Class IA phosphatidylinositide 3-kinases, rather than p110γ, regulate formyl-methionyl-leucyl-phenylalanine-stimulated chemotaxis and superoxide production in differentiated neutrophil-like PLB-985 cells

Journal of Immunology

Volumn 176, Issue 12, 2006, Pages 7621-7627

  Boulven, Isaline ^b   Levasseur, Sylvain ^b   Marois, Sébastien ^b   Paré, Guillaume ^b   Rollet Labelle, Emmanuelle ^b   Naccache, Paul H ^a  

^a LAVAL UNIVERSITY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

FORMYLMETHIONYLLEUCYLPHENYLALANINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PROTEIN P110; PROTEIN P110 GAMMA; PROTEIN P85; PROTEIN P85 ALPHA; SUPEROXIDE; UNCLASSIFIED DRUG; ISOENZYME; PHOSPHATIDYLINOSITOL 3,4,5-TRIPHOSPHATE; POLYPHOSPHOINOSITIDE;

ARTICLE; BONE MARROW CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; BIOSYNTHESIS; CELL LINE; CELL NUCLEUS; CLASSIFICATION; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; LEUKOCYTE MIGRATION INHIBITION TEST; METABOLISM; NEUTROPHIL; PHYSIOLOGY; TIME;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL DIFFERENTIATION; CELL LINE; CELL MIGRATION INHIBITION; CELL NUCLEUS; CHEMOTAXIS, LEUKOCYTE; HUMANS; ISOENZYMES; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PHOSPHATIDYLINOSITOL PHOSPHATES; SUPEROXIDES; TIME FACTORS; TRANSFECTION;

EID: 33744926913     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.12.7621     Document Type: Article

References (42)

