Intracellular generation of superoxide by the phagocyte NADPH oxidase: How, where, and what for?

Free Radical Biology and Medicine

Volumn 49, Issue 12, 2010, Pages 1834-1845

  Bylund, Johan ^a   Brown, Kelly L ^a   Movitz, Charlotta ^a   Dahlgren, Claes ^a   Karlsson, Anna ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Activating receptors; CGD; Free radicals; Granule fusion; Inflammation; Intracellular oxidase activity; Phagocyte; Signaling; Subcellular granules

Indexed keywords

DIHYDRORHODAMINE 123; PROTEIN P40; PROTEIN P40PHOX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; UNCLASSIFIED DRUG;

ARTICLE; CHEMOLUMINESCENCE; CHRONIC GRANULOMATOUS DISEASE; ENZYME ACTIVATION; FLUORESCENCE; GENE MUTATION; HUMAN; LYSOSOME; PHAGOCYTE; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

EID: 78650180144     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.09.016     Document Type: Review

References (142)

1. B.M.N.A.D.P.H. Babior oxidase: an update Blood 93 1999 1464 1476
2. A.J. Sbarra, and M.J. Karnovsky The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes J. Biol. Chem. 234 1959 1355 1362
3. A.W. Segal How neutrophils kill microbes Annu. Rev. Immunol. 23 2005 197 223
4. D.I. Brown, and K.K. Griendling Nox proteins in signal transduction Free Radic. Biol. Med. 47 2009 1239 1253
5. R. Korhonen, A. Lahti, H. Kankaanranta, and E. Moilanen Nitric oxide production and signaling in inflammation Curr. Drug Targets Inflamm. Allergy 4 2005 471 479
6. G. Fossati, D.A. Moulding, D.G. Spiller, R.J. Moots, M.R. White, and S.W. Edwards The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis J. Immunol. 170 2003 1964 1972
7. G.M. Bokoch, and T. Zhao Regulation of the phagocyte NADPH oxidase by Rac GTPase Antioxid. Redox Signal. 8 2006 1533 1548
8. S.J. Klebanoff Myeloperoxidase friend and foe J. Leukoc. Biol. 77 2005 598 625
9. M. Faurschou, and N. Borregaard Neutrophil granules and secretory vesicles in inflammation Microbes Infect. 5 2003 1317 1327
10. N. Borregaard, J.M. Heiple, E.R. Simons, and R.A. Clark Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation J. Cell Biol. 97 1983 52 61
11. R.A. Clark, K.G. Leidal, D.W. Pearson, and W.M. Nauseef NADPH oxidase of human neutrophils: subcellular localization and characterization of an arachidonate-activatable superoxide-generating system J. Biol. Chem. 262 1987 4065 4074
12. C. Dahlgren, A. Johansson, H. Lundqvist, O.W. Bjerrum, and N. Borregaard Activation of the oxygen-radical-generating system in granules of intact human neutrophils by a calcium ionophore (ionomycin) Biochem. Biophys. Acta 1137 1992 182 188
13. T. Kobayashi, J.M. Robinson, and H. Seguchi Identification of intracellular sites of superoxide production in stimulated neutrophils J. Cell Sci. 111 1998 81 91
14. H. Berendes, R.A. Bridges, and R.A. Good A fatal granulomatosus of childhood: the clinical study of a new syndrome Minn. Med. 40 1957 309 312
15. B. Holmes, A.R. Page, and R.A. Good Studies of the metabolic activity of leukocytes from patients with a genetic abnormality of phagocytic function J. Clin. Invest. 46 1967 1422 1432
