A β1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4391-4403

  Meng, Fanying ^a   Lowell, Clifford A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cbl; Integrin; Macrophages; MAP kinases; PI 3 kinase; Src family kinases

Indexed keywords

INTEGRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SPREADING; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD29; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL ADHESION; CELL MIGRATION INHIBITION; CELL MOVEMENT; DNA; ENZYME ACTIVATION; FIBRONECTINS; INFLAMMATION; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; MUTATION; NF-KAPPA B; OLIGONUCLEOTIDES, ANTISENSE; ONCOGENE PROTEIN V-CBL; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-HCK; RETROVIRIDAE PROTEINS, ONCOGENIC; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TYROSINE;

ANIMALIA;

EID: 0032479979     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4391     Document Type: Article

References (65)

1. Anderson, S.M., Burton, E.A. and Koch, B.L. (1997) Phosphorylation of Cb1 following stimulation with interleukin-3 and its association with Grb2, Fyn and phosphatidylinositol 3-kinase. J. Biol. Chem., 272, 739-745.
2. Beggs, H.E., Soriano, P. and Maness, P.F. (1994) NCAM-dependent neunte outgrowth is inhibited in neurons from Fyn-minus mice. J. Cell. Biol., 127, 825-833.
3. Berton, G., Fumagalli, L., Laudanna, C. and Sorio, C. (1994) β2 integrin-dependent protein tyrosine phosphorylation and activation of the FGR protein tyrosine kinase in human neutrophils. J. Cell. Biol., 126, 1111-1121.
4. Berton, G., Yan, S.R., Fumagalli, L. and Lowell, C.A. (1996) Neutrophil activation by adhesion: mechanisms and pathophysiological implications. Int. J. Clin. Lab. Res., 26, 160-177.
5. Bockholt, S.M. and Burridge, K. (1993) Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J. Biol. Chew., 268, 14565-14567.
6. Bowtell, D.D. and Langdon, W.Y. (1995) The protein product of the c-cbl oncogene rapidly complexes with the EGF receptor and is tyrosine phosphorylated following EGF stimulation. Oncogene, 11, 1561-1567.
7. c-src expression for osteoclasts to form ruffled borders and to resorb bone in mice. J. Clin. Invest., 90, 1622-1627.
8. Burridge, K., Turner, C.E. and Romer, L.H. (1992) Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell. Biol., 119, 893-903.
9. Chan, V.W., Meng, F. Soriano, P., DeFranco, A.L. and Lowell, C.A. (1997) Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity, 7, 69-81.
10. Chan, V.W.F., Lowell, C.A. and DeFranco, A.L. (1998) Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphoyctes. Curr. Biol., 8, 545-553.
11. Chen, Q., Kinch, M.S., Lin, T.H., Burridge, K. and Juliano, R.L. (1994) Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem., 269, 26602-26605.
12. Crowley, M., Costello, P., Fitzer-Attas, C., Turner, M., Meng, F., Lowell, C., Tybulewicz, V. and DeFranco, A. (1997) A critical role for Syk in signal transduction and phagocytosis mediated by Fcγ receptors on macrophages. J. Exp. Med., 186, 1027-1039.
13. De Nichilo, M.O. and Yamada, K.M. (1996) Integrin αvβ5-dependent serine phosphorylation of paxillin in cultured human macrophages adherent to vitronectin. J. Biol. Chem., 271, 11016-11022.
14. Donovan, J.A., Wange, R.L., Langdon, W.Y. and Samelson, L.E. (1994) The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor. J. Biol. Chem., 269, 22921-22924.
15. Eberle, M., Traynor-Kaplan, A.E., Sklar, L.A. and Norgauer, J. (1990) Is there a relationship between phosphatidylinositol trisphosphate and F-actin polymerization in human neutrophils? J. Biol. Chem., 265, 16725-16728.
16. Frenette, P.S., Mayadas, T.N., Rayburn, H., Hynes, R.O. and Wagner, D.D. (1996) Susceptibility to infection and altered hematopoiesis in mice deficient in both P-and E-selectins. Cell, 84, 563-574.
17. Galisteo, M.L., Dikic, I., Batzer, A.G., Langdon, W.Y. and Schlessinger, J. (1995) Tyrosine phosphorylation of the c-cbl proto-oncogene protein product and association with epidermal growth factor (EGF) receptor upon EGF stimulation. J. Biol. Chem., 270, 20242-20245.
18. Gold, M.R., Chan, V.W., Turck, C.W. and DeFranco, A.L. (1992) Membrane Ig cross-linking regulates phosphatidylinositol 3-kinase in B lymphocytes. J. Immunol., 148, 2012-2022.
