Vav1 and Rac control chemokine-promoted T lymphocyte adhesion mediated by the integrin α4β1

Molecular Biology of the Cell

Volumn 16, Issue 7, 2005, Pages 3223-3235

  García Bernal, David ^a   Wright, Natalia ^a   Sotillo Mallo, Elena ^a   Nombela Arrieta, César ^b,d   Stein, Jens V ^b,d   Bustelo, Xosé R ^c   Teixidó, Joaquin ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b PFIZER INC   (United States)

^c CSIC   (Spain)

^d UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; GUANOSINE TRIPHOSPHATASE; RAC PROTEIN; SMALL INTERFERING RNA; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; VAV PROTEIN; VAV1 PROTEIN; VERY LATE ACTIVATION ANTIGEN 4;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIGAND BINDING; LYMPHOCYTE MIGRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

BLOTTING, WESTERN; CELL ADHESION; CELL LINE; CELL MOVEMENT; CHEMOKINES; CHEMOKINES, CXC; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOTHELIUM, VASCULAR; GENES, DOMINANT; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HUMANS; IMMUNOPRECIPITATION; INTEGRIN ALPHA4BETA1; LIGANDS; LYMPHOCYTES; MICROSCOPY, CONFOCAL; PROTO-ONCOGENE PROTEINS C-VAV; RAC GTP-BINDING PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; T-LYMPHOCYTES; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 21844460502     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-12-1049     Document Type: Article

References (66)

