Apolipoprotein B metabolism in subjects with deficiency of apolipoproteins CIII and AI: evidence that apolipoprotein CIII inhibits catabolism of triglyceride-rich lipoproteins by lipoprotein lipase in vivo

Ginsberg, H N; Le, N A; Goldberg, I J; Gibson, J C; Rubinstein, A; Wang-Iverson, P; Norum, R; Brown, W V

doi:10.1172/jci112713

Cited by 424Lipid metabolism and disordersLipoproteins and Cardiovascular HealthCholesterol and Lipid Metabolism

Apolipoprotein B metabolism in subjects with deficiency of apolipoproteins CIII and AI: evidence that apolipoprotein CIII inhibits catabolism of triglyceride-rich lipoproteins by lipoprotein lipase in vivo

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Ginsberg, H N, Le, N A, Goldberg, I J, Gibson, J C, Rubinstein, A, Wang-Iverson, P, Norum, R, Brown, W V·1986·Journal of Clinical Investigation

DOI 10.1172/jci112713PMC PMC423815

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Abstract

Previous data suggest that apolipoprotein (apo) CIII may inhibit both triglyceride hydrolysis by lipoprotein lipase (LPL) and apo E-mediated uptake of triglyceride-rich lipoproteins by the liver. We studied apo B metabolism in very low density (VLDL), intermediate density (IDL), and low density lipoproteins (LDL) in two sisters with apo CIII-apo AI deficiency. The subjects had reduced levels of VLDL triglyceride, normal LDL cholesterol, and near absence of high density lipoprotein (HDL) cholesterol. Compartmental analysis of the kinetics of apo B metabolism after injection of 125I-VLDL and 131I-LDL revealed fractional catabolic rates (FCR) for VLDL apo B that were six to seven times faster than normal. Simultaneous injection of [3H]glycerol demonstrated rapid catabolism of VLDL triglyceride. VLDL apo B was rapidly and efficiently converted to IDL and LDL. The FCR for LDL apo B was normal. In vitro experiments indicated that, although sera from the apo CIII-apo-AI deficient patients were able to normally activate purified LPL, increasing volumes of these sera did not result in the progressive inhibition of LPL activity demonstrable with normal sera. Addition of purified apo CIII to the deficient sera resulted in 20-50% reductions in maximal LPL activity compared with levels of activity attained with the same volumes of the native, deficient sera. These in vitro studies, together with the in vivo results, indicate that in normal subjects apo CIII can inhibit the catabolism of triglyceride-rich lipoproteins by lipoprotein lipase.

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Loss-of-function variants of APOC3 that result in reduced synthesis of apoCIII are associated with absent or low circulating apoCIII levels, increased efficiency of triglyceride removal from triglyceride-rich lipoproteins, and lower plasma triglyceride levels.
“Loss-of-function variants of APOC3 that result in reduced synthesis of the protein are associated with absent or low circulating apoCIII levels, increased efficiency of TG removal from TRL, and lower plasma TG levels,59,60”
From Triglyceride-rich lipoproteins and their remnants: metabolic insights, role in atherosclerotic cardiovascular disease, and emerging therapeutic strategies—a consensus statement from the European Atherosclerosis Society (2021) · cites this paper as [59]
Individuals with LOF APOC3 variants have low plasma TG levels and markedly increased in vivo fractional turnover of VLDL-TG with efficient conversion of VLDL apoB to LDL, indicating increased lipolysis.
“Individuals with LOF APOC3 variants have low plasma TG levels59,60,187 and markedly increased in vivo fractional turnover of VLDL–TG with efficient conversion of VLDL apoB to LDL, indicating increased lipolysis.59,187”
From Triglyceride-rich lipoproteins and their remnants: metabolic insights, role in atherosclerotic cardiovascular disease, and emerging therapeutic strategies—a consensus statement from the European Atherosclerosis Society (2021) · cites this paper as [59]

