Divergence of acetate uptake in proinflammatory and inflammation-resolving macrophages: implications for imaging atherosclerosis
Metabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 (11C)-labeled acetate is a clinically available tracer which accumulat...
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| Published in: | Journal of nuclear cardiology Vol. 29; no. 3; pp. 1266 - 1276 |
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| Abstract | Metabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 (11C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined.
Histological correlates of 14C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE−/− mice. The effect of polarizing stimuli on 14C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. 14C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low 14C-acetate uptake. 14C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline (P < .001). A delayed increase in 14C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% (P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased 14C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased 14C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques (P < .05).
Acetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. |
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| AbstractList | BACKGROUNDMetabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 (11C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined.METHODS AND RESULTSHistological correlates of 14C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE-/- mice. The effect of polarizing stimuli on 14C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. 14C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low 14C-acetate uptake. 14C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline (P < .001). A delayed increase in 14C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% (P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased 14C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased 14C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques (P < .05).CONCLUSIONSAcetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. BackgroundMetabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 (11C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined.Methods and resultsHistological correlates of 14C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE−/− mice. The effect of polarizing stimuli on 14C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. 14C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low 14C-acetate uptake. 14C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline (P < .001). A delayed increase in 14C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% (P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased 14C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased 14C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques (P < .05).ConclusionsAcetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. Background Metabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 ( 11 C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined. Methods and results Histological correlates of 14 C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE −/− mice. The effect of polarizing stimuli on 14 C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. 14 C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low 14 C-acetate uptake. 14 C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline ( P < .001). A delayed increase in 14 C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% ( P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased 14 C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased 14 C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques ( P < .05). Conclusions Acetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. Metabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 (11C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined. Histological correlates of 14C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE−/− mice. The effect of polarizing stimuli on 14C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. 14C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low 14C-acetate uptake. 14C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline (P < .001). A delayed increase in 14C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% (P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased 14C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased 14C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques (P < .05). Acetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. Metabolic divergence of macrophages polarized into different phenotypes represents a mechanistically relevant target for non-invasive characterization of atherosclerotic plaques using positron emission tomography (PET). Carbon-11 ( C)-labeled acetate is a clinically available tracer which accumulates in atherosclerotic plaques, but its biological and clinical correlates in atherosclerosis are undefined. Histological correlates of C-acetate uptake were determined in brachiocephalic arteries of western diet-fed apoE mice. The effect of polarizing stimuli on C-acetate uptake was determined by proinflammatory (interferon-γ + lipopolysaccharide) vs inflammation-resolving (interleukin-4) stimulation of murine macrophages and human carotid endarterectomy specimens over 2 days. C-acetate accumulated in atherosclerotic regions of arteries. CD68-positive monocytes/macrophages vs smooth muscle actin-positive smooth muscle cells were the dominant cells in regions with high vs low C-acetate uptake. C-acetate uptake progressively decreased in proinflammatory macrophages to 25.9 ± 4.5% of baseline (P < .001). A delayed increase in C-acetate uptake was induced in inflammation-resolving macrophages, reaching to 164.1 ± 21.4% (P < .01) of baseline. Consistently, stimulation of endarterectomy specimens with interferon-γ + lipopolysaccharide decreased C-acetate uptake to 66.5 ± 14.5%, while interleukin-4 increased C-acetate uptake to 151.5 ± 25.8% compared to non-stimulated plaques (P < .05). Acetate uptake by macrophages diverges upon proinflammatory and inflammation-resolving stimulation, which may be exploited for immunometabolic characterization of atherosclerosis. |
| Author | Gomez, Delphine Mannes, Philip Z. Tavakoli, Sina Aral, Ali Mubin Demirdelen, Selim Haddad, Joseph Leers, Steven A. |
| AuthorAffiliation | a Department of Radiology, University of Pittsburgh, Pittsburgh, PA d Heart, Lung, Blood, and Vascular Medicine Institute, UPMC Department of Medicine, Pittsburgh, Pennsylvania b Department of Surgery, University of Pittsburgh, Pittsburgh, PA c Department of Medicine, University of Pittsburgh, Pittsburgh, PA |
| AuthorAffiliation_xml | – name: a Department of Radiology, University of Pittsburgh, Pittsburgh, PA – name: b Department of Surgery, University of Pittsburgh, Pittsburgh, PA – name: c Department of Medicine, University of Pittsburgh, Pittsburgh, PA – name: d Heart, Lung, Blood, and Vascular Medicine Institute, UPMC Department of Medicine, Pittsburgh, Pennsylvania |
| Author_xml | – sequence: 1 givenname: Selim surname: Demirdelen fullname: Demirdelen, Selim organization: Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 2 givenname: Philip Z. surname: Mannes fullname: Mannes, Philip Z. organization: Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 3 givenname: Ali Mubin surname: Aral fullname: Aral, Ali Mubin organization: Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 4 givenname: Joseph surname: Haddad fullname: Haddad, Joseph organization: Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 5 givenname: Steven A. surname: Leers fullname: Leers, Steven A. organization: Department of Surgery, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 6 givenname: Delphine surname: Gomez fullname: Gomez, Delphine organization: Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA – sequence: 7 givenname: Sina surname: Tavakoli fullname: Tavakoli, Sina email: sit23@pitt.edu organization: Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33420659$$D View this record in MEDLINE/PubMed |
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| Keywords | atherosclerosis IFN-γ NOS2 IL-4 macrophage polarization metabolism Acetate 18F-FDG IL-1β imaging PET LPS |
| Language | English |
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| SubjectTerms | Acetate Acetates - metabolism Animals Atherosclerosis Atherosclerosis - diagnostic imaging Atherosclerosis - metabolism Cardiology Cytokines Humans Imaging Inflammation Inflammation - diagnostic imaging Interferon-gamma - metabolism Interleukin-4 - metabolism Lipopolysaccharides macrophage polarization Macrophages - metabolism Macrophages - pathology Medicine Medicine & Public Health metabolism Mice Nuclear Medicine Original Article Plaque, Atherosclerotic - diagnostic imaging Plaque, Atherosclerotic - pathology Radiology Smooth muscle Tomography, X-Ray Computed |
| Title | Divergence of acetate uptake in proinflammatory and inflammation-resolving macrophages: implications for imaging atherosclerosis |
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