Cited by 46Proteoglycans and glycosaminoglycans researchCholesterol and Lipid MetabolismLipoproteins and Cardiovascular Health

The DOI matches its Crossref record; 41 of the 41 references it cites were found in a registry or an index.

Glycosaminoglycan-lipoprotein interaction

Olsson, Urban, Östergren-Lundén, Gunnel, Moses, Jonatan·2001·Glycoconjugate Journal

DOI 10.1023/a:1021155518464

Open this paper in CoChat — free account

Abstract

Glycosaminoglycans (GAGs) bound to various proteoglycans (PGs) present in the cardiovascular system have been proposed to perform a wide range of functions. These include conferring viscoelastic properties; interacting with and modulating growth factors and enzymes; and as receptors and co-receptors in lipoprotein metabolism. Binding of apoB-100 lipoproteins, particularly low density lipoproteins (LDL), to GAGs of extracellular matrix PGs in arteries has been proposed to be an initiating event in development of atherosclerosis. This study was initiated with the aim of getting an overview of the binding patterns of different lipoprotein subclasses with individual GAG categories. We thus evaluated the interaction of lipoproteins with GAGs commonly found in the cardiovascular system using a gel mobility-shift assay developed for this purpose. The same procedure was used to measure lipoproteins binding to metabolically [(35)S]-labeled whole PGs prepared from three cell types, arterial smooth muscle cells, THP-1 macrophages and from HepG2 cells. The effect of GAG composition on PGs on lipoprotein binding was evaluated by enzymatic degradation of the carbohydrate chains. Heparan sulfate was found to bind beta very low density lipoproteins (beta-VLDL) and a chylomicron remnant model (beta-VLDL+apoE), but not LDL. Dermatan sulfate was found to bind LDL, but not beta-VLDL or the chylomicron remnant model. Chondroitin sulfate and heparin were found to bind all lipoproteins tested (LDL, beta-VLDL and beta-VLDL+apoE) although with different affinities. We can conclude that each lipoprotein subclass tested binds a specific assortment of the GAGs tested. The observations made contribute to the understanding of new and complex mechanisms by which carbohydrate and lipid metabolism may be linked.

Integrity signals

Registry

Crossref · 10.1023/a:1021155518464

Cites

41 of 41 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Negative regulation of transforming growth factor-β by the proteoglycan decorin
Yamaguchi, Y., Mann, D. M., & Ruoslahti, E. (1990) · Nature · doi:10.1038/346281a0 · Cited by 1,516
Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes
Jackson, R. L., Busch, S. J., & Cardin, A. D. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.2.481 · Cited by 1,104
Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E
Mahley, R. W., & Ji, Z.-S. (1999) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)33334-4 · Cited by 693
Synthesis and sorting of proteoglycans
Prydz, K., & Dalen, K. T. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.2.193 · Cited by 481
The Interaction between Human Plasma Lipoproteins and Connective Tissue Glycosaminoglycans
Iverius, P. (1972) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)45469-0 · Cited by 462
Hep G2 cells as a resource for metabolic studies: lipoprotein, cholesterol, and bile acids
Javitt, N. B. (1990) · The FASEB Journal · doi:10.1096/fasebj.4.2.2153592 · Cited by 357
The Relationship Between Plasma and Tissue Lipids in Human Atherosclerosis
Smith, E. B. (1974) · Advances in lipid research · doi:10.1016/b978-0-12-024912-1.50008-9 · Cited by 355
Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding.
Borén, J., Olin, K., Lee, I., Chait, A., Wight, T. N., & Innerarity, T. L. (1998) · Journal of Clinical Investigation · doi:10.1172/jci2265 · Cited by 331
Role of the glucosamine pathway in fat-induced insulin resistance.
Hawkins, M. A., Barzilai, N., Liu, R., Hu, M., Chen, W., & Rossetti, L. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119390 · Cited by 323
Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells
Ji, Z. S., Brecht, W. J., Miranda, R. D., Hussain, M. M., Innerarity, T. L., & Mahley, R. W. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)82186-x · Cited by 305

Show all 41 references

Research works printed but not linked: 1

Wight TN, The Vascular Extracellular Matrix (Lippincott Raven, Philadelphia, PA, 1996).

