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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Background
Targeting Reactive Oxygen Species in Atherosclerosis via Chinese Herbal Medicines
Zhang, L., Huang, J., Zhang, D., Lei, X., Ma, Y., Cao, Y., & Chang, J. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/1852330 · Cited by 13
“NOX-1 and NOX-4 are mainly expressed in vascular smooth muscle cells [29, 30], while NOX-2 and NOX-4 in endothelial cells [31 – 33].”
Pathophysiology of Primary Hypertension
Carey, R. M. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374530-9.00020-6 · Cited by 13
Sex-specific vascular responses of the rat aorta: effects of moderate term (intermediate stage) streptozotocin-induced diabetes
Han, X., Shaligram, S. S., Zhang, R., Anderson, L. C., & Rahimian, R. (2015) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2015-0272 · Cited by 13
“NADPH oxidase (Nox) is one of the major sources of superoxide in the cardiovascular system (Cai et al. 2003; Gorlach et al. 2000; Griendling et al. 2000).”
Background
Monitoring Oxidative Stress in Vascular Endothelial Cells in Response to Fluid Shear Stress: From Biochemical Analyses to Micro- and Nanotechnologies
Rouhanizadeh, M., Takabe, W., Ai, L., Yu, H., & Hsiai, T. K. (2008) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(08)01207-x · Cited by 13
“NADPH oxidases are made up of three cytosolic protein subunits, p47, p67, and the G-protein, Rac, as well as a membrane-bound cytochrome reductase domain (Görlach et al., 2000).”
Influential
Low-Density Lipoprotein Induced Actin Cytoskeleton Reorganization in Endothelial Cells: Mechanisms of Action
Holland, J. A., Goss, R. A., O’Donnell, R., Chang, M., Johnson, D. K., & Ziegler, L. M. (2001) · Endothelium · doi:10.3109/10623320109165321 · Cited by 13
Lancemaside A from Codonopsis lanceolata prevents hypertension by inhibiting NADPH oxidase 2-mediated MAPK signalling and improving NO bioavailability in rats
Shin, Y. K., Han, A. Y., Hsieh, Y.-S., Kwon, S., Kim, J., Lee, K., & Seol, G. H. (2019) · Journal of Pharmacy and Pharmacology · doi:10.1111/jphp.13140 · Cited by 12
“The involvement of NOX2 in ROS generation was shown by the decrease in phorbol 12-myristate 13-acetate-induced ROS formation in aortas from NOX2 knockout mice.([40]) Although there were no significant changes in NOX1 and NOX4 expression, cardiac NOX2 protein expression was higher in SHR than in Wistar Kyoto rats, and…”
Background
Effects of Senegenin against hypoxia/reoxygenation-induced injury in PC12 cells
Zhu, X.-Q., Li, X., Zhao, Y., Ji, X.-L., Wang, Y., Fu, Y., Wang, H., Lu, D., & Qi, R. (2016) · Chinese Journal of Integrative Medicine · doi:10.1007/s11655-015-2091-8 · Cited by 12
“NADPH oxidases of the NOX family are related to the production of ROS in various cells.((29-31)) Sen was supposed to realize its neuroprotection via suppressing the activity of NADPH oxidase, thereby decreasing intracellular ROS production.”
Background
Expression of CD70 Modulates Nitric Oxide and Redox Status in Endothelial Cells
Pandey, A. K., Waldeck‐Weiermair, M., Wells, Q. S., Xiao, W., Yadav, S., Eroğlu, E., Michel, T. M., & Loscalzo, J. (2022) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.122.317866 · Cited by 12
Dipeptidyl peptidase 4 inhibition rescues PKA-eNOS signaling and suppresses aortic hypercontractility in male rats with heart failure
Fontes, M. T., Arruda-Junior, D. F., dos Santos, D. S., Ribeiro-Silva, J. C., Antônio, E. L., Tucci, P. J. F., Rossoni, L. V., & Girardi, A. C. C. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.121648 · Cited by 12
Cross Talk Between p22phox and ATF4 in the Endothelial Unfolded Protein Response
Petry, A., Zhang, Z.-W., Trautz, B., Rieß, F., & Görlach, A. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7481 · Cited by 11
“Recently, additional homologues of NOX2 have been identiﬁed in nonphagocytic cells (2, 8, 12, 32), through which NOX1, NOX3 and NOX4 form, like NOX2, a membrane-bound complex with p22phox, thus making this small protein an essential component of most NADPH oxidases.”
