Cited by 598Nitric Oxide and Endothelin EffectsNeutrophil, Myeloperoxidase and Oxidative MechanismsRedox biology and oxidative stress

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A gp91phox Containing NADPH Oxidase Selectively Expressed in Endothelial Cells Is a Major Source of Oxygen Radical Generation in the Arterial Wall

Görlach, A., Brandes, R. P., Nguyen, K., Amidi, M., Dehghani, F., Busse, R.·2000·Circulation Research

DOI 10.1161/01.res.87.1.26

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Abstract

Abstract —Reactive oxygen species (ROS) play an important role in regulating vascular tone and intracellular signaling; the enzymes producing ROS in the vascular wall are, however, poorly characterized. We investigated whether a functionally active NADPH oxidase similar to the leukocyte enzyme, ie, containing the subunits p22phox and gp91phox, is expressed in endothelial cells (ECs) and smooth muscle cells (SMCs). Phorbol 12-myristate 13-acetate (PMA), a stimulus for leukocyte NADPH oxidase, increased ROS generation in cultured ECs and endothelium-intact rat aortic segments, but not in SMCs or endothelium-denuded arteries. NADPH enhanced chemiluminescence in all preparations. p22phox mRNA and protein was detected in ECs and SMCs, whereas the expression of gp91phox was confined to ECs. Endothelial gp91phox was identical to the leukocyte form as determined by sequence analysis. In contrast, mitogenic oxidase-1 (mox1) was expressed in SMCs, but not in ECs. To determine the functional relevance of gp91phox expression, experiments were performed in aortic segments from wild-type, gp91phox − /− , and endothelial NO synthase (eNOS) − /− mice. PMA-induced ROS generation was comparable in aortae from wild-type and eNOS − /− mice, but was attenuated in segments from gp91phox − /− mice. Endothelium-dependent relaxation was greater in aortae from gp91phox − /− than from wild-type mice. The ROS scavenger tiron increased endothelium-dependent relaxation in segments from wild-type, but not from gp91phox − /− mice. These data demonstrate that ECs, in contrast to SMCs, express a gp91phox-containing leukocyte-type NADPH oxidase. This enzyme is a major source for arterial ROS generation and affects the bioavailability of endothelium-derived NO. ( Circ Res. 2000;87:26-32.)

