Gene-environment interactions in Alzheimer's disease: A potential path to precision medicine

Eid, Aseel; Mhatre, Isha; Richardson, Jason R.

doi:10.1016/j.pharmthera.2019.03.005

Cited by 164Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchHealth, Environment, Cognitive Aging

Gene-environment interactions in Alzheimer's disease: A potential path to precision medicine

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Eid, Aseel, Mhatre, Isha, Richardson, Jason R.·2019·Pharmacology & Therapeutics

DOI 10.1016/j.pharmthera.2019.03.005PMC PMC6827882

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Abstract

Alzheimer's disease (AD) is the leading cause of dementia in the United States and afflicts >5.7 million Americans in 2018. Therapeutic options remain extremely limited to those that are symptom targeting, while no drugs have been approved for the modification or reversal of the disease itself. Risk factors for AD including aging, the female sex, as well as carrying an APOE4 genotype. These risk factors have been extensively examined in the literature, while less attention has been paid to modifiable risk factors, including lifestyle, and environmental risk factors such as exposures to air pollution and pesticides. This review highlights the most recent data on risk factors in AD and identifies gene by environment interactions that have been investigated. It also provides a suggested framework for a personalized therapeutic approach to AD, by combining genetic, environmental and lifestyle risk factors. Understanding modifiable risk factors and their interaction with non-modifiable factors (age, susceptibility alleles, and sex) is paramount for designing personalized therapeutic interventions.

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An individual's genetic background has been reported to influence how they respond to environmental exposures or lifestyle factors.
“an individual’s genetic background has been reported to influence how they respond to environmental exposures or lifestyle factors [269]”
From Genetic architecture of Alzheimer's disease (2020) · cites this paper as [269]
Several modifiable risk factors have been associated with AD risk across populations, including educational attainment, obesity, cholesterol levels, social isolation, alcohol consumption, and exposure to pesticides.
“Several modifiable risk factors have been associated with AD risk across populations, including educational attainment, obesity, cholesterol levels, social isolation, alcohol consumption, and exposure to pesticides [269, 270]”
From Genetic architecture of Alzheimer's disease (2020) · cites this paper as [269]

