eNOS Uncoupling in Cardiovascular Diseases - the Role of Oxidative Stress and Inflammation

Karbach, Susanne; Wenzel, Philip; Waisman, Ari; Munzel, Thomas; Daiber, Andreas

doi:10.2174/13816128113196660748

Cited by 307Nitric Oxide and Endothelin EffectsCardiovascular Health and Disease PreventionRedox biology and oxidative stress

eNOS Uncoupling in Cardiovascular Diseases - the Role of Oxidative Stress and Inflammation

Karbach, Susanne, Wenzel, Philip, Waisman, Ari, Munzel, Thomas, Daiber, Andreas·2014·Current Pharmaceutical Design

DOI 10.2174/13816128113196660748

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Abstract

Many cardiovascular diseases and drug-induced complications are associated with - or even based on - an imbalance between the formation of reactive oxygen and nitrogen species (RONS) and antioxidant enzymes catalyzing the break-down of these harmful oxidants. According to the "kindling radical" hypothesis, the formation of RONS may trigger in certain conditions the activation of additional sources of RONS. According to recent reports, vascular dysfunction in general and cardiovascular complications such as hypertension, atherosclerosis and coronary artery diseases may be connected to inflammatory processes. The present review is focusing on the uncoupling of endothelial nitric oxide synthase (eNOS) by different mechanisms involving so-called "redox switches". The oxidative depletion of tetrahydrobiopterin (BH4), oxidative disruption of the dimeric eNOS complex, S-glutathionylation and adverse phosphorylation as well as RONS-triggered increases in levels of asymmetric dimethylarginine (ADMA) will be discussed. But also new concepts of eNOS uncoupling and state of the art detection of this process will be described. Another part of this review article will address pharmaceutical interventions preventing or reversing eNOS uncoupling and thereby normalize vascular function in a given disease setting. We finally turn our attention to the inflammatory mechanisms that are also involved in the development of endothelial dysfunction and cardiovascular disease. Inflammatory cell and cytokine profiles as well as their interactions, which are among the kindling mechanisms for the development of vascular dysfunction will be discussed on the basis of the current literature.

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According to the kindling hypothesis of endothelial dysfunction, initial formation of ROS by other sources can promote uncoupling of NOS, amplifying the initial excess of ROS.
“According to the kindling hypothesis of endothelial dysfunction, the initial formation of ROS by other sources can promote uncoupling of NOS, amplifying the initial excess of ROS (488).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [488]
Uncoupling of eNOS has been noted as a target for therapeutic potential.
“As such, the uncoupling of eNOS has been noted as a target for therapeutic potential (488, 569, 570, 600, 784).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [488]
Increased ROS eventually causes eNOS uncoupling via BH4 depletion, Zn/S cluster breakdown, and other routes, further perpetuating the generation of superoxide and other ROS.
“As discussed in previous section, increased ROS eventually causes eNOS uncoupling via BH4 depletion, Zn/S cluster breakdown, and other routes, further perpetuating the generation of superoxide and other ROS (FIGURE 17) (488, 570).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [488]

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Redox Regulation of Sirtuin-1 by S -Glutathiolation
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Hypochlorous Acid Impairs Endothelium-Derived Nitric Oxide Bioactivity Through a Superoxide-Dependent Mechanism
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Targeted Detoxification of Selected Reactive Oxygen Species in the Vascular Endothelium
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NADPH oxidase inhibitor, apocynin, restores the impaired endothelial‐dependent and ‐independent responses and scavenges superoxide anion in rats with type 2 diabetes complicated by NO dysfunction
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Inducible nitric oxide synthase‐derived superoxide contributes to hypereactivity in small mesenteric arteries from a rat model of chronic heart failure
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Myeloperoxidase (MPO) and Interleukin-17 (IL-17) Plasma Levels are Increased in Patients with Acute Coronary Syndromes
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When the endothelium cannot say ?NO? anymoreADMA, an endogenous inhibitor of NO synthase, promotes cardiovascular disease
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Enhanced Immunoglobulin Formation of Immortalized B Cells From Hypertensive Patients
Rosskopf, D., Hartung, K., Hense, J., & Siffert, W. (1995) · Hypertension · doi:10.1161/01.hyp.26.3.432 · Cited by 20 · see citing works
Xanthine oxidoreductase: dehydrogenase to oxidase conversion
RYAN, M. G., BALENDRAN, A., HARRISON, R., WOLSTENHOLME, A., & BULKLEY, G. B. (1997) · Biochemical Society Transactions · doi:10.1042/bst025530s · Cited by 13 · see citing works
Genetic B Lymphocyte Deficiency Attenuates Cold‐induced Hypertension
Wang, X., Stormont, R., Liu, X., Brock, A. J., Stewart, M., & Sun, Z. (2010) · The FASEB Journal · doi:10.1096/fasebj.24.1_supplement.792.6 · Cited by 1 · see citing works

