The Noncanonical Pathway for In Vivo Nitric Oxide Generation: The Nitrate-Nitrite-Nitric Oxide Pathway

Kapil, V.; Khambata, R.S.; Jones, D.A.; Rathod, K.; Primus, C.; Massimo, G.; Fukuto, J.M.; Ahluwalia, A.

doi:10.1124/pr.120.019240

Cited by 248Nitric Oxide and Endothelin EffectsRedox biology and oxidative stressEicosanoids and Hypertension Pharmacology

The Noncanonical Pathway for In Vivo Nitric Oxide Generation: The Nitrate-Nitrite-Nitric Oxide Pathway

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Kapil, V., Khambata, R.S., Jones, D.A., Rathod, K., Primus, C., Massimo, G., Fukuto, J.M., Ahluwalia, A.·2020·Pharmacological Reviews

DOI 10.1124/pr.120.019240

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Abstract

In contrast to nitric oxide, which has well established and important roles in the regulation of blood flow and thrombosis, neurotransmission, the normal functioning of the genitourinary system, and the inflammation response and host defense, its oxidized metabolites nitrite and nitrate have, until recently, been considered to be relatively inactive. However, this view has been radically revised over the past decade and more. Much evidence has now accumulated demonstrating that nitrite serves as a storage form of nitric oxide, releasing nitric oxide preferentially under acidic and/or hypoxic conditions but also occurring under physiologic conditions: a phenomenon that is catalyzed by a number of distinct mammalian nitrite reductases. Importantly, preclinical studies demonstrate that reduction of nitrite to nitric oxide results in a number of beneficial effects, including vasodilatation of blood vessels and lowering of blood pressure, as well as cytoprotective effects that limit the extent of damage caused by an ischemia/reperfusion insult, with this latter issue having been translated more recently to the clinical setting. In addition, research has demonstrated that the other main metabolite of the oxidation of nitric oxide (i.e., nitrate) can also be sequentially reduced through processing in vivo to nitrite and then nitrite to nitric oxide to exert a range of beneficial effects-most notably lowering of blood pressure, a phenomenon that has also been confirmed recently to be an effective method for blood pressure lowering in patients with hypertension. This review will provide a detailed description of the pathways involved in the bioactivation of both nitrate and nitrite in vivo, their functional effects in preclinical models, and their mechanisms of action, as well as a discussion of translational exploration of this pathway in diverse disease states characterized by deficiencies in bioavailable nitric oxide. SIGNIFICANCE STATEMENT: The past 15 years has seen a major revision in our understanding of the pathways for nitric oxide synthesis in the body with the discovery of the noncanonical pathway for nitric oxide generation known as the nitrate-nitrite-nitric oxide pathway. This review describes the molecular components of this pathway, its role in physiology, potential therapeutics of targeting this pathway, and their impact in experimental models, as well as the clinical translation (past and future) and potential side effects.

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The nitrate-nitrite-NO pathway offers an alternative, oxygen-independent mechanism for generating NO, which can partially restore vascular homeostasis under hypoxic or oxidative conditions.
“the nitrate-nitrite-NO pathway offers an alternative, oxygen-independent mechanism for generating NO, which can partially restore vascular homeostasis under hypoxic or oxidative conditions [209,210].”
From Dietary Nitrate-Rich Vegetables as Natural Modulators of Health: Mechanisms and Benefits in Ageing Populations (2026) · cites this paper as [210]
Highly processed nitrate-containing foods often undergo thermal treatment or prolonged storage, which diminishes phytochemical content and may reduce nitrate stability.
“highly processed nitrate-containing foods often undergo thermal treatment or prolonged storage, which diminishes phytochemical content and may reduce nitrate stability [210,215,288].”
From Dietary Nitrate-Rich Vegetables as Natural Modulators of Health: Mechanisms and Benefits in Ageing Populations (2026) · cites this paper as [210]

