Membrane trafficking and signaling: Two sides of the same coin

Seminars in Cell and Developmental Biology

Volumn 23, Issue 2, 2012, Pages 154-164

  Gonnord, Pauline ^a   Blouin, Cédric M ^b,c   Lamaze, Christophe ^b,c  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b INSTITUT CURIE   (France)

^c INSTITUT CURIE   (France)

Author keywords

Clustering; Endocytosis; Imaging; Signaling; Trafficking

Indexed keywords

ACTIN; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GALECTIN; LIPID; PROTEIN; TETRASPANIN;

ACTIN POLYMERIZATION; BIOGENESIS; CAVEOLA; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SELECTION; CLUSTER ANALYSIS; CRYSTAL STRUCTURE; ENDOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOLOGICAL SYNAPSE; LIPID RAFT; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NANOIMAGING; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84858792382     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.11.002     Document Type: Review

References (119)

1. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 1996, 274:2086-2089.
2. Miaczynska M., Pelkmans L., Zerial M. Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 2004, 16:400-406.
3. Sorkin A., Goh L.K. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 2009, 315:683-696.
4. Marchetti M., Monier M.N., Fradagrada A., Mitchell K., Baychelier F., Eid P., et al. Stat-mediated Signaling Induced by Type I and Type II Interferons (IFNs) is differentially controlled through lipid microdomain association and clathrin-dependent endocytosis of IFN receptors. Mol Biol Cell 2006, 17:2896-2909.
5. Damke H., Baba T., Warnock D.E., Schmid S.L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994, 127:915-934.
6. McMahon H.T., Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011, 12:517-533.
7. Benmerah A., Lamaze C. Clathrin-coated pits: vive la différence?. Traffic 2007, 8:970-982.
8. Ehrlich M., Boll W., Van Oijen A., Hariharan R., Chandran K., Nibert M.L., et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004, 118:591-605.
9. Mettlen M., Loerke D., Yarar D., Danuser G., Schmid S.L. Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 2010, 188:919-933.
10. Lamaze C., Schmid S.L. The emergence of clathrin-independent pinocytic pathways. Curr Opin Cell Biol 1995, 7:573-580.
11. Johannes L., Lamaze C. Clathrin-dependent or not: is it still the question?. Traffic 2002, 3:443-451.
12. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
13. Sandvig K., Pust S., Skotland T., van Deurs B. Clathrin-independent endocytosis: mechanisms and function. Curr Opin Cell Biol 2011, 23:413-420.
14. Mayor S., Pagano R.E. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007, 8:603-612.
15. Parton R.G., Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007, 8:185-194.
16. Lajoie P., Goetz J.G., Dennis J.W., Nabi I.R. Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. J Cell Biol 2009, 185:381-385.
17. Pelkmans L., Kartenbeck J., Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001, 3:473-483.
18. Nabi I.R., Le P.U. Caveolae/raft-dependent endocytosis. J Cell Biol 2003, 161:673-677.
19. Hayer A., Stoeber M., Ritz D., Engel S., Meyer H.H., Helenius A. Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 2010, 191:615-629.
20. Sinha B., Koster D., Ruez R., Gonnord P., Bastiani M., Abankwa D., et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011, 144:402-413.
21. Hansen C.G., Nichols B.J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 2010, 20:177-186.
22. Senju Y., Itoh Y., Takano K., Hamada S., Suetsugu S. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 2011, 124:2032-2040.
23. Hansen C.G., Howard G., Nichols B.J. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 2011, 124:2777-2785.