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Endothelial Dysfunction in Atherosclerotic Cardiovascular Diseases and Beyond: From Mechanism to Pharmacotherapies
Xu, S., Ilyas, I., Little, P. J., Li, H., Kamato, D., Zheng, X., Luo, S., Li, Z., Liu, P., Han, J., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000096 · Cited by 1,167 · see citing works
Vascular Inflammation and Oxidative Stress: Major Triggers for Cardiovascular Disease
Steven, S., Frenis, K., Oelze, M. W., Kalinovic, S., Kuntić, M., Jiménez, M. T. B., Vujačić-Mirski, K., Helmstädter, J., Kröller‐Schön, S., Münzel, T. F., et al. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/7092151 · Cited by 729 · see citing works
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Reactive oxygen species (ROS) in macrophage activation and function in diabetes
Rendra, E., Riabov, V., Mossel, D. M., Sevastyanova, T., Harmsen, M. C., & Kzhyshkowska, J. (2019) · Immunobiology · doi:10.1016/j.imbio.2018.11.010 · Cited by 636 · see citing works
Nitric Oxide and Endothelial Dysfunction
Cyr, A. R., Huckaby, L. V., Shiva, S. S., & Zuckerbraun, B. S. (2020) · Critical Care Clinics · doi:10.1016/j.ccc.2019.12.009 · Cited by 674 · see citing works
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Sources 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
Targeting vascular (endothelial) dysfunction
Daiber, A., Steven, S., Weber, A., Shuvaev, V. V., Muzykantov, V. R., Laher, I., Li, H., Lamas, S., & Münzel, T. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13517 · Cited by 501 · see citing works
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Endothelial dysfunction and preeclampsia: role of oxidative stress
Sanchez-Aranguren, L. C., Prada, C. E., RiaÃ±o-Medina, C. E., & López, M. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00372 · Cited by 439 · see citing works
COVID-19 pandemic: the effects of quarantine on cardiovascular risk
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Endothelial dysfunction due to eNOS uncoupling: molecular mechanisms as potential therapeutic targets
Janaszak-Jasiecka, A., Płoska, A., Wierońska, J. M., Dobrucki, L. W., & Kalinowski, L. (2023) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-023-00423-2 · Cited by 358 · see citing works
The Contribution of Homocysteine Metabolism Disruption to Endothelial Dysfunction: State-of-the-Art
Esse, R., Barroso, M., de Almeida, I. T., & Castro, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040867 · Cited by 337 · see citing works
Emerging Roles of the Mineralocorticoid Receptor in Pathology: Toward New Paradigms in Clinical Pharmacology
Jaisser, F., & Farman, N. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.011106 · Cited by 332 · see citing works
Endothelial Dysfunction: Clinical Implications in Cardiovascular Disease and Therapeutic Approaches
Park, K., & Park, W. J. (2015) · Journal of Korean Medical Science · doi:10.3346/jkms.2015.30.9.1213 · Cited by 327 · see citing works
European contribution to the study of ROS: A summary of the findings and prospects for the future from the COST action BM1203 (EU-ROS)
Egea, J., Fabregat, I., Frapart, Y., Ghezzi, P., Görlach, A., Kietzmann, T., Kubaichuk, K. I., Knaus, U. G., López, M. G., González, G. O., et al. (2017) · Redox Biology · doi:10.1016/j.redox.2017.05.007 · Cited by 311 · see citing works
New Therapeutic Implications of Endothelial Nitric Oxide Synthase (eNOS) Function/Dysfunction in Cardiovascular Disease
Daiber, A., Xia, N., Steven, S., Oelze, M. W., Hanf, A., Kröller‐Schön, S., Münzel, T. F., & Li, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20010187 · Cited by 312 · see citing works
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The use of human umbilical vein endothelial cells (HUVECs) as an in vitro model to assess the toxicity of nanoparticles to endothelium: a review
Cao, Y., Gong, Y. L., Liu, L., Zhou, Y., Fang, X., Zhang, C., Li, Y., & Li, J. (2017) · Journal of Applied Toxicology · doi:10.1002/jat.3470 · Cited by 282 · see citing works
