The interaction of activated integrin lymphocyte function-associated antigen 1 with ligand intercellular adhesion molecule 1 induces activation and redistribution of focal adhesion kinase and proline-rich tyrosine kinase 2 in T lymphocytes

Molecular Biology of the Cell

Volumn 10, Issue 6, 1999, Pages 1891-1907

  Rodríguez Fernández, José Luis ^a   Gómez, Manuel ^b   Luque, Alfonso ^a   Hogg, Nancy ^c   Sánchez Madrid, Francisco ^b   Cabañas, Carlos ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; FOCAL ADHESION KINASE; GENISTEIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PROTEIN TYROSINE KINASE; TUBULIN;

ANTIGEN BINDING; ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LYMPHOBLAST; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS;

EID: 0242607362     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.6.1891     Document Type: Article

References (75)

1. FAK) expression correlates with motility of human melanoma cell lines. J. Invest. Dermatol. 105, 104-108.
2. Akiyama, S.K., Yamada, S.S., Yamada, K.M., and LaFlamme, S.E. (1994). Transmembrane signal transduction by integrin cytoplasmic domain expressed in single-subunit chimeras. J. Biol. Chem. 269, 15961-15964.
3. Akiyama, T., Ishida, J., Nakagawa, S., Ogawara, H., Watanabe, S.-i., Itoh, N., Shibuya, M., and Fukami, Y. (1987). Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262, 5592-5595.
4. Arroyo, A.G., Campanero, M.R., Sánchez-Mateos, P., Zapata, J.M., Ursa, M.A., del Pozo, M.A., and Sánchez-Madrid F. (1994). Induction of tyrosine phosphorylation during ICAM-1 and LFA-1 mediated intercellular adhesion and its regulation by CD45 tyrosine phosphatase. J. Cell Biol. 326, 1277-1286.
5. CAS. J. Biol. Chem. 272, 228-232.
6. Avraham, S., et al. (1995). Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol. Chem. 270, 27742-27751.
7. Berendt, A.R., McDowall, A., Craig, A.G., Bates, P.A., Stenberg, M.J.E., Marsh, K., Newbold, C.I., and Hogg, N. (1992). The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1 binding site. Cell 68, 71-81.
8. Cary, L.A., Chang, J.F., and Guan, J.-L. (1996). Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sci. 109, 1787-1794.
9. Clark, E.A., and Brugge, J.S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-139.
10. del Pozo, M.A., Cabañas, C., Montoya, M.C., Ager, A., Sánchez-Mateos, P., and Sánchez-Madrid, F. (1997). ICAMS redistributed by chemokines to cellular uropods as a mechanism for recruitment of T lymphocytes. J. Cell Biol. 137, 493-508.
11. del Pozo, M.A., Sánchez-Mateos, P., and Sánchez-Madrid, F. (1996). Cellular polarization induced by chemokines: a mechanism for leukocyte recruitment?. Immunol. Today 17, 127-131.
12. Dikic, I., Tokiwa, G., Lev, S., Courtneidge, S.A., and Schlessinger, J. (1996). A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383, 547-550.
13. Dransfield, I., Cabañas, C., Barrett, J., and Hogg, N. (1992a). Interaction of leukocyte integrins with ligand is necessary but not sufficient for function. J. Cell Biol. 116, 1527-1535.
14. Dransfield, I., Cabañas, C., Craig, A., and Hogg, N. (1992b). Divalent cation regulation of the function of the leukocyte integrin LFA-1. J. Cell Biol. 116, 219-226.
15. Dustin, M.L., Bromley, S.K., Kam, Z., Peterson, D.A., and Unanue, E.R. (1997). Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. USA 94, 3909-3913.
16. Earp, H.S., Huckle, W.R., Dawson, T.L., Li, X., Graves, L.M., and Dy, R. (1995). Angiotensin II activates at least two tyrosine kinases in rat liver epithelial cells. J. Biol. Chem. 270, 28440-28447.
17. Ganju, R.K., Hatch, W.C., Avraham, H., Ona, M.A., Druker, B., Avraham, S., and Groopman, J. (1997). RAFTK, a novel member of the focal adhesion kinase family, is phosphorylated and associates with signaling molecules upon activation of mature T lymphocytes. J. Exp. Med. 185, 1055-1063.
18. Gates, R.E., King, L.E., Jr., Hanks, S.K., and Nanney, L.B. (1994). Potential role for adhesion kinase in migrating and proliferating keratinocytes near epidermal wounds and in culture. Cell Growth & Differ. 5, 891-899.
19. Geiger, B., Rosen, D., and Berke, G. (1982). Spatial relationships of microtubule organizing center and the contact area of cytotoxic T lymphocytes and target cells. J. Cell Biol. 95, 137-143.
20. Gilmore, A.P., and Romer, L.H. (1996). Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell 7, 1209-1224.