24. Bastiani M., Liu L., Hill M.M., Jedrychowski M.P., Nixon S.J., Lo H.P., et al. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 2009, 185:1259-1273.
25. Kwon H., Jeong K., Hwang E.M., Park J.Y., Pak Y. A novel domain of caveolin-2 that controls nuclear targeting: regulation of insulin-specific ERK activation and nuclear translocation by caveolin-2. J Cell Mol Med 2010, 3.
26. Pelkmans L., Zerial M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 2005, 436:128-133.
27. Lingwood D., Simons K. Lipid rafts as a membrane-organizing principle. Science 2010, 327:46-50.
28. Lamaze C., Dujeancourt A., Baba T., Lo C.G., Benmerah A., Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 2001, 7:661-671.
29. Gibert M., Monier M.N., Ruez R., Hale M.L., Stiles B.G., Benmerah A., et al. Endocytosis and toxicity of clostridial binary toxins depend on a clathrin-independent pathway regulated by Rho-GDI. Cell Microbiol 2011, 13:154-170.
30. Grassart A., Dujeancourt A., Lazarow P.B., Dautry-Varsat A., Sauvonnet N. Clathrin-independent endocytosis used by the IL-2 receptor is regulated by Rac1, Pak1 and Pak2. EMBO Rep 2008, 9:356-362.
31. Guo F., Hildeman D., Tripathi P., Velu C.S., Grimes H.L., Zheng Y. Coordination of IL-7 receptor and T-cell receptor signaling by cell-division cycle 42 in T-cell homeostasis. Proc Natl Acad Sci U S A 2011, 107:18505-18510.
32. Johannes L., Popoff V. Tracing the retrograde route in protein trafficking. Cell 2008, 135:1175-1187.
33. Lauvrak S.U., Walchli S., Iversen T.G., Slagsvold H.H., Torgersen M.L., Spilsberg B., et al. Shiga toxin regulates its entry in a Syk-dependent manner. Mol Biol Cell 2006, 17:1096-1109.
34. Walchli S., Skanland S.S., Gregers T.F., Lauvrak S.U., Torgersen M.L., Ying M., et al. The Mitogen-activated protein kinase p38 links Shiga Toxin-dependent signaling and trafficking. Mol Biol Cell 2008, 19:95-104.
35. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 2006, 8:46-54.
36. Frick M., Bright N.A., Riento K., Bray A., Merrified C., Nichols B.J. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 2007, 17:1151-1156.
37. Mineo C., Gill G.N., Anderson R.G. Regulated migration of epidermal growth factor receptor from caveolae. J Biol Chem 1999, 274:30636-30643.
38. Grande-Garcia A., del Pozo M.A. Caveolin-1 in cell polarization and directional migration. Eur J Cell Biol 2008, 87:641-647.
39. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., Wrana J.L. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003, 5:410-421.
40. Romer W., Berland L., Chambon V., Gaus K., Windschiegl B., Tenza D., et al. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 2007, 450:670-675.
41. Romer W., Pontani L.L., Sorre B., Rentero C., Berland L., Chambon V., et al. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 2010, 140:540-553.
42. Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, Chai W, et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 2009; 12:11-8; suppl. pp. 1-2.
43. Sharma P., Varma R., Sarasij R.C., Ira, Gousset K., Krishnamoorthy G., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 2004, 116:577-589.
44. Johannes L., Romer W. Shiga toxins - from cell biology to biomedical applications. Nat Rev Microbiol 2009, 8:105-116.
45. Claudinon J., Monier M.N., Lamaze C. Interfering with interferon receptor sorting and trafficking: impact on signaling. Biochimie 2007, 89:735-743.
46. Tolar P., Sohn H.W., Liu W., Pierce S.K. The molecular assembly and organization of signaling active B-cell receptor oligomers. Immunol Rev 2009, 232:34-41.
47. Subramaniam P.S., Johnson H.M. Lipid microdomains are required sites for the selective endocytosis and nuclear translocation of IFN-gamma, its receptor chain IFN-gamma receptor-1, and the phosphorylation and nuclear translocation of STAT1alpha. J Immunol 2002, 169:1959-1969.
