Structure and regulation of the neutrophil respiratory burst oxidase: Comparison with nonphagocyte oxidases

Journal of Leukocyte Biology

Volumn 76, Issue 4, 2004, Pages 760-781

  Quinn, Mark T ^a   Gauss, Katherine A ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Chronic granulomatous disease; Free radicals; Nonphagocyte NADPH oxidase; Nox; Oxidants; Phagocyte NADPH oxidase; Superoxide union

Indexed keywords

CYTOSOLIC OXIDASE PROTEIN; FREE RADICAL; HYDROLASE; LACTATE DEHYDROGENASE (CYTOCHROME); MICROBICIDAL PEPTIDE; NONPHAGOCYTE OXIDASE; NOX PROTEIN; NOXA1 PROTEIN; NOXO1 PROTEIN; OXIDIZING AGENT; OXIDOREDUCTASE; OXYGEN; P40 PHOX PROTEIN; P47 PHOX PROTEIN; P67 PHOX PROTEIN; PEPTIDE; PHAGOCYTE OXIDASE; PROTEIN; RAC PROTEIN; RAP1A PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESPIRATORY BURST OXIDASE; SUPEROXIDE; UNCLASSIFIED DRUG;

CELL MEMBRANE; CONFORMATIONAL TRANSITION; CYBA GENE; CYBB GENE; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; GENE; GP91 PHOX GENE; GRANULOMATOSIS; HOST RESISTANCE; IMMUNE RESPONSE; INFLAMMATION; NCF1 GENE; NCF2 GENE; NCF4 GENE; NEUTROPHIL; P22 PHOX GENE; P40 PHOX GENE; P47 PHOX GENE; P67 PHOX GENE; PHAGOCYTE; PHAGOSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN TRANSPORT; RESPIRATORY BURST; REVIEW; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION REGULATION;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; NADPH OXIDASE; NEUTROPHILS; PHAGOCYTES; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST;

EID: 4744349398     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0404216     Document Type: Review

References (282)

1. Janeway, Jr., C. A., Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216.
2. Ricevuti, G. (1997) Host tissue damage by phagocytes. Ann. N. Y. Acad. Sci. 832, 426-448.
3. Haen, P. J. (1995) Principles of Hematology, Dubuque, IA, Wm. C. Brown.
4. Witko-Sarsal, V., Rieu, P., Descamps-Latscha, B., Lesavre, P., Halbwachs-Mecarelli, L. (2000) Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 80, 617-653.
5. Roos, D., Van Bruggen, R., Meischl, C. (2003) Oxidative killing of microbes by neutrophils. Microbes Infect. 5, 1307-1315.
6. Babior, B. M. (2004) NADPH oxidase. Curr. Opin. Immunol. 16, 42-47.
7. Bokoch, G. M., Knans, U. C. (2003) NADPH oxidases: not just for leukocytes anymore! Trends Biochem. Sci. 28, 502-508.
8. Lambeth, J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189.
9. Heyworth, P. G., Cross, A. R., Curnutte, J. T. (2003) Chronic granulomatous disease. Curr. Opin. Immunol. 15, 578-584.
10. Babior, B. M. (1991) The respiratory burst oxidase and the molecular basis of chronic granulomatous disease. Am. J. Hematol. 37, 263-266.
11. phox. Trends Biochem. Sci. 25, 459-461.
12. phox homolog. J. Leukoc. Biol. 71, 319-328.
13. Segal, A. W., Jones, O. T. G. (1978) Novel cytochrome b system in phagocytic vacuoles of human granulocytes. Nature 276, 515-517.
14. Jesaitis, A. J. (1995) Structure of human phagocyte cytochrome b and its relationship to microbicidal Superoxide production. J. Immunol. 155, 3286-3288.
15. Parkos, C. A., Allen, R. A., Cochrane, C. G., Jesaitis, A. J. (1987) Purified cytochrome b from human granulocyte plasma membrane is composed of two polypeptides with relative molecular weights of 91,000 and 22,000. J. Clin. Invest. 80, 732-742.
16. Parkos, C. A., Allen, R. A., Cochrane, C. G., Jesaitis, A. J. (1988) The quaternary structure of the plasma membrane b-type cytochrome of human granulocytes. Biochim. Biophys. Acta 932, 71-83.
17. -245 β-chain. Protein Sci. 2, 1675-1685.
18. 558. Biochemistry 34, 16753-16757.
19. Royer-Pokora, B., Kunkel, L. M., Monaco, A. P., Goff, S. C., Newburger, P. E., Bachner, R. L., Cole, F. S., Curnutte, J. T., Orkin, S. H. (1986) Cloning the gene for an inherited human disorder-chronic granulomatous disease-on the basis of its chromosomal location. Nature 322, 32-38.
20. Parkos, C. A., Dinauer, M. C., Walker, L. E., Allen, R. A., Jesaitis, A. J., Orkin, S. H. (1988) Primary structure and unique expression of the 22-kilodalton light chain of human neutrophil cytochrome b. Proc. Natl. Acad. Sci. USA 85, 3319-3323.
21. Hurst, J. K., Loehr, T. M., Curnutte, J. T., Rosen, H. (1991) Resonance raman and electron paramagnetic resonance structural investigations of neutrophil cytochrome b558. J. Biol. Chem. 266, 1627-1634.
22. Ueno, I., Fujii, S., Ohya-Nishiguchi, H., Iizuka, T., Kanegasaki, S. (1991) Characterization of neutrophil b-type cytochrome in situ by electron paramagnetic resonance spectroscopy. FEBS Lett. 281, 130-132.
23. Quinn, M. T., Mullen, M. L., Jesaitis, A. J. (1992) Human neutrophil cytochrome-b contains multiple hemes. Evidence for heme associated with both subunits. J. Biol. Chem. 267, 7303-7309.
24. phox. J. Biol. Chem. 270, 17075-17077.
25. Parkos, C. A., Quinn, M. T., Sheets, S., Jesaitis, A. J. (1992) The structure of the human neutrophil plasma membrane b-type cytochrome involved in Superoxide production. In Molecular Basis of Oxidative Damage by Leukocytes (A. J. Jesaitis, E. A. Dratz, eds.), Boca Raton, FL, CRC, 45-56.