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Redox signaling of NF-κB by membrane NAD(P)H oxidases in normal and malignant cells
Brar, S., Kennedy, T. P., Quinn, M. T., & Hoidal, J. (2003) · Protoplasma · doi:10.1007/s00709-002-0059-y · Cited by 38
“…efforts to link NOX oxidases to cell signaling events have occurred in the area of vascular diseases (Griendling et al. 2000), where the signaling NAD(P)H oxidase has been rapidly and carefully explored in endothelium (Gorlach et al. 2000) and vascular smooth muscle (Lassegue et al. 2001).”
p47 Participates in Activation of RelA in Endothelial Cells
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Context‐dependent function of ROS in the vascular endothelium: The role of the Notch pathway and shear stress
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“Endothelial specific overexpression of Nox2 increases AngII-induced hypertension, vascular oxidative stress, and ED.”
BackgroundInfluential
Rac-Dependent Monocyte Chemoattractant Protein-1 Production Is Induced by Nutrient Deprivation
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Whole-cell and nuclear NADPH oxidases levels and distribution in human endocardial endothelial, vascular smooth muscle, and vascular endothelial cells
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Activation of PPARδ prevents endothelial dysfunction induced by overexpression of amyloid-β precursor protein
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Endothelial Nanomechanics in the Context of Endothelial (Dys)function and Inflammation
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Coordinated role of voltage-gated sodium channels and the Na+/H+ exchanger in sustaining microglial activation during inflammation
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“…enzyme consisting of six membrane-bound subunits, including gp91phox and P22phox (Cheng et al., 2001; Yu et al., 1998), with gp91phox serving as a primary catalytic subunit responsible for ROS and H2O2 production (Babior, 2000; Gorlach et al., 2000; Qin and Crews, 2012; Ushio-Fukai et al., 2002).”
Background
ROLE OF REACTIVE METABOLITES OF OXYGEN AND NITROGEN IN PARTIAL LIVER TRANSPLANTATION: LESSONS LEARNED FROM REDUCED‐SIZE LIVER ISCHAEMIA AND REPERFUSION INJURY
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“In addition, NADPH oxidase has been found in vascular tissue, most likely associated with the endothelium.(31) Production of even small quantities of ROS at this location following I /R may be important for the initiation of events leading to liver injury, as well as cellular adhesion and PMN infiltration.”
BackgroundMethodInfluential
Microglial Ion Channels as Potential Targets for Neuroprotection in Parkinson’s Disease
Richardson, J. R., & Hossain, M. M. (2013) · Neural Plasticity · doi:10.1155/2013/587418 · Cited by 33
Reconstituted high-density lipoprotein suppresses leukocyte NADPH oxidase activation by disrupting lipid rafts
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“On the other hand, Nox2 is also expressed in endothelial cells and is responsible for superoxide generation [38].”
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gp-91 mediates histone deacetylase inhibition-induced cardioprotection
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Direct Evidence for Increased Hydroxyl Radicals in Angiotensin II-induced Cardiac Hypertrophy through Angiotensin II Type 1a Receptor
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“It has been shown that NADPH oxidase plays a major role as the most important source of superoxide in endothelial and smooth muscle cells (14,16).”
Background
Microvascular Alterations in Hypertension and Vascular Aging
Savoia, C., Battistoni, A., Calvez, V., Cesario, V., Montefusco, G., & Filippini, A. (2017) · Current Hypertension Reviews · doi:10.2174/1573402113666170505115010 · Cited by 34
“ROS is also produced by mitochondria [63-69] and contributes to mitochondrial dysfunction which is progressively increased in vascular aging.”
Background
Role of gp91phox-containing NADPH oxidase in the deoxycorticosterone acetate-salt-induced hypertension
Fujii, A., Nakano, D., Katsuragi, M., Ohkita, M., Takaoka, M., Ohno, Y., & Matsumura, Y. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.09.039 · Cited by 32
Trimer hydroxylated quinone derived from apocynin targets cysteine residues of p47phox preventing the activation of human vascular NADPH oxidase
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“1A, translocation of cytosolic subunits (p47phox, p67phox, p40phox and Rac) occurs through binding to the membrane p22phox and gp91phox subunits [8–11].”
Background
The effect of nicotinamide adenine dinucleotide phosphate oxidase 4 on migration and invasion of fibroblast-like synoviocytes in rheumatoid arthritis
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Statins in Endothelial Signaling and Activation
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Sphingolipids in Atherosclerosis: Chimeras in Structure and Function
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Suppression of atrial natriuretic peptide/natriuretic peptide receptor-A-mediated signaling upregulates angiotensin-II-induced collagen synthesis in adult cardiac fibroblasts
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Glucagon-like peptide-1 preserves coronary microvascular endothelial function after cardiac arrest and resuscitation: potential antioxidant effects
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Short-term regular aerobic exercise reduces oxidative stress produced by acute high intraluminal pressure in the adipose microvasculature
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Reactive Oxygen Species Adversely Impacts Bone Marrow Microenvironment in Diabetes
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“NOX2, previously known as gp91phox, is present in endothelial and phagocytic cells (39, 105).”
Background
Disruption of endothelial adherens junction by invasive breast cancer cells is mediated by reactive oxygen species and is attenuated by AHCC
Haidari, M., Zhang, W., & Wakame, K. (2013) · Life Sciences · doi:10.1016/j.lfs.2013.10.027 · Cited by 30
“The effect of PMA on generation of ROS in HUVECs at the concentration that was used in our study has been previously demonstrated (Eligini et al., 2005; Görlach et al., 2000).”
Method
Localization of NADPH oxidase in sympathetic and sensory ganglion neurons and perivascular nerve fibers
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“…discovered in neutrophils, NADPH oxidase is now thought to be a significant source of ROS in many cell types, including smooth muscle cells (Griendling et al., 1994; Patterson et al., 1999; Ushio-Fukai et al., 1996), endothelial cells (Gorlach et al., 2000) and fibroblasts (Jones et al., 1994).”