Glycosaminoglycans and Glycosaminoglycan Mimetics in Cancer and Inflammation
Morla, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20081963 · Cited by 227
The heparanome and regulation of cell function: structures, functions and challenges
Ori‬‬, A. (2008) · Frontiers in bioscience · doi:10.2741/3007 · Cited by 185
A role for proteoglycans in vascular disease
Wight, T. N. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.02.019 · Cited by 171
Extracellular matrix dynamics in vascular remodeling
Ma, Z., Mao, C., Jia, Y., Fu, Y., & Kong, W. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00147.2020 · Cited by 129
Regulation of glycosaminoglycan structure and atherogenesis
Ballinger, M. L., Nigro, J., Frontanilla, K. V., Dart, A. M., & Little, P. J. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-3389-4 · Cited by 89
Food and Western Disease: Health and Nutrition from an Evolutionary Perspective
Lindeberg, S. (2009) · Wiley eBooks · doi:10.1002/9781444317176 · Cited by 76
Receptor-mediated mechanisms in ovarian follicle and oocyte development
Schneider, W. J. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2008.11.032 · Cited by 76
Antigen-Induced Immunomodulation in the Pathogenesis of Atherosclerosis
Milioti, N., Bermúdez-Fajardo, A., Penichet, M. L., & Oviedo‐Orta, E. (2008) · Clinical and Developmental Immunology · doi:10.1155/2008/723539 · Cited by 62
Reactive oxygen species mediate high glucose-induced heparanase-1 production and heparan sulphate proteoglycan degradation in human and rat endothelial cells: a potential role in the pathogenesis of atherosclerosis
Rao, G., Ding, H. G., Huang, W. C., Le, D., Maxhimer, J. B., Oosterhof, A., Kuppevelt, T. H. V., Lum, H., Lewis, E. J., Reddy, V. K., et al. (2011) · Diabetologia · doi:10.1007/s00125-011-2110-z · Cited by 60
Improving the Purity of Extracellular Vesicles by Removal of Lipoproteins from Size Exclusion Chromatography- and Ultracentrifugation-Processed Samples Using Glycosaminoglycan-Functionalized Magnetic Beads
Chou, C.-Y., Chiang, P.-C., Li, C.-C., Chang, J.-W., Lu, P.-H., Hsu, W.-F., Chang, L.-C., Hsu, J., Wu, M., & Wo, A. M. (2024) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.4c03869 · Cited by 57
Thrombin regulates vascular smooth muscle cell proteoglycan synthesis via PAR-1 and multiple downstream signalling pathways
Ivey, M. E., & Little, P. J. (2008) · Thrombosis Research · doi:10.1016/j.thromres.2008.04.019 · Cited by 56
Role of the N- and C-Terminal Domains in Binding of Apolipoprotein E Isoforms to Heparan Sulfate and Dermatan Sulfate: A Surface Plasmon Resonance Study
Yamauchi, Y., Deguchi, N., Takagi, C., Tanaka, M., Dhanasekaran, P., Nakano, M., Handa, T., Phillips, M. C., Lund-Katz, S., & Saito, H. (2008) · Biochemistry · doi:10.1021/bi8003999 · Cited by 53
Nanoscale anionic macromolecules for selective retention of low-density lipoproteins
Chnari, E., Lari, H. B., Tian, L., Uhrich, K. E., & Moghe, P. V. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2004.09.038 · Cited by 47
Lipid composition of circulating multiple-modified low density lipoprotein
Zakiev, E., Sukhorukov, V. N., Melnichenko, A. А., Sobenin, I. A., Ivanova, E. A., & Orekhov, A. N. (2016) · Lipids in Health and Disease · doi:10.1186/s12944-016-0308-2 · Cited by 46
High binding affinity of electronegative LDL to human aortic proteoglycans depends on its aggregation level
Bancells, C., Benítez, S., Jauhiainen, M., Ordóñez‐Llanos, J., Kovanen, P. T., Villegas, S., Sánchez‐Quesada, J. L., & Öörni, K. (2008) · Journal of Lipid Research · doi:10.1194/jlr.m800318-jlr200 · Cited by 44
Effects of mechanical ventilation on the interstitial extracellular matrix in healthy lungs and lungs affected by acute respiratory distress syndrome: a narrative review
Al-Husinat, L., Azzam, S., Sharie, S. A., Sharie, A. H. A., Battaglini, D., Robba, C., Marini, J. J., Thornton, L. T., Cruz, F. F., Silva, P. L., et al. (2024) · Critical Care · doi:10.1186/s13054-024-04942-y · Cited by 37
Intestinal lipid transport and chylomicron production: Possible links to exacerbated atherogenesis in a rodent model of the metabolic syndrome
Vine, D. F., Glimm, D. R., & Proctor, S. D. (2008) · Atherosclerosis Supplements · doi:10.1016/j.atherosclerosissup.2008.05.004 · Cited by 36
Nanoscale amphiphilic macromolecules as lipoprotein inhibitors: the role of charge and architecture.
Wang, J., Plourde, N. M., Iverson, N. M., Moghe, P. V., & Uhrich, K. E. (2007) · PubMed · doi:10.2147/ijn.s2.4.697 · Cited by 33
Electronegative LDL induces MMP-9 and TIMP-1 release in monocytes through CD14 activation: Inhibitory effect of glycosaminoglycan sulodexide
Ligi, D., Benítez, S., Croce, L., Rivas-Urbina, A., Puig, N., Ordóñez‐Llanos, J., Mannello, F., & Sánchez‐Quesada, J. L. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.09.022 · Cited by 26
Macrophages bind LDL using heparan sulfate and the perlecan protein core
Ng, C., Whitelock, J. M., Williams, H., Kim, H. N., Medbury, H. J., & Lord, M. S. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100520 · Cited by 27
Rapid affinity chromatographic isolation method for LDL in human plasma by immobilized chondroitin-6-sulfate and anti-apoB-100 antibody monolithic disks in tandem
Liangsupree, T., Multia, E., Metso, J., Jauhiainen, M., Forssén, P., Fornstedt, T., Öörni, K., Podgornik, A., & Riekkola, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-47750-z · Cited by 22
Wild blueberry (V. angustifolium)-enriched diets alter aortic glycosaminoglycan profile in the spontaneously hypertensive rat
Kristo, A. S., Malavaki, C. J., Lamari, F. N., Karamanos, N. K., & Klimis‐Zacas, D. J. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2011.05.002 · Cited by 18
