Nanoparticle-based itaconate treatment recapitulates low-cholesterol/low-fat diet-induced atherosclerotic plaque resolution
Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification...
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| Published in | Cell reports (Cambridge) Vol. 43; no. 11; p. 114911 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.11.2024
Elsevier |
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| Online Access | Get full text |
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| Abstract | Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification can be challenging for patients. Unfortunately, incomplete understanding of the underlying mechanisms has thwarted efforts to mimic the protective effects of a LCLFD. Here, we report that the tricarboxylic acid cycle intermediate itaconate (ITA), produced by plaque macrophages, is key to diet-induced plaque resolution. ITA is produced by immunoresponsive gene 1 (IRG1), which we observe is highly elevated in myeloid cells of vulnerable plaques and absent from early or stable plaques in mice and humans. We additionally report development of an ITA-conjugated lipid nanoparticle that accumulates in plaque and bone marrow myeloid cells, epigenetically reduces inflammation via H3K27ac deacetylation, and reproduces the therapeutic effects of LCLFD-induced plaque resolution in multiple atherosclerosis models.
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•Itaconate (ITA) mediates diet-driven plaque resolution in ASCVD•ITA-bearing lipid nanoparticles (ITA-LNPs) target plaque and bone marrow myeloid cells•ITA-LNP treatment recapitulates LCLFD-induced atherosclerotic plaque resolution•ITA-LNP treatment downregulates inflammatory genes via H3K27ac deacetylation
Hong et al. report that the tricarboxylic acid cycle metabolite itaconate (ITA) mediates low-cholesterol/low-fat-diet-induced atherosclerotic plaque resolution. Additionally, administration of nanoparticle-based ITA therapy induces plaque resolution in several models of atherosclerosis via multiple mechanisms, including epigenetic immunomodulation via H3K27ac deacetylation. |
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| AbstractList | Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification can be challenging for patients. Unfortunately, incomplete understanding of the underlying mechanisms has thwarted efforts to mimic the protective effects of a LCLFD. Here, we report that the tricarboxylic acid cycle intermediate itaconate (ITA), produced by plaque macrophages, is key to diet-induced plaque resolution. ITA is produced by immunoresponsive gene 1 (IRG1), which we observe is highly elevated in myeloid cells of vulnerable plaques and absent from early or stable plaques in mice and humans. We additionally report development of an ITA-conjugated lipid nanoparticle that accumulates in plaque and bone marrow myeloid cells, epigenetically reduces inflammation via H3K27ac deacetylation, and reproduces the therapeutic effects of LCLFD-induced plaque resolution in multiple atherosclerosis models.Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification can be challenging for patients. Unfortunately, incomplete understanding of the underlying mechanisms has thwarted efforts to mimic the protective effects of a LCLFD. Here, we report that the tricarboxylic acid cycle intermediate itaconate (ITA), produced by plaque macrophages, is key to diet-induced plaque resolution. ITA is produced by immunoresponsive gene 1 (IRG1), which we observe is highly elevated in myeloid cells of vulnerable plaques and absent from early or stable plaques in mice and humans. We additionally report development of an ITA-conjugated lipid nanoparticle that accumulates in plaque and bone marrow myeloid cells, epigenetically reduces inflammation via H3K27ac deacetylation, and reproduces the therapeutic effects of LCLFD-induced plaque resolution in multiple atherosclerosis models. Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification can be challenging for patients. Unfortunately, incomplete understanding of the underlying mechanisms has thwarted efforts to mimic the protective effects of a LCLFD. Here, we report that the tricarboxylic acid cycle intermediate itaconate (ITA), produced by plaque macrophages, is key to diet-induced plaque resolution. ITA is produced by immunoresponsive gene 1 (IRG1), which we observe is highly elevated in myeloid cells of vulnerable plaques and absent from early or stable plaques in mice and humans. We additionally report development of an ITA-conjugated lipid nanoparticle that accumulates in plaque and bone marrow myeloid cells, epigenetically reduces inflammation via H3K27ac deacetylation, and reproduces the therapeutic effects of LCLFD-induced plaque resolution in multiple atherosclerosis models. Current