Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species

FEBS Journal

Volumn 275, Issue 13, 2008, Pages 3249-3277

  Sumimoto, Hideki ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Duox; Nox; Noxa1; Noxo1; p22phox; p40phox; p47 phox; p67phox; Rac; Rboh

Indexed keywords

CALCIUM BINDING PROTEIN; OXIDOREDUCTASE; PROTEIN P40; PROTEIN P67; RAC PROTEIN; 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; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE A; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE C;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; ENZYME ACTIVATION; ENZYME STRUCTURE; MITOCHONDRION; NAEGLERIA GRUBERI; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CYTOPLASM; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; NAEGLERIA; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; REACTIVE OXYGEN SPECIES;

AMOEBOZOA; ANIMALIA; EMBRYOPHYTA; EUKARYOTA; EXCAVATA; FUNGI/METAZOA GROUP; NAEGLERIA GRUBERI; PLANTAE; PROKARYOTA;

EID: 44949106317     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06488.x     Document Type: Review

References (207)

1. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4, 181 189.
2. Nauseef WM (2004) Assembly of the phagocyte NADPH oxidase. Histochem Cell Biol 122, 277 291.
3. Quinn MT Gauss KA (2004) Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol 76, 760 781.
4. Cross AR Segal AW (2004) The NADPH oxidase of professional phagocytes - prototype of the NOX electron transport chain systems. Biochim Biophys Acta 1657, 1 22.
5. Geiszt M Leto TL (2004) The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279, 51715 51718.
6. Sumimoto H, Miyano K Takeya R (2005) Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem Biophys Res Commun 338, 677 686.
7. Groemping Y Rittinger K (2005) Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J 386, 401 416.
8. Dagher MC Pick E (2007) Opening the black box: lessons from cell-free systems on the phagocyte NADPH-oxidase. Biochimie 89, 1123 1132.
9. Bedard K Krause K-H (2007) The NOX family of ROS-generating NADPH oxidase: physiology and pathophysiology. Physiol Rev 87, 245 313.
10. Lambeth JD, Kawahara T Diebold B (2007) Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 43, 319 331.
11. Roos D, de Boer M, Kuribayashi F, Meischl C, Weening RS, Segal AW, Ahlin A, Nemet K, Hossle JP, Bernatowska-Matuszkiewicz E et al. (1996) Mutations in the X-linked and autosomal recessive forms of chronic granulomatous disease. Blood 87, 1663 1681.
12. Heyworth PG, Cross AR Curnutte JT (2003) Chronic granulomatous disease. Curr Opin Immunol 15, 578 584.
13. Overmyer K, Broschí M Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8, 335 342.
14. Torres MA Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8, 397 403.
15. Sagi M Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141, 336 340.
16. -245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbicidal oxidase of phagocytes. Biochem J 284, 781 788.
17. 558, a component of the phagocyte NADPH oxidase, is a flavoprotein. Biochem Biophys Res Commun 186, 1368 1375.
18. Finegold AA, Shatwell KP, Segal AW, Klausner RD 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.
19. Shatwell KP, Dancis A, Cross AR, Klausner RD Segal AW (1996) The FRE1 ferric reductase of Saccharomyces cerevisiae is a cytochrome b similar to that of NADPH oxidase. J Biol Chem 271, 14240 14244.
20. Georgatsou E, Mavrogiannis LA, Fragiadakis GS Alexandraki D (1997) The yeast Fre1p/Fre2p cupric reductases facilitate copper uptake and are regulated by the copper-modulated Mac1p activator. J Biol Chem 272, 13786 13792.
21. -245 of the neutrophil superoxide-generating system contains two nonidentical hemes. J Biol Chem 270, 17075 17077.
22. Saraste M (1984) Location of haem-binding sites in the mitochondrial cytochrome b. FEBS Lett 166, 367 372.
23. 6-f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81, 674 678.
24. Robertson DE, Farid RS, Moser CC, Urbauer JL, Mulholland SE, Pidikiti R, Lear JD, Wand AJ, DeGrado WF Dutton PL (1994) Design and synthesis of multi-haem proteins. Nature 368, 425 432.
25. 1 complex from bovine heart mitochondria. Science 277, 60 66.
26. 1 complex. Science 281, 64 71.
27. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 302, 1009 1014.
28. 6f complex. Nature 426, 413 418.
