Apolipoprotein E: Structure-Function Relationships

Weisgraber, Karl H.

doi:10.1016/s0065-3233(08)60642-7

Cited by 830Lipid metabolism and disordersCholesterol and Lipid MetabolismLipoproteins and Cardiovascular Health

Apolipoprotein E: Structure-Function Relationships

Weisgraber, Karl H.·1994·Advances in Protein Chemistry

DOI 10.1016/s0065-3233(08)60642-7

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We identified Gly145Asp and Arg154Cys in the same region (amino acids ~148 to 168).
“We identified Gly145Asp and Arg154Cys in the same J o u r n a l P r e -p r o o f region (amino acids ~ 148 to 168) [47]”
From APOE and vascular disease: Sequencing and genotyping in general population cohorts (2023) · cites this paper as [47]
Variants predicted by models to be deleterious or located near or in the receptor binding region (amino acids ~148 to 168) could be suspected to pose ε2-like qualities.
“Variants predicted by models to be deleterious or being located near or in the receptor binding region (amino acids ~ 148 to 168) [47] could be suspected to pose ε2-like qualities.”
From APOE and vascular disease: Sequencing and genotyping in general population cohorts (2023) · cites this paper as [47]
Gly145Asp and Arg154Cys are located in the receptor binding region (amino acids ≈148 to 168) and display a phenotype similar to the ɛ2-defining Arg176Cys residue with high apoE levels and seemingly low risk of dementia (no events).
“Additional support comes from the present data, where Gly145Asp and Arg154Cys are located in the receptor binding region (amino acids ≈148 to 168) 28 and display a phenotype similar to the ɛ2‐defining Arg176Cys residue with high apoE levels and seemingly low risk of dementia (no events).”
From APOE and dementia – resequencing and genotyping in 105,597 individuals (2020) · cites this paper as [28]
Val254Glu and Arg269Gly are located in the lipid-binding carboxyl-terminal domain (amino acids ≈243 to 317).
“Val254Glu and Arg269Gly are located in the lipid‐binding carboxyl‐terminal domain (amino acids ≈243 to 317). 28 , 42”
From APOE and dementia – resequencing and genotyping in 105,597 individuals (2020) · cites this paper as [28]
The receptor-binding sites (AA136-150) for LDLR, LRP1, and HSPGs are located in a region conserved between mouse and human APOE.
“However, the receptor-binding sites (AA136-150) for lipoprotein receptors such as the low-density lipoprotein receptor (LDLR), lipoprotein-related receptor 1 (LRP1), and heparan sulfate proteoglycans (HSPGs) are located in a region conserved between species (Fig. 1a) [11–14].”
From APOE Christchurch enhances a disease-associated microglial response to plaque but suppresses response to tau pathology (2025) · cites this paper as [12]

