FcεRI- and Fcγ receptor-mediated production of reactive oxygen species by mast cells is lipoxygenase- and cyclooxygenase-dependent and NADPH oxidase-independent

Journal of Immunology

Volumn 179, Issue 10, 2007, Pages 7059-7071

  Swindle, Emily J ^a   Coleman, John W ^a   DeLeo, Frank R ^b   Metcalfe, Dean D ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; CYCLOOXYGENASE 1 INHIBITOR; DICHLORODIHYDROFLUORESCEIN; DIPHENYLIODONIUM SALT; DOCEBENONE; FC EPSILON RI RECEPTOR; FC RECEPTOR; FR 122047; IMMUNOGLOBULIN G; LIPOXYGENASE INHIBITOR; NORDIHYDROGUAIARETIC ACID; P47PHOX PROTEIN; PROSTAGLANDIN SYNTHASE; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SILVER; UNCLASSIFIED DRUG; ZILEUTON; CYCLOOXYGENASE 1; CYTOKINE; ENZYME INHIBITOR; IMMUNOGLOBULIN E RECEPTOR; MEMBRANE PROTEIN; PTGS1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CAPPING PHENOMENON; CELL SECRETION; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; FLUORESCENCE; HUMAN; HUMAN CELL; MAST CELL; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; IMMUNOLOGY; METABOLISM;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; BONE MARROW CELLS; CELL DEGRANULATION; CELLS, CULTURED; CYCLOOXYGENASE 1; CYTOKINES; ENZYME INHIBITORS; HUMANS; IMMUNOGLOBULIN G; IMMUNOLOGIC CAPPING; MAST CELLS; MEMBRANE PROTEINS; MICE; NADPH OXIDASE; NEUTROPHILS; REACTIVE OXYGEN SPECIES; RECEPTORS, IGE; RECEPTORS, IGG;

EID: 38449101478     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.10.7059     Document Type: Article

References (70)

1. Hampton, M. B., A. J. Kettle, and C. C. Winterbourn. 1998. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
2. Babior, B. M. 2004. NADPH oxidase. Curr. Opin. Immunol. 16: 42-47.
3. Thannickal, V. J., and B. L. Fanburg. 2000. Reactive oxygen species in cell signaling. Am. J. Physiol. 279: L1005-L1028.
4. Jackson, S. H., S. Devadas, J. Kwon, L. A. Pinto, and M. S. Williams. 2004. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 5: 818-827.
5. Devadas, S., L. Zaritskaya, S. G. Rhee, L. Oberley, and M. S. Williams. 2002. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and Fas ligand expression. J. Exp. Med. 195: 59-70.
6. Reth, M. 2002. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3: 1129-1134.
7. 2+ and an oxidant signal. Cell 121: 281-293.
8. 2 for platelet-derived growth factor signal transduction. Science 270: 296-299.
9. Bae, Y. S., S. W. Kang, M. S. Seo, I. C. Baines, E. Tekle, P. B. Chock, and S. G. Rhee. 1997. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide: role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272: 217-221.
10. Ushio-Fukai, M., R. W. Alexander, M. Akers, Q. Yin, Y. Fujio, K. Walsh, and K. K. Griendling. 1999. Reactive oxygen species mediate the activation of Akt/ protein kinase B by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 274: 22699-22704.
11. Metcalfe, D. D., D. Baram, and Y. A. Mekori. 1997. Mast cells. Physiol. Rev. 77: 1033-1079.
12. Marshall, J. S. 2004. Mast-cell responses to pathogens. Nat. Immunol. 4: 787-799.
13. Galli, S. J., J. Kalesnikoff, M. A. Grimbaldeston, A. M. Piliponsky, C. M. M. Williams, and M. Tsai. 2005. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu. Rev. Immunol. 23: 749-786.
14. Bingham, C. O., and K. F. Austen. 2000. Mast-cell responses in the development of asthma. J. Allergy Clin. Immunol. 105: S527-S534.
15. Malaviya, R., T. Ikeda, E. Ross, and S. N. Abraham. 1996. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-α. Nature 381: 77-80.
16. Echtenacher, B., D. N. Mannel, and L. Hultner. 1996. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381: 75-77.
17. Malaviya, R., E. A. Ross, J. I. MacGregor, T. Ikeda, J. R. Little, B. A. Jakschik, and S. N. Abraham. 1994. Mast cell phagocytosis of FimH-expressing enterobacteria. J. Immunol. 152: 1907-1914.
