Blood Lipoproteins Shape the Phenotype and Lipid Content of Early Atherosclerotic Lesion Macrophages: A Dual-Structured Mathematical Model

Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes . The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balan...

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Veröffentlicht in:	Bulletin of mathematical biology Jg. 86; H. 9; S. 112
Hauptverfasser:	Chambers, Keith L., Myerscough, Mary R., Watson, Michael G., Byrne, Helen M.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	New York Springer US 01.09.2024 Springer Nature B.V
Schlagworte:	Arteriosclerosis Atherosclerosis Atherosclerosis - blood Atherosclerosis - metabolism Atherosclerosis - pathology Blood Cell Biology Cholesterol Computer Simulation Cytokines Density Gene sequencing Genotype & phenotype Heterogeneity High density lipoprotein Humans Immunology Inflammation Lesions Life Sciences Lipid Metabolism Lipids Lipoproteins Lipoproteins - blood Lipoproteins - metabolism Lipoproteins, HDL - blood Lipoproteins, HDL - metabolism Lipoproteins, LDL - blood Lipoproteins, LDL - metabolism Low density lipoprotein Macrophages Macrophages - metabolism Macrophages - pathology Mathematical and Computational Biology Mathematical Concepts Mathematical models Mathematics Mathematics and Statistics Models, Cardiovascular Monocytes Original Original Article Phenotype Phenotypes Subsystems Veins & arteries Continuum Phenotype Discrete Lipid Structured population model Atherosclerosis
ISSN:	0092-8240, 1522-9602, 1522-9602
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Abstract	Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes . The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balance between low density lipoproteins (LDL) and high density lipoproteins (HDL), which carry bad and good cholesterol respectively. To address these issues, we have developed a mathematical model for early atherosclerosis in which the MDM population is structured by phenotype and lipid content. The model admits a simpler, closed subsystem whose analysis shows how lesion composition becomes more pathological as the blood density of LDL increases relative to the HDL capacity. We use asymptotic analysis to derive a power-law relationship between MDM phenotype and lipid content at steady-state. This relationship enables us to understand why, for example, lipid-laden MDMs have a more inflammatory phenotype than lipid-poor MDMs when blood LDL lipid density greatly exceeds HDL capacity. We show further that the MDM phenotype distribution always attains a local maximum, while the lipid content distribution may be unimodal, adopt a quasi-uniform profile or decrease monotonically. Pathological lesions exhibit a local maximum in both the phenotype and lipid content MDM distributions, with the maximum at an inflammatory phenotype and near the lipid content capacity respectively. These results illustrate how macrophage heterogeneity arises in early atherosclerosis and provide a framework for future model validation through comparison with single-cell RNA sequencing data.
AbstractList	Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes . The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balance between low density lipoproteins (LDL) and high density lipoproteins (HDL), which carry bad and good cholesterol respectively. To address these issues, we have developed a mathematical model for early atherosclerosis in which the MDM population is structured by phenotype and lipid content. The model admits a simpler, closed subsystem whose analysis shows how lesion composition becomes more pathological as the blood density of LDL increases relative to the HDL capacity. We use asymptotic analysis to derive a power-law relationship between MDM phenotype and lipid content at steady-state. This relationship enables us to understand why, for example, lipid-laden MDMs have a more inflammatory phenotype than lipid-poor MDMs when blood LDL lipid density greatly exceeds HDL capacity. We show further that the MDM phenotype distribution always attains a local maximum, while the lipid content distribution may be unimodal, adopt a quasi-uniform profile or decrease monotonically. Pathological lesions exhibit a local maximum in both the phenotype and lipid content MDM distributions, with the maximum at an inflammatory phenotype and near the lipid content capacity respectively. These results illustrate how macrophage heterogeneity arises in early atherosclerosis and provide a framework for future model validation through comparison with single-cell RNA sequencing data. Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes. The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balance between low density lipoproteins (LDL) and high density lipoproteins (HDL), which carry bad and good cholesterol respectively. To address these issues, we have developed a mathematical model for early atherosclerosis in which the MDM population is structured by phenotype and lipid content. The model admits a simpler, closed subsystem whose analysis shows how lesion composition becomes more pathological as the blood density of LDL increases relative to the HDL capacity. We use asymptotic analysis to derive a power-law relationship between MDM phenotype and lipid content at steady-state. This relationship enables us to understand why, for example, lipid-laden MDMs have a more inflammatory phenotype than lipid-poor MDMs when blood LDL lipid density greatly exceeds HDL capacity. We show further that the MDM phenotype distribution always attains a local maximum, while the lipid content distribution may be unimodal, adopt a quasi-uniform profile or decrease monotonically. Pathological lesions exhibit a local maximum in both the phenotype and lipid content MDM distributions, with the maximum at an inflammatory phenotype and near the lipid content capacity respectively. These results illustrate how macrophage heterogeneity arises in early atherosclerosis and provide a framework for future model validation through comparison with single-cell RNA sequencing data. Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes. The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balance between low density lipoproteins (LDL) and high density lipoproteins (HDL), which carry bad and good cholesterol respectively. To address these issues, we have developed a mathematical model for early atherosclerosis in which the MDM population is structured by phenotype and lipid content. The model admits a simpler, closed subsystem whose analysis shows how lesion composition becomes more pathological as the blood density of LDL increases relative to the HDL capacity. We use asymptotic analysis to derive a power-law relationship between MDM phenotype and lipid content at steady-state. This relationship enables us to understand why, for example, lipid-laden MDMs have a more inflammatory phenotype than lipid-poor MDMs when blood LDL lipid density greatly exceeds HDL capacity. We show further that the MDM phenotype distribution always attains a local maximum, while the lipid content distribution may be unimodal, adopt a quasi-uniform profile or decrease monotonically. Pathological lesions exhibit a local maximum in both the phenotype and lipid content MDM distributions, with the maximum at an inflammatory phenotype and near the lipid content capacity respectively. These results illustrate how macrophage heterogeneity arises in early atherosclerosis and provide a framework for future model validation through comparison with single-cell RNA sequencing data.Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes. The phenotypic distribution of monocyte-derived macrophages (MDMs), its correlation with MDM lipid content, and relation to blood lipoprotein densities are not well understood. Of particular interest is the balance between low density lipoproteins (LDL) and high density lipoproteins (HDL), which carry bad and good cholesterol respectively. To address these issues, we have developed a mathematical model for early atherosclerosis in which the MDM population is structured by phenotype and lipid content. The model admits a simpler, closed subsystem whose analysis shows how lesion composition becomes more pathological as the blood density of LDL increases relative to the HDL capacity. We use asymptotic analysis to derive a power-law relationship between MDM phenotype and lipid content at steady-state. This relationship enables us to understand why, for example, lipid-laden MDMs have a more inflammatory phenotype than lipid-poor MDMs when blood LDL lipid density greatly exceeds HDL capacity. We show further that the MDM phenotype distribution always attains a local maximum, while the lipid content distribution may be unimodal, adopt a quasi-uniform profile or decrease monotonically. Pathological lesions exhibit a local maximum in both the phenotype and lipid content MDM distributions, with the maximum at an inflammatory phenotype and near the lipid content capacity respectively. These results illustrate how macrophage heterogeneity arises in early atherosclerosis and provide a framework for future model validation through comparison with single-cell RNA sequencing data.
ArticleNumber	112
Author	Watson, Michael G. Chambers, Keith L. Myerscough, Mary R. Byrne, Helen M.
Author_xml	– sequence: 1 givenname: Keith L. orcidid: 0000-0001-6878-8007 surname: Chambers fullname: Chambers, Keith L. email: keith.chambers@maths.ox.ac.uk organization: Wolfson Centre for Mathematical Biology, Mathematical Institute, University of Oxford – sequence: 2 givenname: Mary R. surname: Myerscough fullname: Myerscough, Mary R. organization: School of Mathematics and Statistics, University of Sydney – sequence: 3 givenname: Michael G. surname: Watson fullname: Watson, Michael G. organization: School of Mathematics and Statistics, University of New South Wales – sequence: 4 givenname: Helen M. surname: Byrne fullname: Byrne, Helen M. organization: Wolfson Centre for Mathematical Biology, Mathematical Institute, University of Oxford, Ludwig Institute for Cancer Research, University of Oxford
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/39093509$$D View this record in MEDLINE/PubMed
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Keywords	Continuum Phenotype Discrete Lipid Structured population model Atherosclerosis
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Snippet	Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes . The phenotypic distribution of monocyte-derived macrophages (MDMs), its... Macrophages in atherosclerotic lesions exhibit a spectrum of behaviours or phenotypes. The phenotypic distribution of monocyte-derived macrophages (MDMs), its...
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SubjectTerms	Arteriosclerosis Atherosclerosis Atherosclerosis - blood Atherosclerosis - metabolism Atherosclerosis - pathology Blood Cell Biology Cholesterol Computer Simulation Cytokines Density Gene sequencing Genotype & phenotype Heterogeneity High density lipoprotein Humans Immunology Inflammation Lesions Life Sciences Lipid Metabolism Lipids Lipoproteins Lipoproteins - blood Lipoproteins - metabolism Lipoproteins, HDL - blood Lipoproteins, HDL - metabolism Lipoproteins, LDL - blood Lipoproteins, LDL - metabolism Low density lipoprotein Macrophages Macrophages - metabolism Macrophages - pathology Mathematical and Computational Biology Mathematical Concepts Mathematical models Mathematics Mathematics and Statistics Models, Cardiovascular Monocytes Original Original Article Phenotype Phenotypes Subsystems Veins & arteries
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Title	Blood Lipoproteins Shape the Phenotype and Lipid Content of Early Atherosclerotic Lesion Macrophages: A Dual-Structured Mathematical Model
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