Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: Role of Src and GIT

FASEB Journal

Volumn 17, Issue 15, 2003, Pages 2240-2249

  Shikata, Yasushi ^a   Birukov, Konstantin G ^a   Birukova, Anna A ^a   Verin, Alexander ^a   Garcia, Joe G N ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Barrier function; Cytoskeleton; Human pulmonary artery endothelium

Indexed keywords

F ACTIN; FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE INTERACTING PROTEIN; GIT1 PROTEIN; GIT2 PROTEIN; PAXILLIN; PROTEIN; SPHINGOSINE 1 PHOSPHATE; THROMBIN; UNCLASSIFIED DRUG; YTTRIUM;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; LUNG ARTERY; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE PROTEINS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; CYTOSKELETON; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GTPASE-ACTIVATING PROTEINS; HUMANS; LYSOPHOSPHOLIPIDS; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS PP60(C-SRC); PYRIMIDINES; SPHINGOSINE; THROMBIN; TYROSINE;

EID: 0345529916     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.03-0198com     Document Type: Article

References (50)

1. Borbiev, T., Verin, A. D., Shi, S., Liu, F., and Garcia, J. G. (2001) Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. Am. J. Physiol. 280, L983-L990
2. Macfarlane, S. R., Seatter, M. J., Kanke, T., Hunter, G. D., and Plevin, R. (2001) Proteinase-activated receptors. Pharmacol. Rev. 53, 245-282
3. Garcia, J. G., Fenton, J. W., II, and Natarajan, V. (1992) Thrombin stimulation of human endothelial cell phospholipase D activity. Regulation by phospholipase C, protein kinase C, and cyclic adenosine 3′5′ -monophosphate. Blood 79, 2056-2067
4. Garcia, J. G., Stasek, J., Natarajan, V., Patterson, C. E., and Dominguez, J. (1992) Role of protein kinase C in the regulation of prostaglandin synthesis in human endothelium. Am. J. Respir. Cell Mol. Biol. 6, 315-325
5. Garcia, J. G., Lazar, V., Gilbert-McClain, L. I., Gallagher, P. J., and Verin, A. D. (1997) Myosin light chain kinase in endothelium: molecular cloning and regulation. Am. J. Respir. Cell Mol. Biol. 16, 489-494
6. Garcia, J. G., Davis, H. W., and Patterson, C. E. (1995) Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J. Cell. Physiol. 163, 510-522
7. Patterson, C. E., Davis, H. W., Schaphorst, K. L., and Garcia, J. G. (1994) Mechanisms of cholera toxin prevention of thrombin- and PMA-induced endothelial cell barrier dysfunction. Microvasc. Res. 48, 212-235
8. Dudek, S. M., and Garcia, J. G. (2001) Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91, 1487-1500
9. Lum, H., and Malik, A. B. (1996) Mechanisms of increased endothelial permeability. Can. J. Physiol. Pharmacol. 74, 787-800
10. Gimbrone, M. A., Jr., Aster, R. H., Cotran, R. S., Corkery, J., Jandl, J. H., and Folkman, J. (1969) Preservation of vascular integrity in organs perfused in vitro with a platelet-rich medium. Nature (London) 221, 33-36
11. Roy, A. J., and Djerassi, I. (1972) Effects of platelet transfusions: plug formation and maintenance of vascular integrity. Proc. Soc. Exp. Biol. Med. 139, 137-142
12. Lo, S. K., Burhop, K. E., Kaplan, J. E., and Malik, A. B. (1988) Role of platelets in maintenance of pulmonary vascular permeability to protein. Am. J. Physiol. 254, H763-H771
13. Shepro, D., Welles, S. L., and Hechtman, H. B. (1984) Vasoactive agonists prevent erythrocyte extravasation in thrombocytopenic hamsters. Thromb. Res. 35, 421-430
14. McDonagh, P. F. (1986) Platelets reduce coronary microvascular permeability to macromolecules. Am. J. Physiol. 251, H581-H587
15. An, S., Zheng, Y., and Bleu, T. (2000) Sphingosine 1-phosphate-induced cell proliferation, survival, and related signaling events mediated by G protein-coupled receptors Edg3 and Edg5. J. Biol. Chem. 275, 288-296
16. English, D., Garcia, J. G., and Brindley, D. N. (2001) Platelet-released phospholipids link haemostasis and angiogenesis. Cardiovasc. Res. 49, 588-599
17. Goetzl, E. J., and An, S. (1998) Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 12, 1589-1598
18. Hisano, N., Yatomi, Y., Satoh, K., Akimoto, S., Mitsumata, M., Fujino, M. A., and Ozaki, Y. (1999) Induction and suppression of endothelial cell apoptosis by sphingolipids: a possible in vitro model for cell-cell interactions between platelets and endothelial cells. Blood 93, 4293-4299
19. Lee, M. J., Thangada, S., Claffey, K. P., Ancellin, N., Liu, C. H., Kluk, M., Volpi, M., Sha'afi, R. I., and Hla, T. (1999) Vascular endothelial cell adherensjunction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99, 301-312
20. Yatomi, Y., Ruan, F., Ohta, J., Welch, R. J., Hakomori, S., and Igarashi, Y. (1995) Quantitative measurement of sphingosine 1-phosphate in biological samples by acylation with radioactive acetic anhydride. Anal. Biochem. 230, 315-320
21. Murata, N., Sato, K., Kon, J., Tomura, H., and Okajima, F. (2000) Quantitative measurement of sphingosine 1-phosphate by radioreceptor-binding assay. Anal. Biochem. 282, 115-120
