Cited by 1,957Nitric Oxide and Endothelin EffectsCardiovascular Health and Disease PreventionEicosanoids and Hypertension Pharmacology

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Endothelial Nitric Oxide Synthase in Vascular Disease: From Marvel to Menace

Förstermann, Ulrich, Münzel, Thomas·2006·Circulation

DOI 10.1161/circulationaha.105.602532

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Abstract

Nitric oxide (NO·) is an important protective molecule in the vasculature, and endothelial NO· synthase (eNOS) is responsible for most of the vascular NO· produced. A functional eNOS oxidizes its substrate l -arginine to l -citrulline and NO·. This normal function of eNOS requires dimerization of the enzyme, the presence of the substrate l -arginine, and the essential cofactor (6 R )-5,6,7,8-tetrahydro- l -biopterin (BH 4 ), one of the most potent naturally occurring reducing agents. Cardiovascular risk factors such as hypertension, hypercholesterolemia, diabetes mellitus, or chronic smoking stimulate the production of reactive oxygen species in the vascular wall. Nicotinamide adenine dinucleotide phosphate (NADPH) oxidases represent major sources of this reactive oxygen species and have been found upregulated and activated in animal models of hypertension, diabetes, and sedentary lifestyle and in patients with cardiovascular risk factors. Superoxide (O 2 · − ) reacts avidly with vascular NO· to form peroxynitrite (ONOO − ). The cofactor BH 4 is highly sensitive to oxidation by ONOO − . Diminished levels of BH 4 promote O 2 · − production by eNOS (referred to as eNOS uncoupling). This transformation of eNOS from a protective enzyme to a contributor to oxidative stress has been observed in several in vitro models, in animal models of cardiovascular diseases, and in patients with cardiovascular risk factors. In many cases, supplementation with BH 4 has been shown to correct eNOS dysfunction in animal models and patients. In addition, folic acid and infusions of vitamin C are able to restore eNOS functionality, most probably by enhancing BH 4 levels as well.

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10.1161/res.86.3.347 · DOI
Li H Witte K August M Brausch I Gödtel-Armbrust U Habermeier A Closs EI Oelze M Münzel T Förstermann U. Reversal of eNOS uncoupling and upregulation of eNOS expression lowers blood pressure in hypertensive rats. J Am Coll Cardiol. In press.
10.1161/res.88.2.e14 · DOI
10.1161/circ.99.15.2027 · DOI
10.1161/res.86.5.494 · DOI
10.1161/circ.94.11.2756 · DOI
10.1161/circ.101.11.1261 · DOI
10.1161/circ.100.21.2131 · DOI
10.1161/hyp.30.1.57 · DOI
10.1161/res.77.3.510 · DOI
10.1161/circ.103.9.1282 · DOI
10.1161/hyp.33.6.1353 · DOI
10.1161/res.86.1.e7 · DOI
10.1161/res.86.2.e36 · DOI
10.1161/circ.104.10.1119 · DOI
10.1161/res.87.2.99 · DOI
10.1161/res.87.7.566 · DOI
10.1161/hyp.38.5.1044 · DOI
10.1161/circ.104.22.2673 · DOI
10.1161/circ.94.1.6 · DOI
10.1161/circ.97.3.237 · DOI
10.1161/atvb.22.1.6 · DOI
10.1161/atvb.20.1.185 · DOI