48. Sigismund S., Woelk T., Puri C., Maspero E., Tacchetti C., Transidico P., et al. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 2005, 102:2760-2765.
49. Berkers J.A., van Bergen en Henegouwen P.M., Boonstra J. Three classes of epidermal growth factor receptors on HeLa cells. J Biol Chem 1991, 266:922-927.
50. Roepstorff K., Grandal M.V., Henriksen L., Knudsen S.L., Lerdrup M., Grovdal L., et al. Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 2009, 10:1115-1127.
51. Avraham R., Yarden Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 2011, 12:104-117.
52. Chung I., Akita R., Vandlen R., Toomre D., Schlessinger J., Mellman I. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 2010, 464:783-787.
53. Charrin S., le Naour F., Silvie O., Milhiet P.E., Boucheix C., Rubinstein E. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 2009, 420:133-154.
54. Yanez-Mo M., Barreiro O., Gordon-Alonso M., Sala-Valdes M., Sanchez-Madrid F. Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 2009, 19:434-446.
55. Delacour D., Koch A., Jacob R. The role of galectins in protein trafficking. Traffic 2009, 10:1405-1413.
56. Jaqaman K., Kuwata H., Touret N., Collins R., Trimble W.S., Danuser G., et al. Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 2011, 146:593-606.
57. Suzuki K.G., Fujiwara T.K., Sanematsu F., Iino R., Edidin M., Kusumi A. GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J Cell Biol 2007, 177:717-730.
58. Lajoie P., Partridge E.A., Guay G., Goetz J.G., Pawling J., Lagana A., et al. Plasma membrane domain organization regulates EGFR signaling in tumor cells. J Cell Biol 2007, 179:341-356.
59. Soldati T., Schliwa M. Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 2006, 7:897-908.
60. Lavoie J.N., Landry M.C., Faure R.L., Champagne C. Src-family kinase signaling, actin-mediated membrane trafficking and organellar dynamics in the control of cell fate: lessons to be learned from the adenovirus E4orf4 death factor. Cell Signal 2010, 22:1604-1614.
61. Hupalowska A, Miaczynska M. The new faces of endocytosis in signaling. Traffic 2011.
62. Jares-Erijman E.A., Jovin T.M. Imaging molecular interactions in living cells by FRET microscopy. Curr Opin Chem Biol 2006, 10:409-416.
63. Sorkin A., McClure M., Huang F., Carter R. Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr Biol 2000, 10:1395-1398.
64. Nakamura T., Matsuda M. In vivo imaging of signal transduction cascades with probes based on Forster resonance energy transfer (FRET). Curr Protoc Cell Biol 2009, Chapter 14: Unit 14 0.
65. Calebiro D., Nikolaev V.O., Gagliani M.C., de Filippis T., Dees C., Tacchetti C., et al. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 2009, 7:e1000172.
66. Lu A., Tebar F., Alvarez-Moya B., Lopez-Alcala C., Calvo M., Enrich C., et al. A clathrin-dependent pathway leads to KRas signaling on late endosomes en route to lysosomes. J Cell Biol 2009, 184:863-879.
67. Elson D., Requejo-Isidro J., Munro I., Reavell F., Siegel J., Suhling K., et al. Time-domain fluorescence lifetime imaging applied to biological tissue. Photochem Photobiol Sci 2004, 3:795-801.
68. Treanor B., Lanigan P.M., Kumar S., Dunsby C., Munro I., Auksorius E., et al. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J Cell Biol 2006, 174:153-161.
69. Borgdorff A.J., Choquet D. Regulation of AMPA receptor lateral movements. Nature 2002, 417:649-653.
70. Dahan M., Levi S., Luccardini C., Rostaing P., Riveau B., Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 2003, 302:442-445.
71. Bats C., Groc L., Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007, 53:719-734.
72. Opazo P., Labrecque S., Tigaret C.M., Frouin A., Wiseman P.W., De Koninck P., et al. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 2010, 67:239-252.
