Contact-dependent T cell activation and T cell stopping require talin1

Journal of Immunology

Volumn 187, Issue 12, 2011, Pages 6256-6267

  Wernimont, Sarah A ^a   Wiemer, Andrew J ^a,b   Bennin, David A ^a,b   Monkley, Susan J ^c   Ludwig, Thomas ^d   Critchley, David R ^c   Huttenlocher, Anna ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; REGULATOR PROTEIN; TALIN1; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CELL ADHESION; CELL INTERACTION; CELL POLARITY; CONTROLLED STUDY; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ACTINS; ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL POLARITY; CELL PROLIFERATION; CELLS, CULTURED; IMMUNOLOGICAL SYNAPSES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; TALIN; VINCULIN;

EID: 83755196111     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102028     Document Type: Article

References (51)

1. Smith-Garvin, J. E., G. A. Koretzky, and M. S. Jordan. 2009. T cell activation. Annu. Rev. Immunol. 27: 591-619.
2. Huppa, J. B., M. Gleimer, C. Sumen, and M. M. Davis. 2003. Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat. Immunol. 4: 749-755. (Pubitemid 36986758)
3. Iezzi, G., K. Karjalainen, and A. Lanzavecchia. 1998. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95. (Pubitemid 28097826)
4. Costello, P. S., M. Gallagher, and D. A. Cantrell. 2002. Sustained and dynamic inositol lipid metabolism inside and outside the immunological synapse. Nat. Immunol. 3: 1082-1089. (Pubitemid 35363662)
5. Benvenuti, F., C. Lagaudrière-Gesbert, I. Grandjean, C. Jancic, C. Hivroz, A. Trautmann, O. Lantz, and S. Amigorena. 2004. Dendritic cell maturation controls adhesion, synapse formation, and the duration of the interactions with naive T lymphocytes. J. Immunol. 172: 292-301. (Pubitemid 38020483)
6. Faroudi, M., R. Zaru, P. Paulet, S. Müller, and S. Valitutti. 2003. Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J. Immunol. 171: 1128-1132. (Pubitemid 36900039)
7. Gunzer, M., A. Schäfer, S. Borgmann, S. Grabbe, K. S. Zänker, E. B. Bröcker, E. Kämpgen, and P. Friedl. 2000. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13: 323-332.
8. Bousso, P. 2008. T-cell activation by dendritic cells in the lymph node: lessons from the movies. Nat. Rev. Immunol. 8: 675-684.
9. Hugues, S., A. Boissonnas, S. Amigorena, and L. Fetler. 2006. The dynamics of dendritic cell-T cell interactions in priming and tolerance. Curr. Opin. Immunol. 18: 491-495. (Pubitemid 43965001)
10. Miller, M. J., O. Safrina, I. Parker, and M. D. Cahalan. 2004. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 200: 847-856. (Pubitemid 39362921)
11. Scholer, A., S. Hugues, A. Boissonnas, L. Fetler, and S. Amigorena. 2008. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 28: 258-270. (Pubitemid 351222655)
12. Kandula, S., and C. Abraham. 2004. LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J. Immunol. 173: 4443-4451. (Pubitemid 39280674)
13. Kinashi, T. 2005. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5: 546-559. (Pubitemid 40961332)
14. Abram, C. L., and C. A. Lowell. 2009. The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 27: 339-362.
15. Burbach, B. J., R. B. Medeiros, K. L. Mueller, and Y. Shimizu. 2007. T-cell receptor signaling to integrins. Immunol. Rev. 218: 65-81. (Pubitemid 47052298)
