The redox interplay between nitrite and nitric oxide: From the gut to the brain

Pereira, Cassilda; Ferreira, Nuno R.; Rocha, Bárbara S.; Barbosa, Rui M.; Laranjinha, João

doi:10.1016/j.redox.2013.04.004

Cited by 92Nitric Oxide and Endothelin EffectsRedox biology and oxidative stressAntioxidant Activity and Oxidative Stress

The redox interplay between nitrite and nitric oxide: From the gut to the brain

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Pereira, Cassilda, Ferreira, Nuno R., Rocha, Bárbara S., Barbosa, Rui M., Laranjinha, João·2013·Redox Biology

DOI 10.1016/j.redox.2013.04.004PMC PMC3757698

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Abstract

The reversible redox conversion of nitrite and nitric oxide ((•)NO) in a physiological setting is now widely accepted. Nitrite has long been identified as a stable intermediate of (•)NO oxidation but several lines of evidence support the reduction of nitrite to nitric oxide in vivo. In the gut, this notion implies that nitrate from dietary sources fuels the longstanding production of nitrite in the oral cavity followed by univalent reduction to (•)NO in the stomach. Once formed, (•)NO boosts a network of reactions, including the production of higher nitrogen oxides that may have a physiological impact via the post-translational modification of proteins and lipids. Dietary compounds, such as polyphenols, and different prandial states (secreting specific gastric mediators) modulate the outcome of these reactions. The gut has unusual characteristics that modulate nitrite and (•)NO redox interplay: (1) wide range of pH (neutral vs acidic) and oxygen tension (c.a. 70 Torr in the stomach and nearly anoxic in the colon), (2) variable lumen content and (3) highly developed enteric nervous system (sensitive to (•)NO and dietary compounds, such as glutamate). The redox interplay of nitrite and (•)NO might also participate in the regulation of brain homeostasis upon neuronal glutamatergic stimulation in a process facilitated by ascorbate and a localized and transient decrease of oxygen tension. In a way reminiscent of that occurring in the stomach, a nitrite/(•)NO/ascorbate redox interplay in the brain at glutamatergic synapses, contributing to local (•)NO increase, may impact on (•)NO-mediated process. We here discuss the implications of the redox conversion of nitrite to (•)NO in the gut, how nitrite-derived (•)NO may signal from the digestive to the central nervous system, influencing brain function, as well as a putative ascorbate-driven nitrite/NO pathway occurring in the brain.

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Dietary antioxidants (e.g., polyphenols and ascorbate) may further enhance nitrite reduction and stabilise reactive nitrogen species.
“Dietary antioxidants (e.g., polyphenols and ascorbate) may further enhance this process and stabilise reactive nitrogen species [51].”
From Dietary Nitrate-Rich Vegetables as Natural Modulators of Health: Mechanisms and Benefits in Ageing Populations (2026) · cites this paper as [51]
The ‘Reduction by dietary polyphenols’ section says polyphenol-rich foods, similarly to ascorbate, boost nitric oxide production from nitrite in the acidic stomach. The copy does not say that these compounds stabilise reactive nitrogen species; it instead describes subsequent reactions that form nitroso derivatives and nitrated phenols. Page numbers were not available in the supplied copy. (LLM, conf=0.86)
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Nitrite acts as a redox-active intermediate that serves as both an oxidation product of NO and a substrate for its regeneration.
“At the biochemical level, nitrite acts as a redox-active intermediate that serves as both an oxidation product of NO and a substrate for its regeneration [51].”
From Dietary Nitrate-Rich Vegetables as Natural Modulators of Health: Mechanisms and Benefits in Ageing Populations (2026) · cites this paper as [51]
There exists a broad range of redox-derived nitrogen oxides that exert both cGMP-dependent and -independent signaling actions as a result of nitrosative-, nitrative- and oxidative-induced post-translational protein modifications and subsequent changes in protein function and gene expression profiles.
“There exists a broad range of redox-derived nitrogen oxides that exert both cGMP-dependent and -independent signaling actions as a result of nitrosative-, nitrative- and oxidative-induced post-translational protein modifications and subsequent changes in protein function and gene expression profiles[100–102].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [100]

