Inhibition of phospholipase A2 abrogates intracellular processing of NADPH-oxidase derived reactive oxygen species in human neutrophils

Experimental Cell Research

Volumn 319, Issue 5, 2013, Pages 761-774

  Björnsdottir, Halla ^a   Granfeldt, Daniel ^a   Welin, Amanda ^a   Bylund, Johan ^a   Karlsson, Anna ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Granules; Membrane fusion; Phagocytes; Phospholipases; Respiratory burst

Indexed keywords

GALECTIN 3; HYDROGEN PEROXIDE; IONOMYCIN; LUMINOL; MYELOPEROXIDASE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE A2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ARTICLE; CELL MEMBRANE; CELL METABOLISM; CHEMOLUMINESCENCE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NEUTROPHIL; OXIDATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 84873989700     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.12.020     Document Type: Article

References (76)

1. Babior B.M. NADPH oxidase: an update. Blood 1999, 93:1464-1476.
2. Klebanoff S.J. Myeloperoxidase. Proc. Assoc. Am. Physicians 1999, 111:383-389.
3. DeLeo F.R., Quinn M.T. Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J. Leukocyte Biol. 1996, 60:677-691.
4. Dahlgren C., Johansson A., Lundqvist H., Bjerrum O.W., Borregaard N. Activation of the oxygen-radical-generating system in granules of intact human neutrophils by a calcium ionophore (ionomycin). Biochem. Biophys. Acta 1992, 1137:182-188.
5. Lundqvist H., Follin P., Khalfan L., Dahlgren C. Phorbol myristate acetate induced NADPH-oxidase activity in human neutrophils: only half the story has been told. J. Leukocyte Biol. 1996, 59:270-279.
6. Matute J.D., Arias A.A., Wright N.A., Wrobel I., Waterhouse C.C., Li X.J., Marchal C.C., Stull N.D., Lewis D.B., Steele M., Kellner J.D., Yu W., Meroueh S.O., Nauseef W.M., Dinauer M.C. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood 2009, 114:3309-3315.
7. Borregaard N., Heiple J.M., Simons E.R., Clark R.A. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J. Cell Biol. 1983, 97:52-61.
8. Bylund J., Brown K.L., Movitz C., Dahlgren C., Karlsson A. Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for?. Free Radical. Biol. Med. 2010, 49:1834-1845.
9. Dahlgren C. Difference in extracellular radical release after chemotactic factor and calcium ionophore activation of the oxygen radical-generating system in human neutrophils. Biochim. Biophys. Acta 1987, 930:33-38.
10. Watson F., Robinson J., Edwards S.W. Protein kinase C-dependent and -independent activation of the NADPH oxidase of human neutrophils. J. Biol. Chem. 1991, 266:7432-7439.
11. Karlsson A., Follin P., Leffler H., Dahlgren C. Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils. Blood 1998, 91:3430-3438.
12. Serrander L., Larsson J., Lundqvist H., Lindmark M., Fallman M., Dahlgren C., Stendahl O. Particles binding beta(2)-integrins mediate intracellular production of oxidative metabolites in human neutrophils independently of phagocytosis. Biochim. Biophys. Acta 1999, 1452:133-144.
13. Karlsson A. Wheat germ agglutinin induces NADPH-oxidase activity in human neutrophils by interaction with mobilizable receptors. Infect. Immun. 1999, 67:3461-3468.
14. Karlsson A., Nixon J.B., McPhail L.C. Phorbol myristate acetate induces neutrophil NADPH-oxidase activity by two separate signal transduction pathways: dependent or independent of phosphatidylinositol 3-kinase. J. Leukocyte Biol. 2000, 67:396-404.
15. 2+ influx and activation of the neutrophil respiratory burst. Different regulation of plasma membrane- and granule-localized NADPH-oxidase. J. Leukocyte Biol. 2002, 71:611-617.
16. Karlsson A., Dahlgren C. Assembly and activation of the neutrophil NADPH oxidase in granule membranes. Antioxid Redox Signal 2002, 4:49-60.
17. Ferguson P.J., Lokuta M.A., El-Shanti H.I., Muhle L., Bing X., Huttenlocher A. Neutrophil dysfunction in a family with a SAPHO syndrome-like phenotype. Arthritis Rheum. 2008, 58:3264-3269.
18. 2 for activation of the assembled NADPH oxidase in human neutrophils. Biochem. J. 1994, 297:217-223. Pt 1.
19. 2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 1998, 273:441-445.
20. 2 regulate the release of arachidonic acid for eicosanoid production and superoxide anion generation in neutrophils. J. Immunol. 1998, 160:953-960.
21. 2 affects translocation but not phosphorylation of p67(phox) and p47(phox). J. Biol. Chem. 2002, 277:25385-25392.
