Organizers and activators: Cytosolic Nox proteins impacting on vascular function

Free Radical Biology and Medicine

Volumn 109, Issue , 2017, Pages 22-32

  Schröder, Katrin ^a   Weissmann, Norbert ^b   Brandes, Ralf P ^a  

^a GOETHE UNIVERSITY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

Activity control; NADPH oxidase; Nox; NoxA1; NoxO1; Oxygen derived free radicals; p22phox; p47phox; p67phox; Phosphorylation

Indexed keywords

APOCYNIN; CELL MEMBRANE PROTEIN; CELL PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; NOXA1 PROTEIN; NOXO1 PROTEIN; OXIDOREDUCTASE; P40PHOX PROTEIN; P47PHOX PROTEIN; P67PHOX PROTEIN; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; NEUTROPHIL CYTOSOL FACTOR 67K; NEUTROPHIL CYTOSOLIC FACTOR 1; NOXA1 PROTEIN, HUMAN; NOXO1 PROTEIN, HUMAN; PHOSPHOPROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANGIOGENESIS; ANTIOXIDANT ACTIVITY; BONE MARROW CELL; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CELL MIGRATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CYTOSOL; EXON; HUMAN; INTRON; MOLECULAR WEIGHT; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; VASCULAR ENDOTHELIUM; ANIMAL; CYTOLOGY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CARDIOVASCULAR SYSTEM; CYTOSOL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; NADPH OXIDASES; OXIDATION-REDUCTION; PHOSPHOPROTEINS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 85015983040     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2017.03.017     Document Type: Review

References (150)

1. Brandes, R.P., Weissmann, N., Schroder, K., Nox family NADPH oxidases: molecular mechanisms of activation. Free Radic. Biol. Med. 76 (2014), 208–226.
2. Bedard, K., Krause, K.-H., The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:1 (2007), 245–313.
3. Deken, X., de, Wang, D., Many, M.C., Costagliola, S., Libert, F., Vassart, G., et al. Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J. Biol. Chem. 275:30 (2000), 23227–23233.
4. Gorlach, A., Brandes, R.P., Nguyen, K., Amidi, M., Dehghani, F., Busse, R., A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ. Res 87:1 (2000), 26–32.
5. Brandes, R.P., Weissmann, N., Schroder, K., Redox-mediated signal transduction by cardiovascular Nox NADPH oxidases. J. Mol. Cell Cardiol. 73 (2014), 70–79.
6. Schurmann, C., Rezende, F., Kruse, C., Yasar, Y., Lowe, O., Fork, C., et al. The NADPH oxidase Nox4 has anti-atherosclerotic functions. Eur. Heart J. 36:48 (2015), 3447–3456.
7. Witting, P.K., Rayner, B.S., Wu, B.-J., Ellis, N.A., Stocker, R., Hydrogen peroxide promotes endothelial dysfunction by stimulating multiple sources of superoxide anion radical production and decreasing nitric oxide bioavailability. Cell Physiol. Biochem. 20:5 (2007), 255–268.
8. Cascino, T., Csanyi, G., Al Ghouleh, I., Montezano, A.C., Touyz, R.M., Haurani, M.J., et al. Adventitia-derived hydrogen peroxide impairs relaxation of the rat carotid artery via smooth muscle cell p38 mitogen-activated protein kinase. Antioxid. Redox Signal. 15:6 (2011), 1507–1515.
9. 9] Wenzel, P., Kossmann, S., Munzel, T., Daiber, A., Redox regulation of cardiovascular inflammation - Immunomodulatory function of mitochondrial and Nox-derived reactive oxygen and nitrogen species. Free Radic. Biol. Med., 2017.
10. Graier, W.F., Hoebel, B.G., Paltauf-Doburzynska, J., Kostner, G.M., Effects of Superoxide Anions on Endothelial Ca2+ Signaling Pathways. Arterioscler. Thromb. Vasc. Biol. 18:9 (1998), 1470–1479.
11. Shafique, E., Choy, W.C., Liu, Y., Feng, J., Cordeiro, B., Lyra, A., et al. Oxidative stress improves coronary endothelial function through activation of the pro-survival kinase AMPK. Aging 5:7 (2013), 515–530.
12. Fan, L.M., Douglas, G., Bendall, J.K., McNeill, E., Crabtree, M.J., Hale, A.B., et al. Endothelial cell-specific reactive oxygen species production increases susceptibility to aortic dissection. Circulation 129:25 (2014), 2661–2672.
13. Landmesser, U., Dikalov, S., Price, S.R., McCann, L., Fukai, T., Holland, S.M., et al. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J. Clin. Investig. 111:8 (2003), 1201–1209.
14. Schroder, K., Kohnen, A., Aicher, A., Liehn, E.A., Buchse, T., Stein, S., et al. NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ. Res. 105:6 (2009), 537–544.
15. Kawahara, T., Jackson, H.M., Smith, S.M.E., Simpson, P.D., Lambeth, J.D., Nox5 forms a functional oligomer mediated by self-association of its dehydrogenase domain. Biochemistry 50:12 (2011), 2013–2025.
