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

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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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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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Background
Mitogen-activated Protein Kinase Regulates Transcription of the ApoCIII Gene
Reddy, S. L., Yang, W., Taylor, D. G., Shen, X.-Q., Oxender, D. L., Kust, G. A., & Leff, T. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.46.33050 · Cited by 47
Lipoprotein Metabolism
Shepherd, J. (1994) · Drugs · doi:10.2165/00003495-199400472-00003 · Cited by 49
Effect of Combination Therapy With Fenofibrate and Simvastatin on Postprandial Lipemia in the ACCORD Lipid Trial
Reyes‐Soffer, G., Ngai, C. I., Lovato, L., Karmally, W., Ramakrishnan, R., Holleran, S., & Ginsberg, H. N. (2012) · Diabetes Care · doi:10.2337/dc11-2556 · Cited by 49
“Indeed, we found that both plasma apoCIII and, more importantly, in a subset of subjects, non-HDL apoCIII concentrations were reduced throughout the day-long study in FENO-S compared with PL-S, consistent with better lipolysis in the FENO-S group (37).”
ResultSelf-citation
Efficacy and Safety of Pemafibrate, a Novel Selective Peroxisome Proliferator-Activated Receptor α Modulator (SPPARMα): Pooled Analysis of Phase 2 and 3 Studies in Dyslipidemic Patients with or without Statin Combination
Yamashita, S., Arai, H., Yokote, K., Araki, E., Matsushita, M., Nojima, T., Suganami, H., & Ishibashi, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225537 · Cited by 49
“Decreases in ApoCIII and ApoCIII/ApoCII may reflect accelerated catabolism of TG by lipoprotein lipase (LPL) [28].”
Background
Genetic influences on lipid metabolism trait variability within the Stanislas Cohort
Pallaud, C., Gueguen, R., Sass, C., Grow, M. A., Cheng, S., Siest, G., & Visvikis‐Siest, S. (2001) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31514-5 · Cited by 47
“Evidence is accumulating that apoC-III regulates TRL metabolism by modulating their lipolysis (36) and their receptor-mediated uptake (37).”
Metabolic pathogenesis of familial combined hyperlipidaemia with emphasis on insulin resistance, adipose tissue metabolism and free fatty acids.
Graaf, J. D., Veerkamp, M. J., & Stalenhoef, A. F. H. (2002) · Europe PMC (PubMed Central) · Cited by 47
Apolipoprotein B48 metabolism in chylomicrons and very low-density lipoproteins and its role in triglyceride transport in normo- and hypertriglyceridemic human subjects
Björnson, E., Packard, C. J., Adiels, M., Andersson, L., Matikainen, N., Söderlund, S., Kahri, J., Hakkarainen, A., Lundbom, N., Lundbom, J., et al. (2020) · Journal of Internal Medicine · doi:10.1111/joim.13017 · Cited by 46
Phenotypes and Genotypes of High Density Lipoprotein Cholesterol in Exceptional Longevity
Milman, S., Atzmon, G., Crandall, J. P., & Barzilai, N. (2013) · Current Vascular Pharmacology · doi:10.2174/1570161111666131219101551 · Cited by 46
“It inhibits triglyceride hydrolysis by lipoprotein lipase (LPL) and interferes with clearance of triglyceride rich particles from plasma[32].”
Background
Differential Metabolism of Human VLDL According to Content of ApoE and ApoC-III
Tomiyasu, K., Walsh, B. W., Ikewaki, K., Judge, H., & Sacks, F. M. (2001) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/hq0901.094489 · Cited by 49
Vaccination in Atherosclerosis
Nettersheim, F. S., Vore, L. D., & Winkels, H. (2020) · Cells · doi:10.3390/cells9122560 · Cited by 47
“APOC3 can contribute to hypertriglyceridemia by inhibiting hydrolysis of triglyceride-rich lipoproteins [98] and reducing hepatic uptake of triglyceride-rich lipoproteins [99].”
Background
ApoE ε2/ε3/ε4 polymorphism, ApoC-III/ApoE ratio and metabolic syndrome
Olivieri, O., Martinelli, N., Bassi, A., Trabetti, E., Girelli, D., Pizzolo, F., Friso, S., Pignatti, P. F., & Corrocher, R. (2007) · Clinical and Experimental Medicine · doi:10.1007/s10238-007-0142-y · Cited by 46
“ApoC-III is an essential constituent of these circulating particles [15] with the specific property of inhibiting their hydrolysis by lipoprotein lipase and their ApoE-mediated hepatic uptake [16, 17].”