16. P.G. Quie, J.G. White, B. Holmes, and R.A. Good In vitro bactericidal capacity of human polymorphonuclear leukocytes: diminished activity in chronic granulomatous disease of childhood J. Clin. Invest. 46 1967 668 679
17. D.R. Ambruso, C. Knall, A.N. Abell, J. Panepinto, A. Kurkchubasche, G. Thurman, C. Gonzalez-Aller, A. Hiester, M. deBoer, R.J. Harbeck, R. Oyer, G.L. Johnson, and D. Roos Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation Proc. Natl Acad. Sci. USA 97 2000 4654 4659
18. A.G. Kurkchubasche, J.A. Panepinto, T.F. Tracy Jr., G.W. Thurman, and D.R. Ambruso Clinical features of a human Rac2 mutation: a complex neutrophil dysfunction disease J. Pediatr. 139 2001 141 147
19. J.A. Winkelstein, M.C. Marino, R.B. Johnston Jr., J. Boyle, J. Curnutte, J.I. Gallin, H.L. Malech, S.M. Holland, H. Ochs, P. Quie, R.H. Buckley, C.B. Foster, S.J. Chanock, and H. Dickler Chronic granulomatous disease: report on a national registry of 368 patients Medicine (Baltimore) 79 2000 155 169
20. A.R. Cross, J.L. Yarchover, and J.T. Curnutte The superoxide-generating system of human neutrophils possesses a novel diaphorase activity: evidence for distinct regulation of electron flow within NADPH oxidase by p67-phox and p47-phox J. Biol. Chem. 269 1994 21448 21454
21. B.H. Segal, T.L. Leto, J.I. Gallin, H.L. Malech, and S.M. Holland Genetic, biochemical, and clinical features of chronic granulomatous disease Medicine (Baltimore) 79 2000 170 200
22. J.D. Matute, A.A. Arias, N.A. Wright, I. Wrobel, C.C. Waterhouse, X.J. Li, C.C. Marchal, N.D. Stull, D.B. Lewis, M. Steele, J.D. Kellner, W. Yu, S.O. Meroueh, W.M. Nauseef, and M.C. Dinauer A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity Blood 114 2009 3309 3315
23. C. Dahlgren, and A. Karlsson Respiratory burst in human neutrophils J. Immunol. Meth. 232 1999 3 14
24. C. Dahlgren, A. Karlsson, and J. Bylund Measurement of respiratory burst products generated by professional phagocytes Meth. Mol. Biol. 412 2007 349 363
25. C. Elbim, and G. Lizard Flow cytometric investigation of neutrophil oxidative burst and apoptosis in physiological and pathological situations Cytom. A 75 2009 475 481
26. S. Szucs, G. Vamosi, R. Poka, A. Sarvary, H. Bardos, M. Balazs, J. Kappelmayer, L. Toth, J. Szollosi, and R. Adany Single-cell measurement of superoxide anion and hydrogen peroxide production by human neutrophils with digital imaging fluorescence microscopy Cytometry 33 1998 19 31
27. S.F. van Eeden, M.E. Klut, B.A. Walker, and J.C. Hogg The use of flow cytometry to measure neutrophil function J. Immunol. Meth. 232 1999 23 43
28. S.G. Rhee, T.S. Chang, W. Jeong, and D. Kang Methods for detection and measurement of hydrogen peroxide inside and outside of cells Mol. Cells 29 2010 539 549
29. A. Emmendorffer, M. Hecht, M.L. Lohmann-Matthes, and J. Roesler A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123 J. Immunol. Meth. 131 1990 269 275
30. L.J. van Pelt, R. van Zwieten, R.S. Weening, D. Roos, A.J. Verhoeven, and B.G. Bolscher Limitations on the use of dihydrorhodamine 123 for flow cytometric analysis of the neutrophil respiratory burst J. Immunol. Meth. 191 1996 187 196
31. Molecular Probes. The Handbook: Probes for Reactive Oxygen Species Including Nitric Oxide. URL: www.invitrogen.com ; 2010.
