The phagocyte NADPH oxidase depends on cholesterol-enriched membrane microdomains for assembly

EMBO Journal

Volumn 23, Issue 4, 2004, Pages 739-748

  Vilhardt, Frederik ^a   Van Deurs, Bo ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cholesterol; Lipid rafts; NADPH oxidase; Phagocytes; Superoxide

Indexed keywords

CHOLESTEROL; DETERGENT; GUANOSINE TRIPHOSPHATASE; LACTATE DEHYDROGENASE (CYTOCHROME); PROTEIN P47; PROTEIN P56; RAC PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL FREE SYSTEM; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSOL; ENZYME MECHANISM; ENZYME SUBUNIT; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN TRANSPORT;

ANIMALS; CELL LINE; CHOLESTEROL; CYTOCHROME B GROUP; DETERGENTS; ENZYME ACTIVATION; HL-60 CELLS; HUMANS; ISOENZYMES; MEMBRANE MICRODOMAINS; MICE; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; PHAGOCYTES; PHOSPHOPROTEINS; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; SUPEROXIDES;

ANIMALIA;

EID: 1842510009     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600066     Document Type: Article

References (50)

1. Ago T, Kuribayashi F, Hiroaki H, Takeya R, Ito T, Kohda D, Sumimoto H (2003) Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc Natl Acad Sci USA 100: 4474-4479
2. Ago T, Nunoi H, Ito T, Sumimoto H (1999) Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47(phox). Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47(phox), thereby activating the oxidase. J Biol Chem 274: 33644-33653
3. Allen LA, DeLeo FR, Gallois A, Toyoshima S, Suzuki K, Nauseef WM (1999) Transient association of the nicotinamide adenine dinucleotide phosphate oxidase subunits p47phox and p67phox with phagosomes in neutrophils from patients with X-linked chronic granulomatous disease. Blood 93: 3521-3530
4. Bodin S, Giuriato S, Ragab J, Humbel BM, Viala C, Vieu C, Chap H, Payrastre B (2001) Production of phosphatidylinositol 3,4,5-trisphosphate and phosphatidic acid in platelet rafts: evidence for a critical role of cholesterol-enriched domains in human platelet activation. Biochemistry 40: 15290-15299
5. Bokoch GM, Bohl BP, Chuang TH (1994) Guanine nucleotide exchange regulates membrane translocation of Rac/Rho GTP-binding proteins. J Biol Chem 269: 31674-31679
6. Bokoch GM, Diebold BA (2002) Current molecular models for NADPH oxidase regulation by Rac GTPase. Blood 100: 2692-2696
7. Bokoch GM, Prossnitz V (1992) Isoprenoid metabolism is required for stimulation of the respiratory burst oxidase of HL60 cells. J Clin Invest 89: 402-408
8. Braccia A, Villani M, Immerdal L, Niels-Christiansen LL, Nystrom BT, Hansen GH, Danielsen EM (2003) Microvillar membrane microdomains exist at physiological temperature: Galectin-4's role as lipid raft stabilizer revealed by 'super rafts'. J Biol Chem 278: 15679
9. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533-544
10. Brown MS, Goldstein JL (1980) Mulitvalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth. J Lipid Res 21: 505-517
11. Chamberlain LH, Burgoyne RD, Gould GW (2001) SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc Natl Acad Sci USA 98: 5619-5624
12. Clark RA, Volpp BD, Leidal KG, Nauseef WM (1990) Two cytosolic components of the human neutrophil respiratory burst oxidase translocate to the plasma membrane during cell activation. J Clin Invest 85: 714-721
13. DeLeo FR, Allen LA, Apicella M, Nauseef WM (1999) NADPH oxidase activation and assembly during phagocytosis. J Immunol 163: 6732-6740
14. Drevot P, Langlet C, Guo XJ, Bernard AM, Colard O, Chauvin JP, Lasserre R, He HT (2002) TCR signal initiation machinery is preassembled and activated in a subset of membrane rafts. EMBO J 21: 1899-1908
15. Dusi S, Della Bianca V, Grzeskowiak M, Rossi F (1993) Relationship between phosphorylation and translocation to the plasma membrane of p47phox and p67phox and activation of the NADPH oxidase in normal and Ca(2+)-depleted human neutrophils. Biochem J 290: 173-178
16. Foster LJ, De Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 100: 5813-5818
17. Galandrini R, Tassi I, Mattia G, Lenti L, Piccoli M, Frati L, Santoni A (2002) SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood 100: 4581-4589
18. Gomez-Mouton C, Abad JL, Mira E, Lacalle RA, Gallardo E, Jimenez-Baranda S, Illa I, Bernad A, Manes S, Martinez AC (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 98: 9642-9647
19. Grimmer S, van Deurs B, Sandvig K (2002) Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 115: 2953-2962
20. Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942
21. Heyworth PG, Bohl BP, Bokoch GM, Curnutte JT (1994) Rac translocates independently of the neutrophil NADPH oxidase components p47phox and p67phox. Evidence for its interaction with flavocytochrome b558. J Biol Chem 269: 30749-30752
22. Heyworth PG, Curnutte JT, Nauseef WM, Volpp BD, Pearson DW, Rosen H, Clark RA (1991) Neutrophil nicotinamide adenine dinucleotide phosphate oxidase assembly. Translocation of p47-phox and p67-phox requires interaction between p47-phox and cytochrome b558. J Clin Invest 87: 352-356
