RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation

Molecular and Cellular Biology

Volumn 27, Issue 11, 2007, Pages 4070-4081

  Ménasché, Gaël ^a   Kliche, Stefanie ^b   Chen, Emily J H ^a   Stradal, Theresia E B ^c   Schraven, Burkhart ^b   Koretzky, Gary ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION AND DEGRANULATION PROMOTING ADAPTER PROTEIN; INTEGRIN; PROTEIN DERIVATIVE; RAP1 PROTEIN; SRC KINASE ASSOCIATED PHOSPHOPROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CONJUGATION; CONTROLLED STUDY; GENE MAPPING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL ADHESION; CELL LINE; HUMANS; INTEGRINS; MEMBRANE PROTEINS; MICE; PHOSPHOPROTEINS; PROTEIN BINDING; RAP1 GTP-BINDING PROTEINS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 34347337643     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02011-06     Document Type: Article

References (43)

1. Bazzoni, G., and M. E. Hemler. 1998. Are changes in integrin affinity and conformation overemphasized? Trends Biochem. Sci. 23:30-34.
2. Bivona, T. G., H. H. Wiener, I. M. Ahearn, J. Silletti, V. K. Chiu, and M. R. Philips. 2004. Rap1 up-regulation and activation on plasma membrane regulates T cell adhesion. J. Cell Biol. 164:461-470.
3. Boerth, N. J., B. A. Judd, and G. A. Koretzky. 2000. Functional association between SLAP-130 and SLP-76 in Jurkat T cells. J. Biol. Chem. 275:5143-51452.
4. Bos, J. L. 2005. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17:123-128.
5. Bos, J. L., B. Franke, L. M'Rabet, K. Reedquist, and F. Zwartkruis. 1997. In search of a function for the Ras-like GTPase Rap1. FEBS Lett. 410:59-62.
6. Boussiotis, V. A., G. J. Freeman, A. Berezovskaya, D. L. Barber, and L. M. Nadler. 1997. Maintenance of human T cell anergy: blocking of IL-2 gene transcription by activated Rap1. Science 278:124-128.
7. Coppolino, M. G., M. Krause, P. Hagendorff, D. A. Monner, W. Trimble, S. Grinstein, J. Wehland, and A. S. Sechi. 2001. Evidence for a molecular complex consisting of Fyb/SLAP, SLP-76, Nck, VASP and WASP that links the actin cytoskeleton to Fcgamma receptor signalling during phagocytosis. J. Cell Sci. 114:4307-4318.
8. da Silva, A. J., Z. Li, C. de Vera, E. Canto, P. Findell, and C. E. Rudd. 1997. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA 94:7493-7498.
9. Dustin, M. L., and T. A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341:619-624.
10. Griffiths, E. K., C. Krawczyk, Y. Y. Kong, M. Raab, S. J. Hyduk, D. Bouchard, V. S. Chan, I. Kozieradzki, A. J. Oliveira-Dos-Santos, A. Wakeham, P. S. Ohashi, M. I. Cybulsky, C. E. Rudd, and J. M. Penninger. 2001. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293:2260-2263.
11. Han, J., C. J. Lim, N. Watenabe, A. Soriani, B. Ratnikov, D. A. Calderwood, W. Puzon-McLaughlin, E. M. Lafuente, V. A. Boussiotis, S. J. Shattil, and M. H. Ginsberg. 2006. Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 16:1796-1806.
12. Hogg, N., M. Laschinger, K. Giles, and A. McDowell. 2003. T-cell integrins: more than just sticking points. J. Cell Sci. 116:4695-4705.
13. Huang, Y., D. D. Norton, P. Precht, J. L. Martindale, J. K. Burkhardt, and R. L. Wange. 2005. Deficiency of ADAP/Fyb/SLAP-130 destabilizes SKAP55 in Jurkat T cells. J. Biol. Chem. 280:23576-23583.
14. Jenzora, A., B. Behrendt, J. V. Small, J. Wehland, and T. E. Stradal. 2005. PREL1 provides a link from Ras signalling to the actin cytoskeleton via Ena/VASP proteins. FEBS Lett. 579:455-463.
15. Jo, E. K., H. Wang, and C. E. Rudd. 2005. An essential role for SKAP-55 in LFA-1 clustering on T cells that cannot be substituted by SKAP-55R. J. Exp. Med. 201:1733-1739.
16. Katagiri, K., M. Hattori, N. Minato, S. Irie, K. Takatsu, and T. Kinashi. 2000. Rap1 is a potent activation signal for leukocyte function-associated antigen 1 distinct from protein kinase C and phosphatidylinositol-3-OH kinase. Mol. Cell. Biol. 20:1956-1969.
17. Katagiri, K., M. Hattori, N. Minato, and T. Kinashi. 2002. Rap1 functions as a key regulator of T-cell and antigen-presenting cell interactions and modulates T-cell responses. Mol. Cell. Biol. 22:1001-1015.
18. Katagiri, K., M. Imamura, and T. Kinashi. 2006. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat. Immunol. 7:919-928.
19. Katagiri, K., A. Maeda, M. Shimonaka, and T. Kinashi. 2003. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 4:741-748.
20. Katagiri, K., N. Ohnishi, K. Kabashima, T. Iyoda, N. Takeda, Y. Shinkai, K. Inaba, and T. Kinashi. 2004. Crucial functions of the Rap1 effector molecule RAPL in lymphocyte and dendritic cell trafficking. Nat. Immunol. 5:1045-1051.