16. Manevich-Mendelson, E., S.W. Feigelson, R. Pasvolsky, M. Aker, V. Grabovsky, Z. Shulman, S. S. Kilic, M. A. Rosenthal-Allieri, S. Ben-Dor, A. Mory, et al. 2009. Loss of Kindlin-3 in LAD-III eliminates LFA-1 but not VLA-4 adhesiveness developed under shear flow conditions. Blood 114: 2344-2353.
17. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86. (Pubitemid 28420234)
18. Critchley, D. R. 2009. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys. 38: 235-254.
19. Shattil, S. J., C. Kim, and M. H. Ginsberg. 2010. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 11: 288-300.
20. Simonson, W. T., S. J. Franco, and A. Huttenlocher. 2006. Talin1 regulates TCR-mediated LFA-1 function. J. Immunol. 177: 7707-7714. (Pubitemid 44846286)
21. Nolz, J. C., R. B. Medeiros, J. S. Mitchell, P. Zhu, B. D. Freedman, Y. Shimizu, and D. D. Billadeau. 2007. WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse. Mol. Cell. Biol. 27: 5986-6000. (Pubitemid 47326689)
22. Bartelt, R. R., N. Cruz-Orcutt, M. Collins, and J. C. D. Houtman. 2009. Comparison of T cell receptor-induced proximal signaling and downstream functions in immortalized and primary T cells. PLoS ONE 4: e5430.
23. Bueno, C., C. D. Lemke, G. Criado, M. L. Baroja, S. S. Ferguson, A. K. Rahman, C. D. Tsoukas, J. K. McCormick, and J. Madrenas. 2006. Bacterial superantigens bypass Lck-dependent T cell receptor signaling by activating a Galpha11-dependent, PLC-beta-mediated pathway. Immunity 25: 67-78. (Pubitemid 44066827)
24. Burkhardt, J. K., E. Carrizosa, and M. H. Shaffer. 2008. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26: 233-259. (Pubitemid 351600376)
25. Nolz, J. C., T. S. Gomez, P. Zhu, S. Li, R. B. Medeiros, Y. Shimizu, J. K. Burkhardt, B. D. Freedman, and D. D. Billadeau. 2006. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16: 24-34. (Pubitemid 43049883)
26. Gomez, T. S., S. D. McCarney, E. Carrizosa, C. M. Labno, E. O. Comiskey, J. C. Nolz, P. Zhu, B. D. Freedman, M. R. Clark, D. J. Rawlings, et al. 2006. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 24: 741-752. (Pubitemid 43867363)
27. Mace, E. M., J. Zhang, K. A. Siminovitch, and F. Takei. 2010. Elucidation of the integrin LFA-1-mediated signaling pathway of actin polarization in natural killer cells. Blood 116: 1272-1279.
28. Nieswandt, B., M. Moser, I. Pleines, D. Varga-Szabo, S. Monkley, D. Critchley, and R. Fässler. 2007. Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. J. Exp. Med. 204: 3113-3118.
29. Guo, K., J. E. McMinn, T. Ludwig, Y. H. Yu, G. Yang, L. Chen, D. Loh, C. Li, S. Chua, Jr., and Y. Zhang. 2007. Disruption of peripheral leptin signaling in mice results in hyperleptinemia without associated metabolic abnormalities. Endocrinology 148: 3987-3997. (Pubitemid 47105835)
30. Lafuente, E. M., A. A. F. L. van Puijenbroek, M. Krause, C. V. Carman, G. J. Freeman, A. Berezovskaya, E. Constantine, 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. (Pubitemid 39341843)
31. Wernimont, S.A., K. R. Legate, W. T. N. Simonson, R. Fassler, and A. Huttenlocher. 2010. PIPKI gamma 90 negatively regulates LFA-1-mediated adhesion and activation in antigen-induced CD4+ T cells. J. Immunol. 185: 4714-4723.
32. Friedman, R. S., J. Jacobelli, and M. F. Krummel. 2006. Surface-bound chemokines capture and prime T cells for synapse formation. Nat. Immunol. 7: 1101-1108. (Pubitemid 44420655)
33. Debrand, E., Y. El Jai, L. Spence, N. Bate, U. Praekelt, C. A. Pritchard, S. J. Monkley, and D. R. Critchley. 2009. Talin 2 is a large and complex gene encoding multiple transcripts and protein isoforms. FEBS J. 276: 1610-1628.
