Crystal-induced neutrophil activation. IX. Syk-dependent activation of class Ia phosphatidylinositol 3-kinase

Journal of Leukocyte Biology

Volumn 82, Issue 3, 2007, Pages 763-773

  Popa Nita, Oana ^a   Rollet Labelle, Emmanuelle ^a   Thibault, Nathalie ^a   Gilbert, Caroline ^a   Bourgoin, Sylvain G ^a   Naccache, Paul H ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b Université Laval   (Canada)

Author keywords

Degranulation; Gout; Inflammation; Phospholipase D; PI(3 4 5)P3; Tyrosine phosphorylation

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE D; PICEATANNOL; PROTEIN KINASE SYK; PROTEIN P85; PROTEIN TYROSINE KINASE; TRITON X 114; URATE;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DENSITOMETRY; DRUG EFFECT; GOUT; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKOCYTE ACTIVATION; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TISSUE INJURY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADULT; BLOTTING, WESTERN; CELLS, CULTURED; CRYSTALLIZATION; GOUT; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHOSPHOLIPASE D; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; URIC ACID;

EID: 34548436583     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0307174     Document Type: Article

References (51)

1. Molloy, E. S., McCarthy, G. M. (2004) How crystals damage tissue. Curr. Rheumatol. Rep. 6, 228-234.
2. Agudelo, C. A., Schumacher, H. R. (1973) The synovitis of acute gouty arthritis. A light and electron microscopic study. Hum. Pathol. 4, 265-279.
3. Seegmiller, J. E., Howell, R. R. (1962) The old and new concepts of acute gouty arthritis. Arthritis Rheum. 5, 616-623.
4. Phelps, P. (1969) Polymorphonuclear leukocyte motility in vitro. II. Stimulatory effect of monosodium urate crystals and urate in solution; partial inhibition by colchicine and indomethacin. Arthritis Rheum. 12, 189-196.
5. Matsukawa, A., Yoshimura, T., Maeda, T., Takahashi, T., Ohkawara, S., Yoshinaga, M. (1998) Analysis of the cytokine network among tumor necrosis factor α, interleukin-1β, interleukin-8, and interleukin-1 receptor antagonist in monosodium urate crystal-induced rabbit arthritis. Lab. Invest. 78, 559-569.
6. Rae, S. A., Davidson, E. M., Smith, M. J. (1982) Leukotriene B4, an inflammatory mediator in gout. Lancet 2, 1122-1124.
7. Serhan, C. N., Lundberg, U., Weissmann, G., Samuelsson, B. (1984) Formation of leukotrienes and hydroxy acids by human neutrophils and platelets exposed to monosodium urate. Prostaglandins 27, 563-581.
8. Hachicha, M., Naccache, P. H., McColl, S. R. (1995) Inflammatory microcrystals differentially regulate the secretion of macrophage inflammatory protein 1 and interleukin 8 by human neutrophils: a possible mechanism of neutrophil recruitment to sites of inflammation in synovitis. J. Exp. Med. 182, 2019-2025.
9. Spilberg, I., Bhatt, A. K. (1988) Crystal-induced chemotactic factor. Methods Enzymol. 162, 193-197.
10. Desaulniers, P., Marois, S., Pare, G., Popa-Nita, O., Gilbert, C., Naccache, P. H. (2006) Characterization of an activation factor released from human neutrophils after stimulation by triclinic monosodium urate crystals. J. Rheumatol. 33, 928-938.
11. Roberge, C. J., Gaudry, M., de Medicis, R., Lussier, A., Poubelle, P. E., Naccache, P. H. (1993) Crystal-induced neutrophil activation. IV. Specific inhibition of tyrosine phosphorylation by colchicine. J. Clin. Invest. 92, 1722-1729.
12. Kiefer, F., Brumell, J., Al-Alawi, N., Latour, S., Cheng, A., Veillette, A., Grinstein, S., Pawson, T. (1998) The Syk protein tyrosine kinase is essential for Fcγ receptor signaling in macrophages and neutrophils. Mol. Cell. Biol. 18, 4209-4220.
13. Miller, L. A., Hong, J. J., Kinch, M. S., Harrison, M. L., Geahlen, R. L. (1999) The engagement of β1 integrins on promonocytic cells promotes phosphorylation of Syk and formation of a protein complex containing Lyn and β1 integrin. Eur. J. Immunol. 29, 1426-1434.