An HSPG and LDLR binding site in the APOE sequence is conserved in mice (AA136-150), including arginine 136, which is replaced by serine in the Christchurch (Ch) variant.
“Notably, an HSPG and LDLR binding site in the APOE sequence is conserved in mice (blue boxed area, AA136-150), including arginine 136, which is replaced by serine in the Christchurch (Ch) variant [12, 39].”
From APOE Christchurch enhances a disease-associated microglial response to plaque but suppresses response to tau pathology (2025) · cites this paper as [12]
mAPOE and hAPOE have a conserved LDLR and HSPG binding motif between AA136 to 150 (human numbering), which includes R136S Christchurch variant.
“However, mAPOE and hAPOE have a conserved LDLR and HSPG binding motif between AA136 to 150 (human numbering) [11, 12, 39], which includes the R136S Christchurch variant.”
From APOE Christchurch enhances a disease-associated microglial response to plaque but suppresses response to tau pathology (2025) · cites this paper as [12]
The mature apoE protein consists of 299 amino acids, and an 18-amino acid signal peptide is removed post-translationally.
“The mature apoE protein consists of 299 amino acids and an 18amino acid signal peptide is removed post-translationally [17,28].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
The APOE gene is located on chromosome 19 and consists of four exons.
“The APOE gene is located on chromosome 19 and consists of four exons [28].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
Lipid-free apoE consists of two domains connected by a hinge region: the amino-terminal domain (amino acids 1 to 191) contains the receptor-binding function, and the carboxyl-terminal domain (~amino acids 225 to 299) contains the lipid-binding function.
“Lipid-free apoE consists of two domains connected by a “hinge region”: the amino-terminal domain (amino acids 1 to 191) contains the receptor-binding function and the carboxyl-terminal domain (~amino acids 225 to 299) contains the lipid-binding function [28,33].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
The LDL receptor binding region is situated in helix four between amino acids 136 and 150.
“The low density lipoprotein (LDL) receptor binding region is situated in helix four between amino acids 136 and 150 [17,28].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
ApoE2 exhibits a lower affinity to the LDL receptor compared with apoE3, with ~1% of the binding activity of apoE3 and apoE4.
“ApoE2 exhibits a lower affinity to the LDL receptor compared to apoE3: ~1% of the binding activity of apoE3 and apoE4 [28,36].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
ApoE and apoB share the sequence with highest affinity for arterial proteoglycans, a key phenomenon for lipoprotein deposition in the arterial wall.
“Furthermore, apoE and apoB share the sequence with highest affinity for arterial proteoglycans, a key phenomenon for lipoprotein deposition in the arterial wall [28,63].”
From Plasma levels of apolipoprotein E, APOE genotype and risk of dementia and ischemic heart disease: A review (2016) · cites this paper as [28]
ApoE contains two independently folded functional domains: a 22-kDa N-terminal domain (residues 1-191) and a 10-kDa C-terminal domain (residues 216-299) linked by a hinge region.
“ApoE contains two independently folded functional domains; these are a 22-kDa N-terminal domain (residues 1–191) and a 10-kDa C-terminal domain (residues 216–299) linked by a hinge region (18, 19).”
From Role of the N- and C-Terminal Domains in Binding of Apolipoprotein E Isoforms to Heparan Sulfate and Dermatan Sulfate: A Surface Plasmon Resonance Study (2008) · cites this paper as [18]