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“Various proteins regulate LPL including: apoC1 (25,26), apoC2 (27), apoC3 (26,28), apoA5 (29), angiopoietin-like protein 3 (ANGPTL3) (30), ANGPTL4 (31,32), and ANGPTL8 (33).”
New Perspectives on Atherogenesis: Role of Abnormal Triglyceride-Rich Lipoprotein Metabolism
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Genetic Factors That Affect Risk of Alcoholic and Nonalcoholic Fatty Liver Disease
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Background
Metabolism of triglyceride-rich lipoproteins during alimentary lipemia.
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Pathophysiology of dyslipidaemia in the metabolic syndrome
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Overexpression of human apolipoprotein C-III in transgenic mice results in an accumulation of apolipoprotein B48 remnants that is corrected by excess apolipoprotein E.
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Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats
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LIPOPROTEIN PHYSIOLOGY
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The Roles of ApoC-III on the Metabolism of Triglyceride-Rich Lipoproteins in Humans
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“Inhibition of LPL-Mediated Lipolysis of TRLs Clearance of plasma triglycerides is directly linked to the lipolysis of TRLs by lipoprotein lipase (LPL) which is attached to the capillary endothelium in adipose tissue, skeletal muscle and the heart (63).”
Background
Chylomicronemia due to apolipoprotein CIII overexpression in apolipoprotein E-null mice. Apolipoprotein CIII-induced hypertriglyceridemia is not mediated by effects on apolipoprotein E.
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Familial combined hyperlipidaemia linked to the apolipoprotein AI–CIII–AIV gene cluster on chromosome 11q23q–q24
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Lack of apoA-I is not associated with increased susceptibility to atherosclerosis in mice.
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Inherited Apolipoprotein A-V Deficiency in Severe Hypertriglyceridemia
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Apolipoprotein C-III: from pathophysiology to pharmacology
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“Thus, subjects lacking apoC-III have low TRL levels due to an efficient lipolysis of TG [51], as also observed in mice with genetic deletion of the APOC3 gene [52].”
Background
Modulation of Lipoprotein B Binding to the LDL Receptor by Exogenous Lipids and Apolipoproteins CI, CII, CIII, and E
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LDL Containing Apolipoprotein CIII Is an Independent Risk Factor for Coronary Events in Diabetic Patients
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Expression of apolipoprotein C-III in McA-RH7777 cells enhances VLDL assembly and secretion under lipid-rich conditions
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The crucial roles of apolipoproteins E and C-III in apoB lipoprotein metabolism in normolipidemia and hypertriglyceridemia
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“ApoB metabolism was studied in two patients who had apoC-III deficiency in the context of apoA5/A4/C3/A1 gene cluster mutation [44].”
Background
Effects of the PPARγ agonist pioglitazone on lipoprotein metabolism in patients with type 2 diabetes mellitus
Nagashima, K., Lopez, C., Donovan, D., Ngai, C., Fontanez, N., Bensadoun, A., Fruchart-Najib, J., Holleran, S., Cohn, J. S., Ramakrishnan, R., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci200523219 · Cited by 201 · see citing works
Self-citation
The dual glucose‐dependent insulinotropic peptide and glucagon‐like peptide‐1 receptor agonist, tirzepatide, improves lipoprotein biomarkers associated with insulin resistance and cardiovascular risk in patients with type 2 diabetes
Wilson, J. M., Nikooienejad, A., Robins, D. A., Roell, W. C., Riesmeyer, J. S., Haupt, A., Duffin, K. L., Taskinen, M., & Ruotolo, G. (2020) · Diabetes Obesity and Metabolism · doi:10.1111/dom.14174 · Cited by 164 · see citing works
“It is well known that apoC-III is the inhibitor of lipoprotein lipase (LPL), the rate-limiting enzyme of the hydrolysis.(9,10) Recent data also suggest that apoC-III inhibition reduces plasma triglycerides by LPLindependent pathways by enhancing hepatic uptake of triglyceriderich lipoprotein (TRL) remnants via low-den…”
Background
Transcriptional Activation of Apolipoprotein CIII Expression by Glucose May Contribute to Diabetic Dyslipidemia
Caron, S., Verrijken, A., Mertens, I. L., Samanez, C. H., Mautino, G., Haas, J. T., Duran-Sandoval, D., Prawitt, J., Francque, S., Vallez, E., et al. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.220723 · Cited by 162 · see citing works
Transcriptional control of triglyceride metabolism: fibrates and fatty acids change the expression of the LPL and apo C-III genes by activating the nuclear receptor PPAR
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Hypertriglyceridemia: changes in the plasma lipoproteins associated with an increased risk of cardiovascular disease
