The Src family kinases Hck and Fgr are dispensable for inside-out, chemoattractant-induced signaling regulating β2 integrin affinity and valency in neutrophils, but are required for β2 integrin-mediated outside-in signaling involved in sustained adhesion

Journal of Immunology

Volumn 177, Issue 1, 2006, Pages 604-611

  Giagulli, Cinzia ^a   Ottoboni, Linda ^a   Caveggion, Elena ^a   Rossi, Barbara ^a   Lowell, Clifford ^b   Constantin, Gabriela ^a   Laudanna, Carlo ^a,c   Berton, Giorgio ^a,c  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Institute of General Pathology   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 INTEGRIN; CHEMOATTRACTANT; DIMETHYL SULFOXIDE; GLASS; HEMATOPOIETIC CELL KINASE; INTERCELLULAR ADHESION MOLECULE 1; PADGEM PROTEIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE FGR; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; HEMODYNAMICS; IMAGE ANALYSIS; IMMUNOFLUORESCENCE MICROSCOPY; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; LIGAND BINDING; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

EID: 33745313872     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.1.604     Document Type: Article

References (60)

1. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314.
2. Liu, Y., S. K. Shaw, S. Ma, L. Yang, F. W. Luscinskas, and C. A. Parkos. 2004. Regulation of leukocyte transmigration: cell surface interactions and signaling events. J. Immunol. 172:7-13.
3. Springer, T. A., W. S. Thompson, L. J. Miller, F. C. Schmalstieg, and D. C. Anderson. 1984. Inherited deficiency of the Mac-1, LFA-1, p150,95 glycoprotein family, and its molecular basis. J. Exp. Med. 160: 1901-1918.
4. Anderson, D. C., and T. A. Springer. 1987. Leukocyte adhesion deficiency: an inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. Annu. Rev. Med 38: 175-194.
5. Arnaout, M. A. 1990. Leukocyte adhesion molecules deficiency: its structural basis, pathophysiology and implications for modulating the inflammatory response. Immunol. Rev. 114: 145-180.
6. Shuster, D. E., M. E. Kehrli, Jr., M. R. Ackermann, and R. O. Gilbert. 1992. Identification and prevalence of a genetic defect that causes leukocyte adhesion deficiency in Holstein cattle. Proc. Natl. Acad. Sci. USA 89: 9225-9229.
7. Laudanna, C., J. Y. Kim, G. Constantin, and E. Butcher. 2002. Rapid leukocyte integrin activation by chemokines. Immunol. Rev. 186: 37-46.
8. 2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity 13: 759-769.
9. Calderwood, D. A. 2004. Integrin activation. J. Cell Sci. 117: 657-666.
10. Berton, G., and C. A. Lowell. 1999. Integrin signalling in neutrophils and macrophages. Cell Signal. 11: 621-635.
11. Lowell, C. A., and G. Berton. 1999. Integrin signal transduction in myeloid leukocytes. J. Leukocyte Biol. 65: 313-320.
12. Berton, G., A. Mocsai, and C. A. Lowell. 2005. Src and Syk kinases: key regulators of phagocytic cell activation. Trends Immunol. 26: 208-214.
13. Miranti, C. K., and J. S. Brugge. 2002. Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol. 4: E83-E90.
14. DeMali, K. A., K. Wennerberg, and K. Burridge. 2003. Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 15: 572-582.
15. 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.
16. 1 integrin signaling pathway involving Src-family kinases, Cbl, and PI-3 kinase is required for macrophage spreading and migration. EMBO J. 17: 4391-4403.
17. Suen, P. W., D. Ilic, E. Caveggion, G. Berton, C. H. Damsky, and C. A. Lowell. 1999. Impaired integrin-mediated signal transduction, altered cytoskeletal structure and reduced motility in Hck/Fgr deficient macrophages. J. Cell Sci. 112: 4067-4078.
18. 4 integrins that signal through Src family kinases. J. Immunol. 166: 4115-4123.
19. 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.
20. Lowell, C. A., P. Soriano, and H. E. Varmus. 1994. Functional overlap in the src gene family: inactivation of hck and fgr impairs natural immunity. Genes Dev. 8: 387-398.
21. 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: 235-286.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. Laudanna, C., D. Mochly-Rosen, T. Liron, G. Constantin, and E. C. Butcher. 1998. Evidence of zeta protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J. Biol. Chem. 273: 30306-30315.
