Nitrite reductase activity of cytochrome c

Basu, Swati; Azarova, Natalia A.; Font, Michael D.; King, S. Bruce; Hogg, Neil; Gladwin, Mark T.; Shiva, Sruti; Kim-Shapiro, Daniel B.

doi:10.1074/jbc.m806934200

Cited by 214Hemoglobin structure and functionNitric Oxide and Endothelin EffectsMitochondrial Function and Pathology

Nitrite reductase activity of cytochrome c

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Basu, Swati, Azarova, Natalia A., Font, Michael D., King, S. Bruce, Hogg, Neil, Gladwin, Mark T., Shiva, Sruti, Kim-Shapiro, Daniel B.·2008·Journal of Biological Chemistry

DOI 10.1074/jbc.m806934200PMC PMC2583304

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Abstract

Small increases in physiological nitrite concentrations have now been shown to mediate a number of biological responses, including hypoxic vasodilation, cytoprotection after ischemia/reperfusion, and regulation of gene and protein expression. Thus, while nitrite was until recently believed to be biologically inert, it is now recognized as a potentially important hypoxic signaling molecule and therapeutic agent. Nitrite mediates signaling through its reduction to nitric oxide, via reactions with several heme-containing proteins. In this report, we show for the first time that the mitochondrial electron carrier cytochrome c can also effectively reduce nitrite to NO. This nitrite reductase activity is highly regulated as it is dependent on pentacoordination of the heme iron in the protein and occurs under anoxic and acidic conditions. Further, we demonstrate that in the presence of nitrite, pentacoordinate cytochrome c generates bioavailable NO that is able to inhibit mitochondrial respiration. These data suggest an additional role for cytochrome c as a nitrite reductase that may play an important role in regulating mitochondrial function and contributing to hypoxic, redox, and apoptotic signaling within the cell.

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We subsequently demonstrated that cytochrome-c gained ability to reduce nitrite in the presence of anionic phospholipids.
“We subsequently demonstrated that cytochrome-c gained ability to reduce nitrite in the presence of anionic phospholipids [73].”
From Mechanisms of nitrite bioactivation (2014) · cites this paper as [73]
Under conditions where pentacoordination is favored, cytochrome-c mediated NO production from nitrite could reach 14 nM/s.
“Under conditions where pentacoordination is favored, we previously calculated that cytochrome-c mediated NO production from nitrite could reach 14 nM/s [73].”
From Mechanisms of nitrite bioactivation (2014) · cites this paper as [73]
The nitrite reductase activity of neuroglobin or cytochrome c is negligible when the heme is hexacoordinated.
“the nitrite reductase activity of neuroglobin [63, 64, 70, 76] or cytochrome c [47] is negligible when the heme is hexacoordinated.”
From Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy (2011) · cites this paper as [47]
Exogenous administration of nitrite correlates with increased levels of S-nitrosothiols in red blood cells and other tissues both in vivo and in vitro.
“exogenous administration of nitrite correlates with increased levels of S-nitrosothiols in red blood cells and other tissues both in vivo and in vitro [25, 43, 46-53].”
From Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy (2011) · cites this paper as [47]
A potential mechanism by which nitrite could induce cGMP-independent effects is S-nitrosation of cysteine residues, a potential nitrite-induced post-translational modification that can alter protein function.
“A potential mechanism by which nitrite could induce cGMP-independent effects is S-nitrosation of cysteine residues, which is being increasingly recognized as a potential nitrite-induced post-translational modification that can alter protein function[17, 43, 46, 47, 51, 96].”
From Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy (2011) · cites this paper as [47]

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Reciprocal regulation of cellular nitric oxide formation by nitric oxide synthase and nitrite reductases
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Molecular Bases of Brain Preconditioning
Deryagin, O., Gavrilova, S. A., Латыпович, Г. Х., Golubeva, A. V., Andrianov, V. V., Гульусовна, Я. Г., Валентинович, Б. С., & Кошелев, В. Б. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00427 · Cited by 27 · see citing works

Mitochondrial Signaling: Nitric Oxide Synthesis by Cytochrome c Oxidase and Its Oxygen Sensitivity Are Modulated by Adenine NucleotidesPreprint
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The functional nitrite reductase activity of the heme-globins
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Self-citation
The detection of the nitrite reductase and NO-generating properties of haemoglobin by mitochondrial inhibition
Shiva, S., Rassaf, T., Patel, R. P., & Gladwin, M. T. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq327 · Cited by 46 · see citing works
Self-citation
Nitric oxide and hypoxia
Galkin, A. S., Higgs, A., & Moncada, S. (2007) · Essays in Biochemistry · doi:10.1042/bse0430029 · Cited by 65 · see citing works
Myoglobin Is a Nitrite Reductase That Generates NO and Regulates Mitochondrial Respiration.
Shiva, S., Huang, Z., MacArthur, P. H., Ringwood, L. A., & Gladwin, M. T. (2006) · Blood · doi:10.1182/blood.v108.11.1561.1561 · Cited by 3 · see citing works
Self-citation

Authors: Basu, S., Azarova, N. A., Font, M. D., King, S. B., Hogg, N., Gladwin, M. T., Shiva, S., & Kim-Shapiro, D. B.
Affiliations: Wake Forest University (US)
Medical College of Wisconsin (US)
University of Pittsburgh (US)
Corresponding author: Shiva, Sruti
ORCID: Basu, Swati
King, S. Bruce
Hogg, Neil
Gladwin, Mark T.
Shiva, Sruti
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2008-11
Volume: 283
Issue: 47
Pages: 32590-32597
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m806934200
PMC: PMC2583304
OpenAlex: W2078178926
Cited by: 214
References: 61
Citations by year: 2026: 5 · 2025: 15 · 2024: 6 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 16 · 2019: 6 · 2018: 17 · 2017: 10 · 2016: 14 · 2015: 16 · 2014: 11 · 2013: 14 · 2012: 13
FWCI: 7.00
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 4339 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (HL058091)
National Heart, Lung, and Blood Institute (HL058091, K02HL078706, R37HL058091, HL078706)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: cytochrome c, nitrite reductase activity, nitric oxide, hypoxia signaling, mitochondrial respiration inhibition, mitochondrial function, redox signaling, apoptosis
MeSH terms: Animals, Hypoxia, Cattle, Hydrogen-Ion Concentration, Kinetics, Mitochondria, Nitric Oxide, Nitrite Reductases, Oxygen, Oxygen Consumption, Phosphatidylcholines, Spectrophotometry, Signal Transduction, Apoptosis, Cytochromes c

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