A Unifying Mechanism for Mitochondrial Superoxide Production during Ischemia-Reperfusion Injury
Open accessAbstract
Ischemia-reperfusion (IR) injury occurs when blood supply to an organ is disrupted--ischemia--and then restored--reperfusion--leading to a burst of reactive oxygen species (ROS) from mitochondria. It has been tacitly assumed that ROS production during IR is a non-specific consequence of oxygen interacting with dysfunctional mitochondria upon reperfusion. Recently, this view has changed, suggesting that ROS production during IR occurs by a defined mechanism. Here we survey the metabolic factors underlying IR injury and propose a unifying mechanism for its causes that makes sense of the huge amount of disparate data in this area and provides testable hypotheses and new directions for therapies.
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Reverse electron transport ROS generation occurs when succinate is present in high concentration and is responsible in vivo for ROS generated after ischemia upon reperfusion.
“This type of ROS generation occurs when succinate, the substrate for complex II, is present in high concentration and is responsible in vivo for the ROS generated after ischemia upon reperfusion (171, 172).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [172]
SUCNR1 ligation on MoDC or the U937 macrophage cell line induces cell migration.
“SUCNR1 ligation on MoDC or the U937 macrophage cell line induces cell migration, suggesting that succinate can act as a chemokine4.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [4]
Priming of DCs with succinate and antigen simultaneously elevates antigen-specific T cell activation, increasing TNFα and IFN-γ production.
“Priming of DCs with succinate and antigen simultaneously, elevates antigen-specific T cell activation, increasing TNFα and IFN-γproduction from these cells4.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [4]
SUCNR1 is highly expressed in mouse kidney, liver, spleen, small intestine, and on dendritic cells, and ligand binding induces Gi and Gq signalling cascades.
“SUCNR1 is highly expressed in mouse kidney, liver, spleen, small intestine3, and on dendritic cells (DCs) 4 and ligand binding induces Gi and Gq signalling cascades3.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [4]
Extracellular succinate acts in synergy with TLR ligands to increase TNFα and IL-1β expression and increases the capacity of DCs to act as antigen presenting cells.
“Extracellular succinate addition also acts in synergy with TLR ligands to increase TNFα and IL-1β expression4 and increases the capacity of DCs to act as antigen presenting cells.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [4]
Released succinate likely acts as an inflammatory signal via SUCNR1.
“one likely role is as an inflammatory signal, acting via SUCNR14,5,161,162.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [4]
Numerous metabolic pathways have been implicated in the metabolic reprogramming of immune cells, particularly those that regulate succinate levels, which can influence HIF signaling or other pathways.
“Numerous metabolic pathways have been implicated in the metabolic reprogramming of immune cells, in particular those that regulate succinate levels, which, in turn, can influence HIF signaling or other pathways (13,25,40,41).”
From Immunoresponsive Gene 1 and Itaconate Inhibit Succinate Dehydrogenase to Modulate Intracellular Succinate Levels (2016) · cites this paper as [40]
Inhibition of SDH by endogenously produced itaconate may buffer against potential oxidative damage that can occur under ischemia/reperfusion conditions.
“Notably, SDH inhibition protected against brain injury after ischemia/reperfusion (40,41), suggesting that inhibition of SDH by endogenously produced itaconate may buffer against potential oxidative damage that can occur under such conditions.”
From Immunoresponsive Gene 1 and Itaconate Inhibit Succinate Dehydrogenase to Modulate Intracellular Succinate Levels (2016) · cites this paper as [40]
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- Authors
- Chouchani, E. T., Pell, V. R., James, A. M., Work, L. M., Saeb-Parsy, K., Frezza, C., Krieg, T., & Murphy, M. P.
- Affiliations
- Harvard University (US)
- University of Cambridge (GB)
- MRC Mitochondrial Biology Unit (GB)
- University of Glasgow (GB)
- Corresponding author
- Murphy, Michael P.
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2016-02
- Volume
- 23
- Issue
- 2
- Pages
- 254-263
- ISSN
- 1550-4131 (ISSN-L)
- OpenAlex
- W2239083587
- Semantic Scholar
- 05aae81910c5536362646624d7e2848d0da4e591
- Cited by
- 752
- References
- 106
- Citations by year
- 2026: 62 · 2025: 78 · 2024: 63 · 2023: 79 · 2022: 90 · 2021: 104 · 2020: 83 · 2019: 64 · 2018: 58 · 2017: 50 · 2016: 19 · 2013: 1
- FWCI
- 10.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- Funders
- British Heart Foundation
- Medical Research Council (MC_UU_12022/6)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- ischemia-reperfusion injury, mitochondrial superoxide production, reactive oxygen species, mitochondrial dysfunction, reperfusion, oxidative stress, metabolic factors, tissue damage
- MeSH terms
- Animals, Electron Transport, Humans, Mitochondria, Models, Biological, Sulfhydryl Compounds, Superoxides, Reperfusion Injury
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