16. Bedard, K., Jaquet, V., Krause, K.-H., NOX5: from basic biology to signaling and disease. Free Radic. Biol. Med 52:4 (2012), 725–734.
17. Deken, X., de, Corvilain, B., Dumont, J.E., Miot, F., Roles of DUOX-mediated hydrogen peroxide in metabolism, host defense, and signaling. Antioxid. Redox Signal. 20:17 (2014), 2776–2793.
18. Prior, K.-K., Leisegang, M.S., Josipovic, I., Lowe, O., Shah, A.M., Weissmann, N., et al. CRISPR/Cas9-mediated knockout of p22phox leads to loss of Nox1 and Nox4, but not Nox5 activity. Redox Biol. 9 (2016), 287–295.
19. Stasia, M.J., CYBA encoding p22phox, the cytochrome b558 alpha polypeptide: gene structure, expression, role and physiopathology. Gene 586:1 (2016), 27–35.
20. Geiszt, M., Kopp, J.B., Varnai, P., Leto, T.L., Identification of renox, an NAD(P)H oxidase in kidney. Proc. Natl. Acad. Sci. USA 97:14 (2000), 8010–8014.
21. Ambasta, R.K., Kumar, P., Griendling, K.K., Schmidt, H.H.H.W., Busse, R., Brandes, R.P., Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279:44 (2004), 45935–45941.
22. Takac, I., Schroder, K., Zhang, L., Lardy, B., Anilkumar, N., Lambeth, J.D., et al. The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4. J. Biol. Chem. 286:15 (2011), 13304–13313.
23. Kim, J.-S., Diebold, B.A., Babior, B.M., Knaus, U.G., Bokoch, G.M., Regulation of Nox1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding. J. Biol. Chem. 282:48 (2007), 34787–34800.
24. Lohneysen, K., von, Noack, D., Wood, M.R., Friedman, J.S., Knaus, U.G., Structural insights into Nox4 and Nox2: motifs involved in function and cellular localization. Mol. Cell Biol. 30:4 (2010), 961–975.
25. Cheng, G., Ritsick, D., Lambeth, J.D., Nox3 regulation by NOXO1, p47phox, and p67phox. J. Biol. Chem. 279:33 (2004), 34250–34255.
26. Pick, E., Role of the Rho GTPase Rac in the activation of the phagocyte NADPH oxidase: outsourcing a key task. Small GTPases, 5, 2014, e27952.
27. Hordijk, P.L., Regulation of NADPH oxidases: the role of Rac proteins. Circ. Res. 98:4 (2006), 453–462.
28. Ueyama, T., Geiszt, M., Leto, T.L., Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol. Cell Biol. 26:6 (2006), 2160–2174.
29. Adam, O., Laufs, U., Rac1-mediated effects of HMG-CoA reductase inhibitors (statins) in cardiovascular disease. Antioxid. Redox Signal. 20:8 (2014), 1238–1250.
30. Marinkovic, G., Heemskerk, N., van Buul, J.D., Waard, V. de, The Ins and Outs of Small GTPase Rac1 in the Vasculature. J. Pharmacol. Exp. Ther. 354:2 (2015), 91–102.
31. Lassegue, B., Griendling, K.K., NADPH oxidases: functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 30:4 (2010), 653–661.
32. Banfi, B., Clark, R.A., Steger, K., Krause, K.-H., Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 278:6 (2003), 3510–3513.
33. Takeya, R., Ueno, N., Kami, K., Taura, M., Kohjima, M., Izaki, T., et al. Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases. J. Biol. Chem. 278:27 (2003), 25234–25246.
34. Kawano, M., Miyamoto, K., Kaito, Y., Sumimoto, H., Tamura, M., Noxa1 as a moderate activator of Nox2-based NADPH oxidase. Arch. Biochem. Biophys. 519:1 (2012), 1–7.
35. Banfi, B., Malgrange, B., Knisz, J., Steger, K., Dubois-Dauphin, M., Krause, K.-H., NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279:44 (2004), 46065–46072.
36. Lomax, K.J., Leto, T.L., Nunoi, H., Gallin, J.I., Malech, H.L., Recombinant 47-kilodalton cytosol factor restores NADPH oxidase in chronic granulomatous disease. Science 245:4916 (1989), 409–412 Available from: URL 〈 http://science.sciencemag.org/content/sci/245/4916/409.full.pdf〉.
37. Volpp, B.D., Nauseef, W.M., Donelson, J.E., Moser, D.R., Clark, R.A., Cloning of the cDNA and functional expression of the 47-kilodalton cytosolic component of human neutrophil respiratory burst oxidase. PNAS 86:18 (1989), 7195–7199 Available from: URL 〈 http://www.pnas.org/content/86/18/7195.full.pdf〉.
38. Groemping, Y., Rittinger, K., Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J. 386:3 (2005), 401–416 Available from: URL 〈 http://www.biochemj.org/content/ppbiochemj/386/3/401.full.pdf〉.