1. Aghazadeh, B., Lowry, W. E., Huang, X. Y., and Rosen, M. K. (2000). Structural basis for relief of autoinhibition of the Dbl homology domain of protooncogene Vav by tyrosine phosphorylation. Cell 102, 625-633.
2. Arthur, W. T., Quilliam, L. A., and Cooper, J. A. (2004). Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J. Cell Biol. 167, 111-122.
3. Bartolome, R. A., Sanz-Rodriguez, F., Robledo, M. M., Hidalgo, A., and Teixido, J. (2003). Rapid up-regulation of alpha4 integrin-mediated leukocyte adhesion by transforming growth factor-beta1. Mol. Biol. Cell 14, 54-66.
4. Burridge, K., and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
5. Bustelo, X. R. (2000). Regulatory and signaling properties of the Vav family. Mol. Cell. Biol. 20, 1461-1477.
6. Butcher, E. C., and Picker, L. J. (1996). Lymphocyte homing and homeostasis. Science 272, 60-66.
7. Caloca, M. J., Zugaza, J. L., Vicente-Manzanares, M., Sanchez-Madrid, F., and Bustelo, X. R. (2004). F-Actin-dependent translocation of the Rap1 GDP/GTP exchange factor RasGRP2. J. Biol. Chem. 279, 20435-20446.
8. Carman, C. V., and Springer, T. A. (2003). Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr. Opin. Cell Biol. 15, 547-556.
9. Chan, J. R., Hyduk, S. J., and Cybulsky, M. I. (2001). Chemoattractants induce a rapid and transient up-regulation of monocyte alpha4 integrin affinity for vascular cell adhesion molecule 1 which mediates arrest: an early step in the process of emigration. J. Exp. Med. 193, 1149-1158.
10. Crespo, P., Schuebel, K. E., Ostrom, A. A., Gutkind, J. S., and Bustelo, X. R. (1997). Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 385, 169-172.
11. del Pozo, M. A., Price, L. S., Alderson, N. B., Ren, X. D., and Schwartz, M. A. (2000). Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19, 2008-2014.
12. del Pozo, M. A., Schwartz, M. A., Hu, J., Kiosses, W. B., Altman, A., and Villalba, M. (2003). Guanine exchange-dependent and -independent effects of Vav1 on integrin-induced T cell spreading. J. Immunol. 170, 41-47.
13. Deroanne, C., Vouret-Craviari, V., Wang, B., and Pouyssegur, J. (2003). EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J. Cell Sci. 116, 1367-1376.
14. Deroanne, C. F., Hamelryckx, D., Ho, T. T., Lambert, C. A., Catroux, P., Lapiere, C. M., and Nusgens, B. V. (2005). Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway. J. Cell Sci. 118, 1173-1183.
15. D'Souza-Schorey, C., Boettner, B., and Van Aelst, L. (1998). Rac regulates integrin-mediated spreading and increased adhesion of T lymphocytes. Mol. Cell. Biol. 18, 3936-3946.
16. Ebnet, K., Kaldjian, E. P., Anderson, A. O., and Shaw, S. (1996). Orchestrated information transfer underlying leukocyte endothelial interactions. Annu. Rev. Immunol. 14, 155-177.
17. Emsley, J., Knight, C. G., Farndale, R. W., Barnes, M. J., and Liddington, R. C. (2000). Structural basis of collagen recognition by integrin alpha2beta1. Cell 101, 47-56.
18. Etienne-Manneville, S., and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
19. Feig, L. A. (1999). Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat. Cell Biol. 1, E25-E27.
20. Fischer, K. D. et al. (1998). Vav is a regulator of cytoskeletal reorganization mediated by the T-cell receptor. Curr. Biol. 8, 554-562.
21. Gakidis, M. A., Cullere, X., Olson, T., Wilsbacher, J. L., Zhang, B., Moores, S. L., Ley, K., Swat, W., Mayadas, T., and Brugge, J. S. (2004). Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. J. Cell Biol. 166, 273-282.
22. Gomez, M., Tybulewicz, V., and Cantrell, D. A. (2000). Control of pre-T cell proliferation and differentiation by the GTPase Rac-1. Nat. Immunol. 1, 348-352.
23. Grabovsky, V. et al. (2000). Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J. Exp. Med. 192, 495-506.
24. Gu, Y. et al. (2003). Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302, 445-449.
25. Jakubowski, A., Rosa, M. D., Bixler, S., Lobb, R., and Burkly, L. C. (1995). Vascular cell adhesion molecule (VCAM)-immunoglobulin fusion protein defines distinct affinity states of the very late antigen-4 (VLA-4) receptor. Cell Adhes. Commun. 3, 131-142.
26. Katagiri, K., Shimonaka, M., and Kinashi, T. (2004). Rap1-mediated lymphocyte function-associated antigen-1 activation by the T cell antigen receptor is dependent on phospholipase C-gamma1. J. Biol. Chem. 279, 11875-11881.
27. Kim, M., Carman, C. V., and Springer, T. A. (2003). Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 301, 1720-1725.
28. Kinbara, K., Goldfinger, L. E., Hansen, M., Chou, F. L., and Ginsberg, M. H. (2003). Ras GTPases: integrins' friends or foes? Nat. Rev. Mol. Cell. Biol. 4, 767-776.
29. Krawczyk, C., Oliveira-dos-Santos, A., Sasaki, T., Griffiths, E., Ohashi, P. S., Snapper, S., Alt, F., and Penninger, J. M. (2002). Vav1 controls integrin clustering and MHC/peptide-specific cell adhesion to antigen-presenting cells. Immunity 16, 331-343.
30. Liddington, R. C., and Ginsberg, M. H. (2002). Integrin activation takes shape. J. Cell Biol. 158, 833-839.
31. Liu, S., Calderwood, D. A., and Ginsberg, M. H. (2000). Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113(Pt 20), 3563-3571.
32. Lopez-Lago, M., Lee, H., Cruz, C., Movilla, N., and Bustelo, X. R. (2000). Tyrosine phosphorylation mediates both activation and downmodulation of the biological activity of Vav. Mol. Cell. Biol. 20, 1678-1691.
33. Maillet, M., Robert, S. J., Cacquevel, M., Gastineau, M., Vivien, D., Bertoglio, J., Zugaza, J. L., Fischmeister, R., and Lezoualc'h, F. (2003). Crosstalk between Rap1 and Rac regulates secretion of sAPPalpha. Nat. Cell Biol. 5, 633-639.
34. Matsuguchi, T., Inhorn, R. C., Carlesso, N., Xu, G., Druker, B., and Griffin, J. D. (1995). Tyrosine phosphorylation of p95Vav in myeloid cells is regulated by GM-CSF, IL-3 and steel factor and is constitutively increased by p210BCR/ ABL. EMBO J. 14, 257-265.