Effects of noise on vascular function, oxidative stress, and inflammation: mechanistic insight from studies in mice
Münzel, T. F., Daiber, A., Steven, S., Tran, L. P., Ullmann, E., Kossmann, S., Schmidt, F. P., Oelze, M. W., Xia, N., Li, H., et al. (2017) · European Heart Journal · doi:10.1093/eurheartj/ehx081 · Cited by 285 · see citing works
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Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function
Daiber, A., Lisa, F. D., Oelze, M. W., Kröller‐Schön, S., Steven, S., Schulz, E., & Münzel, T. F. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13403 · Cited by 271 · see citing works
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Mitochondrial ROS Formation in the Pathogenesis of Diabetic Cardiomyopathy
Kaludercic, N., & Lisa, F. D. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.00012 · Cited by 264 · see citing works
Endothelial dysfunction: molecular mechanisms and clinical implications
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Mitochondrial Oxidative Stress, Mitochondrial DNA Damage and Their Role in Age-Related Vascular Dysfunction
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Cellular and Oxidative Mechanisms Associated with Interleukin-6 Signaling in the Vasculature
Didion, S. P. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122563 · Cited by 235 · see citing works
Antioxidants in Translational Medicine
Schmidt, H. H. H. W., Stocker, R., Vollbracht, C., Paulsen, G., Riley, D. P., Daiber, A., & Cuadrado, A. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6393 · Cited by 231 · see citing works
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Health Benefits of Fasting and Caloric Restriction
Golbidi, S., Daiber, A., Korać, B., Li, H., Essop, M. F., & Laher, I. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0951-7 · Cited by 218 · see citing works
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Hyperuricemia and Cardiovascular Disease
Zhang, S., Wang, Y., Cheng, J., Huangfu, N., Zhao, R., Xu, Z., Zhang, F.-X., Zheng, W., & Zhang, D. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190408122557 · Cited by 210 · see citing works
Redox Regulation of Inflammation: Old Elements, a New Story
Lei, Y., Wang, K., Deng, L., Chen, Y., Nice, E. C., & Huang, C. (2014) · Medicinal Research Reviews · doi:10.1002/med.21330 · Cited by 208 · see citing works
Circulating Oxidative Stress Biomarkers in Clinical Studies on Type 2 Diabetes and Its Complications
Bigagli, E., & Lodovici, M. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/5953685 · Cited by 195 · see citing works
Endothelial Dysfunction Driven by Hypoxia—The Influence of Oxygen Deficiency on NO Bioavailability
Janaszak‐Jasiecka, A., Siekierzycka, A., Płoska, A., Dobrucki, I. T., & Kalinowski, L. (2021) · Biomolecules · doi:10.3390/biom11070982 · Cited by 189 · see citing works
Redox regulation of genome stability by effects on gene expression, epigenetic pathways and DNA damage/repair
Mikhed, Y., Görlach, A., Knaus, U. G., & Daiber, A. (2015) · Redox Biology · doi:10.1016/j.redox.2015.05.008 · Cited by 181 · see citing works
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Revisiting pharmacology of oxidative stress and endothelial dysfunction in cardiovascular disease: Evidence for redox-based therapies
Daiber, A., & Chłopicki, S. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.02.026 · Cited by 169 · see citing works
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Redox regulation of cardiovascular inflammation – Immunomodulatory function of mitochondrial and Nox-derived reactive oxygen and nitrogen species
Wenzel, P., Kossmann, S., Münzel, T. F., & Daiber, A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.01.027 · Cited by 158 · see citing works
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Endothelial Dysfunction and Its Clinical Implications
Poredoš, P., Visnovič-Poredoš, A., & Gregorič, I. D. (2021) · Angiology · doi:10.1177/0003319720987752 · Cited by 161 · see citing works
Oxidative Stress, Antioxidants and Hypertension
