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Coding Variation in ANGPTL4, LPL, and SVEP1 and the Risk of Coronary Disease
Open accessAbstract
BACKGROUND: The discovery of low-frequency coding variants affecting the risk of coronary artery disease has facilitated the identification of therapeutic targets. METHODS: Through DNA genotyping, we tested 54,003 coding-sequence variants covering 13,715 human genes in up to 72,868 patients with coronary artery disease and 120,770 controls who did not have coronary artery disease. Through DNA sequencing, we studied the effects of loss-of-function mutations in selected genes. RESULTS: We confirmed previously observed significant associations between coronary artery disease and low-frequency missense variants in the genes LPA and PCSK9. We also found significant associations between coronary artery disease and low-frequency missense variants in the genes SVEP1 (p.D2702G; minor-allele frequency, 3.60%; odds ratio for disease, 1.14; P=4.2×10(-10)) and ANGPTL4 (p.E40K; minor-allele frequency, 2.01%; odds ratio, 0.86; P=4.0×10(-8)), which encodes angiopoietin-like 4. Through sequencing of ANGPTL4, we identified 9 carriers of loss-of-function mutations among 6924 patients with myocardial infarction, as compared with 19 carriers among 6834 controls (odds ratio, 0.47; P=0.04); carriers of ANGPTL4 loss-of-function alleles had triglyceride levels that were 35% lower than the levels among persons who did not carry a loss-of-function allele (P=0.003). ANGPTL4 inhibits lipoprotein lipase; we therefore searched for mutations in LPL and identified a loss-of-function variant that was associated with an increased risk of coronary artery disease (p.D36N; minor-allele frequency, 1.9%; odds ratio, 1.13; P=2.0×10(-4)) and a gain-of-function variant that was associated with protection from coronary artery disease (p.S447*; minor-allele frequency, 9.9%; odds ratio, 0.94; P=2.5×10(-7)). CONCLUSIONS: We found that carriers of loss-of-function mutations in ANGPTL4 had triglyceride levels that were lower than those among noncarriers; these mutations were also associated with protection from coronary artery disease. (Funded by the National Institutes of Health and others.).
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In the citing paper
“rare loss-of-function mutations in the lipoprotein lipase (LPL) gene are associated with higher plasma triglyceride levels and a higher risk of cardiovascular disease”
From Association of Triglyceride-Lowering LPL Variants and LDL-C–Lowering LDLR Variants With Risk of Coronary Heart Disease (2019) · cites this paper as [13]
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
“while rare, loss-of-function mutations in the APOC3, ANGPTL3, and ANGPTL4 genes, which encode for natural inhibitors of LPL, are associated with lower triglyceride levels and a corresponding lower risk of cardiovascular disease.[9][10][11][12][13]”
From Association of Triglyceride-Lowering LPL Variants and LDL-C–Lowering LDLR Variants With Risk of Coronary Heart Disease (2019) · cites this paper as [13]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“ANGPTL4 loss-of-function mutations in humans are associated with lower plasma triglycerides (40, 56–58).”
From Regulation of lipoprotein metabolism by ANGPTL3, ANGPTL4, and ANGPTL8 (2021) · cites this paper as [57]
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In the citing paper
“Importantly, multiple studies found that individuals deficient in one of these three ANGPTL proteins have a lower risk of cardiovascular disease (56, 57, 163–166).”
From Regulation of lipoprotein metabolism by ANGPTL3, ANGPTL4, and ANGPTL8 (2021) · cites this paper as [57]
In the citing paper
“large-scale genetic studies have shown that individuals carrying loss-of-function mutations in ANGPTL4 exhibit a lower risk of coronary artery disease compared to noncarriers [34,35].”
From Identifying novel drug targets for calcific aortic valve disease through Mendelian randomization (2025) · cites this paper as [34]
In the citing paper
“Mendelian randomization studies focused on variants in the genes encoding apoAV, apoCIII, lipoprotein lipase (LpL) and the angiopoietin-like proteins 3, 4, and 8 (ANGPTL3, ANGPTL4, and ANGPTL8) have been highly informative.29–35”
In the citing paper
“Similarly, heterozygous LOF variants in ANGPTL311 and ANGPTL412 genes are associated with reductions both in plasma TG and ASCVD risk.”