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Traumatic brain injury history is associated with an earlier age of dementia onset in autopsy-confirmed Alzheimer’s disease.
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Alcohol and Alzheimer's Disease—Does Alcohol Dependence Contribute to Beta-Amyloid Deposition, Neuroinflammation and Neurodegeneration in Alzheimer's Disease?
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Will the Circle Be Unbroken: A History of the U.S. National Ambient Air Quality Standards
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ABCA7 Mediates Phagocytic Clearance of Amyloid-β in the Brain
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Recent advances in Alzheimer's disease: Mechanisms, clinical trials and new drug development strategies.
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“They may achieve this by altering biological pathways and genetic susceptibility, 23,84 – 86 making it challenging to pinpoint a direct cause of clinical pathology in AD.”
Background
Astrocytes in heavy metal neurotoxicity and neurodegeneration
Li, B., Xia, M., Zorec, R., Parpura, V., & Verkhratsky, A. (2021) · Brain Research · doi:10.1016/j.brainres.2020.147234 · Cited by 166 · see citing works
Alzheimer’s Disease Detection Using Deep Learning on Neuroimaging: A Systematic Review
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Genetic architecture of Alzheimer's disease
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“across populations, including educational attainment, obesity, cholesterol levels, social isolation, alcohol consumption, and exposure to pesticides [269, 270].”
Background
Association Between Ambient Air Pollution and Amyloid Positron Emission Tomography Positivity in Older Adults With Cognitive Impairment
Iaccarino, L., Joie, R. L., Lesman‐Segev, O. H., Lee, E. Y., Hanna, L., Allen, I. E., Hillner, B. E., Siegel, B. A., Whitmer, R. A., Carrillo, M. C., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.3962 · Cited by 125 · see citing works
Redox signaling at the crossroads of human health and disease
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“Bridging the Gap” Everything that Could Have Been Avoided If We Had Applied Gender Medicine, Pharmacogenetics and Personalized Medicine in the Gender-Omics and Sex-Omics Era
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APOE Genotype and Alzheimer’s Disease: The Influence of Lifestyle and Environmental Factors
Angelopoulou, E., Paudel, Y. N., Papageorgiou, S. G., & Piperi, C. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00295 · Cited by 105 · see citing works
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The Effects of Chronic Exposure to Ambient Traffic-Related Air Pollution on Alzheimer’s Disease Phenotypes in Wildtype and Genetically Predisposed Male and Female Rats
Patten, K. T., Valenzuela, A. E., Wallis, C., Berg, E. L., Silverman, J. L., Bein, K. J., Wexler, A. S., & Lein, P. J. (2021) · Environmental Health Perspectives · doi:10.1289/ehp8905 · Cited by 90 · see citing works
Multi-omics approaches for understanding gene-environment interactions in noncommunicable diseases: techniques, translation, and equity issues
Alemu, R. G., Sharew, N. T., Arsano, Y. Y., Ahmed, M. B., Ayele, F. T., Baye, T. M., & Amare, A. T. (2025) · Human Genomics · doi:10.1186/s40246-025-00718-9 · Cited by 94 · see citing works
Links between Cognitive Status and Trace Element Levels in Hair for an Environmentally Exposed Population: A Case Study in the Surroundings of the Estarreja Industrial Area
Cabral-Pinto, M. M. S., Reis, A. P. M., Almeida, A. A., Pinto, E., Neves, O., Inácio, M., Gerardo, B., Freitas, S., Simões, M. R., Dinis, P. A., et al. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16224560 · Cited by 84 · see citing works
The Application of Artificial Intelligence in the Genetic Study of Alzheimer’s Disease
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Neuropathological Mechanisms Associated with Pesticides in Alzheimer’s Disease
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APOE alleles’ association with cognitive function differs across Hispanic/Latino groups and genetic ancestry in the study of Latinos‐investigation of neurocognitive aging (HCHS/SOL)