39. Groemping, Y., Lapouge, K., Smerdon, S.J., Rittinger, K., Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113:3 (2003), 343–355.
40. Leto, T.L., Adams, A.G., Mendez, Id, Assembly of the phagocyte NADPH oxidase: binding of Src homology 3 domains to proline-rich targets. PNAS 91:22 (1994), 10650–10654 Available from: URL 〈 http://www.pnas.org/content/91/22/10650.full.pdf〉.
41. Faust, L.R., Benna, Je, Babior, B.M., Chanock, S.J., The phosphorylation targets of p47phox, a subunit of the respiratory burst oxidase. Functions of the individual target serines as evaluated by site-directed mutagenesis. J. Clin. Investig. 96:3 (1995), 1499–1505 Available from: URL 〈 http://www.jci.org/articles/view/118187/files/pdf〉.
42. Daiber, A., Steven, S., Weber, A., Shuvaev, V.V., Muzykantov, V.R., Laher, I., et al. Targeting vascular (endothelial) dysfunction. Br. J. Pharmacol., 2016.
43. Dutta, S., RITTINGER, K., Regulation of NOXO1 activity through reversible interactions with p22 and NOXA1. PLoS One, 5(5), 2010, e10478.
44. Cheng, G., Lambeth, J.D., NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J. Biol. Chem. 279:6 (2004), 4737–4742.
45. Cheng, G., Lambeth, J.D., Alternative mRNA splice forms of NOXO1: differential tissue expression and regulation of Nox1 and Nox3. Gene 356 (2005), 118–126.
46. Debbabi, M., Kroviarski, Y., Bournier, O., Gougerot-Pocidalo, M.-A., El-Benna, J., Dang, P.M.-C., NOXO1 phosphorylation on serine 154 is critical for optimal NADPH oxidase 1 assembly and activation. FASEB J. 27:4 (2013), 1733–1748.
47. Yamamoto, A., Takeya, R., Matsumoto, M., Nakayama, K.I., Sumimoto, H., Phosphorylation of Noxo1 at threonine 341 regulates its interaction with Noxa1 and the superoxide-producing activity of Nox1. FEBS J. 280:20 (2013), 5145–5159.
48. Nisimoto, Y., Freeman, J.L.R., Motalebi, S.A., Hirshberg, M., Lambeth, J.D., Rac Binding to p67phox: structural basis for interactions of the Rac1 effector region and insert region with components of the respiratory burst oxidase. J. Biol. Chem. 272:30 (1997), 18834–18841.
49. Dang, P.M.-C., Morel, F., Gougerot-Pocidalo, M.-A., El Benna, J., Phosphorylation of the NADPH oxidase component p67(PHOX) by ERK2 and P38MAPK: selectivity of phosphorylated sites and existence of an intramolecular regulatory domain in the tetratricopeptide-rich region. Biochemistry 42:15 (2003), 4520–4526.
50. Wilson, M.I., Gill, D.J., Perisic, O., Quinn, M.T., Williams, R.L., PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol. Cell 12:1 (2003), 39–50.
51. Kami, K., Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67phox, Grb2 and Pex13p. EMBO J. 21:16 (2002), 4268–4276.
52. Nisimoto, Y., Motalebi, S., Han, C.-H., Lambeth, J.D., The p67phox activation domain regulates electron flow from NADPH to flavin in Flavocytochromeb 558. J. Biol. Chem. 274:33 (1999), 22999–23005.
53. Cheng, G., Diebold, B.A., Hughes, Y., Lambeth, J.D., Nox1-dependent reactive oxygen generation is regulated by Rac1. J. Biol. Chem. 281:26 (2006), 17718–17726.
54. Miyano, K., Ueno, N., Takeya, R., Sumimoto, H., Direct involvement of the small GTPase Rac in activation of the superoxide-producing NADPH oxidase Nox1. J. Biol. Chem. 281:31 (2006), 21857–21868.
55. Gianni, D., DerMardirossian, C., Bokoch, G.M., Direct interaction between Tks proteins and the N-terminal proline-rich region (PRR) of NoxA1 mediates Nox1-dependent ROS generation. Eur. J. Cell Biol. 90:2–3 (2011), 164–171.
56. Kroviarski, Y., Debbabi, M., Bachoual, R., Perianin, A., Gougerot-Pocidalo, M.-A., El-Benna, J., et al. Phosphorylation of NADPH oxidase activator 1 (NOXA1) on serine 282 by MAP kinases and on serine 172 by protein kinase C and protein kinase A prevents NOX1 hyperactivation. FASEB J. 24:6 (2010), 2077–2092.
57. J.D. Matute, A.A. Arias, M.C. Dinauer, P.J. Patiño, p40phox: The last NADPH oxidase subunit. Including Workshop on Exosomes: Part III;, 35 (2), pp. 291–302, 2005.
58. Wientjes, F.B., Hsuan, J.J., Totty, N.F., Segal, A.W., p40 phox a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem. J. 296:3 (1993), 557–561.