29. Smith JL, Zhang H, Yan J, Kurisu G Cramer WA (2004) Cytochrome bc complexes: a common core of structure and function surrounded by diversity in the outlying provinces. Curr Opin Struct Biol 14, 432 439.
30. 6f complex for its charge transfer pathways. Biochim Biophys Acta 1757, 339 345.
31. 6f complex. Annu Rev Biochem 75, 769 790.
32. phox. J Biol Chem 276, 31105 31112.
33. 558. J Biol Chem 270, 7853 7857.
34. 558. Evidence that low-spin heme iron is essential for O2- generating activity. J Biol Chem 270, 12685 12689.
35. 558: the flavin-binding component of the phagocyte NADPH oxidase. Science 256, 1459 1462.
36. Sugawara M, Sugawara Y, Wen K Giulivi C (2002) Generation of oxygen free radicals in thyroid cells and inhibition of thyroid peroxidase. Exp Biol Med. 227, 141 146.
37. 2-generating activity. J Biol Chem 280, 30046 30054.
38. Robinson NJ, Procter CM, Connolly EL Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397, 694 697.
39. Waters BM, Blevins DG Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129, 85 94.
40. Schagerlof U, Wilson G, Hebert H, Al-Karadaghi S Hagerhall C (2006) Transmembrane topology of FRO2, a ferric chelate reductase from Arabidopsis thaliana. Plant Mol Biol 62, 215 221.
41. + reductase: prototype for a structurally novel flavoenzyme family. Science 251, 60 66.
42. + reductase catalytic mechanism. Eur J Biochem 270, 1900 1915.
43. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS Kim JJ (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94, 8411 8416.
44. Murataliev MB, Feyereisen R Walker FA (2004) Electron transfer by diflavin reductases. Biochim Biophys Acta 1698, 1 26.
45. Leclerc D, Wilson A, Dumas R, Gafuik C, Song D, Watkins D, Heng HH, Rommens JM, Scherer SW, Rosenblatt DS et al. (1998) Cloning and mapping of a cDNA for methionine synthase reductase, a flavoprotein defective in patients with homocystinuria. Proc Natl Acad Sci USA 95, 3059 3064.
46. Paine MJ, Garner AP, Powell D, Sibbald J, Sales M, Pratt N, Smith T, Tew DG Wolf CR (2000) Cloning and characterization of a novel human dual flavin reductase. J Biol Chem 275, 1471 1478.
47. Olteanu H Banerjee R (2003) Redundancy in the pathway for redox regulation of mammalian methionine synthase: reductive activation by the dual flavoprotein, novel reductase 1. J Biol Chem 278, 38310 38314.
48. Iyanagi T (2005) Structure and function of NADPH-cytochrome P450 reductase and nitric oxide synthase reductase domain. Biochem Biophys Res Commun 338, 520 528.
49. Alderton WK, Cooper CE Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357, 593 615.
50. Baldauf SL (2003) The deep roots of eukaryotes. Science 300, 1703 1706.
51. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20, 670 676.
52. Parfrey LW, Barbero E, Lasser E, Dunthorn M, Bhattacharya D, Patterson DJ Katz LA (2006) Evaluating support for the current classification of eukaryotic diversity. PLoS Genet 2, doi:.
53. Arisue N, Hasegawa M Hashimoto T (2005) Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol Biol Evol 22, 409 420.
54. Embley TM Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440, 623 630.
55. Lardy B, Bof M, Aubry L, Paclet MH, Morel F, Satre M Klein G (2005) NADPH oxidase homologs are required for normal cell differentiation and morphogenesis in Dictyostelium discoideum. Biochim Biophys Acta 1744, 199 212.
56. Lalucque H Silar P (2003) NADPH oxidase: an enzyme for multicellularity? Trends Microbiol 11, 9 12.
57. Takemoto D, Tanaka A Scott B (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44, 1065 1076.
58. Hervé C, Tonon T, Collén J, Corre E Boyen C (2006) NADPH oxidases in eukaryotes: red algae provide new hints!. Curr Genet 49, 190 204.
59. Aguirre J, Ríos-Momberg M, Hewitt D Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13, 111 118.
60. Moreno JC, Bikker H, Kempers MJ, van Trotsenburg AS, Baas F, de Vijlder JJ, 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.
61. Song Y, Driessens N, Costa M, De Deken X, Detours V, Corvilain B, Maenhaut C, Miot F, Van Sande J, Many MC et al. (2007) Roles of hydrogen peroxide in thyroid physiology and disease. J Clin Endocrinol Metab 92, 3764 3773.