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Molecular structure of an apolipoprotein determined at 2.5-.ANG. resolution
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Rate and equilibrium constants for binding of apo-E HDL c (a cholesterol-induced lipoprotein) and low density lipoproteins to human fibroblasts: Evidence for multiple receptor binding of apo-E HDL c
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Polymorphism of Apolipoprotein E
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Lipoprotein Uptake by Neuronal Growth Cones in Vitro
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Nato Advanced Research Workshop
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The Interaction of Heparin with an Apoprotein of Human Very Low Density Lipoprotein
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The low-density lipoprotein receptor-related protein: double agent or decoy?
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Discrete carboxyl-terminal segments of apolipoprotein E mediate lipoprotein association and protein oligomerization
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Apolipoprotein E mediates uptake of Sf 100-400 hypertriglyceridemic very low density lipoproteins by the low density lipoprotein receptor pathway in normal human fibroblasts.
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Interaction of plasma lipoproteins containing apolipoproteins B and E with heparin and cell surface receptors
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Apolipoprotein E localization in rat hepatocytes by immunogold labeling of cryothin sections
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Role of apolipoprotein E in the lipolytic conversion of beta-very low density lipoproteins to low density lipoproteins in type III hyperlipoproteinemia.
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Dynamics of apolipoprotein E metabolism in humans
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Characterization of a unique human apolipoprotein E variant associated with type III hyperlipoproteinemia.
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A New Apoprotein of Human Plasma Very Low Density Lipoproteins
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Isolation and Partial Characterization of an Arginine-Rich Apolipoprotein from Human Plasma Very-Low-Density Lipoproteins: Apolipoprotein E
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Binding of a high reactive heparin to human apolipoprotein E: Identification of two heparin-binding domains
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A novel electrophoretic variant of human apolipoprotein E. Identification and characterization of apolipoprotein E1
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Plasma lipoprotein metabolism in transgenic mice overexpressing apolipoprotein E. Accelerated clearance of lipoproteins containing apolipoprotein B.
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Apoprotein E suppresses phytohemagglutinin-activated phospholipid turnover in peripheral blood mononuclear cells.
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Intravenous infusion of apolipoprotein E accelerates clearance of plasma lipoproteins in rabbits.
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Identification of the disulfide-linked homodimer of apolipoprotein E3 in plasma. Impact on receptor binding activity
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Type III hyperlipoproteinemia associated with apolipoprotein E phenotype E3/3: structure and genetics of an apolipoprotein E3 variant
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Atherogenic hyperlipoproteinemia induced by cholesterol feeding in the Patas monkey
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The functional characteristics of a human apolipoprotein E variant (cysteine at residue 142) may explain its association with dominant expression of type III hyperlipoproteinemia
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Heparan sulfate proteoglycans are concentrated on the sinusoidal plasmalemmal domain and in intracellular organelles of hepatocytes.
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Identical Structural and Receptor Binding Defects in Apolipoprotein E2 in Hypo-, Normo-, and Hypercholesterolemic Dysbetalipoproteinemia
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Increased clearance of plasma cholesterol after injection of apolipoprotein E into Watanabe heritable hyperlipidemic rabbits.
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The Structure and Properties of Monolayers of Synthetic Polypeptides at the Air-Water Interface
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Apolipoprotein E3-Leiden contains a seven-amino acid insertion that is a tandem repeat of residues 121–127
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Apolipoprotein E-1Harrisburg: a new variant of apolipoprotein E dominantly associated with type III hyperlipoproteinemia.
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Activation of lecithin cholesterol acyltransferase by human apolipoprotein E in discoidal complexes with lipids.
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Hepatic lipase hydrolysis of lipid monolayers. Regulation by apolipoproteins.
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Familial apolipoprotein E deficiency and type III hyperlipoproteinemia due to a premature stop codon in the apolipoprotein E gene.
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Expression of the human apolipoprotein E gene suppresses steroidogenesis in mouse Y1 adrenal cells.
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Total deficiency of plasma cholesteryl ester transfer protein in subjects homozygous and heterozygous for the intron 14 splicing defect
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ALTERATIONS IN METABOLIC ACTIVITY OF PLASMA LIPOPROTEINS FOLLOWING SELECTIVE CHEMICAL MODIFICATION OF THE APOPROTEINS
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Heterogeneity of apolipoprotein E epitope expression on human lipoproteins: importance for apolipoprotein E function
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Analysis of Apolipoprotein E7 (Apolipoprotein E-Suita) Gene from a Patient with Hyperlipoproteinemia1
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Suppression of cAMP-mediated signal transduction in mouse adrenocortical cells which express apolipoprotein E.
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Only multimers of a synthetic peptide of human apolipoprotein E are biologically active
