Inhibition of neutrophil oxidative burst and granule secretion by wortmannin: Potential role of MAP kinase and renaturable kinases

Journal of Cellular Physiology

Volumn 172, Issue 1, 1997, Pages 94-108

  Sue A Quan, Andrea K ^a   Fialkow, Lea ^a   Vlahos, Chris J ^b   Schelm, Judi A ^b   Grinstein, Sergio ^c   Butler, Jeff ^a,c   Downey, Gregory P ^a,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b ELI LILLY AND COMPANY   (United States)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FORMYLMETHIONYLLEUCYLPHENYLALANINE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOTRANSFERASE; WORTMANNIN;

ARTICLE; BACTERICIDAL ACTIVITY; CELL ACTIVATION; DEGRANULATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NEUTROPHIL; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY BURST; SECRETORY GRANULE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANTIGENS, CD; ANTIGENS, NEOPLASM; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL ADHESION MOLECULES; CELL DEGRANULATION; CELLS, CULTURED; CHROMONES; ENZYME INHIBITORS; HUMANS; MAP KINASE KINASE 1; MEMBRANE GLYCOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MORPHOLINES; MURAMIDASE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PEROXIDASE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOSPHOTYROSINE; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RESPIRATORY BURST; SUPEROXIDES; TETRADECANOYLPHORBOL ACETATE;

BACTERIA (MICROORGANISMS);

EID: 0030831333     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199707)172:1<94::AID-JCP11>3.0.CO;2-O     Document Type: Article

References (68)

