Apolipoprotein E: Far More Than a Lipid Transport Protein

Mahley, Robert W.; Rall, Stanley C.

doi:10.1146/annurev.genom.1.1.507

Cited by 1,836Alzheimer's disease research and treatmentsLipoproteins and Cardiovascular HealthLipid metabolism and disorders

Apolipoprotein E: Far More Than a Lipid Transport Protein

Mahley, Robert W., Rall, Stanley C.·2000·Annual Review of Genomics and Human Genetics

DOI 10.1146/annurev.genom.1.1.507

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Abstract

First recognized as a major determinant in lipoprotein metabolism and cardiovascular disease, apolipoprotein (apo) E has emerged as an important molecule in several biological processes not directly related to its lipid transport function, including Alzheimer's disease and cognitive function, immunoregulation, and possibly even infectious diseases. ApoE is a polymorphic protein arising from three alleles at a single gene locus. The three major isoforms, apoE4, apoE3, and apoE2, differ from one another only by single amino acid substitutions, yet these changes have profound functional consequences at both the cellular and molecular levels. ApoE3 seems to be the normal isoform in all known functions, while apoE4 and apoE2 can each be dysfunctional. Isoform (allele)-specific effects include the association of apoE2 with the genetic disorder type III hyperlipoproteinemia and with both increased and decreased risk for atherosclerosis and the association of apoE4 with increased risk for both atherosclerosis and Alzheimer's disease, impaired cognitive function, and reduced neurite outgrowth; isoform-specific differences in cellular signaling events may also exist. Functional differences in the apoE isoforms that affect (or did affect) survival before the reproductive years probably account, at least in part, for the allele frequencies of the present day.

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Exchangeable apolipoproteins consist of two functional domains: a lipid-binding domain and a receptor-binding domain.
“Exchangeable apolipoproteins are typically consisting of two functional domains: lipid-binding domain and receptor-binding domain24.”
From Brain-targeted drug delivery by manipulating protein corona functions (2019) · cites this paper as [24]
The striking vasculotropic effects observed in APP/ε2 mice may not be robustly seen in human subjects, where ε2 homozygotes constitute only 1% of the population, with less than 10% of them developing type III hyperlipoproteinemia.
“However, these striking vasculotropic effects observed here in APP/ε2 mice may not be robustly seen in human subjects, where ε2 homozygotes constitute only 1% of the population, with less than 10% of them developing type III hyperlipoproteinemia, what is linked to distinctly different contribution of apoE to VLDL formation between humans and mice [62].”
From APOE Genotype Differentially Modulates Effects of Anti-Aβ, Passive Immunization in APP Transgenic Mice (2017) · cites this paper as [62]
APOE4 has increased binding affinity (up to two-fold) for heparin and HSPG over APOE3.
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From The APOE-R136S mutation protects against APOE4-driven tau pathology, neurodegeneration, and neuroinflammation (2023) · cites this paper as [32]
Mutations in APOE could alter the configuration of the APOE protein and further impact its binding ability to the LDL receptor, which could explain the formation of lipoprotein thrombi in the glomerulus.
“As serum apoE plays its role in lipid metabolism through the LDL receptor, the HSPG and LDL receptor‐related protein (LRP) pathway (Mahley & Rall Jr., 2000), mutations could alter the configuration of the APOE protein and further impact its binding ability to LDL receptor, which could explain the formation of lipoprotein thrombi in the glomerulus.”
From Clinical and genetic analysis of lipoprotein glomerulopathy patients caused by APOE mutations (2020) · cites this paper as Mahley & Rall Jr., 2000
Human apoE is a protein consisting of 299 amino acid residues with a molecular weight of 34 kDa.
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From Impact of Apolipoprotein E Variants: A Review of Naturally Occurring Variants and Clinical Features (2025) · cites this paper as [8]