21. Kavran, J. M., D. E. Klein, A. Lee, M. Falasca, S. J. Isakoff, E. Y. Skolnik, and M. A. Lemmon. 1998. Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273:30497-30508.
22. Kinashi, T. 2005. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5:546-559.
23. Kliche, S., D. Breitling, M. Togni, R. Pusch, K. Heuer, X. Wang, C. Freund, A. Kasirer-Friede, G. Menasche, G. A. Koretzky, and B. Schraven. 2006. The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol. Cell. Biol. 26:7130-7144.
24. Kolanus, W., W. Nagel, B. Schiller, L. Zeitlmann, S. Godar, H. Stockinger, and B. Seed. 1996. Alpha L beta 2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86:233-242.
25. Koretzky, G. A., and P. S. Myung. 2001. Positive and negative regulation of T-cell activation by adaptor proteins. Nat. Rev. Immunol. 1:95-107.
26. Krause, M., A. S. Sechi, M. Konradt, D. Monner, F. B. Gertler, and J. Wehland. 2000. Fyn-binding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/ vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J. Cell Biol. 149:181-194.
27. Lafuente, E. M., A. A. van Puijenbroek, M. Krause, C. V. Carman, G. J. Freeman, A. Berezovskaya, E. Constentine, T. A. Springer, F. B. Gertler, and V. A. Boussiotis. 2004. RIAM, an Ena/VASP and profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev. Cell 7:585-595.
28. Lemmon, M. A. 2004. Pleckstrin homology domains: not just for phosphoinositides. Biochem. Soc. Trans. 32:707-711.
29. Liu, J., H. Kang, M. Raab, A. J. da Silva, S. K. Kraeft, and C. E. Rudd. 1998. FYB (FYN binding protein) serves as a binding partner for lymphoid protein and FYN kinase substrate SKAP55 and a SKAP55-related protein in T cells. Proc. Natl. Acad. Sci. USA 95:8779-8784.
30. Marie-Cardine, A., L. R. Hendricks-Taylor, N. J. Boerth, H. Zhao, B. Schraven, and G. A. Koretzky. 1998. Molecular interaction between the Fyn-associated protein SKAP55 and the SLP-76-associated phosphoprotein SLAP-130. J. Biol. Chem. 273:25789-25795.
31. Medeiros, R. B., D. M. Dickey, H. Chung, A. C. Quale, L. R. Nagarajan, D. D. Billadeau, and Y. Shimizu. 2005. Protein kinase D1 and the beta 1 integrin cytoplasmic domain control beta 1 integrin function via regulation of Rap1 activation. Immunity 23:213-226.
32. Mueller, K. L., M. A. Daniels, A. Felthauser, C. Kao, S. C. Jameson, and Y. Shimizu. 2004. Cutting edge: LFA-1 integrin-dependent T cell adhesion is regulated by both ag specificity and sensitivity. J. Immunol. 173:2222-2226.
33. Musci, M. A., L. R. Hendricks-Taylor, D. G. Motto, M. Paskind, J. Kamens, C. W. Turck, and G. A. Koretzky. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674-11677.
34. Nagel, W., L. Zeitlmann, P. Schilcher, C. Geiger, J. Kolanus, and W. Kolanus. 1998. Phosphoinositide 3-OH kinase activates the beta2 integrin adhesion pathway and induces membrane recruitment of cytohesin-1. J. Biol. Chem. 273:14853-14861.
35. Peterson, E. J., M. L. Woods, S. A. Dmowski, G. Derimanov, M. S. Jordan, J. N. Wu, P. S. Myung, Q. H. Liu, J. T. Pribila, B. D. Freedman, Y. Shimizu, and G. A. Koretzky. 2001. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293:2263-2265.
36. Pribila, J. T., A. C. Quale, K. L. Mueller, and Y. Shimizu. 2004. Integrins and T cell-mediated immunity. Annu. Rev. Immunol. 22:157-180.
37. Sebzda, E., M. Bracke, T. Tugal, N. Hogg, and D. A. Cantrell. 2002. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat. Immunol. 3:251-258.
38. Singer, A. L., S. C. Bunnell, A. E. Obstfeld, M. S. Jordan, J. N. Wu, P. S. Myung, L. E. Samelson, and G. A. Koretzky. 2004. Roles of the proline-rich domain in SLP-76 subcellular localization and T cell function. J. Biol. Chem. 279:15481-15490.
39. Togni, M., J. Lindquist, A. Gerber, U. Kolsch, A. Hamm-Baarke, S. Kliche, and B. Schraven. 2004. The role of adaptor proteins in lymphocyte activation. Mol. Immunol. 41:615-630.
40. Wang, H., E. Y. Moon, A. Azouz, X. Wu, A. Smith, H. Schneider, N. Hogg, and C. E. Rudd. 2003. SKAP-55 regulates integrin adhesion and formation of T cell-APC conjugates. Nat. Immunol. 4:366-374.
41. Weiss, A., and J. D. Stobo. 1984. Requirement for the coexpression of T3 and the T cell antigen receptor on a malignant human T cell line. J. Exp. Med. 160:1284-1299.
42. Wu, J. N., and G. A. Koretzky. 2004. The SLP-76 family of adapter proteins. Semin. Immunol. 16:379-393.
43. Zhong, X. P., E. A. Hainey, B. A. Olenchock, H. Zhao, M. K. Topham, and G. A. Koretzky. 2002. Regulation of T cell receptor-induced activation of the Ras-ERK pathway by diacylglycerol kinase zeta. J. Biol. Chem. 277:31089-31098.