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Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing
Open accessAbstract
Unraveling the mechanisms controlling remnant lipoprotein clearance is important, as these lipoproteins are highly atherogenic. The most critical molecule in this process is apoE, which mediates high-affinity binding of remnant lipoproteins to members of the LDL receptor (LDLR) family and cell-surface heparan sulfate proteoglycans (HSPGs), which have been shown to play major independent as well as cooperative roles in remnant lipoprotein clearance. While all the players may have been identified, our understanding of how they interact and function together continues to evolve. In this issue of the JCI, MacArthur et al. (see the related article beginning on page 153) demonstrated that HSPGs under normal physiological conditions are critically important in the clearance of remnant lipoproteins, independent of LDLR family members. The complexity of VLDL and chylomicron remnant clearance was exemplified by the studies of Jones et al., also in this issue (see the related article beginning on page 165). Despite defective clearance of LDL in mice with a deficiency in the adaptor protein controlling internalization of the LDLR, called autosomal recessive hypercholesterolemia (ARH), remnant lipoprotein clearance was not grossly abnormal. A likely explanation is that the abnormal LDLRs bind the remnants and then transfer them to another acceptor for internalization. While the studies clearly demonstrate that the LDLR-related protein 1 is not involved and suggest a role for an additional unidentified receptor, it remains a possibility that HSPGs are responsible for remnant uptake by hepatocytes in the presence of defective LDLR internalization.
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“Hepatic clearance of VLDL remnants is mediated by either apoB100 or apoE through receptor-dependent and receptor-independent pathways;7,17,71,73 25–75% of these particles are removed directly rather than converted to LDL.”
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“For chylomicron remnants, functional apoE on the particle is required (apoB48 is not a ligand).71”
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“VLDL and remnants are also enriched in apoE and apoCIII, both implicated in binding and retention in the artery wall.5,71,125”
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Citations
Cites
The Metabolic and Molecular Bases of Inherited Disease
Scriver, R. C. (1995) · Medical Entomology and Zoology · Cited by 12,101
Apolipoprotein E: Cholesterol Transport Protein with Expanding Role in Cell Biology
Mahley, R. W. (1988) · Science · doi:10.1126/science.3283935 · Cited by 4,028
Self-citationFunctions of Cell Surface Heparan Sulfate Proteoglycans
Bernfield, M. R., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. M., & Zako, M. (1999) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.68.1.729 · Cited by 2,722
Plump, A. S., Smith, J. D., Hayek, T., Aalto-Setälä, K., Walsh, A., Verstuyft, J. G., Rubin, E. M., & Breslow, J. L. (1992) · Cell · doi:10.1016/0092-8674(92)90362-g · Cited by 2,263
Spontaneous Hypercholesterolemia and Arterial Lesions in Mice Lacking Apolipoprotein E
Zhang, S. H., Reddick, R. L., Piedrahita, J. A., & Maeda, N. (1992) · Science · doi:10.1126/science.1411543 · Cited by 2,237
Order Out of Chaos: Assembly of Ligand Binding Sites in Heparan Sulfate
Esko, J. D., & Selleck, S. B. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135458 · Cited by 1,495
Brodie, S. E. (1996) · Survey of Ophthalmology · doi:10.1016/s0039-6257(96)80075-0 · Cited by 770
Mahley, R. W., & Ji, Z.-S. (1999) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)33334-4 · Cited by 693
Self-citationGarcia, C. K., Wilund, K., Arca, M., Zuliani, G., Fellin, R., Maioli, M., Calandra, S., Bertolini, S., Cossu, F., Grishin, N., et al. (2001) · Science · doi:10.1126/science.1060458 · Cited by 624
Rohlmann, A., Gotthardt, M., Hammer, R. E., & Herz, J. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1240 · Cited by 455
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- Mahley, 1991, JAMA., 265, 78, 10.1001/jama.1991.03460010078035 · DOI
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Items 101–160 of 160
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Feo, E. D., Rowell, J. L., Cadoni, G., Nicolotti, N., Arzani, D., Giorgio, A., Amore, R., Paludetti, G., Ricciardi, G., & Boccia, S. (2010) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0624 · Cited by 17
Diagnosis and Management of Familial Dyslipoproteinemias