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Acute Dietary Nitrate Supplementation Improves Cycling Time Trial Performance
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Altered Fiber Distribution and Fiber-Specific Glycolytic and Oxidative Enzyme Activity in Skeletal Muscle of Patients With Type 2 Diabetes
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Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice
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Activation of Mitochondrial ATP-Dependent Potassium Channels by Nitric Oxide
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Phosphodiesterase-5 Inhibition With Sildenafil Attenuates Cardiomyocyte Apoptosis and Left Ventricular Dysfunction in a Chronic Model of Doxorubicin Cardiotoxicity
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Erythrocytes are the major intravascular storage sites of nitrite in human blood
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Regulation of the Permeability Transition Pore in Skeletal Muscle Mitochondria
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Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury
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Nitrite‐derived nitric oxide: a possible mediator of ‘acidic–metabolic’ vasodilation
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Nitrite reductase activity is a novel function of mammalian mitochondria
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“As such, inhibition of complex III (also known as cytochrome bc1 complex/ cytochrome c reductase) completely abolished nitrite reduction (Kozlov et al., 1999; Nohl et al., 2000).”
BackgroundInfluential
Circulating Nitrite Contributes to Cardioprotection by Remote Ischemic Preconditioning
Rassaf, T., Totzeck, M., Hendgen-Cotta, U. B., Shiva, S., Heusch, G., & Kelm, M. (2014) · Circulation Research · doi:10.1161/circresaha.114.303822 · Cited by 342 · see citing works
Estimation of nitric oxide production and reactionrates in tissue by use of a mathematical model
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Cancer Therapy–Related Cardiac Dysfunction and Heart Failure
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Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites.
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Nitrite Infusion in Humans and Nonhuman Primates: Endocrine Effects, Pharmacokinetics, and Tolerance Formation
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Impact of dietary nitrate supplementation via beetroot juice on exercising muscle vascular control in rats
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The effects of endurance, strength, and power training on muscle fiber type shifting.
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“…the content of Ca21-handling proteins in type II muscle (Kinnunen and Manttari, 2012) to promote both a lower percentage of type II skeletal muscle (Wilson et al., 2012) and lower mitochondrial UCP3 content (Fernstrom et al., 2004), which is an important determinant of exercise efficiency…”
Background
Chlorine Gas Inhalation: Human Clinical Evidence of Toxicity and Experience in Animal Models
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Significance of xanthine oxidase in capillary endothelial cells.
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Infant Methemoglobinemia: The Role of Dietary Nitrate in Food and Water
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Nitrate Supplementation’s Improvement of 10-km Time-Trial Performance in Trained Cyclists
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Kinetic and Mechanistic Studies of the NO•-Mediated Oxidation of Oxymyoglobin and Oxyhemoglobin
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Concentration-dependent Effects of Nitric Oxide on Mitochondrial Permeability Transition and Cytochrome cRelease
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8 of the 774 references couldn’t be matched to a known paper.

