NOX/NADPH oxidase, the superoxide-generating enzyme: Its transcriptional regulation and physiological roles

Journal of Pharmacological Sciences

Volumn 114, Issue 2, 2010, Pages 134-146

  Katsuyama, Masato ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

NADPH oxidase; NOX; Oxidative stress; Superoxide

Indexed keywords

DUAL OXIDASE 1; DUAL OXIDASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OXIDOREDUCTASE; 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; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL TYPE; CELLULAR DISTRIBUTION; COLON MUCOSA; CONGENITAL HYPOTHYROIDISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FEEDBACK SYSTEM; FIBROSIS; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HEART DISEASE; HUMAN; HYPOXIA; KIDNEY DISEASE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TISSUE DISTRIBUTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WILD TYPE;

EID: 78349268323     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.10R01CR     Document Type: Article

References (101)

1. Royer-Pokora B, Kunkel LM, Monaco AP, Goff SC, Newburger PE, Baehner RL, et al. Cloning the gene for an inherited human disorder - chronic granulomatous disease - on the basis of its chromosomal location. Nature. 1986;322:32-38.
2. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, et al. Cell transformation by the superoxide-generating oxidase Mox1. Nature. 1999;401:79-82.
3. Banfi B, Maturana A, Jaconi S, Arnaudeau S, Laforge T, Sinha B, et al. A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science. 2000; 287:138-142.
4. Sumimoto H. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 2008;275:3249-3277.
5. Leto TL, Morand S, Hurt D, Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal. 2009;11:2607-2619.
6. Newburger PE, Skalnik DG, Hopkins PJ, Eklund EA, Curnutte JT. Mutations in the promoter region of the gene for gp91-phox in X-linked chronic granulomatous disease with decreased expression of cytochrome b558. J Clin Invest. 1994;94: 1205-1211.
7. Suzuki S, Kumatori A, Haagen IA, Fujii Y, Sadat MA, Jun HL, et al. PU.1 as an essential activator for the expression of gp91(phox) gene in human peripheral neutrophils, monocytes, and B lymphocytes. Proc Natl Acad Sci U S A. 1998;95:6085-6090.
8. Cassatella MA, Bazzoni F, Flynn RM, Dusi S, Trinchieri G, Rossi F. Molecular basis of interferon-gamma and lipopolysaccharide enhancement of phagocyte respiratory burst capability. Studies on the gene expression of several NADPH oxidase components. J Biol Chem. 1990;265:20241-20246.
9. Eklund EA, Luo W, Skalnik DG. Characterization of three promoter elements and cognate DNA binding protein(s) necessary for IFN-gamma induction of gp91-phox transcription. J Immunol. 1996;157:2418-2429.
10. Eklund EA, Skalnik DG. Characterization of a gp91-phox promoter element that is required for interferon gamma-induced transcription. J Biol Chem. 1995;270:8267-8273.
11. Luo W, Skalnik DG. CCAAT displacement protein competes with multiple transcriptional activators for binding to four sites in the proximal gp91phox promoter. J Biol Chem. 1996;271: 18203-18210.
12. Luo W, Skalnik DG. Interferon regulatory factor-2 directs transcription from the gp91phox promoter. J Biol Chem. 1996;271: 23445-23451.
13. Skalnik DG, Strauss EC, Orkin SH. CCAAT displacement protein as a repressor of the myelomonocytic-specific gp91-phox gene promoter. J Biol Chem. 1991;266:16736-16744.
14. Voo KS, Skalnik DG. Elf-1 and PU.1 induce expression of gp91(phox) via a promoter element mutated in a subset of chronic granulomatous disease patients. Blood. 1999;93:3512-3520.
15. Mazzi P, Donini M, Margotto D, Wientjes F, Dusi S. IFN-gamma induces gp91phox expression in human monocytes via protein kinase C-dependent phosphorylation of PU.1. J Immunol. 2004; 172:4941-4947.
