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The Journal of Lipid Research, Vol. 40, 1-16, January 1999
Copyright © 1999 by Lipid Research, Inc.
Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E
Robert W. Mahleya,b and
Zhong-Sheng Jia
a Gladstone Institute of Cardiovascular Disease, University of California, San Francisco, CA 94141-9100
a Cardiovascular Research Institute, University of California, San Francisco, CA 94141-9100
b Departments of Medicine and Pathology, University of California, San Francisco, CA 94141-9100
Correspondence to:
Robert W. Mahley
The plasma clearance of intestinally derived remnant lipoproteins by the liver is a process that likely involves three steps. Our model suggests that the initial rapid clearance by the liver begins with sequestration of the remnants within the space of Disse, where apolipoprotein E secreted by hepatocytes enhances remnant binding and uptake. Heparan sulfate proteoglycans (HSPG), which are also abundant in the space of Disse, mediate this enhanced binding. Next, the remnants undergo further processing in the space of Disse by hepatic and lipoprotein lipases, which may also serve as ligands mediating remnant uptake. The final step, endocytosis by hepatocytes, appears to be mediated, at least in part, by the low density lipoprotein (LDL) receptor and by the LDL receptor-related protein (LRP). Cell-surface HSPG play a critical role in remnant uptake, not only in the important initial sequestration or capture step in the space of Disse, but also as an essential or integral component of the HSPG-LRP pathway. In addition, HSPG appear to function alone as a receptor and display unique handling properties for specific isoforms of apolipoprotein E.Mahley, R. W., and Z-S. Ji. Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J. Lipid Res. 1999. 40: 116.
Supplementary key words:
remnants, apolipoprotein E, hepatic lipase, heparan sulfate proteoglycans, lipoprotein lipase

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Receptors, Mediators, and Mechanisms Involved in Bacterial Sepsis and Septic Shock
Clin. Microbiol. Rev.,
July 1, 2003;
16(3):
379 - 414.
[Abstract]
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[PDF]
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R. S. Kiss, P. M. M. Weers, V. Narayanaswami, J. Cohen, C. M. Kay, and R. O. Ryan
Structure-guided Protein Engineering Modulates Helix Bundle Exchangeable Apolipoprotein Properties
J. Biol. Chem.,
June 6, 2003;
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A. M. Anisfeld, H. R. Kast-Woelbern, M. E. Meyer, S. A. Jones, Y. Zhang, K. J. Williams, T. Willson, and P. A. Edwards
Syndecan-1 Expression Is Regulated in an Isoform-specific Manner by the Farnesoid-X Receptor
J. Biol. Chem.,
May 23, 2003;
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L. C. Wilsie and R. A. Orlando
The Low Density Lipoprotein Receptor-related Protein Complexes with Cell Surface Heparan Sulfate Proteoglycans to Regulate Proteoglycan-mediated Lipoprotein Catabolism
J. Biol. Chem.,
April 25, 2003;
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H. Saito, P. Dhanasekaran, D. Nguyen, F. Baldwin, K. H. Weisgraber, S. Wehrli, M. C. Phillips, and S. Lund-Katz
Characterization of the Heparin Binding Sites in Human Apolipoprotein E
J. Biol. Chem.,
April 18, 2003;
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[Abstract]
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J. Heeren, T. Grewal, A. Laatsch, D. Rottke, F. Rinninger, C. Enrich, and U. Beisiegel
Recycling of Apoprotein E Is Associated with Cholesterol Efflux and High Density Lipoprotein Internalization
J. Biol. Chem.,
April 11, 2003;
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[Abstract]
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H. Hidaka, M. Tozuka, B. Meyer, K. Yamauchi, M. Sugano, T. Nakabayashi, and T. Katsuyama
Characterization of Triglyceride Rich Lipoproteins with Very Light Density by Ultracentrifugation and Agarose Gel Electrophoresis using Triglyceride- and Cholesterol-Staining
Ann. Clin. Lab. Sci.,
April 1, 2003;
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[Abstract]
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R. L. Raffai, A. H. Hasty, Y. Wang, S. E. Mettler, D. A. Sanan, M. F. Linton, S. Fazio, and K. H. Weisgraber
Hepatocyte-derived ApoE Is More Effective than Non-hepatocyte-derived ApoE in Remnant Lipoprotein Clearance
J. Biol. Chem.,
March 21, 2003;
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E. Paradis, S. Clement, P. Julien, and M. R. Ven Murthy
Lipoprotein Lipase Affects the Survival and Differentiation of Neural Cells Exposed to Very Low Density Lipoprotein
J. Biol. Chem.,
March 7, 2003;
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R. E. Temel, J. S. Parks, and D. L. Williams
Enhancement of Scavenger Receptor Class B Type I-mediated Selective Cholesteryl Ester Uptake from apoA-I-/- High Density Lipoprotein (HDL) by Apolipoprotein A-I Requires HDL Reorganization by Lecithin Cholesterol Acyltransferase
J. Biol. Chem.,
February 7, 2003;
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G. Gerritsen, K. E. Kypreos, A. van der Zee, B. Teusink, V. I. Zannis, L. M. Havekes, and K. W. van Dijk