Amponsah-Offeh, M., Diaba‐Nuhoho, P., Speier, S., & Morawietz, H. (2023) · Antioxidants · doi:10.3390/antiox12020281 · Cited by 160 · see citing works
Endothelial Microparticles From Acute Coronary Syndrome Patients Induce Premature Coronary Artery Endothelial Cell Aging and Thrombogenicity
Abbas, M., Jesel, L., Auger, C., Amoura, L., Messas, N., Manin, G., Rumig, C., León‐González, A. J., Ribeiro, T. P., da Silva, G. C., et al. (2016) · Circulation · doi:10.1161/circulationaha.116.017513 · Cited by 147 · see citing works
Endothelial Nitric Oxide Synthase (eNOS) and the Cardiovascular System: in Physiology and in Disease States
Nauli, S. M. (2022) · American Journal of Biomedical Science & Research · doi:10.34297/ajbsr.2022.15.002087 · Cited by 143 · see citing works
Redox Regulation via Glutaredoxin-1 and Protein S -Glutathionylation
Matsui, R., Ferrán, B., Oh, A., Croteau, D., Shao, D., Han, J., Pimentel, D. R., & Bachschmid, M. M. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7963 · Cited by 139 · see citing works
Microbiota-derived tryptophan metabolites in vascular inflammation and cardiovascular disease
Paeslack, N., Mimmler, M., Becker, S., Gao, Z., Khuu, M. P., Mann, A., Malinarich, F., Regen, T., & Reinhardt, C. (2022) · Amino Acids · doi:10.1007/s00726-022-03161-5 · Cited by 139 · see citing works
Chronic inflammation within the vascular wall in pulmonary arterial hypertension: more than a spectator
Huertas, A., Tu, L., Humbert, M. J. C., & Guignabert, C. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz308 · Cited by 135 · see citing works
Endothelial shear stress signal transduction and atherogenesis: From mechanisms to therapeutics
He, L., Zhang, C., Chen, Q., Wang, L., & Huang, Y. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108152 · Cited by 137 · see citing works
Oxidative stress and inflammation contribute to traffic noise-induced vascular and cerebral dysfunction via uncoupling of nitric oxide synthases
Daiber, A., Kröller‐Schön, S., Oelze, M. W., Hahad, O., Li, H., Schulz, R., Steven, S., & Münzel, T. F. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101506 · Cited by 130 · see citing works
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Endothelial Dysfunction: Redox Imbalance, NLRP3 Inflammasome, and Inflammatory Responses in Cardiovascular Diseases
Penna, C. R. R., & Pagliaro, P. (2025) · Antioxidants · doi:10.3390/antiox14030256 · Cited by 134 · see citing works
The Role of Mitochondrial Reactive Oxygen Species in Cardiovascular Injury and Protective Strategies
Muntean, D. M., Sturza, A., Dănilă, M. D., Borza, C., Duicu, O., & Mornoş, C. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/8254942 · Cited by 122 · see citing works
Evaluation of oxidative stress and antioxidant status: Correlation with the severity of sepsis
Kumar, S., Gupta, E., Kaushik, S., Srivastava, V. K., Mehta, S. K., & Jyoti, A. (2018) · Scandinavian Journal of Immunology · doi:10.1111/sji.12653 · Cited by 120 · see citing works
Oral administration of bisphenol A induces high blood pressure through angiotensin II/CaMKII‐dependent uncoupling of eNOS
Saura, M., Marquez, S. B., Reventún, P., Olea‐Herrero, N., Arenas, M. I., Moreno‐Gómez‐Toledano, R., Gómez‐Parrizas, M., Muñóz‐Moreno, C., Martínez, M. G.-S., Zaragoza, C., et al. (2014) · The FASEB Journal · doi:10.1096/fj.14-252460 · Cited by 113 · see citing works
Insights into SGLT2 inhibitor treatment of diabetic cardiomyopathy: focus on the mechanisms
Huang, K., Luo, X., Liao, B., Li, G., & Feng, J. (2023) · Cardiovascular Diabetology · doi:10.1186/s12933-023-01816-5 · Cited by 112 · see citing works
Peripheral artery disease, redox signaling, oxidative stress – Basic and clinical aspects
Steven, S., Daiber, A., Dopheide, J. F., Münzel, T. F., & Espinola–Klein, C. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.017 · Cited by 109 · see citing works
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Astaxanthin-antioxidant impact on excessive Reactive Oxygen Species generation induced by ischemia and reperfusion injury
