Inhaled Carbon Monoxide Accelerates Resolution of Inflammation via Unique Proresolving Mediator–Heme Oxygenase-1 Circuits
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Resolution of acute inflammation is an active event accompanied by biosynthesis of specialized proresolving mediators (SPM). We employed a systems approach to determine the impact of CO in resolution active programs during self-limited inflammation in mice. Compared with ambient air, inhaled CO gas (250 ppm) significantly limited PMN infiltration (∼44%, 6 h) into peritoneum and shortened resolution interval from 4 to 2 h. We profiled exudate lipid mediators (LM) via metabololipidomics, CO reduced leukotriene B4 (21 ± 11 versus 59 ± 24 pg/mouse, 6 h), and elevated SPM including resolvin (Rv) D1 (27 ± 4 versus 16 ± 5 pg/mouse) and maresin 1 (26 ± 9 versus 15 ± 3 pg/mouse). With human macrophages, SPM (10 pM–10 nM) elevated heme oxygenase (HO)-1 (∼50%, 8 h). CO also enhanced HO-1 expression and accumulation of RvD1 and RvD5, an action reversed by blockage of a key SPM biosynthesis enzyme 15-lipoxygenase type 1. Compared with normoxia, CO increased ∼30% phagocytosis of opsonized zymosan with human macrophage, which was further enhanced by SPM (∼100%). This CO increased phagocytosis was blocked by 15-lipoxygenase inhibition, and SPM stimulated phagocytosis was diminished by HO-1 inhibition. In murine peritonitis, both pre- and posttreatment with CO inhalation significantly increased macrophages carrying ingested apoptotic PMN in exudates and enhanced PMN apoptosis. Taken together, these results indicate that CO accelerates resolution of acute inflammation, shortens resolution intervals, enhances macrophage efferocytosis, and temporally regulates local levels of lipid mediator/SPM. Moreover, they provide proresolving mechanisms for HO-1/CO, which is part of the SPM-initiated resolution circuit.
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In the same murine peritonitis model, inhaled CO raises SPM levels.
“Furthermore, CO inhalation also increased the levels of SPMs133”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [133]
In murine zymosan-induced peritonitis, inhaled CO raises macrophage phagocytosis and lowers exudate granulocyte counts, thereby accelerating complete inflammation resolution.
“In the murine zymosan-induced peritonitis model, inhaled CO increases macrophage phagocytosis and reduces granulocyte numbers in the exudate, thereby shortening the time to achieve complete resolution of inflammation133.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [133]
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- Authors
- Chiang, N., Shinohara, M., Dalli, J., Mirakaj, V., Kibi, M., Choi, A. M. K., & Serhan, C. N.
- Affiliations
- Brigham and Women's Hospital (US)
- Corresponding author
- Chiang, Nan
- Shinohara, Masakazu
- Dalli, Jesmond
- Mirakaj, Valbona
- Kibi, Megumi
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-06
- Volume
- 190
- Issue
- 12
- Pages
- 6378-6388
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC3679316
- OpenAlex
- W2108426267
- Cited by
- 117
- References
- 40
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 7 · 2021: 9 · 2020: 7 · 2019: 8 · 2018: 14 · 2017: 18 · 2016: 12 · 2015: 12 · 2014: 9 · 2013: 2
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL055330, R01HL079904, P01HL108801)
- National Institute of General Medical Sciences (P01GM095467)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Health Sciences › Medicine › Pharmacology › Inflammatory mediators and NSAID effects
- Keywords
- inhaled carbon monoxide, inflammation resolution, specialized pro-resolving mediators, heme oxygenase-1, leukotriene B4, resolvin D1, maresin 1, 15-lipoxygenase, macrophage phagocytosis, efferocytosis, neutrophil apoptosis, peritonitis, lipid mediators
- MeSH terms
- Animals, Carbon Monoxide, Cells, Cultured, Humans, Inflammation, Macrophages, Neutrophils, Signal Transduction, Apoptosis, Inflammation Mediators, Mice, Heme Oxygenase-1
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