Hyperlipidemia in APOE2 transgenic mice is ameliorated by a truncated apoE variant lacking the C-terminal domain
J. Lipid Res.,
February 1, 2003;
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K. Yamauchi, M. Tozuka, E. Hidaka, I. Ueno, K. Matsuda, and T. Katsuyama
Internalization of {beta}-Amyloid Causes Downregulation of Apolipoprotein E mRNA Expression in Neuroblastoma Cells
Ann. Clin. Lab. Sci.,
January 1, 2003;
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K. von Bergmann, D. Lutjohann, B. Lindenthal, and A. Steinmetz
Efficiency of intestinal cholesterol absorption in humans is not related to apoE phenotype
J. Lipid Res.,
January 1, 2003;
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D. J. Blom, P. Byrnes, S. Jones, and A. D. Marais
Non-denaturing polyacrylamide gradient gel electrophoresis for the diagnosis of dysbetalipoproteinemia
J. Lipid Res.,
January 1, 2003;
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D. Y. Hui and P. N. Howles
Carboxyl ester lipase: structure-function relationship and physiological role in lipoprotein metabolism and atherosclerosis
J. Lipid Res.,
December 1, 2002;
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A. E. Mullick, R. J. Deckelbaum, I. J. Goldberg, M. Al-Haideri, and J. C. Rutledge
Apolipoprotein E and Lipoprotein Lipase Increase Triglyceride-Rich Particle Binding but Decrease Particle Penetration in Arterial Wall
Arterioscler. Thromb. Vasc. Biol.,
December 1, 2002;
22(12):
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P. C. R. Hopkins, Y. Huang, J. G. McGuire, and R. E. Pitas
Evidence for differential effects of apoE3 and apoE4 on HDL metabolism
J. Lipid Res.,
November 1, 2002;
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F. E. Thorngate, P. A. Strockbine, S. K. Erickson, and D. L. Williams
Altered adrenal gland cholesterol metabolism in the apoE-deficient mouse
J. Lipid Res.,
November 1, 2002;
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K. Olin-Lewis, R. M. Krauss, M. La Belle, P. J. Blanche, P. H. R. Barrett, T. N. Wight, and A. Chait
ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan
J. Lipid Res.,
November 1, 2002;
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H. N. Ginsberg
New Perspectives on Atherogenesis: Role of Abnormal Triglyceride-Rich Lipoprotein Metabolism
Circulation,
October 15, 2002;
106(16):
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S. Sandgren, F. Cheng, and M. Belting
Nuclear Targeting of Macromolecular Polyanions by an HIV-Tat Derived Peptide. ROLE FOR CELL-SURFACE PROTEOGLYCANS
J. Biol. Chem.,
October 4, 2002;
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M. Guerin, P. Egger, C. Soudant, W. Le Goff, A. van Tol, R. Dupuis, and M. J. Chapman
Cholesteryl ester flux from HDL to VLDL-1 is preferentially enhanced in type IIB hyperlipidemia in the postprandial state
J. Lipid Res.,
October 1, 2002;
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S. Bultel-Brienne, S. Lestavel, A. Pilon, I. Laffont, A. Tailleux, J.-C. Fruchart, G. Siest, and V. Clavey
Lipid Free Apolipoprotein E Binds to the Class B Type I Scavenger Receptor I (SR-BI) and Enhances Cholesteryl Ester Uptake from Lipoproteins
J. Biol. Chem.,
September 20, 2002;
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36092 - 36099.
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C. Vasandani, A. I. Kafrouni, A. Caronna, Y. Bashmakov, M. Gotthardt, J. D. Horton, and D. K. Spady
Upregulation of hepatic LDL transport by n-3 fatty acids in LDL receptor knockout mice
J. Lipid Res.,
May 1, 2002;
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D. C. Chan, G. F. Watts, P. H. R. Barrett, T. A. Mori, L. J. Beilin, and T. G. Redgrave
Mechanism of Action of a 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase Inhibitor on Apolipoprotein B-100 Kinetics in Visceral Obesity
J. Clin. Endocrinol. Metab.,
May 1, 2002;
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E.S. Tai, S. Demissie, L.A. Cupples, D. Corella, P.W. Wilson, E.J. Schaefer, and J.M. Ordovas
Association Between the PPARA L162V Polymorphism and Plasma Lipid Levels: The Framingham Offspring Study
Arterioscler. Thromb. Vasc. Biol.,
May 1, 2002;
22(5):
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S. S. Levinson
High Density- and Beta-Lipoprotein Screening for Risk of Coronary Artery Disease in the Context of New Findings on Reverse Cholesterol Transport
Ann. Clin. Lab. Sci.,
April 1, 2002;
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R. L. Raffai and K. H. Weisgraber
Hypomorphic Apolipoprotein E Mice. A NEW MODEL OF CONDITIONAL GENE REPAIR TO EXAMINE APOLIPOPROTEIN E-MEDIATED METABOLISM
J. Biol. Chem.,
March 22, 2002;
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T. M. Forte, G. Subbanagounder, J. A. Berliner, P. J. Blanche, A. O. Clermont, Z. Jia, M. N. Oda, R. M. Krauss, and J. K. Bielicki
Altered activities of anti-atherogenic enzymes LCAT, paraoxonase, and platelet-activating factor acetylhydrolase in atherosclerosis-susceptible mice
J. Lipid Res.,
March 1, 2002;
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J. D. Harris, I. R. Graham, S. Schepelmann, A. K. Stannard, M. L. Roberts, B. L. Hodges, V. Hill, A. Amalfitano, D. G. Hassall, J. S. Owen, et al.