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BackgroundInfluential
Effect of trelagliptin on vascular endothelial functions and serum adiponectin level in patients with type 2 diabetes: a preliminary single-arm prospective pilot study
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“Detailed description of the formation of O 2 (cid:2) - from uncoupled eNOS has been explained by Forstermann and Munzel (70).”
Meta-analysis on the Effect of Mild Primary Hyperparathyroidism and Parathyroidectomy Upon Arterial Stiffness
Bernardi, S., Giudici, F., Barbato, V., Zanatta, L., Grillo, A., & Fabris, B. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab157 · Cited by 32
Paracrine Shear-Stress-Dependent Signaling from Endothelial Cells Affects Downstream Endothelial Function and Inflammation
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Pulmonary hypertension and vascular oxidative damage in cigarette smoke exposed eNOS−/−mice and human smokers
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Platelet Hyperaggregability: Impaired Responsiveness to Nitric Oxide (“Platelet NO Resistance”) as a Therapeutic Target
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COX-2-Derived Prostanoids and Oxidative Stress Additionally Reduce Endothelium-Mediated Relaxation in Old Type 2 Diabetic Rats
Vessières, E., Guihot, A., Toutain, B., Maquigneau, M., Fassot, C., Loufrani, L., & Henrion, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068217 · Cited by 35
“Dimerization of the enzyme is a key step in the production of NO [13,52] and eNOS dimerization is strongly reduced in ZDF rats’ mesenteric arteries [53].”
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The chemical biology of nitric oxide — an outsider's reflections about its role in osteoarthritis
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Vascular endothelial-cadherin downregulation as a feature of endothelial transdifferentiation in monocrotaline-induced pulmonary hypertension
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Silencing salusin β ameliorates heart failure in aged spontaneously hypertensive rats by ROS-relative MAPK/NF-κB pathways in the paraventricular nucleus
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Vasoplegia: A Review
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Direct evidence that (−)-epicatechin increases nitric oxide levels in human endothelial cells
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“Defects in generation of NO are associated with increased risk for cardiovascular disease [ 4 , 5]. Cardioprotective effects of cocoa, improvement of endothelial function, and lowering of blood pressure are attributed to flavanol-mediated elevation of the NO level [6, 7]. Vasodilatory activity was also observed after…”
Notoginsenoside Ft1 activates both glucocorticoid and estrogen receptors to induce endothelium-dependent, nitric oxide-mediated relaxations in rat mesenteric arteries
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Autocrine VEGF Isoforms Differentially Regulate Endothelial Cell Behavior
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BackgroundInfluential
LAV-BPIFB4 isoform modulates eNOS signalling through Ca2+/PKC-alpha-dependent mechanism
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Protocol of a randomised controlled trial in cardiac surgical patients with endothelial dysfunction aimed to prevent postoperative acute kidney injury by administering nitric oxide gas
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The Role of Antioxidants in the Prevention of Cadmium-Induced Endothelial Dysfunction
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The Role of Single-Nucleotide Variants of NOS1, NOS2, and NOS3 Genes in the Comorbidity of Arterial Hypertension and Tension-Type Headache
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“In addition to NO production, eNOS can function in an uncoupled manner and produce ROS when the available stores of BH4 are removed or oxidized, l-arginine is depleted, or the eNOS inhibitor asymmetric dimethyl-l-arginine is overexpressed [9,10].”
Background
ACE Inhibitory Peptide from Skin Collagen Hydrolysate of Takifugu bimaculatus as Potential for Protecting HUVECs Injury
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“ROS-producing systems in the vascular wall are dominated by NADPH oxidase (NOX), xanthine oxidase (XO), and uncoupled nitric oxide synthase (NOS) and the uncoupling of eNOS contributes markedly to increased ROS production [58].”
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Design of biodegradable 3D-printed cardiovascular stent
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mTOR contributes to endothelium-dependent vasorelaxation by promoting eNOS expression and preventing eNOS uncoupling
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Blood pressure variability, impaired autonomic function and vascular senescence in aged spontaneously hypertensive rats are ameliorated by angiotensin blockade
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Effects of 5-Cyclopropyl-2-[1-(2-fluoro-benzyl)-1 H-pyrazolo[3,4-b]pyridine-3-yl]pyrimidin-4-ylamine (BAY 41-2272) on Smooth Muscle Tone, Soluble Guanylyl Cyclase Activity, and NADPH Oxidase Activity/Expression in Corpus Cavernosum from Wild-Type, Neuronal, and Endothelial Nitric-Oxide Synthase Null Mice
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“Superoxide reacts with NO to form peroxynitrite and other reactive nitrogen species, resulting in a diminished NO bioavailability (Jeremy et al., 2002; Förstermann and Münzel, 2006).”
Background
Endothelial Nitric Oxide Synthase and Superoxide Mediate Hemodynamic Initiation of Intracranial Aneurysms
Liaw, N., Fox, J. M., Siddiqui, A. H., Meng, H., & Kolega, J. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101721 · Cited by 31
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Homocysteine, Paraoxonase-1 and Vascular Endothelial Dysfunction: Omnibus viis Romam Pervenitur
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Endothelial nitric oxide synthase tagSNPs influence the effects of enalapril in essential hypertension
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Effect of exercise intensity on postprandial lipemia, markers of oxidative stress, and endothelial function after a high-fat meal
Krüger, R. L., Teixeira, B. C., Farinha, J. B., Macedo, R. C. O., Boeno, F. P., Rech, A., López, P., Pinto, R. S., & Reischak-Oliveira, Á. (2016) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2016-0262 · Cited by 31