1. Stephens, L., C. Ellson, and P. Hawkins. 2002. Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr. Opin. Cell Biol. 14: 203-213.
2. Moraes, T. J., and G. P. Downey. 2003. Neutrophil cell signaling in infection: role of phosphatidylinositide 3-kinase. Microbes Infect. 5: 1293-1298.
3. Koyasu, S. 2003. The role of PI3K in immune cells. Nat. Immunol. 4: 313-319.
4. Procko, E., and S. R. McColl. 2005. Leukocytes on the move with phosphoinositide 3-kinase and its downstream effectors. BioEssays 27: 153-163.
5. Wymann, M. P., and L. Pirola. 1998. Structure and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta. 1436: 127-150.
6. Vanhaesebroeck, B., and M. D. Waterfield. 1999. Signaling by distinct classes of phosphoinositide 3-kinases. Exp. Cell Res. 253: 239-254.
7. Stephens, L. R., A. Eguinoa, H. Erdjument-Bromage, M. Lui, F. Cooke, J. Coadwell, A. S. Smrcka, M. Thelen, K. Cadwallader, P. Tempst, and P. T. Hawkins. 1997. The G β α sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89: 105-114.
8. Suire, S., J. Coadwell, G. J. Ferguson, K. Davidson, P. Hawkins, and L. Stephens. 2005. p84, a new Gβγ-activated regulatory subunit of the type IB phosphoinositide 3-kinase p110γ. Curr. Biol. 15: 566-570.
9. Rameh, L. E., and L. C. Cantley. 1999. The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274: 8347-8350.
10. Yasui, K., and A. Komiyama. 2001. Roles of phosphatidylinositol 3-kinase and phospholipase D in temporal activation of superoxide production in FMLP-stimulated human neutrophils. Cell Biochem. Funct. 19: 43-50.
11. Coffer, P. J., N. Geijsen, L. M'Rabet, R. C. Schweizer, T. Maikoe, J. A. Raaijmakers, J. W. Lammers, and L. Koenderman. 1998. Comparison of the roles of mitogen-activated protein kinase kinase and phosphatidylinositol 3-kinase signal transduction in neutrophil effector function. Biochem. J. 329: 121-130.
12. Niggli, V., and H. Keller. 1997. The phosphatidylinositol 3-kinase inhibitor wortmannin markedly reduces chemotactic peptide-induced locomotion and increases in cytoskeletal actin in human neutrophils. Eur. J. Pharmacol. 335: 43-52.
13. Nakamura, M., S. Nakashima, Y. Katagiri, and Y. Nozawa. 1997. Effect of wortmannin, and 2-(4-morpholinyl)-8-phenyl-4h-1-benzopyran-4-one (LY294002) on n-formyl-methionyl-leucyl-phenylalanine-induced phospholipase D activation in differentiated HL60 cells: possible involvement of phosphatidylinositol 3-kinase in phospholipase D activation. Biochem. Pharmacol. 53: 1929-1936.
14. Hannigan, M., L. Zhan, Z. Li, Y. Ai, D. Wu, and C. K. Huang. 2002. Neutrophils lacking phosphoinositide 3-kinase γ show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis. Proc. Natl. Acad. Sci. USA 99: 3603-3608.
15. Thomas, M. J., A. Smith, D. H. Head, L. Milne, A. Nicholls, W. Pearce, B. Vanhaesebroeck, M. P. Wymann, E. Hirsch, A. Trifilieff, et al. 2005. Airway inflammation: chemokine-induced neutrophilia and the class I phosphoinositide 3-kinases. Eur. J. Immunol. 35: 1283-1291.
16. Li, Z., H. Jiang, W. Xie, Z. Zhang, A. V. Smrcka, and D. Wu. 2000. Roles of PLC-β2 and -β3 and PI3Kγ in chemoattractant-mediated signal transduction. Science 287: 1046-1049.
17. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 287: 1049-1053.
18. Sasaki, T., J. Irie-Sasaki, R. G. Jones, A. J. Oliveira-dos-Santos, W. L. Stanford, B. Bolon, A. Wakeham, A. Itie, D. Bouchard, I. Kozieradzki, et al. 2000. Function of PI3Kγ in thymocyte development, T cell activation and neutrophil migration. Science 287: 1040-1046.
19. Thelen, M., and S. A. Didichenko. 1997. G-protein coupled receptor-mediated activation of PI 3-kinase in neutrophils. Ann. NY Acad. Sci. 832: 368-382.
20. Ptasznik, A., E. R. Prossnitz, D. Yoshikawa, A. Smrcka, A. E. Traynorkaplan, and G. M. Bokoch. 1996. A tyrosine kinase signaling pathway accounts for the majority of phosphatidylinositol 3,4,5-trisphosphate formation in chemoattractant-stimulated human neutrophils. J. Biol. Chem. 271: 25204-25207.
21. Sadhu, C., K. Dick, W. T. Tino, and D. E. Staunton. 2003. Selective role of PI3K δ in neutrophil inflammatory responses. Biochem. Biophys. Res. Commun. 308: 764-769.
22. Puri, K. D., T. A. Doggett, J. Douangpanya, Y. Hou, W. T. Tino, T. Wilson, T. Graf, E. Clayton, M. Turner, J. S. Hayflick, and T. G. Diacovo. 2004. Mechanisms and implications of phosphoinositide 3-kinase δ in promoting neutrophil trafficking into inflamed tissue. Blood 103: 3448-3456.