26. Finegold, A. A., Shatwell, K. P., Segal, A. W., Klausner, R. D., Dancis, A. (1996) Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase. J. Biol. Chem. 271, 31021-31024.
27. 558 include incorporation of heme as a prerequisite for heterodimer assembly. J. Biol. Chem. 275, 13986-13993.
28. 558 inhibit Superoxide generation in a cell-free system from human neutrophils. Biochem. Biophys. Res. Commun. 204, 924-929.
29. 558 light chain of the NADPH oxidase (p22-phox). Am. J. Hum. Genet. 51, 1127-1135.
30. phox. J. Biol. Chem. 276, 38852-38861.
31. phox is the heme binding subunit of the superoxide-generating NADPH oxidase. Proc. Natl. Acad. Sci. USA 95, 7993-7998.
32. phox. J. Biol. Chem. 276, 31105-31112.
33. Heyworth, P. G., Curnutte, J. T., Rae, J., Noack, D., Roos, D., Van Koppen, E., Cross, A. R. (2001) Hematologically important mutations: X-linked chronic granulomatous disease (second update). Blood Cells Mol. Dis. 27, 16-26.
34. 558 function. J. Biol. Chem. 277, 30368-30374.
35. Babior, B. M. (1984) The respiratory burst of phagocytes. J. Clin. Invest. 73, 599-601.
36. 558. The flavin-binding component of the phagocyte NADPH oxidase. Science 256, 1459-1462.
37. 558, a component of the phagocyte NADPH oxidase, is a flavoprotein. Biochem. Biophys. Res. Commun. 186, 1368-1375.
38. -245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbicidal oxidase of phagocytes. Biochem. J. 284, 781-788.
39. phox, the flavocytochrome of the NADPH oxidase, by site-directed mutagenesis and translation in vitro. Biochem. J. 321, 583-585.
40. --generating oxidase of neutrophils by an azido derivative of FAD. Biochemistry 34, 1760-1770.
41. 559 in the absence of cytosolic activators. FEBS Lett. 327, 57-62.
42. 558. J. Biol. Chem. 270, 7853-7857.
43. Mayo, S. L., Ellis, W. R., Crutchley, R. J., Gray, H. B. (1986) Long range electron transfer in heme proteins. Science 233, 948-952.
44. r-44,000 protein. Nature 316, 547-549.
45. Volpp, B. D., Nauseef, W. M., Clark, R. A. (1988) Two cytosolic neutrophil oxidase components absent in autosomal chronic granulomatous disease. Science 242, 1295-1297.
46. Nunoi, H., Rotrosen, D., Gallin, J. I., Malech, H. L. (1988) Two forms of autosomal chronic granulomatous disease lack distinct neutrophil cytosolic factors. Science 242, 1298-1301.
47. Volpp, B. D., Nauseef, W. M., Donelson, J. E., Moser, D. R., Clark, R. A. (1989) Cloning of the cDNA and functional expression of the 47-kilodalton cytosolic component of human neutrophil respiratory burst oxidase. Proc. Natl. Acad. Sci. USA 86, 7195-7199.
48. Lomax, K. J., Leto, T. L., Nunoi, H., Gallin, J. I., Malech, H. L. (1989) Recombinant 47-kilodalton cytosolic factor restores NADPH oxidase in chronic granulomatous disease. Science 245, 409-412.
49. Hiroaki, H., Ago, T., Ito, T., Sumimoto, H., Kohda, D. (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat. Struct. Biol. 8, 526-530.
50. r approximately 240,000 complex that acquires a membrane-binding site during activation of the oxidase in a cell-free system. J. Biol. Chem. 267, 17327-17332.
51. Iyer, S. S., Pearson, D. W., Nauseef, W. M., Clark, R. A. (1994) Evidence for a readily dissociable complex of p47phox and p67phox in cytosol of unstimulated human neutrophils. J. Biol. Chem. 269, 22405-22411.
52. phox. J. Biol. Chem. 277, 10121-10128.
53. phox to the submembranous actin cytoskeleton during oxidase activation. J. Biol. Chem. 269, 6729-6734.
54. phox have distinct roles in the regulation of electron flow in NADPH oxidase. J. Biol. Chem. 270, 6543-6548.
55. Poinas, A., Gaillard. J., Vignais, P., Doussiere, J. (2002) Exploration of the diaphorase activity of neutrophil NADPH oxidase. Critical assessment of the interaction of iodonitrotetrazolium with the oxidase redox components. Eur. J. Biochem. 269, 1243-1252.
56. 558 J. Clin. Invest. 87, 352-356.
57. Kleinberg, M. E., Malech, H. L., Rotrosen, D. (1990) The phagocyte 47-kilodalton cytosolic oxidase protein is an early reactant in activation of the respiratory burst oxidase. J. Biol. Chem. 265, 15577-15583.
58. Uhlinger, D. J., Taylor, K. L., Lambeth, J. D. (1994) p67-phox enhances the binding of p47-phox to the human neutrophil respiratory burst oxidase complex. J. Biol Chem. 269, 22095-22098.
59. 2+-depleted human neutrophils. Biochem. J. 290, 173-178.
60. Quinn, M. T., Evans, T., Loetterle, L. R., Jesaitis, A. J., Bokoch, C. M. (1993) Translocation of Rac correlates with NADPH oxidase activation: evidence for equimolar translocation of oxidase components. J. Biol. Chem. 268, 20983-20987.
61. phox during phagocytosis. J. Biol. Chem. 279, 9097-9102.
62. Nauseef, W. M. (1999) The NADPH-dependent oxidase of phagocytes. Proc. Assoc. Am. Physicians 111, 373-382.
63. phox, thereby activating the oxidase. J. Biol. Chem. 274, 33644-33653.
64. phox using tryptophan fluorescence spectroscopy. J. Biol. Chem. 272, 29502-29510.
65. Peng, G. H., Huang, J. Boyd, M., Kleinberg, M. E. (2003) Properties of phagocyte NADPH oxidase p47-phox mutants with unmasked SH3 (Src homology 3) domains: full reconstitution of oxidase activity in a semi-recombinant cell-free system lacking arachidonic acid, Biochem. J. 373, 221-229.
66. phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc. Natl. Acad. Sci. USA 100, 4474-4479.
67. phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases. J. Biol. Chem. 269, 23431-23436.
68. phox as determined by two-dimensional phosphopeptide mapping. Phosphorylation by protein kinase C, protein kinase A, and a mitogen-activated protein kinase. J. Biol. Chem. 271, 6374-6378.
69. phox phosphorylation in human neutrophils. J. Immunol. 165, 5238-5244.
70. Knaus, U. G., Morris, S., Dong, H-J., Chernoff, J., Bokoch, G. M. (1995) Regulation of human leukocyte p21-activated kinases through G protein-coupled receptors. Science 269, 221-223.
71. phox by a membrane-targeted phosphoinositide 3-kinase. Curr. Biol. 6, 1271-1278.
72. phox by casein kinase 2: conformation-dependent phosphorylation and modulation of oxidase activity. Biochem. J. 358, 783-790.
73. Waite, K. A., Wallin, R., Qualliotine-Mann, D., McPhail, L. C. (1997) Phosphatidic acid-mediated phosphorylation of the NADPH oxidase component p47-phox. Evidence that phosphatidic acid may activate a novel protein kinase. J. Biol. Chem. 272, 15569-15578.
74. phox in neutrophils. Biochem. J. 344, 859-866.
75. phox and participates in formyl peptide-mediated neutrophil respiratoiy burst. J. Immunol. 166, 1206-1213.
76. phox and on NADPH oxidase activation. Biochemistry 41, 7743-7750.
77. phox and mediates respiratory burst activity in human neutrophils. J. Immunol. 170, 5302-5308.
78. phox activity by site-specific phosphorylation: Akt-dependeut activation of the NADPH oxidase. Proc. Natl. Acad. Sci. USA 100, 5130-5135.
79. Ponting, C. P. (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and Ptdlns 3-kinases: binding partners of SH3 domains? Protein Sci. 5, 2353-2357.
80. Wientjes, F. B., Segal, A. W. (2003) PX domain takes shape. Curr. Opin. Hematol. 10, 2-7.
81. Kanai, F., Liu, H., Field, S. J., Akbary, H., Matsuo, T., Brown, G. E., Cantley, L. C., Yaffe, M. B. (2001) The PX domains of p47phox and p40phox bind to lipid products of Pl(3)K. Nat. Cell Biol. 3, 675-678.
82. Ago, T., Takeya, R., Hiroaki, H., Kuribayashi, F., Ito, T., Kohda, D., Sumimoto, H. (2001) The PX domain as a novel phosphoinositide-binding module. Biochem. Biophys. Res. Commun. 287, 733-738.
83. phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J. Biol. Chem. 277, 4512-4518.
84. phox. J. Biol. Chem. 278, 14469-14479.
85. phox to phosphatidylinositol 3.4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J. 21, 5057-5068.
86. phox bind to moesin through their PX domain. Biochem. Biophys. Res. Commun. 289, 382-388.
87. Paliez, A., Fonbert, T. R., Jesaitis, A. J., Marodi, L., McPhail, L. C. (2001) Phosphatidic acid and diacylglycerol directly activate NADPH oxidase by interacting with enzyme components. J. Biol. Chem. 276, 3090-3097.
88. Leto, T. L., Lomax, K. J., Volpp, B. D., Nunoi, H., Sechler, J. M. G., Nauseef, W. M., Clark, R. A., Gallin, J. I., Malech, H. L. (1990) Cloning of a 67-kD neutrophil oxidase factor with similarity to a noncatalytic region of p60-src. Science 248, 727-730.
89. phox participate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase. J. Biol. Chem. 274, 25051-25060.
90. Vergnaud, S., Paclet, M. H., El Benna, J., Pocidalo, M. A., Morel, F. (2000) Complementation of NADPH oxidase in p67-phox-deficient CGD patients: p67-phox/p40-phox interaction. Eur. J. Biochem. 267, 1059-1067.
91. 558. J. Biol. Chem. 269, 30749-30752.
92. 558 liposomes by atomic force microscopy. Biochemistry 39, 9302-9310.
93. phox in vitro. J. Biol. Chem. 271, 22578-22582.
94. phox is not a sine qua non participant in the activation of NADPH oxidase but is required for optimal Superoxide production. J. Biol. Chem. 271, 30326-30329.
95. phox and the small GTPase Rac1. Biochemistry 40, 14557-14566,
96. phox (1-210) reconstitutes NADPH oxidase with higher activity and stability than the individual components, Biochemistry 40, 14089-14097,
97. 558. Proc. Natl. Acad. Sci. USA 98, 3001-3005.
98. Smith, R. M., Connor, J. A., Chen, L. M., Babior, B. M. (1996) The cytosolic subunit p67phox contains an NADPH-binding site that participates in catalysis by the leukocyte NADPH oxidase. J. Clin. Invest. 98, 977-983.
99. PHOX, a cytosolic subunit of the leukocyte NADPH oxidase. Biochemistry 38, 5746-5753,
100. PHOX, a subunit of the leukocyte nicotinamide adenine dinucleotide phosphate oxidase. Biochemistry 39, 3069-3075.
101. phox and regulation of phagocytic NADPH oxidase activity. Science 265, 531-533,
102. Faris, S. L., Rinckel, L. A., Huang, J., Hong, Y. R., Kleinberg, M. E., (1998) Phagocyte NADPH oxidase p67-phox possesses a novel carboxylterminal binding site for the GTPases Rac2 and Cdc42. Biochem. Biophys. Res. Commun. 247, 271-276,
103. Lapouge, K., Smith, S. J. M., Walker, P. A., Gamblin, S. J., Smerdon, S. J., Rittinger, K. (2000) Structure of the TPR domain of p67phox in complex with Rac•GTP. Mol. Cell 6, 899-907.
104. phox-structure at 1.8 Å resolution and biochemical characterizations of the A128V mutant implicated in chronic granulomatous disease, J. Biol. Chem. 276, 21627-21631.