19. Hambleton, J., McMahon, M. and DeFranco, A.L. (1995) Activation of Raf-1 and mitogen-activated protein kinase in murine macrophages partially mimics lipopolysaccharide-induced signaling events. J. Exp. Med., 182, 147-154.
20. Hanke, J.H., Gardner, J.P., Dow, R.L., Changelian, P.S., Brissette, W.H., Weringer, E.J., Pollok, B.A. and 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.
21. Hartwig, J.H., Kung, S., Kovacsovics, T., Janmey, P.A., Cantley, L.C., Stossel, T.P. and Toker, A. (1996) D3 phosphoinositides and outside-in integrin signaling by glycoprotein IIb-IIIa mediate platelet actin assembly and filopodial extension induced by phorbol 12-myristate 13-acetate. J. Biol. Chem., 271, 32986-32993.
22. Haskill, S., Beg, A.A., Tompkins, S.M., Morris, J.S., Yurochko, A.D., Sampson-Johannes, A., Mondal, K., Ralph, P. and Baldwin, A.S.,Jr (1991) Characterization of an immediate-early gene induced in adherent monocytes that encodes Iκ B-like activity. Cell, 65, 1281-1289.
23. Jongeward, G.D., Clandinin, T.R. and Sternberg, P.W. (1995) sli-1, a negative regulator of let-23-mediated signaling in C.elegans. Genetics, 139, 1553-1566.
24. Kaplan, K.B., Bibbins, K.B., Swedlow, J.R., Arnaud, M., Morgan, D.O. and Varmus, H.E. (1994) Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J., 13, 4745-4756.
25. Khwaja, A., Hallberg, B., Warne, P.H. and Downward, J. (1996) Networks of interaction of p120cbl and p130cas with Crk and Grb2 adaptor proteins. Oncogene, 12, 2491-2498.
26. King, W.G., Mattaliano, M.D., Chan, T.O., Tsichlis, P.N. and Brugge, J.S. (1997) Phosphatidylinositol 3-kinase is required for integrin-stimulaled AKT and Raf-1/mitogen-activated protein kinase pathway activation. Mol. Cell. Biol., 17, 4406-4418.
27. Li, JL., Avraham, H., Rogers, R.A., Raja, S. and Avraham, S. (1996) Characterization of RAFTK, a novel focal adhesion kinase and its integrin-dependent phosphorylation and activation in megakaryocytes. Blood, 88, 417-428.
28. Lin, T.H., Yurochko, A., Kornberg, L., Morris, J., Walker, J.J., Haskill, S. and Juliano, R.L. (1994) The role of protein tyrosine phosphorylation in integrin-mediated gene induction in monocytes. J. Cell. Biol., 126, 1585-1593.
29. Lin, T.H., Aplin, A.E., Shen, Y., Chen, Q., Schaller, M., Romer, L., Aukhil, I. and Juliano, R.L. (1997) Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J. Cell. Biol., 136, 1385-1395.
30. Lowe, C., Yoneda, T., Boyce, B.F., Chen, H., Mundy, G.R. and Soriano, P. (1993) Osteopetrosis in Src-deficient mice is due to an autonomous defect of osteoclasts. Proc. Natl Acad. Sci. USA, 90, 4485-1489.
31. Lowell, C.A. and Berton, G. (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.
32. Lowell, C.A., Soriano, P. and Varmus, H.E. (1994) Functional overlap in the src gene family: inactivation of hck and fgr impairs natural immunity. Genes Dev., 8, 387-398.
33. c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell. Biol., 133, 895-910.
34. Manie, S.N. et al. (1997) Tyrosine phosphorylation of the product of the c-cbl protooncogenes is induced after integrin stimulation. Exp. Hematol., 25, 45-50.
35. Marcilla, A., Rivero-Lezcano, O.M., Agarwal, A. and Robbins, K.C. (1995) Identification of the major tyrosine kinase substrate in signaling complexes formed after engagement of Fc gamma receptors. J. Biol. Chem., 270, 9115-9120.
36. Matsuo, T., Hazeki, K., Hazeki, O., Katada, T. and Ui, M. (1996) Specific association of phosphatidylinositol 3-kinase with the protooncogene product Cbl in Fc gamma receptor signaling. FEBS Lett., 382, 11-14.
37. Meng, F. and Lowell, C.A. (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.
38. erk-2. J. Biol. Chem., 270, 269-273.
39. Odai, H., Sasaki, K., Iwamatsu, A., Hanazono, Y., Tanaka, T., Mitani, K., Yazaki, Y. and Hirai, H. (1995) The proto-oncogene product c-Cbl becomes tyrosine phosphorylated by stimulation with GM-CSF or Epo and constitutively binds to the SH3 domain of Grb2/Ash in human hematopoietic cells. J. Biol. Chem., 270, 10800-10805.
40. cbl links c-Src and phosphatidylinositol 3′-kinase to the integrin signaling pathway. J. Biol. Chem., 272, 3780-3787.