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Nitrite confers protection against myocardial infarction: Role of xanthine oxidoreductase, NADPH oxidase and KATP channels
Baker, J. E., Su, J., Fu, X., Hsu, A., Gross, G. J., Tweddell, J. S., & Hogg, N. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.07.057 · Cited by 137 · see citing works
NITRIC OXIDE PHYSIOLOGY
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The ingestion of inorganic nitrate increases gastric S-nitrosothiol levels and inhibits platelet function in humans
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Mitochondria and Hypoxic Signaling
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In Vivo Real‐Time Measurement of Nitric Oxide in Anesthetized Rat Brain
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Active/de‐active state transition of the mitochondrial complex I as revealed by specific sulfhydryl group labeling
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Electrochemical measurement of endogenously produced nitric oxide in brain slices using Nafion/o-phenylenediamine modified carbon fiber microelectrodes
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Nitrite activates AMP kinase to stimulate mitochondrial biogenesis independent of soluble guanylate cyclase
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A Method to Study Kinetics of Transnitrosation with Nitrosoglutathione: Reactions with Hemoglobin and Other Thiols
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A comparative study of carbon fiber-based microelectrodes for the measurement of nitric oxide in brain tissue
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Nitrite infusion increases cerebral blood flow and decreases mean arterial blood pressure in rats: A role for red cell NO
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Roles of nitric oxide, nitrite and myoglobin on myocardial efficiency in trout (Oncorhynchus mykiss) and goldfish (Carassius auratus): implications for hypoxia tolerance
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The potent vasodilator ethyl nitrite is formed upon reaction of nitrite and ethanol under gastric conditions
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Nitrate–Nitrite–Nitric Oxide Pathway in Pulmonary Arterial Hypertension Therapeutics
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Acid-Induced Structural Modifications of Unsaturated Fatty Acids and Phenolic Olive Oil Constituents by Nitrite Ions: A Chemical Assessment
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Glutamate receptors modulate sodium‐dependent and calcium‐independent vitamin C bidirectional transport in cultured avian retinal cells
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Pepsin is nitrated in the rat stomach, acquiring antiulcerogenic activity: A novel interaction between dietary nitrate and gut proteins
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Evidence for a pathway that facilitates nitric oxide diffusion in the brain
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Diffusion of nitric oxide through the gastric wall upon reduction of nitrite by red wine: Physiological impact
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Studies in the hydrolysis and alcoholysis of some organic nitrites
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“derivatives or, due to the high oxygen tension in the stomach (≈70 Torr [22]), NO may be oxidized to NO2 which, in turn, can combine with the phenoxyl radicals yielding nitrated phenols [23].”
Background
The Nitrate–Nitrite–Nitric Oxide Pathway in Mammals
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New Therapeutic Strategy for Amino Acid Medicine: Effects of Dietary Glutamate on Gut and Brain Function
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[12] Nitric oxide-cyclic GMP pathway in brain slices
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Electrochemical sensors and biosensors based on redox polymer/carbon nanotube modified electrodes: A review
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Gastric S-nitrosothiol formation drives the antihypertensive effects of oral sodium nitrite and nitrate in a rat model of renovascular hypertension
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Effects of Citrulline Supplementation on Exercise Performance in Humans: A Review of the Current Literature
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Nitrosative stress in Parkinson’s disease
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Acute beetroot juice supplementation on sympathetic nerve activity: a randomized, double-blind, placebo-controlled proof-of-concept study
