Strategies to increase nitric oxide signalling in cardiovascular disease
Abstract
Nitric oxide (NO) is a key signalling molecule in the cardiovascular, immune and central nervous systems, and crucial steps in the regulation of NO bioavailability in health and disease are well characterized. Although early approaches to therapeutically modulate NO bioavailability failed in clinical trials, an enhanced understanding of fundamental subcellular signalling has enabled a range of novel therapeutic approaches to be identified. These include the identification of: new pathways for enhancing NO synthase activity; ways to amplify the nitrate-nitrite-NO pathway; novel classes of NO-donating drugs; drugs that limit NO metabolism through effects on reactive oxygen species; and ways to modulate downstream phosphodiesterases and soluble guanylyl cyclases. In this Review, we discuss these latest developments, with a focus on cardiovascular disease.
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Three main strategies for increasing NO bioavailability are exercise/diet, drugs that alter enzymatic NO production, and modified polymeric materials that deliver NO exogenously.
“There are three main strategies for increasing NO bioavailability: 1) by participating in physical exercise and controlling certain dietary components (e.g., nitrate-rich diet);132,133 2) by administrating drugs that alter the enzymatic production of NO through nitric oxide synthases (NOSs) and increase the biosynthesis of NO endogenously;117 and 3) by using modified polymeric materials that can”
From Recent advances in thromboresistant and antimicrobial polymers for biomedical applications: just say yes to nitric oxide (NO) (2016) · cites this paper as [132]
Reduced NO levels are associated with high blood pressure, deep vein thrombosis, intimal hypertension, restenosis, endothelial dysfunction, and prolonged wound healing in diabetic patients.
“Reduced NO levels are associated with many health complications and/or diseases, such as high blood pressure, deep vein thrombosis, intimal hypertension, restenosis, endothelial dysfunction, and prolonged wound healing times in diabetic patients, etc.1,131,132”
From Recent advances in thromboresistant and antimicrobial polymers for biomedical applications: just say yes to nitric oxide (NO) (2016) · cites this paper as [132]
Nitrite reduction can generate NO through enzymatic and non-enzymatic pathways.
“Reduction of nitrite can generate NO via both enzymatic (nitrite reductase, xanthine oxidoreductase, etc.) and non-enzymatic (gastrointestinal acid, ascorbate, myoglobin, etc.) pathways.132”
From Recent advances in thromboresistant and antimicrobial polymers for biomedical applications: just say yes to nitric oxide (NO) (2016) · cites this paper as [132]
Procedures such as placing stents, grafts, catheters, or other biomedical devices disrupt endothelial cells and destroy vascular homeostasis.
“However, many procedures (such as placing stents, grafts, catheters, or other biomedical devices) disrupt the endothelial cells lining and destroy the delicate balance of vascular homeostasis.132”
From Recent advances in thromboresistant and antimicrobial polymers for biomedical applications: just say yes to nitric oxide (NO) (2016) · cites this paper as [132]
NO acts directly on smooth muscle cells via activation of soluble guanylyl cyclase leading to formation of cGMP, which promotes smooth muscle relaxation and inhibits platelet function and vascular smooth muscle cell proliferation and migration.
“Chiefly, NO acts directly on smooth muscle cells via activation of soluble guanylyl cyclase leading to formation of the second-messenger, cyclic guanosine monophosphate (cGMP), that in turn promotes smooth muscle relaxation and inhibits both platelet function and vascular smooth muscle cell proliferation and migration[19–21].”
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 [19]
These numbers, along with the relative incidence of CVD and vascular risk factors, support the hypothesis of a possible synergistic, diet-mediated NO-effect between inorganic nitrates and unsaturated fatty acids.
“These numbers, along with the relative incidence of CVD and vascular risk factors support the hypothesis of a possible synergistic, diet-mediated NO-effect between inorganic nitrates and unsaturated fatty acids[19].”