Inhibition of endothelial nitric oxyde synthase increases capillary formation via Rac1-dependent induction of hypoxia-inducible factor-1α and plasminogen activator inhibitor-1
Weitnauer, M., Petry, A., BelAiba, R. S., & Görlach, A. (2012) · Thrombosis and Haemostasis · doi:10.1160/th12-04-0277 · Cited by 12
“While endothelial NO synthase (eNOS) is the main source of NO in endothelial cells (9), and has been considered to exert a protective effect on the vessel wall, NADPH oxidases have been shown to contribute to endothelial ROS generation (10, 11).”
BackgroundResult
gp91phox-containing NAD(P)H oxidase mediates attenuation of nitric oxide-dependent control of myocardial oxygen consumption by ANG II
Kinugawa, S., Zhang, J., Messina, E. J., Walsh, E. K., Huang, H., Kaminski, P. M., Wolin, M. S., & Hintze, T. H. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00076.2005 · Cited by 12
“A gp91-containing oxidase is known to be expressed in endothelium (3, 10), fibroblasts (34), and cardiomyocytes (21).”
Background
ABCG1 Attenuates Oxidative Stress Induced by H2O2 through the Inhibition of NADPH Oxidase and the Upregulation of Nrf2-Mediated Antioxidant Defense in Endothelial Cells
Xue, J., Fan, J., Li, Y., Wu, W., Yan, Q., & Zheng, Q. (2020) · Analytical Cellular Pathology · doi:10.1155/2020/2095645 · Cited by 11
“Nox4 expression is high in endothelial cells, as compared to other Nox isoforms [22, 23].”
BackgroundInfluential
Selective inhibition of NADPH-oxidase isoforms as a therapeutic strategy in hypertension
Miller, A. A., Drummond, G. R., & Sobey, C. G. (2005) · Drug Discovery Today Therapeutic Strategies · doi:10.1016/j.ddstr.2005.08.002 · Cited by 11
Attenuation of Oxidative Stress, Interleukin-6, High-Sensitivity C-Reactive Protein, Plasminogen Activator Inhibitor-1, and Fibrinogen with Oral Vitamin D Supplementation in Patients with T2DM having Vitamin D Deficiency
Pasupuleti, P., Suchitra, M. M., Bitla, A. R. R., & Sachan, A. (2021) · Journal of Laboratory Physicians · doi:10.1055/s-0041-1742285 · Cited by 10
Diabetes mellitus, oxidative stress and endothelial dysfunction
Sydow, K., & Münzel, T. F. (2003) · International Congress Series · doi:10.1016/s0531-5131(02)01280-3 · Cited by 11
Oxidants and Endothelial Dysfunction
Lund, A. K. (2010) · Elsevier eBooks · doi:10.1016/b978-0-08-046884-6.00712-0 · Cited by 12
Potential Role for Oxidative Stress in 2,2′-Dichlorobiphenyl–Induced Inhibition of Uterine Contractions but not Myometrial Gap Junctions
Chung, D., & Loch-Caruso, R. K. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl031 · Cited by 10
“Superoxide anion is produced by a membrane-bound nicotinamide dinucleotide phosphate (NADPH) oxidase in phagocytes as well as in nonphagocytic cells, such as endothelial cells and vascular smooth muscle cells (Görlach et al., 2000).”
