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Variant ASGR1 Associated with a Reduced Risk of Coronary Artery Disease
Open accessAbstract
BACKGROUND: Several sequence variants are known to have effects on serum levels of non-high-density lipoprotein (HDL) cholesterol that alter the risk of coronary artery disease. METHODS: We sequenced the genomes of 2636 Icelanders and found variants that we then imputed into the genomes of approximately 398,000 Icelanders. We tested for association between these imputed variants and non-HDL cholesterol levels in 119,146 samples. We then performed replication testing in two populations of European descent. We assessed the effects of an implicated loss-of-function variant on the risk of coronary artery disease in 42,524 case patients and 249,414 controls from five European ancestry populations. An augmented set of genomes was screened for additional loss-of-function variants in a target gene. We evaluated the effect of an implicated variant on protein stability. RESULTS: We found a rare noncoding 12-base-pair (bp) deletion (del12) in intron 4 of ASGR1, which encodes a subunit of the asialoglycoprotein receptor, a lectin that plays a role in the homeostasis of circulating glycoproteins. The del12 mutation activates a cryptic splice site, leading to a frameshift mutation and a premature stop codon that renders a truncated protein prone to degradation. Heterozygous carriers of the mutation (1 in 120 persons in our study population) had a lower level of non-HDL cholesterol than noncarriers, a difference of 15.3 mg per deciliter (0.40 mmol per liter) (P=1.0×10(-16)), and a lower risk of coronary artery disease (by 34%; 95% confidence interval, 21 to 45; P=4.0×10(-6)). In a larger set of sequenced samples from Icelanders, we found another loss-of-function ASGR1 variant (p.W158X, carried by 1 in 1850 persons) that was also associated with lower levels of non-HDL cholesterol (P=1.8×10(-3)). CONCLUSIONS: ASGR1 haploinsufficiency was associated with reduced levels of non-HDL cholesterol and a reduced risk of coronary artery disease. (Funded by the National Institutes of Health and others.).
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“Loss-of-function mutations in the ASGR1 gene are associated with decreased levels of non-high-density lipoprotein cholesterol and triglycerides in the blood plasma, resulting in a reduction in the risk of atherosclerosis and CVD [43].”
From Post-translational regulation of the low-density lipoprotein receptor provides new targets for cholesterol regulation (2024) · cites this paper as [43]
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“In 2016, a human genetic study identified two loss-of-function variants in the asialoglycoprotein receptor 1 (ASGR1), del12 and p.W158X, that were associated with decreased circulating non-HDL cholesterol levels and a reduced risk of cardiovascular disease [82].”
From The low-density lipoprotein receptor: Emerging post-transcriptional regulatory mechanisms (2025) · cites this paper as [82]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“two human ASGR1-deletion variants found in Iceland, resulting in truncated proteins, likely inactive, are associated with a modest ∼10% to 14% reduction in LDLc”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Comparison of plasma LDLc decrease in LOF PCSK9 R46L (−17 mg/dl; ∼30% reduction in CVD risk) with that in LOF ASGR1 del12 mutation (−11 mg/dl) illustrates that reduction in CVD risk observed in this ASGR1 mutant (∼34%) was ∼2-fold greater than would have been predicted (i.e., ∼18%) from the associated modest reduction of LDLc (12).”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In addition, the del12 mutation was associated with a significant 34% lower risk of CVD.”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
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“Indeed, loss of function mutations in ASGR1 are associated with decreased non-HDL cholesterol levels and decreased risk of CAD148.”
From Pathways and Molecular Mechanisms Governing LDL Receptor Regulation (2025) · cites this paper as [148]
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“Human heterozygote carriers of ASGR1 deletions exhibit ∼34% lower risk of coronary artery disease and ∼10% to 14% reduction of non-HDL cholesterol.”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
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In the citing paper
“Our data provide a mechanism for the modest reduction of LDLc in humans lacking functional ASGR1 (12).”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
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“A human population genetic study provided evidence that variant asialoglycoprotein receptor 1 (ASGR1) is associated with lower non–HDL-c content and reduced risk of coronary artery disease (CAD), indicating a potential target for CVD prevention and treatment (3).”
From Hypomorphic ASGR1 modulates lipid homeostasis via INSIG1-mediated SREBP signaling suppression (2021) · cites this paper as [3]
The cited source says what the claim attributes to it.
In the citing paper
“A human population genetic study provided evidence that variant asialoglycoprotein receptor 1 (ASGR1) is associated with lower non–HDL-c content and reduced risk of coronary artery disease (CAD), indicating a potential target for CVD prevention and treatment (3).”
From Hypomorphic ASGR1 modulates lipid homeostasis via INSIG1-mediated SREBP signaling suppression (2021) · cites this paper as [3]
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In the citing paper
“The heterozygous mutation carriers had a lower level of non–HDL-c and TG, and the ASGR1 haploinsufficiency was associated with a lower risk of CAD (3).”
From Hypomorphic ASGR1 modulates lipid homeostasis via INSIG1-mediated SREBP signaling suppression (2021) · cites this paper as [3]
In the citing paper
“Founder populations (such as those from Finland and Iceland) have provided multiple examples of otherwise rare risk alleles driven to higher frequency locally through drift and/or selection49–52.”