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Apolipoprotein E Inhibition of Proliferation of Mitogen-Activated T Lymphocytes: Production of Interleukin 2 with Reduced Biological Activity
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Novel mechanism for defective receptor binding of apolipoprotein E2 in type III hyperlipoproteinemia
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Arginine residues at codons 112 and 158 in the apolipoprotein E gene correspond to the ancestral state in humans
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Immunoregulatory plasma lipoproteins. Role of apoprotein E and apoprotein B.
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A Minimally Lipidated Form of Cell-derived Apolipoprotein E Exhibits Isoform-specific Stimulation of Neurite Outgrowth in the Absence of Exogenous Lipids or Lipoproteins
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Preclinical memory decline in cognitively normal apolipoprotein E–ε4 homozygotes
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Apolipoprotein A-I and its amphipathic helix peptide analogues inhibit human immunodeficiency virus-induced syncytium formation.
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Salt bridge relay triggers defective LDL receptor binding by a mutant apolipoprotein.
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Prolonged postprandial responses of lipids and apolipoproteins in triglyceride-rich lipoproteins of individuals expressing an apolipoprotein epsilon 4 allele.
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Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes.
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Amyloid β‐Protein, APOE Genotype and Head Injury
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Decreased selective uptake of high density lipoprotein cholesteryl esters in apolipoprotein E knock-out mice
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Apolipoprotein E2 Reduces the Low Density Lipoprotein Level in Transgenic Mice by Impairing Lipoprotein Lipase-mediated Lipolysis of Triglyceride-rich Lipoproteins
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Overexpression of Apolipoprotein E3 in Transgenic Rabbits Causes Combined Hyperlipidemia by Stimulating Hepatic VLDL Production and Impairing VLDL Lipolysis
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Are men carrying the apolipoprotein ε4- or ε2 allele less fertile than ε3ε3 genotypes?
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Memory Self-Appraisal in Middle-Aged and Older Adults With the Apolipoprotein E-4 Allele
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The LDL-receptor-related protein ??? portrait of a multifunctional receptor
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The apolipoprotein E polymorphism in Greenland Inuit in its global perspective
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Expression of apolipoprotein E by cultured vascular smooth muscle cells is controlled by growth state.
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Lipoproteins, neurobiology, and Alzheimer's disease: structure and function of apolipoprotein E
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Both Lipolysis and Hepatic Uptake of VLDL Are Impaired in Transgenic Mice Coexpressing Human Apolipoprotein E*3Leiden and Human Apolipoprotein C1
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Apolipoprotein E2 Transgenic Rabbits
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Susceptibility to diet-induced atherosclerosis in transgenic mice expressing a dysfunctional human apolipoprotein E(Arg 112,Cys142).
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Immunoregulation by low density lipoproteins in man. Inhibition of mitogen-induced T lymphocyte proliferation by interference with transferrin metabolism.
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Only multimers of a synthetic peptide of human apolipoprotein E are biologically active
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Modulation of human lymphocyte responses by low density lipoproteins (LDL): enhancement but not immunosuppression is mediated by LDL receptors.
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Functions of the LDL Receptor Gene Family
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Apolipoprotein A-1 interacts with the N-terminal fusogenic domains of SIV (simian immunodeficiency virus) GP32 and HIV (human immunodeficiency virus) GP41: Implications in viral entry
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Genetic Factors Precipitating Type III Hyperlipoproteinemia in Hypolipidemic Transgenic Mice Expressing Human Apolipoprotein E2
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In LDL receptor-deficient mice, catabolism of remnant lipoproteins requires a high level of apoE but is inhibited by excess apoE
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Apolipoprotein E (ApoE), a novel heparin-binding protein inhibits the development of Kaposi's sarcoma-like lesions in BALB/c nu/nu mice.
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Susceptibility to diet-induced atherosclerosis in transgenic mice expressing a dysfunctional human apolipoprotein E(Arg 112,Cys142).
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Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy
Liu, C.-C., Kanekiyo, T., Xu, H., & Bu, G. (2013) · Nature Reviews Neurology · doi:10.1038/nrneurol.2012.263 · Cited by 3,459 · see citing works
2018 Alzheimer's disease facts and figures
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Lipids and Lipid-Based Formulations: Optimizing the Oral Delivery of Lipophilic Drugs
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TREM2 Binds to Apolipoproteins, Including APOE and CLU/APOJ, and Thereby Facilitates Uptake of Amyloid-Beta by Microglia
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Apolipoprotein E in Alzheimer’s disease and other neurological disorders
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Apolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease
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Progesterone receptors: form and function in brain
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Age, APOE and sex: triad of risk of Alzheimer’s disease.
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Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS
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Lipid- and receptor-binding regions of apolipoprotein E4 fragments act in concert to cause mitochondrial dysfunction and neurotoxicity
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Apolipoprotein E–dependent accumulation of Alzheimer disease–related lesions begins in middle age
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Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration
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Herpes Simplex Virus Type 1 and Other Pathogens are Key Causative Factors in Sporadic Alzheimer’s Disease
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HumanAPOEIsoform-Dependent Effects on Brain β-Amyloid Levels in PDAPP Transgenic Mice
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Apolipoprotein (apo) E4 enhances amyloid β peptide production in cultured neuronal cells: ApoE structure as a potential therapeutic target
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Brain Differences in Infants at Differential Genetic Risk for Late-Onset Alzheimer Disease: A Cross-sectional Imaging Study
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Lipid and Lipoprotein Metabolism in Microglia
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Authors: Mahley, R. W., & Rall, S. C.
Affiliations: University of California, San Francisco (US)
ORCID: Mahley, Robert W.
Venue: Annual Review of Genomics and Human Genetics
Publisher: Annual Reviews
Published: 2000-09
Volume: 1
Issue: 1
Pages: 507-537
ISSN: 1527-8204 (ISSN-L)
1545-293X
DOI: 10.1146/annurev.genom.1.1.507
OpenAlex: W2121101037
Cited by: 1,836
References: 114
Citations by year: 2026: 54 · 2025: 85 · 2024: 71 · 2023: 55 · 2022: 95 · 2021: 103 · 2020: 70 · 2019: 79 · 2018: 64 · 2017: 80 · 2016: 86 · 2015: 75 · 2014: 100 · 2013: 80 · 2012: 83
FWCI: 3.13
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Genomics and Human Genetics (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p01hl047660-10)
National Heart, Lung, and Blood Institute (HL-47660)
National Institute of Allergy and Infectious Diseases (R37AI020565)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
Keywords: apolipoprotein E, apolipoprotein E isoforms, APOE ε4, APOE3, APOE2, APOE polymorphism, Alzheimer's disease, cognitive function, immune regulation, infectious diseases, type III hyperlipoproteinemia, atherosclerosis, cardiovascular disease, neurite outgrowth, allele frequency
MeSH terms: Alleles, Animals, Apolipoproteins E, Arteriosclerosis, Biological Transport, Active, Communicable Diseases, Female, Heart Diseases, Humans, Hyperlipoproteinemia Type III, Immunity, Lipoproteins, Male, Models, Molecular, Neurobiology, Phenotype, Polymorphism, Genetic, Reproduction, Risk Factors, Protein Isoforms, Lipid Metabolism

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Apolipoprotein E: Far More Than a Lipid Transport Protein

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