32. A.K. Campbell Chemiluminescence: Principles and Applications in Biology and Medicine 1988 Ellis Horwood Chichester
33. - production Arch. Biochem. Biophys. 373 2000 447 450
34. C.D. Porter, M.H. Parkar, M.K. Collins, R.J. Levinsky, and C. Kinnon Superoxide production by normal and chronic granulomatous disease (CGD) patient-derived EBV-transformed B cell lines measured by chemiluminescence-based assays J. Immunol. Meth. 155 1992 151 157
35. H. Aniansson, O. Stendahl, and C. Dahlgren Comparison between luminol- and lucigenin-dependent chemiluminescence of polymorphonuclear leukocytes Acta Pathol. Microbiol. Immunol. Scand. C 92 1984 357 361 (Pubitemid 15153350)
36. C. Dahlgren, H. Aniansson, and K.E. Magnusson Pattern of formylmethionyl-leucyl-phenylalanine-induced luminol- and lucigenin-dependent chemiluminescence in human neutrophils Infect. Immun. 47 1985 326 328
37. H. Lundqvist, and C. Dahlgren Isoluminol-enhanced chemiluminescence: a sensitive method to study the release of superoxide anion from human neutrophils Free Radic. Biol. Med. 20 1996 785 792
38. C. Dahlgren Polymorphonuclear leukocyte chemiluminescence induced by formylmethionyl-leucyl-phenylalanine and phorbol myristate acetate: effects of catalase and superoxide dismutase Agents Actions 21 1987 104 112
39. R. Lock, A. Johansson, K. Orselius, and C. Dahlgren Analysis of horseradish peroxidase-amplified chemiluminescence produced by human neutrophils reveals a role for the superoxide anion in the light emitting reaction Anal. Biochem. 173 1988 450 455
40. 2: studies with normal and cytochalasin B-treated cells J. Clin. Invest. 60 1977 1266 1279
41. L. Mauch, A. Lun, M.R. O'Gorman, J.S. Harris, I. Schulze, A. Zychlinsky, T. Fuchs, U. Oelschlagel, S. Brenner, D. Kutter, A. Rosen-Wolff, and J. Roesler Chronic granulomatous disease (CGD) and complete myeloperoxidase deficiency both yield strongly reduced dihydrorhodamine 123 test signals but can be easily discerned in routine testing for CGD Clin. Chem. 53 2007 890 896
42. C. Dahlgren, A. Johansson, and K. Orselius Difference in hydrogen peroxide release between human neutrophils and neutrophil cytoplasts following calcium ionophore activation: a role of the subcellular granule in activation of the NADPH-oxidase in human neutrophils? Biochim. Biophys. Acta 1010 1989 41 48
43. W.M. Nauseef How human neutrophils kill and degrade microbes: an integrated view Immunol. Rev. 219 2007 88 102
44. E.W. Odell, and A.W. Segal The bactericidal effects of the respiratory burst and the myeloperoxidase system isolated in neutrophil cytoplasts Biochim. Biophys. Acta 971 1988 266 274
45. A.J. Jesaitis, E.S. Buescher, D. Harrison, M.T. Quinn, C.A. Parkos, S. Livesey, and J. Linner Ultrastructural localization of cytochrome b in the membranes of resting and phagocytosing human granulocytes J. Clin. Invest. 85 1990 821 835
46. R.C. Allen, R.L. Stjernholm, M.A. Reed, T.B. Harper III, Gupta S., R.H. Steele, and W.W. Waring Correlation of metabolic and chemiluminescent responses of granulocytes from three female siblings with chronic granulomatous disease J. Infect. Dis. 136 1977 510 518
47. D. Granfeldt, and C. Dahlgren An intact cytoskeleton is required for prolonged respiratory burst activity during neutrophil phagocytosis Inflammation 25 2001 165 169
48. R. Lock, C. Dahlgren, M. Linden, O. Stendahl, A. Svensbergh, and L. Öhman Neutrophil killing of two type 1 fimbria-bearing Escherichia coli strains: dependence on respiratory burst activation Infect. Immun. 58 1990 37 42