A discoidal lipoprotein from the coelomic fluid of the polychaete Nereis virens
Schenk, S., Harris, J. R., & Hoeger, U. (2005) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2005.11.012 · Cited by 14
High-fat/high-cholesterol diet promotes a S1P receptor-mediated antiapoptotic activity for VLDL
Mihovilovic, M., Robinette, J. B., DeKroon, R. M., Sullivan, P. M., & Strittmatter, W. J. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m600201-jlr200 · Cited by 12
Carbohydrate composition of circulating multiple-modified low-density lipoprotein
Zakiev, E., Sobenin, I. A., Sukhorukov, V. N., Myasoedova, V. A., Ivanova, E. A., & Orekhov, A. N. (2016) · Vascular Health and Risk Management · doi:10.2147/vhrm.s112948 · Cited by 12
Breaking Bruch's: How changes in Bruch's membrane influence retinal homeostasis
Clark, S. J., Curcio, C. A., Dick, A. D., Doyle, S., Edwards, M. M., Flores‐Bellver, M., Hass, D. T., Lennon, R., Toomey, C. B., & Rohrer, B. (2025) · Experimental Eye Research · doi:10.1016/j.exer.2025.110343 · Cited by 11
Identification of a Novel Chondroitin-sulfated Collagen in the Membrane Separating Theca and Granulosa Cells in Chicken Ovarian Follicles
Hummel, S., Christian, S., Osanger, A., Heid, H., Nimpf, J., & Schneider, W. J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m606029200 · Cited by 11
Bruch’s membrane heparan sulfate retains lipoproteins in the early stages of age-related macular degeneration
Toomey, C. B., Pflugmacher, S., Park, K., Pihl, J., Novak, S. W., Rodriguez, J. W., Jalali, M., Jung, J., Mozafari, M., Omran, S. P., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2500727122 · Cited by 11
Perlecan: An Extracellular Matrix Heparan Sulfate Proteoglycan that Regulates Key Events in Vascular Development and Disease
Kinsella, M. G., & Wight, T. N. (2005) · Elsevier eBooks · doi:10.1016/b978-008044859-6/50023-x · Cited by 9
Monoclonal Antibody chP3R99 Reduces Subendothelial Retention of Atherogenic Lipoproteins in Insulin‐Resistant Rats: Acute Treatment Versus Long‐Term Protection as an Idiotypic Vaccine for Atherosclerosis
Soto, Y., Hernández, A., Sarduy, R., Navarro, V. B., Marleau, S., Vine, D. F., Vázquez, A. M., & Proctor, S. D. (2024) · Journal of the American Heart Association · doi:10.1161/jaha.123.032419 · Cited by 5
Role of chondroitin sulphate in the uptake of β‐VLDL by brain cells
Rapp, A., & Hüttinger, M. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04313.x · Cited by 4
GPR182 is a lipoprotein receptor for dietary fat absorption
Sun, Z., Torphy, R. J., Miller, E. N., Darehshouri, A., Vigil, I., Terai, T., Eck, E., Sun, Y., Guo, Y., Fykstra, D. P., et al. (2026) · Journal of Clinical Investigation · doi:10.1172/jci200857 · Cited by 4
Physiological, Pathophysiological and Therapeutic Roles of Heparin and Heparan Sulfate
Xie, J., Murugesan, S., & Linhardt, R. J. (2008) · Elsevier eBooks · doi:10.1016/b978-0-08-054816-6.00010-0 · Cited by 4
Enhanced delivery of low-density lipoprotein-based nanoparticles to the mouse glioblastoma using focused ultrasound as a novel therapy
Brambila, C. J., Vaighan, N. S., Youssef, I., Chaudhary, J., Anwar, A., Bachoo, R. M., Patel, T., Chopra, R., & Corbin, I. R. (2026) · Biomaterials · doi:10.1016/j.biomaterials.2026.124198 · Cited by 2
Wild Blueberries (Vaccinium angustifolium): Modulators of Vascular Function, Structure, and Metabolism
Klimis‐Zacas, D. J., & Kristo, A. S. (2012) · ACS symposium series · doi:10.1021/bk-2012-1093.ch009 · Cited by 2
Analysis of Apolipoprotein B Protein of Circulating Multiple-Modified Low-Density Lipoprotein
Zakiev, E., Sukhorukov, V. N., Ivanova, E. A., & Orekhov, A. N. (2016) · International Journal of Angiology · doi:10.1055/s-0036-1588062 · Cited by 2
Seasonality of Atherosclerotic Cardiovascular Disease: Role of Natural and Anthropogenic Factors
Churilov, L. P., Gurevich, V. S., Садовников, П. С., Soprun, L. A., & Stroev, Y. I. (2024) · Advances in biochemistry in health and disease · doi:10.1007/978-3-031-62806-1_3 · Cited by 1
Dual Receptor Targeting Ensures Uptake and Anticancer Efficacy of Low-Density Lipoprotein-Docosahexaenoic Acid Nanoparticles Across Breast Cancer Cell Subtypes
Bower, J., Anwar, A., Chaudhary, J., Chen, Z., Schumacher, M. M., DeBose‐Boyd, R. A., & Corbin, I. R. (2025) · Breast Cancer Targets and Therapy · doi:10.2147/bctt.s554396 · Cited by 1
N-Unsubstituted Glucosamine Residues in Heparan Sulfate and Their Potential Relation to Alzheimer's Disease
Westling, C. (2003) · Uppsala University Publications (Uppsala University) · Cited by 1
An investigation of the atherogenicity of intermediate density lipoprotein in people with and without type 2 diabetes mellitus
Cheung, C.-L. (2009) · Research Online (University of Wollongong)
New insights in platelet signaling by Low Density Lipoprotein
Relou, I. A. M. (2003) · Utrecht University Repository (Utrecht University)
The perlecan LDL-binding receptor needs sugar: Implication of perlecan core protein interaction with LDL for atherosclerosis
(2015) · Receptors & Clinical Investigation · doi:10.14800/rci.867
Multifunctional polymers for inhibition of oxidized lipoprotein accumulation and inflammation in macrophage cells
Iverson, N. M. (2010) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t3fn1684
References
(2009) · Wiley eBooks · doi:10.1002/9781444317176.refs
Characterization of inflammation in coronary artery disease
Cheng, W. H. (2026) · cIRcle (University of British Columbia) · doi:10.14288/1.0451760
The Influence of Lipid Composition on the Binding of LDL to Chondroitin 6-Sulphate
Espiritu, W. (2005) · VCU Scholars Compass (Virginia Commonwealth University) · doi:10.25772/fsqb-w390