22. 2-alfa in regulation of phagocytic functions. Biochim. Biophys. Acta 2006, 1761:1323-1334.
23. 2-alpha does not regulate neutrophil NADPH oxidase activity. J. Biol. Chem. 2005, 280:7519-7529.
24. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Scand. J. Lab. Invest. 1968, 21:77-89.
25. Dahlgren C., Karlsson A. Respiratory burst in human neutrophils. J. Immunol. Methods 1999, 232:3-14.
26. Lundqvist H., Dahlgren C. Isoluminol-enhanced chemiluminescence: a sensitive method to study the release of superoxide anion from human neutrophils. Free Radical. Biol. Med. 1996, 20:785-792.
27. Hyslop P.A., Sklar L.A. A quantitative fluorimetric assay for the determination of oxidant production by polymorphonuclear leukocytes: its use in the simultaneous fluorimetric assay of cellular activation processes. Anal. Biochem. 1984, 141:280-286.
28. Root R.K., Metcalf J., Oshino N., Chance B. H2O2 release from human granulocytes during phagocytosis. I. Documentation, quantitation, and some regulating factors. J. Clin. Invest. 1975, 55:945-955.
29. 2: studies with normal and cytochalasin B-treated cells. J. Clin. Invest. 1977, 60:1266-1279.
30. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981, 391:85-100.
31. 2+ in Living Cells 1994, vol. 40. Academic Press, San Diego.
32. Laudanna C., Rossi F., Berton G. Effect of inhibitors of distinct signalling pathways on neutrophil Q2- generation in response to tumor necrosis factor-alpha, and antibodies against CD18 and CD11a: evidence for a common and unique pattern of sensitivity to wortmannin and protein tyrosine kinase inhibitors. Biochem. Biophys. Res. Commun. 1993, 190:935-940.
33. Vlahos C.J., Matter W.F., Brown R.F., Traynor-Kaplan A.E., Heyworth P.G., Prossnitz E.R., Ye R.D., Marder P., Schelm J.A., Rothfuss K.J. Investigation of neutrophil signal transduction using a specific inhibitor of phosphatidylinositol 3-kinase. J. Immunol. 1995, 154:2413-2422.
34. Rosenthal M.D., Franson R.C. Separation of agonist-stimulated arachidonate mobilization from subsequent leukotriene B4 synthesis in human neutrophils: different effects of oleoylacetylglycerol and phorbol myristate acetate as priming agents. J. Cell. Physiol. 1994, 160:522-530.
35. Stevens P., Winston D.J., Van Dyke K. In vitro evaluation of opsonic and cellular granulocyte function by luminol-dependent chemiluminescence: utility in patients with severe neutropenia and cellular deficiency states. Infect. Immun. 1978, 22:41-51.
36. Dahlgren C., Stendahl O. Role of myeloperoxidase in luminol-dependent chemiluminescence of polymorphonuclear leukocytes. Infect. Immun. 1983, 39:736-741.
37. Dahlgren C., Karlsson A., Bylund J. Measurement of respiratory burst products generated by professional phagocytes. Methods Mol. Biol. 2007, 412:349-363.
38. Faurschou M., Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microb. Infect. 2003, 5:1317-1327.
39. Fernandez J.M., Neher E., Gomperts B.D. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 1984, 312:453-455.
40. 2. Agents Actions 39 Spec No 1993, C39-42.
41. 2. J. Am. Chem. Soc. 1996, 118:5519-5525.
42. Seno K., Okuno T., Nishi K., Murakami Y., Watanabe F., Matsuura T., Wada M., Fujii Y., Yamada M., Ogawa T., Okada T., Hashizume H., Kii M., Hara S., Hagishita S., Nakamoto S., Yamada K., Chikazawa Y., Ueno M., Teshirogi I., Ono T., Ohtani M. Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J. Med. Chem. 2000, 43:1041-1044.
43. Ghomashchi F., Stewart A., Hefner Y., Ramanadham S., Turk J., Leslie C.C., Gelb M.H. A pyrrolidine-based specific inhibitor of cytosolic phospholipase A(2)alpha blocks arachidonic acid release in a variety of mammalian cells. Biochim. Biophys. Acta 2001, 1513:160-166.
44. Bylund J., Samuelsson M., Collins L.V., Karlsson A. NADPH-oxidase activation in murine neutrophils via formyl peptide receptors. Exp. Cell. Res. 2003, 282:70-77.
45. Nauseef W.M., Metcalf J.A., Root R.K. Role of myeloperoxidase in the respiratory burst of human neutrophils. Blood 1983, 61:483-492.
46. Borregaard N., Cowland J.B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 1997, 89:3503-3521.
47. Kobayashi T., Robinson J.M., Seguchi H. Identification of intracellular sites of superoxide production in stimulated neutrophils. J. Cell Sci. 1998, 111:81-91. Pt 1.
48. Martin-Martin B., Nabokina S.M., Blasi J., Lazo P.A., Mollinedo F. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 2000, 96:2574-2583.