105. Han, C-H., Freeman, J. L. R., Lee, T. H., Motalebi, S. A., Lambeth, J. D. (1998) Regulation of the neutrophil respiratory burst oxidase-identification of an activation domain in p67phox. J. Biol. Chem. 273, 16663-16668.
106. 558. J. Biol. Chem. 274, 22999-23005.
107. phox during human neutrophil activation-regulation by protein kinase C-dependent and independent pathways. J. Biol. Chem. 272, 17204-17208.
108. phox is Thr233. Biochem. J. 338, 99-105,
109. phox. FEBS Lett. 449, 225-229,
110. PHOX by ERK2 and P38MAPK: selectivity of phosphorylated sites and existence of an intramolecular regulatory domain in the tetratricopeptide-rich region. Biochemistry 42, 4520-4526.
111. phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem. J. 296, 557-561.
112. phox. SH3 domain-containing cytosolic factors of the phagocyte NADPH oxidase. Eur. J. Biochem. 251, 583-589.
113. phox. Biochem. J. 317, 919-924.
114. phox is phosphorylated on threonine 154 and serine 315 during activation of the phagocyte NADPH oxidase-implication of a protein kinase C type kinase in the phosphorylation process. J. Biol. Chem. 273, 30097-30103.
115. phox. J. Exp. Med. 184, 893-902.
116. phox down-regulates NADPH oxidase activity through interactions with its SH3 domain. J. Biol. Chem. 272, 9141-9146.
117. 558. Biochem. J. 349, 113-117.
118. phox as a positive regulator of the superoxide-producing phagocyte oxidase. EMBO J. 21, 6312-6320,
119. phox bound to phosphatidylinositol 3-phosphate, Mol. Cell 8, 829-839,
120. Ellson, C. D., Andrews, S., Stephens, L. R., Hawkins, P. T. (2002) The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 115, 1099-1105,
121. Ellson, C. D., Anderson, K. E., Morgan, G., Chilvers, E. R., Lipp, P., Stephens, L. R., Hawkins, P. T. (2001) Phosphatidylinositol 3-phosphate is generated in phagosomal membranes. Curr. Biol. 11, 1631-1635.
122. phox. Nat. Cell Biol. 3, 679-682.
123. Ito, T., Matsui, Y., Ago, T., Ota, K., Sumimoto, H. (2001) Novel modular domain PB1 recognizes PC motif to mediate functional protein-protein interactions, EMBO J. 20, 3938-3946.
124. Bokoch, G. M., Diebold, B. A., (2002) Current molecular models for NADPH oxidase regulation by Rac GTPase. Blood 100, 2692-2696.
125. Dorseuil, O., Vazquez, A., Lang, P., Bertoglio, J., Gacon, G., Leca, G. (1992) Inhibition of Superoxide production in lymphocytes-b by rac antisense oligonucleotides. J. Biol. Chem, 267, 20540-20542,
126. Roberts, A. W., Kim, C., Zhen, L., Lowe, J. B., Kapur, R., Petryniak, B., Spaetti, A., Pollock, J. D., Borneo, J. B., Bradford, G. B., Atkinson, S. J., Dinauer, M. C., Williams, D. A. (1999) Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10, 183-196.
127. Kim, C., Dinauer, M. C. (2001) Rac2 is an essential regulator of neutrophil nicotinamide adenine dinucleotide phosphate oxidase activation in response to specific signaling pathways. J. Immunol, 166, 1223-1232.
128. Glogauer, M., Marchal, C. C., Zhu, F., Worku, A., Clausen, B, E., Foerster, I., Marks, P., Downey, G. P., Dinauer, M., Kwiatkowski, D. J. (2003) Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions, J. Immunol. 170, 5652-5657,
129. Gu, Y., Filippi, M. D., Cancelas, J. A., Siefring, J. E., Williams, E. P., Jasti, A. C., Harris, C. E., Lee, A. W., Prabhakar, R., Atkinson, S. J., Kwiatkowski, D. J., Williams, D. A. (2003) Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases, Science 302, 445-449.
130. Williams, D. A., Tao, W., Yang, F. C., Kim, C., Gu, Y., Mansfield, P., Levine, J. E., Petryniak, B., Derrow, C. W., Harris, C., Jia, B. Q., Zheng, Y., Ambruso, D. R., Lowe, J. B., Atkinson, S. J., Dinauer, M. C., Boxer, L. (2000) Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96, 1646-1654.
131. Ambruso, D. R., Knall, C., Abell, A. N., Panepinto, J., Kurkchubasche, A., Thurman, G., Gonzalez-Aller, C., Hiester. A., deBoer, M., Harbeck. R. J., Over, R., Johnson, G. L., Roos, D. (2000) Human neutrophil immunodeficiency syndrome is associated wilh an inhibitory Rac2 mutation. Proc. Natl. Acad. Sci. USA 97, 4654-4659.
132. rac from its inhibitory GDP/GTP exchange protein (rhoGDI) followed by its translocation to the plasma membrane. Biochem. J. 298, 585-591.
133. Dorseuil, O., Quinn, M. T., Bokoch, G. M. (1995) Dissociation of Rac translocalion from p47-phox/p67-phox movements in human neutrophils by tyrosine kinase inhibitors. J. Leukoc. Biol. 58, 108-113.
134. phox cells, and the level of Superoxide production is exchange factor-dependent. J. Biol. Chem. 277, 19220-19228.
135. Quinn, M. T., Parkos, C. A., Jesaitis, A. J. (1989) The lateral organization of components of the membrane skeleton and Superoxide generation in the plasma membrane of stimulated human neutrophils. Biochim. Biophys. Acta 987, 83-94.
136. Burridge, K., Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167-179.
137. Quinn, M. T., Parkos, C. A., Walker, L., Orkin, S. H., Dinauer, M. C., Jesaitis, A. J. (1989) Association of a ras-related protein with cytochrome b of human neutrophils. Nature 342, 198-200.
138. 558 of NADPH oxidase by phosphorylation of Rap1A. Science 254, 1794-1796.
139. Maly, F-E., Quilliam, L. A., Dorseuil, O., Der, C. J., Bokoch, G. M. (1994) Activated or dominant inhibitory mutants of Rap1A decrease the oxidative burst of Epstein-Barr virus-transformed human B lymphocytes. J. Biol. Chem. 269, 18743-18746.
