The extracellular A-loop of dual oxidases affects the specificity of reactive oxygen species release

Journal of Biological Chemistry

Volumn 290, Issue 10, 2015, Pages 6495-6506

  Ueyama, Takehiko ^a   Sakuma, Megumi ^a   Ninoyu, Yuzuru ^a   Hamada, Takeshi ^a   Dupuy, Corinne ^b   Geiszt, Miklós ^c   Leto, Thomas L ^d   Saito, Naoaki ^a  

^a KOBE UNIVERSITY   (Japan)

^b Gustave Roussy Comprehensive Cancer Institute   (France)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; OXYGEN; PROTEINS;

COMPLEX FORMATIONS; ENDOGLYCOSIDASE; ENZYME COMPLEXES; IMMUNOPRECIPITATIONS; LOOP RESIDUES; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; STRUCTURAL DETERMINANTS;

MOLECULAR OXYGEN;

DUAL OXIDASE; DUAL OXIDASE 1; DUAL OXIDASE 2; DUAL OXIDASE ACTIVATOR 1; DUAL OXIDASE ACTIVATOR 2; ENDOGLYCOSIDASE H; GLYCOSIDASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; SUPEROXIDE; UNCLASSIFIED DRUG; DUOX1 PROTEIN, HUMAN; DUOX2 PROTEIN, HUMAN; NOX1 PROTEIN, HUMAN; OXYGEN; THYROID HORMONE;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR INTERACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; GLYCOSYLATION; HEK293 CELL LINE; METABOLISM; MUTATION;

CELL MEMBRANE; GLYCOSYLATION; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; MUTATION; NADPH OXIDASE; OXYGEN; REACTIVE OXYGEN SPECIES; SUPEROXIDES; THYROID HORMONES;

EID: 84924942012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.592717     Document Type: Article

References (33)

