NOX2 and NOX4 Mediate Proliferative Response in Endothelial Cells
Abstract
Increased levels of reactive oxygen species (ROS) contribute to many cardiovascular diseases. In neutrophils, ROS are generated by a NADPH oxidase containing p22phox and NOX2. NADPH oxidases are also major sources of vascular ROS. Whereas an active NOX2-containing enzyme has been described in endothelial cells, the contribution of recently identified NOX homologues to endothelial ROS production and proliferation has been controversial. The authors, therefore, compared the role of NOX2 with NOX4 and NOX1 in endothelial EaHy926 and human microvascular endothelial cells. NOX2 and NOX4 were abundantly expressed, whereas NOX1 expression was less prominent. NOX2, NOX4, and NOX1 were simultaneously present in a single cell in a perinuclear compartment. NOX2 and NOX4 co-localized with the endoplasmic reticulum (ER) marker calreticulin. Additionally, NOX2 co-localized with F-actin at the plasma membrane. NOX2 and NOX4, which interacted with p22phox, as was shown by bimolecular fluorescent complementation, contributed equally to endothelial ROS production and proliferation, whereas NOX1 depletion did not alter ROS levels under basal conditions. These data show that endothelial cells simultaneously express NOX2, NOX4, and NOX1. NOX2 and NOX4, but not NOX1, equally contributed to ROS generation and proliferation under basal conditions, indicating that a complex relation between NOX homologues controls endothelial function.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Apocynin is an antioxidant and scavenger of ROS like HOCl and hydrogen peroxide.
“Moreover, there are several factors that question the inhibitory effects of apocynin; notably, apocynin is an antioxidant and scavenger of ROS like HOCl and hydrogen peroxide (426, 735).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [735]
Cites
1 retracted
Ushio‐Fukai, M., Tang, Y., Fukai, T., Dikalov, S., Ma, Y., Fujimoto, M., Quinn, M. T., Pagano, P. J., Johnson, C., & Alexander, R. W. (2002) · Circulation Research · doi:10.1161/01.res.0000046227.65158.f8 · Cited by 463 · see citing works
RetractedFree Radicals in the Physiological Control of Cell Function
Dröge, W. (2002) · Physiological Reviews · doi:10.1152/physrev.00018.2001 · Cited by 9,855 · see citing works
NOX enzymes and the biology of reactive oxygen
Lambeth, J. D. (2004) · Nature Reviews Immunology · doi:10.1038/nri1312 · Cited by 3,125 · see citing works
Segal, A. W. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115653 · Cited by 1,783 · see citing works
Hu, C., Chinenov, Y. V., & Kerppola, T. K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00496-3 · Cited by 1,537 · see citing works
Permanent cell line expressing human factor VIII-related antigen established by hybridization.
Edgell, C. J., McDonald, C., & Graham, J. B. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.12.3734 · Cited by 1,480 · see citing works
Reactive Oxygen Species in the Vasculature
Taniyama, Y., & Griendling, K. K. (2003) · Hypertension · doi:10.1161/01.hyp.0000100443.09293.4f · Cited by 1,067 · see citing works
Vascular NAD(P)H oxidases: specific features, expression, and regulation
Lassegue, B. P., & Clempus, R. E. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00758.2002 · Cited by 1,016 · see citing works
BABIOR, B. M., Lambeth, J. D., & Nauseef, W. M. (2002) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2001.2642 · Cited by 911 · see citing works
Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases
Martyn, K. D., Frederick, L. M., von Loehneysen, K., Dinauer, M. C., & Knaus, U. G. (2006) · Cellular Signalling · doi:10.1016/j.cellsig.2005.03.023 · Cited by 783 · see citing works
Hu, C., & Kerppola, T. K. (2003) · Nature Biotechnology · doi:10.1038/nbt816 · Cited by 783 · see citing works
Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology
Li, J.-M., & Shah, A. M. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00124.2004 · Cited by 773 · see citing works
The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases
Cai, H., Griendling, K. K., & Harrison, D. G. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00233-5 · Cited by 687 · see citing works
The Endoplasmic Reticulum: Folding, Calcium Homeostasis, Signaling, and Redox Control
