Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation
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The S-nitrosation of mitochondrial proteins as a consequence of NO metabolism is of physiological and pathological significance. We previously developed a MitoSNO (mitochondria-targeted S-nitrosothiol) that selectively S-nitrosates mitochondrial proteins. To identify these S-nitrosated proteins, here we have developed a selective proteomic methodology, SNO-DIGE (S-nitrosothiol difference in gel electrophoresis). Protein thiols in control and MitoSNO-treated samples were blocked, then incubated with copper(II) and ascorbate to selectively reduce S-nitrosothiols. The samples were then treated with thiol-reactive Cy3 (indocarbocyanine) or Cy5 (indodicarbocyanine) fluorescent tags, mixed together and individual protein spots were resolved by 2D (two-dimensional) gel electrophoresis. Fluorescent scanning of these gels revealed S-nitrosated proteins by an increase in Cy5 red fluorescence, allowing for their identification by MS. Parallel analysis by Redox-DIGE enabled us to distinguish S-nitrosated thiol proteins from those which became oxidized due to NO metabolism. We identified 13 S-nitrosated mitochondrial proteins, and a further four that were oxidized, probably due to evanescent S-nitrosation relaxing to a reversible thiol modification. We investigated the consequences of S-nitrosation for three of the enzymes identified using SNO-DIGE (aconitase, mitochondrial aldehyde dehydrogenase and α-ketoglutarate dehydrogenase) and found that their activity was selectively and reversibly inhibited by S-nitrosation. We conclude that the reversible regulation of enzyme activity by S-nitrosation modifies enzymes central to mitochondrial metabolism, whereas identification and functional characterization of these novel targets provides mechanistic insight into the potential physiological and pathological roles played by this modification. More generally, the development of SNO-DIGE facilitates robust investigation of protein S-nitrosation across the proteome.
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The S-nitrosated mitochondrial proteins detected in vivo were probably membrane-protein complexes, which resolve poorly by two-dimensional gel electrophoresis.
“suggesting that the S-nitrosated mitochondrial proteins detected in vivo (Fig. 1a) were probably membrane-protein complexes, which resolve poorly by two-dimensional gel electrophoresis12.”
From Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I (2013) · cites this paper as [12]
The SNO-DIGE experiment used a biological variance analysis design with four biological replicates per experiment, comparing each treatment to a pooled standard.
“To assess differences in protein fluorescence using two-dimensional DIGE, we used an experimental design that included biological variance analysis (BVA)12. In each DIGE experiment, we used four biological replicates, where a biological replicate is an independently prepared heart tissue subjected to the CyDye sample preparations described above.”
From Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I (2013) · cites this paper as [12]
These S-nitrosating compounds target other mitochondrial proteins as well and may have other cellular effects neither completely understood nor well characterized.
“These S-nitrosating compounds, however, target other mitochondrial proteins as well (91), and may have other cellular effects neither completely understood nor well characterized.”
From Redox regulation of mitochondrial function (2012) · cites this paper as [91]
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- Authors
- Chouchani, E. T., Hurd, T. R., Nadtochiy, S. M., Brookes, P. S., Fearnley, I. M., Lilley, K. S., Smith, R. A. J., & Murphy, M. P.
- Affiliations
- MRC Mitochondrial Biology Unit (GB)
- University of Rochester Medicine (US)
- University of Cambridge (GB)
- University of Otago (NZ)
- Corresponding author
- Murphy, Michael P.
- ORCID
- Venue
- Biochemical Journal
- Publisher
- Portland Press Ltd.
- Published
- 2010-07-28
- Volume
- 430
- Issue
- 1
- Pages
- 49-59
- ISSN
- 0264-6021 (ISSN-L)
- 1470-8728
- PMC
- PMC2911678
- OpenAlex
- W2036982001
- Cited by
- 137
- References
- 53
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 4 · 2023: 3 · 2022: 7 · 2021: 7 · 2020: 6 · 2019: 6 · 2018: 6 · 2017: 12 · 2016: 4 · 2015: 8 · 2014: 15 · 2013: 13 · 2012: 16
- FWCI
- 6.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Biochemical Journal (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion, other-oa)
- Funders
- National Heart, Lung, and Blood Institute (HL-071158, R01HL071158)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- S-nitrosylation, S-nitrosothiols, mitochondrial proteins, nitric oxide metabolism, reversible protein modification, aconitase, mitochondrial aldehyde dehydrogenase, alpha-ketoglutarate dehydrogenase, enzyme inhibition, thiol oxidation, mitochondrial metabolism, proteomic identification
- MeSH terms
- Animals, Male, Mice, Inbred C57BL, Mitochondria, Myocardium, Oxidation-Reduction, Superoxides, Electrophoresis, Gel, Two-Dimensional, Myocardial Reperfusion Injury, Mitochondrial Proteins, S-Nitrosothiols, Proteomics, Mice, Rats, Membrane Potential, Mitochondrial, In Vitro Techniques
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