BackgroundInfluential
NADPH Oxidase Pathway Is Involved in Aortic Contraction Induced by A3 Adenosine Receptor in Mice
El‐Awady, M. S., Ansari, H. R., Fil, D., Tilley, S. L., & Mustafa, S. J. (2011) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.111.180828 · Cited by 30
NADPH oxidase produces reactive oxygen species and maintains survival of rat astrocytes
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Inducible Endothelium-derived Hyperpolarizing Factor
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Endothelial arginase II and atherosclerosis
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“system is activated [69].”
Pro-Resolving FPR2 Agonists Regulate NADPH Oxidase-Dependent Phosphorylation of HSP27, OSR1, and MARCKS and Activation of the Respective Upstream Kinases
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Pulsatile shear stress increased mitochondrial membrane potential: Implication of Mn-SOD
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“While eNOS is the major source of RNS, NADPH oxidase system is considered as a major source of ROS in vascular endothelial cells [4,7].”
Dissociation between metabolic and vascular insulin resistance in aging
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“A major source of endothelial reactive oxygen species (ROS) generation is the NAD(P)H oxidase complex, composed of a membrane-bound flavocytochrome b558 consisting of gp91 (Nox2) and p22 and two cytosolic subunits (p47 and p67) (15, 23).”
Background
NOX2 Antisense Attenuates Hypoxia-Induced Oxidative Stress and Apoptosis in Cardiomyocyte
Yu, B., Meng, F., Yang, Y., Liu, D., & Shi, K. (2016) · International Journal of Medical Sciences · doi:10.7150/ijms.15177 · Cited by 28
“NOX2, known as gp91phox, was first discovered in neutrophils and macrophages [3] and was described later in nonphagocytic cells, including neurons [4], skeletal muscle myocytes [5], hepatocytes [6], endothelial cells [7-9], hematopoietic stem cells [10], and cardiomyocytes [11].”
Background
Desbalanço redox: NADPH oxidase como um alvo terapêutico no manejo cardiovascular
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The Pathophysiological Role of NOX2 in Hypertension and Organ Damage
Forte, M., Nocella, C., FALCO, E. D., Palmerio, S., Schirone, L., Valenti, V., Frati, G., Carnevale, R., & Sciarretta, S. (2016) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-016-0175-y · Cited by 29
Malfunction of Vascular Control in Lifestyle-Related Diseases: Mechanisms Underlying Endothelial Dysfunction in the Insulin-Resistant State
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Inhibition of the yeast metal reductase heme protein fre1 by nitric oxide (NO): a model for inhibition of NADPH oxidase by NO
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Physical activity for coronary heart disease: cardioprotective mechanisms and effects on prognosis
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Update on Nox function, site of action and regulation in Botrytis cinerea
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Protein kinase C-α and -δ are required for NADPH oxidase activation in WKYMVm-stimulated IMR90 human fibroblasts
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The Ins and Outs of Small GTPase Rac1 in the Vasculature
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“Fibroblasts also have extensive NOX-mediated signaling.”
Background
Defining the molecular role of gp91phox in the immune manifestation of acute allergic asthma using a preclinical murine model
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CML/CD36 accelerates atherosclerotic progression via inhibiting foam cell migration
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Antiatherogenic Effect of Bisvanillyl-Hydralazone, a New Hydralazine Derivative with Antioxidant, Carbonyl Scavenger, and Antiapoptotic Properties
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“These effects are reinforced by the inhibitory effect of BVH on the expression of the gp91 phox subunit of NADPH-oxidase, in agreement with reports showing the role of gp91 phox in extracellular ROS generation (19, 20).”
Over-expression of a cardiac-specific human dopamine D5 receptor mutation in mice causes a dilated cardiomyopathy through ROS over-generation by NADPH oxidase activation and Nrf2 degradation
Jiang, X., Liu, Y., Liu, X., Wang, W., Wang, Z., Hu, Y., Zhang, Y., Zhang, Y., José, P. A., Wei, Q., et al. (2018) · Redox Biology · doi:10.1016/j.redox.2018.07.008 · Cited by 25
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Chronic exposure to tramadol induces cardiac inflammation and endothelial dysfunction in mice
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Authors: Görlach, A., Brandes, R. P., Nguyen, K., Amidi, M., Dehghani, F., & Busse, R.
Affiliations: From the Institut für Kardiovaskuläre Physiologie (A.G., R.P.B., K.N., M.A., R.B.), and Institut für Anatomie II (F.D.), Klinikum der J.W. Goethe-Universität, Frankfurt/Main, Germany.
Goethe University Frankfurt (DE)
Corresponding author: Brandes, R. P.
ORCID: Brandes, R. P.
Nguyen, K.
Dehghani, F.
Venue: Circulation Research
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2000-07-07
Volume: 87
Issue: 1
Pages: 26-32
ISSN: 0009-7330 (ISSN-L)
1524-4571
DOI: 10.1161/01.res.87.1.26
OpenAlex: W2169235788
Cited by: 598
References: 28
Citations by year: 2026: 3 · 2024: 4 · 2023: 5 · 2022: 14 · 2021: 12 · 2020: 8 · 2019: 11 · 2018: 10 · 2017: 17 · 2016: 23 · 2015: 13 · 2014: 25 · 2013: 18 · 2012: 28
FWCI: 26.10
Type: journal article
Language: en
Open access: closed
Locations: Circulation Research (publishedVersion)
PubMed (publishedVersion)
Funders: Deutscher Akademischer Austauschdienst
Deutsche Forschungsgemeinschaft (SFB 553, TP B1)
Genentech
Topics: Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: gp91phox, NADPH oxidase, endothelial cells, reactive oxygen species, oxygen free radicals, arterial wall, smooth muscle cells, p22phox, endothelium-dependent relaxation, nitric oxide bioavailability, endothelial nitric oxide synthase, chemiluminescence, Tiron, aorta
MeSH terms: NADPH Oxidase 2, Acetylcholine, Animals, Aorta, Endothelium, Vascular, Free Radicals, Membrane Glycoproteins, Muscle, Smooth, Vascular, Nitric Oxide, Tetradecanoylphorbol Acetate, Reactive Oxygen Species, NADPH Oxidases, Reverse Transcriptase Polymerase Chain Reaction, Mice, Rats

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A gp91phox Containing NADPH Oxidase Selectively Expressed in Endothelial Cells Is a Major Source of Oxygen Radical Generation in the Arterial Wall

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