49. J.K. Femling, V.V. Cherny, D. Morgan, B. Rada, A.P. Davis, G. Czirjak, P. Enyedi, S.K. England, J.G. Moreland, E. Ligeti, W.M. Nauseef, and T.E. DeCoursey The antibacterial activity of human neutrophils and eosinophils requires proton channels but not BK channels J. Gen. Physiol. 127 2006 659 672
50. B. Musset, V.V. Cherny, D. Morgan, and T.E. DeCoursey The intimate and mysterious relationship between proton channels and NADPH oxidase FEBS Lett. 583 2009 7 12
51. I.S. Ramsey, M.M. Moran, J.A. Chong, and D.E. Clapham A voltage-gated proton-selective channel lacking the pore domain Nature 440 2006 1213 1216
52. M. Sasaki, M. Takagi, and Y. Okamura A voltage sensor-domain protein is a voltage-gated proton channel Science 312 2006 589 592
53. T.E. DeCoursey Voltage-gated proton channels find their dream job managing the respiratory burst in phagocytes Physiology (Bethesda) 25 2010 27 40
54. A. El Chemaly, Y. Okochi, M. Sasaki, S. Arnaudeau, Y. Okamura, and N. Demaurex VSOP/Hv1 proton channels sustain calcium entry, neutrophil migration, and superoxide production by limiting cell depolarization and acidification J. Exp. Med. 207 2010 129 139
55. D. Morgan, V.V. Cherny, M.O. Price, M.C. Dinauer, and T.E. DeCoursey Absence of proton channels in COS-7 cells expressing functional NADPH oxidase components J. Gen. Physiol. 119 2002 571 580
56. A. Karlsson, and C. Dahlgren Assembly and activation of the neutrophil NADPH oxidase in granule membranes Antioxid. Redox Signaling 4 2002 49 60
57. J.M. Robinson Reactive oxygen species in phagocytic leukocytes Histochem. Cell Biol. 130 2008 281 297
58. J.M. Robinson Phagocytic leukocytes and reactive oxygen species Histochem. Cell Biol. 131 2009 465 469
59. F.J. Miller Jr., M. Filali, G.J. Huss, B. Stanic, A. Chamseddine, T.J. Barna, and F.S. Lamb Cytokine activation of nuclear factor kappa B in vascular smooth muscle cells requires signaling endosomes containing Nox1 and ClC-3 Circ. Res. 101 2007 663 671
60. H. Seguchi, and T. Kobayashi Study of NADPH oxidase-activated sites in human neutrophils J. Electron Microsc. (Tokyo) 51 2002 87 91
61. C. Vaissiere, V. Le Cabec, and I. Maridonneau-Parini NADPH oxidase is functionally assembled in specific granules during activation of human neutrophils J. Leukoc. Biol. 65 1999 629 634
62. C. Dahlgren Difference in extracellular radical release after chemotactic factor and calcium ionophore activation of the oxygen radical-generating system in human neutrophils Biochim. Biophys. Acta 930 1987 33 38
63. 2+ concentrations are essential and synergize with a kinetically distinct second signal Biochem. J. 322 1997 709 718
64. H. Lundqvist, P. Follin, L. Khalfan, and C. Dahlgren Phorbol myristate acetate-induced NADPH oxidase activity in human neutrophils: only half the story has been told J. Leukoc. Biol. 59 1996 270 279
65. O.J. Holt, F. Gallo, and G.M. Griffiths Regulating secretory lysosomes J. Biochem. 140 2006 7 12
66. O. Utermohlen, J. Herz, M. Schramm, and M. Kronke Fusogenicity of membranes: the impact of acid sphingomyelinase on innate immune responses Immunobiology 213 2008 307 314
67. K. Lollike, M. Lindau, J. Calafat, and N. Borregaard Compound exocytosis of granules in human neutrophils J. Leukoc. Biol. 71 2002 973 980
68. S. Scepek, and M. Lindau Exocytotic competence and intergranular fusion in cord blood-derived eosinophils during differentiation Blood 89 1997 510 517
69. N. Borregaard, L. Kjeldsen, K. Rygaard, L. Bastholm, M.H. Nielsen, H. Sengelov, O.W. Bjerrum, and A.H. Johnsen Stimulus-dependent secretion of plasma proteins from human neutrophils J. Clin. Invest. 90 1992 86 96
70. A. Karlsson, P. Follin, H. Leffler, and C. Dahlgren Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils Blood 91 1998 3430 3438