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Oxidation and nitrosation of meat proteins under gastro-intestinal conditions: Consequences in terms of nutritional and health values of meat
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Is beetroot juice more effective than sodium nitrate? The effects of equimolar nitrate dosages of nitrate-rich beetroot juice and sodium nitrate on oxygen consumption during exercise
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Putting xanthine oxidoreductase and aldehyde oxidase on the NO metabolism map: Nitrite reduction by molybdoenzymes
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Nitrate from diet might fuel gut microbiota metabolism: Minding the gap between redox signaling and inter-kingdom communication
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Self-citation
Nitrated meat products are associated with mania in humans and altered behavior and brain gene expression in rats
Khambadkone, S. G., Cordner, Z. A., Dickerson, F., Severance, E. G., Prandovszky, E., Pletnikov, M. V., Xiao, J., Li, Y., Boersma, G. J., Talbot, C. C., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0105-6 · Cited by 48 · see citing works
Dietary fibre confers therapeutic effects in a preclinical model of Huntington’s disease
Gubert, C., Kong, G., Costello, C., Adams, C. D., Masson, B. A., Qin, W., Choo, J. M., Narayana, V. K., Rogers, G. B., Renoir, T., et al. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.12.023 · Cited by 45 · see citing works
Dysregulation of stress systems and nitric oxide signaling underlies neuronal dysfunction in Alzheimer’s disease
Spiers, J. G., Chen, H. C., Bourgognon, J.-M., & Steinert, J. R. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.025 · Cited by 45 · see citing works
Reactive Oxygen Species/Reactive Nitrogen Species as Messengers in the Gut: Impact on Physiology and Metabolic Disorders
Abot, A., Fried, S. G., Cani, P. D., & Knauf, C. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0100 · Cited by 46 · see citing works
Simultaneous Determination of Nitrite and Nitrate in Milk Samples by Ion Chromatography Method and Estimation of Dietary Intake
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Discovery of bioactive nitrated lipids and nitro-lipid-protein adducts using mass spectrometry-based approaches
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The role of nitrogen metabolism on polyethylene biodegradation
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The PPARα Regulation of the Gut Physiology in Regard to Interaction with Microbiota, Intestinal Immunity, Metabolism, and Permeability
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Biological role of nitrite and nitric oxide in the stomach: from diet to protein tyrosine with implications for gastric physiology
Rocha, B. S. (2012) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
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Authors: Pereira, C., Ferreira, N. R., Rocha, B. S., Barbosa, R. M., & Laranjinha, J.
Affiliations: Centro de Neurociências e Biologia Celular (PT)
Corresponding author: Laranjinha, João
ORCID: Pereira, Cassilda
Ferreira, Nuno R.
Rocha, Bárbara S.
Barbosa, Rui M.
Laranjinha, João
Venue: Redox Biology
Publisher: Elsevier BV
Published: 2013
Volume: 1
Issue: 1
Pages: 276-284
ISSN: 2213-2317 (ISSN-L)
DOI: 10.1016/j.redox.2013.04.004
PMC: PMC3757698
OpenAlex: W2050609518
Cited by: 92
References: 135
Citations by year: 2026: 7 · 2025: 10 · 2024: 8 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 9 · 2019: 5 · 2018: 8 · 2017: 9 · 2016: 6 · 2015: 7 · 2014: 1 · 2013: 1
FWCI: 0.55
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/3.0/ (vor, 196 d)
Locations: Redox Biology (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by-nc-nd)
Funders: Fundação para a Ciência e Tecnologia (Portugal) (PTDC/AGR-ALI/115744/2009, PTDC/SAU-NEU/108992/2008, PTDC/SAU-NEU/103538/2008)
CNC (PEst-C/SAU/LA0001/2011)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
Keywords: nitrite, nitric oxide, redox conversion, nitrate, gut-brain axis, polyphenols, vitamin C, glutamate, enteric nervous system, oxygen partial pressure, post-translational modification, brain homeostasis, glutamatergic synapses
MeSH terms: Animals, Brain, Humans, Nitric Oxide, Nitrites, Oxidation-Reduction, Gastrointestinal Tract

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The redox interplay between nitrite and nitric oxide: From the gut to the brain

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