Preconditioning Results in S -Nitrosylation of Proteins Involved in Regulation of Mitochondrial Energetics and Calcium Transport
Abstract
Nitric oxide has been shown to be an important signaling messenger in ischemic preconditioning (IPC). Accordingly, we investigated whether protein S -nitrosylation occurs in IPC hearts and whether S -nitrosoglutathione (GSNO) elicits similar effects on S -nitrosylation and cardioprotection. Preceding 20 minutes of no-flow ischemia and reperfusion, hearts from C57BL/6J mice were perfused in the Langendorff mode and subjected to the following conditions: (1) control perfusion; (2) IPC; or (3) 0.1 mmol/L GSNO treatment. Compared with control, IPC and GSNO significantly improved postischemic recovery of left ventricular developed pressure and reduced infarct size. IPC and GSNO both significantly increased S -nitrosothiol contents and S -nitrosylation levels of the L-type Ca 2+ channel α1 subunit in heart membrane fractions. We identified several candidate S -nitrosylated proteins by proteomic analysis following the biotin switch method, including the cardiac sarcoplasmic reticulum Ca 2+ -ATPase, α-ketoglutarate dehydrogenase, and the mitochondrial F1-ATPase α1 subunit. The activities of these enzymes were altered in a concentration-dependent manner by GSNO treatment. We further developed a 2D DyLight fluorescence difference gel electrophoresis proteomic method that used DyLight fluors and a modified biotin switch method to identify S -nitrosylated proteins. IPC and GSNO produced a similar pattern of S -nitrosylation modification and cardiac protection against ischemia/reperfusion injury, suggesting that protein S -nitrosylation may play an important cardioprotective role in heart.
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Prior work showed that complex I is inhibited by various nitric oxide donors in vitro and that this inhibition is associated with S-nitrosation.
“previous work has shown that complex I is inhibited by various nitric oxide donors in vitro and that this inhibition is associated with S-nitrosation2,10,11,21–24.”
From Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I (2013) · cites this paper as [10]
NO· inhibits complex IV (cytochrome c oxidase) or the ATPase complex.
“other studies have found a role for NO· in the inhibition of complex IV (cytochrome c oxidase) (97, 474) or in the ATPase complex (405).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [405]
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- Authors
- Sun, J., Morgan, M., Shen, R.-F., Steenbergen, C., & Murphy, E.
- Affiliations
- National Institutes of Health (US)
- From the Vascular Medicine Branch (J.S., E.M.) and Proteomics Core Facility (M.M., R.-F.S.), National Heart Lung and Blood Institute, NIH, Bethesda; and Department of Pathology (C.S.), Johns Hopkins University, Baltimore, Md.
- Venue
- Circulation Research
- Published
- 2007-11-26
- Volume
- 101
- Issue
- 11
- Pages
- 1155-1163
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- OpenAlex
- W2126788226
- Cited by
- 367
- References
- 45
- Citations by year
- 2026: 4 · 2025: 13 · 2024: 11 · 2023: 11 · 2022: 3 · 2021: 14 · 2020: 12 · 2019: 18 · 2018: 16 · 2017: 20 · 2016: 15 · 2015: 20 · 2014: 35 · 2013: 34 · 2012: 32
- FWCI
- 16.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL039752, HL 39752)
- National Institute of Environmental Health Sciences
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- ischemic preconditioning, S-nitrosylation, S-nitrosoglutathione, nitric oxide signaling, cardioprotection, myocardial ischemia-reperfusion injury, sarcoplasmic reticulum Ca2+-ATPase, alpha-ketoglutarate dehydrogenase, mitochondrial F1-ATPase, mitochondrial bioenergetics, calcium transport
- MeSH terms
- Animals, Biological Transport, Calcium, Cardiotonic Agents, Energy Metabolism, Mice, Inbred C57BL, Mitochondria, Nitrogen Oxides, Perfusion, Proteins, Myocardial Reperfusion Injury, Ventricular Dysfunction, Left, Ischemic Preconditioning, Myocardial, Mice, In Vitro Techniques
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