Tamayo, M. Z., Gueguen, V., Letourneur, D., & Pavon‐Djavid, G. (2017) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2017.11.012 · Cited by 109 · see citing works
Therapeutic potential of natural compounds in inflammation and chronic venous insufficiency
Lichota, A., Gwoździński, Ł., & Gwoździński, K. (2019) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2019.04.075 · Cited by 107 · see citing works
Redox-related biomarkers in human cardiovascular disease - classical footprints and beyond
Daiber, A., Hahad, O., Andreadou, I., Steven, S., Daub, S., & Münzel, T. F. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101875 · Cited by 107 · see citing works
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Mechanisms and Clinical Implications of Endothelial Dysfunction in Arterial Hypertension
Ambrosino, P., Bachetti, T., D’Anna, S. E., Galloway, B., Bianco, A., D’Agnano, V., Papa, A., Motta, A., Perrotta, F., & Maniscalco, M. (2022) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd9050136 · Cited by 102 · see citing works
Folic Acid Promotes Recycling of Tetrahydrobiopterin and Protects Against Hypoxia-Induced Pulmonary Hypertension by Recoupling Endothelial Nitric Oxide Synthase
Chalupský, K., Kračun, D., Kanchev, I., Bertram, K., & Görlach, A. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6329 · Cited by 101 · see citing works
Nanodomain Regulation of Cardiac Cyclic Nucleotide Signaling by Phosphodiesterases
Kokkonen-Simon, K. M., & Kass, D. A. (2016) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104756 · Cited by 101 · see citing works
Central Role of Metabolism in Endothelial Cell Function and Vascular Disease
Bierhansl, L., Conradi, L., Treps, L., Dewerchin, M. A., & Carmeliet, P. (2017) · Physiology · doi:10.1152/physiol.00031.2016 · Cited by 101 · see citing works
Allopurinol as a therapeutic option in cardiovascular disease
Okafor, O., Farrington, K., & Gorog, D. A. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.12.004 · Cited by 102 · see citing works
Interplay Between Reactive Oxygen/Reactive Nitrogen Species and Metabolism in Vascular Biology and Disease
Ushio‐Fukai, M., Ash, D., Nagarkoti, S., de Chantemèle, E. J. B., Fulton, D. J., & Fukai, T. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8161 · Cited by 96 · see citing works
Oxidative Stress and Erectile Dysfunction: Pathophysiology, Impacts, and Potential Treatments
Kaltsas, A., Zikopoulos, A., Dimitriadis, F., Sheshi, D., Politis, M., Moustakli, E., Symeonidis, E. N., Chrisofos, M., Sofikitis, N., & Zachariou, A. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46080521 · Cited by 95 · see citing works
Redox implications in adipose tissue (dys)function-A new look at old acquaintances
Jankovic, A., Korac, A., Buzadzic, B., Otasevic, V., Stancic, A., Daiber, A., & Korac, B. (2015) · Redox Biology · doi:10.1016/j.redox.2015.06.018 · Cited by 91 · see citing works
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Sirtuin 1 in Endothelial Dysfunction and Cardiovascular Aging
Ministrini, S., Puspitasari, Y. M., Beer, G., Liberale, L., Montecucco, F., & Camici, G. G. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.733696 · Cited by 93 · see citing works
Tobacco smoking and vascular biology and function: evidence from human studies
Hahad, O., Kuntić, M., Kuntić, I., Daiber, A., & Münzel, T. F. (2023) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-023-02805-z · Cited by 91 · see citing works
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Serum high concentrations of homocysteine and low levels of folic acid and vitamin B12 are significantly correlated with the categories of coronary artery diseases
Ma, Y., Peng, D., Liu, C., Chen, H., & Luo, J. (2017) · BMC Cardiovascular Disorders · doi:10.1186/s12872-017-0475-8 · Cited by 82 · see citing works
Role of Hyperhomocysteinemia and Hyperuricemia in Pathogenesis of Atherosclerosis
Zhao, J., Chen, H., Liu, N., Chen, J., Gu, Y., Chen, J., & Yang, K. (2017) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2016.10.012 · Cited by 87 · see citing works