62. Wong JL, Creton R Wessel GM (2004) The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1. Dev Cell 7, 801 814.
63. phox. J Cell Biol 154, 879 891.
64. Ha EM, Oh CT, Bae YS Lee WJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847 850.
65. 2+ treatment. Biochem J 283, 591 595.
66. 2+ activation of the NADPH oxidase 5 (NOX5). J Biol Chem 279, 18583 18591.
67. Grasberger H, De Deken X, Miot F, Pohlenz J Refetoff S (2007) Missense mutations of dual oxidase 2 (DUOX2) implicated in congenital hypothyroidism have impaired trafficking in cells reconstituted with DUOX2 maturation factor. Mol Endocrinol 21, 1408 1421.
68. 2 generation in thyroid cells does not involve Rac1 activation. Eur J Endocrinol 152, 127 133.
69. 2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276, 37594 37601.
70. Ritsick DR, Edens WA, Finnerty V Lambeth JD (2007) Nox regulation of smooth muscle contraction. Free Rad Biol Med 43, 31 38.
71. phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126, 1281 1290.
72. 2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 42, 798 809.
73. Jagnandan D, Church JE, Bánfi B, Stuehr DJ, Marrero MB Fulton DJ (2007) Novel mechanism of activation of NADPH oxidase 5. Calcium sensitization via phosphorylation. J Biol Chem 282, 6494 6507.
74. Tirone F Cox JA (2007) NADPH oxidase 5 (NOX5) interacts with and is regulated by calmodulin. FEBS Lett 581, 1202 1208.
75. Gapper C Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141, 341 345.
76. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T et al. (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022 4034.
77. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065 1680.
78. Nühse TS, Bottrill AR, Jones AM Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51, 931 940.
79. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H Shimamoto K (1999) The small GTP-binding protein rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96, 10922 10926.
80. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438, 1013 1016.
81. Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T Shimamoto K (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci USA 103, 230 235.
82. Pawson T, Raina M Nash P (2002) Interaction domains: from simple binding events to complex cellular behavior. FEBS Lett 513, 2 10.
83. Pawson T Nash P (2003) Assembly of cell regulatory systems through protein interaction domains. Science 300, 445 452.
84. 558 include incorporation of heme as a prerequisite for heterodimer assembly. J Biol Chem 275, 13986 13993.
85. Grasberger H Refetoff S (2006) Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J Biol Chem 281, 18269 18272.
86. Zamproni I, Grasberger H, Cortinovis F, Vigone MC, Chiumello G, Mora S, Onigata K, Fugazzola L, Refetoff S, Persani L et al. (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.
87. Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R Brandes RP (2004) Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 279, 45935 45941.
88. phox-dependent manner: its regulation by oxidase organizers and activators. J Biol Chem 280, 23328 23339.
89. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC Knaus UG (2006) Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18, 69 82.
90. phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J Biol Chem 280, 31859 31869.
91. Kuroda J, Nakagawa K, Yamasaki T, Nakamura K, Takeya R, Kuribayashi F, Imajoh-Ohmi S, Igarashi K, Shibata Y, Sueishi K et al. (2005) The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells 10, 1139 1151.
92. phox in the structural maturation and subcellular targeting of Nox3. Biochem J 403, 97 108.
93. phox causes vestibular and immune defects in mice. J Clin Invest 118, 1176 1185.
94. Kawahara T Lambeth JD (2007) Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol Biol 7, 178, doi:.
95. Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB et al. (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85 88.
96. Delsuc F, Brinkmann H, Chourrout D Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965 968.
97. Inoue Y, Ogasawara M, Moroi T, Satake M, Azumi K, Moritomo T Nakanishi T (2005) Characteristics of NADPH oxidase genes (Nox2, p22, p47, and p67) and Nox4 gene expressed in blood cells of juvenile Ciona intestinalis. Immunogenetics 57, 520 534.
98. Kawahara BT, Quinn MT Lambeth JD (2007) Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol 7, 109, doi:.
99. phoxin vitro. J Biol Chem 271, 22578 22582.
100. 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.
101. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling K Lambeth JD (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79 82.
102. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287, 138 142.
103. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H et al. (2005) Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112, 2677 2685.
104. Dikalova A, Clempus R, Lassègue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D et al. (2005) Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112, 2668 2676.
105. Gavazzi G, Bánfi B, Deffert C, Fiette L, Schappi M, Herrmann F Krause K-H (2006) Decreased blood pressure in NOX1-deficient mice. FEBS Lett 580, 497 504.