Görlach, A., Klappa, P., & Kietzmann, T. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.1391 · Cited by 616 · see citing works
Self-citationGörlach, A., Brandes, R. P., Nguyen, K., Amidi, M., Dehghani, F., & Busse, R. (2000) · Circulation Research · doi:10.1161/01.res.87.1.26 · Cited by 598 · see citing works
Self-citationDistinct Subcellular Localizations of Nox1 and Nox4 in Vascular Smooth Muscle Cells
Hilenski, L. L., Clempus, R. E., Quinn, M. T., Lambeth, J. D., & Griendling, K. K. (2004) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000112024.13727.2c · Cited by 573 · see citing works
Hydrogen peroxide regulation of endothelial function: Origins, mechanisms, and consequences
Cai, H. “. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.06.021 · Cited by 568 · see citing works
Ambasta, R. K., Kumar, P., Griendling, K. K., Schmidt, H. H. H. W., Busse, R., & Brandes, R. P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406486200 · Cited by 541 · see citing works
A Novel Superoxide-producing NAD(P)H Oxidase in Kidney
Shiose, A., Kuroda, J., Tsuruya, K., Hirai, M., Hirakata, H., Naito, S., Hattori, M., Sakaki, Y., & Sumimoto, H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007597200 · Cited by 517 · see citing works
Nox4 as the Major Catalytic Component of an Endothelial NAD(P)H Oxidase
Ago, T., Kitazono, T., Ooboshi, H., Iyama, T., Han, Y. H., Takada, J., Wakisaka, M., Ibayashi, S., Utsumi, H., & Iida, M. (2004) · Circulation · doi:10.1161/01.cir.0000105680.92873.70 · Cited by 497 · see citing works
Reactive oxygen species as mediators of angiogenesis signaling. Role of NAD(P)H oxidase
Ushio‐Fukai, M., & Alexander, R. W. (2004) · Molecular and Cellular Biochemistry · doi:10.1023/b:mcbi.0000044378.09409.b5 · Cited by 473 · see citing works
The Nox Family of NAD(P)H Oxidases: Host Defense and Beyond
Geiszt, M., & Leto, T. L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.r400024200 · Cited by 452 · see citing works
Pédruzzi, E., Guichard, C., Ollivier, V., Driss, F., Fay, M., Prunet, C., Marie, J., Pouzet, C., Samadi, M. H., Elbim, C., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.24.10703-10717.2004 · Cited by 435 · see citing works
Assembly of the phagocyte NADPH oxidase
Nauseef, W. M. (2004) · Histochemistry and Cell Biology · doi:10.1007/s00418-004-0679-8 · Cited by 427 · see citing works
Thrombin Activates the Hypoxia-Inducible Factor-1 Signaling Pathway in Vascular Smooth Muscle Cells
Görlach, A., Diebold, I., Schini‐Kerth, V. B., Berchner‐Pfannschmidt, U., Roth, U., Brandes, R. P., Kietzmann, T., & Busse, R. (2001) · Circulation Research · doi:10.1161/hh1301.092678 · Cited by 416 · see citing works
Self-citationLi, J., & Shah, A. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110073200 · Cited by 395 · see citing works
Sorescu, G. P., Song, H. W., Tressel, S. L., Hwang, J., Dikalov, S., Smith, D. A., Boyd, N. L., Platt, M. O., Lassegue, B. P., Griendling, K. K., et al. (2004) · Circulation Research · doi:10.1161/01.res.0000145728.22878.45 · Cited by 379 · see citing works
Reactive Oxygen Species Produced by NAD(P)H Oxidase Inhibit Apoptosis in Pancreatic Cancer Cells
Vaquero, E. C., Edderkaoui, M., Pandol, S. J., Gukovsky, I., & Gukovskaya, A. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400078200 · Cited by 366 · see citing works
Expression and Localization of NOX2 and NOX4 in Primary Human Endothelial Cells
van Buul, J. D., Fernandez‐Borja, M., Anthony, E. C., & Hordijk, P. L. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.308 · Cited by 326 · see citing works
Differential Expression of Voltage-Gated K + Channel Subunits in Adult Rat Heart
Barry, D. M., Trimmer, J. S., Merlie, J. P., & Nerbonne, J. M. (1995) · Circulation Research · doi:10.1161/01.res.77.2.361 · Cited by 255 · see citing works
VEGF Signaling Through NADPH Oxidase-Derived ROS
Ushio‐Fukai, M. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1556 · Cited by 244 · see citing works
Janiszewski, M., Lopes, L. R., Carmo, A. O., Pedro, M. D. A., Brandes, R. P., Santos, C. X. C., & Laurindo, F. R. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509255200 · Cited by 243 · see citing works
Kawahara, T., Ritsick, D., Cheng, G., & Lambeth, J. D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501882200 · Cited by 231 · see citing works
