Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions

Öörni, Katariina; Pentikäinen, Markku O.; Ala-Korpela, Mika; Kovanen, Petri T.

doi:10.1016/s0022-2275(20)31964-7

Cited by 252Atherosclerosis and Cardiovascular DiseasesCholesterol and Lipid MetabolismLipoproteins and Cardiovascular Health

Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions

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Öörni, Katariina, Pentikäinen, Markku O., Ala-Korpela, Mika, Kovanen, Petri T.·2000·Journal of Lipid Research

DOI 10.1016/s0022-2275(20)31964-7

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Abstract

Initiation of atherosclerosis is characterized by accumulation of aggregates of small lipid droplets and vesicles in the extracellular matrix of the arterial intima. The droplets and vesicles have features that suggest that they are formed from modified plasma-derived low density lipoprotein (LDL) particles. A variety of hydrolytic enzymes and prooxidative agents that could lead to extracellular assembly of LDL-derived droplets and vesicles are present in the arterial intima. In fact, in vitro studies have demonstrated that extensive oxidation of LDL and treatment of LDL with either proteolytic or lipolytic enzymes will induce LDL aggregation and fusion and treatment of LDL with cholesterol esterase will cause formation of vesicles. Fusion of LDL particles proceeds faster in vitro when they are bound to components of the extracellular matrix derived from the arterial intima, such as proteoglycans, and, depending on the type of modification, the strength of binding of modified LDL to the matrix components may either increase or decrease. In the present article, we discuss molecular mechanisms that provide clues as to how aggregated lipid droplets and vesicles may be derived from modified LDL particles. We also describe how these modified forms of LDL, by means of their trapping to the extracellular matrix, may lead to extracellular lipid accumulation in the arterial intima.

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Retained lipoproteins bound to the arterial intima extracellular matrix are susceptible to modification by intimal oxidizing agents, proteases, and lipases.
“The retained lipoproteins (that is, those bound to the extracellular matrix of the arterial intima) are susceptible to modification by intimal oxidizing agents, proteases and lipases43,46,47.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [46]
Oxidative, proteolytic, and lipolytic modifications induce LDL aggregation, and LDL aggregation susceptibility is associated with risk of cardiovascular death.
“Oxidative, proteolytic and lipolytic modifications induce LDL aggregation46, and the aggregation susceptibility of LDL was shown to be associated with the risk of cardiovascular death55.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [46]

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Subendothelial Lipoprotein Retention as the Initiating Process in Atherosclerosis: Update and Therapeutic Implications
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Identification of Immune Responses Against Aldehyde-Modified Peptide Sequences in ApoB Associated With Cardiovascular Disease
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Prevention of atherosclerosis from childhood
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Reactive Oxygen Species and Thiol Redox Signaling in the Macrophage Biology of Atherosclerosis
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Modified Lipoproteins Induce Arterial Wall Inflammation During Atherogenesis
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Macrophage-specific expression of group IIA sPLA2 results in accelerated atherogenesis by increasing oxidative stress
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Elevated Cholesterol Levels in the Plasma Membranes of Macrophages Inhibit Migration by Disrupting RhoA Regulation
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Lysosomal oxidation of LDL alters lysosomal pH, induces senescence, and increases secretion of pro-inflammatory cytokines in human macrophages
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Cathepsin G activity lowers plasma LDL and reduces atherosclerosis
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Modulation of Autoimmunity and Atherosclerosis – Common Targets and Promising Translational Approaches Against Disease –
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Protein damage in diabetes and uremia—identifying hotspots of proteome damage where minimal modification is amplified to marked pathophysiological effect
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Low Density Lipoprotein Aged in Plasma Forms Clusters Resembling Subendothelial Droplets: Aggregation via Surface Sites
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Selective regulation of macrophage lipid metabolism via nanomaterials’ surface chemistry
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Dietary fat quality, plasma atherogenic lipoproteins, and atherosclerotic cardiovascular disease: An overview of the rationale for dietary recommendations for fat intake
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Aggregation and fusion of low-density lipoproteins in vivo and in vitro
Lu, M., & Gursky, O. (2013) · BioMolecular Concepts · doi:10.1515/bmc-2013-0016 · Cited by 68 · see citing works
Aggregation and fusion of modified low density lipoprotein
Pentikäinen, M. O., Lehtonen-Smeds, E. M. P., & Kovanen, P. T. (1996) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37467-8 · Cited by 96 · see citing works
Self-citation
Altered ultrastructural morphology of self-aggregated low density lipoproteins: coalescence of lipid domains forming droplets and vesicles.
Guyton, J., Klemp, K. F., & Mims, M. (1991) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)41992-3 · Cited by 67 · see citing works
Sphingomyelinase Induces Aggregation and Fusion, but Phospholipase A2 Only Aggregation, of Low Density Lipoprotein (LDL) Particles
Öörni, K., Hakala, J. K., Annila, A., Ala‐Korpela, M., & Kovanen, P. T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.29127 · Cited by 137 · see citing works
Self-citation
Lipolysis of LDL by Human Secretory Phospholipase A 2 Induces Particle Fusion and Enhances the Retention of LDL to Human Aortic Proteoglycans
Hakala, J. K., Öörni, K., Pentikäinen, M. O., Hurt‐Camejo, E., & Kovanen, P. T. (2001) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.21.6.1053 · Cited by 111 · see citing works
Self-citation

Authors: Öörni, K., Pentikäinen, M. O., Ala-Korpela, M., & Kovanen, P. T.
Affiliations: Wihuri Research Institute (FI)
Corresponding author: Kovanen, Petri T.
ORCID: Öörni, Katariina
Pentikäinen, Markku O.
Kovanen, Petri T.
Venue: Journal of Lipid Research
Publisher: Elsevier BV
Published: 2000-11
Volume: 41
Issue: 11
Pages: 1703-1714
ISSN: 0022-2275 (ISSN-L)
DOI: 10.1016/s0022-2275(20)31964-7
OpenAlex: W1853133898
Cited by: 252
References: 148
Citations by year: 2026: 2 · 2025: 9 · 2024: 4 · 2023: 5 · 2022: 6 · 2021: 13 · 2020: 9 · 2019: 8 · 2018: 11 · 2017: 4 · 2016: 5 · 2015: 8 · 2014: 12 · 2013: 8 · 2012: 21
FWCI: 2.48
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 7234 d)
Locations: Journal of Lipid Research (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Keywords: modified low-density lipoprotein, LDL oxidation, lipoprotein aggregation, vesicle formation, lipid droplets, atherosclerosis initiation, extracellular matrix, proteoglycans, cholesterol esterase, lipolytic enzymes, proteolytic enzymes, arterial intima
MeSH terms: Animals, Arteries, Arteriosclerosis, Chemistry, Physical, Extracellular Matrix, Humans, Lipolysis, Lipoproteins, LDL, Liposomes, Endopeptidases, Proteoglycans, Chemical Phenomena

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Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions

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