From A brief history of human disease genetics (2020) · cites this paper as [51]
In the citing paper
“yet with a significant ∼34% reduced risk of coronary artery disease.”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
In the citing paper
“Recent studies showed that heterozygous carriers of the early termination LOF del12 mutation in the ASGR1 gene (1 in 120 persons in the Icelandic study) and another early termination heterozygote LOF ASGR1 mutant (W158X) had lower plasma levels of non-HDL cholesterol than noncarriers (12).”
From Asialoglycoprotein receptor 1 is a novel PCSK9-independent ligand of liver LDLR cleaved by furin (2021) · cites this paper as [12]
In the citing paper
“The first report of ASGR1 mutation was based on a population genetic study and found a 12 bp deletion in ASGR1, which led to a loss of function.”
From Hypomorphic ASGR1 modulates lipid homeostasis via INSIG1-mediated SREBP signaling suppression (2021) · cites this paper as [3]
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Metadata
- Authors
- Nioi, P., Sigurdsson, A., Thorleifsson, G., Helgason, H., Agustsdottir, A. B., Norddahl, G. L., Helgadottir, A., Magnusdottir, A., Jonasdottir, A., Gretarsdottir, S., Jonsdottir, I., Steinthorsdottir, V., Rafnar, T., Swinkels, D. W., Galesloot, T. E., Grarup, N., Jørgensen, T., Vestergaard, H., Hansen, T., Lauritzen, T., Linneberg, A., Friedrich, N., Krarup, N. T., Fenger, M., Abildgaard, U., Hansen, P. R., Galløe, A. M., Braund, P. S., Nelson, C. P., Hall, A. S., Williams, M. J. A., van Rij, A. M., Jones, G. T., Patel, R. S., Levey, A. I., Hayek, S., Shah, S. H., Reilly, M., Eyjolfsson, G. I., Sigurdardottir, O., Olafsson, I., Kiemeney, L. A., Quyyumi, A. A., Rader, D. J., Kraus, W. E., Samani, N. J., Pedersen, O., Thorgeirsson, G., Masson, G., Holm, H., Gudbjartsson, D., Sulem, P., Thorsteinsdottir, U., & Stefansson, K.
- Affiliations
- University of Iceland (IS)
- Radboud University Nijmegen (NL)
- University of Copenhagen (DK)
- University of Leicester (GB)
- University of Leeds (GB)
- Emory University (US)
- ORCID
- Nioi, Paul
- Norddahl, Gudmundur L.
- Swinkels, Dorine W.
- Galesloot, Tessel E.
- Grarup, Niels
- Jørgensen, Torben
- Vestergaard, Henrik
- Hansen, Torben
- Lauritzen, Torsten
- Linneberg, Allan
- Krarup, Nikolaj T.
- Fenger, Mogens
- Hansen, Peter R.
- Braund, Peter S.
- Nelson, Christopher P.
- Hall, Alistair S.
- Williams, Michael J.A.
- Jones, Gregory T.
- Patel, Riyaz S.
- Levey, Allan I.
- Hayek, Salim
- Shah, Svati H.
- Reilly, Muredach
- Kiemeney, Lambertus A.
- Quyyumi, Arshed A.
- Rader, Daniel J.
- Kraus, William E.
- Samani, Nilesh J.
- Pedersen, Oluf
- Gudbjartsson, Daniel
- Sulem, Patrick
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2016-06-02
- Volume
- 374
- Issue
- 22
- Pages
- 2131-2141
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- OpenAlex
- W2404380044
- Cited by
- 189
- References
- 38
- Citations by year
- 2026: 22 · 2025: 15 · 2024: 30 · 2023: 18 · 2022: 13 · 2021: 19 · 2020: 15 · 2019: 12 · 2018: 11 · 2017: 27 · 2016: 7
- FWCI
- 15.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Leicester Research Archive (University of Leicester) (submittedVersion, cc-by-nc-nd)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Scopus (Elsevier) (submittedVersion)
- VBN Forskningsportal (Aalborg Universitet) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, other-oa)
- Hirsla (Landspítali University Hospital) (submittedVersion)
- Funders
- Emory University (RR025008, P30NS055077)
- National Institute for Health and Care Research (CL-2011-11-003, NF-SI-0611-10170)
- British Heart Foundation (FS/14/76/30933)
- Novo Nordisk
- Novo Nordisk Fonden
- Novo Nordisk Foundation Center for Basic Metabolic Research
- National Institutes of Health (RR025008)
- Medical Research Council (MR/L01629X/1)
- National Heart, Lung, and Blood Institute (R01HL089650)
- National Institute of Neurological Disorders and Stroke (P30NS055077)
- National Center for Research Resources (UL1RR025008)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Keywords
- ASGR1, asialoglycoprotein receptor, non-HDL cholesterol, coronary artery disease, haploinsufficiency, loss-of-function mutations, cryptic splice site, frameshift mutation, protein stability, genetic association, serum cholesterol
- MeSH terms
- Adult, Aged, Aged, 80 and over, Base Sequence, Cholesterol, Coronary Artery Disease, Female, Humans, Iceland, Male, Middle Aged, Molecular Sequence Data, Myocardial Infarction, Risk, Sequence Analysis, DNA, Genetic Predisposition to Disease, Asialoglycoprotein Receptor, White People, Kaplan-Meier Estimate, Haploinsufficiency
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