Novel NAD(P)H oxidases in the cardiovascular system: Table 1
Griendling, K. K. (2004) · Heart · doi:10.1136/hrt.2003.029397 · Cited by 213 · see citing works
An NAD(P)H oxidase regulates growth and transcription in melanoma cells
Brar, S. S., Kennedy, T. P., Sturrock, A., Huecksteadt, T. P., Quinn, M. T., Whorton, A. R., & Hoidal, J. R. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00496.2001 · Cited by 178 · see citing works
NAD(P)H oxidase plays a crucial role in PDGF‐induced proliferation of hepatic stellate cells
Adachi, T., Togashi, H., Suzuki, A., Kasai, S., Ito, J., Sugahara, K., & Kawata, S. (2005) · Hepatology · doi:10.1002/hep.20719 · Cited by 169 · see citing works
Djordjevic, T., BelAiba, R. S., Bonello, S., Pfeilschifter, J. M., Hess, J., & Görlach, A. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000154279.98244.eb · Cited by 164 · see citing works
Self-citationCalafat, J., Kuijpers, T. W., Janssen, H., Borregaard, N., Verhoeven, A. J., & Roos, D. (1993) · Blood · doi:10.1182/blood.v81.11.3122.3122 · Cited by 137 · see citing works
NAD(P)H Oxidases in Rat Basilar Arterial Endothelial Cells
Ago, T., Kitazono, T., Kuroda, J., Kumai, Y., Kamouchi, M., Ooboshi, H., Wakisaka, M., Kawahara, T., Rokutan, K., Ibayashi, S., et al. (2005) · Stroke · doi:10.1161/01.str.0000163111.05825.0b · Cited by 135 · see citing works
Djordjevic, T., Pogrebniak, A., BelAiba, R. S., Bonello, S., Wotzlaw, C., Acker, H., Hess, J., & Görlach, A. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.09.036 · Cited by 134 · see citing works
Self-citationIkeda, S., Yamaoka‐Tojo, M., Hilenski, L. L., Patrushev, N. A., Anwar, G. M., Quinn, M. T., & Ushio‐Fukai, M. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000187472.55437.af · Cited by 129 · see citing works
Peng, T., Lu, X., & Feng, Q. (2005) · Circulation · doi:10.1161/01.cir.0000160366.50210.e9 · Cited by 123 · see citing works
Guzik, T. J., Sadowski, J., Kapelak, B., Jopek, A., Rudziński, P., Pillai, R. G., Korbut, R., & Channon, K. M. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000139011.94634.9d · Cited by 119 · see citing works
Herkert, O., Diebold, I., Brandes, R. P., Hess, J., Busse, R., & Görlach, A. (2002) · Circulation · doi:10.1161/01.cir.0000014611.28864.1e · Cited by 117 · see citing works
Self-citationRegulation of NADPH oxidase subunit p22phoxby NF-kB in human aortic smooth muscle cells
Manea, A., Manea, S., Gafencu, A. V., & Raicu, M. (2007) · Archives of Physiology and Biochemistry · doi:10.1080/13813450701531235 · Cited by 113 · see citing works
Yamagishi, S., Nakamura, K., Ueda, S., Kato, S., & Imaizumi, T. (2005) · Cell and Tissue Research · doi:10.1007/s00441-005-1094-8 · Cited by 111 · see citing works
Fürst, R., Brueckl, C., Kuebler, W. M., Stefan Zahler, A., Krötz, F., Görlach, A., Vollmar, A. M., & Kiemer, A. K. (2004) · Circulation Research · doi:10.1161/01.res.0000151983.01148.06 · Cited by 110 · see citing works
Self-citationShen, W., Gao, P., Che, Z.-Q., Ji, K., Yin, M., Chen, Y., Berk, B. C., & Zhu, D. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.10.207 · Cited by 90 · see citing works
Herkert, O., Djordjevic, T., BelAiba, R. S., & Görlach, A. (2004) · Antioxidants and Redox Signaling · doi:10.1089/1523086041361695 · Cited by 71 · see citing works
Self-citationReactive oxygen species modulate HIF-1 mediated PAI-1 expression: involvement of the GTPase Rac1
Berchner-Pfannschmidt, U., Wotzlaw, C., Cool, R., Fandrey, J., Acker, H., Jungermann, K., Görlach, A., & Kietzmann, T. (2003) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1613480 · Cited by 68 · see citing works
Self-citationNox2 regulates endothelial cell cycle arrest and apoptosis via p21cip1 and p53
Li, J., Fan, L. M., George, V. T., & Brooks, G. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.06.001 · Cited by 65 · see citing works
Kobayashi, S., Nojima, Y., Shibuya, M., & Maru, Y. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.07.023 · Cited by 65 · see citing works
NADPH Oxidases: New Regulators of Old Functions
Griendling, K. K. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.1443 · Cited by 55 · see citing works
Reactive oxygen species modulate HIF-1 mediated PAI-1 expression: involvement of the GTPase Rac1.