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 [19]
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Regulation of Mitochondrial Respiration by Oxygen and Nitric Oxide
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Arginase inhibition mediates cardioprotection during ischaemia–reperfusion
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Vasculopathy and pulmonary hypertension in sickle cell disease
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Self-citationCross-talk Between Nitrate-Nitrite-NO and NO Synthase Pathways in Control of Vascular NO Homeostasis
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Ethanol Metabolism and Effects: Nitric Oxide and its Interaction
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Endogenous Nitrated Nucleotide Is a Key Mediator of Autophagy and Innate Defense against Bacteria
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Nitric oxide signaling in health and disease
Lundberg, J. O., & Weitzberg, E. (2022) · Cell · doi:10.1016/j.cell.2022.06.010 · Cited by 850 · see citing works
Self-citationPathophysiology of Sickle Cell Disease
Sundd, P., Gladwin, M. T., & Novelli, E. M. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012418-012838 · Cited by 813 · see citing works
Self-citationSources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation
Tejero, J., Shiva, S., & Gladwin, M. T. (2019) · Physiological Reviews · doi:10.1152/physrev.00036.2017 · Cited by 541 · see citing works
Self-citationApplication of Radiosensitizers in Cancer Radiotherapy
Gong, L., Zhang, Y., Liu, C., Zhang, M., & Han, S. (2021) · International Journal of Nanomedicine · doi:10.2147/ijn.s290438 · Cited by 484 · see citing works
Inflammatory Response Mechanisms of the Dentine–Pulp Complex and the Periapical Tissues
Galler, K. M., Weber, M., Korkmaz, Y., Widbiller, M., & Feuerer, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031480 · Cited by 457 · see citing works
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“Likewise, dietary nitrite and nitrate can be reduced by the oral and gut microbial flora to NO, contributing to circulating nitrite levels and mildly lower blood pressure (25, 117); together with the enterosalivary recirculation pathway, this has become known as the mammalian N-oxide cycle (25, 116).”
Metabolic Effects of Dietary Nitrate in Health and Disease
Lundberg, J. O., Carlström, M., & Weitzberg, E. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.007 · Cited by 374 · see citing works
Self-citationEffects of Chlorhexidine mouthwash on the oral microbiome
Bescós, R., Ashworth, A., Clarke, C., Brookes, Z. L. S., Belfield, L., Rodiles, A., Casas‐Agustench, P., Farnham, G., Liddle, L., Burleigh, M. C., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-61912-4 · Cited by 351 · see citing works
Progress and Promise of Nitric Oxide‐Releasing Platforms
Yang, T., Zelikin, A. N., & Chandrawati, R. (2018) · Advanced Science · doi:10.1002/advs.201701043 · Cited by 308 · see citing works
Lai, Y.-C., Tabima, D. M., Dube, J. J., Hughan, K. S., Vanderpool, R. R., Goncharov, D. A., St. Croix, C. M., Garcia-Ocaña, A., Goncharova, E. A., Tofovic, S. P., et al. (2016) · Circulation · doi:10.1161/circulationaha.115.018935 · Cited by 270 · see citing works
“An increasing number of therapeutic approaches, which enhance NO generation and bioactivity, have been proposed over the past decade and include the administration of nitrite and nitrate.(13,14) Recent publications from our group and others have shown that nitrite exhibits therapeutic efficacy in mouse, rat, and sheep…”
BackgroundHeart in space: effect of the extraterrestrial environment on the cardiovascular system
Hughson, R. L., Helm, A., & Durante, M. (2018) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.157 · Cited by 257 · see citing works
Oxidative Stress in Pulmonary Fibrosis
Otoupalova, E., Smith, S., Cheng, G., & Thannickal, V. J. (2020) · Comprehensive physiology · doi:10.1002/cphy.c190017 · Cited by 309 · see citing works
Endothelial dysfunction: molecular mechanisms and clinical implications
Wang, X., & He, B. (2024) · MedComm · doi:10.1002/mco2.651 · Cited by 280 · see citing works
“32 The scope of approved clinical applications remains restricted.”
BackgroundNitric oxide signalling in kidney regulation and cardiometabolic health
Carlström, M. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00429-z · Cited by 264 · see citing works
Wo, Y., Brisbois, E. J., Bartlett, R. H., & Meyerhoff, M. E. (2016) · Biomaterials Science · doi:10.1039/c6bm00271d · Cited by 251 · see citing works
Heme: emergent roles of heme in signal transduction, functional regulation and as catalytic centres
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Nitric oxide: what’s new to NO?
