Class i phosphoinositide-3-kinases and Src kinases play a nonredundant role in regulation of adhesion-independent and -dependent neutrophil reactive oxygen species generation

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3648-3660

  Fumagalli, Laura ^a   Campa, Carlo C ^b   Germena, Giulia ^b   Lowell, Clifford A ^c   Hirsch, Emilio ^b   Berton, Giorgio ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CLASS I PHOSPHOINOSITIDE 3 KINASE; HEMATOPOIETIC CELL KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PHOSPHOINOSITIDE 3 KINASE ALPHA; PHOSPHOINOSITIDE 3 KINASE DELTA; PROTEIN FGR; PROTEIN KINASE B; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VAV PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LEUKOCYTE ADHERENCE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

ANIMALS; CELL ADHESION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; ISOENZYMES; MICE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-VAV; PROTO-ONCOGENE PROTEINS P21(RAS); REACTIVE OXYGEN SPECIES; SRC-FAMILY KINASES; TUMOR NECROSIS FACTORS;

EID: 84875428631     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201951     Document Type: Article

References (50)

1. Lambeth, J. D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4: 181-189.
2. Nathan, C., and A. Ding 2010. SnapShot: Reactive Oxygen Intermediates (ROI). Cell 140: 951-951.e2.
3. Nathan, C. F. 1987. Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J. Clin. Invest. 80: 1550-1560.
4. Berton, G., C. Laudanna, C. Sorio, and F. Rossi. 1992. Generation of signals activating neutrophil functions by leukocyte integrins: LFA-1 and gp150/95, but not CR3, are able to stimulate the respiratory burst of human neutrophils. J. Cell Biol. 116: 1007-1017.
5. Berton, G., and C. A. Lowell. 1999. Integrin signalling in neutrophils and macrophages. Cell. Signal. 11: 621-635.
6. 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 gamma in inflammation. Science 287: 1049-1053.
7. Lowell, C. A., L. Fumagalli, and G. Berton. 1996. Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133: 895-910.
8. Mócsai, A., M. Zhou, F. Meng, V. L. Tybulewicz, and C. A. Lowell. 2002. Syk is required for integrin signaling in neutrophils. Immunity 16: 547-558.
9. Berton, G., A. Mócsai, and C. A. Lowell. 2005. Src and Syk kinases: key regulators of phagocytic cell activation. Trends Immunol. 26: 208-214.
10. Mócsai, A., J. Ruland, and V. L. Tybulewicz. 2010. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10: 387-402.
11. 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 PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood 106: 1432-1440.
12. Nijhuis, E., J. W. Lammers, L. Koenderman, and P. J. Coffer. 2002. Src kinases regulate PKB activation and modulate cytokine and chemoattractant- controlled neutrophil functioning. J. Leukoc. Biol. 71: 115-124.
13. Gao, X. P., X. Zhu, J. Fu, Q. Liu, R. S. Frey, and A. B. Malik. 2007. Blockade of class IA phosphoinositide 3-kinase in neutrophils prevents NADPH oxidase activation- and adhesion-dependent inflammation. J. Biol. Chem. 282: 6116-6125.
14. Fumagalli, L., H. Zhang, A. Baruzzi, C. A. Lowell, and G. Berton. 2007. The Src family kinases Hck and Fgr regulate neutrophil responses to N-formyl-methionylleucyl- phenylalanine. J. Immunol. 178: 3874-3885.
15. Chen, J., H. Tang, N. Hay, J. Xu, and R. D. Ye. 2010. Akt isoforms differentially regulate neutrophil functions. Blood 115: 4237-4246.
16. Roberts, A. W., C. Kim, L. Zhen, J. B. Lowe, R. Kapur, B. Petryniak, A. Spaetti, J. D. Pollock, J. B. Borneo, G. B. Bradford, et al. 1999. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10: 183-196.