Görlach, A., Berchner‐Pfannschmidt, U., Wotzlaw, C., Cool, R. H., Fandrey, J., Acker, H., Jungermann, K. A., & Kietzmann, T. (2003) · PubMed · doi:10.1267/thro03050926 · Cited by 54 · see citing works
Self-citationRedox Signaling through NADPH Oxidases: Involvement in Vascular Proliferation and Coagulation
Görlach, A., Kietzmann, T., & Hess, J. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04691.x · Cited by 53 · see citing works
Self-citationPari, G. S., & Keown, W. A. (2003) · Humana Press eBooks · doi:10.1385/0-89603-480-1:301 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Reactive Oxygen Species in Inflammation and Tissue Injury
Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P., & Malik, A. B. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.5149 · Cited by 4,897 · see citing works
Calcium and ROS: A mutual interplay
Görlach, A., Bertram, K., Hudecova, S., & Krizanova, O. (2015) · Redox Biology · doi:10.1016/j.redox.2015.08.010 · Cited by 1,546 · see citing works
Self-citationCombating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets
Drummond, G. R., Selemidis, S., Griendling, K. K., & Sobey, C. G. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3403 · Cited by 899 · see citing works
Biochemistry, Physiology, and Pathophysiology of NADPH Oxidases in the Cardiovascular System
Lassegue, B. P., Martín, A. S., & Griendling, K. K. (2012) · Circulation Research · doi:10.1161/circresaha.111.243972 · Cited by 768 · see citing works
Kerppola, T. K. (2008) · Annual Review of Biophysics · doi:10.1146/annurev.biophys.37.032807.125842 · Cited by 712 · see citing works
Oxidative stress in angiogenesis and vascular disease
Kim, Y.-W., & Byzova, T. V. (2013) · Blood · doi:10.1182/blood-2013-09-512749 · Cited by 709 · see citing works
Nox enzymes, ROS, and chronic disease: An example of antagonistic pleiotropy
Lambeth, J. D. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.03.027 · Cited by 677 · see citing works
Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy
Ushio‐Fukai, M., & Nakamura, Y. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.02.044 · Cited by 651 · see citing works
Reactive Oxygen Species Activate the HIF-1α Promoter Via a Functional NFκB Site
Bonello, S., Zähringer, C., BelAiba, R. S., Djordjevic, T., Hess, J., Michiels, C., Kietzmann, T., & Görlach, A. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000258979.92828.bc · Cited by 626 · see citing works
Self-citationThe Endoplasmic Reticulum: Folding, Calcium Homeostasis, Signaling, and Redox Control
Görlach, A., Klappa, P., & Kietzmann, T. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.1391 · Cited by 616 · see citing works
Self-citationNADPH Oxidases: Functions and Pathologies in the Vasculature
Lassègue, B., & Griendling, K. K. (2010) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.181610 · Cited by 592 · see citing works
Jiang, F., Zhang, Y., & Dusting, G. J. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.002980 · Cited by 574 · see citing works
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
Evolution of nadph oxidase inhibitors: Selectivity and mechanisms for target engagement
Altenhöfer, S., Radermacher, K. A., Kleikers, P. W. M., Wingler, K., & Schmidt, H. H. H. W. (2015) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5814 · Cited by 521 · see citing works
Reactive oxygen species and vascular biology: implications in human hypertension
Touyz, R. M., & Briones, A. M. (2010) · Hypertension Research · doi:10.1038/hr.2010.201 · Cited by 469 · see citing works
Regulation of ROS signal transduction by NADPH oxidase 4 localization
Chen, K., Kirber, M. T., Xiao, H. Q., Yang, Y., & Keaney, J. F. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200709049 · Cited by 468 · see citing works
NADPH Oxidase-Dependent Signaling in Endothelial Cells: Role in Physiology and Pathophysiology
Frey, R. S., Ushio‐Fukai, M., & Malik, A. B. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2220 · Cited by 423 · see citing works
Kellner, M., Noonepalle, S. K. R., Lü, Q., Srivastava, A., Zemskov, E. A., & Black, S. M. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-63245-2_8 · Cited by 411 · see citing works
Dikalov, S., Dikalova, A., Bikineyeva, A. T., Schmidt, H. H. H. W., Harrison, D. G., & Griendling, K. K. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.08.013 · Cited by 386 · see citing works
Thomas, S. R., Witting, P. K., & Drummond, G. R. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2027 · Cited by 383 · see citing works
The NOX toolbox: validating the role of NADPH oxidases in physiology and disease
Altenhöfer, S., Kleikers, P. W. M., Radermacher, K. A., Scheurer, P., Rob Hermans, J. J., Schiffers, P., Ho, H., Wingler, K., & Schmidt, H. H. H. W. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1010-9 · Cited by 371 · see citing works
Compartmentalization of Redox Signaling Through NADPH Oxidase–Derived ROS
Ushio‐Fukai, M. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2333 · Cited by 365 · see citing works
Reactive oxygen species, nutrition, hypoxia and diseases: Problems solved?
