T lymphocytes sense antigens within seconds and make a decision within one minute

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2064-2071

  Brodovitch, Alexandre ^a,b,c   Bongrand, Pierre ^a,b,c,d   Pierres, Anne ^a,b,c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSERM   (France)

^c CNRS   (France)

^d Service des Maladies Infectieuses   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; HLA ANTIGEN; PHOSPHOLIPASE C GAMMA1; T LYMPHOCYTE RECEPTOR;

ANTIGEN DETECTION; ARTICLE; CELL ADHESION; CELL CONTACT; CELL SPREADING; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LIGAND BINDING; LYMPHOCYTE MEMBRANE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY;

ANTIGENS; HUMANS; LYMPHOCYTE ACTIVATION; MICROSCOPY, FLUORESCENCE; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TIME;

EID: 84883417144     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300523     Document Type: Article

References (52)

1. Bongrand, P., and B. Malissen. 1998. Quantitative aspects of T-cell recognition: from within the antigen-presenting cell to within the T cell. Bioessays 20: 412-422.
2. van der Merwe, P. A., and O. Dushek. 2011. Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 11: 47-55.
3. 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.
4. Bousso, P., N. R. Bhakta, R. S. Lewis, and E. Robey. 2002. Dynamics of thymocyte-stromal cell interactions visualized by two-photon microscopy. Science 296: 1876-1880.
5. Sykulev, Y., M. Joo, I. Vturina, T. J. Tsomides, and H. N. Eisen. 1996. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4: 565-571.
6. Irvine, D. J., M. A. Purbhoo, M. Krogsgaard, and M. M. Davis. 2002. Direct observation of ligand recognition by T cells. Nature 419: 845-849.
7. McKeithan, T. W. 1995. Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. USA 92: 5042-5046.
8. Huppa, J. B., M. Axmann, M. A. Mörtelmaier, B. F. Lillemeier, E. W. Newell, M. Brameshuber, L. O. Klein, G. J. Schütz, and M. M. Davis. 2010. TCRpeptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463: 963-967.
9. Robert, P., M. Aleksic, O. Dushek, V. Cerundolo, P. Bongrand, and P. A. van der Merwe. 2012. Kinetics and mechanics of two-dimensional interactions between T cell receptors and different activating ligands. Biophys. J. 102: 248-257.
10. Dushek, O., R. Das, and D. Coombs. 2009. A role for rebinding in rapid and reliable T cell responses to antigen. PLOS Comput. Biol. 5: e1000578.
11. He, H. T., and P. Bongrand. 2012. Membrane dynamics shape TCR-generated signalling. Frontiers Immunol. 3: 90.
12. Campi, G., R. Varma, and M. L. Dustin. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202: 1031-1036.
13. Huse, M., L. O. Klein, A. T. Girvin, J. M. Faraj, Q.-J. Li, M. S. Kuhns, and M. M. Davis. 2007. Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 27: 76-88.
14. Dustin, M. L., S. K. Bromley, Z. Kan, D. A. Peterson, and E. R. Unanue. 1997. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. USA 94: 3909-3913.
15. Bunnell, S. C., V. Kapoor, R. P. Trible, W. Zhang, and L. E. Samelson. 2001. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14: 315-329.
16. Etienne, J., and A. Duperray. 2011. Initial dynamics of cell spreading are governed by dissipation in the actin cortex. Biophys. J. 101: 611-621.
17. Kingeter, L. M., S. Paul, S. K. Maynard, N. G. Cartwright, and B. C. Schaefer. 2010. Cutting edge: TCR ligation triggers digital activation of NF-kappaB. J. Immunol. 185: 4520-4524.
18. Tay, S., J. J. Hughey, T. K. Lee, T. Lipniacki, S. R. Quake, and M. W. Covert. 2010. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466: 267-271.
19. Fleire, S. J., J. P. Goldman, Y. R. Carrasco, M. Weber, D. Bray, and F. D. Batista. 2006. B cell ligand discrimination through a spreading and contraction response. Science 312: 738-741.
20. Crétel, E., D. Touchard, P. Bongrand, and A. Pierres. 2011. A new method for rapid detection of T lymphocyte decision to proliferate after encountering activating surfaces. J. Immunol. Methods 364: 33-39.
21. Crétel, E., D. Touchard, A.-M. Benoliel, P. Bongrand, and A. Pierres. 2010. Early contacts between T lymphocytes and activating surfaces. J. Phys. Condens. Matter 22: 194107.
22. Döbereiner, H.-G., B. J. Dubin-Thaler, J. M. Hofman, H. S. Xenias, T. N. Sims, G. Giannone, M. L. Dustin, C. H. Wiggins, and M. P. Sheetz. 2006. Lateral membrane waves constitute a universal dynamic pattern of motile cells. Phys. Rev. Lett. 97: 038102.
23. Sims, T. N., T. J. Soos, H. S. Xenias, B. Dubin-Thaler, J. M. Hofman, J. C.Waite, T. O. Cameron, V. K. Thomas, R. Varma, C. H. Wiggins, et al. 2007. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell 129: 773-785.
24. Lo Schiavo, V., P. Robert, L. Limozin, and P. Bongrand. 2012. Quantitative modeling assesses the contribution of bond strengthening, rebinding and force sharing to the avidity of biomolecule interactions. PLoS ONE 7: e44070.
25. Pierres, A., A.-M. Benoliel, D. Touchard, and P. Bongrand. 2008. How cells tiptoe on adhesive surfaces before sticking. Biophys. J. 94: 4114-4122.