59. Bravo, J., Karathanassis, D., Pacold, C.M., Pacold, M.E., Ellson, C.D., Anderson, K.E., et al. The Crystal Structure of the PX Domain from p40phox Bound to Phosphatidylinositol 3-Phosphate. Mol. Cell 8:4 (2001), 829–839.
60. Lopes, L.R., Dagher, M.-C., Gutierrez, A., Young, B., Bouin, A.-P., Fuchs, A., et al. Phosphorylated p40PHOX as a negative regulator of NADPH oxidase. Biochemistry 43:12 (2004), 3723–3730.
61. Serrander, L., Cartier, L., Bedard, K., Banfi, B., Lardy, B., Plastre, O., et al. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem. J. 406:1 (2007), 105–114.
62. Brandes, R.P., Miller, F.J., Beer, S., Haendeler, J., Hoffmann, J., Ha, T., et al. The vascular NADPH oxidase subunit p47phox is involved in redox-mediated gene expression. Free Radic. Biol. Med. 32:11 (2002), 1116–1122.
63. Lavigne, M.C., Malech, H.L., Holland, S.M., Leto, T.L., Genetic demonstration of p47phox-dependent superoxide anion production in murine vascular smooth muscle cells. Circulation 104:1 (2001), 79–84.
64. JM, Li, Shah, Am, Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277:22 (2002), 19952–19960.
65. Li, J.-M., Shah, A.M., Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit. J. Biol. Chem. 278:14 (2003), 12094–12100.
66. Hwang, J., Saha, A., Boo, Y.C., Sorescu, G.P., McNally, J.S., Holland, S.M., et al. Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J. Biol. Chem. 278:47 (2003), 47291–47298.
67. Wu, F., Schuster, D.P., Tyml, K., Wilson, J.X., Ascorbate inhibits NADPH oxidase subunit p47phox expression in microvascular endothelial cells. Free Radic. Biol. Med. 42:1 (2007), 124–131.
68. Harrison, C.B., Drummond, G.R., Sobey, C.G., Selemidis, S., Evidence that nitric oxide inhibits vascular inflammation and superoxide production via a p47phox-dependent mechanism in mice. Clin. Exp. Pharm. Physiol. 37:4 (2010), 429–434.
69. Jones, S.A., O'Donnell, V.B., Wood, J.D., Broughton, J.P., Hughes, E.J., Jones, O.T., Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 271:4 Pt 2 (1996), H1626–H1634.
70. Pagano, P.J., Chanock, S.J., Siwik, D.A., Colucci, W.S., Clark, J.K., Angiotensin II induces p67phox mRNA expression and NADPH oxidase superoxide generation in rabbit aortic adventitial fibroblasts. Hypertension 32:2 (1998), 331–337.
71. Rueckschloss, U., Galle, J., Holtz, J., Zerkowski, H.R., Morawietz, H., Induction of NAD(P)H oxidase by oxidized low-density lipoprotein in human endothelial cells: antioxidative potential of hydroxymethylglutaryl coenzyme A reductase inhibitor therapy. Circulation 104:15 (2001), 1767–1772.
72. Oelze, M., Kroller-Schon, S., Steven, S., Lubos, E., Doppler, C., Hausding, M., et al. Glutathione peroxidase-1 deficiency potentiates dysregulatory modifications of endothelial nitric oxide synthase and vascular dysfunction in aging. Hypertension 63:2 (2014), 390–396.
73. Touyz, R.M., Chen, X., Tabet, F., Yao, G., He, G., Quinn, M.T., et al. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ. Res. 90:11 (2002), 1205–1213.
74. Ambasta, R.K., Schreiber, J.G., Janiszewski, M., Busse, R., Brandes, R.P., Noxa1 is a central component of the smooth muscle NADPH oxidase in mice. Free Radic. Biol. Med. 41:2 (2006), 193–201.
75. Feng, Di, Yang, C., Geurts, A.M., Kurth, T., Liang, M., Lazar, J., et al. Increased expression of NAD(P)H oxidase subunit p67(phox) in the renal medulla contributes to excess oxidative stress and salt-sensitive hypertension. Cell Metab. 15:2 (2012), 201–208.
76. Brandes, R.P., Koddenberg, G., Gwinner, W., Kim, D., Kruse, H.J., Busse, R., et al. Role of increased production of superoxide anions by NAD(P)H oxidase and xanthine oxidase in prolonged endotoxemia. Hypertension 33:5 (1999), 1243–1249.
77. Guzik, T.J., Hoch, N.E., Brown, K.A., La, Mc.Cann, Rahman, A., Dikalov, S., et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J. Exp. Med. 204:10 (2007), 2449–2460.
78. Cifuentes, M.E., Rey, F.E., Carretero, O.A., Pagano, P.J., Upregulation of p67 phox and gp91 phox in aortas from angiotensin II-infused mice. Am. J. Physiol. - Heart Circ. Physiol. 279:5 (2000), H2234–H2240 Available from: URL 〈 http://ajpheart.physiology.org/content/ajpheart/279/5/H2234.full.pdf〉.