1. Quinn, M. T., Ammons, M. C., and Deleo, F. R. (2006) The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin. Sci. 111, 1-20
2. Leto, T. L., Morand, S., Hurt, D., and Ueyama, T. (2009) Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid. Redox. Signal 11, 2607-2619
3. Matsushima, S., Tsutsui, H., and Sadoshima, J. (2014) Physiological and pathological functions of NADPH oxidases during myocardial ischemiareperfusion. Trends Cardiovasc. Med. 24, 202-205
4. De Deken, X., Wang, D., Many, M. C., Costagliola, S., Libert, F., Vassart, G., Dumont, J. E., and Miot, F. (2000) Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J. Biol. Chem. 275, 23227-23233
5. Dupuy, C., Ohayon, R., Valent, A., Noël-Hudson, M. S., Dème, D., and Virion, A. (1999) Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas. J. Biol. Chem. 274, 37265-37269
6. Grasberger, H., and Refetoff, S. (2006) Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J. Biol. Chem. 281, 18269-18272
7. Morand, S., Ueyama, T., Tsujibe, S., Saito, N., Korzeniowska, A., and Leto, T. L. (2009) Duox maturation factors form cell surface complexes with Duox affecting the specificity of reactive oxygen species generation. FASEB J. 23, 1205-1218
8. Moreno, J. C., Pauws, E., van Kampen, A. H., Jedlicková, M., de Vijlder, J. J., and Ris-Stalpers, C. (2001) Cloning of tissue-specific genes using serial analysis of gene expression and a novel computational substraction approach. Genomics 75, 70-76
9. Johnson, K. R., Marden, C. C., Ward-Bailey, P., Gagnon, L. H., Bronson, R. T., and Donahue, L. R. (2007) Congenital hypothyroidism, dwarfism, and hearing impairment caused by a missense mutation in the mouse dual oxidase 2 gene, Duox2. Mol. Endocrinol. 21, 1593-1602
10. Grasberger, H., De Deken, X., Mayo, O. B., Raad, H., Weiss, M., Liao, X. H., and Refetoff, S. (2012) Mice deficient in dual oxidase maturation factors are severely hypothyroid. Mol. Endocrinol. 26, 481-492
11. Donkó, A., Ruisanchez, E., Orient, A., Enyedi, B., Kapui, R., Péterfi, Z., de Deken, X., Benyó, Z., and Geiszt, M. (2010) Urothelial cells produce hydrogen peroxide through the activation of Duox1. Free Radic. Biol. Med. 49, 2040-2048
12. Maruo, Y., Takahashi, H., Soeda, I., Nishikura, N., Matsui, K., Ota, Y., Mimura, Y., Mori, A., Sato, H., and Takeuchi, Y. (2008) Transient congenital hypothyroidism caused by biallelic mutations of the dual oxidase 2 gene in Japanese patients detected by a neonatal screening program. J. Clin. Endocrinol. Metab. 93, 4261-4267
13. Hulur, I., Hermanns, P., Nestoris, C., Heger, S., Refetoff, S., Pohlenz, J., and Grasberger, H. (2011) A single copy of the recently identified dual oxidase maturation factor (DUOXA) 1 gene produces only mild transient hypothyroidism in a patient with a novel biallelic DUOXA2 mutation and monoallelic DUOXA1 deletion. J. Clin. Endocrinol. Metab. 96, E841-E845
14. Geiszt, M., Witta, J., Baffi, J., Lekstrom, K., and Leto, T. L. (2003) Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 17, 1502-1504
15. El Hassani, R. A., Benfares, N., Caillou, B., Talbot, M., Sabourin, J. C., Belotte, V., Morand, S., Gnidehou, S., Agnandji, D., Ohayon, R., Kaniewski, J., Noël-Hudson, M. S., Bidart, J. M., Schlumberger, M., Virion, A., and Dupuy, C. (2005) Dual oxidase2 is expressed all along the digestive tract. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G933-G942
16. van der Vliet, A. (2011) Nox enzymes in allergic airway inflammation. Biochim. Biophys. Acta 1810, 1035-1044
17. Ha, E. M., Oh, C. T., Bae, Y. S., and Lee, W. J. (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847-850
18. Moskwa, P., Lorentzen, D., Excoffon, K. J., Zabner, J., McCray, P. B., Jr., Nauseef, W. M., Dupuy, C., and Bánfi, B. (2007) A novel host defense system of airways is defective in cystic fibrosis. Am. J. Respir. Crit. Care Med. 175, 174-183
19. Grasberger, H., El-Zaatari, M., Dang, D. T., and Merchant, J. L. (2013) Dual oxidases control release of hydrogen peroxide by the gastric epithelium to prevent helicobacter felis infection and inflammation in mice. Gastroenterology 145, 1045-1054
20. Sumimoto, H. (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275, 3249-3277
21. 2-generating activity. J. Biol. Chem. 280, 30046-30054
22. De Deken, X., Corvilain, B., Dumont, J. E., and Miot, F. (2014) Roles of DUOX-mediated hydrogen peroxide in metabolism, host defense, and signaling. Antioxid. Redox. Signal 20, 2776-2793
23. Kawahara, T., Quinn, M. T., and Lambeth, J. D. (2007) Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol. Biol. 7, 109
24. Meitzler, J. L., and Ortiz de Montellano, P. R. (2009) Caenorhabditis elegans and human dual oxidase 1 (DUOX1) "peroxidase" domains: insights into heme binding and catalytic activity. J. Biol. Chem. 284, 18634-18643
25. Meitzler, J. L., and Ortiz de Montellano, P. R. (2011) Structural stability and heme binding potential of the truncated human dual oxidase 2 (DUOX2) peroxidase domain. Arch. Biochem. Biophys. 512, 197-203
26. Zamproni, I., Grasberger, H., Cortinovis, F., Vigone, M. C., Chiumello, G., Mora, S., Onigata, K., Fugazzola, L., Refetoff, S., Persani, L., and Weber, G. (2008) Biallelic inactivation of the dual oxidase maturation factor 2 (DUOXA2) gene as a novel cause of congenital hypothyroidism. J. Clin. Endocrinol. Metab. 93, 605-610
27. phox. Mol. Biol. Cell 18, 441-454
28. Nauseef, W. M. (2014) Detection of superoxide anion and hydrogen peroxide production by cellular NADPH oxidases. Biochim. Biophys. Acta 1840, 757-767
29. Ueyama, T., Son, J., Kobayashi, T., Hamada, T., Nakamura, T., Sakaguchi, H., Shirafuji, T., and Saito, N. (2013) Negative charges in the flexible N-terminal domain of rho GDP-dissociation inhibitors (RhoGDIs) regulate the targeting of the RhoGDI-Rac1 complex to membranes. J. Immunol. 191, 2560-2569
30. Pick, E. (2014) Cell-free NADPH oxidase activation assays: "in vitro veritas." Methods Mol. Biol. 1124, 339-403
31. Hoste, C., Dumont, J. E., Miot, F., and De Deken, X. (2012) The type of DUOX-dependent ROS production is dictated by defined sequences in DUOXA. Exp. Cell Res. 318, 2353-2364
32. Cheng, G., Cao, Z., Xu, X., van Meir, E. G., and Lambeth, J. D. (2001) Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140
33. Takac, I., Schröder, K., Zhang, L., Lardy, B., Anilkumar, N., Lambeth, J. D., Shah, A. M., Morel, F., and Brandes, R. P. (2011) The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4. J. Biol. Chem. 286, 13304-13313Association.