The Src family kinases Hck and Fgr regulate neutrophil responses to N-formyl-methionyl-leucyl-phenylalanine

Journal of Immunology

Volumn 178, Issue 6, 2007, Pages 3874-3885

  Fumagalli, Laura ^a   Zhang, Hong ^b   Baruzzi, Anna ^a   Lowell, Clifford A ^b   Berton, Giorgio ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; CALCIUM ION; CELL PROTEIN; CHEMOTACTIC PEPTIDE; F ACTIN; FORMYLMETHIONYLLEUCYLPHENYLALANINE; HEMATOPOIETIC CELL KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; P21 ACTIVATED KINASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE B; PROTEIN KINASE FGR; PROTEIN TYROSINE KINASE; PROTEIN VAV1; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL MIGRATION; CONTROLLED STUDY; DEGRANULATION; ENZYME PHOSPHORYLATION; FEMALE; FGR GENE; GENE; HCK GENE; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

EID: 33947198166     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.6.3874     Document Type: Article

References (73)

1. Murphy, P. M. 1994. The molecular biology of leukocyte chemoattractant receptors. Annu. Rev. Immunol. 12: 593-633.
2. Gao, J. L., E. J. Lee, and P. M. Murphy. 1999. Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med. 189: 657-662.
3. Bokoch, G. M. 1995. Chemoattractant signaling and leukocyte activation. Blood 86: 1649-1660.
4. Cockcroft, S. 1992. G-protein-regulated phospholipases C, D and A2-mediated signalling in neutrophils. Biochim. Biophys. Acta 1113: 135-160.
5. Billah, M. M. 1993. Phospholipase D and cell signaling. Curr. Opin. Immunol. 5: 114-123.
6. Thelen, M., and U. Wirthmueller. 1994. Phospholipases and protein kinases during phagocyte activation. Curr. Opin. Immunol. 6: 100-112.
7. 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.
8. Wymann, M. P., S. Sozzani, F. Altruda, A. Mantovani, and E. Hirsch. 2000. Lipids on the move: phosphoinositide 3-kinases in leukocyte function. Immunol. Today 21: 260-264.
9. 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.
10. Gomez-Cambronero, J., C. K. Huang, V. A. Bonak, E. Wang, J. E. CasneMe, T. Shiraishi, and R. I. Sha'afi. 1989. Tyrosine phosphorylation in human neutrophil. Biochem. Biophys. Res. Commun. 162: 1478-1485.
11. Rollet, E., A. C. Caon, C. J. Roberge, N. W. Liao, S. E. Malawista, S. R. McColl, and P. H. Naccache. 1994. Tyrosine phosphorylation in activated human neutrophils: comparison of the effects of different classes of agonists and identification of the signaling pathways involved. J. Immunol. 153: 353-363.
12. Yan, S. R., L. Fumagalli, and G. Berton. 1996. Activation of SRC family kinases in human neutrophils: evidence that p58C-FGR and p53/56LYN redistributed to a Triton X-100-insoluble cytoskeletal fraction, also enriched in the caveolar protein caveolin, display an enhanced kinase activity. FEBS Lett. 380: 198-203.
13. Gutkind, J. S., and K. C. Robbins. 1989. Translocation of the FGR protein-tyrosine kinase as a consequence of neutrophil activation. Proc. Natl. Acad. Sci. USA 86: 8783-8787.
14. 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.
15. Gaudry, M., C. Gilbert, F. Barabe, P. E. Poubelle, and P. H. Naccache. 1995. Activation of Lyn is a common element of the stimulation of human neutrophils by soluble and particulate agonists. Blood 86: 3567-3574.
16. Mocsai, A., B. Banfi, A. Kapus, G. Farkas, M. Geiszt, L. Buday, A. Farago, and E. Ligeti. 1997. Differential effects of tyrosine kinase inhibitors and an inhibitor of the mitogen-activated protein kinase cascade on degranulation and superoxide production of human neutrophil granulocytes. Biochem. Pharmacol. 54: 781-789.
17. Mocsai, A., Z. Jakus, T. Vantus, G. Berton, C. A. Lowell, and E. Ligeti. 2000. Kinase pathways in chemoattractant-induced degranulation of neutrophils: the role of p38 mitogen-activated protein kinase activated by Src family kinases. J. Immunol. 164: 4321-4331.
18. Mocsai, 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.