106. phox participate in activation of superoxide-producing NADPH oxidases. J Biol Chem 278, 25234 25246.
107. phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J Biol Chem 278, 20006 20012.
108. Bánfi B, Clark RA, Steger K Krause K-H (2003) Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem 278, 3510 3513.
109. Cheng G Lambeth JD (2004) NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the phox homology (PX) domain. J Biol Chem 279, 4737 4742.
110. Ueyama T, Geiszt M Leto TL (2006) Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol Cell Biol 26, 2160 2174.
111. Miyano K, Ueno N, Takeya R Sumimoto H (2006) Direct involvement of the small GTPase Rac in activation of the superoxide-producing NADPH oxidase Nox1. J Biol Chem 281, 21857 21868.
112. Cheng G, Diebold BA, Hughes Y Lambeth JD (2006) Nox1-dependent reactive oxygen generation is regulated by Rac1. J Biol Chem 281, 17718 17726.
113. Paffenholz R, Bergstrom RA, Pasutto F, Wabnitz P, Munroe RJ, Jagla W, Heinzmann U, Marquardt A, Bareiss A, Laufs J et al. (2004) Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev 18, 486 491.
114. Bánfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M Krause K-H (2004) NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 279, 46065 46072.
115. phox. J Biol Chem 279, 34250 34255.
116. phox-dependent NADPH oxidases. Biochimie 89, 1133 1144.
117. Geiszt M, Kopp JB, Varnai P Leto TL (2000) Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97, 8010 8014.
118. 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.
119. Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, Takada J, Wakisaka M, Ibayashi S, Utsumi H Iida M (2004) Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109, 227 233.
120. Serrander L, Cartier L, Bedard K, Bánfi B, Lardy B, Plastre O, Sienkiewicz A, Forro L, Schlegel W Krause K-H (2007) NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406, 105 114.
121. Gorin Y, Ricono JM, Kim NH, Bhandari B, Choudhury GG Abboud HE (2003) Nox4 mediates angiotensin II-induced activation of Akt/protein kinase B in mesangial cells. Am J Physiol Renal Physiol 285, F219 F229.
122. Sumimoto H, Kage Y, Nunoi H, Sasaki H, Nose T, Fukumaki Y, Ohno M, Minakami S Takeshige K (1994) Role of Src homology 3 domains in assembly and activation of the phagocyte NADPH oxidase. Proc Natl Acad Sci USA 91, 5345 5349.
123. Leto TL, Adams AG 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.
124. phox. J Exp Med 180, 2329 2334.
125. Groemping Y, Lapouge K, Smerdon SJ Rittinger K (2003) Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113, 343 355.
126. phox-derived proline-rich peptide. J Biol Chem 281, 3660 3668.
127. phox. Biochem J 396, 183 192.
128. Lang BF, O'Kelly C, Nerad T, Gray MW Burger G (2002) The closest unicellular relatives of animals. Curr Biol 12, 1773 1778.
129. King N (2004) The unicellular ancestry of animal development. Dev Cell 7, 313 325.
130. phox maturation and NADPH oxidase activity. J Biol Chem 281, 30336 30346.
131. phox. Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47phox, thereby activating the oxidase. J Biol Chem 274, 33644 33653.
132. phox, the regulatory subunit of the phagocyte NADPH oxidase. Genes Cells 9, 443 456.
133. phox in an autoinhibited form. J Biol Chem 279, 29752 29760.
134. phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases. J Biol Chem 269, 23431 23436.
135. PHOX on serine 303 or 304. J Biol Chem 273, 9539 9543.
136. phox to activate the phagocyte NADPH oxidase. J Biol Chem 275, 13793 137801.
137. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y et al. (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447, 714 719.
138. phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem J 296, 557 561.
139. Chenevert J (1994) Cell polarization directed by extracellular cues in yeast. Mol Biol Cell 5, 1169 1175.
140. Ponting CP (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci 5, 2353 2357.
141. Sumimoto H, Ito T, Hata K, Mizuki K, Nakamura R, Kage Y, Sakaki Y, Nakamura M Takeshige K (1997) Membrane translocation of cytosolic factors in activation of the phagocyte NADPH oxidase: role of protein-protein interaction. In Membrane Proteins: Structure, Function and Expression Control (Hamasaki N Mihara K, eds pp. 235 245. Kyushu University Press, Fukuoka,/S. Karger AG, Basel.