Background
Effects of glucocorticoids on the respiratory burst of Chlamydia-primed THP-1 cells
Mouithys-Mickalad, A. A., Deby-Dupont, G. P., Mathy-Hartert, M., Habraken, Y., Nys, M., Henrotin, Y. E., Lamy, M., & Deby, C. M. T. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.04.120 · Cited by 10
NOX2 Expression Is Increased in Keratinocytes After Burn Injury
Korkmaz, H. I., Ulrich, M. M. W., Çelik, G., van Wieringen, W. N., van Zuijlen, P. P. M., Krijnen, P. A. J., & Niessen, H. W. M. (2019) · Journal of Burn Care & Research · doi:10.1093/jbcr/irz162 · Cited by 9
Expression of a homolog in Caco-2 cells giving O2−-reconstituting ability to cytochrome b558 together with recombinant
Yoshida, L. S., Nishida, S., Shimoyama, T., Kawahara, T., Rokutan, K., & Tsunawaki, S. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02059-4 · Cited by 9
Angiotensin II Upregulates CaV1.2 Protein Expression in Cultured Arteries via Endothelial H2O2 Production
Wang, W., Pang, L., & Palade, P. (2010) · Journal of Vascular Research · doi:10.1159/000318776 · Cited by 9
“Our H 2 O 2 determination (fig. 5 ) showed that after endothelial damage angiotensin II had no effect on H 2 O 2 production. We also observed that catalase partially blocked angiotensin II-induced tension increases in mesenteric arteries with intact endothelium, but had no action in arteries with damaged endothelium (…”
Result
Medroxyprogesterone Acetate Aggravates Oxidative Stress and Left Ventricular Dysfunction in Rats with Chronic Myocardial Infarction
Arias-Loza, P.-A., Hu, K., Frantz, S., Dienesch, C., Bayer, B., Wu, R., Ertl, G., & Pelzer, T. (2011) · Toxicologic Pathology · doi:10.1177/0192623311410441 · Cited by 9
“…myocardial cells and that NADPH oxidase subunits are expressed not only in cardiomyocytes, but also in vascular cells, we suspect that the main source of ROS detected in our sections was originated in the microvasculature (Zak 1973; Gorlach et al. 2000; Pagano et al. 1997; Mohazzab et al. 1997).”
Background
The use of reverse transcription-PCR for the diagnosis of X-linked chronic granulomatous disease
Agudelo-Flórez, P. M., López, J. A., Redher, J., Carneiro-Sampaio, M. M. S., Costa-Carvalho, B. T., Grumach, A. S., & Condino‐Neto, A. (2004) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2004000500001 · Cited by 10
Possible Role of Extracellular Vesicles in Hepatotoxicity of Acetaminophen
Gajdošik, M. Š., Peić, A. K., Begić, M., Grbčić, P., Brilliant, K. E., Hixson, D. C., & Josić, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168870 · Cited by 7
“P30839 Aldehyd dehydrogenase 6 17 77 Hepatocytes, Some non-parenchymal cells [23]”
MethodInfluential
Remote ischemic preconditioning differentially affects NADPH oxidase isoforms during hepatic ischemia–reperfusion
Garab, D., Fet, N., Szabó, A., Tolba, R. H., Boros, M., & Hartmann, P. (2014) · Life Sciences · doi:10.1016/j.lfs.2014.04.014 · Cited by 8
“Furthermore, the expression of NOX4 is at least 20-fold greater than that of NOX2 in the endothelial cells (Sorescu and Griendling, 2002), while the expression of NOX2 cannot be detected in the vascular smooth muscle cells (Görlach et al., 2000; Lassègue et al., 2001).”
Background
Hypoxia and Reactive Oxygen Species
Görlach, A. (2013) · Cancer drug discovery and develogment/Cancer drug discovery and development · doi:10.1007/978-1-4614-9167-5_4 · Cited by 8
Candidate gene analysis in the São Paulo Epidemiologic Sleep Study (EPISONO) shows an association of variant in PDE4D and sleepiness
Pak, V. M., Mazzotti, D. R., Keenan, B. T., Hirotsu, C., Gehrman, P., Bittencourt, L., Pack, A. I., & Tufik, S. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2017.12.010 · Cited by 8
Effects of Chronic Administration of L-Arginine on Vasoactive Responses induced by Endothelin-1 and its Plasma Level in Streptozotocin-Induced Diabetic Rats.