21. Gismondi. A., Bisogno, L., Mainiero, F., Palmeri, G., Piccoli, M., Frati, L., and Santoni, A. (1997). Proline-rich tyrosine kinase-2 activation by β1 integrin fibronectin receptor cross-linking and association with paxillin in human natural killer cells. J. Immunol. 159, 4729-4736.
22. FAK both by cellular adhesion and by oncogene transformation. Nature 358, 690-692.
23. FAK by the aggregation of high affinity immunoglobulin E receptor requires cell adherence. J. Biol. Chem. 268, 6851-6854.
24. Hanks, S.K., Calalb, M.B., Harper, M.C., and Patel, S.K. (1992). Focal adhesion protein tyrosine kinase phosphorylated in response to cell spreading on fibronectin. Proc. Natl. Acad. Sci. USA 89, 8487-8491.
25. Hanks, S.K., and Polte, T.R. (1997). Signaling through focal adhesion kinase. Bioessays 19, 137-145.
26. Herzog, H., Nicholl, J., Hort, Y.J., Sutherland, G.R., and Shine, J. (1996). Molecular cloning and assignment of FAK2, a novel human focal adhesion kinase, to 8p11.2-p22, by nonisotopic in situ hybridization. Genomics 32, 484-486.
27. Hiregowdara, D., Avraham, H., Fy, Y., London, R., and Avraham, S. (1997). Tyrosine phosphorylation of the related adhesion tyrosine kinase (RAFTK) in megakaryocytes upon stem cell factor and PMA stimulation and its association with paxillin. J. Biol. Chem. 272, 10804-10810.
28. Ilic, D., et al. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
29. Kanner, S.B. (1996). Focal adhesion kinase-related fakB is regulated by the integrin LFA-1 and interacts with the SH3 domain of phospholipase Cγ1. Cell. Immunol. 171, 164-169.
30. Kanner, S.B., Aruffo, A., and Chan, P.-Y. (1994). Lymphocyte antigen receptor activation of a focal adhesion kinase-related tyrosine kinase substrate. Proc. Natl. Acad. Sci. USA 91, 10484-10487.
31. Kanner, S.B., Grosmaire, L.S., Ledbetter, J.A., and Damle, N.K. (1993). β2 integrin LFA-1 signaling through phospholipase C-γ-1 activation. Proc. Natl. Acad. Sci. USA 90, 7099-7103.
32. Kornberg, L.J., Earp, H.S., Turner, C.E., Prockop, C., and Juliano, R.L. (1991). Signal transduction by integrins: increased protein phosphorylation caused by integrin clustering. Proc. Natl. Acad. Sci. USA 88, 8392-8396.
33. Kupfer, A., Mosmann, T.R., and Kupfer, H. (1991). Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. USA 88, 775-779.
34. 2+-induced regulation of ion channel and MAP kinase functions. Nature 376, 737-745.
35. Ley, S.C., Verbi, W., Pappin, D.J., Druker, B., Davies, A.A., and Crumpton, M.J. (1994). Tyrosine phosphorylation of alpha tubulin in human T lymphocytes. Eur. J. Immunol. 24, 99-106.
36. Li, J., 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.
37. FAK in platelets. J. Cell Biol. 119, 905-912.
38. Lowin-Kropf, B., Shapiro, V.S., and Weiss, A. (1998). Cytoskeletal polarization of T cells is regulated by an immunoreceptor tyrosine-based activation motif-dependent mechanism. J. Cell Biol. 140, 861-871.
39. Lub, M., van Kooyk, Y., and Figdor, C.G. (1995). Ins and outs of LFA-1. Immunol. Today 16, 479-483.
40. Luque, A., Gómez, M., Puzon, W., Takada, Y., Sánchez-Madrid, F., and Cabañas, C. (1996). Activated conformations of VLA integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355-425) of the common β1 chain. J. Biol. Chem. 271, 11067-11075.
41. Ma, E.A., Lou, O., Berg, N.N., and Ostergaard, H.L. (1997). Cytotoxic T lymphocytes express a β3 integrin which can induce the phosphorylation of focal adhesion kinase and the related PYK-2. Eur. J. Immunol. 27, 329-335.
42. FAK) in human T cells. J. Exp. Med. 182, 2079-2090.
43. Marie-Cardine, A., Kirchgessner, H., Eckerskorn, C., Meuer, S.C., and Schraven, B. (1995). Human T lymphocyte activation induces tyrosine phosphorylation of alpha tubulin and its association with the SH2 domain of the p59fyn protein tyrosine kinase. Eur. J. Immunol. 25, 3290-3297.
44. FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269, 31807-31813.
45. CAS related proteins and GTPase-activating protein, graf. Biochem. J. 330, 1249-1254.
46. Ortlepp, S., Stephens, P.E., Hogg, N., Figdor, CC, and Robinson, M.K. (1995). Antibodies that activate β2 integrins can generate different ligand binding states signals. Eur. J. Immunol. 25, 637-643.
47. FAK in the focal adhesion. Int. Rev. Cytol. 167, 161-183.
48. Raja, S., Avraham, S., and Avraham, H. (1997). Tyrosine phosphorylation of the novel protein tyrosine kinase RAFTK during an early phase of platelet activation by an integrin glycoprotein gpIIb-IIIa-independent mechanism. J. Biol. Chem. 272, 10941-10947.
