Single-molecule microscopy reveals heterogeneous dynamics of lipid raft components upon TCR engagement

International Immunology

Volumn 19, Issue 5, 2007, Pages 675-684

  Drbal, Karel ^a   Moertelmaier, Manuel ^b   Holzhauser, Christa ^c   Muhammad, Arshad ^c   Fuertbauer, Elke ^c   Howorka, Stefan ^d   Hinterberger, Maria ^c   Stockinger, Hannes ^a,c   Schütz, Gerhard J ^b  

^a Competence Centre for Biomolecular Therapeutics Research Vienna ^*  (Austria)

^b JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d Upper Austrian Research GmbH   (Austria)

Author keywords

Cell surface molecules; Lateral mobility; Membrane microdomains; Signal transduction; T cell activation

Indexed keywords

CD45 ANTIGEN; CD48 ANTIGEN; CD59 ANTIGEN; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE RECEPTOR; T LYMPHOCYTE RECEPTOR;

ARTICLE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID RAFT; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANTIGENS, CD; ANTIGENS, CD3; ANTIGENS, CD45; ANTIGENS, CD59; CELL MEMBRANE; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; KINETICS; LYMPHOCYTE ACTIVATION; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MICROSCOPY, CONFOCAL; MOTION; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 34447508103     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm032     Document Type: Article

References (51)