140. Gabig, T. G., Crean, C. D., Mantel, P. U, Rosli, R. (1995) Function of wild-type or mutant Rac2 and Rap1a GTPases in differentiated HL60 cell NADPH oxidase activation. Blood 85, 804-811.
141. Griendling, K. K. (2004) Novel NAD(P)H oxidases in the cardiovascular system. Heart 90, 491-493.
142. Meier, B. (2001) Superoxide generation of phagocytes and nonphagocytic cells. Protoplasma 217, 117-124.
143. Sun, Y. A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K., Lambeth, J. D. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82.
144. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287, 138-142.
145. Dupuy, C., Ohayon, R., Valent, A., Noël-Hudson, M. S., Dème, D., Virion, A. (1999) Purification of a novel flavoprolein involved in the thyroid NADPH oxidase-cloning of the porcine and human cDNAs. J. Biol. Chem. 274, 37265-37269.
146. De Deken, X., Wang, D. T., Many, M. C., Costagliola, S., Liberi, F., Vassart, G., Dumont, J. E., Miot, F. (2000) Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J. Biol. Chem. 275, 23227-23233.
147. Geiszt, M., Kopp, J. B., Várnai, P., Leto, T. L. (2000) Identification of Renox, an NAD(P)H oxidase in kidney. Proc. Natl. Acad. Sci. USA 97, 8010-8014.
148. Shiose, A., Kuroda, J., Tsuruya, K., Hirai, M., Hirakata, H., Naito, S., Hattori, M., Sakaki, Y., Sumimoto, H. (2001) A novel superoxide-producing NAD(P)H oxidase in kidney. J. Biol. Chem. 276, 1417-1423.
149. phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140.
150. Paffenholz, R., Bergstrom, R. A., Pasutto, F., Wabnitz, R, Munroe, R. J., Jagla, W., Heinzmann, U., Marquardt, A., Bareiss, A., Laufs, J., Russ, A., Stumm, G., Schimenti, J. C., Bergstrom, D. E. (2004) Vestibular defects in head-tilt mice result from mutations in Nox3, encoding un NADPH oxidase. Genes Dev. 18, 486-491.
151. 2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J. Biol. Chem. 276, 37594-37601.
152. Griendling, K. K., Ushio-Fukai, M. (1997) NADH/NADPH oxidase and vascular function. Trends Cardiovasc. Med. 7, 301-307.
153. phox to form a functional oxidase in vascular smooth muscle cells (VSMCs). Circulation 106, S11-164 (abstract).
154. phox participate in activation of superoxide-producing NADPH oxidases. J. Biol. Chem. 278, 25234-25246.
155. Geiszt, M., Lekstrom, K., Brenner, S., Hewitt, S. M., Dana, R., Malech, H. L., Leto, T. L. (2003) NAD(P)H oxirlase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of Superoxide by phagocytes. J. Immunol. 171, 299-306.
156. Bánfi, B., Clark, R. A., Steger, K., Krause, K. H. (2003) Two novel proteins activate Superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 278, 3510-3513.
157. phox support Superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J. Biol. Chem. 278, 20006-20012.
158. Leusen, J. H. W., Verhoeven, A. J., Roos, D. (1996) Interactions between the components of the human NADPH oxidase: intrigues in the phox family. J. Lab. Clin. Med. 128, 461-476.
159. phox. J. Biol. Chem. 274, 19731-19737.
160. phox to activate the phagocyte NADPH oxidase. J. Biol. Chem. 275, 13793-13801.
161. Leto, T. L., Adams, A. G., de Mendez, I. (1994) Assembly of the phagocyte NADPH oxidase: binding of Src homology 3 domains to proline-rich targets. Proc. Natl. Acad. Sci. USA 91, 10650-10654.
162. Finan, P., Shimizu, Y., Gout, I., Hsuan, J., Truong, O., Butcher, C., Bennett, P., Waterfield, M. D., Kellie, S. (1994) An SH3 domain and proline-rich sequence mediate an interaction between two components of the phagocyte NADPH oxidase complex. J. Biol. Chem. 269, 13752-13755.
163. phox. FEBS Lett. 385, 229-232.
164. phox. Biochemistry 40, 3127-3133.
165. 558. Biochim. Biophys. Acta 1567, 221-231.
166. Groemping, Y., Lapouge, K., Smerdon, S. J., Rittinger, K. (2003) Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113, 343-355.
167. 2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 273, 441-445.
168. Agwu, D. E., McPhail, L. C., Sozzani, S., Bass, D. A., McCall, C. E. (1991) Phosphatidic acid as a second messenger in human polymorphonuclear leukocytes. Effects on activation of NADPH oxidase. J. Clin. Invest. 88, 531-539.
169. phox. J. Biol. Chem. 271, 17013-17020.
170. Rotrosen, D., Leto, T. L. (1990) Phosphorylalion of neutrophil 47-kDa cytosolic oxidase factor. Translocation to membrane is associated with distinct phosphorylation events. J. Biol. Chem. 265, 19910-19915.
171. Heyworth, P. G., Badwey. J. A. (1990) Continuous phosphorylation of both the 47 and the 49 kDa proteins during Superoxide production by neutrophils. Biochim. Biophys. Acta 1052, 299-305.
172. phox is required for activation of the NADPH oxidase. J. Biol. Chem. 271, 22152-22158.
173. phox SH3 domain interactions in NADPH oxidase assembly and activation. Mol. Cell. Biol. 17, 2177-2185.
174. phox phosphorylation. J. Biol. Chem. 275, 28406-28412.
175. Gorzalczany, Y., Sigal, N., Itan, M., Lotan, O., Pick, E. (2000) Targeting of Rac1 to the phagocyte membrane is sufficient for the induction of NADPH oxidase assembly. J. Biol. Chem. 275, 40073-40081.
176. Rotrosen, D., Kleinberg, M. E., Nunoi, H., Leto, T., Gallin, J. I., Malech. H. L. (1990) Evidence for a functional cytoplasmic domain of phagocyte oxidase cytochrome b-558. J. Biol. Chem. 265, 8745-8750.