Ghimire, K., Altmann, H. M., Straub, A. C., & Isenberg, J. S. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00315.2016 · Cited by 233 · see citing works
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Enzyme-responsive polymer hydrogels for therapeutic delivery
Chandrawati, R. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216647186 · Cited by 199 · see citing works
Wang, W., Tan, B., Chen, J., Bao, R., Zhang, X., Liang, S., Shang, Y., Liang, W., Cui, Y., Fan, G., et al. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.01.021 · Cited by 189 · see citing works
“Among them, NO is established as a pivotal regulator of a vast number of physiological events, such as endothelial cell growth, migration, vascular remodeling, and angiogenesis [9, 26, 27], all of which are the most important to restore cardiovascular functions [28-30].”
BackgroundKoch, C. D., Gladwin, M. T., Freeman, B. A., Lundberg, J. O., Weitzberg, E., & Morris, A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.12.015 · Cited by 186 · see citing works
“possible synergistic, diet-mediated NO-effect between inorganic nitrates and unsaturated fatty acids [19].”
BackgroundSelf-citationSoluble Guanylate Cyclase Stimulators and Activators
Sandner, P., Zimmer, D. P., Milne, G. T., Follmann, M., Hobbs, A. J., & Stasch, J. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_197 · Cited by 183 · see citing works
“…channels, and phosphodiesterases, making the NO/sGC/cGMP signaling a central vasoprotective signaling pathway (Lucas et al. 2000; Feil et al. 2003; Lundberg et al. 2015). sGC is a key signal-transduction enzyme in the cardiovascular system, and many cardiovascular diseases, such as hypertension,…”
BackgroundHydrogen sulfide, an enhancer of vascular nitric oxide signaling: mechanisms and implications
Szabó, C. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00282.2016 · Cited by 179 · see citing works
“, nitrite) and can be regenerated from it under certain conditions (59, 76, 77), H2S converts into thiosulfate, which can regenerate biologically active H2S (79, 117, 141).”
BackgroundTian, H., Qian, M., Zhang, Y., Liu, Q., Midgley, A. C., Liu, Y., Che, Y., Hou, J., & Zhao, Q. (2022) · Advanced Science · doi:10.1002/advs.202105408 · Cited by 173 · see citing works
Erythrocytes and Vascular Function: Oxygen and Nitric Oxide
Helms, C. C., Gladwin, M. T., & Kim‐Shapiro, D. B. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00125 · Cited by 166 · see citing works
“This is only a very small selection of a strong body of work that displays the role of NO in vascular function, which has been recently reviewed (Lundberg et al., 2015).”
BackgroundSelf-citationNitrite and nitrate chemical biology and signalling
DeMartino, A. W., Kim‐Shapiro, D. B., Patel, R. P., & Gladwin, M. T. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14484 · Cited by 156 · see citing works
“Indeed, to date, several preclinical animal model studies have demonstrated that nitrite administered during the ischaemia phase or very soon thereafter affords protection (see more detail in Lundberg et al., 2009, 2015; Calvert and Lefer, 2010; Vitturi and Patel, 2011).”
BackgroundSelf-citationWang, C., Lundh, M., Fu, A., Kriszt, R., Huang, T. L., Lynes, M. D., Leiria, L. O., Shamsi, F., Darcy, J., Greenwood, B. P., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aaz8664 · Cited by 148 · see citing works
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Effects of chlorhexidine mouthwash on the oral microbiome
Brookes, Z. L. S., Belfield, L., Ashworth, A., Casas‐Agustench, P., Raja, M., Pollard, A. J., & Bescós, R. (2021) · Journal of Dentistry · doi:10.1016/j.jdent.2021.103768 · Cited by 154 · see citing works
Microplasma Bubbles: Reactive Vehicles for Biofilm Dispersal
Zhou, R., Zhou, R., Wang, P., Luan, B., Zhang, X., Fang, Z. M., Xian, Y., Lu, X., Ostrikov, K., & Bazaka, K. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b03961 · Cited by 138 · see citing works
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Mitochondrial Dysfunction in Adipocytes as a Primary Cause of Adipose Tissue Inflammation
Woo, C.-Y., Jang, J. E., Lee, S. E., Koh, E. H., & Lee, K. (2019) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2018.0221 · Cited by 126 · see citing works
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Reciprocal regulation of eNOS and caveolin-1 functions in endothelial cells
Chen, Z., Oliveira, S. D., Zimnicka, A. M., Jiang, Y., Sharma, T., Chen, S., Lazarov, O., Bonini, M. G., Haus, J. M., & Minshall, R. D. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-01-0049 · Cited by 121 · see citing works
“The activity of eNOS in endothelial cells (ECs) is enhanced by agonists such as acetylcholine (ACh), bradykinin, and histamine, which increase intracellular calcium (Ca2+), whereas hemodynamic shear stress and hormones such as insulin and plasma albumin increase eNOS-derived NO production independent of changes in int…”
BackgroundInfluentialThe Microbiome and Blood Pressure: Can Microbes Regulate Our Blood Pressure?