79. Wenzel, P., Knorr, M., Kossmann, S., Stratmann, J., Hausding, M., Schuhmacher, S., et al. Lysozyme M-positive monocytes mediate angiotensin II-induced arterial hypertension and vascular dysfunction. Circulation 124:12 (2011), 1370–1381.
80. Shimosawa, T., Shibagaki, Y., Ishibashi, K., Kitamura, K., Kangawa, K., Kato, S., et al. Adrenomedullin, an endogenous peptide, counteracts cardiovascular damage. Circulation 105:1 (2002), 106–111.
81. Kawai, J., Ando, K., Tojo, A., Shimosawa, T., Takahashi, K., Onozato, M.L., et al. Endogenous adrenomedullin protects against vascular response to injury in mice. Circulation 109:9 (2004), 1147–1153.
82. Vaziri, N.D., Ni, Z., Expression of NOX-I, gp91phox, p47phox and P67phox in the aorta segments above and below coarctation. Biochim. Biophys. Acta 1723:1–3 (2005), 321–327.
83. Guzik, T.J., Sadowski, J., Guzik, B., Jopek, A., Kapelak, B., Przybylowski, P., et al. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 26:2 (2006), 333–339.
84. Mannheim, D., Herrmann, J., Versari, D., Gossl, M., Meyer, F.B., McConnell, J.P., et al. Enhanced expression of Lp-PLA2 and lysophosphatidylcholine in symptomatic carotid atherosclerotic plaques. Stroke 39:5 (2008), 1448–1455.
85. Herrmann, J., Mannheim, D., Wohlert, C., Versari, D., Meyer, F.B., McConnell, J.P., et al. Expression of lipoprotein-associated phospholipase A(2) in carotid artery plaques predicts long-term cardiac outcome. Eur. Heart J. 30:23 (2009), 2930–2938.
86. Dworakowski, R., Walker, S., Momin, A., Desai, J., El-Gamel, A., Wendler, O., et al. Reduced nicotinamide adenine dinucleotide phosphate oxidase-derived superoxide and vascular endothelial dysfunction in human heart failure. J. Am. Coll. Cardiol. 51:14 (2008), 1349–1356.
87. West, N., Guzik, T., Black, E., Channon, K., Enhanced superoxide production in experimental venous bypass graft intimal hyperplasia: role of NAD(P)H oxidase. Arterioscler. Thromb. Vasc. Biol. 21:2 (2001), 189–194.
88. Bouvet, C., Belin dCE, Guihot, A.L., Vessieres, E., Bocquet, A., Dumont, O., et al. Flow-induced remodeling in resistance arteries from obese Zucker rats is associated with endothelial dysfunction. Hypertension 50:1 (2007), 248–254.
89. Brennan, La, Steinhorn, R.H., Wedgwood, S., Mata-Greenwood, E., Roark, E.A., Russell, J.A., et al. Increased superoxide generation is associated with pulmonary hypertension in fetal lambs: a role for NADPH oxidase. Circ. Res. 92:6 (2003), 683–691.
90. Simmons, G.H., Padilla, J., Laughlin, M.H., Heterogeneity of endothelial cell phenotype within and amongst conduit vessels of the swine vasculature. Exp. Physiol. 97:9 (2012), 1074–1082.
91. Shi, Y., Niculescu, R., Wang, D., Patel, S., Davenpeck, K.L., Zalewski, A., Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler. Thromb. Vasc. Biol. 21:5 (2001), 739–745.
92. Oelze, M., Daiber, A., Brandes, R.P., Hortmann, M., Wenzel, P., Hink, U., et al. Nebivolol inhibits superoxide formation by NADPH oxidase and endothelial dysfunction in angiotensin II-treated rats. Hypertension 48:4 (2006), 677–684.
93. Guzik, T.J., Mussa, S., Gastaldi, D., Sadowski, J., Ratnatunga, C., Pillai, R., et al. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105:14 (2002), 1656–1662.
94. Koibuchi, N., Hasegawa, Y., Katayama, T., Toyama, K., Uekawa, K., Sueta, D., et al. DPP-4 inhibitor linagliptin ameliorates cardiovascular injury in salt-sensitive hypertensive rats independently of blood glucose and blood pressure. Cardiovasc. Diabetol., 13, 2014, 157.
95. Cynis, H., Hoffmann, T., Friedrich, D., Kehlen, A., Gans, K., Kleinschmidt, M., et al. The isoenzyme of glutaminyl cyclase is an important regulator of monocyte infiltration under inflammatory conditions. EMBO Mol. Med 3:9 (2011), 545–558.
96. Brandes, R.P., Harenkamp, S., Schurmann, C., Josipovic, I., Rashid, B., Rezende, F., et al. The cytosolic NADPH oxidase subunit NoxO1 promotes an endothelial stalk cell phenotype. Arterioscler Thromb. Vasc. Biol. 36:8 (2016), 1558–1565.