18. McLachlan, J. B., J. P. Hart, S. V. Pizzo, C. P. Shelburne, H. F. Staats, M. D. Gunn, and S. N. Abraham. 2003. Mast cell-derived tumour necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat. Immunol. 4: 1199-1205.
19. Jawdat, D. M., G. Rowden, and J. S. Marshall. 2006. Mast cells have a pivotal role in TNF-independent lymph node hypertrophy and the mobilization of langerhans cells in response to bacterial peptidoglycan. J. Immunol. 177: 1755-1762.
20. Swindle, E. J., D. D. Metcalfe, and J. W. Coleman. 2004. Rodent and human mast cells produce functionally significant intracellular reactive oxygen species but not nitric oxide. J. Biol. Chem. 279: 48751-48759.
21. Swindle, E. J., J. A. Hunt, and J. W. Coleman. 2002. A comparison of reactive oxygen species generation by rat peritoneal macrophages and mast cells using the highly sensitive real-time chemiluminescent probe pholasin: inhibition of antigen-induced mast cell degranulation by macrophage-derived hydrogen peroxide. J. Immunol. 169: 5866-5873.
22. Suzuki, Y., T. Yoshimaru, T. Matsui, T. Inoue, O. Niide, S. Nunomura, and C. Ra. 2003. FcεRI signaling of mast cells activates intracellular production of hydrogen peroxide: role in the regulation of calcium signals. J. Immunol. 171: 6119-6127.
23. Kim, J. Y., and J. Y. Ro. 2005. Signal pathway of cytokines produced by reactive oxygen species generated from phorbol myristate acetate-stimulated HMC-1 cells. Scand. J. Immunol. 62: 25-35.
24. Clark R. A., and W. M. Nauseef. 2003. Isolation and functional analysis of neutrophils. In Current Protocols in Immunology. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. Wiley and Sons, Hobeken, N.J. p. 7.23.1.
25. Keston, A. S., and R. Brandt. 1965. The fluorometric analysis of ultramicro quantities of hydrogen peroxide. Anal. Biochem. 11: 1-5.
26. Ali, H., J. Ahamed, C. Hernandez-Munain, J. L. Baron, M. S. Krangel, and D. D. Patel. 2000. Chemokine production by G protein-coupled receptor activation in a human mast cell line: roles of extracellular signal-regulated kinase and NFAT. J. Immunol. 165: 7215-7223.
27. Vines, C. M., M. Xue, D. C. Maestas, D. F. Cimino, and E. R. Prossnitz. 2002. Regulation of N-formyl peptide-mediated degranulation by receptor phosphorylation. J. Immunol. 169: 6760-6766.
28. Iwaki, S., C. Tkaczyk, A. B. Satterthwaite, K. Halcomb, M. A. Beaven, D. D. Metcalfe, and A. M. Gilfillan. 2005. Btk plays a crucial role in the amplification of FcεRI-mediated mast cell activation by kit. J. Biol. Chem. 280: 40261-40270.
29. Klein, M., S. Klein-Hessling, A. Palmetshofer, E. Serfling, C. Tertilt, T. Bopp, V. Heib, M. Becker, C. Taube, H. Schild, E. Schmitt, and M. Stassen. 2006. Specific and redundant roles for NFAT transcription factors in the expression of mast cell-derived cytokines. J. Immunol. 177: 6667-6674.
30. Hernandez-Hansen, V., J. D. J. Bard, C. A. Tarleton, J. A. Wilder, C. A. Lowell, B. S. Wilson, and J. M. Oliver. 2005. Increased expression of genes linked to FcεRI signalling and to cytokine and chemokine production in Lyn-deficient mast cells. J. Immunol. 175: 7880-7888.
31. Matsui, T., Y. Suzuki, K. Yamashita, T. Yoshimaru, M. Suzuki-Karasaki, S. Hayakawa, M. Yamaki, and K. Shimizu. 2000. Diphenyleneiodonium prevents reactive oxygen species generation, tyrosine phosphorylation, and histamine release in RBL-2H3 mast cells. Biochem. Biophys. Res. Commun. 276: 742-748.