14. Desaulniers, P., Fernandes, M., Gilbert, C., Bourgoin, S. G., Naccache, P. H. (2001) Crystal-induced neutrophil activation. VII. Involvement of Syk in the responses to monosodium urate crystals. J. Leukoc. Biol. 70, 659-668.
15. Ibarrola, I., Vossebeld, P. J., Homburg, C. H., Thelen, M., Roos, D., Verhoeven, A. J. (1997) Influence of tyrosine phosphorylation on protein interaction with FcγRIIa. Biochim. Biophys. Acta 1357, 348-358.
16. Vanhaesebroeck, B., Leevers, S. J., Ahmadi, K., Timms, J., Katso, R., Driscoll, P. C., Woscholski, R., Parker, P. J., Waterfield, M. D. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70, 535-602.
17. Cuevas, B. D., Lu, Y., Mao, M., Zhang, J., LaPushin, R., Siminovitch, K., Mills, G. B. (2001) Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 27455-27461.
18. Beitz, L. O., Fruman, D. A., Kurosaki, T., Cantley, L. C., Scharenberg, A. M. (1999) SYK is upstream of phosphoinositide 3-kinase in B cell receptor signaling. J. Biol. Chem. 274, 32662-32666.
19. Okada, T., Maeda, A., Iwamatsu, A., Gotoh, K., Kurosaki, T. (2000) BCAP: the tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 13, 817-827.
20. Moon, K. D., Post, C. B., Durden, D. L., Zhou, Q., De, P., Harrison, M. L., Geahlen, R. L. (2005) Molecular basis for a direct interaction between the Syk protein-tyrosine kinase and phosphoinositide 3-kinase. J. Biol. Chem. 280, 1543-1551.
21. Kodama, T., Hazeki, K., Hazeki, O., Okada, T., Ui, M. (1999) Enhancement of chemotactic peptide-induced activation of phosphoinositide 3-kinase by granulocyte-macrophage colony-stimulating factor and its relation to the cytokine-mediated priming of neutrophil superoxide-anion production. Biochem. J. 337, 201-209.
22. Boulven, I., Levasseur, S., Marois, S., Pare, G., Rollet-Labelle, E., Naccache, P. H. (2006) Class IA phosphatidylinositide 3-kinases, rather than p110 γ, regulate formyl-methionyl-leucyl-phenylalanine-stimulated chemotaxis and superoxide production in differentiated neutrophil-like PLB-985 cells. J. Immunol. 176, 7621-7627.
23. Jackson, J. K., Lauener, R., Duronio, V., Burt, H. M. (1997) The involvement of phosphatidylinositol 3-kinase in crystal induced human neutrophil activation. J. Rheumatol. 24, 341-348.
24. Naccache, P. H., Grimard, M., Roberge, C. J., Gilbert, C., Lussier, A., de Medicis, R., Poubelle, P. E. (1991) Crystal-induced neutrophil activation. I. Initiation and modulation of calcium mobilization and superoxide production by microcrystals. Arthritis Rheum. 34, 333-342.
25. Boyum, A. (1968) Isolation of leucocytes from human blood. A two-phase system for removal of red cells with methylcellulose as erythrocyte-aggregating agent. Scand. J. Clin. Lab. Invest. Suppl. 97, 9-29.
26. Oliver, J. M., Burg, D. L., Wilson, B. S., McLaughlin, J. L., Geahlen, R. L. (1994) Inhibition of mast cell Fc ε R1-mediated signaling and effector function by the Syk-selective inhibitor, piceatannol. J. Biol. Chem. 269, 29697-29703.
27. Gilbert, C., Rollet-Labelle, E., Caon, A. C., Naccache, P. H. (2002) Immunoblotting and sequential lysis protocols for the analysis of tyrosine phosphorylation-dependent signaling. J. Immunol. Methods 271, 185-201.
28. Al-Shami, A., Gilbert, C., Barabe, F., Gaudry, M., Naccache, P. H. (1997) Preservation of the pattern of tyrosine phosphorylation in human neutrophil lysates. J. Immunol. Methods 202, 183-191.
29. Gilbert, C., Rollet-Labelle, E., Naccache, P. H. (2002) Preservation of the pattern of tyrosine phosphorylation in human neutrophil lysates. II. A sequential lysis protocol for the analysis of tyrosine phosphorylation-dependent signaling. J. Immunol. Methods 261, 85-101.
30. Marcil, J., Harbour, D., Houle, M. G., Naccache, P. H., Bourgoin, S. (1999) Monosodium urate-crystal-stimulated phospholipase D in human neutrophils. Biochem. J. 337, 185-192.
31. Hannigan, M. O., Huang, C. K., Wu, D. Q. (2004) Roles of PI3K in neutrophil function. Curr. Top. Microbiol. Immunol. 282, 165-175.
