Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils
Abstract
Nitric oxide (.NO) plays a central role in the pathogenesis of diverse inflammatory and infectious disorders. The toxicity of .NO is thought to be engendered, in part, by its reaction with superoxide (O2.-), yielding the potent oxidant peroxynitrite (ONOO-). However, evidence for a role of ONOO- in vivo is based largely upon detection of 3-nitrotyrosine in injured tissues. We have recently demonstrated that nitrite (NO2-), a major end-product of .NO metabolism, readily promotes tyrosine nitration through formation of nitryl chloride (NO2Cl) and nitrogen dioxide (.NO2) by reaction with the inflammatory mediators hypochlorous acid (HOCl) or myeloperoxidase. We now show that activated human polymorphonuclear neutrophils convert NO2- into NO2Cl and .NO2 through myeloperoxidase-dependent pathways. Polymorphonuclear neutrophil-mediated nitration and chlorination of tyrosine residues or 4-hydroxyphenylacetic acid is enhanced by addition of NO2- or by fluxes of .NO. Addition of 15NO2- led to 15N enrichment of nitrated phenolic substrates, confirming its role in polymorphonuclear neutrophil-mediated nitration reactions. Polymorphonuclear neutrophil-mediated inactivation of endothelial cell angiotensin-converting enzyme was exacerbated by NO2-, illustrating the physiological significance of these reaction pathways to cellular dysfunction. Our data reveal that NO2- may regulate inflammatory processes through oxidative mechanisms, perhaps by contributing to the tyrosine nitration and chlorination observed in vivo.
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Intrinsic to the metabolism of NO3− and NO2− is the formation of the nitrogen dioxide radical (·NO2).
“Intrinsic to the metabolism of NO3− and NO2− is the formation of the nitrogen dioxide radical (·NO2).”
From Nitrite and nitrate-dependent generation of anti-inflammatory fatty acid nitroalkenes (2015) · cites this paper as [23]
·NO2 is formed by metalloprotein-catalyzed oxidation of NO2−, the autoxidation of ·NO, the protonation of NO2− to N2O3 followed by its disproportionation, decomposition of nitrous acid, and the homolytic scission of peroxynitrous acid and nitrosoperoxocarbonate.
“This species is formed by metalloprotein-catalyzed oxidation of NO2−, the autoxidation of ·NO, the protonation of NO2− to N2O3 followed by its disproportionation, decomposition of nitrous acid, and the homolytic scission of two key products of ·NO and superoxide (O2 ·−) reaction, peroxynitrous acid and nitrosoperoxocarbonate [21–23].”
From Nitrite and nitrate-dependent generation of anti-inflammatory fatty acid nitroalkenes (2015) · cites this paper as [23]
Mechanisms giving rise to NO2 include exposure to NO2 gas, O2-derived inflammatory by-products ONOOH and nitrosoperoxocarbonate (ONOOCO2), and heme protein-catalyzed oxidation of NO2− to NO2.
“These include exposure to ⅐ NO 2 gas, the O 2 . -derived inflammatory by-products ONOOH and nitrosoperoxocarbonate (ONOOCO 2 ) (45), and heme protein-catalyzed oxidation of NO 2 Ϫ to ⅐ NO 2 (46).”
From Conjugated linoleic acid is a preferential substrate for fatty acid nitration (2012) · cites this paper as [46]
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Flores-Santana, W., Switzer, C., Ridnour, L. A., Basudhar, D., Mancardi, D., Donzelli, S., Thomas, D. D., Miranda, K. M., Fukuto, J. M., & Wink, D. A. (2009) · Archives of Pharmacal Research · doi:10.1007/s12272-009-1805-x · Cited by 50 · see citing works
Cell signaling mediated by nitrated cyclic guanine nucleotide
Akaike, T., Fujii, S., Sawa, T., & Ihara, H. (2010) · Nitric Oxide · doi:10.1016/j.niox.2010.06.006 · Cited by 49 · see citing works
Vitamin C fails to protect amino acids and lipids from oxidation during acute inflammation
Gaut, J. P., Belaaouaj, A., Byun, J., Roberts, L. J., Maeda, N., Frei, B., & Heinecke, J. W. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.12.013 · Cited by 48 · see citing works
DNA damage by nitrite and peroxynitrite: Protection by dietary phenols
Zhao, K., Whiteman, M., Spencer, J. P. E., & Halliwell, B. (2001) · Methods in Enzymology · doi:10.1016/s0076-6879(01)35252-7 · Cited by 46 · see citing works
Self-citationNox1/nadph oxidase in bone marrow-derived cells modulates intestinal barrier function
Liu, J., Iwata, K., Zhu, K., Matsumoto, M., Matsumoto, K., Asaoka, N., Zhang, X., Ibi, M., Katsuyama, M., Tsutsui, M., et al. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.12.009 · Cited by 28 · see citing works
- Authors
- Eiserich, J. P., Hristova, M., Cross, C. E., Jones, A. D., Freeman, B. A., Halliwell, B., & van der Vliet, A.
- Affiliations
- University of Alabama at Birmingham (US)
- University of California, Davis (US)
- University of London (GB)
- Corresponding author
- Eiserich, Jason P.
- Venue
- Nature
- Published
- 1998-01
- Volume
- 391
- Issue
- 6665
- Pages
- 393-397
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1725300350
- Cited by
- 1,496
- References
- 32
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 25 · 2023: 17 · 2022: 31 · 2021: 27 · 2020: 30 · 2019: 25 · 2018: 32 · 2017: 26 · 2016: 27 · 2015: 23 · 2014: 35 · 2013: 35 · 2012: 44
- FWCI
- 43.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- nitric oxide, nitrite, myeloperoxidase, neutrophils, peroxynitrite, tyrosine nitration, nitryl chloride, hypochlorous acid, nitrotyrosine, 4-hydroxyphenylacetic acid, 15N labeling
- MeSH terms
- Animals, Cattle, Chlorides, Endothelium, Vascular, Humans, Hypochlorous Acid, Peroxidase, Neutrophils, Nitric Oxide, Nitrites, Oxidants, Inflammation Mediators, In Vitro Techniques
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