Protective actions of nuclear factor erythroid 2-related factor 2 (NRF2) and downstream pathways against environmental stressors
Jiménez, M. T. B., Frenis, K., Hahad, O., Steven, S., Cohen, G., Cuadrado, A., Münzel, T. F., & Daiber, A. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.05.016 · Cited by 74 · see citing works
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Endothelial-Derived Oxidative Stress Drives Myofibroblastic Activation and Calcification of the Aortic Valve
Farrar, E. J., Huntley, G. D., & Butcher, J. T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123257 · Cited by 72 · see citing works
Exploiting the Pleiotropic Antioxidant Effects of Established Drugs in Cardiovascular Disease
Steven, S., Münzel, T. F., & Daiber, A. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160818185 · Cited by 66 · see citing works
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Sex differences in abdominal aortic aneurysms
Boese, A. C., Chang, L., Yin, K., Chen, Y. E., Lee, J., & Hamblin, M. H. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00519.2017 · Cited by 65 · see citing works
Old dog, new tricks: novel cardiac targets and stress regulation by protein kinase G
Rainer, P. P., & Kass, D. A. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw107 · Cited by 63 · see citing works
Inhibiting inflammation and modulating oxidative stress in oxalate-induced nephrolithiasis with the Nrf2 activator dimethyl fumarate
Zhu, J., Wang, Q., Li, C., Lu, Y., Hu, H., Qin, B., Xun, Y., Zhu, Y., Wu, Y., Zhang, J., et al. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.12.033 · Cited by 62 · see citing works
Taking up the cudgels for the traditional reactive oxygen and nitrogen species detection assays and their use in the cardiovascular system
Daiber, A., Oelze, M. W., Steven, S., Kröller‐Schön, S., & Münzel, T. F. (2017) · Redox Biology · doi:10.1016/j.redox.2017.02.001 · Cited by 62 · see citing works
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Mitochondrial Transfer in Cardiovascular Disease: From Mechanisms to Therapeutic Implications
Chen, J., Zhong, J., Wang, L., & Chen, Y. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.771298 · Cited by 61 · see citing works
Polydatin Protects Diabetic Heart against Ischemia‐Reperfusion Injury via Notch1/Hes1‐Mediated Activation of Pten/Akt Signaling
Yu, L., Li, Z., Dong, X., Xue, X., Liu, Y., Xu, S. C., Zhang, J., Han, J., Yang, Y., & Wang, H. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/2750695 · Cited by 61 · see citing works
Omega-3 Polyunsaturated Fatty Acids: Structural and Functional Effects on the Vascular Wall
Zanetti, M., Grillo, A., Losurdo, P., Panizon, E., Mearelli, F., Cattin, L., Barazzoni, R., & Carretta, R. (2015) · BioMed Research International · doi:10.1155/2015/791978 · Cited by 59 · see citing works
Targeting the NO/superoxide ratio in adipose tissue: relevance to obesity and diabetes management
Janković, A., Korać, A., Buzadžić, B., Stančić, A., Otašević, V., Ferdinándy, P., Daiber, A., & Korać, B. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13498 · Cited by 60 · see citing works
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Endothelial injury in rheumatoid arthritis: a crosstalk between dimethylarginines and systemic inflammation
Dimitroulas, T., Hodson, J. A., Sandoo, A., Smith, J., & Kitas, G. D. (2017) · Arthritis Research & Therapy · doi:10.1186/s13075-017-1232-1 · Cited by 59 · see citing works
Regulation of Vascular Function and Inflammation via Cross Talk of Reactive Oxygen and Nitrogen Species from Mitochondria or NADPH Oxidase—Implications for Diabetes Progression
Daiber, A., Steven, S., Vujačić-Mirski, K., Kalinovic, S., Oelze, M. W., Lisa, F. D., & Münzel, T. F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103405 · Cited by 58 · see citing works
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The Implication of a Polymorphism in the Methylenetetrahydrofolate Reductase Gene in Homocysteine Metabolism and Related Civilisation Diseases