1. Ahn, N.G., Seger, R., and Krebs, E.G. (1992) The mitogen activated protein kinase activator. Curr. Opin. Cell Biol., 4:992-999.
2. Arcaro, A., and Wymann, M.P. (1993) Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: The role of phosphatidylinositol 3, 4, 5-trisphosphate in neutrophil responses. Biochem. J., 296:297-301.
3. Baggiolini, M., Dewald, B., Schnyder, J., Ruch, W., Cooper, P.H., and Payne, T.G. (1987) Inhibition of the phagocytosis-induced respiratory burst by the fungal metabolite wortmannin and some analogues. Exp. Cell Res., 169:408-418.
4. Berkow, R.L., and Dodson, R.W. (1990) Tyrosine-specific protein phosphorylation during activation of human neutrophils. Blood, 75:2445-2452.
5. Blenis, J. (1993) Signal transduction via the MAP kinases: Proceed at your own RSK. Proc. Nat. Acad. Sci., 90:5889-5892.
6. Borregaard, N., Kjeldsen, L.K., Sengelov, L., Bastholm, H., Nielsen, L., Bainton, M.H., and Bainton, D.F. (1993) Human neutrophil granules and secretory vesicles. Eur. J. Haematol., 51:187-198.
7. Buhl, A.M., AvdI, N., Worthen, G.S., and Johnson, G.L. (1994) Mapping of the C5a receptor signal transduction network in human neutrophils. Proc. Natl. Acad. Sci. USA, 91:9190-9194.
8. Clark-Lewis, I., Sanghera, J.S., and Pelech, S.L. (1991) Definition of a consensus sequence for peptide substrate recognition by p44mpk, the meiosis-activated myelin basic protein kinase. J. Biol. Chem., 266:15180-15184.
9. Crews, C.M., and Erikson, R.L. (1993) Extracellular signals and reversible protein phosphorylation: What to Mek of it all. Cell, 74:335-342.
10. Cross, D.A.E., Alessi, D.R., Vandenheede, J.R., McDowell, H.E., Hundal, H.S., and Cohen, P. (1994) The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: Evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem. J., 303:21-26.
11. Christopoulos, T., and Diamandis, E.P. (1992) Enzymatically amplified time-resolved fluorescence immunoassay with terbium chelates. Anal. Chem., 64:342-346.
12. Dewald, B., Thelen, M., and Baggiolini, M. (1988) Two transduction sequences are necessary for neutrophil activation by receptor agonists. J. Biol. Chem., 263:16179-16184.
13. Ding, J., and Badwey, J.A. (1993a) Neutrophils stimulated with a chemotactic peptide or a phorbol ester exhibit different alterations in the activities of a battery of protein kinases. J. Biol. Chem., 268:5234-5240.
14. Ding, J., and Badwey, J.A. (1993b) Stimulation of neutrophils with a chemoattractant activates several novel protein kinases that can catalyze the phosphorylation of peptides derived from the 47-kDa protein component of the phagocyte oxidase and myristoylated alanine-rich C kinase substrate. J. Biol. Chem., 268:17326-17333.
15. Ding, J., and Badwey, J.A. (1994) Wortmannin and 1-butanol block activation of a novel family of protein kinases in neutrophils. FEBS Lett., 348:149-152.
16. Downey, G.P., Fukushima, T., and Fialkow, L. (1995) Signaling mechanisms in human neutrophils. Curr. Opin. Hematol., 2:76-88.
17. Downey, G.P., and O'Brodovich, H. (1997) In: Textbook of Pediatric Respiratory Medicine. L.M. Taussig, ed., Mosby, Inc., St. Louis. In Press.
18. 2 translocates to membrane fraction in human neutrophils activated by stimuli that phosphorylate mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA, 91:3142-3146.
19. Eberle, M., Traynor-Kaplan, A.E., Sklar, L.A., and Norgauer, J. (1990) Is there a relationship between phosphatidylinositol triphosphate and f-actin polymerization in human neutrophils. J. Biol. Chem., 265:16725-16728.
20. phox during neutrophil activation. J. Biol. Chem., 269:23431-23436.
21. Ely, C.M., Oddie, K.M., Litz, J.S., Rossomando, A.J., Kanner, S.B., Sturgill, T.W., and Parsons, S.J. (1990) A 42-kD tyrosine kinase substrate linked to chromaffin cell secretion exhibits an associated MAP kinase activity and is highly related to a 42-kD mitogen-stimulated protein in fibroblasts. J. Cell Biol., 110:731-739.
22. Ferby, I.M., Waga, I., Sakanaka, C., Kume, K., and Shimizu, T. (1994) Wortmannin inhibits mitogen-activated protein kinase activation induced by platelet-activating factor in guinea pig neutrophils. J. Biol. Chem., 269:30485-30488.
23. Fialkow, L., Chan, C.K., Rotin, D., Grinstein, S., and Downey, G.P. (1994) Activation of the mitogen-activated protein kinase signaling pathway in neutrophils. J. Biol. Chem., 49:31234-31242.