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Apolipoprotein E1 Lys-146----Glu with type III hyperlipoproteinemia.
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PROPERTIES OF APOLIPOPROTEINS AT THE AIR‐WATER INTERFACE *
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Identification of Human Apolipoprotein E Variant Gene: Apolipoprotein E7 (Glu244,245↑Lys244,245)1
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Effect of particle size and temperature on the conformation and physiological behavior of apolipoprotein E bound to model lipoprotein particles
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Apolipoprotein E2-Dunedin (228 Arg replaced by Cys): an apolipoprotein E2 variant with normal receptor-binding activity.
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Circular dichroic spectra of apolipoprotein E in model complexes and cholesterol-rich lipoproteins: lipid contribution
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Normolipemic dysbetalipoproteinemia and hyperlipoproteinemia type III in subjects homozygous for a rare genetic apolipoprotein E variant (apoE1).
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Nucleotide sequence of the cynomolgus monkey apolipoprotein E cDNA
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Enhanced binding activity of an apolipoprotein E mutant, apo E5, to LDL receptors on human fibroblasts
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Cellular and Molecular Biology of Lipoprotein Metabolism: Characterization of Lipoprotein Receptor-Ligand Interactions
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Lipoproteins in pinnipeds: analysis of a high molecular weight form of apolipoprotein E.
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Crystallization and preliminary X-ray diffraction studies on the amino-terminal (receptor-binding) domain of human apolipoprotein E3 from serum very low density lipoproteins
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Cholesterol metabolism, LDL and the LDL receptor
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Hepatic and renal expression of rat apolipoprotein E under control of the metallothionein promotor in transgenic mice
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Self-associated tetramer of human apolipoprotein E does not lead to its accumulation on a lipid particle
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Primary structure of guinea pig apolipoprotein E
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Amino acid sequence of rabbit apolipoprotein E.
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Human Apolipoprotein Mutants
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Apolipoprotein E: Far More Than a Lipid Transport Protein
Mahley, R. W., & Rall, S. C. (2000) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.1.1.507 · Cited by 1,836 · see citing works
Apolipoprotein E4: A causative factor and therapeutic target in neuropathology, including Alzheimer’s disease
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Apolipoprotein E: Structure and function in lipid metabolism, neurobiology, and Alzheimer’s diseases
Huang, Y., & Mahley, R. W. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.08.025 · Cited by 829 · see citing works
Apolipoprotein E: from cardiovascular disease to neurodegenerative disorders
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ApoE in Alzheimer’s disease: pathophysiology and therapeutic strategies
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Receptors, Mediators, and Mechanisms Involved in Bacterial Sepsis and Septic Shock
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Differential Effects of Apolipoproteins E3 and E4 on Neuronal Growth in Vitro
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Apolipoprotein E structure: insights into function
Hatters, D. M., Peters-Libeu, C. A., & Weisgraber, K. H. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.06.008 · Cited by 583 · see citing works
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Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS
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Targeted Replacement of the Mouse Apolipoprotein E Gene with the Common Human APOE3 Allele Enhances Diet-induced Hypercholesterolemia and Atherosclerosis
Sullivan, P. M., Mezdour, H., Aratani, Y., Knouff, C., Najib, J., Reddick, R. L., Quarfordt, S. H., & Maeda, N. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.29.17972 · Cited by 575 · see citing works
APOLIPOPROTEIN E ALLELES AS RISK FACTORS IN ALZHEIMER'S DISEASE
Roses, M. D. (1996) · Annual Review of Medicine · doi:10.1146/annurev.med.47.1.387 · Cited by 707 · see citing works
Structure of apolipoprotein B-100 in low density lipoproteins
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Apolipoprotein E is essential for amyloid deposition in the APP V717F transgenic mouse model of Alzheimer's disease
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Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease.
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Pathogenesis of type III hyperlipoproteinemia (dysbetalipoproteinemia): questions, quandaries, and paradoxes
Mahley, R. W., Huang, Y., & Rall, S. C. (1999) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)32417-2 · Cited by 447 · see citing works
Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro.
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Apolipoprotein E Variation at the Sequence Haplotype Level: Implications for the Origin and Maintenance of a Major Human Polymorphism
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Apolipoprotein e sets the stage: response to injury triggers neuropathology
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APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response
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Apolipoprotein E
Mahley, R. W., & Huang, Y. (1999) · Current Opinion in Lipidology · doi:10.1097/00041433-199906000-00003 · Cited by 388 · see citing works
STRUCTURE AND PHYSIOLOGIC FUNCTION OF THE LOW-DENSITY LIPOPROTEIN RECEPTOR
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Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease.
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Apolipoprotein E: an important gene and protein to follow in laboratory medicine
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Covalent Linkage of Apolipoprotein E to Albumin Nanoparticles Strongly Enhances Drug Transport into the Brain
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Apo E structure determines VLDL clearance and atherosclerosis risk in mice
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Human apolipoprotein E: the Alzheimer's disease connection