71. T. Weber, B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Sollner, and J.E. Rothman SNAREpins: minimal machinery for membrane fusion Cell 92 1998 759 772
72. B. Martin-Martin, S.M. Nabokina, J. Blasi, P.A. Lazo, and F. Mollinedo Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis Blood 96 2000 2574 2583
73. J.H. Brumell, A. Volchuk, H. Sengelov, N. Borregaard, A.M. Cieutat, D.F. Bainton, S. Grinstein, and A. Klip Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments J. Immunol. 155 1995 5750 5759
74. F. Mollinedo, and P.A. Lazo Identification of two isoforms of the vesicle-membrane fusion protein SNAP-23 in human neutrophils and HL-60 cells Biochem. Biophys. Res. Commun. 231 1997 808 812
75. I. Ofek, J. Goldhar, Y. Keisari, and N. Sharon Nonopsonic phagocytosis of microorganisms Annu. Rev. Microbiol. 49 1995 239 276
76. L. Serrander, J. Larsson, H. Lundqvist, M. Lindmark, M. Fallman, C. Dahlgren, and O. Stendahl Particles binding beta(2)-integrins mediate intracellular production of oxidative metabolites in human neutrophils independently of phagocytosis Biochim. Biophys. Acta 1452 1999 133 144
77. H. Fu, A.A. Belaaouaj, C. Dahlgren, and J. Bylund Outer membrane protein A deficient Escherichia coli activates neutrophils to produce superoxide and shows increased susceptibility to antibacterial peptides Microbes Infect. 5 2003 781 788
78. P. Follin, A. Johansson, and C. Dahlgren Intracellular production of reactive oxygen species in human neutrophils following activation by the soluble stimuli FMLP, dioctanoylglycerol and ionomycin Cell Biochem. Funct. 9 1991 29 37
79. J. Almkvist, and A. Karlsson Galectins as inflammatory mediators Glycoconj. J. 19 2004 575 581
80. H. Leffler, S. Carlsson, M. Hedlund, Y. Qian, and F. Poirier Introduction to galectins Glycoconj. J. 19 2004 433 440
81. J. Almkvist, C. Dahlgren, H. Leffler, and A. Karlsson Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1 J. Immunol. 168 2002 4034 4041
82. S. Carlsson, C.T. Oberg, M.C. Carlsson, A. Sundin, U.J. Nilsson, D. Smith, R.D. Cummings, J. Almkvist, A. Karlsson, and H. Leffler Affinity of galectin-8 and its carbohydrate recognition domains for ligands in solution and at the cell surface Glycobiology 17 2007 663 676
83. A. Yamaoka, I. Kuwabara, L.G. Frigeri, and F.T. Liu A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils J. Immunol. 154 1995 3479 3487
84. A. Karlsson Wheat germ agglutinin induces NADPH-oxidase activity in human neutrophils by interaction with mobilizable receptors Infect. Immun. 67 1999 3461 3468
85. A. Martner, C. Dahlgren, J.C. Paton, and A.E. Wold Pneumolysin released during Streptococcus pneumoniae autolysis is a potent activator of intracellular oxygen radical production in neutrophils Infect. Immun. 76 2008 4079 4087
86. M.J. Rabiet, E. Huet, and F. Boulay The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview Biochimie 89 2007 1089 1106
87. C. Dahlgren, T. Christophe, F. Boulay, P.N. Madianos, M.J. Rabiet, and A. Karlsson The synthetic chemoattractant Trp-Lys-Tyr-Met-Val-DMet activates neutrophils preferentially through the lipoxin A(4) receptor Blood 95 2000 1810 1818
88. K.E. Anderson, K.B. Boyle, K. Davidson, T.A. Chessa, S. Kulkarni, G.E. Jarvis, A. Sindrilaru, K. Scharffetter-Kochanek, O. Rausch, L.R. Stephens, and P.T. Hawkins CD18-dependent activation of the neutrophil NADPH oxidase during phagocytosis of Escherichia coli or Staphylococcus aureus is regulated by class III but not class I or II PI3Ks Blood 112 2008 5202 5211
89. S.A. Bissonnette, C.M. Glazier, M.Q. Stewart, G.E. Brown, C.D. Ellson, and M.B. Yaffe Phosphatidylinositol 3-phosphate-dependent and -independent functions of p40phox in activation of the neutrophil NADPH oxidase J. Biol. Chem. 283 2008 2108 2119