177. DeLeo, F. R., Yu, L., Burritt, J. B., Loetterle, L. R., Bond, C. W., Jesaitix, A. J., Quinn, M. T. (1995) Mapping sites of interaction of p47-phox and flavocytochrome b with random-sequence peptide phage display libraries. Proc. Natl. Acad. Sci. USA 92, 7110-7114.
178. 558 II. Proc. Natl. Acad. Sci. USA 99, 4262-4265.
179. phox. Structural basis for interactions of the Rac1 effector region and insert region with components of the respiratory burst oxidase. J. Biol. Chem. 272, 18834-18841.
180. Diebold, B. A., Bokoch, G. M. (2001) Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat. Immunol. 2, 211-215.
181. phox: conversion of a pagan NADPH oxidase to monotheism. J. Biol. Chem. 277, 18605-18610.
182. -245 are required for the activation of NADPH oxidase by anionic amphiphiles-evidence for an intermediate state of oxidase activation. J. Biol. Chem. 274, 15519-15525.
183. phox binding: a novel role for Rac in NADPH oxidase activation. Biochem. Biophys. Res. Commun. 263, 118-122.
184. 558 initiates NADPH oxidase activation: MRP8/MRP14 regulation. J. Biol. Chem. 278, 25499-25508.
185. phox J. Biol. Chem., In press.
186. Cheng, G., Lambeth, J. D. (2003) NOXO1: regulation of lipid binding, localization and activation of Nox1 by the PX domain. J. Biol. Chem. 279, 4737-4742.
187. Terasawa, H., Noda, Y., Ito, T., Hatanaka, H., Ichikawa, S., Ogura, K., Sumimoto, H., Inagaki, F. (2001) Structure and ligand recognition of the PB1 domain: a novel protein module binding to the PC motif. EMBO J. 20, 3947-3956.
188. Bainton, D. F., Ullyot, J. L., Farquhar, M. G. (1971) The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J. Exp. Med. 134, 907-934.
189. Jack, R. M., Fearon, D. T. (1988) Selective synthesis of mRNA and proteins by human peripheral blood neutrophils. J. Immunol. 140, 4286-4293.
190. Kobayashi, S. D., Voyich, J. M., DeLeo, F. R. (2003) Regulation of the neutrophil-mediated inflammatory response to infection. Microbes Infect. 5, 1337-1344.
191. Hua, J., Hasebe, T., Someya, A., Nakamura, S., Sugimoto, K., Nagaoka, I. (2000) Evaluation of the expression of NADPH oxidase components during maturation of HL-60 cells to neutrophil lineage. J. Leukoc. Biol. 68, 216-224.
192. Skalnik, D. G. (2002) Transcriptional mechanisms regulating myeloid-specific genes. Gene 284, 1-21.
193. phox transcription during granulocytic differentiation of myeloid cells. Blood 99, 4578-4587.
194. phox promoter activity in myeloid cells. J. Biol. Chem. 272, 17802-17809.
195. phox gene: role of AP-1 in concert with myeloid-specific transcription factors. J. Biol. Chem. 276, 39368-39378.
196. phox expression. J. Immunol. 163, 6095-6105.
197. phox promoter activity. J. Leukoc. Biol. 71, 163-172.
198. PHOX expression by inhibiting interaction of PU.1, IRF1, interferon consensus sequence-binding protein, and CREB-binding protein with homologous Cis elements in the CYBB and NCF2 genes. J. Biol. Chem. 276, 37868-37878.
199. phox via a promoter element mutated in a subset of chronic granulomatous disease patients. Blood 93, 3512-3520.
200. Jacobsen, B. M., Skalnik, D. G. (1999) YY1 binds live cis-elements and trans-activates the myeloid cell-restricted gp91 (phox) promoter. J. Biol. Chem. 274, 29984-29993.
201. Skalnik, D. G., Strauss, K. C., Orkin. S. H. (1991) CCAAT displacement protein as a repressor of the myelomonoeytic-specific gp91-phox gene promoter. J. Biol. Chem. 266, 16736-16744.
202. phox promoter. J. Biol. Chem. 271, 18203-18210.
203. phox promoter. Blood 94, 3151-3160.
204. Eklund, E. A., Jalava, A., Kakar, R. (2000) Tyrosine phosphorylation of HoxA10 decreases DNA binding and transcriptional repression during interferon γ-induced differentiation of myeloid leukemia cell lines. J. Biol. Chem. 275, 20117-20126.
205. phox promoter and is down-regulated during myeloid differentiation. J. Biol. Chem. 276, 44472-44480.
206. phox promoter activity. Microbiol. Immunol. 47, 803-811.
207. phox gene expression in eosinophil-committed HL-60-C15 cells. FEBS Lett, 436, 390-394.
208. Skalnik, D. G., Dorfman, D. M., Perkins, A. S., Jenkins, N. A., Copeland, N. G., Orkin, S. H. (1991) Targeting of transgene expression to monocyte/macrophages by the gp91-phox promoter and consequent histiocytic malignancies. Proc. Natl. Acad. Sci. USA 88, 8505-8509.
209. Lien, L. L., Lee, Y., Orkin, S. H. (1997) Regulation of the myeloid-cell-expressed human gp91-phox gene as studied by transfer of yeast artificial chromosome clones into embryonic stem cells: suppression of a variegated cellular pattern of expression requires a full complement of distant cis elements. Mol. Cell. Biol. 17, 2279-2290.
210. phox gene in human peripheral neutrophils, monocytes, and B lymphocytes. Proc. Natl. Acad. Sci. USA 95, 6085-6090.
211. Eklund, E. A., Skalnik, D. G. (1995) Characterization of a gp91-phox promoter element that is required for interferon γ-induced transcription. J. Biol. Chem. 270, 8267-8273.
212. phox Promoter in human monocytic PLB-985 cells. J. Biochem. 131, 533-540.
213. Newburger, P. E., Ezekowitz, C., Whitney, J., Wright, J., Orkin, S. H. (1988) Induction of phagocyte cytochrome b heavy chain gene expression by interferon γ. Proc. Natl. Acad. Sci. USA 85, 5215-5219.