29. + stem cells restores dystrophin in mdx mice. J. Cell Biol. 152: 335-348.
30. Ley, K., and P. Gaehtgens. 1991. Endothelial, not hemodynamic, differences are responsible for preferential leukocyte rolling in rat mesenteric venules. Circ. Res. 69: 1034-1041.
31. Warnock, R. A., S. Askari, E. C. Butcher, and U. H. von Andrian. 1998. Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J. Exp. Med. 187: 205-216.
32. Mann, H. B., and Whitney, D. R. 1947. On a test of whether one of to random variables is stochastically larger than the other. Ann. Math Stat. 18: 50-60.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Laudanna, C., J. J. Campbell, and E. C. Butcher. 1996. Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271: 981-983.
39. He, R., L. Tan, D. D. Browning, J. M. Wang, and R. D. Ye. 2000. The synthetic peptide Trp-Lys-Tyr-Met-Val-D-Met is a potent chemotactic agonist for mouse formyl peptide receptor. J. Immunol. 165: 4598-4605.
40. Gotsch, U., U. Jager, M. Dominis, and D. Vestweber. 1994. Expression of P-selectin on endothelial cells is up-regulated by LPS and TNF-α in vivo. Cell Adhes. Commun. 2: 7-14.
41. Henninger, D. D., J. Panes, M. Eppihimer, J. Russell, M. Gerritsen, D. C. Anderson, and D. N. Granger. 1997. Cytokine-induced VCAM-1 and ICAM-1 expression in different organs of the mouse. J. Immunol. 158: 1825-1832.
42. Piccio, L., B. Rossi, E. Scarpini, C. Laudanna, C. Giagulli, A. C. Issekutz, D. Vestweber, E. C. Butcher, and G. Constantin. 2002. Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric unlinked receptors. J. Immunol. 168: 1940-1949.
43. Xiao, T., J. Takagi, B. S. Coller, J. H. Wang, and T. A. Springer. 2004. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 432: 59-67.
44. Shamri, R., V. Grabovsky, J. M. Gauguet, S. Feigelson, E. Manevich, W. Kolanus, M. K. Robinson, D. E. Staunton, U. H. von Andrian, and R. Alon. 2005. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat. Immunol. 6: 497-506.
45. Giagulli, C., E. Scarpini, L. Ottoboni, S. Narumiya, E. C. Butcher, G. Constantin, and C. Laudanna. 2004. ρA and ζPKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity 20: 25-35.
46. Kinashi, T. 2005. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5: 546-559.
47. Bokoch, G. M. 1995. Chemoattractant signaling and leukocyte activation. Blood 86: 1649-1660.
48. 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.
49. 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 toward the phagosome during cell activation. Biochem. J. 309: 657-665.
50. Fincham, V. J., A. Chudleigh, and M. C. Frame. 1999. Regulation of p190 ρGAP by v-Src is linked to cytoskeletal disruption during transformation. J. Cell Sci. 112: 947-956.
51. Arthur, W. T., L. A. Fetch, and K. Burridge. 2000. Integrin engagement suppresses ρA activity via a c-Src-dependent mechanism. Curr. Biol. 10: 719-722.
52. Continolo, S., A. Baruzzi, M. Majeed, E. Caveggion, L. Fumagalli, C. A. Lowell, and G. Berton. 2005. The proto-oncogene Fgr regulates cell migration and this requires its plasma membrane localization. Exp. Cell Res. 302: 253-269.
53. Arias-Salgado, E. G., S. Lizano, S. J. Shattil, and M. H. Ginsberg. 2005. Specification of the direction of adhesive signaling by the integrin β cytoplasmic domain. J. Biol. Chem. 280: 29699-29707.
54. 2-integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leukocytes tethered on E-selectin. Biochem J. 396: 89-98.
55. Chiu, J. J., P. L. Lee, C. N. Chen, C. I. Lee, S. F. Chang, L. J. Chen, S. C. Lien, Y. C. Ko, S. Usami, and S. Chien. 2004. Shear stress increases ICAM-1 and decreases VCAM-1 and E-selectin expressions induced by tumor necrosis factor-α in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 24: 73-79.
56. 2 integrin-dependent functions of neutrophils. J. Cell Biol. 166: 273-282.
57. Turner, M., and D. D. Billadeau. 2002. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2: 476-486.
58. 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.
59. 4-cytoplasmic domain. J. Cell Biol. 171: 1073-1084.
60. 4 integrin-paxillin interaction selectively impairs mononuclear leukocyte recruitment to an inflammatory site. J. Clin. Invest. 116: 715-723.