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The Biologically Relevant Coordination Chemistry of Iron and Nitric Oxide: Electronic Structure and Reactivity
Lehnert, N., Kim, E., Dong, H. T., Harland, J. B., Hunt, A. P., Manickas, E. C., Oakley, K. M., Pham, J., Reed, G. C., & Alfaro, V. S. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00253 · Cited by 277 · see citing works
A systematic framework for understanding the microbiome in human health and disease: from basic principles to clinical translation
Ma, Z., Zuo, T., Frey, N., & Rangrez, A. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01946-6 · Cited by 297 · see citing works
Diet for the prevention and management of sarcopenia
Calvani, R., Picca, A., Coelho‐Júnior, H. J., Tosato, M., Marzetti, E., & Landi, F. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155637 · Cited by 153 · see citing works
The role of gut microbiota in intestinal disease: from an oxidative stress perspective
Sun, Y., Wang, X., Li, L., Zhong, C., Zhang, Y., Yang, X., Li, M., & Yang, C. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1328324 · Cited by 130 · see citing works
L‐Arginine‐Loaded Gold Nanocages Ameliorate Myocardial Ischemia/Reperfusion Injury by Promoting Nitric Oxide Production and Maintaining Mitochondrial Function
Wang, Z., Yang, N., Hou, Y., Li, Y., Yin, C., Yang, E., Cao, H., Hu, G., Xue, J., Yang, J., et al. (2023) · Advanced Science · doi:10.1002/advs.202302123 · Cited by 118 · see citing works
Looking Back at the Early Stages of Redox Biology
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Pathways Linking Oral Bacteria, Nitric Oxide Metabolism, and Health
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Emerging Targets and Treatments for Sarcopenia: A Narrative Review
Cacciatore, S., Calvani, R., Esposito, I., Massaro, C., Gava, G., Picca, A., Tosato, M., Marzetti, E., & Landi, F. (2024) · Nutrients · doi:10.3390/nu16193271 · Cited by 71 · see citing works
Factors that Moderate the Effect of Nitrate Ingestion on Exercise Performance in Adults: A Systematic Review with Meta-Analyses and Meta-Regressions
Silva, K. V. C., Costa, B. D., Gomes, A. C., Saunders, B., & Mota, J. F. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac054 · Cited by 64 · see citing works
Mechanisms of Nitrosamine Mutagenicity and Their Relationship to Rodent Carcinogenic Potency
Snodin, D. J., Trejo‐Martin, A., Ponting, D. J., Smith, G. F., Czich, A., Cross, K. P., Custer, L. L., Elloway, J. M., Greene, N., Kalgutkar, A. S. S., et al. (2024) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.3c00327 · Cited by 61 · see citing works
Hydrogen sulfide signalling in neurodegenerative diseases
Tripathi, S. J., Chakraborty, S., Miller, E., Pieper, A. A., & Paul, B. D. (2023) · British Journal of Pharmacology · doi:10.1111/bph.16170 · Cited by 59 · see citing works
The role of nitric oxide in sepsis-associated kidney injury
Oliveira, F. R. M. B., Assreuy, J., & Sordi, R. (2022) · Bioscience Reports · doi:10.1042/bsr20220093 · Cited by 52 · see citing works
Homeostatic medicine: a strategy for exploring health and disease
Wang, S., & Qin, L. (2022) · Current Medicine · doi:10.1007/s44194-022-00016-9 · Cited by 56 · see citing works
Nutraceuticals and Dietary Supplements for Older Adults with Long COVID-19
Tosato, M., Ciciarello, F., Zazzara, M. B., Pais, C., Savera, G., Picca, A., Galluzzo, V., Coelho‐Júnior, H. J., Calvani, R., Marzetti, E., et al. (2022) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2022.04.004 · Cited by 50 · see citing works
Dietary Inorganic Nitrate as an Ergogenic Aid: An Expert Consensus Derived via the Modified Delphi Technique
Shannon, O. M., Allen, J. D., Bescós, R., Burke, L. M., Clifford, T., Easton, C., Gonzalez, J. T., JONES, A. M., Jonvik, K. L., Larsen, F. J., et al. (2022) · Sports Medicine · doi:10.1007/s40279-022-01701-3 · Cited by 51 · see citing works
Astrocytes produce nitric oxide via nitrite reduction in mitochondria to regulate cerebral blood flow during brain hypoxia
Christie, I. N., Theparambil, S. M., Braga, A., Doronin, M., Hosford, P. S., Brazhe, A., Mascarenhas, A., Nizari, S., Hadjihambi, A., Wells, J. A., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113514 · Cited by 51 · see citing works
The Reactive Species Interactome in the Brain
Malard, E., Valable, S., Bernaudin, M., Pérès, E. A., & Châtre, L. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8238 · Cited by 46 · see citing works
Inorganic nitrate benefits contrast-induced nephropathy after coronary angiography for acute coronary syndromes: the NITRATE-CIN trial