32. Yoshimaru, T., Y. Suzuki, T. Matsui, K. Yamashita, T. Ochiai, M. Yamaki, and K. Shimuzi. 2002. Blockade of superoxide generation prevents high-affinity immunoglobulin E receptor-mediated release of allergic mediators by rat mast cell line and human basophils. Clin. Exp. Allergy 32: 612-618.
33. 2+ influx. Free Radic. Biol. Med. 40: 1949-1959.
34. Schewe, C., T. Schewe, and A. Wendel. 1994. Strong inhibition of mammalian lipoxygenases by the antiinflammatory seleno-organic ebselen in the absence of glutathione. Biochem. Pharmacol. 48: 65-74.
35. Safayhi, H., G. Tiegs, and A. Wendel. 1985. A novel biologically active selenoorganic compound-V: inhibition by ebselen (PZ51) of rat peritoneal neutrophil lipoxygenase. Biochem. Pharmacol. 34: 2691-2694.
36. Weitzel, F., and A. Wendel. 1993. Selenoenzymes regulate the activity of leukocyte 5-lipoxygenase via the peroxide tone. J. Biol. Chem. 268: 6288-6292.
37. Huang, H.-S., C.-J. Chen, H. Suzuki, S. Yamamoto, and W.-C. Chang. 1999. Inhibitory effect of phospholipid hydroperoxide glutathione peroxidase on the activity of lipoxygenases and cyclooxygenases. Prostaglandins Other Lipid Mediat. 58: 65-75.
38. Imai, H., K. Narashima, M. Arai, H. Sakamoto, N. Chiba, and Y. Nakagawa. 1998. Suppression of leukotriene formation in RBL-2H3 cells that overexpressed phospholipid hydroperoxide glutathione peroxidase. J. Biol. Chem. 273: 1990-1997.
39. 2 synthesis. J. Biol. Chem. 275: 40028-40035.
40. Nakano, N., A. Nakao, T. Uchida, N. Shirasaka, H. Yoshizumi, K. Okumura, R. Tsuboi, and H. Ogawa. 2005. Effects of arachidonic acid analogs on FcεRI-mediated activation of mast cells. Biochim. Biophys. Acta 1738: 19-28.
41. Murphy, R. C., S. Hammarström, and B. Samuelsson. 1979. Leukotriene C: a slow-reacting substance from mouse mastocytoma cells. Proc. Natl. Acad. Sci. USA 76: 4275-4279.
42. Corey, E. J., and P. T. Lansbury, Jr. 1983. Stereochemical course of 5-lipoxygenation of arachidonate by rat basophil leukemic cell (RBL-1) and potato enzymes. J. Am. Chem. Soc. 105: 4093-4094.
43. Werz, O. 2002. 5-Lipoxygenase: cellular biology and molecular pharmacology. Curr. Drug Targets Inflamm. Allergy 1: 23-44.
44. Chamulitrat, W., M. F. Hughes, T. E. Eling, and R. P. Mason. 1991. Lipid peroxyl radical intermediates in the peroxidation of polyunsaturated fatty acids by lipoxygenase. Arch. Biochem. Biophys. 290: 153-159.
45. Kukreja, R. C., H. A. Kontos, M. L. Hess, and E. F. Ellis. 1986. PGH synthase and lipoxygenase generate superoxide in the presence of NADH or NADPH. Circ. Res. 59: 612-619.
46. Roy, P., S. K. Roy, A. Mitra, and A. P. Kulkarni. 1994. Superoxide generation by lipoxygenase in the presence of NADH and NADPH. Biochim. Biophys. Acta 1214: 171-179.
47. Ivanov, I., J. Samm, H. Kuhn, and H.-G. Holzhütter. 2005. Dual role of oxygen during lipoxygenase reactions. FEBS J. 272: 2523-2535.
48. Mason, R. P., B. Kalyanaraman, B. E. Tainer, and T. E. Eling. 1980. A carboncentered free radical intermediate in the prostaglandin synthetase oxidation of arachidonic acid. J. Biol. Chem. 255: 5019-5022.
49. Schreiber, J., G. L. Foureman, M. F. Hugher, R. P. Mason, and T. E. Eling. 1989. Detection of glutathione thiyl free radical catalyzed by prostaglandin H synthase present in keratinocytes. J. Biol. Chem. 264: 7936-7943.