pharmacologic treatments for atherosclerosis do not completely protect patients; additional protection can be achieved by dietary modifications, such as a low-cholesterol/low-fat diet (LCLFD), that mediate plaque stabilization and inflammation reduction. However, this lifestyle modification can be challenging for patients. Unfortunately, incomplete understanding of the underlying mechanisms has thwarted efforts to mimic the protective effects of a LCLFD. Here, we report that the tricarboxylic acid cycle intermediate itaconate (ITA), produced by plaque macrophages, is key to diet-induced plaque resolution. ITA is produced by immunoresponsive gene 1 (IRG1), which we observe is highly elevated in myeloid cells of vulnerable plaques and absent from early or stable plaques in mice and humans. We additionally report development of an ITA-conjugated lipid nanoparticle that accumulates in plaque and bone marrow myeloid cells, epigenetically reduces inflammation via H3K27ac deacetylation, and reproduces the therapeutic effects of LCLFD-induced plaque resolution in multiple atherosclerosis models. [Display omitted] •Itaconate (ITA) mediates diet-driven plaque resolution in ASCVD•ITA-bearing lipid nanoparticles (ITA-LNPs) target plaque and bone marrow myeloid cells•ITA-LNP treatment recapitulates LCLFD-induced atherosclerotic plaque resolution•ITA-LNP treatment downregulates inflammatory genes via H3K27ac deacetylation Hong et al. report that the tricarboxylic acid cycle metabolite itaconate (ITA) mediates low-cholesterol/low-fat-diet-induced atherosclerotic plaque resolution. Additionally, administration of nanoparticle-based ITA therapy induces plaque resolution in several models of atherosclerosis via multiple mechanisms, including epigenetic immunomodulation via H3K27ac deacetylation. |
| ArticleNumber | 114911 |
| Author | Asase, Courteney Cameron, Mark J. Finn, Aloke V. Nayak, Lalitha Cherepanova, Olga Gangwar, Roopesh Singh Di, Lin Bevan, Graham H. Chaplin, Alice Pieper, Andrew A. Hong, Natalie E. Gao, Huiyun Mignery, Matthew Ravodina, Anastasia Maiseyeu, Andrei |
| Author_xml | – sequence: 1 givenname: Natalie E. orcidid: 0000-0003-4749-9200 surname: Hong fullname: Hong, Natalie E. organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 2 givenname: Alice surname: Chaplin fullname: Chaplin, Alice organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 3 givenname: Lin surname: Di fullname: Di, Lin organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 4 givenname: Anastasia surname: Ravodina fullname: Ravodina, Anastasia organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 5 givenname: Graham H. surname: Bevan fullname: Bevan, Graham H. organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 6 givenname: Huiyun surname: Gao fullname: Gao, Huiyun organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 7 givenname: Courteney surname: Asase fullname: Asase, Courteney organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 8 givenname: Roopesh Singh surname: Gangwar fullname: Gangwar, Roopesh Singh organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 9 givenname: Mark J. surname: Cameron fullname: Cameron, Mark J. organization: Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA – sequence: 10 givenname: Matthew surname: Mignery fullname: Mignery, Matthew organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 11 givenname: Olga surname: Cherepanova fullname: Cherepanova, Olga organization: Department of Cardiovascular and Metabolic Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA – sequence: 12 givenname: Aloke V. surname: Finn fullname: Finn, Aloke V. organization: Department of Internal Medicine, Cardiovascular Division, University of Maryland School of Medicine, Baltimore, MD, USA – sequence: 13 givenname: Lalitha surname: Nayak fullname: Nayak, Lalitha organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA – sequence: 14 givenname: Andrew A. surname: Pieper fullname: Pieper, Andrew A. organization: Department of Psychiatry, Case Western Reserve University, Cleveland, OH, USA – sequence: 15 givenname: Andrei surname: Maiseyeu fullname: Maiseyeu, Andrei email: axm1079@case.edu organization: Cardiovascular Research Institute, School of Medicine, Case Western Reserve University, Cleveland, OH, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39466775$$D View this record in MEDLINE/PubMed |
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| Keywords | atherosclerosis CP: Immunology itaconate plaque resolution TCA cycle cholesterol nanoparticle ApoE−/− mice ApoE(−/−) mice |
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| Title | Nanoparticle-based itaconate treatment recapitulates low-cholesterol/low-fat diet-induced atherosclerotic plaque resolution |
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