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Yao, X., Dai, C., Fredriksson, K., Lam, J. Y., Gao, M., Keeran, K. J., Nugent, G. Z., Qu, X., Yu, Z., Jeffries, N. O., et al. (2011) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00110.2011 · Cited by 14
Anower-E-Khuda, F., Singh, G., Deng, Y., Gordts, P. L. S. M., & Esko, J. D. (2019) · Glycobiology · doi:10.1093/glycob/cwz037 · Cited by 14
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Papaioannou, I., Simons, J. P., & Owen, J. S. (2012) · Cardiology Research and Practice · doi:10.1155/2012/148796 · Cited by 15
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Garai, J., Uddo, R. B., Mohler, M. C., Pelligrino, N. E., Scribner, R. A., SOTHERN, M. S., & Zabaleta, J. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1804-1_36 · Cited by 13
Johnson, L. A., Altenburg, M. K., Walzem, R. L., Scanga, L., & Maeda, N. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.169680 · Cited by 13
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EDEM3 Modulates Plasma Triglyceride Level Through Its Regulation of LRP1 Expression
Xu, Y., Peloso, G. M., Nagai, T. H., Mizoguchi, T., Deik, A., Bullock, K. H., Lin, H., Musunuru, K., Yang, Q., Vasan, R. S., et al. (2019) · iScience · doi:10.1016/j.isci.2020.100973 · Cited by 11
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Ahmad, N., Girardet, J., Akbar, S., Lanhers, M., Paris, C., Yen, F. T., & Corbier, C. (2012) · FEBS Journal · doi:10.1111/febs.12026 · Cited by 10
Bamji‐Mirza, M., Sundaram, M., Zhong, S., Yao, E. F., Parks, R. J., & Yao, Z. (2010) · Journal of Lipid Research · doi:10.1194/jlr.m012476 · Cited by 10
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Lv, Q., Jiao, X., Yu, H., Sun, Q., Fan, L., Wang, Y., Sun, H., Du, Z., Li, L., Hu, C., et al. (2022) · Journal of the American Heart Association · doi:10.1161/jaha.122.025955 · Cited by 8
Gui, Y., Duan, Z., Qiu, X., Tang, W., Gober, H.-J., Li, D., & Wang, L. (2016) · BioScience Trends · doi:10.5582/bst.2016.01006 · Cited by 8
Structure and Function of the Lipolysis Stimulated Lipoprotein Receptor
Stenger, C., Corbier, C., & Frances, T. (2012) · InTech eBooks · doi:10.5772/34657 · Cited by 14
Wakita, K., Morita, S., Okamoto, N., Takata, E., Handa, T., & Nakano, M. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2015.01.015 · Cited by 6
Tada, H., Kawashiri, M., Nohara, A., Inazu, A., Mabuchi, H., Yamagishi, M., & Hayashi, K. (2015) · Practical Laboratory Medicine · doi:10.1016/j.plabm.2015.03.001 · Cited by 6
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Jacobs, F., Craeyveld, E. V., Feng, Y., & Geest, B. D. (2009) · Cardiovascular Pathology · doi:10.1016/j.carpath.2009.09.002 · Cited by 5
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[Atherogenic lipoprotein remnants in humans].
Wikinski, R. L. W., Schreier, L. E., Berg, G. A., Brites, F. D., Lopez, G. I., González, A. I., & Zago, V. (2010) · PubMed · Cited by 3
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Olivieri, P. H., Hayashi, J. Y., Torquato, R. J. S., Lima, A. F., Pereira, T. P., Lima, I. F., Fonseca, F. L. A., Iwai, L. K., Nader, H. B., Tashima, A. K., et al. (2025) · ACS Nano · doi:10.1021/acsnano.5c19714 · Cited by 2
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Charrière, S., Moulin, P., métaboliques, N. E. D. R. R., & Sciences-Santé, É. D. I. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique)
(2008) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328303e27e
Matsuura, H., Akahane, S., Kaido, T., Kamijo, T., Sakamoto, K., & Yamauchi, K. (2023) · Research Square · doi:10.21203/rs.3.rs-3292146/v1
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Metadata
- Authors
- Mahley, R. W., & Huang, Y.
- Affiliations
- Gladstone Institutes (US)
- Corresponding author
- Mahley, Robert W.
- Venue
- Journal of Clinical Investigation
- Published
- 2007-01-02
- Volume
- 117
- Issue
- 1
- Pages
- 1-5
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC1716223
- OpenAlex
- W2047465218
- Cited by
- 159
- References
- 43
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 5 · 2023: 6 · 2022: 4 · 2021: 8 · 2020: 7 · 2019: 6 · 2018: 5 · 2017: 4 · 2016: 10 · 2015: 5 · 2014: 12 · 2013: 12 · 2012: 12
- FWCI
- 12.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
- Keywords
- remnant lipoproteins, heparan sulfate proteoglycans, lipoprotein clearance, apolipoprotein E, LDL receptor, VLDL remnants, chylomicron remnants, autosomal recessive hypercholesterolemia, hepatocyte uptake, atherosclerosis
- MeSH terms
- Biological Transport, Humans, Lipoproteins, Liver, Models, Biological, Proteoglycans, Receptors, LDL, Triglycerides, Heparan Sulfate Proteoglycans, Atherosclerosis
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