50. Cathcart, R., E. Schwiers, and B. N. Ames. 1983. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134: 111-116.
51. Chance, B., H. Sies, and A. Boveris. 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59: 527-605.
52. Larsen, L. N., and E. D. J. Bremer. 1996. Peroxidative oxidation of leuco-dichlorofluorescein by prostaglandin H synthase in prostaglandin biosynthesis from polyunstaturated fatty acids. Biochim. Biophys. Acta 1299: 47-53.
53. Igarashi, Y., J. D. Lundgren, J. H. Shelhamer, M. A. Kaliner, and M. V. White. 1993. Effects of inhibitors of arachidonic acid metabolism on serotonin release from rat basophilic leukemia cells. Immunopharmacol. 25: 131-144.
54. Son, A., H. Nakamura, N. Kondo, Y. Matsuo, W. Liu, S. Oka, Y. Ishii, and J. Yodoi. 2006. Redox regulation of mast cell histamine release in thioredoxin-1 (TRX) transgenic mice. Cell Research 16: 230-239.
55. 2-linked cascade. J. Biol. Chem. 275: 32357-32362.
56. Catalano, A., S. Rodilossi, P. Caprari, V. Coppola, and A. Procopio. 2005. 5-Lipoxygenase regulates senescence-like growth arrest by promoting ROS-dependent p53 activation. EMBO J. 24: 170-179.
57. Sekharam, M., J. M. Cunnick, and J. Wu. 2000. Involvement of lipoxygenase in lysophosphatidic acid-stimulated hydrogen peroxide release in human HaCaT keratinocytes. Biochem. J. 346: 751-758.
58. Chen, X.-S., T. A. Naumann, U. Kurre, N. A. Jenkins, N. G. Copeland, and C. D. Funk. 1995. cDNA cloning, expression, mutagenesis, intracellular localization, and gene chromosomal assignment of mouse 5-lipoxygenase. J. Biol. Chem. 270: 17993-17999.
59. Brown, J. M., E. J. Swindle, N. M. Kushnir-Sukhov, A. Holian, and D. D. Metcalfe. 2006. Silica-directed mast cell activation is enhanced by scavenger receptors. Am. J. Respir. Cell. Mol. Biol. 36: 43-52.
60. Okayama, Y., D. D. Hagaman, and D. D. Metcalfe. 2001. A comparison of mediators released or generated by IFN-γ-treated human mast cells following aggregation of FcγRI or FcεRI. J. Immunol. 166: 4705-4712.
61. Woolhiser, M. R., Y. Okayama, A. M. Gilfillan, and D. D. Metcalfe. 2001. IgG-dependent activation of human mast cells following up-regulation of FcγRI by IFN-γ. Eur. J. Immunol. 31: 3298-3307.
62. 2 in zymosan-induced eicosanoid generation and vascular permeability revealed by targeted gene disruption. J. Biol. Chem. 279: 16488-16494.
63. 2 translocates to the phagosome after zymosan stimulation of mouse peritoneal macrophages and regulates phagocytosis. J. Biol. Chem. 281: 6691-6698.
64. Meslier, N., A. J. Aldrich, and T. D. Bigby. 1992. Effect of interferon-γ on the 5-lipoxygenase pathway of rat lung macrophages. Am. J. Respir. Cell Mol. Biol. 6: 93-99.
65. Nassar, G. M., A. Montero, M. Fukunaga, and K. F. Badr. 1997. Contrasting effects of proinflammatory and T-helper lymphocyte subset-2 cytokines on the 5-lipoxygenase pathway in monocytes. Kidney Int. 51: 1520-1528.
66. 2 in intact human neutrophils but not in the cell-free system. Biochem. Biophys. Res. Commun. 138: 1099-1105.
67. 2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 273: 441-445.
68. phox phosphorylation and membrane translocation in polyunsaturated fatty acid-stimulated neutrophils. J. Leukocyte Biol. 78: 976-984.
69. Ozaki, Y., T. Ohashi, and Y. Niwa. 1986. A comparative study on the effects of inhibitors of the lipoxygenase pathway on neutrophil function: inhibitory effects on neutrophil function may not be attributed to inhibition of the lipoxygenase pathway. Biochem. Pharmacol. 35: 3481-3488.
70. 2α does not regulate neutrophil NADPH oxidase activity. J. Biol. Chem. 280: 7519-7529.