73. Valentine C.D., Haggie P.M. Confinement of {beta}1- and {beta}2-adrenergic receptors in the plasma membrane of cardiomyocyte-like H9c2 cells is mediated by selective interactions with PDZ domain and A-kinase anchoring proteins but not caveolae. Mol Biol Cell 2011, 22:2970-2982.
74. Kusumi A., Ike H., Nakada C., Murase K., Fujiwara T. Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules. Semin Immunol 2005, 17:3-21.
75. Liu B.R., Huang Y.W., Winiarz J.G., Chiang H.J., Lee H.J. Intracellular delivery of quantum dots mediated by a histidine- and arginine-rich HR9 cell-penetrating peptide through the direct membrane translocation mechanism. Biomaterials 2011, 32:3520-3537.
76. Huang B., Babcock H., Zhuang X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2010, 143:1047-1058.
77. Schermelleh L., Heintzmann R., Leonhardt H. A guide to super-resolution fluorescence microscopy. J Cell Biol 2010, 190:165-175.
78. Shroff H., Galbraith C.G., Galbraith J.A., Betzig E. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 2008, 5:417-423.
79. Westphal V., Rizzoli S.O., Lauterbach M.A., Kamin D., Jahn R., Hell S.W. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 2008, 320:246-249.
80. Kner P., Chhun B.B., Griffis E.R., Winoto L., Gustafsson M.G. Super-resolution video microscopy of live cells by structured illumination. Nat Methods 2009, 6:339-342.
81. Pellett P.A., Sun X., Gould T.J., Rothman J.E., Xu M.Q., Correa I.R., et al. Two-color STED microscopy in living cells. Biomed Opt Express 2011, 2:2364-2371.
82. Willig K.I., Stiel A.C., Brakemann T., Jakobs S., Hell S.W. Dual-label STED nanoscopy of living cells using photochromism. Nano Lett 2011.
83. Pinaud F., Dahan M. Targeting and imaging single biomolecules in living cells by complementation-activated light microscopy with split-fluorescent proteins. Proc Natl Acad Sci U S A 2011, 108:E201-E210.
84. Lasserre R., Guo X.J., Conchonaud F., Hamon Y., Hawchar O., Bernard A.M., et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 2008, 4:538-547.
85. Smith-Garvin J.E., Koretzky G.A., Jordan M.S. T cell activation. Annu Rev Immunol 2009, 27:591-619.
86. Fooksman D.R., Vardhana S., Vasiliver-Shamis G., Liese J., Blair D.A., Waite J., et al. Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 2010, 28:79-105.
87. Huse M., Klein L.O., Girvin A.T., Faraj J.M., Li Q.J., Kuhns M.S., et al. Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 2007, 27:76-88.
88. Campi G., Varma R., Dustin M.L. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J Exp Med 2005, 202:1031-1036.
89. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., et al. The immunological synapse: a molecular machine controlling T cell activation. Science 1999, 285:221-227.
90. Valitutti S., Muller S., Cella M., Padovan E., Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 1995, 375:148-151.
91. Choudhuri K., Dustin M.L. Signaling microdomains in T cells. FEBS Lett 2010, 584:4823-4831.
92. Bunnell S.C., Hong D.I., Kardon J.R., Yamazaki T., McGlade C.J., Barr V.A., et al. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 2002, 158:1263-1275.
93. Douglass A.D., Vale R.D. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 2005, 121:937-950.
94. Williamson D.J., Owen D.M., Rossy J., Magenau A., Wehrmann M., Gooding J.J., et al. Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat Immunol 2011, 12:655-662.
95. Lillemeier B.F., Mortelmaier M.A., Forstner M.B., Huppa J.B., Groves J.T., Davis M.M. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 2010, 11:90-96.
96. Bonello G., Blanchard N., Montoya M.C., Aguado E., Langlet C., He H.T., et al. Dynamic recruitment of the adaptor protein LAT: LAT exists in two distinct intracellular pools and controls its own recruitment. J Cell Sci 2004, 117:1009-1016.
