Regulated vesicle fusion generates signaling nanoterritories that control T cell activation at the immunological synapse

Journal of Experimental Medicine

Volumn 210, Issue 11, 2013, Pages 2415-2433

  Soares, Helena ^a,b   Henriques, Ricardo ^a,b   Sachse, Martin ^a   Ventimiglia, Leandro ^c   Alonso, Miguel A ^c   Zimmer, Christophe ^a,b   Thoulouze, Maria Isabel ^a,b   Alcover, Andrés ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CALCIUM; GAMMA INTERFERON; INTERLEUKIN 2; LAT PROTEIN; MYELIN AND LYMPHOCYTE PROTEIN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; PROTEIN SLP76; SYNAPTOTAGMIN; SYNAPTOTAGMIN 7; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ZETA CHAIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOLOGICAL SYNAPSE; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CALCIUM; CELL COMPARTMENTATION; CYTOKINES; EXOCYTOSIS; GENE SILENCING; HUMANS; IMMUNOLOGICAL SYNAPSES; JURKAT CELLS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE FUSION; MEMBRANE PROTEINS; MYELIN AND LYMPHOCYTE-ASSOCIATED PROTEOLIPID PROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SYNAPTOTAGMINS; T-LYMPHOCYTES; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84886820997     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130150     Document Type: Article

References (42)