Görlach, A., Dimova, E. Y., Petry, A., Martı́nez-Ruiz, A., Hernansanz‐Agustín, P., Rolo, A. P., Palmeira, C. M., & Kietzmann, T. (2015) · Redox Biology · doi:10.1016/j.redox.2015.08.016 · Cited by 351 · see citing works
Self-citationAldosterone: effects on the kidney and cardiovascular system
Briet, M. B., & Schiffrin, E. L. (2010) · Nature Reviews Nephrology · doi:10.1038/nrneph.2010.30 · Cited by 337 · see citing works
Mittal, M., Roth, M., König, P., Hofmann, S., Dony, E., Goyal, P., Selbitz, A.-C., SCHERMULY, R. T., Ghofrani, H. A., Kwapiszewska, G., et al. (2007) · Circulation Research · doi:10.1161/circresaha.107.148015 · Cited by 328 · see citing works
Expression and Localization of NOX2 and NOX4 in Primary Human Endothelial Cells
van Buul, J. D., Fernandez‐Borja, M., Anthony, E. C., & Hordijk, P. L. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.308 · Cited by 326 · see citing works
Reactive oxygen species and fibrosis: further evidence of a significant liaison
Richter, K., & Kietzmann, T. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2445-3 · Cited by 322 · see citing works
Self-citationEgea, 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
Self-citationCross-Talk between NADPH Oxidase and Mitochondria: Role in ROS Signaling and Angiogenesis
Fukai, T., & Ushio‐Fukai, M. (2020) · Cells · doi:10.3390/cells9081849 · Cited by 302 · see citing works
The NADPH Oxidase Subunit NOX4 Is a New Target Gene of the Hypoxia-inducible Factor-1
Diebold, I., Petry, A., Hess, J., & Görlach, A. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-12-1003 · Cited by 296 · see citing works
Self-citationOxidative 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
NOX5 variants are functionally active in endothelial cells
BelAiba, R. S., Djordjevic, T., Petry, A., Diemer, K., Bonello, S., Banfi, B., Hess, J., Pogrebniak, A., Bickel, C., & Görlach, A. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.10.054 · Cited by 255 · see citing works
Self-citationKim, Y.-M., Kim, S.-J., Tatsunami, R., Yamamura, H., Fukai, T., & Ushio-Fukai, M. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00346.2016 · Cited by 251 · see citing works
Ghouleh, I. A., Khoo, N. K. H., Knaus, U. G., Griendling, K. K., Touyz, R. M., Thannickal, V. J., Barchowsky, A., Nauseef, W. M., Kelley, E. E., Bauer, P. M., et al. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.06.011 · Cited by 249 · see citing works
VEGF Signaling Through NADPH Oxidase-Derived ROS
Ushio‐Fukai, M. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1556 · Cited by 244 · see citing works
Selemidis, S., Sobey, C. G., Wingler, K., Schmidt, H. H. H. W., & Drummond, G. R. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.08.005 · Cited by 241 · see citing works
Redox-fibrosis: Impact of TGFβ1 on ROS generators, mediators and functional consequences
Richter, K., Konzack, A., Pihlajaniemi, T. A., Heljäsvaara, R., & Kietzmann, T. (2015) · Redox Biology · doi:10.1016/j.redox.2015.08.015 · Cited by 240 · see citing works
Self-citationNADPH oxidase 4 is an oncoprotein localized to mitochondria
Graham, K., Kulawiec, M., Owens, K. M., Li, X., Desouki, M. M., Chandra, D., & Singh, K. K. (2010) · Cancer Biology & Therapy · doi:10.4161/cbt.10.3.12207 · Cited by 236 · see citing works
Nox enzymes as novel targets for drug development
Lambeth, J. D., Krause, K.-H., & Clark, R. A. (2008) · Seminars in Immunopathology · doi:10.1007/s00281-008-0123-6 · Cited by 212 · see citing works
NADPH Oxidases: A Perspective on Reactive Oxygen Species Production in Tumor Biology
Meitzler, J. L., Antony, S., Wu, Y., Juhasz, A. N., Liu, H., Jiang, G., Lu, J., Roy, K., & Doroshow, J. H. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5603 · Cited by 205 · see citing works
Li, J., Wang, J. J., Yu, Q., Chen, K., Mahadev, K., & Zhang, S. X. (2010) · Diabetes · doi:10.2337/db09-1057 · Cited by 199 · see citing works
The superoxide radical switch in the biology of nitric oxide and peroxynitrite
Piacenza, L., Zeida, A., Trujillo, M., & Radí, R. (2022) · Physiological Reviews · doi:10.1152/physrev.00005.2022 · Cited by 204 · see citing works
Guo, Z. J., Niu, H. X., Hou, F. F., Zhang, L., Fu, N., Nagai, R., Lu, X., Chen, B. H., Shan, Y., Tian, J. W., et al. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1999 · Cited by 193 · see citing works
Montezano, A. C., Burger, D., Paravicini, T. M., Chignalia, A. Z., Yusuf, H., Almasri, M., He, Y., Callera, G. E., He, G., Krause, K.-H., et al. (2010) · Circulation Research · doi:10.1161/circresaha.109.216036 · Cited by 188 · see citing works