97. Siu, K.L., Gao, L., Cai, H., Differential roles of protein complexes NOX1-NOXO1 and NOX2-p47phox in mediating endothelial redox responses to oscillatory and unidirectional laminar shear stress. J. Biol. Chem. 291:16 (2016), 8653–8662.
98. Ago, T., Kitazono, T., Kuroda, J., Kumai, Y., Kamouchi, M., Ooboshi, H., et al. NAD(P)H Oxidases in Rat Basilar Arterial Endothelial Cells. Stroke 36:5 (2005), 1040–1046 Available from: URL 〈 http://stroke.ahajournals.org/content/strokeaha/36/5/1040.full.pdf〉.
99. Madrigal-Matute, J., Fernandez-Garcia, C.E., Gomez-Guerrero, C., Lopez-Franco, O., Munoz-Garcia, B., Egido, J., et al. HSP90 inhibition by 17-DMAG attenuates oxidative stress in experimental atherosclerosis. Cardiovasc. Res. 95:1 (2012), 116–123.
100. Teruya, R., Ikejiri, A.T., Somaio Neto, F., Chaves, J.C., Bertoletto, P.R., Taha, M.O., et al. Expression of oxidative stress and antioxidant defense genes in the kidney of inbred mice after intestinal ischemia and reperfusion. Acta Cir. Bras. 28:12 (2013), 848–855.
101. Fletcher, N.M., Saed, M.G., Abuanzeh, S., Abu-Soud, H.M., Al-Hendy, A., Diamond, M.P., et al. Nicotinamide adenine dinucleotide phosphate oxidase is differentially regulated in normal myometrium versus leiomyoma. Reprod. Sci. 21:9 (2014), 1145–1152.
102. Ali, M.I., Ketsawatsomkron, P., Belin de Chantemele, E.J., Mintz, J.D., Muta, K., Salet, C., et al. Deletion of protein tyrosine phosphatase 1b improves peripheral insulin resistance and vascular function in obese, leptin-resistant mice via reduced oxidant tone. Circ. Res. 105:10 (2009), 1013–1022.
103. Honjo, T., Otsui, K., Shiraki, R., Kawashima, S., Sawamura, T., Yokoyama, M., et al. Essential role of NOXA1 in generation of reactive oxygen species induced by oxidized low-density lipoprotein in human vascular endothelial cells. Endothelium 15:3 (2008), 137–141.
104. Niu, X.-L., Madamanchi, N.R., Vendrov, A.E., Tchivilev, I., Rojas, M., Madamanchi, C., et al. Nox activator 1: a potential target for modulation of vascular reactive oxygen species in atherosclerotic arteries. Circulation 121:4 (2010), 549–559.
105. Fan, L.M., Teng, L., Li, J.-M., Knockout of p47 phox uncovers a critical role of p40 phox in reactive oxygen species production in microvascular endothelial cells. Arterioscler Thromb. Vasc. Biol. 29:10 (2009), 1651–1656.
106. Schafer, N., Lohmann, C., Winnik, S., van Tits, L.J., Miranda, M.X., Vergopoulos, A., et al. Endothelial mineralocorticoid receptor activation mediates endothelial dysfunction in diet-induced obesity. Eur. Heart J. 34:45 (2013), 3515–3524.
107. Jackson, S.H., The p47phox mouse knock-out model of chronic granulomatous disease. J. Exp. Med. 182:3 (1995), 751–758.
108. Kuhns, D.B., Alvord, W.G., Heller, T., Feld, J.J., Pike, K.M., Marciano, B.E., et al. Residual NADPH oxidase and survival in chronic granulomatous disease. N. Engl. J. Med. 363:27 (2010), 2600–2610.
109. Violi, F., Sanguigni, V., Carnevale, R., Plebani, A., Rossi, P., Finocchi, A., et al. Hereditary deficiency of gp91(phox) is associated with enhanced arterial dilatation: results of a multicenter study. Circulation 120:16 (2009), 1616–1622.
110. Landmesser, U., Cai, H., Dikalov, S., McCann, L., Hwang, J., Jo, H., et al. Role of p47phox in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40:4 (2002), 511–515.
111. Grote, K., Ortmann, M., Salguero, G., Doerries, C., Landmesser, U., Luchtefeld, M., et al. Critical role for p47phox in renin-angiotensin system activation and blood pressure regulation. Cardiovasc. Res. 71:3 (2006), 596–605.
112. Li, J.-M., Wheatcroft, S., Fan, L.M., Kearney, M.T., Shah, A.M., Opposing roles of p47phox in basal versus angiotensin II-stimulated alterations in vascular O2- production, vascular tone, and mitogen-activated protein kinase activation. Circulation 109:10 (2004), 1307–1313.
113. Thomas, M., Gavrila, D., McCormick, M.L., Miller, F.J. JR, Daugherty, A., Cassis, L.A., et al. Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation 114:5 (2006), 404–413.