214. Cassatella, M. A., Bazzoni, F., Amezaga, M. A., Rossi, F. (1990) Molecular basis of interferon-γ and lipopolysaccharide enhancement of phagocyte respiratory burst capability. Studies on the gene expression of several NADPH oxidase components. J. Biol. Chem. 265, 20241-20246.
215. Newburger, P. E., Dai, Q., Whitney, C. (1991) In vitro regulation of human phagocyte cytochrome b heavy and light chain gene expression by bacterial lipopolysaccharide and recombinant human cytokines. J. Biol. Chem. 266, 16171-16177.
216. Levy, R., Malech, H. L. (1991) Effect of 1,25-dihydroxyvitamin-D3, lipopolysaccharide, or lipoteichoic acid on the expression of NADPH oxidase components in cultured human monocytes. J. Immunol. 147, 3066-3071.
217. phox gene transcription is associated with changes in PU.1 phosphorylation and increased binding affinity. Biochem. Biophys. Res. Commun. 305, 193-202.
218. Anderson, K. L., Smith, K. A., Pio, F., Torbett, B. E., Maki, R. A. (1998) Neutrophils deficient in PU.1 do not terminally differentiate or become functionally competent. Blood 92, 1576-1585.
219. Li, S. L., Schlegel, W., Valente, A. J., Clark, R. A. (1999) Critical flanking sequences of PU.1 binding sites in myeloid-specific promoters. J. Biol. Chem. 274, 32453-32460.
220. McKercher, S. R., Henkel, G. W., Maki, R. A. (1999) The transcription factor PU.1 does not regulate lineage commitment but has lineage-specific effects. J. Leukoc. Biol. 66, 727-732.
221. Pagano, P. J., Clark, J. K., Cifuentes-Pagano, M. E., Clark, S. M., Callis, C. M., Quinn, M. T. (1997) Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc. Natl. Acad. Sci. USA 94, 14483-14488.
222. Bayraktutan, U., Draper, N., Lang, D., Shah, A. M. (1998) Expression of a functional neutrophil-type NADPH oxidase in cultured rat coronary microvascular endothelial cells. Cardiovasc. Res. 38, 256-262.
223. phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 105, 293-296.
224. phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ. Res. 80, 45-51.
225. phox mRNA expression and NADPH oxidase Superoxide generation in rabbit aortic adventitial fibroblasts. Hypertension 32, 331-337.
226. phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries. Regulation by angiotensin II. Circ. Res. 90, 1205-1213.
227. Chabrashvili, T., Kitiyakara, C., Blau, J., Karber, A., Aslam, S., Welch W. J., Wilcox, C. S. (2003) Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R117-R124,
228. phox-based NADH oxidase in vascular smooth muscle. Biochem. J. 329, 653-657.
229. 558-dependent NAD(P)H oxidase-phox units in smooth muscle and macrophages of atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 22, 2037-2043.
230. Javesghani, D., Hussain, S. N. A., Scheidel, J., Quinn, M. T., Magder, S. A. (2003) Superoxide production in the vasculature of lipopolysaccharide- treated rats and pigs. Shock 19, 486-493.
231. Gosgnach, W., Messika-Zeitoun, D., Gonzalez, W., Philipe, M., Michel, J. B. (2000) Shear stress induces iNOS expression in cultured smooth muscle cells: role of oxidative stress. Am. J. Physiol. Cell Physiol. 279, C1880-C1888.
232. Matsushita, H., Lee, K. H., Tsao, P. S. (2001) Cyclic strain induces reactive oxygen species production via an endothelial NAD(P)H oxidase. J. Cell. Biochem. 81, 99-106.
233. Sorescu, D., Weiss, D., Lassegue, B., Clempus, R. E., Szocs, K., Sorescu, G. P., Valppu, L., Quinn, M. T., Lambeth, J. D., Vega, J. D., Taylor. W. R., Griendling, K. K. (2002) Superoxide production and expression of Nox family proteins in human atherosclerosis. Circulation 105, 1429-1435.
234. Chabrashvili, T., Tojo, A., Onozato, M. L., Kitiyakara, C., Quinn, M. T., Fujita, T., Welch, W. J., Wilcox, C. S. (2002) Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension 39, 269-274.
235. Szocs, K., Lassegue, B., Sorescu, D., Hilenski, L. L., Valppu, I., Couse, T. L., Wilcox, J. N., Quinn, M. T., Lambeth, J. D., Griendling, K. K. (2002) Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler. Thromb. Vasc. Biol. 22, 21-27.
236. Souza, H. P., Souza, L. C., Anastacio, V. M., Pereira, A. C., Junqueira, M. D., Krieger, J. E., Da Luz, P. L., Augusto, O., Laurindo, F. K. M. (2000) Vascular oxidant stress early after balloon injury: evidence for increased NAD(P)H oxidoreductase activity. Free Radic. Biol. Med. 28, 1232-1242.
237. Grote, K., Flach, I., Luchtefeld, M., Akin, E., Holland, S. M., Drexler, H., Schieffer, B. (2003) Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circ. Res. 92, E80-E86.
238. Inoue, I., Goto, S., Mizotani, K., Awata, T., Mastunaga, T., Kawai, S., Nakajima, T., Hokari, S., Komoda, T., Katayama, S. (2000) Lipophilic HMG-CoA reductase inhibitor has an anti-inflammatory effect. Reduction of mRNA levels for interleukin-1β, interleukin-6, cyclooxygenase-2, and p22phox by regulation of peroxisome proliferator-activated receptor α (PPARα) in primary endothelial cells. Life Sci. 67, 863-876.
239. Wagner, A. H., Schroeter, M. R., Heeker, M. (2001) 17β-estradiol inhibition of NADPH oxidase expression in human endothelial cells. FASEB J. 15, 2121-2130.
240. Roos, D., Winterbourn, C. C. (2002) Lethal weapons. Science 296, 669-671.
241. Segal, A. W. (1995) The NADPH oxidase of phagocytic cells is an electron pump that alkalinizes the phagocytic vacuole. Protoplasma 184, 86-103.
242. + flux. Nature 416, 291-297.