Background
Peroxisome proliferator-activated receptor subtype-specific regulation of hepatic and peripheral gene expression in the zucker diabetic fatty rat
Dana, S. L., Hoener, P. A., Bilakovics, J. M., Crombie, D. L., Ogilvie, K. M., Kauffman, R. F., Mukherjee, R., & Paterniti, J. R. (2001) · Metabolism · doi:10.1053/meta.2001.24870 · Cited by 46
Treatment with high-dose simvastatin reduces secretion of apolipoprotein B-lipoproteins in patients with diabetic dyslipidemia
Myerson, M. L., Ngai, C. I., Jones, J. E., Holleran, S., Ramakrishnan, R., Berglund, L., & Ginsberg, H. N. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500335-jlr200 · Cited by 42
“Although we did not study normal subjects in this investigation, we have previously reported secretion rates of 15 and 13 mg/kg/day for VLDL- and LDLapoB, respectively, in normal individuals (40), consistent with reports from other laboratories (41).”
ResultSelf-citation
Lipoprotein transport in the metabolic syndrome: pathophysiological and interventional studies employing stable isotopy and modelling methods
Chan, D. C., Barrett, P. H. R., & Watts, G. F. (2004) · Clinical Science · doi:10.1042/cs20040109 · Cited by 44
Effects of Bariatric Surgery on Hepatic and Intestinal Lipoprotein Particle Metabolism in Obese, Nondiabetic Humans
Padilla, N., Maraninchi, M., Béliard, S., Berthet, B., Nogueira, J. P., Wolff, E., Nicolay, A., Corroller, A. B., Dubois, N., Grangeot, R., et al. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303849 · Cited by 44
Kinetics of lipolysis of very low density lipoproteins by lipoprotein lipase. Importance of particle number and noncompetitive inhibition by particles with low triglyceride content.
Connelly, P. W., Maguire, G. F., Vézina, C., Hegele, R. A., & Kuksis, A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32029-x · Cited by 45
P-407-induced Mouse Model of Dose-controlled Hyperlipidemia and Atherosclerosis: 25 Years Later
Johnston, T. P., Короленко, Т. А., & Sahebkar, A. (2017) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000522 · Cited by 42
Characterization of Recombinant Wild Type and Site-Directed Mutations of Apolipoprotein C-III: Lipid Binding, Displacement of ApoE, and Inhibition of Lipoprotein Lipase
Liu, H., Talmud, P. J., Lins, L., Brasseur, R., Olivecrona, G., Peelman, F., Vandekerckhove, J. S., Rosseneu, M., & Labeur, C. (2000) · Biochemistry · doi:10.1021/bi0009441 · Cited by 42
Cell Culture Conditions Determine Apolipoprotein CIII Secretion and Regulation by Fibrates in Human Hepatoma HepG2 Cells
Barthelemy-Clavey, V., Copin, C., Mariotte, M. C., Baugé, E., Chinetti, G., Fruchart, J., Fruchart, J. C., Dallongeville, J., & Staels, B. (1999) · Cellular Physiology and Biochemistry · doi:10.1159/000016311 · Cited by 43
Apolipoprotein CIII bound to apoB-containing lipoproteins is associated with small, dense LDL independent of plasma triglyceride levels in healthy men
Shin, M., & Krauss, R. M. (2010) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2010.02.025 · Cited by 40
Characterization of the lipid-binding properties and lipoprotein lipase inhibition of a novel apolipoprotein C-III variant Ala23Thr
Liu, H., Labeur, C., Xu, C., Ferrell, R. E., Lins, L., Brasseur, R., Rosseneu, M., Weiss, K. M., Humphries, S. E., & Talmud, P. J. (2000) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31969-6 · Cited by 43
A variation in the apolipoprotein C-III gene is associated with an increased number of circulating VLDL and IDL particles in familial combined hyperlipidemia
Ribalta, J., Ville, A. E. L., Vallvé, J.-C., Humphries, S. E., Turner, P. R., & Masana, L. (1997) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37189-3 · Cited by 42
Severe hypertriglyceridemia: Existing and emerging therapies
Malick, W. A., Do, R., & Rosenson, R. S. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108544 · Cited by 45
Lack of effect of apolipoprotein C3 polymorphisms on indices of liver steatosis, lipid profile and insulin resistance in obese Southern Europeans
Sentinelli, F., Romeo, S., Maglio, C., Incani, M., Burza, M. A., Scano, F., Coccia, F., Cossu, E., Leonetti, F., & Baroni, M. G. (2011) · Lipids in Health and Disease · doi:10.1186/1476-511x-10-93 · Cited by 39
“Apolipoprotein C3 inhibits the hydrolysis of TG-rich particles by lipoprotein lipase and their apoE-mediated hepatic uptake [8,9].”
Background
Interaction between the APOC3 gene promoter polymorphisms, saturated fat intake and plasma lipoproteins
Brown, S. (2003) · Atherosclerosis · doi:10.1016/s0021-9150(03)00293-4 · Cited by 41
“ApoCIII inhibits lipoprotein lipase and hepatic clearance of triglyceride-rich lipoproteins in vitro [2,3].”