Khodor, S. A., Reichert, B., & Shatat, I. F. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00138 · Cited by 120 · see citing works
“NO acts directly on smooth muscle cells to promote relaxation and inhibits both platelet function and vascular smooth muscle cell proliferation and migration (78).”
BackgroundPhenotypic Consequences of a Genetic Predisposition to Enhanced Nitric Oxide Signaling
Emdin, C. A., Khera, A. V., Klarin, D. M., Natarajan, P., Zekavat, S. M., Nomura, A., Haas, M. E., Aragam, K. G., Ardissino, D., Wilson, J. G., et al. (2017) · Circulation · doi:10.1161/circulationaha.117.028021 · Cited by 119 · see citing works
“These variants were selected because: (1) they have been robustly associated with blood”
BackgroundMethodTargeted delivery of nitric oxide via a ‘bump-and-hole’-based enzyme–prodrug pair
Hou, J., Pan, Y., Zhu, D., Fan, Y., Feng, G., Wei, Y., Wang, H., Qin, K., Zhao, T., Yang, Q., et al. (2018) · Nature Chemical Biology · doi:10.1038/s41589-018-0190-5 · Cited by 117 · see citing works
Nitric Oxide Signaling and Regulation in the Cardiovascular System: Recent Advances
Carlström, M., Weitzberg, E., & Lundberg, J. O. (2024) · Pharmacological Reviews · doi:10.1124/pharmrev.124.001060 · Cited by 103 · see citing works
Self-citationCovid-19 accelerates endothelial dysfunction and nitric oxide deficiency
Green, S. J. (2020) · Microbes and Infection · doi:10.1016/j.micinf.2020.05.006 · Cited by 113 · see citing works
Nitric Oxide to Fight Viral Infections
Lisi, F., Zelikin, A. N., & Chandrawati, R. (2021) · Advanced Science · doi:10.1002/advs.202003895 · Cited by 101 · see citing works
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Riociguat: Mode of Action and Clinical Development in Pulmonary Hypertension
Ghofrani, H. A., Humbert, M. J. C., Langleben, D., SCHERMULY, R. T., Stasch, J., Wilkins, M. R., & Klinger, J. R. (2016) · CHEST Journal · doi:10.1016/j.chest.2016.05.024 · Cited by 102 · see citing works
“To this end, recent efforts have centered on identifying pharmacologic agents that enhance sGC-induced cGMP synthesis directly.(50,58-60) sGC stimulators such as riociguat have a dual mode of action that enhances sGC response to endogenous NO and directly stimulates sGC independent of NO binding.”
BackgroundVegetable-derived bioactive nitrate and cardiovascular health
Bondonno, C. P., Blekkenhorst, L. C., Liu, A. H., Bondonno, N. P., Ward, N. C., Croft, K. D., & Hodgson, J. M. (2018) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.08.001 · Cited by 101 · see citing works
Nitric Oxide-Loaded Antimicrobial Polymer for the Synergistic Eradication of Bacterial Biofilm
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Targeting Nitric Oxide with Natural Derived Compounds as a Therapeutic Strategy in Vascular Diseases
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“Currently, the best strategy is based on the drugs administration in order to activate downstream effectors of eNOS/NO from one side and to reduce eNOS uncoupling [16], improving BH 4 and L-arginine bioavailability and regulating post-translational modifications of eNOS, from the other side.”
BackgroundCordero‐Herrera, I., Kozyra, M., Zhuge, Z., Haworth, S. M., Moretti, C. H., Peleli, M., Caldeira-Dias, M., Jahandideh, A., Huirong, H., Cruz, J. C., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809406115 · Cited by 99 · see citing works
“One such candidate mechanism, linking cardiometabolic disease in humans, is impaired nitric oxide (NO) bioavailability and signaling (4, 5).”
