Tyrosine 766 in the fibroblast growth factor receptor-1 is required for FGF-stimulation of phospholipase C, phospholipase D, phospholipase A2, phosphoinositide 3-kinase and cytoskeletal reorganisation in porcine aortic endothelial cells

Journal of Cell Science

Volumn 113, Issue 4, 2000, Pages 643-651

  Cross, Michael J ^a   Hodgkin, Matthew N ^b   Roberts, Sally ^b   Landgren, Eva ^a   Wakelam, Michael J O ^b   Claesson Welsh, Lena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Cytoskeleton; Fibroblast growth factor; Phospholipase

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; PHOSPHOLIPASE C; PHOSPHOLIPASE D; TYROSINE;

ANIMAL CELL; AORTA; ARTICLE; CELL PROLIFERATION; CELL SHAPE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; SWINE; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AORTA; CELL DIVISION; CELLS, CULTURED; CYTOSKELETON; ENDOTHELIUM, VASCULAR; MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PHOSPHOLIPASES; PHOSPHOLIPASES A; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; SWINE; TRANSFECTION; TYROSINE;

ANIMALIA; SUIDAE; SUS SCROFA;

EID: 0034009706     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Ahmed, A., Plevin, R., Shoaibi, M. A., Fountain, S. A., Ferriani, R. A. and Smith, S. K. (1994). Basic FGF activates phospholipase D in endothelial cells in the absence of inisitol-lipid hydrolysis. Am. J. Physiol. 266, C206-C212.
2. Chellaiah, M., Fitzgerald, C., Alvarez, U. and Hruska, K. (1998). C-Src is required for stimulation of gelsolin-associated phosphatidylinositol 3-kinase. J. Biol. Chem. 19, 11908-11916.
3. Claesson-Welsh, L., Eriksson, A., Moren, A., Severinsson, L., Ek, B., Östman, A., Betsholtz, C. and Heldin, C-H. (1988). cDNA cloning and expression of a human platelet-derived growth factor (PDGF) receptor specific for B-chain-containing PDGF molecules. Mol. Cell. Biol. 8, 3476-3486.
4. Clyman, R. I., Peters, K. G., Chen, Y. Q., Escobedo, J., Williams, L. T., Ives, H. E. and Wilson, E. (1994). Phospholipase C-γ activation, phosphotidylinositol hydrolysis, and calcium mobilization are not required for FGF receptor-mediated chemotaxis. Cell. Adhes. Commun. 1, 333-342.
5. Cook, S. J., Briscoe, C. P. and Wakelam, M. J. O. (1991). The regulation of phospholipase D activity and its role in sn-1,2-diradylglycerol formation in bombesin- and phorbol 12-myristate 13-acetate-stimulated Swiss 3T3 cells. Biochem. J. 280, 431-438.
6. Cross, M. J., Roberts, S., Ridley, A. J., Hodgkin, M. N., Stewart, A., Claesson-Welsh, L. and Wakelam, M. J. O. (1996). Stimulation of actin stress fibre formation mediated by activation of phospholipase D. Curr. Biol. 6, 588-597.
7. Divecha, N. and Irvine, R. F. (1995). Phospholipid signalling. Cell 80, 269-278.
8. Hall, H., Williams, E. J., Moore, S. E., Walsh, F. S., Prochiantz, A. and Doherty, P. (1996). Inhibition of FGF-stimulated phosphatidylinositol hydrolysis and neurite outgrowth by a cell-membrane permeable phosphopeptide. Curr. Biol. 6, 580-587.
9. Hartwig, J. H., Bokoch, G. M., Carpenter, C. L., Janmey, P. A., Taylor, L. A., Toker, A. and Stossel, T. P. (1995). Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82, 643-653.
10. Hawkins, P. T., Eguinoa, A., Qiu, R. G., Stokoe, D., Cooke, F. T., Walters, R., Wennström, S., Claesson-Welsh, L., Evans, T., Symons, M. and Stephens, L. R. (1995). PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr. Biol. 5, 393-403.
11. Hess, J. A., Ji, Q.-S., Carpenter, G. and Exton, J. H. (1998). Analysis of platelet-derived growth factor-induced phospholipase D activation in mouse embryo fibroblasts lacking phospholipase C-γ1. J. Biol. Chem. 273, 20517-20524.