Granot‐Hershkovitz, E., Tarraf, W., Kurniansyah, N., Daviglus, M., Isasi, C. R., Kaplan, R., Lamar, M., Perreira, K. M., Wassertheil‐Smoller, S., Stickel, A., et al. (2021) · Alzheimer's & Dementia · doi:10.1002/alz.12205 · Cited by 71 · see citing works
AlCl3 induced learning and memory deficit in zebrafish
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Activities of mitochondrial respiratory chain complexes in platelets of patients with Alzheimer's disease and depressive disorder
Fišar, Z., Hansíková, H., Křížová, J., Jirák, R., Kitzlerová, E., Zvěřová, M., Hroudová, J., Wenchich, L., Zeman, J., & Raboch, J. (2019) · Mitochondrion · doi:10.1016/j.mito.2019.07.013 · Cited by 63 · see citing works
Novelties on Neuroinflammation in Alzheimer’s Disease–Focus on Gut and Oral Microbiota Involvement
Popescu, C., Munteanu, C., Anghelescu, A., Ciobanu, V., Spînu, A., Andone, I., Mandu, M., Bistriceanu, R., Băilă, M., Postoiu, R.-L., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252011272 · Cited by 56 · see citing works
Air pollution interacts with genetic risk to influence cortical networks implicated in depression
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Multi-omics signature of brain amyloid deposition in asymptomatic individuals at-risk for Alzheimer's disease: The INSIGHT-preAD study
Xicota, L., Ichou, F., Lejeune, F.-X., Colsch, B., Tenenhaus, A., Leroy, I., Fontaine, G., Lhomme, M., Bertin, H., Habert, M.-O., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.08.051 · Cited by 51 · see citing works
Environmental Risk Factors for Early-Onset Alzheimer’s Dementia and Frontotemporal Dementia: A Case-Control Study in Northern Italy
Adani, G., Filippini, T., Garuti, C., Malavolti, M., Vinceti, G., Zamboni, G., Tondelli, M., Galli, C., Costa, M., Vinceti, M., et al. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17217941 · Cited by 51 · see citing works
Genetic susceptibility and lifestyle modify the association of long-term air pollution exposure on major depressive disorder: a prospective study in UK Biobank
Li, D., Xie, J., Wang, L., Sun, Y., Hu, Y., & Tian, Y. (2023) · BMC Medicine · doi:10.1186/s12916-023-02783-0 · Cited by 49 · see citing works
Supplementation with Nicotinamide Riboside Reduces Brain Inflammation and Improves Cognitive Function in Diabetic Mice
Lee, H. J., & Yang, S. J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174196 · Cited by 48 · see citing works
Combined use of Donepezil and Memantine increases the probability of five-year survival of Alzheimer’s disease patients
Yaghmaei, E., Lu, H., Ehwerhemuepha, L., Zheng, J., Danioko, S., Rezaie, A., Sajjadi, S. A., & Rakovski, C. (2024) · Communications Medicine · doi:10.1038/s43856-024-00527-6 · Cited by 47 · see citing works
Death-associated protein kinase 1 as a therapeutic target for Alzheimer's disease
Zhang, T., Kim, B. M., & Lee, T. H. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-023-00395-5 · Cited by 47 · see citing works
Addressing the Discrepancies Between Animal Models and Human Alzheimer’s Disease Pathology: Implications for Translational Research
Polis, B., & Samson, A. O. (2024) · Journal of Alzheimer's Disease · doi:10.3233/jad-240058 · Cited by 43 · see citing works
Brain Disorders and Chemical Pollutants: A Gap Junction Link?
Mesnil, M., Defamie, N., Naus, C. C. G., & Sarrouilhe, D. (2020) · Biomolecules · doi:10.3390/biom11010051 · Cited by 45 · see citing works
Metabolic determinants of Alzheimer’s disease: A focus on thermoregulation
Tournissac, M., Leclerc, M., Valentin‐Escalera, J., Vandal, M., Bosoi, C. R., Planel, E., & Calon, F. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101462 · Cited by 41 · see citing works
Environmental Toxins and Alzheimer’s Disease: a Comprehensive Analysis of Pathogenic Mechanisms and Therapeutic Modulation
Dhapola, R., Sharma, P., Kumari, S., Bhatti, J. S., & HariKrishnaReddy, D. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03805-x · Cited by 41 · see citing works
Dual-acting agents for improving cognition and real-world function in Alzheimer’s disease: Focus on 5-HT6 and D3 receptors as hubs
Millan, M. J., Dekeyne, A., Gobert, A., Brocco, M., la Cour, C. M., Ortuno, J., Watson, D. J., & Fone, K. C. F. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108099 · Cited by 37 · see citing works
Do glutathione and copper interact to modify Alzheimer's disease pathogenesis?