26. Mattheyses, A. L., and D. Axelrod. 2006. Direct measurement of the evanescent field profile produced by objective-based total internal reflection fluorescence. J. Biomed. Opt. 11: 014006.
27. Saarikangas, J., H. Zhao, and P. Lappalainen. 2010. Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol. Rev. 90: 259-289.
28. Bentley, D., and A. Toroian-Raymond. 1986. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323: 712-715.
29. Faix, J., and K. Rottner. 2006. The making of filopodia. Curr. Opin. Cell Biol. 18: 18-25.
30. Sage, P. T., L. M. Varghese, R. Martinelli, T. E. Sciuto, M. Kamei, A. M. Dvorak, T. A. Springer, A. H. Sharpe, and C. V. Carman. 2012. Antigen recognition is facilitated by invadosome-like protrusions formed by memory/effector T cells. J. Immunol. 188: 3686-3699.
31. Pierres, A., V. Monnet-Corti, A.-M. Benoliel, and P. Bongrand. 2009. Do membrane undulations help cells probe the world? Trends Cell Biol. 19: 428-433.
32. Husson, J., K. Chemin, A. Bohineust, C. Hivroz, and N. Henry. 2011. Force generation upon T cell receptor engagement. PLoS ONE 6: e19680.
33. Malawista, S. E., E. O. Smith, and J. P. Seibyl. 2006. Cryopreservable neutrophil surrogates: granule-poor, motile cytoplasts from polymorphonuclear leukocytes home to inflammatory lesions in vivo. Cell Motil. Cytoskeleton 63: 254-257.
34. Nalbant, P., L. Hodgson, V. Kraynov, A. Toutchkine, and K. M. Hahn. 2004. Activation of endogenous Cdc42 visualized in living cells. Science 305: 1615-1619.
35. Neves, S. R., and R. Iyengar. 2009. Models of spatially restricted biochemical reaction systems. J. Biol. Chem. 284: 5445-5449.
36. Knight, J. D., M. G. Lerner, J. G. Marcano-Velázquez, R. W. Pastor, and J. J. Falke. 2010. Single molecule diffusion of membrane-bound proteins: window into lipid contacts and bilayer dynamics. Biophys. J. 99: 2879-2887.
37. Huang, J., V. I. Zarnitsyna, B. Liu, L. J. Edwards, N. Jiang, B. D. Evavold, and C. Zhu. 2010. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464: 932-936.
38. Kim, S. T., K. Takeuchi, Z.-Y. J. Sun, M. Touma, C. E. Castro, A. Fahmy, M. J. Lang, G. Wagner, and E. L. Reinherz. 2009. The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284: 31028-31037.
39. Li, Y.-C., B.-M. Chen, P.-C. Wu, T.-L. Cheng, L.-S. Kao, M.-H. Tao, A. Lieber, and S. R. Roffler. 2010. Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184: 5959-5963.
40. Ma, Z., D. E. Discher, and T. H. Finkel. 2012. Mechanical forces in T cell receptor signal initiation. Frontiers Immunol. 3: 217.
41. O'Connor, R. S., X. Hao, K. Shen, K. Bashour, T. Akimova, W. W. Hancock, L. C. Kam, and M. C. Milone. 2012. Substrate rigidity regulates human T cell activation and proliferation. J. Immunol. 189: 1330-1339.
42. Wei, X., B. J. Tromberg, and M. D. Cahalan. 1999. Mapping the sensitivity of T cells with an optical trap: polarity and minimal number of receptors for Ca(2+) signaling. Proc. Natl. Acad. Sci. USA 96: 8471-8476.
43. Viola, A., and A. Lanzavecchia. 1996. T cell activation determined by T cell receptor number and tunable thresholds. Science 273: 104-106.
44. Dustin, M. L., J. M. Miller, S. Ranganath, D. A. A. Vignali, N. J. Viner, C. A. Nelson, and E. R. Unanue. 1996. TCR-mediated adhesion of T cell hybridomas to planar bilayers containing purified MHC class II/peptide complexes and receptor shedding during detachment. J. Immunol. 157: 2014-2021.
45. Brown, M. J., R. Nijhara, J. A. Hallam, M. Gignac, K. M. Yamada, S. L. Erlandsen, J. Delon, M. Kruhlak, and S. Shaw. 2003. Chemokine stimu-lation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 102: 3890-3899.
46. Tomar, A., S. P. George, S. Mathew, and S. Khurana. 2009. Differential effects of lysophosphatidic acid and phosphatidylinositol 4,5-bisphosphate on actin dynamics by direct association with the actin-binding protein villin. J. Biol. Chem. 284: 35278-35282.
47. Tsai, F.-C., and T. Meyer. 2012. Ca2+ pulses control local cycles of lamellipodia retraction and adhesion along the front of migrating cells. Curr. Biol. 22: 837-842.
48. 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.
49. Kaplanski, G., C. Farnarier, A.-M. Benoliel, C. Foa, S. Kaplanski, and P. Bongrand. 1994. A novel role for E- and P-selectins: shape control of endothelial cell monolayers. J. Cell Sci. 107: 2449-2457.
50. Negulescu, P. A., T. B. Krasieva, A. Khan, H. H. Kerschbaum, and M. D. Cahalan. 1996. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 4: 421-430.
51. Robert, P., M. Canault, C. Farnarier, A. Nurden, C. Grosdidier, V. Barlogis, P. Bongrand, A. Pierres, H. Chambost, and M.-C. Alessi. 2011. A novel leukocyte adhesion deficiency III variant: kindlin-3 deficiency results in integrinand nonintegrin-related defects in different steps of leukocyte adhesion. J. Immunol. 186: 5273-5283.
52. Sundd, P., E. Gutierrez, M. K. Pospieszalska, H. Zhang, A. Groisman, and K. Ley. 2010. Quantitative dynamic footprinting microscopy reveals mechanisms of neutrophil rolling. Nat. Methods 7: 821-824.