Yetkin-Arik, B., Vogels, I. M. C., Nowak-Sliwinska, P. M., Weiss, A., Houtkooper, R. H., Noorden, C. J. F. V., Klaassen, I., & Schlingemann, R. O. (2019) · Scientific Reports · doi:10.1038/s41598-019-48676-2 · Cited by 186 · see citing works
Regulation of myocardial growth and death by NADPH oxidase
Maejima, Y., Kuroda, J., Matsushima, S., Ago, T., & Sadoshima, J. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.12.018 · Cited by 185 · see citing works
Datla, S. R., Peshavariya, H., Dusting, G. J., Mahadev, K., Goldstein, B. J., & Jiang, F. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.149450 · Cited by 178 · see citing works
Role of Reactive Oxygen Species in Tumor Necrosis Factor-alpha Induced Endothelial Dysfunction
Chen, X., Andresen, B. T., Hill, M. A., Zhang, J., Booth, F. W., & Zhang, C. (2008) · Current Hypertension Reviews · doi:10.2174/157340208786241336 · Cited by 179 · see citing works
From form to function: the role of Nox4 in the cardiovascular system
Chen, F., Haigh, S. B., Barman, S. A., & Fulton, D. J. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00412 · Cited by 172 · see citing works
ACE2–angiotensin-(1–7)–Mas axis and oxidative stress in cardiovascular disease
Rabelo, L. A., Alenina, N. V., & Bäder, M. (2010) · Hypertension Research · doi:10.1038/hr.2010.235 · Cited by 171 · see citing works
Reactive Oxygen Species Scavenging Nanomedicine for the Treatment of Ischemic Heart Disease
Zhang, Z., Dalan, R., Hu, Z., Wang, J., Chew, N., Poh, K. K., Tan, R., Soong, T. W., Dai, Y., Ye, L., et al. (2022) · Advanced Materials · doi:10.1002/adma.202202169 · Cited by 174 · see citing works
Nox4 regulates Nrf2 and glutathione redox in cardiomyocytes in vivo
Brewer, A. C., Murray, T. V., Arno, M. J., Zhang, M., Anilkumar, N. P., Mann, G. E., & Shah, A. M. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.022 · Cited by 167 · see citing works
Receptor Activation of NADPH Oxidases
Petry, A., Weitnauer, M., & Görlach, A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.3026 · Cited by 162 · see citing works
Self-citationChan, E. C., Jiang, F., Peshavariya, H., & Dusting, G. J. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.005 · Cited by 162 · see citing works
Targeting Vascular NADPH Oxidase 1 Blocks Tumor Angiogenesis through a PPARα Mediated Mechanism
Garrido-Urbani, S., Jemelin, S., Deffert, C., Carnesecchi, S., Basset, O., Szyndralewiez, C., Heitz, F., Page, P., Montet, X., Michalik, L., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014665 · Cited by 143 · see citing works
Novel Role of NADPH Oxidase in Angiogenesis and Stem/Progenitor Cell Function
Ushio‐Fukai, M., & Urao, N. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2582 · Cited by 142 · see citing works
Soucy-Faulkner, A., Mukawera, E., Fink, K., Martel, A., Jouan, L., Nzengue, Y., Lamarre, D., Velde, C. V., & Grandvaux, N. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000930 · Cited by 142 · see citing works
Reactive oxygen species, Nox and angiotensin II in angiogenesis: implications for retinopathy
Wilkinson‐Berka, J. L., Rana, I., Armani, R., & Agrotis, A. (2013) · Clinical Science · doi:10.1042/cs20120212 · Cited by 140 · see citing works
Redox State of the Endoplasmic Reticulum Is Controlled by Ero 1L-alpha and Intraluminal Calcium
Enyedi, B., Várnai, P., & Geiszt, M. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2880 · Cited by 135 · see citing works
The NADPH Oxidase Family and its Inhibitors
Kleniewska, P., Piechota-Polańczyk, A., Skibska, B., & Gorąca, A. (2012) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-012-0176-z · Cited by 129 · see citing works
Li, S., Tabar, S. S., Malec, V., Eul, B. G., Klepetko, W., Weißmann, N., Grimminger, F., Seeger, W., Rose, F., & Hänze, J. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2035 · Cited by 129 · see citing works
Redox regulation of Nox proteins
Pendyala, S., & Natarajan, V. (2010) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2010.09.016 · Cited by 126 · see citing works
Pendyala, S., Usatyuk, P. V., Gorshkova, I. A., Garcia, J. G. N., & Natarajan, V. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2231 · Cited by 123 · see citing works
Regulation of NAD(P)H oxidases by AMPK in cardiovascular systems
Song, P., & Zou, M. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.01.025 · Cited by 119 · see citing works