114. Youn, J.Y., Gao, L., Cai, H., The p47phox- and NADPH oxidase organiser 1 (NOXO1)-dependent activation of NADPH oxidase 1 (NOX1) mediates endothelial nitric oxide synthase (eNOS) uncoupling and endothelial dysfunction in a streptozotocin-induced murine model of diabetes. Diabetologia 55:7 (2012), 2069–2079.
115. Aoki, T., Nishimura, M., Kataoka, H., Ishibashi, R., Nozaki, K., Hashimoto, N., Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox(-/-) mice. Lab. Investig. 89:7 (2009), 730–741.
116. Frey, R.S., PKCzeta regulates TNF-alpha-induced activation of NADPH oxidase in endothelial cells. Circ. Res. 90:9 (2002), 1012–1019.
117. Hsich, E., Segal, B.H., Pagano, P.J., Rey, F.E., Paigen, B., Deleonardis, J., et al. Vascular effects following homozygous disruption of p47phox: an essential component of NADPH oxidase. Circulation 101:11 (2000), 1234–1236.
118. Holmdahl, R., Sareila, O., Olsson, L.M., Backdahl, L., Wing, K., Ncf1 polymorphism reveals oxidative regulation of autoimmune chronic inflammation. Immunol. Rev. 269:1 (2016), 228–247.
119. Rezende, F., Lowe, O., Helfinger, V., Prior, K.-K., Walter, M., Zukunft, S., et al. Unchanged NADPH oxidase activity in Nox1-Nox2-Nox4 triple knockout mice: what do NADPH-stimulated chemiluminescence assays really detect?. Antioxid. Redox Signal. 24:7 (2016), 392–399.
120. Salguero, G., Akin, E., Templin, C., Kotlarz, D., Doerries, C., Landmesser, U., et al. Renovascular hypertension by two-kidney one-clip enhances endothelial progenitor cell mobilization in a p47phox-dependent manner. J. Hypertens. 26:2 (2008), 257–268.
121. Guzik, T.J., Hoch, N.E., Brown, K.A., McCann, L.A., Rahman, A., Dikalov, S., et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J. Exp. Med. 204:10 (2007), 2449–2460.
122. Ghosh, C.C., Mukherjee, A., David, S., Milam, K.E., Hunter, J.T., Parikh, S.M., Angiopoietin-1 requires oxidant signaling through p47phox to promote endothelial barrier defense. PLoS One, 10(3), 2015, e0119577.
123. –/– mice. J. Clin. Investig. 108:10 (2001), 1513–1522 Available from: URL 〈 http://www.jci.org/articles/view/11927/files/pdf〉.
124. Brandes, R.P., Weissmann, N., Schroder, K., NADPH oxidases in cardiovascular disease. Free Radic. Biol. Med. 49:5 (2010), 687–706.
125. Kirk, E.A., Dinauer, M.C., Rosen, H., Chait, A., Heinecke, J.W., LeBoeuf, R.C., Impaired Superoxide Production Due to a Deficiency in Phagocyte NADPH Oxidase Fails to Inhibit Atherosclerosis in Mice. Arterioscler. Thromb. Vasc. Biol. 20:6 (2000), 1529–1535.
126. Kiss, P.J., Knisz, J., Zhang, Y., Baltrusaitis, J., Sigmund, C.D., Thalmann, R., et al. Inactivation of NADPH oxidase organizer 1 results in severe imbalance. Curr. Biol. 16:2 (2006), 208–213.
127. Sorescu, G.P., Song, H., Tressel, S.L., Hwang, J., Dikalov, S., Smith, D.A., et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress induces monocyte adhesion by stimulating reactive oxygen species production from a nox1-based NADPH oxidase. Circ. Res. 95:8 (2004), 773–779.
128. Evans, L.C., Ryan, R.P., Broadway, E., Skelton, M.M., Kurth, T., Cowley, A.W. JR., Null mutation of the nicotinamide adenine dinucleotide phosphate-oxidase subunit p67phox protects the Dahl-S rat from salt-induced reductions in medullary blood flow and glomerular filtration rate. Hypertension 65:3 (2015), 561–568.
129. Weaver, M., Liu, J., Pimentel, D., Reddy, D.J., Harding, P., Peterson, E.L., et al. Adventitial delivery of dominant-negative p67phox attenuates neointimal hyperplasia of the rat carotid artery. Am. J. Physiol. Heart Circ. Physiol. 290:5 (2006), H1933–H1941.
130. Richter, C., Juan, M.H.S., Will, J., Brandes, R.P., Kalinke, U., Akira, S., et al. Ncf1 provides a reactive oxygen species-independent negative feedback regulation of TLR9-induced IL-12p70 in murine dendritic cells. J. Immunol. 182:7 (2009), 4183–4191.
131. Touyz, R.M., Yao, G., Quinn, M.T., Pagano, P.J., Schiffrin, E.L., p47phox associates with the cytoskeleton through cortactin in human vascular smooth muscle cells: role in NAD(P)H oxidase regulation by angiotensin II. Arterioscler. Thromb. Vasc. Biol. 25:3 (2005), 512–518.