Acute regression of advanced and retardation of early aortic atheroma in immunocompetent apolipoprotein-E (apoE) deficient mice by administration of a second generation [E1-, E3-, polymerase-] adenovirus vector expressing human apoE
Hum. Mol. Genet.,
January 1, 2002;
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43 - 58.
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M. H. MOGHADASIAN, B. M. McMANUS, L. B. NGUYEN, S. SHEFER, M. NADJI, D. V. GODIN, T. J. GREEN, J. HILL, Y. YANG, C. H. SCUDAMORE, et al.
Pathophysiology of apolipoprotein E deficiency in mice: relevance to apo E-related disorders in humans
FASEB J,
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D. T. Stein, S. Devaraj, D. Balis, B. Adams-Huet, and I. Jialal
Effect of Statin Therapy on Remnant Lipoprotein Cholesterol Levels in Patients With Combined Hyperlipidemia
Arterioscler. Thromb. Vasc. Biol.,
December 1, 2001;
21(12):
2026 - 2031.
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J. Heeren, T. Grewal, S. Jackle, and U. Beisiegel
Recycling of Apolipoprotein E and Lipoprotein Lipase through Endosomal Compartments in Vivo
J. Biol. Chem.,
November 2, 2001;
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J. Fan, H. Unoki, N. Kojima, H. Sun, H. Shimoyamada, H. Deng, M. Okazaki, H. Shikama, N. Yamada, and T. Watanabe
Overexpression of Lipoprotein Lipase in Transgenic Rabbits Inhibits Diet-induced Hypercholesterolemia and Atherosclerosis
J. Biol. Chem.,
October 19, 2001;
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C. P. Libeu, S. Lund-Katz, M. C. Phillips, S. Wehrli, M. J. Hernaiz, I. Capila, R. J. Linhardt, R. L. Raffai, Y. M. Newhouse, F. Zhou, et al.
New Insights into the Heparan Sulfate Proteoglycan-binding Activity of Apolipoprotein E
J. Biol. Chem.,
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T. Hirano, T. Takahashi, S. Saito, H. Tajima, T. Ebara, and M. Adachi
Apoprotein C-III deficiency markedly stimulates triglyceride secretion in vivo: comparison with apoprotein E
Am J Physiol Endocrinol Metab,
October 1, 2001;
281(4):
E665 - E669.
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J. W. Burgess and Y. L. Marcel
Dynamic and stable pools of apoE differ functionally at the HepG2 cell surface
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September 1, 2001;
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U. Olsson, A.-C. Egnell, M. R. Lee, G. O. Lunden, M. Lorentzon, M. Salmivirta, G. Bondjers, and G. Camejo
Changes in Matrix Proteoglycans Induced by Insulin and Fatty Acids in Hepatic Cells May Contribute to Dyslipidemia of Insulin Resistance
Diabetes,
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S. Lund-Katz, S. Wehrli, M. Zaiou, Y. Newhouse, K. H. Weisgraber, and M. C. Phillips
Effects of polymorphism on the microenvironment of the LDL receptor-binding region of human apoE
J. Lipid Res.,
June 1, 2001;
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M.-a. Kawashiri, Y. Zhang, D. Usher, M. Reilly, E. Puré, and D. J. Rader
Effects of coexpression of the LDL receptor and apoE on cholesterol metabolism and atherosclerosis in LDL receptor-deficient mice
J. Lipid Res.,
June 1, 2001;
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G. Datta, D. W. Garber, B. H. Chung, M. Chaddha, N. Dashti, W. A. Bradley, S. H. Gianturco, and G. M. Anantharamaiah
Cationic domain 141-150 of apoE covalently linked to a class A amphipathic helix enhances atherogenic lipoprotein metabolism in vitro and in vivo
J. Lipid Res.,
June 1, 2001;
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H. Relas, H. Gylling, and T. A. Miettinen
Fate of intravenously administered squalene and plant sterols in human subjects
J. Lipid Res.,
June 1, 2001;
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K. J. Bame
Heparanases: endoglycosidases that degrade heparan sulfate proteoglycans
Glycobiology,
June 1, 2001;
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Copyright © 1999 by the American Society for Biochemistry and Molecular Biology.
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