16. Bei L, Lu Y, Eklund EA. HOXA9 activates transcription of the gene encoding gp91Phox during myeloid differentiation. J Biol Chem. 2005;280:12359-12370.
17. Lindsey S, Zhu C, Lu YF, Eklund EA. HoxA10 represses transcription of the gene encoding p67phox in phagocytic cells. J Immunol. 2005;175:5269-5279.
18. Kakar R, Kautz B, Eklund EA. JAK2 is necessary and sufficient for interferon-gamma-induced transcription of the gene encoding gp91PHOX. J Leukoc Biol. 2005;77:120-127.
19. Lindsey S, Huang W, Wang H, Horvath E, Zhu C, Eklund EA. Activation of SHP2 protein-tyrosine phosphatase increases HoxA10-induced repression of the genes encoding gp91(PHOX) and p67(PHOX). J Biol Chem. 2007;282:2237-2249.
20. Yang D, Suzuki S, Hao LJ, Fujii Y, Yamauchi A, Yamamoto M, et al. Eosinophil-specific regulation of gp91(phox) gene expression by transcription factors GATA-1 and GATA-2. J Biol Chem 2000;275:9425-9432.
21. Anrather J, Racchumi G, Iadecola C. NF-kappaB regulates phagocytic NADPH oxidase by inducing the expression of gp-91phox. J Biol Chem 2006;281:5657-5667.
22. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin IIinduced cardiac hypertrophy in mice. Circulation. 2002;105: 293-296.
23. Kishida KT, Hoeffer CA, Hu D, Pao M, Holland SM, Klann E. Synaptic plasticity deficits and mild memory impairments in mouse models of chronic granulomatous disease. Mol Cell Biol. 2006;26:5908-5920.
24. Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, et al. Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88:888-894.
25. Lee SH, Park DW, Park SC, Park YK, Hong SY, Kim JR, et al. Calcium-independent phospholipase A2beta-Akt signaling is involved in lipopolysaccharide-induced NADPH oxidase 1 expression and foam cell formation. J Immunol. 2009;183:7497-7504.
26. Kim GY, Lee JW, Ryu HC, Wei JD, Seong CM, Kim JH. Proinflammatory cytokine IL-1beta stimulates IL-8 synthesis in mast cells via a leukotriene B4 receptor 2-linked pathway, contributing to angiogenesis. J Immunol. 2010;184:3946-3954.
27. Kawahara T, Kohjima M, Kuwano Y, Mino H, Teshima-Kondo S, Takeya R, et al. Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase Nox1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am J Physiol Cell Physiol. 2005;288:C450-C457.
28. Ueyama T, Geiszt M, Leto TL. Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol Cell Biol. 2006;26:2160-2174.
29. Banfi B, Clark RA, Steger K, Krause KH. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem. 2003;278:3510-3513.
30. Geiszt M, Lekstrom K, Witta J, Leto TL. Proteins homologous to p47phox and p67phox support superoxide production by NAD(P) H oxidase 1 in colon epithelial cells. J Biol Chem. 2003;278: 20006-20012.
31. 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. 2003;278:25234-25246.
32. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004; 24:677-683.
33. Miller FJ Jr, Filali M, Huss GJ, Stanic B, Chamseddine A, Barna TJ, et al. Cytokine activation of nuclear factor kappa B in vascular smooth muscle cells requires signaling endosomes containing Nox1 and ClC-3. Circ Res. 2007;101:663-671.
34. Brewer AC, Sparks EC, Shah AM. Transcriptional regulation of the NADPH oxidase isoform, Nox1, in colon epithelial cells: role of GATA-binding factor(s). Free Radic Biol Med. 2006;40: 260-274.
35. Valente AJ, Zhou Q, Lu Z, He W, Qiang M, Ma W, et al. Regulation of NOX1 expression by GATA, HNF-1alpha, and Cdx transcription factors. Free Radic Biol Med. 2008;44:430-443.
36. Adachi Y, Shibai Y, Mitsushita J, Shang WH, Hirose K, Kamata T. Oncogenic Ras upregulates NADPH oxidase 1 gene expression through MEK-ERK-dependent phosphorylation of GATA-6. Oncogene. 2008;27:4921-932.
37. Kuwano Y, Kawahara T, Yamamoto H, Teshima-Kondo S, Tominaga K, Masuda K, et al. Interferon-gamma activates transcription of NADPH oxidase 1 gene and upregulates production of superoxide anion by human large intestinal epithelial cells. Am J Physiol Cell Physiol. 2006;290:C433-C443.