41. Ota, Y. and Samelson, L.E. (1997) The product of the proto-oncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science, 276, 418-420.
42. cbl is a major substrate of tyrosine phosphorylation upon B cell antigen receptor stimulation and interacts in vivo with Fyn and Syk tyrosine kinases, Grb2 and She adaptors and the p85 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem., 271, 3187-3194.
43. Reddy, S.A., Huang, J.H. and Liao, W.S.-L. (1997) Phosphtidylinositol 3-kinase in interleukin 1 signaling. J. Biol. Chem., 272, 29167-29173.
44. Roach, T., Slater, S., Koval, M., White, L., McFarland, E.C., Okumura, M., Thomas, M. and Brown, E. (1997) CD45 regulates Src family member kinase activity associated with macrophage integrin-mediated adhesion. Curr. Biol., 7, 408-417.
45. 3 potentiate bone resorption. J. Biol. Chem., 268, 9901-9905.
46. CAS forms a signaling complex with the adapter protein CRKL in hematopoietic cells transformed by the BCR/ ABL oncogene. J. Biol. Chem., 271, 25198-25203.
47. Sambrook, J., Fritsch, E. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. HEF1. J. Biol. Chem., 272, 14320-14326.
49. Schaller, M.D. and Parsons, J.T. (1994) Focal adhesion kinase and associated proteins. Curr. Opin. Cell. Biol., 6, 705-710.
50. Shaw, L.M., Rabinovitz, I., Wang, H.H.F., Toker, A. and Mercurio, A.M. (1997) Activation of phosphoinositide 3-OH kinase by the α4β6 integrin promotes carcinoma invasion. Cell, 91, 949-960.
51. Smit, L., van der Horst, G. and Borst, J. (1996) Formation of Shc/Grb2-and Crk adaptor complexes containing tyrosine phosphorylated Cb1 upon stimulation of the B-cell antigen receptor. Oncogene, 13, 381-389.
52. Tanaka, S., Neff, L., Baron, R. and Levy, J.B. (1995) Tyrosine phosphorylation and translocation of the c-Cbl protein after activation of tyrosine kinase signaling pathways. J. Biol. Chem., 270, 14347-14351.
53. Tanaka, S., Amling, M., Neff, L., Peyman, A., Uhlmann, E., Levy, J.B. and Baron, R. (1996) c-Cbl is downstream of c-Src in a signalling pathway necessary for bone resorption. Nature, 383, 528-531.
54. Tezuka, T., Umemori, H., Fusaki, N., Yagi, T., Takata, M., Kurosaki, T. and Yamamoto, T. (1996) Physical and functional association of the cbl protooncogene product with an src-family protein tyrosine kinase, p53/561yn, in the B cell antigen receptor-mediated signaling. J. Exp. Med., 183, 675-680.
55. Thomas, S.M., Soriano, P. and Imamoto, A. (1995) Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature, 376, 267-271.
56. Toker, A. and Cantley, L.C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature, 387, 673-676.
57. Uddin, S., Gardziola, C., Dangat, A., Yi, T. and Platanias, L.C. (1996) Interaction of the c-cbl proto-oncogene product with the Tyk-2 protein tyrosine kinase. Biochem. Biophys. Res. Commun., 225, 833-838.
58. Ueno, H., Sasaki, K., Miyagawa, K., Honda, H., Mitani, K., Yazaki, Y. and Hirai, H. (1997) Antisense repression of proto-oncogene c-cbl enhances activation of the JAK-STAT pathway but not the Ras pathway in epidermal growth factor receptor signaling. J. Biol. Chem., 272, 8739-8743.
59. van der Pluijm, G., Mouthaan, H., Baas, C., de Groot, H., Papapoulos, S. and Lowik, C. (1994) Integrins and osteoclastic resorption in three bone organ cultures: differential sensitivity to synthetic Arg-Gly-Asp peptides during osteoclast formation. J. Bone Miner. Res., 9, 1021-1028.
60. Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem., 270, 22259-22262.
61. cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol., 16, 2606-2613.
62. Wang, Y., Yeung, Y.G., Langdon, W.Y. and Stanley, E.R. (1996) c-Cbl is transiently tyrosine-phosphorylated, ubiquitinated and membrane-targeted following CSF-1 stimulation of macrophages. J. Biol. Chem., 271, 17-20.
63. Xu, H., Gonzalo, J.A., St Pierre, Y. Williams, I.R., Kupper, T.S., Cotran, R.S., Springer, T.A. and Gutierrez-Ramos, J.C. (1994) Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J. Exp. Med., 180, 95-109.
64. lyn 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.
65. Yoon, C.H., Lee, J., Jongeward, G.D. and Sternberg, P.W. (1995) Similarity of sli-1, a regulator of vulval development in C.elegans. to the mammalian proto-oncogene c-cbl. Science, 269, 1102-1105.