19. Lachance, G., S. Levasseur, and P. H. Naccache. 2002. Chemotactic factor-induced recruitment and activation of Tec family kinases in human neutrophils: implication of phosphatidynositol 3-kinases. J. Biol. Chem. 277: 21537-21541.
20. Miura, Y., Y. Tohyama, T. Hishita, A. Lala, E. De Nardin, Y. Yoshida, H. Yamamura, T. Uchiyama, and K. Tohyama. 2000. Pyk2 and Syk participate in functional activation of granulocytic HL-60 cells in a different manner. Blood 96: 1733-1739.
21. 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 β-arrestin by CXCRI. Nat. Immunol. 1: 227-233.
22. El-Shazly, A., N. Yamaguchi, K. Masuyama, T. Suda, and T. Ishikawa. 1999. Novel association of the src family kinases, hck and c-fgr, with CCR3 receptor stimulation: a possible mechanism for eotaxin-induced human eosinophil chemotaxis. Biochem. Biophys. Res. Commun. 264: 163-170.
23. 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.
24. 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. Leukocyte Biol. 71: 115-124.
25. 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.
26. Mocsai, A., H. Zhang, Z. Jakus, J. Kitaura, T. Kawakami, and C. A. Lowell. 2003. G-protein-coupled receptor signaling in Syk-deficient neutrophils and mast cells. Blood 101: 4155-4163.
27. Mohn, H., V. Le Cabec, S. Fischer, and I. Maridonneau-Parini. 1995. The src-family protein-tyrosine kinase p59hck is located on the secretory granules in human neutrophils and translocates towards the phagosome during cell activation. Biochem. J. 309: 657-665.
28. Zhang, H., F. Meng, C. L. Chu, T. Takai, and C. A. Lowell. 2005. The Src family kinases Hck and Fgr negatively regulate neutrophil and dendritic cell chemokine signaling via PIR-B. Immunity 22: 235-246.
29. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 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.
30. 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.
31. Hart, P. H., L. K. Spencer, M. F. Nulsen, P. J. McDonald, and J. J. Finlay-Jones. 1986. Neutrophil activity in abscess-bearing mice: comparative studies with neutrophils isolated from peripheral blood, elicited peritoneal exudates, and abscesses. Infect. Immun. 51: 936-941.
32. Pember, S. O., K. C. Barnes, S. J. Brandt, and J. M. Kinkade, Jr. 1983. Density heterogeneity of neutrophilic polymorphonuclear leukocytes: gradient fractionation and relationship to chemotactic stimulation. Blood 61: 1105-1115.
33. 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.
34. + indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450.
35. 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.
36. Berton, G., A. Mocsai, and C. A. Lowell. 2005. Src and Syk kinases: key regulators of phagocytic cell activation. Trends Immunol. 26: 208-214.
37. Lowell, C. A., and G. Berton. 1999. Integrin signal transduction in myeloid leukocytes. J. Leukocyte Biol. 65: 313-320.
38. Mocsai, 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.
39. Baggiolini, M., B. Dewald, J. Schnyder, W. Ruch, P. H. Cooper, and T. G. Payne. 1987. Inhibition of the phagocytosis-induced respiratory burst by the fungal metabolite wortmannin and some analogues. Exp. Cell Res. 169: 408-418.
40. Arcaro, A., and M. P. Wymann. 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.
41. 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.
42. Krump, E., J. S. Sanghera, S. L. Pelech, W. Furuya, and S. Grinstein. 1997. Chemotactic peptide N-formyl-Met-Leu-Phe activation of p38 mitogen-activated protein kinase (MAPK) and MAPK-activated protein kinase-2 in human neutrophils. J. Biol. Chem. 272: 937-944.
43. Torres, M., F. L. Hall, and K. O'Neill. 1993. Stimulation of human neutrophils with formyl-methionyl-leucyl-phenylalariine induces tyrosine phosphorylation and activation of two distinct mitogen-activated protein-kinases. J. Immunol. 150: 1563-1577.
44. 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.
45. 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.
46. Diebold, B. A., and G. M. Bokoch. 2001. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat. Immunol. 2: 211-215.
47. phox cells, and the level of superoxide production is exchange factor-dependent. J. Biol Chem. 277: 19220-19228.