23. Inoue H, Sawada M, Ryo A, Tanahashi H, Wakatsuki T, Hada A, Kondoh N, Nakagaki K, Takahashi K, Suzumura A, Yamamoto M, Tabira T (1999) Serial analysis of gene expression in a microglial cell line. Glia 28: 265-271
24. Jutras I, Abrami L, Dautry-Varsat A (2003) Entry of the lymphogranuloma venereum strain of Chlamydia trachomatis into host cells involves cholesterol-rich membrane domains. Infect Immun 71: 260-266
25. Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE, Cantley LC, Yaffe MB (2001) The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol 3: 675-678
26. Kilsdonk EP, Yancey PG, Stoudt GW, Bangerter FW, Johnson WJ, Phillips MC, Rothblat GH (1995) Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 270: 17250-17256
27. Klopfenstein DR, Tomishige M, Stuurman N, Vale RD (2002) Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109: 347-358
28. Knoller S, Shpungin S, Pick E (1991) The membrane-associated component of the amphiphile-activated, cytosol-dependent superoxide-forming NADPH oxidase of macrophages is identical to cytochrome b559. J Biol Chem 266: 2795-2804
29. Korchak HM, Rossi MW, Kilpatrick LE (1998) Selective role for beta-protein kinase C in signaling for O-2 generation but not degranulation or adherence in differentiated HL60 cells. J Biol Chem 273: 27292-27299
30. Kumanogoh H, Miyata S, Sokawa Y, Maekawa S (2001) Biochemical and morphological analysis on the localization of Rac1 in neurons. Neurosci Res 39: 189-196
31. Leusen JH, Bolscher BG, Hilarius PM, Weening RS, Kaulfersch W, Seger RA, Roos D, Verhoeven AJ (1994a) 156Pro- > Gln substitution in the light chain of cytochrome b558 of the human NADPH oxidase (p22-phox) leads to defective translocation of the cytosolic proteins p47-phox and p67-phox. J Exp Med 180: 2329-2334
32. Leusen JH, de Boer M, Bolscher BG, Hilarius PM, Weening RS, Ochs HD, Roos D, Verhoeven AJ (1994b) A point mutation in gp91-phox of cytochrome b558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox. J Clin Invest 93: 2120-2126
33. Madore N, Smith KL, Graham CH, Jen A, Brady K, Hall S, Morris R (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J 18: 6917-6926
34. Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, Brown DA (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem 274: 3910-3917
35. Michaely PA, Mineo C, Ying YS, Anderson RG (1999) Polarized distribution of endogenous Rac1 and RhoA at the cell surface. J Biol Chem 274: 21430-21436
36. Nauseef WM, Volpp BD, McCormick S, Leidal KG, Clark RA (1991) Assembly of the neutrophil respiratory burst oxidase. Protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components. J Biol Chem 266: 5911-5917
37. Park JW, Ma M, Ruedi JM, Smith RM, Babior BM (1992) The cytosolic components of the respiratory burst oxidase exist as a M(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
38. Pierini LM, Eddy RJ, Fuortes M, Seveau S, Casulo C, Maxfield FR (2003) Membrane lipid organization is critical for human neutrophil polarization. J Biol Chem 278: 10831-10841
39. Pralle A, Keller P, Florin EL, Simons K, Horber JK (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148: 997-1008
40. Quinn MT, Evans T, Loetterle LR, Jesaitis AJ, Bokoch GM (1993) Translocation of Rac correlates with NADPH oxidase activation. Evidence for equimolar translocation of oxidase components. J Biol Chem 268: 20983-20987
41. Roper K, Corbeil D, Huttner WB (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2: 582-592
42. Shao D, Segal AW, Dekker LV (2003) Lipid rafts determine efficiency of NADPH oxidase activation in neutrophils. FEBS lett 550: 101-106
43. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387: 569-572
44. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39
45. Toporik A, Gorzalczany Y, Hirshberg M, Pick E, Lotan O (1998) Mutational analysis of novel effector domains in Rac1 involved in the activation of nicotinamide adenine dinucleotide phosphate (reduced) oxidase. Biochemistry 37: 7147-7156
46. Varma R, Mayor S (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394: 798-801
47. Vilhardt F, Plastre O, Sawada M, Suzuki K, Wiznerowicz M, Kiyokawa E, Trono D, Krause K-H (2002) The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem 277: 42136-42143
48. Wientjes FB, Segal AW, Hartwig JH (1997) Immunoelectron microscopy shows a clustered distribution of NADPH oxidase components in the human neutrophil plasma membrane. J Leukoc Biol 61: 303-312
49. Woodman RC, Ruedi JM, Jesaitis AJ, Okamura N, Quinn MT, Smith RM, Curnutte JT, Babior BM (1991) Respiratory burst oxidase and three of four oxidase-related polypeptides are associated with the cytoskeleton of human neutrophils. J Clin Invest 87: 1345-1351
50. 2 produced by human neutrophils during the respiratory burst. Anal Biochem 165: 371-378