Background
Is apolipoprotein A5 a novel regulator of triglyceride‐rich lipoproteins?
Jäkel, H., Nowak, M., Helleboid‐Chapman, A., Fruchart‐Najib, J., & Fruchart, J. (2006) · Annals of Medicine · doi:10.1080/07853890500407488 · Cited by 40
“Apolipoproteins are important mediators of plasma lipids and members of this family such as apo-CIII are known to strongly influence plasma triglyceride concentrations (10).”
Background
Apolipoprotein CIII Deficiency Protects Against Atherosclerosis in Knockout Rabbits
Yan, H., Niimi, M., Matsuhisa, F., Zhou, H., Kitajima, S., Chen, Y., Wang, C., Yang, X., Yao, J. Q., Yang, D., et al. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.314368 · Cited by 39
High-density lipoprotein and transport of cholesterol and triglyceride in blood
Brown, W. V. (2007) · Journal of clinical lipidology · doi:10.1016/j.jacl.2007.02.001 · Cited by 42
Self-citation
Dose-dependent effect of rosuvastatin on apolipoprotein B-100 kinetics in the metabolic syndrome
Ooi, E. M. M., Barrett, P. H. R., Chan, D. C., Nestel, P. J., & Watts, G. F. (2007) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2007.03.004 · Cited by 39
The SsíI polymorphism of the apolipoprotein C-III gene determines the insulinresponse to an oral-glucose-tolerance test after consumption of a diet rich in saturated fats
Salas-Coronas, J., Jansen, S., López‐Miranda, J., Ordovás, J. M., Castro, P., Marin, C., Ostos, M. A., Bravo, M. D., Jiménez-Perepérez, J., Blanco, A., et al. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/68.2.396 · Cited by 39
Loganin inhibits the inflammatory response in mouse 3T3L1 adipocytes and mouse model
Li, Y., Li, Z., Shi, L., Zhao, C., Shen, B., Tian, Y., & Feng, H. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.04.026 · Cited by 38
The apolipoprotein C-III (Gln38Lys) variant associated with human hypertriglyceridemia is a gain-of-function mutation
Sundaram, M., Curtis, K. R., Alipour, M. A., LeBlond, N. D., Margison, K. D., Yaworski, R., Parks, R. J., McIntyre, A. D., Hegele, R. A., Fullerton, M. D., et al. (2017) · Journal of Lipid Research · doi:10.1194/jlr.m077313 · Cited by 40
Targeting apoC-III and ANGPTL3 in the treatment of hypertriglyceridemia
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“Underlining this concept, transgenic mice expressing 100 copies of the APOC3 gene are severely hypertriglyceridemic [43].”
Background
Apolipoprotein C3 SstI polymorphism and triglyceride levels in Asian Indians
Chhabra, S., Narang, R., Krishnan, L., Vasisht, S., Agarwal, D., Lm, S., Manchanda, S., & Das, N. (2002) · BMC Genetics · doi:10.1186/1471-2156-3-9 · Cited by 40
Apolipoprotein C-III displacement of apolipoprotein E from VLDL: effect of particle size
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Self-citation
Novel drugs approved by the EMA, the FDA and the MHRA in 2024: A year in review
Topouzis, S., Papapetropoulos, A., Alexander, S. P. H., Cortese-Krott, M. M., Kendall, D. A., Martemyanov, K. A., Mauro, C., Nagercoil, N., Panettieri, R. A., Patel, H. H., et al. (2025) · British Journal of Pharmacology · doi:10.1111/bph.17458 · Cited by 42
“In addition, apoC3 can also inhibit hepatic lipase activity-mediated hepatic clearance of remnants of triglyceride-rich lipoproteins (Gaudet et al., 2014; Ginsberg et al., 1986).”
Hypertriglyceridemia and delayed clearance of fat load in transgenic rabbits expressing human apolipoprotein CIII
Ding, Y., Wang, Y., Zhu, H., Fan, J., Yu, L., Liu, C., & Liu, E. (2010) · Transgenic Research · doi:10.1007/s11248-010-9467-5 · Cited by 36
“Moreover, LPL inhibitory effect of apoCIII had been documented long time ago in human studies in vitro (Kinnunen and Ehnolm 1976) and in vivo ( Ginsberg et al. 1986 ).”
BackgroundInfluential
Reduced kidney lipoprotein lipase and renal tubule triglyceride accumulation in cisplatin-mediated acute kidney injury
Li, S., Nagothu, K. K., Ranganathan, G., Ali, S. M., Shank, B. B., Gökden, N., Ayyadevara, S., Megyesi, J. K., Olivecrona, G., Chugh, S. S., et al. (2012) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00111.2012 · Cited by 37

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 › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › 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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