132. Patel, V.B., Wang, Z., Fan, D., Zhabyeyev, P., Basu, R., Das, S.K., et al. Loss of p47phox subunit enhances susceptibility to biomechanical stress and heart failure because of dysregulation of cortactin and actin filaments. Circ. Res. 112:12 (2013), 1542–1556.
133. Drummond, G.R., Selemidis, S., Griendling, K.K., Sobey, C.G., Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10:6 (2011), 453–471.
134. Babelova, A., Sedding, D.G., Brandes, R.P., Anti-atherosclerotic mechanisms of statin therapy. Curr. Opin. Pharmacol. 13:2 (2013), 260–264.
135. Macias-Perez, M.E., Martinez-Ramos, F., Padilla-Martinez, I.I., Correa-Basurto, J., Kispert, L., Mendieta-Wejebe, J.E., et al. Ethers and esters derived from apocynin avoid the interaction between p47phox and p22phox subunits of NADPH oxidase: evaluation in vitro and in silico. Biosci. Rep., 33, 2013, 4.
136. Mora-Pale, M., Kwon, S.J., Linhardt, R.J., Dordick, J.S., Trimer hydroxylated quinone derived from apocynin targets cysteine residues of p47phox preventing the activation of human vascular NADPH oxidase. Free Radic. Biol. Med. 52:5 (2012), 962–969.
137. Hart, B.A. ‘t., Copray, S., Philippens, I., Apocynin, a low molecular oral treatment for neurodegenerative disease. Biomed. Res. Int., 2014 (2014:298020).
138. Schluter, T., Steinbach, A.C., Steffen, A., Rettig, R., Grisk, O., Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovasc. Res. 80:2 (2008), 271–279.
139. Heumuller, S., Wind, S., Barbosa-Sicard, E., Schmidt, H.H.H.W., Busse, R., Schroder, K., et al. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51:2 (2008), 211–217.
140. Dahan, I., Pick, E., Strategies for identifying synthetic peptides to act as inhibitors of NADPH oxidases, or “all that you did and did not want to know about Nox inhibitory peptides”. Cell Mol. Life Sci. 69:14 (2012), 2283–2305.
141. Jacobson, G.M., Dourron, H.M., Liu, J., Carretero, O.A., Reddy, D.J., Andrzejewski, T., et al. Novel NAD(P)H oxidase inhibitor suppresses angioplasty-induced superoxide and neointimal hyperplasia of rat carotid artery. Circ. Res 92:6 (2003), 637–643.
142. Jung, O., Schreiber, J.G., Geiger, H., Pedrazzini, T., Busse, R., Brandes, R.P., gp91phox-containing NADPH oxidase mediates endothelial dysfunction in renovascular hypertension. Circulation 109:14 (2004), 1795–1801.
143. Keller, M., Lidington, D., Vogel, L., Peter, B.F., Sohn, H.-Y., Pagano, P.J., et al. Sphingosine kinase functionally links elevated transmural pressure and increased reactive oxygen species formation in resistance arteries. FASEB J. 20:6 (2006), 702–704.
144. Park, L., Anrather, J., Girouard, H., Zhou, P., Iadecola, C., Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J. Cereb. Blood Flow. Metab. 27:12 (2007), 1908–1918.
145. Ranayhossaini, D.J., Rodriguez, A.I., Sahoo, S., Chen, B.B., Mallampalli, R.K., Kelley, E.E., et al. Selective recapitulation of conserved and nonconserved regions of putative NOXA1 protein activation domain confers isoform-specific inhibition of Nox1 oxidase and attenuation of endothelial cell migration. J. Biol. Chem. 288:51 (2013), 36437–36450.
146. Rodriguez, A.I., Csanyi, G., Ranayhossaini, D.J., Feck, D.M., Blose, K.J., Assatourian, L., et al. MEF2B-Nox1 signaling is critical for stretch-induced phenotypic modulation of vascular smooth muscle cells. Arterioscler Thromb. Vasc. Biol. 35:2 (2015), 430–438.
147. Mousslim, M., Pagano, A., Andreotti, N., Garrouste, F., Thuault, S., Peyrot, V., et al. Peptide screen identifies a new NADPH oxidase inhibitor: impact on cell migration and invasion. Eur. J. Pharmacol. 794 (2017), 162–172.
148. Smith, S.M.E., Min, J., Ganesh, T., Diebold, B., Kawahara, T., Zhu, Y., et al. Ebselen and congeners inhibit NADPH oxidase 2-dependent superoxide generation by interrupting the binding of regulatory subunits. Chem. Biol. 19:6 (2012), 752–763.
149. Daiber, A., Zou, M.H., Bachschmid, M., Ullrich, V., Ebselen as a peroxynitrite scavenger in vitro and ex vivo. Biochem. Pharmacol. 59:2 (2000), 153–160.
150. Cifuentes-Pagano, E., Csanyi, G., Pagano, P.J., NADPH oxidase inhibitors: a decade of discovery from Nox2ds to HTS. Cell Mol. Life Sci. 69:14 (2012), 2315–2325.