38. Kuwano Y, Tominaga K, Kawahara T, Sasaki H, Takeo K, Nishida K, et al. Tumor necrosis factor alpha activates transcription of the NADPH oxidase organizer 1 (NOXO1) gene and upregulates superoxide production in colon epithelial cells. Free Radic Biol Med. 2008;45:1642-1652.
39. Coant N, Ben Mkaddem S, Pedruzzi E, Guichard C, Treton X, Ducroc R, et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol Cell Biol. 2010;30:2636-2650.
40. Katsuyama M, Fan C, Yabe-Nishimura C. NADPH oxidase is involved in prostaglandin F2alpha-induced hypertrophy of vascular smooth muscle cells: induction of NOX1 by PGF2alpha. J Biol Chem. 2002;277:13438-13442.
41. Fan C, Kawai Y, Inaba S, Arakawa K, Katsuyama M, Kajinami K, et al. Synergy of aldosterone and high salt induces vascular smooth muscle hypertrophy through up-regulation of NOX1. J Steroid Biochem Mol Biol. 2008;111:29-36.
42. Arakawa N, Katsuyama M, Matsuno K, Urao N, Tabuchi Y, Okigaki M, et al. Novel transcripts of Nox1 are regulated by alternative promoters and expressed under phenotypic modulation of vascular smooth muscle cells. Biochem J. 2006;398:303-310.
43. Katsuyama M, Fan C, Arakawa N, Nishinaka T, Miyagishi M, Taira K, et al. Essential role of ATF-1 in induction of NOX1, a catalytic subunit of NADPH oxidase: involvement of mitochondrial respiratory chain. Biochem J. 2005;386:255-261.
44. Fan C, Katsuyama M, Nishinaka T, Yabe-Nishimura C. Transactivation of the EGF receptor and a PI3 kinase-ATF-1 pathway is involved in the upregulation of NOX1, a catalytic subunit of NADPH oxidase. FEBS Lett. 2005;579:1301-1305.
45. Fan C, Katsuyama M, Yabe-Nishimura C. PKCdelta mediates up-regulation of NOX1, a catalytic subunit of NADPH oxidase, via transactivation of the EGF receptor: possible involvement of PKCdelta in vascular hypertrophy. Biochem J. 2005;390: 761-767.
46. Katsuyama M, Cevik MO, Arakawa N, Kakehi T, Nishinaka T, Iwata K, et al. Myocyte enhancer factor 2B is involved in the inducible expression of NOX1/NADPH oxidase, a vascular superoxide- producing enzyme. Febs J. 2007;274:5128-5136.
47. Cevik MO, Katsuyama M, Kanda S, Kaneko T, Iwata K, Ibi M, et al. The AP-1 site is essential for the promoter activity of NOX1/NADPH oxidase, a vascular superoxide-producing enzyme: Possible involvement of the ERK1/2-JunB pathway. Biochem Biophys Res Commun. 2008;374:351-355.
48. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, et al. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation. 2005;112: 2677-2685.
49. Ibi M, Matsuno K, Shiba D, Katsuyama M, Iwata K, Kakehi T, et al. Reactive oxygen species derived from NOX1/NADPH oxidase enhance inflammatory pain. J Neurosci. 2008;28:9486-9494.
50. Paffenholz R, Bergstrom RA, Pasutto F, Wabnitz P, Munroe RJ, Jagla W, et al. Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev. 2004;18:486-491.
51. Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem. 2004;279:46065-46072.
52. Ueno N, Takeya R, Miyano K, Kikuchi H, Sumimoto H. The NADPH oxidase Nox3 constitutively produces superoxide in a p22phox-dependent manner: its regulation by oxidase organizers and activators. J Biol Chem. 2005;280:23328-23339.
53. Nakano Y, Banfi B, Jesaitis AJ, Dinauer MC, Allen LA, Nauseef WM. Critical roles for p22phox in the structural maturation and subcellular targeting of Nox3. Biochem J. 2007;403:97-108.
54. Kawahara T, Quinn MT, Lambeth JD. Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol. 2007;7:109.
55. Mukherjea D, Jajoo S, Kaur T, Sheehan KE, Ramkumar V, Rybak LP. Transtympanic administration of short interfering (si)RNA for the NOX3 isoform of NADPH oxidase protects against cisplatin- induced hearing loss in the rat. Antioxid Redox Signal. 2010;13:589-598.
56. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci U S A. 2000;97: 8010-8014.
