Mitochondrial nitroalkene formation and mild uncoupling in ischaemic preconditioning. Implications for cardioprotection
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AIMS: Both mitochondria and nitric oxide (NO*) contribute to cardioprotection by ischaemic preconditioning (IPC). IPC causes mild uncoupling of mitochondria via uncoupling proteins (UCPs) and the adenine nucleotide translocase (ANT), and mild uncoupling per se is cardioprotective. Although electrophilic lipids are known to activate mitochondrial uncoupling, the role of such species in IPC-induced uncoupling and cardioprotection is unclear. We hypothesized that endogenous formation of NO*-derived electrophilic lipids (nitroalkenes such as nitro-linoleate, LNO2) during IPC may stimulate mitochondrial uncoupling via post-translational modification of UCPs and ANT, thus affording cardioprotection. METHODS: Hearts from male Sprague-Dawley rats were Langendorff-perfused and subjected to IPC. Nitroalkene formation was measured by HPLC-ESI-MS/MS. The effects of exogenous LNO2 and biotin-tagged LNO2 on isolated heart mitochondria and cardiomyocytes were also investigated. RESULTS: Nitroalkenes including LNO2 were endogenously generated in mitochondria of IPC hearts. Synthetic LNO2 (<1 microM) activated mild uncoupling, an effect blocked by UCP and ANT inhibitors. LNO2 (<1 microM) also protected cardiomyocytes against simulated ischaemia-reperfusion injury. Biotinylated LNO2 covalently modified ANT thiols and possibly UCP-2. No effects of LNO2 were attributable to NO* release, cGMP signalling, mitochondrial KATP channels, or protective kinase signalling. CONCLUSION: Components of a novel signalling pathway are inferred, wherein nitroalkenes formed by IPC-stimulated nitration reactions may induce mild mitochondrial uncoupling via post-translational modification of ANT and UCP-2, subsequently conferring resistance to ischaemia-reperfusion injury.
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Fatty acid nitroalkene administration protects against ischemia-reperfusion injury.
“Thus, in murine models of metabolic and inflammatory injury, fatty acid nitroalkene administration at nanomolar concentrations prevents restenosis after vessel injury (49), limits weight gain and loss of insulin sensitivity in murine models of metabolic syndrome (14), protects against ischemia-reperfusion injury (17,47,50), reduces plaque formation in a rodent model of atherosclerosis (51), and in”
From Conjugated linoleic acid is a preferential substrate for fatty acid nitration (2012) · cites this paper as [47]
In activated macrophages and rodent hearts subjected to ischemia-reoxygenation, inhibition of nitric-oxide synthase (NOS) activity suppresses fatty acid nitration by approximately 50%.
“In activated macrophages and rodent hearts subjected to ischemiareoxygenation, inhibition of nitric-oxide synthase (NOS) activity suppresses fatty acid nitration by ϳ50% (Fig. 3d) (19,47).”
From Conjugated linoleic acid is a preferential substrate for fatty acid nitration (2012) · cites this paper as [47]
Electrophilic lipids present in plants, generated by digestion of plant lipids, produced by oxidative inflammatory reactions or administered as pure synthetic homologs can regulate metabolism and the resolution of inflammatory processes.
“Consequently, electrophilic lipids which are present in plants, generated by digestion of plant lipids, produced by oxidative inflammatory reactions or administered as pure synthetic homologs [24], [26], [47], [56], can regulate metabolism and the resolution of inflammatory processes.”
From Olives and olive oil are sources of electrophilic fatty acid nitroalkenes (2014) · cites this paper as [47]
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Ferreira, A. M., Minarrieta, L., Lamas Bervejillo, M., & Rubbo, H. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.08.572 · Cited by 16 · see citing works
- Authors
- Nadtochiy, S. M., Baker, P. R. S., Freeman, B. A., & Brookes, P. S.
- Affiliations
- University of Rochester Medicine (US)
- University of Pittsburgh (US)
- Corresponding author
- Brookes, Paul S.
- Venue
- Cardiovascular Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-12-02
- Volume
- 82
- Issue
- 2
- Pages
- 333-340
- ISSN
- 0008-6363 (ISSN-L)
- 1755-3245
- PMC
- PMC2675927
- OpenAlex
- W2042149164
- Cited by
- 131
- References
- 59
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 6 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 8 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 10 · 2015: 9 · 2014: 8 · 2013: 12 · 2012: 9
- FWCI
- 8.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cardiovascular Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Diabetes Association
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL 64937, R01HL064937, HL 58115, R37HL058115, R01HL058115, R01HL071158)
- 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
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- ischemic preconditioning, mitochondrial uncoupling, nitroalkenes, nitric oxide, uncoupling proteins, adenine nucleotide translocase, UCP2, post-translational modification, cardioprotection, ischemia-reperfusion injury, cardiomyocytes, nitration
- MeSH terms
- Uncoupling Protein 2, Mitochondrial ADP, ATP Translocases, Alkenes, Animals, Disease Models, Animal, Cyclic GMP, Ion Channels, Linoleic Acids, Male, Mitochondria, Heart, Nitric Oxide, Nitro Compounds, Myocardial Reperfusion Injury, Rats, Sprague-Dawley, Ischemic Preconditioning, Myocardial, Mitochondrial Proteins, Rats
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