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Detection, quantification, and characterization of potentially atherogenic triglyceride-rich remnant lipoproteins
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The role and mode of action of apolipoproteins CIII and AV: synergistic actors in triglyceride metabolism?
Willems van Dijk, K., Rensen, P. C., Voshol, P. J., & Havekes, L. M. (2004) · Current Opinion in Lipidology · doi:10.1097/00041433-200406000-00002 · Cited by 154 · see citing works
Metabolism and Modification of Apolipoprotein B-Containing Lipoproteins Involved in Dyslipidemia and Atherosclerosis
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Hypertriglyceridemia in the genomic era: a new paradigm
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Retinoids increase human apo C-III expression at the transcriptional level via the retinoid X receptor. Contribution to the hypertriglyceridemic action of retinoids.
Vu-Dac, N., Gervois, P., Torra, I. P., Fruchart, J. C., Kosykh, V, Kooistra, T., Princen, H. M., Dallongeville, J., & Staels, B. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1581 · Cited by 143 · see citing works
“First, apo C-III deficiency results in increased VLDL catabolism, whereas increased apo C-III synthesis occurs in hypertriglyceridemic patients (9, 10).”
Background
Fibrates, dyslipoproteinaemia and cardiovascular disease
Watts, G. F., & Dimmitt, S. B. (1999) · Current Opinion in Lipidology · doi:10.1097/00041433-199912000-00011 · Cited by 145 · see citing works
Metabolism of Very-Low-Density Lipoprotein and Low-Density Lipoprotein Containing Apolipoprotein C-III and Not Other Small Apolipoproteins
Mendivil, C. O., Zheng, C., Furtado, J., Lel, J., & Sacks, F. M. (2010) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.109.197830 · Cited by 145 · see citing works
The risk of cardiovascular events with increased apolipoprotein CIII: a systematic review and meta-analysis
Wyler von Ballmoos, M. C., Haring, B., & Sacks, F. M. (2015) · Journal of Clinical Lipidology · doi:10.1016/j.jacl.2015.05.002 · Cited by 134 · see citing works
“ApoC-III dampens clearance of apoB lipoproteins from the circulation by interfering with their binding to hepatic apoB/E receptors,1,2 and this is its most wellestablished property, supported by transgenic mouse experiments3–5 and human lipoprotein metabolism.6–8 Inhibition of VLDL clearance by apoC-III leads to hyper…”
Apolipoprotein C-III, metabolic syndrome, and risk of coronary artery disease
Olivieri, O., Bassi, A., Stranieri, C., Trabetti, E., Martinelli, N., Pizzolo, F., Girelli, D., Friso, S., Pignatti, P. F., & Corrocher, R. (2003) · Journal of Lipid Research · doi:10.1194/jlr.m300253-jlr200 · Cited by 139 · see citing works
“ApoC-III inhibits the hydrolysis of TG-rich particles by the lipoprotein lipase and their hepatic uptake mediated by apoE (9, 10 ).”
Background
PPARγ activators improve glucose homeostasis by stimulating fatty acid uptake in the adipocytes
Martin, G., Schoonjans, K., Staels, B., & Auwerx, J. H. (1998) · Atherosclerosis · doi:10.1016/s0021-9150(97)00315-8 · Cited by 138 · see citing works
Apolipoprotein C-III deficiency accelerates triglyceride hydrolysis by lipoprotein lipase in wild-type and apoE knockout mice
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Lipoprotein metabolism and its relationship to atherosclerosis
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Self-citation
Transcriptional Regulation of Apolipoprotein C-III Gene Expression by the Orphan Nuclear Receptor RORα
Raspé, E., Duez, H., Gervois, P., Fiévet, C., Fruchart, J., Besnard, S., Mariani, J., Tedgui, A., & Staels, B. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m004982200 · Cited by 134 · see citing works
Apolipoprotein B-100 kinetics in visceral obesity: Associations with plasma apolipoprotein C-III concentration
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Cholesterol Metabolism in CKD
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“In CKD, there is an upsurge in triglyceride-rich lipoproteins such as VLDL because of decreased levels of endothelium-bound LPL and mounting levels of apolipoprotein C-III (Apo-CIII), a competitive inhibitor of LPL activity.(38) LPL anchors to the capillary endothelial surface and catalyzes the hydrolysis of triglycer…”
Background
Triglycerides and remnant cholesterol associated with risk of aortic valve stenosis: Mendelian randomization in the Copenhagen General Population Study
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Update on the molecular biology of dyslipidemias
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Impaired chylomicron remnant clearance in familial combined hyperlipidemia.
Cabezas, M. C., de Bruin, T. W. A., Jansen, H., Kock, L. A., Kortlandt, W., & Erkelens, D. W. (1993) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.13.6.804 · Cited by 123 · see citing works
“-(31) The elimination of chylomicron remnants is predominantly dependent on apo E ligand function,(25) the putative apo E receptor (LDL receptor-related protein),(26) LPL protein binding,(32) HL activity,(33) and inhibitory factors like the apo C proteins.(34)-(36) The apo B/E receptor may also bind remnant particles…”
Background
Effect of Estrogen on Very Low Density Lipoprotein and Low Density Lipoprotein Subclass Metabolism in Postmenopausal Women1