Relation of Elevated Serum Uric Acid Level to Endothelial Dysfunction in Patients with Acute Coronary Syndrome
Saito, Y., Kitahara, H., Nakayama, T., Fujimoto, Y., & Kobayashi, Y. (2018) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.45179 · Cited by 31
Role of endothelial-derived nitric oxide in hypertension and renal disease
Marin, E. P., & Sessa, W. C. (2007) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0b013e328017f893 · Cited by 31
Molecular, genetic and epigenetic pathways of peroxynitrite-induced cellular toxicity
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“ISSN: 1337-6853 (print version) | 1337-9569 (electronic version) response and vascular events (Forstermann and Munzel, 2006; Pacher et al., 2007).”
Plasma Arginine/Asymmetric Dimethylarginine Ratio and Incidence of Cardiovascular Events: A Case-Cohort Study
Yu, E., Ruiz-Canela, M., Hu, F. B., Clish, C. B., Corella, D., Salas-Salvadó, J., Hruby, A., Fitó, M., Liang, L., Toledo, E., et al. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3569 · Cited by 30
Diosmin and its glycocalyx restorative and anti‐inflammatory effects on injured blood vessels
Mitra, R., Nersesyan, A., Pentland, K., Melin, M. M., Levy, R. M., & Ebong, E. E. (2022) · The FASEB Journal · doi:10.1096/fj.202200053rr · Cited by 30
Targeting endothelial cells with golden spice curcumin: A promising therapy for cardiometabolic multimorbidity
Tang, F., Liu, D., Zhang, L., Xu, L.-Y., Zhang, J., Zhao, X., Ao, H., & Peng, C. Y. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106953 · Cited by 32
Sulphur mustard induces time- and concentration-dependent regulation of NO-synthesizing enzymes
Steinritz, D., Elischer, A., Balszuweit, F., Gonder, S., Heinrich, A., Bloch, W., Thiermann, H., & Kehe, K. (2009) · Toxicology Letters · doi:10.1016/j.toxlet.2009.04.012 · Cited by 30
Potential role of antioxidants in the treatment of portal hypertension
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Effects of aerobic exercise training on metabolism of nitric oxide and endothelin-1 in lung parenchyma of rats with pulmonary arterial hypertension
Zimmer, A., Teixeira, R. B., Bonetto, J. H. P., Siqueira, R., Carraro, C. C., Donatti, L. M., Hickmann, A. R., Litvin, I. E., Godoy, A. E. G., Araújo, A. S. D. R., et al. (2017) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-016-2937-1 · Cited by 30
“In this case, and in the presence of reactive species, NO can react rapidly with O2 to generate peroxynitrite (ONOO−), dramatically increasing oxidative damage [2, 9, 17] and aggravating endothelial dysfunction.”
Use of Computational Biochemistry for Elucidating Molecular Mechanisms of Nitric Oxide Synthase
Bignon, E., Rizza, S., Filomeni, G., & Papaleo, E. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.03.011 · Cited by 30
“…mainly in vascular endothelium to guarantee vasorelaxation [23,24], cellular proliferation, white blood cells adhesion, and platelet aggregation [24,25]. cNOSs exert their functions functions mainly by producing low, controlled ﬂ uxes of NO, whereas iNOS acts mainly as a cytotoxic, antimicrobial…”
Background
Neuroprotective Panel of Olive Polyphenols: Mechanisms of Action, Anti-Demyelination, and Anti-Stroke Properties
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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
Distribution and biomarkers of carbon‐14‐labeled fullerene C60 ([14C(U)]C60) in female rats and mice for up to 30 days after intravenous exposure
Sumner, S., Snyder, R. W., Wingard, C. J., Mortensen, N. P., Holland, N. A., Shannahan, J. H., Dhungana, S., Pathmasiri, W., Han, L., Lewin, A. H., et al. (2015) · Journal of Applied Toxicology · doi:10.1002/jat.3110 · Cited by 30
“eNOS is responsible for most of the vascular NO production, which protects the vasculature from oxidative stress (Forstermann and Munzel, 2006).”
Background
Nitric Oxide- and Heme-Independent Activation of Soluble Guanylate Cyclase Attenuates Peroxynitrite-Induced Endothelial Dysfunction in Rat Aorta
Korkmaz, S., Loganathan, S., Mikles, B., Radovits, T., Barnucz, E., Hirschberg, K., Li, S., Hegedűs, P., Páli, S., Weymann, A., et al. (2012) · Journal of Cardiovascular Pharmacology and Therapeutics · doi:10.1177/1074248412455696 · Cited by 30
“Moreover, in higher concentration, peroxynitrite-mediated oxidation of tetrahydrobiopterin, an essential NO synthase (NOS) cofactor, leads to the dysfunction of NOS, thereby causing endothelial NOS uncoupling.(30) Pharmacological activation of sGC by cinaciguat can potently bind and activate the oxidized and/or heme-f…”
Background
HMG-CoA Reductase Inhibitor Improves Endothelial Dysfunction in Spontaneous Hypertensive Rats Via Down-regulation of Caveolin-1 and Activation of Endothelial Nitric Oxide Synthase
Suh, J., Choi, D., Chang, H., Cho, Y., Youn, T., Chae, I., Kim, K., Kim, C.-H., Kim, H.-S., Oh, B., et al. (2009) · Journal of Korean Medical Science · doi:10.3346/jkms.2010.25.1.16 · Cited by 30
“The impairment of endothelium-dependent dilatation, which is accompanied by the alteration in the expression and/or activity of the endothelial NO synthase, has consistently been observed in conduit arteries and resistance vessels as an effect of hypertension (3, 4).”
Background
Endothelium dependent hyperpolarization-type relaxation compensates for attenuated nitric oxide-mediated responses in subcutaneous arteries of diabetic patients
Mokhtar, S. S., Vanhoutte, P. M., Leung, S. W. S., Yusof, M. I., Sulaiman, W. A. W., Saad, A. Z. M., Suppıan, R., & Rasool, A. H. G. (2016) · Nitric Oxide · doi:10.1016/j.niox.2015.12.007 · Cited by 31
Nanomedical studies of the restoration of nitric oxide/peroxynitrite balance in dysfunctional endothelium by 1,25-dihydroxy vitamin D3 – clinical implications for cardiovascular diseases
Khan, A., Dawoud, H., & Maliñski, T. (2018) · International Journal of Nanomedicine · doi:10.2147/ijn.s152822 · Cited by 30
“excessive O 2 − and ONOO− can oxidize tetrahydrobiopterin, BH 4 , an important cofactor of eNOS and a stabilizer of eNOS dimer.(27,28) In the absence of BH 4 , eNOS produces mostly O 2 −.”
Background
CTRP13 Preserves Endothelial Function by Targeting GTP Cyclohydrolase 1 in Diabetes
Wang, C., Chao, Y., Xu, W., Liang, M., Deng, S., Zhang, D., & Huang, K. (2019) · Diabetes · doi:10.2337/db19-0635 · Cited by 30
“eNOS is responsible for vascular NO production (23).”
Background