12. Huang, J., Mohammadi, M., Rodrigues, G. A. and Schlessinger, J. (1995). Reduced activation of RAF-1 and MAP kinase by a fibroblast growth factor receptor mutant deficient in stimulation of phosphatidylinositol hydrolysis. J. Biol. Chem. 270, 5065-5072.
13. Jackson, T. R., Stephens, L. R. and Hawkins, P. T. (1992). Receptor specificity of growth-factor stimulated synthesis of 3-phosphorylated inositol lipids in Swiss 3T3 cells. J. Biol. Chem. 267, 16627-16636.
14. Janmey, P. A. (1994). Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56, 169-191.
15. Kodaki, T., Woscholski, R., Hallberg, B., Rodriguez-Viciana, P., Downward, J. and Parker, P. J. (1994) The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol. 4, 798-806.
16. Kouhara, H., Hadari, Y. R., Spivak-Kroizman, T., Schilling, J., Bar-Sagi, D., Lax, I. and Schlessinger, J. (1997). A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89, 693-702.
17. 2 is a 100-kDa protein in human monoblast U937 cells. J. Biol. Chem. 266, 5268-5272.
18. Landgren, E., Blume-Jensen, P., Courtneidge, S. A. and Claesson-Welsh, L. (1995). Fibroblast growth factor receptor-1 regulation of Src family kinases. Oncogene 10, 2027-2035.
19. Landgren, E., Klint, P., Yokote, K. and Claesson-Welsh, L. (1998). Fibroblast growth factor receptor-1 mediates chemotaxis independently of direct SH2-domain protein binding. Oncogene 17, 283-291.
20. Larsson, H., Klint, P., Landgren, E. and Claesson-Welsh, L. (1999). Fibroblast growth factor receptor-1-mediated endothelial cell proliferation is dependent on the Src homology (SH) SH2/SH3 domain-containing adaptor protein Crk. J. Biol. Chem. 274, 25726-25734.
21. 2 from a macrophage cell line, RAW 264.7. Biochim. Biophys. Acta 963, 476-492.
22. Lu, P.-J., Shieh, W.-R., Rhee, S. G., Yin, H. L. and Chen, C.-H. (1996). Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity. Biochemistry. 35, 14027-14034.
23. Mohammadi, M., Dikic, I., Sorokin, A., Burgess, W. H., Jaye, M. and Schlessinger, J. (1996). Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol. Cell. Biol. 16, 977-989.
24. Mohammadi, M., Dionne, C. A., Li, W., Li, N., Spivak, T., Honegger, A. M., Jaye, M. and Schlessinger, J. (1992). Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 358, 681-684.
25. Mohammadi, M., Honegger, A. M., Rotin, D., Fischer, R., Bellot, F., Li, W., Dionne, C. A., Jaye, M., Rubinstein, M. and Schlessinger, J. (1991). A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor (FIg) is a binding site for the SH2 domain of phospholipase C-y1. Mol. Cell. Biol. 11, 5068-5078.
26. Molloy, C. J., Bottaro, D. P., Fleming, M. S., Gibbs, J. B. and Aaronson, S.A. (1989). PDGF induction of tyrosine phosphorylation of the GTPase activating protein. Nature 342, 711-714.
27. 2 by p42 microtubule-associated protein 2 kinase and protein kinase C. J. Biol. Chem. 268, 1960-1964.
28. Peppelenbosch, M. P., Qiu, R. G., de Vries-Smits, A. M., Tertoolen, L. G., de Laat, S. W., McCormick, F., Hall, A., Symons, M. H. and Bos, J. L. (1995). Rac mediates growth factor-induced arachidonic acid release. Cell 81, 849-856.
29. 2+ flux but not mitogenesis. Nature 358, 678-681.
30. Plevin, R., Palmer, S., Gardner, S. and Wakelam, M. J. O. (1990). Regulation of bombesin-stimulated inositol 1,4,5-trisphosphate generation in Swiss 3713 fibroblasts by a guanine-nucleotide binding protein. Biochem. J. 268 605-610.
31. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-bindmg protein rac regulates growth factor-induced membrane ruffling. Cell. 70, 401-410.
32. Rodriguez-Viciana, P., Warne, P. H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M. J., Waterfield, M. D. and Downward, J. (1994). Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370, 527-532