49. Ratner, S., Sherrod, W.S., and Lichlyter, D. (1997). Microtubule retraction into the uropod and its role in T cell polarization and motility. J. Immunol. 159, 1063-1067.
50. Richardson, A., and Parsons, T. (1995). Signal transduction through integrins: a central role for focal adhesion kinase? Bioessays 17, 229-236.
51. FAK. Nature 380, 538-540.
52. Rodríguez-Fernández, J.L., Geiger, B., Salomon, D., Sabanay, I., Zöller, M., and Ben-Ze'ev, A. (1992). Suppression of tumorigenicity in transformed cells transfected with vinculin cDNA. J. Cell Biol. 119, 427-438.
53. Rodríguez-Fernández, J.L., and Rozengurt, E. (1996). Bombesin, bradykinin, vasopressin, and phorbol esters rapidly and transiently activate Src family tyrosine kinases in Swiss 3T3 cells. J. Biol. Chem. 271, 27895-27901.
54. Rodríguez-Fernández, J.L., and Rozengurt, E. (1998). Bombesin, vasopressin, lysophosphatidic acid and sphingosylphosphorylcholine stimulate focal adhesion kinase activity in intact Swiss 3T3 cells. J. Biol. Chem. 273, 19321-19328.
55. Rothlein, R., and Springer, T.A. (1986). The requirement for LFA-1 in homotypic leukocyte adhesion stimulated by phorbol ester. J. Exp. Med. 163, 1132-1149.
56. Sanchez-Madrid, F., and del Pozo, M.A. (1999). Leukocyte polarization in cell migration and immune interactions. EMBO J. 18, 501-511.
57. Sasaki, H., Nagura, K., Ishino, M., Tobioka, H., Kotani, K., and Sasaki, T. (1995). Cloning and characterization of cell adhesion kinase β, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270, 21206-21219.
58. FAK, a structurally unique protein kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89, 5192-5196.
59. FAK. Mol. Cell. Biol. 13, 785-791.
60. Schaller, M.D., Otey, C.A., Hildebrand, J.D., and Parsons, J.T. (1995). Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domain. J. Cell Biol. 130, 1181-1187.
61. Schlaepfer, D.D., Jones, K.C., and Hunter, T. (1998). Multiple Grb-2-mediated integrin stimulated signaling pathways to ERK-2/mitogen-activated protein kinase: summation of both c-src-and focal adhesion kinase-initiated tyrosine phophorylation events. Mol. Cell. Biol. 18, 2571-2585.
62. Schwartz, M.A., Schaller, M.D., and Gingsberg, M.H. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell. Dev. Biol. 11, 549-599.
63. Serrador, J., Alonso-Lebrero, J.L., del Pozo, M.A., Furthmayr, H., Schwartz-Albiez, R., Calvo, J., Lozano, F., and Sánchez-Madrid, F. (1997). Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization. J. Cell Biol. 138, 1409-1423.
64. FAK requires coordinated signaling through integrin and agonist receptors. J. Biol. Chem. 269, 14738-14745.
65. Singer, S.J. (1992). Intercellular communication and cell-cell adhesion. Science 255, 1671-1677.
66. 2+ mobilization, and the actin cytoskeleton. J. Biol. Chem. 268, 14261-14268.
67. Springer, T.A. (1990). Adhesion receptors in the immune system. Nature 346, 425-434.
68. Stephens, P., Romer, J.T., Shock, A., Ortlepp, S., Figdor, C., and Robinson, M.K. (1995). KIM-127, an antibody that promotes adhesion, maps to a region of CD18 that includes cystein-rich repeats. Cell Adhes. Commun. 3, 375-384.
69. Stewart, M.P., Cabañas, C., and Hogg, N. (1996). T cell adhesion to intercercellular adhesion molecule-1 (ICAM-1) is controlled by spreading and by activation of integrin LFA-1. J. Immunol. 156, 1810-1817.
70. 2+-dependent epitope stimulates lymphocyte adhesion. J. Cell Biol. 112, 345-354.
71. Wacholtz, M.C., Patel, S.S., and Lipsky, P.E. (1989). Leukocyte function-associated antigen 1 is an activation molecule for human T cells. J. Exp. Med. 170, 431-448.
72. Wilkinson, P.C., and Higgins, A. (1987). OKT3-activated locomotion of human blood lymphocytes: a phenomenon requiring contact of T cells with Fc receptor-bearing cells. Immunology 60, 445-451.
73. Xiong, W.-C., and Parsons, J.T. (1997). Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J. Cell Biol. 139, 529-539.
74. 2+-dependent protein tyrosine kinase. Correlation with c-jun N-terminal kinase but not mitogen-activated protein kinase activation. J. Biol. Chem. 271, 29993-29998.
75. Zheng, C., Zheng, X., Bian, Z.C., Guo, C., Akbay, A., Warner, L., and Guan, J.-L. (1998). Differential regulation of Pyk2 and focal adhesion kinase (FAK). J. Biol. Chem. 273, 2384-2389.