BackgroundSelf-citationThi, T. T. H., Lee, Y., Thi, P. L., & Park, K. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.12.005 · Cited by 78 · see citing works
Nitric oxide and cyclic GMP functions in bone
Kalyanaraman, H., Schall, N., & Pilz, R. B. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.03.007 · Cited by 94 · see citing works
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“Nitrite in swallowed saliva is then absorbed, and, upon entry into the systemic circulation, further reduced to NO by metalloproteins (e.g., hemoglobin and deoxyhemoglobin), enzymes (e.g., xanthine oxidoreductase) and other compounds with redox potential (e.g., polyphenols) [5–7].”
InfluentialBlood Pressure–Lowering Effect of Orally Ingested Nitrite Is Abolished by a Proton Pump Inhibitor
Montenegro, M. F., Sundqvist, M. L., Larsen, F. J., Zhuge, Z., Carlström, M., Weitzberg, E., & Lundberg, J. O. (2017) · Hypertension · doi:10.1161/hypertensionaha.116.08081 · Cited by 102 · see citing works
Self-citationAnti-obesity and anti-diabetic effects of nitrate and nitrite
Ghasemi, A., & Jeddi, S. (2017) · Nitric Oxide · doi:10.1016/j.niox.2017.08.003 · Cited by 89 · see citing works
Blekkenhorst, L. C., Bondonno, N. P., Liu, A. H., Ward, N. C., Prince, R. L., Lewis, J. R., Devine, A., Croft, K. D., Hodgson, J. M., & Bondonno, C. P. (2018) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqx046 · Cited by 89 · see citing works
“The regulation of eNOS activity is via intracellular 105 calcium (Ca2+) (18) and several signal transduction pathways, including phosphoinoside 3106 kinase (PI3K) and adenylate cyclase (AC) pathways (19).”
BackgroundGut microbiota, hypertension and chronic kidney disease: Recent advances
Sircana, A., Michieli, F. D., Parente, R., Framarin, L., Leone, N., Berrutti, M., Paschetta, E., Bongiovanni, D., & Musso, G. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.01.013 · Cited by 86 · see citing works
Montenegro, M. F., Sundqvist, M. L., Nihlén, C., Hezel, M. P., Carlström, M., Weitzberg, E., & Lundberg, J. O. (2016) · Redox Biology · doi:10.1016/j.redox.2016.10.011 · Cited by 87 · see citing works
“This is apparently a very powerful system allowing much nitrate to be reduced to nitrite by oral bacteria, eventually giving rise to a number of potentially bioactive nitrogen oxides [17].”
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- Authors
- Lundberg, J. O., Gladwin, M. T., & Weitzberg, E.
- Affiliations
- Karolinska Institutet (SE)
- University of Pittsburgh (US)
- Corresponding author
- Lundberg, Jon O.
- Gladwin, Mark T.
- Weitzberg, Eddie
- Venue
- Nature Reviews Drug Discovery
- Published
- 2015-08-07
- Volume
- 14
- Issue
- 9
- Pages
- 623-641
- ISSN
- 1474-1776 (ISSN-L)
- 1474-1784
- OpenAlex
- W1119734502
- Cited by
- 576
- References
- 269
- Citations by year
- 2026: 27 · 2025: 55 · 2024: 48 · 2023: 46 · 2022: 69 · 2021: 55 · 2020: 65 · 2019: 46 · 2018: 62 · 2017: 57 · 2016: 44 · 2015: 2
- FWCI
- 6.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Drug Discovery (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P01HL103455, T32HL007563, R01HL125886, R01HL098032, T32HL110849)
- Topics
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Eicosanoids and Hypertension Pharmacology
- Keywords
- nitric oxide signaling, nitric oxide bioavailability, cardiovascular disease, nitric oxide synthase, nitrate-nitrite-nitric oxide pathway, reactive oxygen species, phosphodiesterase, soluble guanylate cyclase
- MeSH terms
- Animals, Cardiovascular Diseases, Humans, Nitric Oxide, Signal Transduction, Reactive Oxygen Species, Risk Reduction Behavior
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