22. Panetti, T. S. (2002) Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim. Biophys. Acta 1582, 190-196
23. Lee, M. J., Van Brocklyn, J. R., Thangada, S., Liu, C. H., Hand, A. R., Menzeleev, R., Spiegel, S., and Hla, T. (1998) Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279, 1552-1555
24. Wang, F., Van Brocklyn, J. R., Hobson, J. P., Movafagh, S., Zukowska-Grojec, Z., Milstien, S., and Spiegel, S. (1999) Sphingosine 1-phosphate stimulates cell migration through a G(i)-coupled cell surface receptor. Potential involvement in angiogenesis. J. Biol. Chem. 274, 35343-35350
25. Garcia, J. G., Liu, F., Verin, A. D., Birukova, A., Dechert, M. A., Gerthoffer, W. T., Bamberg, J. R., and English, D. (2001) Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108, 689-701
26. Sastry, S. K., and Burridge, K. (2000) Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261, 25-36
27. Birge, R. B., Fajardo, J. E., Reichman, C., Shoelson, S. E., Songyang, Z., Cantley, L. C., and Hanafusa, H. (1993) Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-phosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13, 4648-4656
28. Salgia, R., Li, J. L., Lo, S. H., Brunkhorst, B., Kansas, G. S., Sobhany, E. S., Sun, Y., Pisick, E., Hallek, M., Ernst, T., et al. (1995) Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by P210BCR/ABL. J. Biol. Chem. 270, 5039-5047
29. Turner, C. E., and Miller, J. T. (1994) Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J. Cell Sci. 107, 1583-1591
30. Turner, C. E., Glenney, J. R., Jr., and Burridge, K. (1990) Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111, 1059-1068
31. Weng, Z., Taylor, J. A., Turner, C. E., Brugge, J. S., and Seidel-Dugan, C. (1993) Detection of Src homology 3-binding proteins, including paxillin, in normal and v-Src-transformed Balb/c 3T3 cells. J. Biol. Chem. 268, 14956-14963
32. Wood, C. K., Turner, C. E., Jackson, P., and Critchley, D. R. (1994) Characterisation of the paxillin-binding site and the C-terminal focal adhesion targeting sequence in vinculin. J. Cell Sci. 107, 709-717
33. Bellis, S. L., Miller, J. T., and Turner, C. E. (1995) Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270, 17437-17441
34. Brown, M. C., Perrotta, J. A., and Turner, C. E. (1998) Serine and threonine phosphorylation of the paxillin LIM domains regulates paxillin focal adhesion localization and cell adhesion to fibronectin. Mol. Biol. Cell 9, 1803-1816
35. Schaller, M. D., and Parsons, J. T. (1995) pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15, 2635-2645
36. Turner, C. E. (1998) Paxillin. Int. J. Biochem. Cell Biol. 30, 955-959
37. Schaller, M. D. (2001) Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 1540, 1-21
38. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature (London) 377, 539-544
39. Ren, X. D., Kiosses, W. B., Sieg, D. J., Otey, C. A., Schlaepfer, D. D., and Schwartz, M. A. (2000) Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113, 3673-3678
40. Turner, C. E., West, K. A., and Brown, M. C. (2001) Paxillin-ARF GAP signaling and the cytoskeleton. Curr. Opin. Cell Biol. 13, 593-599
41. Mazaki, Y., Hashimoto, S., Okawa, K., Tsubouchi, A., Nakamura, K., Yagi, R., Yano, H., Kondo, A., Iwamatsu, A., Mizoguchi, A., et al. (2001) An ADP-ribosylation factor GTPase-activating protein Git2-short/KIAA0148 is involved in subcellular localization of paxillin and actin cytoskeletal organization. Mol. Biol. Cell 12, 645-662
42. West, K. A., Zhang, H., Brown, M. C., Nikolopoulos, S. N., Riedy, M. C., Horwitz, A. F., and Turner, C. E. (2001) The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J. Cell Biol. 154, 161-176
43. Zhao, Z. S., Manser, E., Loo, T. H., and Lim, L. (2000) Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20, 6354-6363
44. Shikata, Y., Birukov, K. G., and Garcia, J. G. (2003) S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK and paxillin. J. Appl. Physiol. 94, 1193-1203
45. Shikata, Y., Shikata, K., Matsuda, M., Sugimoto, H., Wada, J., and Makino, H. (1999) Signaling transduction pathway of angiotensin II in human mesangial cells: mediation of focal adhesion and GTPase activating proteins. Biochem. Biophys. Res. Commun. 257, 234-238
46. Wang, F., Nobes, C. D., Hall, A., and Spiegel, S. (1997) Sphingosine 1-phosphate stimulates rho-mediated tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 fibroblasts. Biochem. J. 324, 481-488
47. Vouret-Craviari, V., Bourcier, C., Boulter, E., and van Obberghen-Schilling, E. (2002) Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J. Cell Sci. 115, 2475-2484
48. Fincham, V. J., Wyke, J. A., and Frame, M. C. (1995) v-Src-induced degradation of focal adhesion kinase during morphological transformation of chicken embryo fibroblasts. Oncogene 10, 2247-2252
49. Parsons, J. T., Martin, K. H., Slack, J. K., Taylor, J. M., and Weed, S. A. (2000) Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606-5613
50. Parsons, J. T. (2003) Focal adhesion kinase: the first ten years. J. Cell Sci. 116, 1409-1416