142. phox bind to lipid products of PI(3)K. Nat Cell Biol 3, 675 678.
143. 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.
144. phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc Natl Acad Sci USA 100, 4474 4479.
145. phox to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J 21, 5057 5068.
146. 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.
147. Mayumi M, Takeda Y, Hoshiko M, Serada K, Murata M, Moritomo T, Takizawa F, Kobayashi I, Araki K, Nakanishi T et al. (2008) Characterization of teleost phagocyte NADPH oxidase: molecular cloning and expression analysis of carp (Cyprinus carpio) phagocyte NADPH oxidase. Mol Immunol 45, 1720 1731.
148. phox.. J Biol Chem 278, 14469 14479.
149. Yamamoto A, Kami K, Takeya R Sumimoto H (2007) Interaction between the SH3 domains and C-terminal proline-rich region in NADPH oxidase organizer 1 (Noxo1). Biochem Biophys Res Commun 352, 560 565.
150. Takeya R, Taura M, Yamasaki T, Naito S Sumimoto H (2006) Expression and function of Noxo1gamma, an alternative splicing form of the NADPH oxidase organizer 1. FEBS J 273, 3663 3677.
151. Ueyama T, Lekstrom K, Tsujibe S, Saito N Leto TL (2007) Subcellular localization and function of alternatively spliced Noxo1 isoforms. Free Rad Biol Med 42, 180 190.
152. Kiss PJ, Knisz J, Zhang Y, Baltrusaitis J, Sigmund CD, Thalmann R, Smith RJ, Verpy E Bánfi B (2006) Inactivation of NADPH oxidase organizer 1 results in severe imbalance. Curr Biol 16, 208 213.
153. phox SH3 domains in assembly of the NADPH oxidase system. J Biol Chem 269, 16326 16332.
154. phox, SH3-domain-containing proteins involved in the phagocyte NADPH oxidase complex. Eur J Biochem 251, 573 582.
155. Finan P, Shimizu Y, Gout I, Hsuan J, Truong O, Butcher C, Bennett P, Waterfield MD 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.
156. phox of the human neutrophil NADPH oxidase that are not required for activation in the cell-free system. J Biol Chem 270, 11216 11221.
157. phox, Grb2 and Pex13p. EMBO J 21, 4268 4276.
158. phox. Structural and functional comparison of p40phox and p67phox SH3 domains. J Biol Chem 280, 13752 13761.
159. phox. Arch Biochem Biophys 444, 185 194.
160. Abo A, Pick E, Hall A, Totty N, Teahan CG Segal AW (1991) Activation of
161. Knaus UG, Heyworth PG, Evans T, Curnutte JT Bokoch GM (1991) Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science 254, 1512 1515.
162. Mizuno T, Kaibuchi K, Ando S, Musha T, Hiraoka K, Takaishi K, Asada M, Nunoi H, Matsuda I Takai Y (1992) Regulation of the superoxide-generating NADPH oxidase by a small GTP-binding protein and its stimulatory and inhibitory GDP/GTP exchange proteins. J Biol Chem 267, 10215 10218.
163. Ambruso DR, Knall C, Abell AN, Panepinto J, Kurkchubasche A, Thurman G, Gonzalez-Aller C, Hiester A, deBoer M, Harbeck RJ et al. (2000) Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc Natl Acad Sci USA 97, 4654 4659.
164. Williams DA, Tao W, Yang F, Kim C, Gu Y, Mansfield P, Levine JE, Petryniak B, Derrow CW, Harris C et al. (2000) Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96, 1646 1654.
165. phox and regulation of phagocytic NADPH oxidase activity. Science 265, 531 533.
166. phox participate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase. J Biol Chem 274, 25051 25060.
167. D'Andrea LD Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28, 655 662.
168. phox in complex with Rac.GTP. Mol Cell 6, 899 907.
169. 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.
170. Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18, 2807 2821.
171. phox in the phagocyte NADPH oxidase activation in vitro. Biochem Biophys Res Commun 241, 226 231.
172. Han C-H, Freeman JL, Lee T, Motalebi SA Lambeth JD (1998) Regulation of the neutrophil respiratory burst oxidase. Identification of an activation domain in p67phox. J Biol Chem 273, 16663 16668.
173. Price MO, McPhail LC, Lambeth JD, Han CH, Knaus UG Dinauer MC (2002) Creation of a genetic system for analysis of the phagocyte respiratory burst: high-level reconstitution of the NADPH oxidase in a nonhematopoietic system. Blood 99, 2653 2661.