Authors: Förstermann, U., & Münzel, T.
Affiliations: From the Departments of Pharmacology (U.F.) and Internal Medicine II (Cardiology) (T.M.), Johannes Gutenberg University Hospitals, Mainz, Germany.
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2006-04-04
Volume: 113
Issue: 13
Pages: 1708-1714
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/circulationaha.105.602532
OpenAlex: W2146190354
Cited by: 1,957
References: 67
Citations by year: 2026: 93 · 2025: 76 · 2024: 99 · 2023: 86 · 2022: 110 · 2021: 113 · 2020: 110 · 2019: 89 · 2018: 105 · 2017: 105 · 2016: 117 · 2015: 101 · 2014: 123 · 2013: 98 · 2012: 85
FWCI: 62.52
Type: journal article
Language: en
Open access: closed
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology (medical) › 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: endothelial nitric oxide synthase, nitric oxide, tetrahydrobiopterin, eNOS uncoupling, NADPH oxidase, reactive oxygen species, superoxide, peroxynitrite, oxidative stress, cardiovascular risk factors, hypertension, hypercholesterolemia, diabetes mellitus, smoking, folic acid, vitamin C, L-arginine
MeSH terms: Animals, Endothelium, Vascular, Humans, Nitric Oxide, Vascular Diseases, Reactive Oxygen Species, Oxidative Stress, Nitric Oxide Synthase Type III

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Endothelial Nitric Oxide Synthase in Vascular Disease: From Marvel to Menace

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