1. Acuto, O., V. Di Bartolo, and F. Michel. 2008. Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 8:699-712. http://dx.doi.org/10.1038/nri2397
2. Alcover, A., and M.I. Thoulouze. 2010. Vesicle traffic to the immunological synapse: a multifunctional process targeted by lymphotropic viruses. Curr. Top. Microbiol. Immunol. 340:191-207. http://dx.doi.org/10.1007/978-3-642-03858-7_10
3. Antón, O., A. Batista, J. Millán, L. Andrés-Delgado, R. Puertollano, I. Correas, and M.A. Alonso. 2008. An essential role for the MAL protein in targeting Lck to the plasma membrane of human T lymphocytes. J. Exp. Med. 205:3201-3213. http://dx.doi.org/10.1084/jem.20080552
4. Balagopalan, L., V.A. Barr, R.L. Kortum, A.K. Park, and L.E. Samelson. 2013. Cutting edge: cell surface linker for activation of T cells is recruited to microclusters and is active in signaling. J. Immunol. 190:3849-3853. http://dx.doi.org/10.4049/jimmunol.1202760
5. Bates, M., B. Huang, G.T. Dempsey, and X. Zhuang. 2007. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science. 317:1749-1753. http://dx.doi.org/10.1126/science.1146598
6. Bonello, G., N. Blanchard, M.C. Montoya, E. Aguado, C. Langlet, H.T. He, S. Nunez-Cruz, M. Malissen, F. Sanchez-Madrid, D. Olive, et al. 2004. Dynamic recruitment of the adaptor protein LAT: LAT exists in two distinct intracellular pools and controls its own recruitment. J. Cell Sci. 117:1009-1016. http://dx.doi.org/10.1242/jcs.00968
7. Chaineau, M., L. Danglot, and T. Galli. 2009. Multiple roles of the vesicular- SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Lett. 583:3817-3826. http://dx.doi.org/10.1016/j.febslet.2009.10.026
8. Colvin, R.A., T.K. Means, T.J. Diefenbach, L.F. Moita, R.P. Friday, S. Sever, G.S. Campanella, T. Abrazinski, L.A. Manice, C. Moita, et al. 2010. Synaptotagmin-mediated vesicle fusion regulates cell migration. Nat. Immunol. 11:495-502. http://dx.doi.org/10.1038/ni.1878
9. Das, V., B. Nal, A. Dujeancourt, M.I. Thoulouze, T. Galli, P. Roux, A. Dautry-Varsat, and A. Alcover. 2004. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity. 20:577-588. http://dx.doi.org/10.1016/S1074-7613(04)00106-2
10. de Saint Basile, G., G. Ménasché, and A. Fischer. 2010. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 10:568-579. http://dx.doi.org/10.1038/nri2803
11. Douglass, A.D., and R.D. Vale. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell. 121:937-950. http://dx.doi.org/10.1016/j.cell.2005.04.009
12. Dustin, M.L., and D. Depoil. 2011. New insights into the T cell synapse from single molecule techniques. Nat. Rev. Immunol. 11:672-684. http://dx.doi.org/10.1038/nri3066
13. Edelstein, A., N. Amodaj, K. Hoover, R. Vale, and N. Stuurman. 2010. Computer control of microscopes using microManager. Curr Protoc Mol Biol Chapter 14:Unit14 20.
14. Ehrlich, L.I.R., P.J.R. Ebert, M.F. Krummel, A. Weiss, and M.M. Davis. 2002. Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity. 17:809-822. http://dx.doi.org/10.1016/S1074-7613(02)00481-8
15. Finetti, F., S.R. Paccani, M.G. Riparbelli, E. Giacomello, G. Perinetti, G.J. Pazour, J.L. Rosenbaum, and C.T. Baldari. 2009. Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse. Nat. Cell Biol. 11:1332-1339. http://dx.doi.org/10.1038/ncb1977
16. Frank, E., M. Hall, L. Trigg, G. Holmes, and I.H. Witten. 2004. Data mining in bioinformatics using Weka. Bioinformatics. 20:2479-2481. http://dx.doi.org/10.1093/bioinformatics/bth261
17. Fukuda, M. 2008. Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65:2801-2813. http://dx.doi.org/10.1007/s00018-008-8351-4
18. Heilemann, M., S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer. 2008. Subdiffractionresolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. Engl. 47:6172-6176. http://dx.doi.org/10.1002/anie.200802376
19. Henriques, R., M. Lelek, E.F. Fornasiero, F. Valtorta, C. Zimmer, and M.M. Mhlanga. 2010. QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat. Methods. 7:339-340. http://dx.doi.org/10.1038/nmeth0510-339
20. Holden, S.J., S. Uphoff, and A.N. Kapanidis. 2011. DAOSTORM: an algorithm for high- density super-resolution microscopy. Nat. Methods. 8:279-280. http://dx.doi.org/10.1038/nmeth0411-279
21. Houtman, J.C., H. Yamaguchi, M. Barda-Saad, A. Braiman, B. Bowden, E. Appella, P. Schuck, and L.E. Samelson. 2006. Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat. Struct. Mol. Biol. 13:798-805. http://dx.doi.org/10.1038/nsmb1133