174. 558. J Biol Chem 274, 22999 23005.
175. phox: conversion of a pagan NADPH oxidase to monotheism. J Biol Chem 277, 18605 18610.
176. phox-Rac1 chimeras. J Biol Chem 279, 16007 16016.
177. Mizrahi A, Berdichevsky Y, Ugolev Y, Molshanski-Mor S, Nakash Y, Dahan I, Alloul N, Gorzalczany Y, Sarfstein R, Hirshberg M et al. (2006) Assembly of the phagocyte NADPH oxidase complex: chimeric constructs derived from the cytosolic components as tools for exploring structure-function relationships. J Leukoc Biol 79, 881 895.
178. Diebold BA Bokoch GM (2001) Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat Immunol 2, 211 215.
179. phox, and Rac1 elicit activator-independent superoxide production by phagocyte membranes: an essential role for anionic membrane phospholipids. J Biol Chem 282, 22122 22139.
180. Sumimoto H, Kamakura S Ito T (2007) Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci STKE, doi:.
181. phox as a positive regulator of the superoxide-producing phagocyte oxidase. EMBO J 21, 6312 6320.
182. phox activates the NADPH oxidase during FcγIIA receptor-induced phagocytosis. J Exp Med 203, 1915 1925.
183. phox-/- mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing. J Exp Med 203, 1927 1937.
184. 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.
185. 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.
186. Yoshinaga S, Kohjima M, Ogura K, Yokochi M, Takeya R, Ito T, Sumimoto H Inagaki F (2003) The PB1 domain and the PC motif-containing region are structurally similar protein binding modules. EMBO J 22, 4888 4897.
187. Wilson MI, Gill DJ, Perisic O, Quinn MT Williams RL (2003) PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol Cell 12, 39 50.
188. Noda Y, Kohjima M, Izaki T, Ota K, Yoshinaga S, Inagaki F, Ito T Sumimoto H (2003) Molecular recognition in dimerization between PB1 domains. J Biol Chem 278, 43516 43524.
189. Hirano Y, Yoshinaga S, Takeya R, Suzuki NN, Horiuchi M, Kohjima M, Sumimoto H Inagaki F (2005) Structure of a cell polarity regulator, a complex between atypical PKC and Par6 PB1 domains. J Biol Chem 280, 9653 9661.
190. phox, SH3 domain-containing cytosolic factors of the phagocyte NADPH oxidase. Eur J Biochem 251, 583 589.
191. phox. Nat Cell Biol 3, 679 682.
192. Ellson CD, Anderson KE, Morgan G, Chilvers ER, Lipp P, Stephens LR Hawkins PT (2001) Phosphatidylinositol 3-phosphate is generated in phagosomal membranes. Curr Biol 11, 1631 1635.
193. Minakami R Sumimoto H (2006) Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the NADPH oxidase (Nox) family. Int J Hematol 84, 193 198.
194. phox structure suggests a basis for regulation mechanism of its membrane binding. EMBO J 26, 1176 1186.
195. phox. Mol Biol Cell 18, 441 454.
196. phox bound to phosphatidylinositol 3-phosphate. Mol Cell 8, 829 839.
197. phox. FEBS Lett 385, 229 232.
198. Dehal P Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3, doi:.
199. Nakatani Y, Takeda H, Kohara Y Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17, 1254 1265.
200. Valante AJ, El Jamali A, Epperson TK, Gamez MJ, Pearson DW Clark RA (2007) NOX1 NADPH oxidase regulation by the NOXA1 SH3 domain. Free Rad Biol Med 43, 384 396.
201. Malagnac F, Lalucque H, Lepere G Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anseina. Fungal Genet Biol 41, 982 997.
202. Tanaka A, Christensen MJ, Takemoto D, Park P Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18, 1052 1066.
203. Kamiguti AS, Serrander L, Lin K, Harris RJ, Cawley JC, Allsup DJ, Slupsky JR, Krause K-H Zuzel M (2005) Expression and activity of NOX5 in the circulating malignant B cells of hairy cell leukemia. J Immunol 175, 8424 8430.
204. 2+ binding motifs. Plant Cell 10, 255 266.
205. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27, 401 410.
206. Gribaldo S Philippe H (2002) Ancient phylogenetic relationships. Theor Popul Biol 61, 391 408.
207. Baldauf SL (2003) Phylogeny for the faint of heart: a tutorial. Trends Genet 19, 345 351.