From Clinical review on triglycerides (2020) · cites this paper as [12]
In the citing paper
“Genetically attenuated ANGPTL4 is associated with favourable lipid and glycaemia profiles, and with reduced ASCVD risk.12,99”
From Clinical review on triglycerides (2020) · cites this paper as [12]
In the citing paper
“defects in genes controlling TG metabolism, including APOC3, ANGPTL3 and ANGPTL4 that have been linked to reduced TG and are associated with reduced coronary calcification25 or reduced CVD risk.26-30”
From Is Isolated Low High-Density Lipoprotein Cholesterol a Cardiovascular Disease Risk Factor?: New Insights From the Framingham Offspring Study (2016) · cites this paper as [29]
In the citing paper
“Like mice, humans deficient in ANGPTL3, ANGPTL4, or ANGPTL8 have lower plasma triglycerides (56–58, 163–166).”
From Regulation of lipoprotein metabolism by ANGPTL3, ANGPTL4, and ANGPTL8 (2021) · cites this paper as [57]
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Metadata
- Authors
- Myocardial Infarction Genetics and CARDIoGRAM Exome Consortia Investigators
- Corresponding author
- Myocardial Infarction Genetics and CARDIoGRAM Exome Consortia Investigators
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2016-03-24
- Volume
- 374
- Issue
- 12
- Pages
- 1134-1144
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC4850838
- OpenAlex
- W2294822677
- Cited by
- 493
- References
- 25
- Citations by year
- 2026: 16 · 2025: 31 · 2024: 26 · 2023: 26 · 2022: 50 · 2021: 63 · 2020: 58 · 2019: 52 · 2018: 58 · 2017: 69 · 2016: 44
- FWCI
- 60.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Figshare (submittedVersion)
- IrInSubria (University of Insubria) (submittedVersion)
- Leicester Research Archive (University of Leicester) (submittedVersion, other-oa)
- Lund University Publications (Lund University) (submittedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Research Portal (Queen's University Belfast) (submittedVersion)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
- OPUS (Augsburg University) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- American Heart Association
- Massachusetts General Hospital (R01HL107816)
- Foundation for Barnes-Jewish Hospital
- Donovan Family Foundation
- University of Dundee
- Queen Mary University of London
- Wellcome Trust (098381, 090532, 090532/Z/09/Z, 090532/Z/09/)
- Deutsches Zentrum für Herz-Kreislaufforschung
- Massachusetts Medical Society
- NIHR Biomedical Research Centre, Royal Marsden NHS Foundation Trust/Institute of Cancer Research
- National Institute for Health and Care Research (NF-SI-0512-10165, NF-SI-0611-10170, NF-SI-0611-10099)
- British Heart Foundation (090532/Z/09/Z, RG/13/13/30194, RG/08/014/24067, RG/14/5/30893)
- University of Leicester
- University College London
- University of Oxford
- European Commission (EU-FP7, 261123, 098381)
- University of Glasgow
- Deutsche Forschungsgemeinschaft (SFB1123)
- Fondation Leducq (12CVD02)
- Universiteit van Amsterdam
- Bundesministerium für Bildung und Forschung
- Ministero della Salute
- Novo Nordisk Fonden (NNF16OC0021370, NNF14OC0011049, NNF15OC0016320)
- Exzellenzclusters Entzündungsforschung
- National Institutes of Health (UL1TR001070)
- Medical Research Council (MC_UU_12015/1, MR/N005813/1, MC_PC_13048, EU FP7, MR/L003120/1)
- Barts and The London School of Medicine and Dentistry
- National Heart, Lung, and Blood Institute (R01HL127564, K08HL114642, K01HL125751, R01HL107816)
- National Human Genome Research Institute (U01HG008672)
- National Cancer Institute (R25CA094880)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
- Keywords
- coronary artery disease, ANGPTL4, lipoprotein lipase, SVEP1, missense mutations, loss-of-function mutations, gain-of-function mutations, myocardial infarction, triglyceride levels, PCSK9, LPA, genetic risk factors, triglyceride lowering
- MeSH terms
- Angiopoietin-Like Protein 4, Aged, Coronary Artery Disease, Female, Humans, Lipoprotein Lipase, Male, Middle Aged, Mutation, Risk Factors, Triglycerides, Cell Adhesion Molecules, Sequence Analysis, DNA, Mutation, Missense, Angiopoietins, Genotyping Techniques
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