Veith, C., Boots, A. W., Idris, M., van Schooten, F., & van der Vliet, A. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7742 · Cited by 113 · see citing works
The human Nox4: gene, structure, physiological function and pathological significance
Guo, S., & Chen, X. (2015) · Journal of drug targeting · doi:10.3109/1061186x.2015.1036276 · Cited by 113 · see citing works
NOX Isoforms and Reactive Oxygen Species in Vascular Health
Touyz, R. M., Briones, A. M., Sedeek, M. H., Burger, D. E., & Montezano, A. C. (2011) · Molecular Interventions · doi:10.1124/mi.11.1.5 · Cited by 113 · see citing works
Nox2 impairs VEGF-A-induced angiogenesis in placenta via mitochondrial ROS-STAT3 pathway
Hu, C., Wu, Z.-F., Huang, Z., Hao, X.-Y., Wang, S., Deng, J.-P., Yin, Y.-L., & Tan, C.-Q. (2021) · Redox Biology · doi:10.1016/j.redox.2021.102051 · Cited by 104 · see citing works
Regulation of NADPH oxidase subunit p22phoxby NF-kB in human aortic smooth muscle cells
Manea, A., Manea, S., Gafencu, A. V., & Raicu, M. (2007) · Archives of Physiology and Biochemistry · doi:10.1080/13813450701531235 · Cited by 113 · see citing works
Mechanisms of mineralocorticoid receptor-mediated cardiac fibrosis and vascular inflammation
Young, M. J. (2008) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0b013e3282f56854 · Cited by 112 · see citing works
Reactive Oxygen Species and Endothelial Activation
Alom-Ruiz, S. P., Anilkumar, N. P., & Shah, A. M. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.2007 · Cited by 111 · see citing works
Tong, X., Hou, X., Jourd’heuil, D., Weisbrod, R. M., & Cohen, R. A. (2010) · Circulation Research · doi:10.1161/circresaha.110.221242 · Cited by 110 · see citing works
Knock, G. A. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.09.029 · Cited by 108 · see citing works
AP-1–Dependent Transcriptional Regulation of NADPH Oxidase in Human Aortic Smooth Muscle Cells
Manea, A., Manea, S., Gafencu, A. V., Raicu, M., & Simionescu, M. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.163592 · 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
Paradoxical Activation of Endothelial Nitric Oxide Synthase by NADPH Oxidase
Zhang, Q., Malik, P., Pandey, D., Gupta, S. A., Jagnandan, D., de Chantemèle, E. J. B., Bánfi, B., Marrero, M. B., Rudic, R. D., Stepp, D. W., et al. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.168278 · Cited by 107 · see citing works
NADPH oxidases: redox regulation of cell homeostasis and disease
Kračun, D., Lopes, L. R., Cifuentes-Pagano, E., & Pagano, P. J. (2025) · Physiological Reviews · doi:10.1152/physrev.00034.2023 · Cited by 104 · see citing works
NADPH oxidase isoform selective regulation of endothelial cell proliferation and survival
Peshavariya, H., Dusting, G. J., Jiang, F., Halmos, L. R., Sobey, C. G., Drummond, G. R., & Selemidis, S. (2009) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-009-0413-0 · Cited by 101 · see citing works
NADPH Oxidases as Regulators of Tumor Angiogenesis: Current and Emerging Concepts
Coso, S., Harrison, I., Harrison, C. B., Vinh, A., Sobey, C. G., Drummond, G. R., Williams, E. D., & Selemidis, S. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4489 · Cited by 99 · see citing works
Wei, X. F., Zhou, Q. G., Hou, F. F., Liu, B. Y., & Liang, M. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.90536.2008 · Cited by 98 · see citing works
Evidence for a Superoxide Permeability Pathway in Endosomal Membranes
Mumbengegwi, D. R., Li, Q., Li, C., Bear, C. E., & Engelhardt, J. F. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.02038-07 · Cited by 98 · see citing works
Nitric Oxide, NAD(P)H Oxidase, and Atherosclerosis
Müller, G. M., & Morawietz, H. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2403 · Cited by 96 · see citing works
Hong, D., Bai, Y., Gao, H.-C., Wang, X., Li, L., Zhang, G., & Hu, C.-P. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.04.028 · Cited by 97 · see citing works
The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells
Lener, B., Kozieł, R., Pircher, H., Hütter, E., Greussing, R., Herndler‐Brandstetter, D., Hermann, M., Unterluggauer, H., & Jansen‐Dürr, P. (2009) · Biochemical Journal · doi:10.1042/bj20090666 · Cited by 97 · see citing works
NOX2 As a Target for Drug Development: Indications, Possible Complications, and Progress
Diebold, B. A., Smith, S. M., Yang, L., & Lambeth, J. D. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5862 · Cited by 96 · see citing works
Basuroy, S., Tcheranova, D., Bhattacharya, S., Leffler, C. W., & Parfenova, H. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00272.2010 · Cited by 96 · see citing works