17. Ambruso, D. R., C. Knall, A. N. Abell, J. Panepinto, A. Kurkchubasche, G. Thurman, C. Gonzalez-Aller, A. Hiester, M. deBoer, R. J. Harbeck, et al. 2000. Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc. Natl. Acad. Sci. USA 97: 4654-4659.
18. Kim, C., and M. C. Dinauer. 2001. Rac2 is an essential regulator of neutrophil nicotinamide adenine dinucleotide phosphate oxidase activation in response to specific signaling pathways. J. Immunol. 166: 1223-1232.
19. Kim, C., C. C. Marchal, J. Penninger, and M. C. Dinauer. 2003. The hemopoietic Rho/Rac guanine nucleotide exchange factor Vav1 regulates N-formylmethionyl-leucyl-phenylalanine-activated neutrophil functions. J. Immunol. 171: 4425-4430.
20. Welch, H. C., A. M. Condliffe, L. J. Milne, G. J. Ferguson, K. Hill, L. M. Webb, K. Okkenhaug, W. J. Coadwell, S. R. Andrews, M. Thelen, et al. 2005. P-Rex1 regulates neutrophil function. Curr. Biol. 15: 1867-1873.
21. Dong, X., Z. Mo, G. Bokoch, C. Guo, Z. Li, and D. Wu. 2005. P-Rex1 is a primary Rac2 guanine nucleotide exchange factor in mouse neutrophils. Curr. Biol. 15: 1874-1879.
22. Kunisaki, Y., A. Nishikimi, Y. Tanaka, R. Takii, M. Noda, A. Inayoshi, K. Watanabe, F. Sanematsu, T. Sasazuki, T. Sasaki, and Y. Fukui. 2006. DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J. Cell Biol. 174: 647-652.
23. Lawson, C. D., S. Donald, K. E. Anderson, D. T. Patton, and H. C. Welch. 2011. P-Rex1 and Vav1 cooperate in the regulation of formyl-methionyl- leucylphenylalanine-dependent neutrophil responses. J. Immunol. 186: 1467-1476.
24. 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.
25. Sadhu, C., K. Dick, W. T. Tino, and D. E. Staunton. 2003. Selective role of PI3K delta in neutrophil inflammatory responses. Biochem. Biophys. Res. Commun. 308: 764-769.
26. Boyle, K. B., D. Gyori, A. Sindrilaru, K. Scharffetter-Kochanek, P. R. Taylor, A. Mócsai, L. R. Stephens, and P. T. Hawkins. 2011. Class IA phosphoinositide 3-kinase b and d regulate neutrophil oxidase activation in response to Aspergillus fumigatus hyphae. J. Immunol. 186: 2978-2989.
27. Gakidis, M. A., X. Cullere, T. Olson, J. L. Wilsbacher, B. Zhang, S. L. Moores, K. Ley, W. Swat, T. Mayadas, and J. S. Brugge. 2004. Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. J. Cell Biol. 166: 273-282.
28. Jakus, Z., E. Simon, D. Frommhold, M. Sperandio, and A. Mócsai. 2009. Critical role of phospholipase Cgamma2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis. J. Exp. Med. 206: 577-593.
29. Meng, F., and C. A. Lowell. 1997. Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J. Exp. Med. 185: 1661-1670.
30. Lundqvist, H., and C. Dahlgren. 1996. Isoluminol-enhanced chemiluminescence: a sensitive method to study the release of superoxide anion from human neutrophils. Free Radic. Biol. Med. 20: 785-792.
31. Vanhaesebroeck, B., J. Guillermet-Guibert, M. Graupera, and B. Bilanges. 2010. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11: 329-341.
32. Cadwallader, K. A., A. M. Condliffe, A. McGregor, T. R. Walker, J. F. White, L. R. Stephens, and E. R. Chilvers. 2002. Regulation of phosphatidylinositol 3-kinase activity and phosphatidylinositol 3,4,5-trisphosphate accumulation by neutrophil priming agents. J. Immunol. 169: 3336-3344.
33. Suire, S., C. Lécureuil, K. E. Anderson, G. Damoulakis, I. Niewczas, K. Davidson, H. Guillou, D. Pan, J. Clark, P. T. Hawkins, and L. Stephens. 2012. GPCR activation of Ras and PI3Kc in neutrophils depends on PLCb2/b3 and the RasGEF RasGRP4. EMBO J. 31: 3118-3129.
34. Anderson, D. C., F. C. Schmalstieg, M. A. Arnaout, S. Kohl, M. F. Tosi, N. Dana, G. J. Buffone, B. J. Hughes, B. R. Brinkley, W. D. Dickey, et al. 1984. Abnormalities of polymorphonuclear leukocyte function associated with a heritable deficiency of high molecular weight surface glycoproteins (GP138): common relationship to diminished cell adherence. J. Clin. Invest. 74: 536-551.