33. 2 activity. J. Biol. Chem. 269, 3219-3222.
34. Songyang, Z., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. C., King, F., Roberts, T., Ratnofsky, S., Lechleider, R. J. et al. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
35. Sorokin, A., Mohammadi, M., Huang, J. and Schlessinger, J. (1994). Internalization of fibroblast growth factor receptor is inhibited by a point mutation at tyrosine 766. J. Biol. Chem. 269, 17056-17061.
36. Spivak-Kroizman, T., Mohammadi, M., Hu, P., Jaye, M., Schlessinger, J. and Lax, I. (1994). Point mutation in the fibroblast growth factor receptor eliminates phosphatidylinositol hydrolysis without affecting neuronal differentiation of PC12 cells. J. Biol. Chem. 269, 14419-14423.
37. Stephens, L. R., Jackson, T. R. and Hawkins, P. T. (1993). Agonist-stimulated synthesis of phosphatidylinositol(3,4,5)-trisphosphate: a new intracellular signalling system? Biochim. Biophys. Acta 1179, 27-75.
38. 2 activity in the neutrophil model system, differentiated HL60 cells. Br. J. Pharmacol. 122, 13-20.
39. Toullec, D., Pianetti, P., Coste, H., Bellevergue, P., Grand-Perett, T., Ajakane, M., Baudet, V., Boissin, P., Boursier, E., Loriolle, F., Duhamel, L., Charon, D. and Kirilovsky, J. (1991). The bisindolymaleimide GF 109203X is a potent and selective inhibitor of Protein Kinase C. J. Biol.Chem. 266, 15771-15781.
40. Ullrich, A. and Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212.
41. Vainikka, S., Joukov, V., Wennström, S., Bergman, M., Pelicci, P. G. and Alitalo, K. (1994). Signal transduction by fibroblast growth factor receptor-4 (FGFR-4). Comparison with FGFR-1. J. Biol. Chem. 269, 18320-18326.
42. van Dijk, M. C. and van Blitterswijk, W. J. (1998). Lipid metabolism in fibroblast growth factor-stimulated L6 myoblasts: a receptor mutation (Y766F) abrogates phospholipase D and diacylglycerol kinase activities. Biochim. Biophys. Acta 1391, 273-279.
43. van Weering, D. H., de Rooij, J., Marte, B., Downward, J., Bos, J. L. and Burgering, B. M. (1998). Protein kinase B activation and lamellipodium formation are independent phosphoinositide 3-kinase-mediated events differentially regulated by endogenous Ras. Mol. Cell. Biol. 18, 1802-1811.
44. Virdee, K., Brown, B. L. and Dobson, P. R. (1994). Stimulation of arachidonic-acid release from Swiss 3T3 cells by recombinant basic fibroblast growth factor: independence from phosphoinositide turnover. Biochim. Biophys. Acta 1220, 171-180.
45. Wennström, S., Hawkins, P., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L. and Stephens, L. (1994). Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
46. Wennström, S., Landgren, E., Blume-Jensen, P. and Claesson-Welsh, L. (1992). The platelet-derived growth factor β-receptor kinase insert confers specific signaling properties to a chimeric fibroblast growth factor receptor. J. Biol. Chem. 267, 13749-13756.
47. Wennström, S., Sandström, C. and Claesson-Welsh, L. (1991). cDNA cloning and expression of a human FGF receptor which binds acidic and basic FGF. Growth Factors 4, 197-208.
48. Wong, N. S., Barker, C. J., Morris, A. J., Craxton, A., Kirk, C. J. and Michell, R. H. (1992). The inositol phosphates in WRK1 rat mammary tumour cells. Biochem. J. 286, 459-468.
49. Xu, H., Lee, K. W. and Goldfarb, M. (1998). Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J. Biol. Chem. 273, 17987-17990.
50. Yeo, E. J., Kazlauskas, A. and Exton, J. H. (1994). Activation of phospholipase C-γ is necessary for stimulation of phospholipase D by platelet-derived growth factor. J. Biol. Chem. 269, 27823-27826.