57. Shiose A, Kuroda J, Tsuruya K, Hirai M, Hirakata H, Naito S, et al. A novel superoxide-producing NAD(P)H oxidase in kidney. J Biol Chem. 2001;276:1417-1423.
58. Yang S, Madyastha P, Bingel S, Ries W, Key L. A new superoxide- generating oxidase in murine osteoclasts. J Biol Chem. 2001; 276:5452-5458.
59. von Lohneysen K, Noack D, Wood MR, Friedman JS, Knaus UG. Structural insights into Nox4 and Nox2: motifs involved in function and cellular localization. Mol Cell Biol. 2010;30: 961-975.
60. Nisimoto Y, Jackson HM, Ogawa H, Kawahara T, Lambeth JD. Constitutive NADPH-dependent electron transferase activity of the Nox4 dehydrogenase domain. Biochemistry. 2010;49:2433-2442.
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. 2007;406:105-114.
62. Lyle AN, Deshpande NN, Taniyama Y, Seidel-Rogol B, Pounkova L, Du P, et al. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res. 2009;105: 249-259.
63. Mittal M, Roth M, Konig P, Hofmann S, Dony E, Goyal P, et al. Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ Res. 2007;101:258-267.
64. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci U S A. 2009; 106:14385-14390.
65. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res. 2010;106: 1253-1264.
66. Zhang L, Sheppard OR, Shah AM, Brewer AC. Positive regulation of the NADPH oxidase NOX4 promoter in vascular smooth muscle cells by E2F. Free Radic Biol Med. 2008;45:679-685.
67. Diebold I, Petry A, Hess J, Gorlach A. The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell. 2010;21:2087-2096.
68. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, Dikalov S, et al. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res. 2005;97:900-907.
69. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, et al. Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2006;290:L661-L673.
70. Sturrock A, Huecksteadt TP, Norman K, Sanders K, Murphy TM, Chitano P, et al. Nox4 mediates TGF-beta1-induced retinoblastoma protein phosphorylation, proliferation, and hypertrophy in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2007;292:L1543-L1555.
71. Carmona-Cuenca I, Roncero C, Sancho P, Caja L, Fausto N, Fernandez M, et al. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J Hepatol. 2008;49:965-976.
72. McKallip RJ, Jia W, Schlomer J, Warren JW, Nagarkatti PS, Nagarkatti M. Cannabidiol-induced apoptosis in human leukemia cells: A novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol Pharmacol. 2006;70:897-908.
73. Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, Prunet C, et al. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol. 2004;24:10703-10717.
74. Steinkamp-Fenske K, Bollinger L, Voller N, Xu H, Yao Y, Bauer R, et al. Ursolic acid from the Chinese herb danshen (Salvia miltiorrhiza L.) upregulates eNOS and downregulates Nox4 expression in human endothelial cells. Atherosclerosis. 2007;195: e104-e111.
75. Caja L, Sancho P, Bertran E, Iglesias-Serret D, Gil J, Fabregat I. Overactivation of the MEK/ERK pathway in liver tumor cells confers resistance to TGF-{beta}-induced cell death through impairing up-regulation of the NADPH oxidase NOX4. Cancer Res. 2009;69:7595-7602.
76. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, et al. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 2009;15: 1077-1081.
77. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, et al. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene. 2006;25:3699-3707.
78. Block K, Eid A, Griendling KK, Lee DY, Wittrant Y, Gorin Y. Nox4 NAD(P)H oxidase mediates Src-dependent tyrosine phosphorylation of PDK-1 in response to angiotensin II: role in mesangial cell hypertrophy and fibronectin expression. J Biol Chem. 2008;283:24061-24076.
79. Clempus RE, Sorescu D, Dikalova AE, Pounkova L, Jo P, Sorescu GP, et al. Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol. 2007;27:42-48.
80. Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL, et al. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem. 2005; 280:39616-39626.
81. Banfi B, Molnar G, Maturana A, Steger K, Hegedus B, Demaurex N, et al. A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem. 2001;276:37594-37601.
82. Banfi B, Tirone F, Durussel I, Knisz J, Moskwa P, Molnar GZ, et al. Mechanism of Ca2+ activation of the NADPH oxidase 5 (NOX5). J Biol Chem. 2004;279:18583-18591.
83. Kawahara T, Lambeth JD. Phosphatidylinositol (4,5)-bisphosphate modulates Nox5 localization via an N-terminal polybasic region. Mol Biol Cell 2008;19:4020-4031.
84. El Jamali A, Valente AJ, Lechleiter JD, Gamez MJ, Pearson DW, Nauseef WM, et al. Novel redox-dependent regulation of NOX5 by the tyrosine kinase c-Abl. Free Radic Biol Med. 2008;44: 868-881.
85. Jay DB, Papaharalambus CA, Seidel-Rogol B, Dikalova AE, Lassegue B, Griendling KK. Nox5 mediates PDGF-induced proliferation in human aortic smooth muscle cells. Free Radic Biol Med. 2008;45:329-335.
86. Brar SS, Corbin Z, Kennedy TP, Hemendinger R, Thornton L, Bommarius B, et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am J Physiol Cell Physiol. 2003;285:C353-C369.
87. Kamiguti AS, Serrander L, Lin K, Harris RJ, Cawley JC, Allsup DJ, et al. Expression and activity of NOX5 in the circulating malignant B cells of hairy cell leukemia. J Immunol. 2005; 175:8424-8430.
88. Si J, Behar J, Wands J, Beer DG, Lambeth D, Chin YE, et al. STAT5 mediates PAF-induced NADPH oxidase NOX5-S expression in Barrett's esophageal adenocarcinoma cells. Am J Physiol Gastrointest Liver Physiol. 2008;294:G174-G183.
89. Dupuy C, Ohayon R, Valent A, Noel-Hudson MS, Deme D, Virion A. Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas. J Biol Chem. 1999;274:37265-37269.
90. De Deken X, Wang D, Many MC, 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. 2000; 275:23227-23233.
91. Moreno JC, Bikker H, Kempers MJ, van Trotsenburg AS, Baas F, de Vijlder JJ, et al. Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. N Engl J Med. 2002;347:95-102.
92. Vigone MC, Fugazzola L, Zamproni I, Passoni A, Di Candia S, Chiumello G, et al. Persistent mild hypothyroidism associated with novel sequence variants of the DUOX2 gene in two siblings. Hum Mutat 2005;26:395.
93. Grasberger H, Refetoff S. Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J Biol Chem. 2006;281:18269-18272.
94. Morand S, Ueyama T, Tsujibe S, Saito N, Korzeniowska A, Leto TL. Duox maturation factors form cell surface complexes with Duox affecting the specificity of reactive oxygen species generation. FASEB J. 2009;23:1205-1218.
95. Zamproni I, Grasberger H, Cortinovis F, Vigone MC, Chiumello G, Mora S, et al. Biallelic inactivation of the dual oxidase matu ration factor 2 (DUOXA2) gene as a novel cause of congenital hypothyroidism. J Clin Endocrinol Metab. 2008;93:605-610.
96. Rigutto S, Hoste C, Grasberger H, Milenkovic M, Communi D, Dumont JE, et al. Activation of dual oxidases Duox1 and Duox2: differential regulation mediated by camp-dependent protein kinase and protein kinase C-dependent phosphorylation. J Biol Chem. 2009;284:6725-6734.
97. Edens WA, Sharling L, Cheng G, Shapira R, Kinkade JM, Lee T, et al. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol. 2001; 154:879-891.
98. Geiszt M, Witta J, Baffi J, Lekstrom K, Leto TL. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 2003;17:1502-1504.
99. El Hassani RA, Benfares N, Caillou B, Talbot M, Sabourin JC, Belotte V, et al. Dual oxidase2 is expressed all along the digestive tract. Am J Physiol Gastrointest Liver Physiol. 2005;288: G933-G942.
100. Harper RW, Xu C, Eiserich JP, Chen Y, Kao CY, Thai P, et al. Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett. 2005;579:4911-4917.
101. Luxen S, Belinsky SA, Knaus UG. Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res. 2008;68:1037-1045.