22. Huse, M., B.F. Lillemeier, M.S. Kuhns, D.S. Chen, and M.M. Davis. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7:247-255. http://dx.doi.org/10.1038/ni1304
23. Kusumi, A., Y.M. Shirai, I. Koyama-Honda, K.G. Suzuki, and T.K. Fujiwara. 2010. Hierarchical organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett. 584:1814-1823. http://dx.doi.org/10.1016/j.febslet.2010.02.047
24. Larghi, P., D.J. Williamson, J.M. Carpier, S. Dogniaux, K. Chemin, A. Bohineust, L. Danglot, K. Gaus, T. Galli, and C. Hivroz. 2013. VAMP7 controls T cell activation by regulating the recruitment and phosphorylation of vesicular Lat at TCR-activation sites. Nat. Immunol. 14:723-731. http://dx.doi.org/10.1038/ni.2609
25. Lasserre, R., and A. Alcover. 2010. Cytoskeletal cross-talk in the control of T cell antigen receptor signaling. FEBS Lett. 584:4845-4850. http://dx.doi.org/10.1016/j.febslet.2010.09.001
26. Lillemeier, B.F., J.R. Pfeiffer, Z. Surviladze, B.S. Wilson, and M.M. Davis. 2006. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc. Natl. Acad. Sci. USA. 103:18992-18997. http://dx.doi.org/10.1073/pnas.0609009103
27. Lillemeier, B.F., M.A. Mörtelmaier, M.B. Forstner, J.B. Huppa, J.T. Groves, and M.M. Davis. 2010. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 11:90-96. http://dx.doi.org/10.1038/ni.1832
28. Marcet-Palacios, M., S.O. Odemuyiwa, J.J. Coughlin, D. Garofoli, C. Ewen, C.E. Davidson, M. Ghaffari, K.P. Kane, P. Lacy, M.R. Logan, et al. 2008. Vesicle-associated membrane protein 7 (VAMP-7) is essential for target cell killing in a natural killer cell line. Biochem. Biophys. Res. Commun. 366:617-623. http://dx.doi.org/10.1016/j.bbrc.2007.11.079
29. Ménager, M.M., G. Ménasché, M. Romao, P. Knapnougel, C.H. Ho, M. Garfa, G. Raposo, J. Feldmann, A. Fischer, and G. de Saint Basile. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8:257-267. http://dx.doi.org/10.1038/ni1431
30. Nika, K., C. Soldani, M. Salek, W. Paster, A. Gray, R. Etzensperger, L. Fugger, P. Polzella, V. Cerundolo, O. Dushek, et al. 2010. Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity. 32:766-777. http://dx.doi.org/10.1016/j.immuni.2010.05.011
31. +-triggered exocytosis. Curr. Opin. Cell Biol. 22:496-505. http://dx.doi.org/10.1016/j.ceb.2010.05.001
32. Purbhoo, M.A., H. Liu, S. Oddos, D.M. Owen, M.A. Neil, S.V. Pageon, P.M. French, C.E. Rudd, and D.M. Davis. 2010. Dynamics of subsynaptic vesicles and surface microclusters at the immunological synapse. Sci. Signal. 3:ra36. http://dx.doi.org/10.1126/scisignal.2000645
33. Rao, S.K., C. Huynh, V. Proux-Gillardeaux, T. Galli, and N.W. Andrews. 2004. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J. Biol. Chem. 279:20471-20479. http://dx.doi.org/10.1074/jbc. M400798200
34. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 9:676-682. http://dx.doi.org/10.1038/nmeth.2019
35. Sengupta, P., T. Jovanovic-Talisman, D. Skoko, M. Renz, S.L. Veatch, and J. Lippincott-Schwartz. 2011. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat. Methods. 8:969-975. http://dx.doi.org/10.1038/nmeth.1704
36. Sherman, E., V. Barr, S. Manley, G. Patterson, L. Balagopalan, I. Akpan, C.K. Regan, R.K. Merrill, C.L. Sommers, J. Lippincott-Schwartz, and L.E. Samelson. 2011. Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. Immunity. 35:705-720. http://dx.doi.org/10.1016/j.immuni.2011.10.004
37. Simonson, P.D., E. Rothenberg, and P.R. Selvin. 2011. Single-molecule-based super-resolution images in the presence of multiple fluorophores. Nano Lett. 11:5090-5096. http://dx.doi.org/10.1021/nl203560r
38. Stinchcombe, J.C., D.C. Barral, E.H. Mules, S. Booth, A.N. Hume, L.M. Machesky, M.C. Seabra, and G.M. Griffiths. 2001. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152:825-834. http://dx.doi.org/10.1083/jcb.152.4.825
39. +-regulated exocytosis and SNARE function. Trends Endocrinol. Metab. 16:81-83. http://dx.doi.org/10.1016/j.tem.2005.02.002
40. Sugawara, K., T. Shibasaki, A. Mizoguchi, T. Saito, and S. Seino. 2009. Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells. 14:445-456. http://dx.doi.org/10.1111/j.1365-2443.2009.01285.x
41. Wei, C., X. Wang, M. Chen, K. Ouyang, L.S. Song, and H. Cheng. 2009. Calcium flickers steer cell migration. Nature. 457:901-905. http://dx.doi.org/10.1038/nature07577
42. Williamson, D.J., D.M. Owen, J. Rossy, A. Magenau, M. Wehrmann, J.J. Gooding, and K. Gaus. 2011. Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat. Immunol. 12:655-662. http://dx.doi.org/10.1038/ni.2049