Zarembska, E., Ślusarczyk, K., & Wrzosek, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms25010193 · Cited by 56 · see citing works
CD40/CD40L and Related Signaling Pathways in Cardiovascular Health and Disease—The Pros and Cons for Cardioprotection
Daub, S., Lutgens, E., Münzel, T. F., & Daiber, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228533 · Cited by 55 · see citing works
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Therapeutic augmentation of NO-sGC-cGMP signalling: lessons learned from pulmonary arterial hypertension and heart failure
Triposkiadis, F. K., Xanthopoulos, A. V., Skoularigis, J. S., & Starling, R. C. (2022) · Heart Failure Reviews · doi:10.1007/s10741-022-10239-5 · Cited by 52 · see citing works
l-Leucine and NO-mediated cardiovascular function
Yang, Y., Wu, Z., Meininger, C. J., & Wu, G. (2014) · Amino Acids · doi:10.1007/s00726-014-1904-y · Cited by 52 · see citing works
CD40L controls obesity-associated vascular inflammation, oxidative stress, and endothelial dysfunction in high fat diet-treated and db/db mice
Steven, S., Dib, M., Hausding, M., Kashani, F., Oelze, M. W., Kröller‐Schön, S., Hanf, A., Daub, S., Roohani, S., Gramlich, Y., et al. (2017) · Cardiovascular Research · doi:10.1093/cvr/cvx197 · Cited by 52 · see citing works
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Resveratrol and vascular health: evidence from clinical studies and mechanisms of actions related to its metabolites produced by gut microbiota
Godos, J., Romano, G. L., Gozzo, L., Laudani, S., Paladino, N., Azpíroz, I. D., López, N. M. M., Giampieri, F., Quiles, J. L., Battino, M. A., et al. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1368949 · Cited by 53 · see citing works
Phthalate exposure as a risk factor for hypertension
Lu, X., Xu, X., Lin, Y., Zhang, Y., & Huo, X. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-018-2367-6 · Cited by 51 · see citing works
Impacts of aging and fluid shear stress on vascular endothelial metabolism and atherosclerosis development
Wang, W.-L., Shih, Y.-T., Wei, S.-Y., & Chiu, J.-J. (2025) · Journal of Biomedical Science · doi:10.1186/s12929-025-01177-z · Cited by 50 · see citing works
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Endothelial Nitric Oxide Synthase Uncoupling And Oxidative Stress
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Endothelial dysfunction due to eNOS uncoupling: molecular mechanisms as potential therapeutic targets
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Authors: Karbach, S., Wenzel, P., Waisman, A., Munzel, T., & Daiber, A.
Affiliations: University Medical Center of the Johannes Gutenberg University Mainz (DE)
ORCID: Karbach, Susanne
Wenzel, Philip
Waisman, Ari
Daiber, Andreas
Venue: Current Pharmaceutical Design
Publisher: Bentham Science Publishers Ltd.
Published: 2014-06
Volume: 20
Issue: 22
Pages: 3579-3594
ISSN: 1381-6128 (ISSN-L)
DOI: 10.2174/13816128113196660748
OpenAlex: W2157350806
Cited by: 307
References: 155
Citations by year: 2026: 19 · 2025: 22 · 2024: 21 · 2023: 20 · 2022: 34 · 2021: 40 · 2020: 26 · 2019: 23 · 2018: 23 · 2017: 29 · 2016: 19 · 2015: 24 · 2014: 7
FWCI: 17.51
Type: journal article
Language: en
Open access: closed
Locations: Current Pharmaceutical Design (publishedVersion)
PubMed (publishedVersion)
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 › Molecular Biology › Redox biology and oxidative stress
Keywords: endothelial nitric oxide synthase, eNOS uncoupling, oxidative stress, inflammation, tetrahydrobiopterin, S-glutathionylation, asymmetric dimethylarginine, reactive oxygen and nitrogen species, endothelial dysfunction, hypertension, atherosclerosis, coronary artery disease, vascular dysfunction, cytokines, redox switch
MeSH terms: Cardiovascular Diseases, Humans, Inflammation, Oxidative Stress, Nitric Oxide Synthase Type III

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eNOS Uncoupling in Cardiovascular Diseases - the Role of Oxidative Stress and Inflammation

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