Jones, D. A., Beirne, A., Kelham, M., Wynne, L., Andiapen, M., Rathod, K. S., Parakaw, T., Adams, J., Learoyd, A., Khan, K., et al. (2024) · European Heart Journal · doi:10.1093/eurheartj/ehae100 · Cited by 43 · see citing works
Self-citation
Dietary nitrate and population health: a narrative review of the translational potential of existing laboratory studies
Shannon, O. M., Easton, C., Shepherd, A. I., Siervo, M., Bailey, S. J., & Clifford, T. (2021) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/s13102-021-00292-2 · Cited by 40 · see citing works
Posttranslational S-nitrosylation modification regulates HMGB1 secretion and promotes its proinflammatory and neurodegenerative effects
Yang, R., Gao, Y., Li, H., Huang, W. C., Tu, D., Yang, M., Liu, X., Hong, J., & Gao, H. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111330 · Cited by 37 · see citing works
Endogenous Hemoprotein-Dependent Signaling Pathways of Nitric Oxide and Nitrite
Dent, M. R., DeMartino, A. W., Tejero, J., & Gladwin, M. T. (2021) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.1c01048 · Cited by 35 · see citing works
Gasotransmitter delivery for bone diseases and regeneration
Xu, Y., Li, Y., Gao, A., Chu, P. K.-H., & Wang, H. (2023) · The Innovation Life · doi:10.59717/j.xinn-life.2023.100015 · Cited by 35 · see citing works
Gut microbiota mediated the toxicity of high concentration of dietary nitrite in C57BL/6 mice
Xu, J., Wang, M., Liu, Q., Lin, X., Pu, K., & He, Z. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113224 · Cited by 35 · see citing works
Sodium nitrite poisoning: A series of 20 fatalities in which post-mortem blood nitrite and nitrate concentrations are reported
Hikin, L., Ho, J., Morley, S. R., Ahluwalia, A., & Smith, P. R. (2023) · Forensic Science International · doi:10.1016/j.forsciint.2023.111610 · Cited by 33 · see citing works
Self-citation
Photochemical Generation of Peroxynitrite: Concurrent Inhibition of Glycolysis and Glutamine Metabolism for Enhanced Metabolic Therapy
Yuan, L., Yang, L., Song, W. L., Song, H., Hu, J., Lou, X., Xia, F., & Yoon, J. (2025) · Journal of the American Chemical Society · doi:10.1021/jacs.5c07860 · Cited by 32 · see citing works
Effects of Dietary Nitrate Supplementation on Performance during Single and Repeated Bouts of Short-Duration High-Intensity Exercise: A Systematic Review and Meta-Analysis of Randomised Controlled Trials
Alsharif, N. S., Clifford, T., Alhebshi, A., Rowland, S. N., & Bailey, S. J. (2023) · Antioxidants · doi:10.3390/antiox12061194 · Cited by 33 · see citing works
Low levels of nitric oxide promotes heme maturation into several hemeproteins and is also therapeutic
Ghosh, A., Sumi, M. P., Tupta, B., Okamoto, T., Aulak, K. S., Tsutsui, M., Shimokawa, H., ERZURUM, S. C., & Stuehr, D. J. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102478 · Cited by 27 · see citing works
Dietary Nitrate from Plant Foods: A Conditionally Essential Nutrient for Cardiovascular Health
Pinaffi-Langley, A. C. D. C., Dajani, R. M., Prater, M. C., Nguyen, H. V. M., Vrancken, K., Hays, F. A., & Hord, N. G. (2024) · Advances in Nutrition · doi:10.1016/j.advnut.2023.100158 · Cited by 30 · see citing works
Nitric oxide’s physiologic effects and potential as a therapeutic agent against COVID-19
Ricciardolo, F. L. M., Bertolini, F., Carriero, V. M. A., & Högman, M. (2020) · Journal of Breath Research · doi:10.1088/1752-7163/abc302 · Cited by 29 · see citing works
Nanonitrator: novel enhancer of inorganic nitrate’s protective effects, predicated on swarm learning approach
Pan, W., Hu, G., Li, S., Li, G., Feng, X., Wu, Z., Zhang, D., Qin, L., Wang, X., Hu, L., et al. (2023) · 中国科学通报：英文版 · doi:10.1016/j.scib.2023.03.043 · Cited by 29 · see citing works
The Role of Oral Nitrate-Reducing Bacteria in the Prevention of Caries: A Review Related to Caries and Nitrate Metabolism
Feng, J., Liu, J., Jiang, M., Chen, Q., Zhang, Y., Yang, M., & Zhai, Y. (2023) · Caries Research · doi:10.1159/000529162 · Cited by 28 · see citing works
Emerging strategies for nitric oxide production and their topical application as nanodressings to promote diabetic wound healing
Xia, D., Guo, Y., Xu, R., & Li, N. (2025) · Journal of Nanobiotechnology · doi:10.1186/s12951-025-03135-1 · Cited by 32 · see citing works
Nitric oxide bioavailability for red blood cell deformability in the microcirculation: A review of recent progress
Kobayashi, J., Ohtake, K., Murata, I., & Sonoda, K. (2022) · Nitric Oxide · doi:10.1016/j.niox.2022.09.004 · Cited by 28 · see citing works