48. phox: conversion of a pagan NADPH oxidase to monotheism. J. Biol. Chem. 277: 18605-18610.
49. Dinauer, M. C. 2003. Regulation of neutrophil function by Rac GTPases. Curr. Opin. Hematol. 10: 8-15.
50. Bokoch, G. M. 2005. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15: 163-171.
51. Bishop, A. L., and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348: 241-255.
52. Gallo, K. A., and G. L. Johnson. 2002. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell. Biol. 3: 663-672.
53. Benard, V., B. P. Bohl, and G. M. Bokoch. 1999. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274: 13198-13204.
54. Turner, M., and D. D. Billadeau. 2002. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2: 476-486.
55. Kim, C., C. C. Marchal, J. Penninger, and M. C. Dinauer. 2003. The hemopoietic Rho/Rac guanine nucleotide exchange factor Vav1 regulates N-formyl-methionyl-leucyl-phenylalanine-activated neutrophil functions. J. Immunol. 171: 4425-4430.
56. Billadeau, D. D., S. M. Mackie, R. A. Schoon, and P. J. Leibson. 2000. Specific subdomains of Vav differentially affect T cell and NK cell activation. J. Immunol. 164: 3971-3981.
57. Lopez-Lago, M., H. Lee, C. Cruz, N. Movilla, and X. R. Bustelo. 2000. Tyrosine phosphorylation mediates both activation and downmodulation of the biological activity of Vav. Mol. Cell Biol. 20: 1678-1691.
58. Bokoch, G. M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72: 743-781.
59. Lindbom, L. 2003. Regulation of vascular permeability by neutrophils in acute inflammation. In The Neutrophil: An Emerging Regulator of Inflammatory and Immune Response, Vol. 83. M. A. Cassatella, ed. Karger, Basel, pp. 146-166.
60. phox-/- mice. J. Immunol. 168: 3974-3982.
61. Glogauer, M., C. C. Marchal, F. Zhu, A. Worku, B. E. Clausen, I. Foerster, P. Marks, G. P. Downey, M. Dinauer, and D. J. Kwiatkowski. 2003. Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J. Immunol. 170: 5652-5657.
62. Gu, Y., M. D. Filippi, J. A. Cancelas, J. E. Siefring, E. P. Williams, A. C. Jasti, C. E. Harris, A. W. Lee, R. Prabhakar, S. J. Atkinson, et al. 2003. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302: 445-449.
63. 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.
64. Dong, X., Z. Mo, G. Bokoch, C. Quo, Z. Li, and D. Wu. 2005. P-Rex1 is a primary Rac2 guanine nucleotide exchange factor in mouse neutrophils. Curr. Biol. 15: 1874-1879.
65. Welch, H. C., W. J. Coadwell, C. D. Ellson, G. J. Ferguson, S. R. Andrews, H. Erdjument-Bromage, P. Tempst, P. T. Hawkins, and L. R. Stephens. 2002. P-Rex1, a PtdIns(3,4,5)P3- and unregulated guanine-nucleotide exchange factor for Rac. Cell 108: 809-821.
66. 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.
67. Lowell, C. A., and G. Berton. 1998. Resistance to endotoxic shock and reduced neutrophil migration in mice deficient for the Src family kinases Hck and Fgr. Proc. Natl. Acad. Sci. USA 95: 7580-7584.
68. Vicentini, L., P. Mazzi, E. Caveggion, S. Continolo, L. Fumagalli, J. A. Lapinet-Vera, C. A. Lowell, and G. Berton. 2002. Fgr deficiency results in defective eosinophil recruitment to the lung during allergic airway inflammation. J. Immunol. 168: 6446-6454.
69. Thomas, R. M., C. Schmedt, M. Novelli, B. K. Choi, J. Skok, A. Tarakhovsky, and J. Roes. 2004. C-terminal SRC kinase controls acute inflammation and granulocyte adhesion. Immunity 20: 181-191.
70. Ernst, M., M. Inglese, G. M. Scholz, K. W. Harder, F. J. Clay, S. Bozinovski, P. Waring, R. Darwiche, T. Kay, P. Sly, et al. 2002. Constitutive activation of the SRC family kinase Hck results in spontaneous pulmonary inflammation and an enhanced innate immune response. J. Exp. Med. 196: 589-604.
71. 2 integrin-mediated outside-in signaling involved in sustained adhesion. J. Immunol. 177: 604-611.
72. 2-integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leukocytes tethered on E-selectin. Biochem. J. 396: 89-98.
73. 2 integrin-dependent functions of neutrophils. J. Cell Biol. 166: 273-282.