35. Marone, R., V. Cmiljanovic, B. Giese, and M. P. Wymann. 2008. Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim. Biophys. Acta 1784: 159-185.
36. Turner, M., and D. D. Billadeau. 2002. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2: 476-486.
37. Boulven, I., S. Levasseur, S. Marois, G. Paré, E. Rollet-Labelle, and P. H. Naccache. 2006. Class IA phosphatidylinositide 3-kinases, rather than p110 gamma, regulate formyl-methionyl-leucyl-phenylalanine-stimulated chemotaxis and superoxide production in differentiated neutrophil-like PLB-985 cells. J. Immunol. 176: 7621-7627.
38. Zhu, J. W., K. Doan, J. Park, A. H. Chau, H. Zhang, C. A. Lowell, and A. Weiss. 2011. Receptor-like tyrosine phosphatases CD45 and CD148 have distinct functions in chemoattractant-mediated neutrophil migration and response to S. aureus. Immunity 35: 757-769.
39. Crowley, C. A., J. T. Curnutte, R. E. Rosin, J. André-Schwartz, J. I. Gallin, M. Klempner, R. Snyderman, F. S. Southwick, T. P. Stossel, and B. M. Babior. 1980. An inherited abnormality of neutrophil adhesion. Its genetic transmission and its association with a missing protein. N. Engl. J. Med. 302: 1163-1168.
40. Zheng, L., A. Sjölander, J. Eckerdal, and T. Andersson. 1996. Antibody-induced engagement of beta 2 integrins on adherent human neutrophils triggers activation of p21ras through tyrosine phosphorylation of the protooncogene product Vav. Proc. Natl. Acad. Sci. USA 93: 8431-8436.
41. Graham, D. B., C. M. Robertson, J. Bautista, F. Mascarenhas, M. J. Diacovo, V. Montgrain, S. K. Lam, V. Cremasco, W. M. Dunne, R. Faccio, et al. 2007. Neutrophil-mediated oxidative burst and host defense are controlled by a Vav-PLCgamma2 signaling axis in mice. J. Clin. Invest. 117: 3445-3452.
42. Kamen, L. A., J. Schlessinger, and C. A. Lowell. 2011. Pyk2 is required for neutrophil degranulation and host defense responses to bacterial infection. J. Immunol. 186: 1656-1665.
43. Luttrell, D. K., and L. M. Luttrell. 2004. Not so strange bedfellows: G-proteincoupled receptors and Src family kinases. Oncogene 23: 7969-7978.
44. McGarrigle, D., and X. Y. Huang. 2007. GPCRs signaling directly through Srcfamily kinases. Sci. STKE 2007: pe35.
45. Ptasznik, A., A. Traynor-Kaplan, and G. M. Bokoch. 1995. G protein-coupled chemoattractant receptors regulate Lyn tyrosine kinase.Shc adapter protein signaling complexes. J. Biol. Chem. 270: 19969-19973.
46. Mócsai, A., E. Ligeti, C. A. Lowell, and G. Berton. 1999. Adhesion-dependent degranulation of neutrophils requires the Src family kinases Fgr and Hck. J. Immunol. 162: 1120-1126.
47. Gutkind, J. S., and K. C. Robbins. 1989. Translocation of the FGR proteintyrosine kinase as a consequence of neutrophil activation. Proc. Natl. Acad. Sci. USA 86: 8783-8787.
48. Barlic, J., J. D. Andrews, A. A. Kelvin, S. E. Bosinger, M. E. DeVries, L. Xu, T. Dobransky, R. D. Feldman, S. S. Ferguson, and D. J. Kelvin. 2000. Regulation of tyrosine kinase activation and granule release through beta-arrestin by CXCRI. Nat. Immunol. 1: 227-233.
49. Scapini, P., M. Morini, C. Tecchio, S. Minghelli, E. Di Carlo, E. Tanghetti, A. Albini, C. Lowell, G. Berton, D. M. Noonan, and M. A. Cassatella. 2004. CXCL1/macrophage inflammatory protein-2-induced angiogenesis in vivo is mediated by neutrophil-derived vascular endothelial growth factor-A. J. Immunol. 172: 5034-5040.
50. Kulkarni, S., C. Sitaru, Z. Jakus, K. E. Anderson, G. Damoulakis, K. Davidson, M. Hirose, J. Juss, D. Oxley, T. A. Chessa, et al. 2011. PI3Kβ plays a critical role in neutrophil activation by immune complexes. Sci. Signal. 4: ra23.