90. C. Ellson, K. Davidson, K. Anderson, L.R. Stephens, and P.T. Hawkins PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation EMBO J. 25 2006 4468 4478
91. C.I. Suh, N.D. Stull, X.J. Li, W. Tian, M.O. Price, S. Grinstein, M.B. Yaffe, S. Atkinson, and M.C. Dinauer The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgammaIIA receptor-induced phagocytosis J. Exp. Med. 203 2006 1915 1925
92. A. Karlsson, J.B. Nixon, and L.C. McPhail Phorbol myristate acetate induces neutrophil NADPH-oxidase activity by two separate signal transduction pathways: dependent or independent of phosphatidylinositol 3-kinase J. Leukoc. Biol. 67 2000 396 404
93. C.D. Ellson, K.E. Anderson, G. Morgan, E.R. Chilvers, P. Lipp, L.R. Stephens, and P.T. Hawkins Phosphatidylinositol 3-phosphate is generated in phagosomal membranes Curr. Biol. 11 2001 1631 1635
94. F. Kanai, H. Liu, S.J. Field, H. Akbary, T. Matsuo, G.E. Brown, L.C. Cantley, and M.B. Yaffe The PX domains of p47phox and p40phox bind to lipid products of PI(3)K Nat. Cell Biol. 3 2001 675 678
95. A.S. Nicot, and J. Laporte Endosomal phosphoinositides and human diseases Traffic 9 2008 1240 1249
96. A.M. Condliffe, K. Davidson, K.E. Anderson, C.D. Ellson, T. Crabbe, K. Okkenhaug, B. Vanhaesebroeck, M. Turner, L. Webb, M.P. Wymann, E. Hirsch, T. Ruckle, M. Camps, C. Rommel, S.P. Jackson, E.R. Chilvers, L.R. Stephens, and P.T. Hawkins Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils Blood 106 2005 1432 1440
97. A. Fontayne, P.M. Dang, M.A. Gougerot-Pocidalo, and J. El-Benna Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation Biochemistry 41 2002 7743 7750
98. J.D. Kent, S. Sergeant, D.J. Burns, and L.C. McPhail Identification and regulation of protein kinase C-delta in human neutrophils J. Immunol. 157 1996 4641 4647
99. G.E. Brown, M.Q. Stewart, H. Liu, V.L. Ha, and M.B. Yaffe A novel assay system implicates PtdIns(3, 4)P(2), PtdIns(3)P, and PKC delta in intracellular production of reactive oxygen species by the NADPH oxidase Mol. Cell 11 2003 35 47
100. S. Sergeant, and L.C. McPhail Opsonized zymosan stimulates the redistribution of protein kinase C isoforms in human neutrophils J. Immunol. 159 1997 2877 2885
101. P.M. Dang, S. Rais, J. Hakim, and A. Perianin Redistribution of protein kinase C isoforms in human neutrophils stimulated by formyl peptides and phorbol myristate acetate Biochem. Biophys. Res. Commun. 212 1995 664 672
102. 2+ influx and activation of the neutrophil respiratory burst: different regulation of plasma membrane- and granule-localized NADPH-oxidase J. Leukoc. Biol. 71 2002 611 617
103. D.S. Regier, D.G. Greene, S. Sergeant, A.J. Jesaitis, and L.C. McPhail Phosphorylation of p22phox is mediated by phospholipase D-dependent and -independent mechanisms: correlation of NADPH oxidase activity and p22phox phosphorylation J. Biol. Chem. 275 2000 28406 28412
104. T. Bengtsson, K. Orselius, and J. Wettero Role of the actin cytoskeleton during respiratory burst in chemoattractant-stimulated neutrophils Cell Biol. Int. 30 2006 154 163
105. J. Chen, R. He, R.D. Minshall, M.C. Dinauer, and R.D. Ye Characterization of a mutation in the Phox homology domain of the NADPH oxidase component p40phox identifies a mechanism for negative regulation of superoxide production J. Biol. Chem. 282 2007 30273 30284
106. J. Bylund, D. Goldblatt, and D.P. Speert Chronic granulomatous disease: from genetic defect to clinical presentation Adv. Exp. Med. Biol. 568 2005 67 87
107. S.M. Holland Chronic granulomatous disease Clin. Rev. Allergy Immunol. 38 2010 3 10
108. S.D. Rosenzweig Inflammatory manifestations in chronic granulomatous disease (CGD) J. Clin. Immunol. 28 Suppl. 1 2008 S67 S72