23. Naccache, P. H., S. Levasseur, G. Lachance, S. Chakravarti, S. G. Bourgoin, and S. R. McColl. 2000. Stimulation of human neutrophils by chemotactic factors is associated with the activation of phosphatidylinositol 3-kinase γ. J. Biol. Chem. 275: 23636-23641.
24. Bondeva, T., L. Pirola, G. BulgarelliLeva, I. Rubio, R. Wetzker, and M. P. Wymann. 1998. Bifurcation of lipid and protein kinase signals of PI3K γ to the protein kinases PKB and MAPK. Science 282: 293-296.
25. Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. R. Jackson, et al. 1994. 1-Phosphatidyl- inositol 3-kinase activity is required for insulin-stimulated glucose transport but not for RAS activation in CHO cells. Proc. Natl. Acad. Sci. USA 91: 7415-7419.
26. Gilbert, C., S. Levasseur, P. Desaulniers, A. A. Dusseault, N. Thibault, S. G. Bourgoin, and P. H. Naccache. 2003. Chemotactic factor-induced recruitment and activation of Tec family kinases in human neutrophils. II. Effects of LFM-A13, a specific Btk inhibitor. J. Immunol. 170: 5235-5243.
27. Tucker, K. A., M. B. Lilly, L. Heck, Jr., and T. A. Rado. 1987. Characterization of a new human diploid myeloid leukemia cell line (PLB-985) with granulocytic and monocytic differentiating capacity. Blood 70: 372-378.
28. Dana, R. R., C. Eigsti, K. L. Holmes, and T. L. Leto. 2000. A regulatory role for ADP-ribosylation factor 6 (ARF6) in activation of the phagocyte NADPH oxidase. J. Biol. Chem. 275: 32566-32571.
29. Sasaki, T., A. Suzuki, J. Sasaki, and J. M. Penninger. 2002. Phosphoinositide 3-kinases in immunity: lessons from knockout mice. J. Biochem. 131: 495-501.
30. Stephens, L., A. Eguinoa, S. Corey, T. Jackson, and P. T. Hawkins. 1993. Receptor stimulated accumulation of phosphatidylinositol (3,4,5)-trisphosphate by G-protein mediated pathways in human myeloid derived cells. EMBO J. 12: 2265-2273.
31. Condliffe, A. M., K. Davidson, K. E. Anderson, C. D. Ellson, T. Crabbe, K. Okkenhaug, B. Vanhaesebroeck, M. Turner, L. Webb, M. P. Wymann, et al. 2005. Sequential activation of Class IB and Class IA PI3Ks is important for the primed respiratory burst of human but not murine neutrophils. Blood 106: 1432-1440.
32. Kurosu, H., T. Maehama, T. Okada, T. Yamamoto, S. Hoshino, Y. Fukui, M. Ui, O. Hazeki, and T. Katada. 1997. Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110 β is synergistically activated by the β γ subunits of G proteins and phosphotyrosyl peptide. J. Biol Chem. 272: 24252-24256.
33. Maier, U., A. Babich, and B. Nurnberg. 1999. Roles of non-catalytic subunits in Gβγ-induced activation of class I phosphoinositide 3-kinase isoforms β and γ. J. Biol. Chem. 274: 29311-29317.
34. Lachance, G., S. Levasseur, and P. H. Naccache. 2002. Chemotactic factor-induced recruitment and activation of Tec family kinases in human neutrophils: implication of phosphatidylinositol 3-kinases. J. Biol. Chem. 277: 21537-21541.
35. Weiner, O. D., P. O. Neilsen, G. D. Prestwich, M. W. Kirschner, L. C. Cantley, and H. R. Bourne. 2002. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4: 509-513.
36. Rickert, P., O. D. Weiner, F. Wang, H. R. Bourne, and G. Servant. 2000. Leukocytes navigate by compass: roles of PI3K γ and its lipid products. Trends Cell Biol. 10: 466-473.
37. Wu, D. Q., C. K. Huang, and H. P. Jiang. 2000. Roles of phospholipid signaling in chemoattractant-induced responses. J. Cell Sci. 113: 2935-2940.
38. Niggli, V. 2003. Signaling to migration in neutrophils: importance of localized pathways. Int. J. Biochem. Cell Biol. 35: 1619-1638.
39. Van Haastert, P. J., and P. N. Devreotes. 2004. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5: 626-634.
40. Hannigan, M. O., C. K. Huang, and D. Q. Wu. 2004. Roles of PI3K in neutrophil function. Curr. Top. Microbiol. Immunol. 282: 165-175.
41. Vanhaesebroeck, B., J. L. Rohn, and M. D. Waterfield. 2004. Gene targeting: attention to detail. Cell 118: 274-276.
42. Nakanishi, S., S. Kakita, I. Takahashi, K. Kawahara, E. Tsukuda, T. Sano, K. Yamada, M. Yoshida, H. Kase, and Y. Matsuda. 1992. Wortmannin, a microbial product inhibitor of myosin light chain kinase. J. Biol. Chem. 267: 2157-2163.