Reactive Oxygen Species in Endothelial Function – From Disease to Adaptation –
Craige, S. M., Kant, S., & Keaney, J. F. (2015) · Circulation Journal · doi:10.1253/circj.cj-15-0464 · Cited by 91 · see citing works
Reactive oxygen species and the neuronal fate
Kennedy, K. A. M., Sandiford, S. D. E., Skerjanc, I. S., & Li, S. S.-C. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0807-2 · Cited by 89 · see citing works
Cannabidiol modulation of oxidative stress and signalling
Pereira, S. R., Hackett, B., O’Driscoll, D. N., Sun, M. C., & Downer, E. J. (2021) · Neuronal Signaling · doi:10.1042/ns20200080 · Cited by 90 · see citing works
Reactive Oxygen Species in Vascular Formation and Development
Zhou, Y., Yan, H. M., Guo, M., Zhu, J., Xiao, Q., & Zhang, L. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/374963 · Cited by 85 · see citing works
ROS-activated calcium signaling mechanisms regulating endothelial barrier function
Di, A., Mehta, D., & Malik, A. B. (2016) · Cell Calcium · doi:10.1016/j.ceca.2016.02.002 · Cited by 82 · see citing works
Microvascular NADPH oxidase in health and disease
Li, Y., & Pagano, P. J. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.02.049 · Cited by 79 · see citing works
Evangelista, A. M., Thompson, M. D., Bolotina, V. M., Tong, X., & Cohen, R. A. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.546 · Cited by 78 · see citing works
Diebold, I., Djordjevic, T., Petry, A., Hatzelmann, A., Tenor, H., Hess, J., & Görlach, A. (2009) · Circulation Research · doi:10.1161/circresaha.109.196592 · Cited by 75 · see citing works
Self-citationShafique, E., Torina, A. G., Reichert, K., Colantuono, B. J., Nur, N., Zeeshan, K., Ravichandran, V. S., Liu, Y., Feng, J., Zeeshan, K., et al. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw249 · Cited by 74 · see citing works
Daiber, A., Andreadou, I., Oelze, M. W., Davidson, S. M., & Hausenloy, D. J. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.12.026 · Cited by 73 · see citing works
Siegmund, U., Heller, J., van Kan, J. A. L., & Tudzynski, P. (2013) · PLoS ONE · doi:10.1371/annotation/84c258cf-4f98-43d8-a4f0-7032cba36f22 · Cited by 73 · see citing works
Sipkens, J. A., Hahn, N. E., den Brand, C. S., Meischl, C., Cillessen, S. A. G. M., Smith, D. E. C., Juffermans, L. J. M., Musters, R. J. P., Roos, D., Jakobs, C., et al. (2011) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-011-9297-y · Cited by 71 · see citing works
The Importance of NADPH Oxidases and Redox Signaling in Angiogenesis
Prieto-Bermejo, R., & Hernández‐Hernández, Á. (2017) · Antioxidants · doi:10.3390/antiox6020032 · Cited by 73 · see citing works
Sima, A. V., Botez, G. M., Stancu, C. S., Manea, A., Raicu, M., & Simionescu, M. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00933.x · Cited by 70 · see citing works
- Authors
- Petry, A., Djordjevic, T., Weitnauer, M., Kietzmann, T., Hess, J., & Görlach, A.
- Affiliations
- Deutsches Herzzentrum München (DE)
- University of Kaiserslautern (DE)
- Venue
- Antioxidants & Redox Signaling
- Publisher
- SAGE Publications
- Published
- 2006-09
- Volume
- 8
- Issue
- 9-10
- Pages
- 1473-1484
- ISSN
- 1523-0864 (ISSN-L)
- 1557-7716
- OpenAlex
- W1985234565
- Cited by
- 243
- References
- 56
- Citations by year
- 2026: 1 · 2025: 8 · 2024: 3 · 2023: 7 · 2022: 6 · 2021: 9 · 2020: 12 · 2019: 14 · 2018: 8 · 2017: 11 · 2016: 8 · 2015: 12 · 2014: 11 · 2013: 19 · 2012: 21
- FWCI
- 11.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Antioxidants and Redox Signaling (publishedVersion)
- PubMed (publishedVersion)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Health Sciences › Medicine › Physiology › 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
- NOX2, NOX4, NOX1, NADPH oxidase, endothelial cells, reactive oxygen species, endothelial cell proliferation, p22phox, calreticulin, endoplasmic reticulum, F-actin, microvascular endothelial cells, EA.hy926 cells, endothelial function
- MeSH terms
- NADPH Oxidase 1, NADPH Oxidase 2, NADPH Oxidase 4, Actins, Cell Line, Endoplasmic Reticulum, Humans, Membrane Glycoproteins, Microsomes, Phosphorylation, Transfection, Gene Expression, Reactive Oxygen Species, NADPH Oxidases, Protein Interaction Mapping, RNA, Small Interfering, Calreticulin, Endothelial Cells, Protein Kinase Inhibitors, Immunoprecipitation, p38 Mitogen-Activated Protein Kinases, Cell Proliferation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review