Makino, A., & Kamata, K. (2002) · Journal of Smooth Muscle Research · doi:10.1540/jsmr.38.101 · Cited by 8
“Many components of the leucocyte- NADPH-oxidase complex — including p22phox, p47phox, p67phox and gp91phox (or a related homologue) — have been identified in endothelial cells or vascular smooth muscle cells (Jones et al., 1996; Bayraktutan et al., 1998; Gorlach et al., 2000; Patterson et al., 1999; Ushio-Fukai et al.…”
Background
Atorvastatin reduces the plasma lipids and oxidative stress but did not reverse the inhibition of prostacyclin generation by aortas in streptozotocin diabetic rats
Mahfouz, M., & Kummerow, F. A. (2005) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2004.12.002 · Cited by 8
Pathophysiology of Primary Hypertension
Carey, R. M. (2008) · Comprehensive physiology · doi:10.1002/cphy.cp020418 · Cited by 9
Out Phoxing the Endothelium
Lassegue, B. P., & Griendling, K. K. (2002) · Circulation Research · doi:10.1161/res.90.2.123 · Cited by 8
Outgrowth endothelial progenitor cells restore cerebral barrier function following ischaemic damage: The impact of NOX2 inhibition
Alwjwaj, M., Kadir, R. R. A., & Bayraktutan, U. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15627 · Cited by 7
“(NOX) constitutes the major enzymatic source of ROS in vasculature, with many studies reporting that NOX2 (previously known as gp91) is the main element required for ROS generation (16, 19-21).”
Background
Benefits of Vitamin D Supplementation on Pregnancy of Rats with Pregestational Diabetes and Their Offspring
Klöppel, E., Sinzato, Y. K., Rodrigues, T., Gallego, F. Q., Karki, B., Volpato, G. T., Corrente, J. E., Roy, S., & Damasceno, D. C. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-01056-0 · Cited by 7
Reactivity of renal and mesenteric resistance vessels to angiotensin II is mediated by NOXA1/NOX1 and superoxide signaling
Stevenson, M. D., Vendrov, A. E., Yang, X., Chen, Y., Navarro, H. A., Moss, N., Runge, M. S., Arendshorst, W. J., & Madamanchi, N. R. (2023) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00236.2022 · Cited by 8
Differential modulation of bradykinin-induced relaxation of endothelin-1 and phenylephrine contractions of rat aorta by antioxidants
Anozie, O., Richonda, R. O. S. S., Oyekan, A., & Yakubu, M. A. (2007) · Acta Pharmacologica Sinica · doi:10.1111/j.1745-7254.2007.00631.x · Cited by 7
Electrophilic Nitro-Fatty Acids: Nitric Oxide and Nitrite-Derived Metabolic and Inflammatory Signaling Mediators
Freeman, B. Α., Pekarová, M., Rubbo, H., & Trostchansky, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804273-1.00016-8 · Cited by 7
Stress oxydant, fonctions vasculaires et athérosclérose
Bonnefont‐Rousselot, D., Peynet, J., Beaudeux, J., Thérond, P., Legrand, A., & Delattre, J. (2002) · Nutrition Clinique et Métabolisme · doi:10.1016/s0985-0562(02)00169-3 · Cited by 7
Oxidative Stress and Protein Oxidation
Grune, T., Catalgol, B., & Jung, T. (2012) · Wiley eBooks · doi:10.1002/9781118493038.ch1 · Cited by 7
Characterization of signaling mechanisms regulating cardiac contractility
Kubin, A. (2011) · Cited by 7
Angiotensin II and Superoxide Generation
Dikalov, S., & Harrison, D. G. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_59 · Cited by 6
Effect of 4‐week inhalation exposure to 1‐bromopropane on blood pressure in rats
Huang, F., Ichihara, S., Yamada, Y., Banu, S., & Ichihara, G. (2016) · Journal of Applied Toxicology · doi:10.1002/jat.3364 · Cited by 6
“Nox2 ( gp91phox) is localized primarily in endothelial and adventitial cells and affects endothelium-dependent relaxation and vascular homeostasis (Görlach et al., 2000).”
Background

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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