Inorganic nitrate: A potential prebiotic for oral microbiota dysbiosis associated with type 2 diabetes
Bahadoran, Z., Mirmiran, P., Carlström, M., & Ghasemi, A. (2021) · Nitric Oxide · doi:10.1016/j.niox.2021.09.001 · Cited by 26 · see citing works
Quantitative aspects of nitric oxide production from nitrate and nitrite
Ghasemi, A. (2022) · EXCLI journal · doi:10.17179/excli2022-4727 · Cited by 27 · see citing works
Gases in Sepsis: Novel Mediators and Therapeutic Targets
Zhu, Z., Chambers, S. T., Zeng, Y., & Bhatia, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073669 · Cited by 26 · see citing works
Effect of inorganic nitrate on metabolic parameters in patients with type 2 diabetes: A 24-week randomized double-blind placebo-controlled clinical trial
Bahadoran, Z., Norouzirad, R., Mirmiran, P., Gaeini, Z., Jeddi, S., Shokri, M., Azizi, F., & Ghasemi, A. (2020) · Nitric Oxide · doi:10.1016/j.niox.2020.12.005 · Cited by 25 · see citing works
Electrocatalytic generation of reactive species and implications in microbial inactivation
Nichols, F., Ozoemena, K. I., & Chen, S. W. (2022) · CHINESE JOURNAL OF CATALYSIS (CHINESE VERSION) · doi:10.1016/s1872-2067(21)63941-4 · Cited by 25 · see citing works
Effect of fucoidan on gut microbiota and its clinical efficacy in Helicobacter pylori eradication: A randomized controlled trial
Wang, S., Tian, Z. B., Chen, J., Cong, P. S., Ding, X. L., Zhang, C. P., Yin, X. Y., Yang, L., Jing, X., Mao, T., et al. (2023) · Journal of Digestive Diseases · doi:10.1111/1751-2980.13215 · Cited by 24 · see citing works
Inorganic nitrate attenuates cardiac dysfunction: roles for xanthine oxidoreductase and nitric oxide
Gee, L. C., Massimo, G., Lau, C. W. Z., Primus, C., Fernandes, D., Chen, J., Rathod, K. S., Hamers, A. J. P., Filomena, F., Nuredini, G., et al. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15636 · Cited by 22 · see citing works
Self-citation
Role of nitric oxide in type 1 diabetes-induced osteoporosis
Jeddi, S., Yousefzadeh, N., Kashfi, K., & Ghasemi, A. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114888 · Cited by 24 · see citing works
The Reactive Species Interactome in Red Blood Cells: Oxidants, Antioxidants, and Molecular Targets
Cortese-Krott, M. M. (2023) · Antioxidants · doi:10.3390/antiox12091736 · Cited by 25 · see citing works
Application of machine learning and laser optical-acoustic spectroscopy to study the profile of exhaled air volatile markers of acute myocardial infarction
Borisov, A. V., Геннадьевна, С. А., Kuzmin, D. A., Ryabov, V. V., Boyko, А. А., Zaharova, O., Zasedatel, V. S., & Kistenev, Y. V. (2021) · Journal of Breath Research · doi:10.1088/1752-7163/abebd4 · Cited by 23 · see citing works
Inhaled nitric oxide suppresses neuroinflammation in experimental ischemic stroke
Sienel, R. I., Mamrak, U., Biller, J., Roth, S., Zellner, A., Parakaw, T., Khambata, R. S., Liesz, A., Haffner, C., Ahluwalia, A., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02988-3 · Cited by 22 · see citing works
Self-citation
Control of rat muscle nitrate levels after perturbation of steady state dietary nitrate intake
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Authors: Kapil, V., Khambata, R. S., Jones, D. A., Rathod, K., Primus, C., Massimo, G., Fukuto, J. M., & Ahluwalia, A.
Affiliations: Sonoma State University (US)
ORCID: Kapil, V.
Khambata, R.S.
Jones, D.A.
Rathod, K.
Primus, C.
Massimo, G.
Fukuto, J.M.
Ahluwalia, A.
Venue: Pharmacological Reviews
Publisher: Elsevier BV
Published: 2020-07
Volume: 72
Issue: 3
Pages: 692-766
ISSN: 0031-6997 (ISSN-L)
DOI: 10.1124/pr.120.019240
OpenAlex: W3037888613
Cited by: 248
References: 774
Citations by year: 2026: 32 · 2025: 42 · 2024: 38 · 2023: 46 · 2022: 46 · 2021: 35 · 2020: 9
FWCI: 4.33
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc/4.0/ (vor, 1645 d)
Locations: Pharmacological Reviews (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc)
Funders: Barts Charity (MRC0213, MGU0284, MRC0223)
British Heart Foundation (PG/19/4/33995)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Eicosanoids and Hypertension Pharmacology
Keywords: nitrate-nitrite-nitric oxide pathway, nitrite reductase, nitric oxide storage, vasodilation, blood pressure reduction, hypertension, ischemia-reperfusion injury, cytoprotection
MeSH terms: Animals, Blood Pressure, Humans, Nitrates, Nitric Oxide, Nitrites, Signal Transduction, Randomized Controlled Trials as Topic

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The Noncanonical Pathway for In Vivo Nitric Oxide Generation: The Nitrate-Nitrite-Nitric Oxide Pathway

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