24. Gaudry, M., Caon, A.C., Gilbert, C., Lille, S., and Naccache, P.H. (1992) Evidence for the involvement of tyrosine kinases in the locomotory responses of human neutrophils. J. Leuk. Biol., 51:103-108.
25. Gomez-Cambronero, J., Colasanto, J.M., Huang, C.K., and Sha'afi, R.I. (1993) Direct stimulation by tyrosine phosphorylation of microtubule-associated protein (MAP) kinase activity by granulocyte-macrophage colony-stimulating factor in human neutrophils. Biochem. J., 291:211-217.
26. Gonzalez, F., Raden, D., and Davis, R. (1991) Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases. J. Biol. Chem., 266:22159-22163.
27. Grinstein, S., and Furuya, W. (1991) Tyrosine phosphorylation and oxygen consumption induced by G proteins in neutrophils. Am. J. Physiol., 260:C1019-1027.
28. Grinstein, S., and Furuya, W. (1992) Chemoattractant-induced tyrosine phosphorylation and activation of microtubule-associated protein kinase in human neutrophils. J. Biol. Chem., 264:18122-18125.
29. Grinstein, S., Furuya, W., Butler, J.R., and Tseng, J. (1993) Receptor-mediated activation of multiple serine/threonine kinases in human leukocytes. J. Biol. Chem., 265:17326-17333.
30. Haslett, C., Guthris, L.A., Kopaniak, M.M., and Johnston, R.B., Jr. (1985) Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am. J. Pathol., 119:101-110.
31. Kameshita, I., and Fujisawa, H. (1989) A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel. Anal. Biochem., 183:139-143.
32. Kelly, K.L., and Ruderman, N.B. (1993) Insulin-stimulated phosphatidylinositol 3-Kinase: Association with a 185-kDa tyrosine-phosphorylated protein (IRS-1) and localization in a low density membrane vesicle. J. Biol. Chem., 268:4391-4398.
33. Kujipers, T.W., Tool, A.T.J., Schoot, C.E.v.d., Ginsel, L.A., Onderwater, J.J.M., Roos, D., and Verhoeven, A.J. (1991) Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood, 78:1105-1111.
34. Lange-Carter, C.A., Pleiman, C.M., Gardner, A.M., Blumer, K.J., and Johnson, G.L. (1993) A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf. Science, 260:315-319.
35. Laudanna, C., Rossi, F., and Berton, G. (1993) Effect of inhibitors of distince signalling pathways on neutrophil O2-generation in response to tumor necrosis factor-α and antibodies against CD18 and CD11a: Evidence for a common and unique pattern of sensitivity to wortmannin and protein kinase inhibitors. Biochem. Biophys. Res. Commun., 190:935-940.
36. Martin, G.A., Bollag, G., McCormick, F., and Abo, A. (1995) A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J., 14:1970-1978.
37. Morel, F., Doussiere, J., and Vignais, P.V. (1991) The superoxide generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects. Eur. J. Biochem., 201:523-546.
38. Naccache, P.H., Caon, A.C., Gilbert, C., Gaudry, M., Roberge, C.J., Poubelle, P.E., and Bourgoin, S. (1993) Inhibition of tyrosine phosphorylation by wortmannin in human neutrophils; dissociation from its inhibitory effects on phospholipase D. Lab. Invest., 69:19-23.
39. Nakanishi, H., Brewer, K.A., and Exton, J.H. (1993) Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3, 4, 5-trisphosphate. J. Biol. Chem., 268:13-16.
40. Niessen, H.W.M., and Verhoeven, A.J. (1992) Differential up-regulation of specific and azurophilic granule membrane markers in electropermeabilized neutrophils. Cell Signal., 5:501-509.
41. O'Brien, P.J. (1984) Superoxide production. Methods Enzymol., 105:370-378.
42. Offermanns, S., Jones, S.V.P., Bombien, E., and Schultz, G. (1994) Stimulation of mitogen-activated protein kinase activity by different secretory stimuli in rat basophilic leukemia cells. The J. Immunol., 152:250-261.
43. Okada, T., Sakuma, L., Fukui, Y., Hazeki, O., and Ui, M. (1994) Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphtidylinositol 3-kinase. J. Biol. Chem., 269:3563-3567.
44. Pawson, T. (1995) Protein modules and signaling networks. Nature, 373:573-579.
45. Pleiman, C.M., Hertz, W.M., and Cambier, J.C. (1994) Activation of phosphatidylinositol-3′ kinase by src-family kinase SH3 binding to the p85 subunit. Science, 263:1609-1612.
46. Ptasznik, A., Traynor-Kaplan, A., and Bokoch, G.M. (1995) G protein-coupled chemoattractant receptors regulate Lyn tyrosine kinase. Shc adapter protein signaling complexes. J. Biol. Chem., 270:19969-19973.