1. Bunnell, S. C., Hong, D. I., Kardon, J. R. et al. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:1263.
2. Grakoui, A., Bromley, S. K., Sumen, C. et al. 1999. The immunological synapse: A molecular machine controlling T cell activation. Science 285:221.
3. Choudhuri, K., Wiseman, D., Brown, M. H., Gould, K. and van der Merwe, P. A. 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436:578.
4. Barda-Saad, M., Braiman, A., Titerence, R., Bunnell, S. C., Barr, V. A. and Samelson, L. E. 2005. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immun. 6:80.
5. Das, V., Nal, B., Dujeancourt, A. et al. 2004. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 20:577.
6. Gaus, K., Chklovskaia, E., Fazekas de St Groth, B., Jessup, W. and Harder, T. 2005. Condensation of the plasma membrane at the site of T lymphocyte activation. J. Cell Biol. 171:121.
7. Burack, W. R., Lee, K. H., Holdorf, A. D., Dustin, M. L. and Shaw, A. S. 2002. Cutting edge: Quantitative imaging of raft accumulation in the immunological synapse. J. Immunol. 169:2837.
8. Harder, T. and Kuhn, M. 2000. Selective accumulation of raft-associated membrane protein LAT in T cell receptor signaling assemblies. J Cell Biol. 151:199.
9. Montixi, C., Langlet, C., Bernard, A. M. et al. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17:5334.
10. Drevot, P., Langlet, C., Guo, X. J. et al. 2002. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21:1899.
11. Moran, M. and Miceli, M. C. 1998. Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: A role for lipid rafts in T cell activation. Immunity 9:787.
12. Xavier, R., Brennan, T., Li, Q., McCormack, C. and Seed, B. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8:723.
13. Janes, P. W., Ley, S. C. and Magee, A. I. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:447.
14. Viola, A., Schroeder, S., Sakakibara, Y. and Lanzavecchia, A. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283:680.
15. Cinek, T., Hilgert, I. and Horejsi, V. 1995. An alternative way of CD4 and CD8 association with protein kinases of the Src family. Immunogenetics 41:110.
16. Horejsi, V., Drbal, K., Cebecauer, M. et al. 1999. GPI-microdomains: A role in signalling via immunoreceptors. Immunol. Today 20:356.
17. Dykstra, M., Cherukuri, A., Sohn, H. W., Tzeng, S. J. and Pierce, S. K. 2003. Location is everything: Lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21:457.
18. Horejsi, V. 2003. The roles of membrane microdomains (rafts) in T cell activation. Immunol. Rev. 191:148.
19. Pike, L. J. 2004. Lipid raft: Heterogeneity on the high seas. Biochem. J. 378:281.
20. Gomez-Mouton, C., Abad, J. L., Mira, E. et al. 2001. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl Acad. Sci. USA 98:9642.
21. Millan, J., Qaidi, M. and Alonso, M. A. 2001. Segregation of co-stimulatory components into specific T cell surface lipid rafts. Eur. J. Immunol. 31:467.
22. Schade, A. E. and Levine, A. D. 2002. Lipid raft heterogeneity in human peripheral blood T lymphoblasts: A mechanism for regulating the initiation of TCR signal transduction. J. Immunol. 168:2233.
23. Wilson, B. S., Steinberg, S. L., Liederman, K. et al. 2004. Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in native membranes. Mol. Biol. Cell 15:2580.
24. Bohuslav, J., Horejsi, V., Hansmann, C. et al. 1995. Urokinase plasminogen activator receptor, beta 2-integrins, and Src-kinases within a single receptor complex of human monocytes. J. Exp. Med. 181:1381.
25. Kiyokawa, E., Baba, T., Otsuka, N., Makino, A., Ohno, S. and Kobayashi, T. 2005. Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J. Biol. Chem. 280:24072.
26. Brugger, B., Graham, C., Leibrecht, I. et al. 2004. The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279:7530.
27. Pammer, P., Schlapak, R., Sonnleitner, M. et al. 2005. Nano-patterning of biomolecules with microscale beads. Chemphyschem 6:900,
28. Moertelmaier, M., Axmann, M., Sonnleitner, A. et al. 2003. Single molecule fluorescence microscopy on biomembranes. Recent Res. Dev. Biophys. 2:95.
29. Sako, Y. and Yanagida, T. 2003. Single-molecule visualization in cell biology. Nat. Cell Biol. (Suppl):SS1.
30. Mashanov, G. I., Tacon, D., Knight, A. E., Peckham, M. and Molloy, J. E. 2003. Visualizing single molecules inside living cells using total internal reflection fluorescence microscopy. Methods 29:142.
31. Sako, Y. 2003. Imaging single molecules in living cells for systems biology. Mol. Syst. Biol. 2:56.
32. Moertelmaier, M. A., Kögler, E. J., Hesse, J., Sonnleitner, M., Huber, L. A. and Schütz, G. J. 2002. Single molecule microscopy in living cells: Subtraction of autofluorescence based on two color recording. Single Mol. 3:225.
33. Schütz, G. J., Kada, G., Pastushenko, V. P. and Schindler, H. 2000. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J 19:892.
34. Cerny, J., Stockinger, H. and Horejsi, V. 1996. Noncovalent associations of T lymphocyte surface proteins. Eur. J. Immunol. 26:2335.
35. Seveau, S., Eddy, R. J., Maxfield, F. R. and Pierini, L. M. 2001. Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12:3550.
36. Zhang, M., Moran, M., Round, J. et al. 2005. CD45 signals outside of lipid rafts to promote ERK activation, synaptic raft clustering, and IL-2 production. J. Immunol. 174:1479.
37. Heerklotz, H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83:2693.
38. Douglass, A. D. and Vale, R. D. 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.
39. Lee, K. H., Holdorf, A. D., Dustin, M. L., Chan, A. C., Allen, P. M. and Shaw, A. S. 2002. T cell receptor signaling precedes immunological synapse formation. Science 295:1539.
40. Tuosto, L., Parolini, I., Schroder, S., Sargiacomo, M., Lanzavecchia, A. and Viola, A. 2001. Organization of plasma membrane functional rafts upon T cell activation. Eur. J. Immunol. 31:345.
41. Kakoi, H., Anniko, M., Erwall, C., Pettersson, C. A. and Jansson, B. 1996. Morphological changes in rat submandibular gland mucous cells during fixation with 10% formalin. Eur. Arch. Otorhinolaryngol. 253:214.
42. Vereb, G., Matko, J., Vamosi, G. et al. 2000. Cholesterol-dependent clustering of IL-2Ralpha and its colocalization with HLA and CD48 on T lymphoma cells suggest their functional association with lipid rafts. Proc. Natl Acad. Sci. USA 97:6013.
43. Kenworthy, A. K., Nichols, B. J., Remmert, C. L. et al. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165:735.
44. Irles, C., Symons, A., Michel, F., Bakker, T. R., van der Merwe, P. A. and Acuto, O. 2003. CD45 ectodomain controls interaction with GEMs and Lck activity for optimal TCR signaling. Nat. Immunol. 4:189.
45. Pradhan, D. and Morrow, J. 2002. The spectrin-ankyrin skeleton controls CD45 surface display and interleukin-2 production. Immunity 17:303.
46. Zhu, B., Davies, E. A., van der Merwe, P. A., Calvert, T. and Leckband, D. E. 2002. Direct measurements of heterotypic adhesion between the cell surface proteins CD2 and CD48. Biochemistry 41:12163.
47. Kaplan, A. J., Chavin, K. D., Yagita, H. et al. 1993. Production and characterization of soluble and transmembrane murine CD2. Demonstration that CD48 is a ligand for CD2 and that CD48 adhesion is regulated by CD2. J. Immunol. 151:4022.
48. Munro, S. 2003. Lipid rafts: Elusive or illusive? Cell 115:377.
49. Sharma, P., Varma, R., Sarasij, R. C. et al. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116:577.
50. Pralle, A., Keller, P., Florin, E. L., Simons, K. and Horber, J. K. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:997.
51. Lenne, P. F., Wawrezinieck, L., Conchonaud, F. et al. 2006. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25:3245.