Ho, T., Ahmadi, S., & Kerman, K. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.01.025 · Cited by 37 · see citing works
Role of Astrocytes in Manganese Neurotoxicity Revisited
Ke, T., Sidoryk‐Wȩgrzynowicz, M., Pajarillo, E. A. B., Rizor, A., Soares, F. A. A., Lee, E.-S., & Aschner, M. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02881-7 · Cited by 35 · see citing works
Personalizing progressive changes to brain structure in Alzheimer's disease using normative modeling
Verdi, S., Rutherford, S. E., Fraza, C., Tosun, D., Altmann, A., Rakêt, L. L., Schott, J. M., Marquand, A. F., Cole, J. H., & Initiative, A. D. N. (2024) · Alzheimer s & Dementia · doi:10.1002/alz.14174 · Cited by 43 · see citing works
Education Exerts Different Effects on Cognition in Individuals with Subjective Cognitive Decline and Cognitive Impairment: A Population-Based Study
Chen, G., Zhao, M., Yang, K. Y., Lin, H., Han, C., Wang, X., & Han, Y. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-201170 · Cited by 34 · see citing works
The role of the gut microbiome in mediating neurotoxic outcomes to PCB exposure
Rude, K. M., Keogh, C. E., & Gareau, M. G. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.010 · Cited by 31 · see citing works
Dehydroepiandrosterone (DHEA) and its Sulphate (DHEAS) in Alzheimer’s Disease
Štrac, D. Š., Konjevod, M., Perković, M. N., Tudor, L., Erjavec, G. N., & Pivac, N. (2020) · Current Alzheimer Research · doi:10.2174/1567205017666200317092310 · Cited by 30 · see citing works
Effects of DDT on Amyloid Precursor Protein Levels and Amyloid Beta Pathology: Mechanistic Links to Alzheimer’s Disease Risk
Eid, A., Mhatre‐Winters, I., Sammoura, F. M., Edler, M. K., von Stein, R., Hossain, M. M., Han, Y., Lisci, M., Carney, K., Konsolaki, M., et al. (2022) · Environmental Health Perspectives · doi:10.1289/ehp10576 · Cited by 30 · see citing works
Self-citation
Going beyond established model systems of Alzheimer’s disease: companion animals provide novel insights into the neurobiology of aging
de Sousa, A. A., Dames, B. A. R., Graff, E. C., Mohamedelhassan, R., Vassilopoulos, T., & Charvet, C. J. (2023) · Communications Biology · doi:10.1038/s42003-023-05034-3 · Cited by 30 · see citing works
Exploring the Causal Pathway From Telomere Length to Alzheimer’s Disease: An Update Mendelian Randomization Study
Gao, K., Chen, W., Zhu, J. L., Wang, X., Chen, G., Luo, Y., Zhang, D., Yue, W., & Yu, H. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00843 · Cited by 29 · see citing works
Glutamine Antagonist JHU-083 Normalizes Aberrant Hippocampal Glutaminase Activity and Improves Cognition in APOE4 Mice
Hollinger, K. R., Zhu, X., Khoury, E. S., Thomas, A. G., Liaw, K., Tallon, C., Wu, Y., Prchalová, E., Kamiya, A., Rojas, C. J., et al. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-190588 · Cited by 28 · see citing works
Decoding the role of the CCL2/CCR2 axis in Alzheimer’s disease and innovating therapeutic approaches: Keeping All options open
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Authors: Eid, A., Mhatre, I., & Richardson, J. R.
Affiliations: Florida International University (US)
Corresponding author: Richardson, Jason R.
ORCID: Richardson, Jason R.
Venue: Pharmacology & Therapeutics
Publisher: Elsevier BV
Published: 2019-07
Volume: 199
Pages: 173-187
ISSN: 0163-7258 (ISSN-L)
DOI: 10.1016/j.pharmthera.2019.03.005
PMC: PMC6827882
OpenAlex: W2922392851
Cited by: 164
References: 268
Citations by year: 2026: 21 · 2025: 28 · 2024: 34 · 2023: 20 · 2022: 15 · 2021: 13 · 2020: 24 · 2019: 9
FWCI: 1.80
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Pharmacology & Therapeutics (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (R01ES021800, R01ES026057, R01ES026067-S2, U01NS108956)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Health, Environment, Cognitive Aging
Keywords: Alzheimer's disease, gene-environment interaction, modifiable risk factors, lifestyle risk factors, air pollution exposure, pesticide exposure, APOE ε4, sex differences, aging, personalized medicine, precision medicine, dementia
MeSH terms: Alzheimer Disease, Animals, Humans, Risk Factors, Precision Medicine, Gene-Environment Interaction

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Gene-environment interactions in Alzheimer's disease: A potential path to precision medicine

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