35. Moores, S. L., Selfors, L. M., Fredericks, J., Breit, T., Fujikawa, K., Alt, F. W., Brugge, J. S., and Swat, W. (2000). Vav family proteins couple to diverse cell surface receptors. Mol. Cell. Biol. 20, 6364-6373.
36. Mould, A. P., Askari, J. A., Craig, S. E., Garratt, A. N., Clements, J., and Humphries, M. J. (1994). Integrin alpha 4 beta 1-mediated melanoma cell adhesion and migration on vascular cell adhesion molecule-1 (VCAM-1) and the alternatively spliced IIICS region of fibronectin. J. Biol. Chem. 269, 27224-27230.
37. Munoz, M., Serrador, J., Sanchez-Madrid, F., and Teixido, J. (1996). A region of the integrin VLA alpha 4 subunit involved in homotypic cell aggregation and in fibronectin but not vascular cell adhesion molecule-1 binding. J. Biol. Chem. 271, 2696-2702.
38. Nishita, M., Aizawa, H., and Mizuno, K. (2002). Stromal cell-derived factor 1alpha activates LIM kinase 1 and induces cofilin phosphorylation for T-cell chemotaxis. Mol. Cell. Biol. 22, 774-783.
39. Reedquist, K. A., Ross, E., Koop, E. A., Wolthuis, R. M., Zwartkruis, F. J., van Kooyk, Y., Salmon, M., Buckley, C. D., and Bos, J. L. (2000). The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 148, 1151-1158.
40. Reynolds, L. F., Smyth, L. A., Norton, T., Freshney, N., Downward, J., Kioussis, D., and Tybulewicz, V. L. (2002). Vav1 transduces T cell receptor signals to the activation of phospholipase C-gamma1 via phosphoinositide 3-kinase-dependent and -independent pathways. J. Exp. Med. 195, 1103-1114.
41. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T., and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
42. Rose, D. M., Han, J., and Ginsberg, M. H. (2002). Alpha4 integrins and the immune response. Immunol. Rev. 186, 118-124.
43. Sanchez-Madrid, F., and del Pozo, M. A. (1999). Leukocyte polarization in cell migration and immune interactions. EMBO J. 38, 501-511.
44. Sander, E. E., van Delft, S., ten Klooster, J. P., Reid, T., van der Kammen, R. A., Michiels, F., and Collard, J. G. (1998). Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143, 1385-1398.
45. Schmidt, A., and Hall, A. (2002). Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16, 1587-1609.
46. Schuebel, K. E., Movilla, N., Rosa, J. L., and Bustelo, X. R. (1998). Phosphorylation-dependent and constitutive activation of Rho proteins by wild-type and oncogenic Vav-2. EMBO J. 17, 6608-6621.
47. Sebzda, E., Bracke, M., Tugal, T., Hogg, N., and Cantrell, D. A. (2002). Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat. Immunol. 3, 251-258.
48. Shimaoka, M. et al. (2003). Structures of the alpha L 1 domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112, 99-111.
49. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O., and Kinashi, T. (2003). Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 161, 417-427.
50. Springer, T. A. (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301-314.
51. Stein, J. V., Soriano, S. F., M'Rini, C., Nombela-Arrieta, C., de Buitrago, G. G., Rodriguez-Frade, J. M., Mellado, M., Girard, J. P., and Martinez, A. C. (2003). CCR7-mediated physiological lymphocyte homing involves activation of a tyrosine kinase pathway. Blood 101, 38-44.
52. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H., and Calderwood, D. A. (2003). Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106.
53. Takagi, J., Petre, B. M., Walz, T., and Springer, T. A. (2002). Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110, 599-611.
54. Ticchioni, M., Charvet, C., Noraz, N., Lamy, L., Steinberg, M., Bernard, A., and Deckert, M. (2002). Signaling through ZAP-70 is required for CXCL12-mediated T-cell transendothelial migration. Blood 99, 3111-3118.
55. Turner, M., and Billadeau, D. D. (2002). VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2, 476-486.
56. Tybulewicz, V. L., Ardouin, L., Frisco, A., and Reynolds, L. F. (2003). Vav1, a key signal transducer downstream of the TCR. Immunol. Rev. 192, 42-52.
57. Vila-Coro, A. J., Rodriguez-Frade, J. M., Martin De Ana, A., Moreno-Ortiz, M. C., Martinez, A. C., and Mellado, M. (1999). The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. 13, 1699-1710.
58. Vinogradova, O., Vaynberg, J., Kong, X., Haas, T. A., Plow, E. F., and Qin, J. (2004). Membrane-mediated structural transitions at the cytoplasmic face during integrin activation. Proc. Natl. Acad. Sci. USA 101, 4094-4099.
59. Vinogradova, O., Velyvis, A., Velyviene, A., Hu, B., Haas, T., Plow, E., and Qin, J. (2002). A structural mechanism of integrin alpha(IIb)beta(3) "inside-out" activation as regulated by its cytoplasmic face. Cell 110, 587-597.
60. von Andrian, U. H., and Mackay, C. R. (2000). T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 343, 1020-1034.
61. Worthylake, R. A., and Burridge, K. (2001). Leukocyte transendothelial migration: orchestrating the underlying molecular machinery. Curr. Opin. Cell Biol. 13, 569-577.
62. Wright, N., Hidalgo, A., Rodriguez-Frade, J. M., Soriano, S. F., Mellado, M., Parmo-Cabanas, M., Briskin, M. J., and Teixido, J. (2002). The chemokine stromal cell-derived factor-1 alpha modulates alpha 4 beta 7 integrin-mediated lymphocyte adhesion to mucosal addressin cell adhesion molecule-1 and fibronectin. J. Immunol. 168, 5268-5277.
63. Xiong, J. P., Stehle, T., Diefenbach, B., Zhang, R., Dunker, R., Scott, D. L., Joachimiak, A., Goodman, S. L., and Arnaout, M. A. (2001). Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science 294, 339-345.
64. Yang, F. C., Atkinson, S. J., Gu, Y., Borneo, J. B., Roberts, A. W., Zheng, Y., Pennington, J., and Williams, D. A. (2001). Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc. Natl. Acad. Sci. USA 98, 5614-5618.
65. Yron, I., Deckert, M., Reff, M. E., Munshi, A., Schwartz, M. A., and Altman, A. (1999). Integrin-dependent tyrosine phosphorylation and growth regulation by Vav. Cell Adhes. Commun. 7, 1-11.
66. Zugaza, J. L., Lopez-Lago, M. A., Caloca, M. J., Dosil, M., Movilla, N., and Bustelo, X. R. (2002). Structural determinants for the biological activity of Vav proteins. J. Biol. Chem. 277, 45377-45392.