Campos, H., Walsh, B. W., Judge, H., & Sacks, F. M. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.12.4437 · Cited by 125 · see citing works
“ApoCIII inhibits VLDL binding to the LDL receptor and to the LDL receptor-related protein (37) and inhibits triglyceride hydrolysis by both lipoprotein and hepatic lipase ( 38 ).”
Background
Plasma apolipoprotein A-I, A-II, B, E and C-III containing particles in men with premature coronary artery disease
GENESTJR, J., Bard, J., Fruchart, J., Ordovás, J. M., WILSON, P., & Schaefer, E. J. (1991) · Atherosclerosis · doi:10.1016/0021-9150(91)90109-g · Cited by 122 · see citing works
Endocrine and paracrine role of bile acids
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Markers of triglyceride-rich lipoprotein remnant metabolism in visceral obesity
Chan, D. C., Watts, G. F., Barrett, P. H., Mamo, J. C., & Redgrave, T. G. (2002) · Clinical Chemistry · doi:10.1093/clinchem/48.2.278 · Cited by 117 · see citing works
Combined hyperlipidemia in transgenic mice overexpressing human apolipoprotein Cl.
Shachter, N. S., Ebara, T., Ramakrishnan, R., Steiner, G. A., Breslow, J. L., Ginsberg, H. N., & Smith, J. D. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118857 · Cited by 117 · see citing works
“The role of apo CIII in elevating triglycerides has now been extensively validated by clinical observation (6–8), the study of the deficiency state (9), genetic linkage studies (10), and both transgenic (11–13) and knockout mice (14).”
BackgroundSelf-citation
ApoA-I deficiency causes both hypertriglyceridemia and increased atherosclerosis in human apoB transgenic mice
Voyiaziakis, E., Goldberg, I. J., Plump, A. S., Rubin, E. M., Breslow, J. L., & Huang, L. (1998) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)33893-1 · Cited by 111 · see citing works
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Postprandial hyperlipidemia, endothelial dysfunction and cardiovascular risk: focus on incretins
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“tant inhibitor of RLPs clearance [38,39].”
[2] Significance of apolipoproteins for structure, function, and classification of plasma lipoproteins
Alaupovic, P. (1996) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(96)63004-3 · Cited by 110 · see citing works
Regulation of Triglyceride Metabolism by PPARs : Fibrates and Thiazolidinediones have Distinct Effects
Auwerx, J. H., Schoonjans, K., Fruchart, J., & Staels, B. (1996) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat1994.3.81 · Cited by 110 · see citing works
GPIHBP1, an endothelial cell transporter for lipoprotein lipase
Young, S. G., Davies, B. S. J., Voss, C. V., Gin, P., Weinstein, M. M., Tontonoz, P., Reue, K., Bensadoun, A., Fong, L. G., & Beigneux, A. P. (2011) · Journal of Lipid Research · doi:10.1194/jlr.r018689 · Cited by 109 · see citing works
The Role of Lipids and Lipoproteins in Atherosclerosis
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Missense Mutation in APOC3 within the C-terminal Lipid Binding Domain of Human ApoC-III Results in Impaired Assembly and Secretion of Triacylglycerol-rich Very Low Density Lipoproteins
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Independent regulation of plasma apolipoprotein C–II and C–III concentrations in very low density and high density lipoproteins: implications for the regulation of the catabolism of these lipoproteins
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Self-citation
HDLs and alimentary lipemia. Studies in men with previous myocardial infarction at a young age.
Karpe, F., Bard, J., Steiner, G. A., Carlson, L. A., Fruchart, J., & Hamsten, A. (1993) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.13.1.11 · Cited by 101 · see citing works
Apolipoprotein CIII links dyslipidemia with atherosclerosis
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Effects of APOC3 Heterozygous Deficiency on Plasma Lipid and Lipoprotein Metabolism
Reyes-Soffer, G., Sztalryd, C., Horenstein, R. B., Holleran, S., Matveyenko, A., Thomas, T., Nandakumar, R., Ngai, C., Karmally, W., Ginsberg, H. N., et al. (2019) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.118.311476 · Cited by 97 · see citing works
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Saroglitazar, a novel PPAR α / γ agonist with predominant PPAR α activity, shows lipid‐lowering and insulin‐sensitizing effects in preclinical models
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“ApoCIII on the other hand appears to antagonize plasma TG metabolism, as it inhibits TG hydrolysis by LPL and hepatic lipase (Quarfordt et al. 1982; Ginsberg et al. 1986).”
Background
Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions.
Chunyu, Z., Christina, K., Katsunori, I., & Sacks, F. M. (2007) · Journal of Lipid Research · doi:10.1194/jlr.p600011-jlr200 · Cited by 95 · see citing works
“Patients with combined deficiency of apoC-III and apoA-I experience rapid VLDL clearance (20).”
Background
An ABC of apolipoprotein C-III: a clinically useful new cardiovascular risk factor?
Chan, D. C., Chen, M. M., Ooi, E. M. M., & Watts, G. F. (2008) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2007.01678.x · Cited by 85 · see citing works