243. Reeves, E. P., Nagl, M., Goduvac-Zimmermann, J., Segal, A. W. (2003) Reassessment of the microbicidal activity of reactive oxygen species and hypochlorous acid with reference to the phagocytic vacuole of the neutrophil granulocyte. J. Med. Microbiol. 52, 643-651.
244. + channel is essential for innate immunity. Nature 427, 853-858.
245. Winterbourn, C. C., Vissers, M. C., Kettle, A. J. (2000) Myeloperoxidase. Curr. Opin. Hematol. 7, 53-58.
246. Klebanoff, S. J. (1999) Myeloperoxidase. Proc. Assoc. Am. Physicians 111, 383-389.
247. Aratani, Y., Kura, F., Watanabe, H., Akagawa, H., Takano, Y., Suzuki, K., Dinauer, M. C., Maeda, N., Koyama, H. (2002) Relative contributions of myeloperoxidase and NADPH-oxidase to the early host defense against pulmonary infections with Candida albicans and Aspergillus fumigatus. Med. Mycol. 40, 557-563.
248. Segal, B. H., Leto, T. L., Gallin, J. I., Malech, H. L., Holland, S. M. (2000) Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore) 79, 170-200.
249. Holland, S. M., Gallin, J. I. (1998) Evaluation of the patient with recurrent bacterial infections. Annu. Rev. Med. 49, 185-199.
250. Messina, C. G. M., Reeves, E. P., Roes, E., Segal, A. W. (2002) Catalase negative Staphylococcus aureus retain virulence in mouse model of chronic granulomatous disease. FEBS Lett. 518, 107-110.
251. 2 production. Clin. Immunol. 106, 226-230.
252. phox. J. Gen. Physiol. 120, 759-765.
253. phox modulate proton conduction by the phagocyte NADPH oxidase. J. Biol. Chem. 276, 30277-30284.
254. phox requires histidine 115. Protoplasma 221, 101-108.
255. + conductance in eosinophils: unique characteristics and absence in chronic granulomatous disease. J. Exp. Med. 190, 183-194.
256. phox component of NADPH oxidase is not a voltage-gated proton channel. J. Gen. Physiol. 120, 773-779.
257. + conductance in neutrophils requires assembly of components of the respiratory burst oxidase but not its redox function. J. Clin. Invest. 93, 1770-1775.
258. phox component of NADPH oxidase is not the voltage-gated proton channel in phagocytes, but it helps. J. Biol. Chem. 276, 36063-36066.
259. Morgan, D., Cherny, V. V., Price, M. O., Dinauer, M. C., DeCoursey, T. E. (2002) Absence of proton channels in COS-7 cells expressing functional NADPH oxidase components. J. Gen. Physiol. 119, 571-580.
260. DeCoursey, T. E., Morgan, D., Cherny, V. V. (2003) The voltage dependence of NADPH oxidase reveals why phagocytes need proton channels. Nature 422, 531-534.
261. Forman, H. J., Torres. M. (2002) Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 166, S4-S8.
262. Lambeth, J. D. (2002) Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr. Opin. Hematol. 9, 11-17.
263. 2 generator in human thyroid tissue. Biochimie 81, 373-380.
264. 2-generating system. Exp. Cell Res. 273, 187-196.
265. Moreno, J. C., Bikker, H., Kempers, M. J., van Trotsenburg, A. S., Baas, F., de Vijlder, I. J., Vulsma, T., Ris-Stalpers, C. (2002) Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. N. Engl. J. Med. 347, 95-102.
266. Geiszt, M., Witta, J., Bafli, J., Lekstrom, K., Leto, T. L. (2003) Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 17, 1502-1504.
267. Chen, K., Thomas, S. R., Keaney Jr., J. F. (2003) Beyond LDL oxidation: ROS in vascular signal transduction. Free Radic. Biol. Med. 35, 117-132.
268. Tonyz, R. M. (2003) Reactive oxygen species in vascular biology: role in arterial hypertension. Expert Rev. Cardiovasc. Ther. 1, 91-106.
269. Hilenski, L. I., Clempus, R. E., Quinn, M. T., Lambeth, J. D., Griendling, K. K. (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 677-683.
270. MeIntyre, M., Rohr, D. K., Dominiczak, A. F. (1999) Endothelial function hypertension: the rule of Superoxide anion, Hypertension 34, 539-545.
271. Wang, H. D., Pagano, P. J., Du, Y., Cayatte, A. J., Quinn, M. T., Brecher, P., Cohen, R. A. (1998) Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ. Res. 82, 810-818.
272. - and systolic blood pressure in mice. Circ. Res. 89, 408-414.
273. Saran, M. (2003) To what end does nature produce Superoxide? NADPH oxidase as an autocrine modifier of membrane phospholipids generating paracrine lipid messengers. Free Radic. Res. 37, 1045-1059.
274. Brar, S. S., Kennedy, T. P., Quinn, M., Hoidal, J. R. (2003) Redox signaling of NF-κB by membrane NAD(P)H oxidases in normal and malignant cells. Protoplasma 221, 117-127.
275. Jones, R. D., Hancock. J. T., Morice, A. H. (2000) NADPH oxidase: a universal oxygen sensor? Free Radic. Biol. Med. 29, 416-424.
276. +-channels-in tbe carotid body. Microsc. Res. Tech. 59, 234-242.
277. 558-containing nicotinamide adenine dinucleotide phosphate oxidase. Blood 87, 756-761.
278. 2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase. Proc. Natl. Acad. Sci. USA 96, 7944-7949.
279. + current modulation in wild-type and oxidase-deficient mice. Proc. Natl. Acad. Sci. USA 97, 4374-4379.
280. - sensing in model airway chemoreceptor cells. Biochem. Biophys. Res. Commun. 283, 1131-1134.
281. Kazemian, P., Stephenson, R., Yeger, H., Cutz, E. (2001) Respiratory control in neonatal mice with NADPH oxidase deficiency. Respir. Physiol. 126, 89-101.
282. Sanders, K. A., Sundar, K. M., He, L., Dinger, B., Fidone, S., Hoidal, J. R. (2002) Role of components of the phagocytic NADPH oxidase in oxygen sensing. J. Appl. Physiol. 93, 1357-1364.