47. Reif, K., Gout, I., Waterfield, M.D., and Cantrell, D.A. (1993) Divergent regulation of phosphatidylinositol 3-kinase p85α and p85β. J. Biol. Chem., 268:10780-10788.
48. Rodriguez-Viciana, P., Warne, P.H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M.J., Waterfield, M.D., and Downward, J. (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature, 370:527-532.
49. Ruderman, J.V. (1993) MAP kinase and the activation of quiescent cells. Curr. Opin. Cell. Biol., 5:207-213.
50. Scha'afi, R., and Molski, T. (1988) Activation of the neutrophil. Prog. Allergy, 42:1-64.
51. Smith, R.M., and Curnette, J.T. (1991) Molecular basis of chronic granulomatous disease. Blood, 77:673-686.
52. Stack, J.H., Herman, P.K., Schu, P.V., and Emr, S.D. (1993) A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J., 12:2195-2204.
53. Stephens, L., Smrcka, A., and Cook, F. (1994) A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by g protein By subunits. Cell, 77:83-93.
54. Stoyanov, B.S., Volinia, T., Hanck, I., Rubio, M., Loubtchenkov, M., Malek, D., Stoyanova, S., Vanhaesebroeck, B., Dhand, R., and Nurnberg, B. (1995) Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science, 269:690-695.
55. Thelen, M., Wymann, M.P., and Langen, H. (1994) Wortmannin binds specifically to 1-phosphatidylinositiol 3-kinase while inhibiting guanine nucleotide-binding protein-coupled receptor signaling in neutrophil leukocytes. Proc. Natl. Acad. Sci., 91:4960-4964.
56. Thompson, H.L., Marshall, C.J., and Saklatvala, J. (1994) Characterization of two different forms of mitogen-activated protein kinase kinase induced in polymorphonuclear leukocytes following stimulation by N-formylmethionyl-leucyl-phenylalanine or granulocyte-macrophage colony-stimulating factor. J. Biol. Chem., 269:9486-9492.
57. Torres, M., Hall, F.L., and O'Neill, K. (1992) Stimulation of human neutrophils with formyl-methionyl-leucyl-phenylalanine induces tyrosine phosphorylation and activation of two distinct mitogen-activated protein-kinases. J. Immunol., 150:1563-1577.
58. Traynor-Kaplan, A., Thompson, B.L., Harris, A.L., Taylor, P., Oman, G.M., and Sklar, L.A. (1989) Transient Increse in phosphatidylinositol 3, 4-bisphosphate and phosphatidylinositol trisphosphate during activation of human neutrophils. J. Biol. Chem., 264:15668-15673.
59. Vlahos, C.J. (1992) Signal transduction in neutrophil activation. Phosphatidylinositol 3-kinase is stimulated without tyrosine phosphorylation. FEBS Lett., 309:242-248.
60. Vlahos C.J., Matter, W.F., Kwan, Y.H., and Brown, R.F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-Morpholinyl)-8-phenyl-benzopyran-4-one (LY294002). J. Biol. Chem., 269:5241-5248.
61. 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., Serlin, B.S., and Simpson, P.J. (1995) Investigation of neutrophil signal transduction using a specific inhibitor of phosphatidylinositol 3-kinase. J. Immunol., 154:2413-2422.
62. Weiss, S.J. (1989) Tissue destruction by neutrophils. New Eng. J. Med., 320:365-376.
63. Welsh, G.I., Foulstone, E.J., Young, S.W., Tavare, J.M., and Proud, C.G. (1994) Wortmannin inhibits the effects of insulin and serum on the activities of glycogen synthase kinase-3 and mitogen-activated protein kinase. Biochem. J., 303:15-20.
64. Wolff, S., Dale, D., Clark, R., Root, R., and Kimball, H. (1972) The Chédiak-Higashi syndrome: Studies in host defenses. Ann. Int. Med., 76:293-306.
65. Worthen, G.S., Avdi, N., Buhl, A.M., Suzuki, N., and Johnson, G.L. (1994) FMLP activates Ras and Raf in human neutrophils. Potential role in activation of MAP kinase. J. Clin. Invest., 94:815-823.
66. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y., and Matsuda, Y. (1993) Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem., 268:25846-25856.
67. Yu, H., Suchard, S.J., Nairn, R., and Jove, R. (1995) Dissociation of mitogen-activated protein kinase activation from the oxidative burst in differentiated HL-60 cells and human neutrophils. J. Biol. Chem., 270:15719-15724.
68. Zhang, J., Zhang, J., Benovic, J.L., Sugai, M., Wetzker, R., Gout, I., and Ritterhouse, S.E. (1995) Sequestration of a G-protein βγ subunit or ADP-ribosylation of rho can inhibit thrombin-induced activation of platelet phosphoinosit 3-kinases. J. Biol. Chem., 270:6589-6594.