109. D. Roos, and C.C. Winterbourn Immunology: lethal weapons Science 296 2002 669 671
110. A. George-Chandy, I. Nordstrom, E. Nygren, I.M. Jonsson, J. Postigo, L.V. Collins, and K. Eriksson Th17 development and autoimmune arthritis in the absence of reactive oxygen species Eur. J. Immunol. 38 2008 1118 1126
111. D.E. Morgenstern, M.A. Gifford, L.L. Li, C.M. Doerschuk, and M.C. Dinauer Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus J. Exp. Med. 185 1997 207 218
112. J.D. Pollock, D.A. Williams, M.A. Gifford, L.L. Li, X. Du, J. Fisherman, S.H. Orkin, C.M. Doerschuk, and M.C. Dinauer Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production Nat. Genet. 9 1995 202 209
113. M. Schappi, C. Deffert, L. Fiette, G. Gavazzi, F. Herrmann, D. Belli, and K.H. Krause Branched fungal beta-glucan causes hyperinflammation and necrosis in phagocyte NADPH oxidase-deficient mice J. Pathol. 214 2008 434 444
114. B.H. Segal, W. Han, J.J. Bushey, M. Joo, Z. Bhatti, J. Feminella, C.G. Dennis, R.R. Vethanayagam, F.E. Yull, M. Capitano, P.K. Wallace, H. Minderman, J.W. Christman, M.B. Sporn, J. Chan, D.C. Vinh, S.M. Holland, L.R. Romani, S.L. Gaffen, M.L. Freeman, and T.S. Blackwell NADPH oxidase limits innate immune responses in the lungs in mice PLoS ONE 5 2010 e9631
115. J. Bylund, K.L. MacDonald, K.L. Brown, P. Mydel, L.V. Collins, R.E. Hancock, and D.P. Speert Enhanced inflammatory responses of chronic granulomatous disease leukocytes involve ROS-independent activation of NF-kappa B Eur. J. Immunol. 37 2007 1087 1096
116. E. Hatanaka, B.T. Carvalho, A. Condino-Neto, and A. Campa Hyperresponsiveness of neutrophils from gp 91phox deficient patients to lipopolysaccharide and serum amyloid A Immunol. Lett. 94 2004 43 46
117. J.A. Lekstrom-Himes, D.B. Kuhns, W.G. Alvord, and J.I. Gallin Inhibition of human neutrophil IL-8 production by hydrogen peroxide and dysregulation in chronic granulomatous disease J. Immunol. 174 2005 411 417
118. F. Meissner, R.A. Seger, D. Moshous, A. Fischer, J. Reichenbach, and A. Zychlinsky Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease Blood 116 2010 1370 1373
119. K.L. Brown, J. Bylund, K.L. MacDonald, G.X. Song-Zhao, M.R. Elliott, R. Falsafi, R.E. Hancock, and D.P. Speert ROS-deficient monocytes have aberrant gene expression that correlates with inflammatory disorders of chronic granulomatous disease Clin. Immunol. 129 2008 90 102
120. S.D. Kobayashi, J.M. Voyich, K.R. Braughton, A.R. Whitney, W.M. Nauseef, H.L. Malech, and F.R. DeLeo Gene expression profiling provides insight into the pathophysiology of chronic granulomatous disease J. Immunol. 172 2004 636 643
121. L. Zhen, A.A. King, Y. Xiao, S.J. Chanock, S.H. Orkin, and M.C. Dinauer Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox Proc. Natl Acad. Sci. USA 90 1993 9832 9836
122. S.J. Vowells, S. Sekhsaria, H.L. Malech, M. Shalit, and T.A. Fleisher Flow cytometric analysis of the granulocyte respiratory burst: a comparison study of fluorescent probes J. Immunol. Meth. 178 1995 89 97
123. K.A. Gelderman, M. Hultqvist, J. Holmberg, P. Olofsson, and R. Holmdahl T cell surface redox levels determine T cell reactivity and arthritis susceptibility Proc. Natl Acad. Sci. USA 103 2006 12831 12836
124. S.H. Jackson, J.I. Gallin, and S.M. Holland The p47phox mouse knock-out model of chronic granulomatous disease J. Exp. Med. 182 1995 751 758
125. Q. Liu, L.I. Cheng, L. Yi, N. Zhu, A. Wood, C.M. Changpriroa, J.M. Ward, and S.H. Jackson p47phox deficiency induces macrophage dysfunction resulting in progressive crystalline macrophage pneumonia Am. J. Pathol. 174 2009 153 163