Authors: Olsson, U., Östergren-Lundén, G., & Moses, J.
Affiliations: Sahlgrenska University Hospital (SE)
Corresponding author: Olsson, Urban
Venue: Glycoconjugate Journal
Publisher: Springer Science and Business Media LLC
Published: 2001-10
Volume: 18
Issue: 10
Pages: 789-797
ISSN: 0282-0080 (ISSN-L)
1573-4986
DOI: 10.1023/a:1021155518464
OpenAlex: W1760442572
Cited by: 46
References: 41
Citations by year: 2026: 1 · 2025: 4 · 2024: 4 · 2023: 1 · 2021: 1 · 2020: 1 · 2019: 2 · 2018: 2 · 2016: 3 · 2015: 1 · 2012: 1
FWCI: 0.45
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Glycoconjugate Journal (publishedVersion)
PubMed (publishedVersion)
Funders: AstraZeneca
Vetenskapsrådet
Magnus Bergvalls Stiftelse
Socialstyrelsen
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
Keywords: lipoprotein binding, heparan sulfate, dermatan sulfate, chondroitin sulfate, heparin, low-density lipoprotein, beta-VLDL, chylomicron remnants, apolipoprotein E, proteoglycans, atherosclerosis, lipoprotein metabolism, carbohydrate metabolism
MeSH terms: Autoradiography, Cardiovascular System, Glycosaminoglycans, Humans, Lipoproteins, Models, Biological, Protein Binding, Recombinant Proteins, Substrate Specificity, Sulfur Radioisotopes, Tumor Cells, Cultured, Electrophoretic Mobility Shift Assay

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.

Glycosaminoglycan-lipoprotein interaction

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks

Data sources