32. Chan, T. O., Tsichlis, P. N. (2001) PDK2: a complex tail in one Akt. Sci. STKE 2001, PE1.
33. Brown, D. A. (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21, 430-439.
34. Kindzelskii, A. L., Sitrin, R. G., Petty, H. R. (2004) Cutting edge: optical microspectrophotometry supports the existence of gel phase lipid rafts at the lamellipodium of neutrophils: apparent role in calcium signaling. J. Immunol. 172, 4681-4685.
35. Schuck, S., Honsho, M., Ekroos, K., Shevchenko, A., Simons, K. (2003) Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. USA 100, 5795-5800.
36. Berton, G., Mocsai, A., Lowell, C. A. (2005) Src and Syk kinases: key regulators of phagocytic cell activation. Trends Immunol. 26, 208-214.
37. Hanke, J. H., Gardner, J. P., Dow, R. L., Changelian, P. S., Brissette, W. H., Weringer, E. J., Pollok, B. A., Connelly, P. A. (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701.
38. Naccache, P. H., Bourgoin, S., Plante, E., Roberge, C. J., de Medicis, R., Lussier, A., Poubelle, P. E. (1993) Crystal-induced neutrophil activation. II. Evidence for the activation of a phosphatidylcholine-specific phospholipase D. Arthritis Rheum. 36, 117-125.
39. Zhou, H. L., Chabot-Fletcher, M., Foley, J. J., Sarau, H. M., Tzimas, M. N., Winkler, J. D., Torphy, T. J. (1993) Association between leukotriene B4-induced phospholipase D activation and degranulation of human neutrophils. Biochem. Pharmacol. 46, 139-148.
40. Lollike, K., Kjeldsen, L., Sengelov, H., Borregaard, N. (1995) Lysozyme in human neutrophils and plasma. A parameter of myelopoietic activity. Leukemia 9, 159-164.
41. Detmers, P. A., Zhou, D., Powell, D., Lichenstein, H., Kelley, M., Pironkova, R. (1995) Endotoxin receptors (CD14) are found with CD16 (Fc γ RIII) in an intracellular compartment of neutrophils that contains alkaline phosphatase. J. Immunol. 155, 2085-2095.
42. Pouliot, M., James, M. J., McColl, S. R., Naccache, P. H., Cleland, L. G. (1998) Monosodium urate microcrystals induce cyclooxygenase-2 in human monocytes. Blood 91, 1769-1776.
43. Wallace, K. L., Riedel, A. A., Joseph-Ridge, N., Wortmann, R. (2004) Increasing prevalence of gout and hyperuricemia over 10 years among older adults in a managed care population. J. Rheumatol. 31, 1582-1587.
44. Kang, D. H., Park, S. K., Lee, I. K., Johnson, R. J. (2005) Uric acid-induced C-reactive protein expression: implication on cell proliferation and nitric oxide production of human vascular cells. J. Am. Soc. Nephrol. 16, 3553-3562.
45. Pascual, E., Sivera, F. (2007) Therapeutic advances in gout. Curr. Opin. Rheumatol. 19, 122-127.
46. Barabe, F., Gilbert, C., Liao, N., Bourgoin, S. G., Naccache, P. H. (1998) Crystal-induced neutrophil activation VI. Involvment of FcγRIIIB (CD16) and CD11b in response to inflammatory microcrystals. FASEB J. 12, 209-220.
47. Fernandes, M. J., Rollet-Labelle, E., Pare, G., Marois, S., Tremblay, M. L., Teillaud, J. L., Naccache, P. H. (2006) CD16b associates with high-density, detergent-resistant membranes in human neutrophils. Biochem. J. 393, 351-359.
48. Huang, Z. Y., Barreda, D. R., Worth, R. G., Indik, Z. K., Kim, M. K., Chien, P., Schreiber, A. D. (2006) Differential kinase requirements in human and mouse Fc-γ receptor phagocytosis and endocytosis. J. Leukoc. Biol. 80, 1553-1562.
49. Gewirtz, A. T., Simons, E. R. (1997) Phospholipase D mediates Fc γ receptor activation of neutrophils and provides specificity between high-valency immune complexes and fMLP signaling pathways. J. Leukoc. Biol. 61, 522-528.
50. Rittner, H. L., Labuz, D., Schaefer, M., Mousa, S. A., Schulz, S., Schafer, M., Stein, C., Brack, A. (2006) Pain control by CXCR2 ligands through Ca2+-regulated release of opioid peptides from polymorphonuclear cells. FASEB J. 20, 2627-2629.
51. Scott, P., Ma, H., Viriyakosol, S., Terkeltaub, R., Liu-Bryan, R. (2006) Engagement of CD14 mediates the inflammatory potential of monosodium urate crystals. J. Immunol. 177, 6370-6378.