126. E.S. Buescher, D.W. Alling, and J.I. Gallin Use of an X-linked human neutrophil marker to estimate timing of lyonization and size of the dividing stem cell pool J. Clin. Invest. 76 1985 1581 1584
127. C.M. Cale, L. Morton, and D. Goldblatt Cutaneous and other lupus-like symptoms in carriers of X-linked chronic granulomatous disease: incidence and autoimmune serology Clin. Exp. Immunol. 148 2007 79 84
128. N. Mossberg, C. Movitz, K. Hellstrand, T. Bergstrom, S. Nilsson, and O. Andersen Oxygen radical production in leukocytes and disease severity in multiple sclerosis J. Neuroimmunol. 213 2009 131 134
129. N. Mossberg, O. Andersen, S. Nilsson, C. Dahlgren, K. Hellstrand, M. Lindh, A. Svedhem, T. Bergstrom, and C. Movitz Oxygen radical production and severity of the Guillain-Barre syndrome J. Neuroimmunol. 192 2007 186 191
130. R.A. Clark, and S. Szot Chemotactic factor inactivation by stimulated human neutrophils mediated by myeloperoxidase-catalyzed methionine oxidation J. Immunol. 128 1982 1507 1513
131. H. Forsman, E. Salomonsson, K. Onnheim, J. Karlsson, A. Bjorstad, H. Leffler, J. Bylund, A. Karlsson, and C. Dahlgren The beta-galactoside binding immunomodulatory lectin galectin-3 reverses the desensitized state induced in neutrophils by the chemotactic peptide f-Met-Leu-Phe: role of reactive oxygen species generated by the NADPH-oxidase and inactivation of the agonist Glycobiology 18 2008 905 912
132. M. Hultqvist, L.M. Olsson, K.A. Gelderman, and R. Holmdahl The protective role of ROS in autoimmune disease Trends Immunol. 30 2009 201 208
133. P.J. Ferguson, M.A. Lokuta, H.I. El-Shanti, L. Muhle, X. Bing, and A. Huttenlocher Neutrophil dysfunction in a family with a SAPHO syndrome-like phenotype Arthritis Rheum. 58 2008 3264 3269
134. J.D. Rioux, R.J. Xavier, K.D. Taylor, M.S. Silverberg, P. Goyette, A. Huett, T. Green, P. Kuballa, M.M. Barmada, L.W. Datta, Y.Y. Shugart, A.M. Griffiths, S.R. Targan, A.F. Ippoliti, E.J. Bernard, L. Mei, D.L. Nicolae, M. Regueiro, L.P. Schumm, A.H. Steinhart, J.I. Rotter, R.H. Duerr, J.H. Cho, M.J. Daly, and S.R. Brant Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis Nat. Genet. 39 2007 596 604
135. R.L. Roberts, J.E. Hollis-Moffatt, R.B. Gearry, M.A. Kennedy, M.L. Barclay, and T.R. Merriman Confirmation of association of IRGM and NCF4 with ileal Crohn's disease in a population-based cohort Genes Immun. 9 2008 561 565
136. L.M. Olsson, A.K. Lindqvist, H. Kallberg, L. Padyukov, H. Burkhardt, L. Alfredsson, L. Klareskog, and R. Holmdahl A case-control study of rheumatoid arthritis identifies an associated single nucleotide polymorphism in the NCF4 gene, supporting a role for the NADPH-oxidase complex in autoimmunity Arthritis Res. Ther. 9 2007 R98
137. J.A. Knight Free radicals, antioxidants, and the immune system Ann. Clin. Lab. Sci. 30 2000 145 158
138. H. Liu, R. Colavitti, I.I. Rovira, and T. Finkel Redox-dependent transcriptional regulation Circ. Res. 97 2005 967 974
139. G. Gloire, S. Legrand-Poels, and J. Piette NF-kappaB activation by reactive oxygen species: fifteen years later Biochem. Pharmacol. 72 2006 1493 1505
140. S. Carta, P. Castellani, L. Delfino, S. Tassi, R. Vene, and A. Rubartelli DAMPs and inflammatory processes: the role of redox in the different outcomes J. Leukoc. Biol. 86 2009 549 555
141. K. Schroder, and J. Tschopp The inflammasomes Cell 140 2010 821 832
142. F.L. van de Veerdonk, S.P. Smeekens, L.A. Joosten, B.J. Kullberg, C.A. Dinarello, J.W. van der Meer, and M.G. Netea Reactive oxygen species-independent activation of the IL-1beta inflammasome in cells from patients with chronic granulomatous disease Proc. Natl Acad. Sci. USA 107 2010 3030 3033