49. Lollike K., Lindau M., Calafat J., Borregaard N. Compound exocytosis of granules in human neutrophils. J. Leukocyte Biol. 2002, 71:973-980.
50. Mollinedo F., Martin-Martin B., Calafat J., Nabokina S.M., Lazo P.A. Role of vesicle-associated membrane protein-2, through Q-soluble N-ethylmaleimide-sensitive factor attachment protein receptor/R-soluble N-ethylmaleimide-sensitive factor attachment protein receptor interaction, in the exocytosis of specific and tertiary granules of human neutrophils. J. Immunol. 2003, 170:1034-1042.
51. 2 in mammalian sperm-egg fusion: development of hamster oolemma fusibility by lysophophatidylcholine. J. Exp. Zool. 1997, 279:81-88.
52. 2-treated presynaptic membranes in vitro. Biochem. J. 1996, 318:981-987.
53. 2 in endocytosis. Proc. Nat. Acad. Sci. U.S.A. 1993, 90:10225-10229.
54. Mayorga L.S., Beron W., Sarrouf M.N., Colombo M.I., Creutz C., Stahl P.D. Calcium-dependent fusion among endosomes. J. Biol. Chem. 1994, 269:30927-30934.
55. 2 promotes fusion between PMN-specific granules and complex liposomes. J. Leukocyte Biol. 1996, 59:663-670.
56. McLaren D.J., Mackenzie C.D., Ramalho-Pinto F.J. Ultrastructural observations on the in vitro interaction between rat eosinophils and some parasitic helminths (Schistosoma mansoni, Trichinella spiralis and Nippostrongylus brasiliensis). Clin. Exp. Immunol. 1977, 30:105-118.
57. Scepek S., Lindau M. Focal exocytosis by eosinophils-compound exocytosis and cumulative fusion. EMBO J. 1993, 12:1811-1817.
58. 2+ and GTP analogs. J. Biol. Chem. 2003, 278:44929-44934.
59. Guo Z., Turner C., Castle D. Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells. Cell 1998, 94:537-548.
60. Orci L., Malaisse W. Hypothesis: single and chain release of insulin secretory granules is related to anionic transport at exocytotic sites. Diabetes 1980, 29:943-944.
61. Bokvist K., Holmqvist M., Gromada J., Rorsman P. Compound exocytosis in voltage-clamped mouse pancreatic beta-cells revealed by carbon fibre amperometry. Pflugers Arch. 2000, 439:634-645.
62. Cochilla A.J., Angleson J.K., Betz W.J. Differential regulation of granule-to-granule and granule-to-plasma membrane fusion during secretion from rat pituitary lactotrophs. J. Cell Biol. 2000, 150:839-848.
63. Sorensen O.E., Follin P., Johnsen A.H., Calafat J., Tjabringa G.S., Hiemstra P.S., Borregaard N. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 2001, 97:3951-3959.
64. Peppin G.J., Weiss S.J. Activation of the endogenous metalloproteinase, gelatinase, by triggered human neutrophils. Proc. Nat. Acad. Sci. U.S.A. 1986, 83:4322-4326.
65. Mihalache C.C., Yousefi S., Conus S., Villiger P.M., Schneider E.M., Simon H.U. Inflammation-associated autophagy-related programmed necrotic death of human neutrophils characterized by organelle fusion events. J. Immunol. 2011, 186:6532-6542.
66. 2 in vitro and prostaglandin E2 production in vivo of the macrophage-like P388D1 cell. Effects of manoalide, 7,7-dimethyl-5,8-eicosadienoic acid, and p-bromophenacyl bromide. J. Biol. Chem. 1989, 264:8520-8528.
67. Cohen N., Weber G., Banner B.L., Welton A.F., Hope W.C., Crowley H., Anderson W.A., Simko B.A., O'Donnell M., Coffey J.W., et al. Analogs of arachidonic acid methylated at C-7 and C-10 as inhibitors of leukotriene biosynthesis. Prostaglandins 1984, 27:553-562.
68. 2 (AdPLA). J. Biol. Chem. 2008, 283:25428-25436.
69. 2 by bromoenol lactone and trifluoromethyl ketones. J. Biol. Chem. 1995, 270:445-450.
70. 2+ responses in Madin Darby canine kidney cells. Arch. Toxicol. 2000, 74:447-451.
71. 2 enzymes present in P388D1 macrophages. J. Biol. Chem. 1996, 271:6758-6765.
72. 2, on human neutrophil function. Biochem. Pharmacol. 1994, 47:1661-1667.
73. 2. Biochim. Biophys. Acta 1998, 1394:57-64.
74. 2 in arachidonic acid release from human neutrophils. J. Immunol. 2000, 164:2084-2091.
75. 2 by methyl arachidonyl fluorophosphonate. Biochim. Biophys. Acta 1996, 1302:55-60.
76. Huang Z., Liu S., Street I., Laliberte F., Abdullah K., Desmarais S., Wang Z., Kennedy B., Payette P., Riendeau D., Weech P., Gresser M. Methyl arachidonyl fluorophosphonate, a potent irreversible cPLA inhibitor, blocks the mobilization of arachidonic acid in human platelets and neutrophils, IAIS symposium on novel molecular approaches to anti-inflammatory therapy. Mediators Inflamm, Toronto, Canada 1994, 3:303-311.