97. Billadeau D.D., Nolz J.C., Gomez T.S. Regulation of T-cell activation by the cytoskeleton. Nat Rev Immunol 2007, 7:131-143.
98. Purbhoo M.A., Liu H., Oddos S., Owen D.M., Neil M.A., Pageon S.V., et al. Dynamics of subsynaptic vesicles and surface microclusters at the immunological synapse. Sci Signal 2010, 3:ra36.
99. Saito T., Yokosuka T. Immunological synapse and microclusters: the site for recognition and activation of T cells. Curr Opin Immunol 2006, 18:305-313.
100. Taner S.B., Onfelt B., Pirinen N.J., McCann F.E., Magee A.I., Davis D.M. Control of immune responses by trafficking cell surface proteins, vesicles and lipid rafts to and from the immunological synapse. Traffic 2004, 5:651-661.
101. Harder T., Rentero C., Zech T., Gaus K. Plasma membrane segregation during T cell activation: probing the order of domains. Curr Opin Immunol 2007, 19:470-475.
102. Owen D.M., Gaus K., Magee A.I., Cebecauer M. Dynamic organization of lymphocyte plasma membrane: lessons from advanced imaging methods. Immunology 2010, 131:1-8.
103. Gaus K., Chklovskaia E., Fazekas de St Groth B., Jessup W., Harder T. Condensation of the plasma membrane at the site of T lymphocyte activation. J Cell Biol 2005, 171:121-131.
104. Lin J., Shaw A.S. Getting downstream without a Raft. Cell 2005, 121:815-816.
105. Valitutti S., Dessing M., Aktories K., Gallati H., Lanzavecchia A. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J Exp Med 1995, 181:577-584.
106. Varma R., Campi G., Yokosuka T., Saito T., Dustin M.L. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 2006, 25:117-127.
107. Seminario M.C., Bunnell S.C. Signal initiation in T-cell receptor microclusters. Immunol Rev 2008, 221:90-106.
108. Gomez T.S., Billadeau D.D. T cell activation and the cytoskeleton: you cannot have one without the other. Adv Immunol 2008, 97:1-64.
109. Kaizuka Y., Douglass A.D., Varma R., Dustin M.L., Vale R.D. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc Natl Acad Sci U S A 2007, 104:20296-20301.
110. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86.
111. Monjas A., Alcover A., Alarcon B., Engaged, bystander T cell receptors are down-modulated by different endocytotic pathways. J Biol Chem 2004, 279:55376-55384.
112. Balagopalan L., Barr V.A., Samelson L.E. Endocytic events in TCR signaling: focus on adapters in microclusters. Immunol Rev 2009, 232:84-98.
113. Martinez-Martin N., Fernandez-Arenas E., Cemerski S., Delgado P., Turner M., Heuser J., et al. T Cell Receptor Internalization from the Immunological Synapse Is Mediated by TC21 and RhoG GTPase-Dependent Phagocytosis. Immunity 2011, 35:208-222.
114. Barr V.A., Balagopalan L., Barda-Saad M., Polishchuk R., Boukari H., Bunnell S.C., et al. T-cell antigen receptor-induced signaling complexes: internalization via a cholesterol-dependent endocytic pathway. Traffic 2006, 7:1143-1162.
115. Vardhana S., Choudhuri K., Varma R., Dustin M.L. Essential role of ubiquitin and TSG101 protein in formation and function of the central supramolecular activation cluster. Immunity 2010, 32:531-540.
116. Jones E.L., Demaria M.C., Wright M.D. Tetraspanins in cellular immunity. Biochem Soc Trans 2011, 39:506-511.
117. Vogt A.B., Spindeldreher S., Kropshofer H. Clustering of MHC-peptide complexes prior to their engagement in the immunological synapse: lipid raft and tetraspan microdomains. Immunol Rev 2002, 189:136-151.
118. + T-cell activation at the immunological synapse. Proc Natl Acad Sci U S A 2009, 106:14496-14501.
119. Grigorian A., Torossian S., Demetriou M. T-cell growth, cell surface organization, and the galectin-glycoprotein lattice. Immunol Rev 2009, 230:232-246.