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Apolipoprotein E isoforms and lipoprotein metabolism
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Human apolipoprotein E: Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms
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Apolipoprotein E4 Causes Age- and Tau-Dependent Impairment of GABAergic Interneurons, Leading to Learning and Memory Deficits in Mice
Andrews-Zwilling, Y., Bien-Ly, N., Xu, Q., Li, G., Bernardo, A., Yoon, S. Y., Zwilling, D., Yan, T. X., Chen, L., & Huang, Y. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4040-10.2010 · Cited by 326 · see citing works
Human Apolipoprotein E4 Domain Interaction
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Lipid- and receptor-binding regions of apolipoprotein E4 fragments act in concert to cause mitochondrial dysfunction and neurotoxicity
Chang, S., Ma, T. R., Miranda, R. D., Balestra, M. E., Mahley, R. W., & Huang, Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508254102 · Cited by 319 · see citing works
Causative and susceptibility genes for Alzheimer’s disease: a review
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Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth
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APOE2: protective mechanism and therapeutic implications for Alzheimer’s disease
Li, Z., Shue, F., Zhao, N., Shinohara, M., & Bu, G. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00413-4 · Cited by 306 · see citing works
Apolipoprotein E: Structural Insights and Links to Alzheimer Disease Pathogenesis
Chen, Y., Strickland, M. R., Soranno, A., & Holtzman, D. M. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.008 · Cited by 298 · see citing works
Apolipoprotein E: From lipid transport to neurobiology
Hauser, P. S., Narayanaswami, V., & Ryan, R. O. (2011) · Progress in Lipid Research · doi:10.1016/j.plipres.2010.09.001 · Cited by 320 · see citing works
The genetic architecture of Alzheimer's disease: beyond APP, PSENs and APOE
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Macrophage-specific expression of human apolipoprotein E reduces atherosclerosis in hypercholesterolemic apolipoprotein E-null mice
Bellosta, S., Mahley, R. W., Sanan, D. A., Murata, J., Newland, D. L., Taylor, J. M., & Pitas, R. E. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118271 · Cited by 284 · see citing works
APOE in the bullseye of neurodegenerative diseases: impact of the APOE genotype in Alzheimer’s disease pathology and brain diseases
Fernández-Calle, R., Konings, S. C., Frontiñán-Rubio, J., García-Revilla, J., Camprubí-Ferrer, L., Svensson, M., Martinson, I., Boza-Serrano, A., Venero, J. L., Nielsen, H. M., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00566-4 · Cited by 278 · see citing works
The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerization
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HumanAPOEIsoform-Dependent Effects on Brain β-Amyloid Levels in PDAPP Transgenic Mice
Bales, K. R., Liu, F., Wu, S., Lin, S., Koger, D., DeLong, C., Hansen, J. C., Sullivan, P. M., & Paul, S. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0887-09.2009 · Cited by 274 · see citing works
Apolipoprotein (apo) E4 enhances amyloid β peptide production in cultured neuronal cells: ApoE structure as a potential therapeutic target
Ye, S., Huang, Y., Müllendorff, K., Dong, L., Giedt, G., Meng, E. C., Cohen, F. E., Kuntz, I. D., Weisgraber, K. H., & Mahley, R. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508693102 · Cited by 275 · see citing works
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Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions
Chen, J., Li, Q., & Wang, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106420108 · Cited by 283 · see citing works
Molecular imaging with nanoparticles: giant roles for dwarf actors
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High Density Lipoprotein Structure–Function and Role in Reverse Cholesterol Transport
Lund-Katz, S., & Phillips, M. C. (2010) · Subcellular Biochemistry · doi:10.1007/978-90-481-8622-8_7 · Cited by 262 · see citing works
Uptake Mechanism of ApoE-Modified Nanoparticles on Brain Capillary Endothelial Cells as a Blood-Brain Barrier Model
Wagner, S., Zensi, A., Wien, S., Tschickardt, S., Maier, W., Vogel, T., Worek, F., Pietrzik, C. U., Kreuter, J., & von Briesen, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032568 · Cited by 260 · see citing works
Functional Anthology of Intrinsic Disorder. 2. Cellular Components, Domains, Technical Terms, Developmental Processes, and Coding Sequence Diversities Correlated with Long Disordered Regions
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Clearance mechanisms of Alzheimer's amyloid-β peptide: implications for therapeutic design and diagnostic tests
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Apolipoprotein E: Diversity of Cellular Origins, Structural and Biophysical Properties, and Effects in Alzheimer's Disease
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Increased Microglial Exosomal miR-124-3p Alleviates Neurodegeneration and Improves Cognitive Outcome after rmTBI
Ge, X., Guo, M., Hu, T., Li, W., Huang, S., Yin, Z., Li, Y., Chen, F., Zhu, L., Kang, C., et al. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2019.11.017 · Cited by 242 · see citing works
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Authors: Weisgraber, K. H.
Affiliations: Gladstone Institutes (US)
Corresponding author: Weisgraber, Karl H.
Venue: Advances in Protein Chemistry
Publisher: Elsevier
Published: 1994
Volume: 45
Pages: 249-302
ISSN: 0065-3233 (ISSN-L)
DOI: 10.1016/s0065-3233(08)60642-7
OpenAlex: W98152484
Cited by: 830
References: 194
Citations by year: 2026: 16 · 2025: 25 · 2024: 14 · 2023: 17 · 2022: 12 · 2021: 20 · 2020: 12 · 2019: 13 · 2018: 14 · 2017: 20 · 2016: 18 · 2015: 15 · 2014: 18 · 2013: 23 · 2012: 26
FWCI: 89.45
Type: book chapter
Language: en
Open access: closed
Locations: Advances in protein chemistry (publishedVersion)
PubMed (publishedVersion)
Funders: National Heart, Lung, and Blood Institute (HL-41633, P01HL041633)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Keywords: apolipoprotein E, lipoprotein metabolism, apolipoprotein structure, APOE isoforms, lipid transfer proteins, lipoprotein receptors, triglyceride-rich lipoproteins, reverse cholesterol transport, lipolysis, serum lipoproteins
MeSH terms: Amino Acid Sequence, Animals, Apolipoproteins E, Humans, Molecular Sequence Data, Protein Conformation, Structure-Activity Relationship, Lipid Metabolism

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