Carbon monoxide-loaded red blood cells ameliorate metabolic dysfunction-associated steatohepatitis progression via enhancing AMP-activated protein kinase activity and inhibiting Kupffer cell activation
Open accessAbstract
Metabolic dysfunction-associated steatohepatitis (MASH) is a progressive form of nonalcoholic fatty liver disease characterised by fat accumulation, inflammation, oxidative stress, fibrosis, and impaired liver regeneration. In this study, we found that heme oxygenase-1 (HO-1) is induced in both MASH patients and in a MASH mouse model. Further, hepatic carbon monoxide (CO) levels in MASH model mice were >2-fold higher than in healthy mice, suggesting that liver HO-1 is activated as MASH progresses. Based on these findings, we used CO-loaded red blood cells (CO-RBCs) as a CO donor in the liver, and evaluated their therapeutic effect in methionine-choline deficient diet (MCDD)-induced and high-fat-diet (HFD)-induced MASH model mice. Intravenously administered CO-RBCs effectively delivered CO to the MASH liver, where they prevented fat accumulation by promoting fatty acid oxidation via AMP-activated protein kinase (AMPK) activation and peroxisome proliferator-activated receptor induction. They also markedly suppressed Kupffer cell activation and their corresponding anti-inflammatory and antioxidative stress activities in MASH mice. CO-RBCs also helped to restore liver regeneration in mice with HFD-induced MASH by activating AMPK. We confirmed the underlying mechanisms by performing in vitro experiments in RAW264.7 cells and palmitate-stimulated HepG2 cells. Taken together, CO-RBCs show potential as a promising cellular treatment for MASH.
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AMPK plays a central role in macrophage metabolic reprogramming.
“AMP-activated protein kinase (AMPK), a master regulator of cellular energy homeostasis, plays a central role in this process (33–36).”
From Strategies to promote liver fibrosis amelioration with involvement of restorative macrophages (2026) · cites this paper as [35]
The Results section ('CO-RBCs restore fatty acid oxidation in MCDD-fed MASH mice'; page unavailable) links AMPK activation to hepatic fatty acid oxidation. Another Results section reports an anti-inflammatory effect in macrophages but measures AMPK activity in HepG2 liver cells, not macrophages. The paper therefore supports AMPK’s role in liver metabolism, but not the specific claim that it plays a central role in macrophage metabolic reprogramming. (LLM, conf=0.85)
Experimental — accuracy not yet measuredUpregulation of PPARα together with PPARγ may depend on AMPK activation.
“Pharmacological activation of PPARα increases restorative macrophage populations (30), and its upregulation, together with PPARγ, may depend on AMPK activation, linking transcriptional control with metabolic reprogramming (35).”
From Strategies to promote liver fibrosis amelioration with involvement of restorative macrophages (2026) · cites this paper as [35]
The Discussion (page unavailable) proposes that CO-RBCs may increase PPAR-α expression through AMPK activation in MASH liver, and the Results report increased AMPK activity alongside restored PPAR-α levels. The paper mentions PPAR-γ only in the context of dual-agonist drugs; it does not say that PPAR-γ upregulation depends on AMPK activation. (LLM, conf=0.87)
Experimental — accuracy not yet measured
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- Authors
- Yanagisawa, H., Maeda, H., Noguchi, I., Tanaka, M., Wada, N., Nagasaki, T., Kobayashi, K., Kanazawa, G., Taguchi, K., Chuang, V. T. G., Sakai, H., Nakashima, H., Kinoshita, M., Kitagishi, H., Iwakiri, Y., Sasaki, Y., Tanaka, Y., Otagiri, M., Watanabe, H., & Maruyama, T.
- Affiliations
- Kumamoto University (JP)
- Saiseikai Kumamoto Hospital (JP)
- Keio University (JP)
- Curtin University (AU)
- Nara Medical University (JP)
- National Defense Medical College (JP)
- Doshisha University (JP)
- Yale University (US)
- Sojo University (JP)
- Corresponding author
- Watanabe, Hiroshi
- Maruyama, Toru
- ORCID
- Venue
- Redox Biology
- Publisher
- Elsevier BV
- Published
- 2024-10
- Volume
- 76
- Pages
- 103314
- ISSN
- 2213-2317 (ISSN-L)
- PMC
- PMC11381851
- OpenAlex
- W4401668016
- Cited by
- 10
- References
- 82
- Citations by year
- 2026: 6 · 2025: 4
- FWCI
- 1.36
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Redox Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- EA Pharma Co., Ltd.
- Japan Society for the Promotion of Science (N-227205)
- Pharmaceutical Society of Japan
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- nonalcoholic steatohepatitis, non-alcoholic fatty liver disease, AMPK, Kupffer cell activation, heme oxygenase-1, carbon monoxide delivery, fatty acid oxidation, peroxisome proliferator-activated receptors, liver regeneration, methionine-choline-deficient diet, high-fat diet, oxidative stress
- MeSH terms
- Animals, Carbon Monoxide, Disease Models, Animal, Erythrocytes, Humans, Kupffer Cells, Liver, Male, Oxidative Stress, Mice, Heme Oxygenase-1, AMP-Activated Protein Kinases, Diet, High-Fat, Non-alcoholic Fatty Liver Disease
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