I. A. C., Fang, X. T., Wiesmann, M., Mutsaers, M. P. C., Dederen, P. J. W. C., Janssen, C. I. F., & Kiliaan, A. J. (2013) · Journal of Neurodegenerative Diseases · doi:10.1155/2013/531326 · Cited by 27 · see citing works
APOE 4 increases the risk of progression from amnestic mild cognitive impairment to Alzheimer's disease among ethnic Chinese in Taiwan
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Glucose metabolism and gray-matter concentration in apolipoprotein E ε4 positive normal subjects
Samuraki, M., Matsunari, I., Chen, W., Shima, K., Yanase, D., Takeda, N., Matsuda, H., & Yamada, M. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.11.020 · Cited by 20 · see citing works
Neuropsychiatric symptoms, apolipoprotein E gene, and risk of progression to cognitive impairment, no dementia and dementia: the Aging, Demographics, and Memory Study (ADAMS)
Beaudreau, S. A., Fairchild, J. K., Spira, A. P., Lazzeroni, L. C., & O'Hara, R. M. (2012) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.3868 · Cited by 17 · see citing works
Clinical trial methodologies for disease-modifying therapeutic approaches
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A genomic scan for age at onset of alzheimer's disease in 437 families from the NIMH genetic initiative
Dickson, M. R., Li, J., Wiener, H. W., Perry, R. T., Blacker, D., Bassett, S. S., & Go, R. C. P. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30689 · Cited by 14 · see citing works
Should the ApoE genotype be a covariate for clinical trials in Alzheimer disease?
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Accelerated Memory Decline in Alzheimer's Disease With Apolipoprotein 4 Allele
Hirono, N. (2003) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.15.3.354 · Cited by 12 · see citing works
P1–256: APOE genotype by gender interaction revealed in CSF biomarkers and clinical conversion rates in the ADNI database
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2016 Alzheimer's disease facts and figures
Alzheimer's Association (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.03.001 · Cited by 5,069 · see citing works
2023 Alzheimer's disease facts and figures
(2023) · Alzheimer's & Dementia · doi:10.1002/alz.13016 · Cited by 3,212 · see citing works
2024 Alzheimer's disease facts and figures
(2024) · Alzheimer's & Dementia · doi:10.1002/alz.13809 · Cited by 2,536 · see citing works
2019 Alzheimer’s disease facts and figures.
Alzheimer's Association (2019) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2019.01.010 · Cited by 2,461 · see citing works
2022 Alzheimer's disease facts and figures
Anonymous (2022) · Alzheimer s & Dementia · doi:10.1002/alz.12638 · Cited by 2,384 · see citing works
2020 Alzheimer's disease facts and figures
(2020) · Alzheimer's & Dementia · doi:10.1002/alz.12068 · Cited by 2,353 · see citing works
2021 Alzheimer's disease facts and figures
Anonymous (2021) · Alzheimer s & Dementia · doi:10.1002/alz.12328 · Cited by 2,236 · see citing works
2018 Alzheimer's disease facts and figures
Alzheimer's Association (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.02.001 · Cited by 1,912 · see citing works
2015 Alzheimer's disease facts and figures
Alzheimer's Association (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.02.003 · Cited by 1,641 · see citing works
2017 Alzheimer's disease facts and figures
(, T. D. B. T. A.-R. C. C. A. S. O. A. C. B. S., different, ). J. A. I. A., destroyed, S. A. T. A. S. T. M. E. T. M. C. I. S. I. A. G. W. A. T. R. N. I. T. O. B. T. F. N. T. B. D. A. D. A. U. I. B. R. I. I. F. N. M. A. N. I. O. P. O. T. B. A. D. A., difficulties, I. E. O., agitation, I. N. S. S. A., & delusions., S. A. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.02.001 · Cited by 1,322 · see citing works
2014 Alzheimer's disease facts and figures
Alzheimer's Association (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.02.001 · Cited by 1,032 · see citing works
Sex differences in Alzheimer disease — the gateway to precision medicine
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Self-citation

Authors: Ungar, L., Altmann, A., & Greicius, M. D.
Affiliations: Stanford Medicine (US)
Corresponding author: Ungar, Leo
ORCID: Greicius, Michael D.
Venue: Brain Imaging and Behavior
Publisher: Springer Science and Business Media LLC
Published: 2013-11-30
Volume: 8
Issue: 2
Pages: 262-273
ISSN: 1931-7557 (ISSN-L)
1931-7565
DOI: 10.1007/s11682-013-9272-x
PMC: PMC4282773
OpenAlex: W2007870551
Semantic Scholar: a36142356acf18bedeb996827856502949b3d3b7
Cited by: 246
References: 140
Citations by year: 2026: 17 · 2025: 25 · 2024: 42 · 2023: 21 · 2022: 14 · 2021: 29 · 2020: 24 · 2019: 22 · 2018: 19 · 2017: 10 · 2016: 12 · 2015: 8 · 2014: 3
FWCI: 0.89
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Brain Imaging and Behavior (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS073498)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Complementary and alternative medicine › Medicinal Plants and Neuroprotection
Keywords: Alzheimer's disease, apolipoprotein E, APOE ε4, sex differences, gender interaction, genetic risk factors, mild cognitive impairment, neuroimaging
MeSH terms: Alzheimer Disease, Animals, Female, Humans, Male, Sex Factors, Genetic Predisposition to Disease, Apolipoprotein E4

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Apolipoprotein E, gender, and Alzheimer’s disease: an overlooked, but potent and promising interaction

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