Metabolism of Very-Low-Density Lipoprotein and Low-Density Lipoprotein Containing Apolipoprotein C-III and Not Other Small Apolipoproteins
Mendivil, C. O., Zheng, C., Furtado, J., Lel, J., & Sacks, F. M. (2010) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.109.197830 · Cited by 145 · see citing works
Metabolism of Very-Low-Density Lipoprotein and Low-Density Lipoprotein Containing Apolipoprotein C-III and Not Other
Apolipoproteins, S., Mendivil, C. O., Zheng, C., Furtado, J., Lel, J., & Sacks, F. M. (2016)
Editorial Apolipoprotein
Old, Y., Interesting, E. M., Ginsberg, H. N., & Brown, W. V. (2016)
Self-citation
Modulation of lipoprotein lipase activity by apolipoproteins. Effect of apolipoprotein C-III.
Wang, C. S., McConathy, W. J., Kloer, H. U., & Alaupovic, P. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111711 · Cited by 414 · see citing works
Life is complicated: so is apoCIII
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Self-citation

Authors: Ginsberg, H. N., Le, N. A., Goldberg, I. J., Gibson, J. C., Rubinstein, A., Wang-Iverson, P., Norum, R., & Brown, W. V.
Affiliations: Columbia University Irving Medical Center (US)
Icahn School of Medicine at Mount Sinai (US)
Henry Ford Hospital (US)
ORCID: Ginsberg, H N
Le, N A
Goldberg, I J
Rubinstein, A
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 1986-11-01
Volume: 78
Issue: 5
Pages: 1287-1295
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci112713
PMC: PMC423815
OpenAlex: W2057271976
Cited by: 424
References: 38
Citations by year: 2026: 4 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 11 · 2021: 15 · 2020: 23 · 2019: 9 · 2018: 15 · 2017: 18 · 2016: 12 · 2015: 18 · 2014: 11 · 2013: 14 · 2012: 8
FWCI: 4.39
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Heart, Lung, and Blood Institute (HL-23077, HL-00949)
National Center for Research Resources (RR 71)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Keywords: apolipoprotein C-III, apolipoprotein A-I deficiency, lipoprotein lipase inhibition, triglyceride-rich lipoproteins, VLDL, IDL, low-density lipoprotein, fractional catabolic rate, lipoprotein catabolism, lipoprotein lipase activation
MeSH terms: Adult, Apolipoproteins A, Apolipoproteins B, Apolipoproteins C, Cholesterol, Humans, Hypolipoproteinemias, Kinetics, Lipoprotein Lipase, Lipoproteins, LDL, Lipoproteins, VLDL, Models, Biological, Triglycerides, Apolipoprotein A-I, Apolipoprotein C-II

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Apolipoprotein B metabolism in subjects with deficiency of apolipoproteins CIII and AI: evidence that apolipoprotein CIII inhibits catabolism of triglyceride-rich lipoproteins by lipoprotein lipase in vivo

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