34. Monkley, S. J., C. A. Pritchard, and D. R. Critchley. 2001. Analysis of the mammalian talin2 gene TLN2. Biochem. Biophys. Res. Commun. 286: 880-885. (Pubitemid 32924855)
35. Zhang, X., G. Jiang, Y. Cai, S. J. Monkley, D. R. Critchley, and M. P. Sheetz. 2008. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10: 1062-1068.
36. Berlin-Rufenach, C., F. Otto, M. Mathies, J. Westermann, M. J. Owen, A. Hamann, and N. Hogg. 1999. Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J. Exp. Med. 189: 1467-1478. (Pubitemid 29227533)
37. Marski, M., S. Kandula, J. R. Turner, and C. Abraham. 2005. CD18 is required for optimal development and function of CD4+CD25+ T regulatory cells. J. Immunol. 175: 7889-7897. (Pubitemid 41798349)
38. Harriague, J., and G. Bismuth. 2002. Imaging antigen-induced PI3K activation in T cells. Nat. Immunol. 3: 1090-1096. (Pubitemid 35363663)
39. Hioe, C. E., P. C. Chien, Jr., C. Lu, T. A. Springer, X. H. Wang, J. Bandres, and M. Tuen. 2001. LFA-1 expression on target cells promotes human immunodeficiency virus type 1 infection and transmission. J. Virol. 75: 1077-1082. (Pubitemid 32037313)
40. 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. (Pubitemid 36986757)
41. Riedl, J., A. H. Crevenna, K. Kessenbrock, J. H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T. A. Holak, Z.Werb, et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5: 605-607. (Pubitemid 351911864)
42. Burkel, B. M., G. von Dassow, and W. M. Bement. 2007. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton 64: 822-832. (Pubitemid 350035031)
43. Cooper, K. M., D. A. Bennin, and A. Huttenlocher. 2008. The PCH family member proline-serine-threonine phosphatase-interacting protein 1 targets to the leukocyte uropod and regulates directed cell migration. Mol. Biol. Cell 19: 3180-3191.
44. Yoo, S. K., Q. Deng, P. J. Cavnar, Y. I. Wu, K. M. Hahn, and A. Huttenlocher. 2010. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 18: 226-236.
45. Graf, B., T. Bushnell, and J. Miller. 2007. LFA-1-mediated T cell costimulation through increased localization of TCR/class II complexes to the central supramolecular activation cluster and exclusion of CD45 from the immunological synapse. J. Immunol. 179: 1616-1624.
46. Miertzschke, M., P. Stanley, T. D. Bunney, F. Rodrigues-Lima, N. Hogg, and M. Katan. 2007. Characterization of interactions of adapter protein RAPL/Nore1B with RAP GTPases and their role in T cell migration. J. Biol. Chem. 282: 30629-30642. (Pubitemid 350035226)
47. Valitutti, S., M. Dessing, K. Aktories, H. Gallati, and A. Lanzavecchia. 1995. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181: 577-584.
48. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227. (Pubitemid 29329988)
49. Humphries, J. D., P. Wang, C. Streuli, B. Geiger, M. J. Humphries, and C. Ballestrem. 2007. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179: 1043-1057. (Pubitemid 350223497)
50. Wang, C., S. C. Morley, D. Donermeyer, I. Peng, W. P. Lee, J. Devoss, D. M. Danilenko, Z. Lin, J. Zhang, J. Zhou, P. M. Allen, and E. J. Brown. 2010. Actin-bundling protein L-plastin regulates T cell activation. J. Immunol. 185: 7487-7497.
51. Bousso, P., and E. Robey. 2003. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat. Immunol. 4: 579-585. (Pubitemid 36701342)