Compartmentalization in T-cell signalling: Membrane microdomains and polarity orchestrate signalling and morphology

Immunology and Cell Biology

Volumn 84, Issue 1, 2006, Pages 107-113

  Russell, Sarah ^a,b   Oliaro, Jane ^a  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Cell polarity; Immunological synapse; Lipid rafts; Scribble

Indexed keywords

APC PROTEIN; CELL SURFACE PROTEIN; CELL SURFACE RECEPTOR; F ACTIN; GLYCOGEN SYNTHASE KINASE 3; GUANOSINE TRIPHOSPHATASE; LAT PROTEIN; PROTEIN CDC42; PROTEIN KINASE C; RAC1 PROTEIN; RHO FACTOR; SCAFFOLD PROTEIN; SHORT HAIRPIN RNA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT;

ACTIN POLYMERIZATION; CELL COMPARTMENTALIZATION; CELL FATE; CELL FUNCTION; CELL MEMBRANE; CELL MOTILITY; CELL POLARITY; CELL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; LIPID RAFT; MICROTUBULE ORGANIZING CENTER; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

CELL COMPARTMENTATION; CELL POLARITY; HUMANS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 33645075194     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1111/j.1440-1711.2005.01415.x     Document Type: Review

References (94)

1. Jun JE Goodnow CC Scaffolding of antigen receptors for immunogenic versus tolerogenic signaling Nat. Immunol 2003 4 1057 64
2. Harder T Lipid raft domains and protein networks in T-cell receptor signal transduction Curr. Opin. Immunol 2004 16 353 9
3. Abraham RT Weiss A Jurkat T cells and development of the T-cell receptor signalling paradigm Nat. Rev. Immunol 2004 4 301 8
4. He HT Lellouch A Marguet D Lipid rafts and the initiation of T cell receptor signaling Semin. Immunol 2005 17 23 33
5. Lichtenberg D Goni FM Heerklotz H Detergent-resistant membranes should not be identified with membrane rafts Trends Biochem. Sci 2005 30 430 36
6. Bunnell SC Hong DI Kardon JR et al T cell receptor ligation induces the formation of dynamically regulated signaling assemblies J. Cell. Biol 2002 158 1263 75
7. Glebov OO Nichols BJ Lipid raft proteins have a random distribution during localized activation of the T-cell receptor Nat. Cell Biol 2004 6 238 43
8. Mayor S Rao M Rafts: scale-dependent, active lipid organization at the cell surface Traffic 2004 5 231 40
9. Sharma P Varma R Sarasij RC et al Nanoscale organization of multiple GPI-anchored proteins in living cell membranes Cell 2004 116 577 89
10. Douglass AD Vale RD 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 50
11. 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 31
12. Gaus K Gratton E Kable EP et al Visualizing lipid structure and raft domains in living cells with two-photon microscopy Proc. Natl Acad. Sci. USA 2003 100 15 554 9
13. Campi G Varma R Dustin ML Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling J. Exp. Med 2005 202 1031 6
14. del Pozo MA Nieto M Serrador JM et al The two poles of the lymphocyte: specialized cell compartments for migration and recruitment Cell Adhes. Commun 1998 6 125 33
15. Vicente-Manzanares M Sancho D Yanez-Mo M Sanchez-Madrid F The leukocyte cytoskeleton in cell migration and immune interactions Int. Rev. Cytol 2002 216 233 89
16. Biberfeld P Uropod formation in phytohaemagglutinin (PHA) stimulated lymphocytes Exp. Cell Res 1971 66 433 45
17. Bruehl RE Moore KL Lorant DE et al Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1 J. Leukoc. Biol 1997 61 489 99
18. del Pozo MA Cabanas C Montoya MC Ager A Sanchez-Mateos P Sanchez-Madrid F ICAMs redistributed by chemokines to cellular uropods as a mechanism for recruitment of T lymphocytes J. Cell Biol 1997 137 493 508
19. del Pozo MA Sanchez-Mateos P Sanchez-Madrid F Cellular polarization induced by chemokines: a mechanism for leukocyte recruitment? Immunol. Today 1996 17 127 31
20. McFarland W Microspikes on the lymphocyte uropod Science 1969 163 818 20
21. Ratner S Sherrod WS Lichlyter D Microtubule retraction into the uropod and its role in T cell polarization and motility J. Immunol 1997 159 1063 7
22. Savage ND Kimzey SL Bromley SK Johnson KG Dustin ML Green JM Polar redistribution of the sialoglycoprotein CD43: implications for T cell function J. Immunol 2002 168 3740 46
23. Sanchez-Madrid F del Pozo MA Leukocyte polarization in cell migration and immune interactions EMBO J 1999 18 501 11
24. Schmalstieg FC Goldman AS Significance of uropod-bearing lymphocytes J. Pediatr 1979 94 343 4
25. Dustin ML Shmoos, rafts, and uropods - the many facets of cell polarity Cell 2002 110 13 18
26. Meili R Firtel RA Two poles and a compass Cell 2003 114 153 6
27. Jacobelli J Chmura SA Buxton DB Davis MM Krummel MF A single class II myosin modulates T cell motility and stopping, but not synapse formation Nat. Immunol 2004 5 531 8
28. van der Merwe PA Formation and function of the immunological synapse Curr. Opin. Immunol 2002 14 293 8
29. van Der Merwe PA Davis SJ Immunology. The immunological synapse - a multitasking system Science 2002 295 1479 80
30. Friedl P Storim J Diversity in immune-cell interactions: states and functions of the immunological synapse Trends Cell. Biol 2004 14 557 67
31. Davis DM Dustin ML What is the importance of the immunological synapse? Trends Immunol 2004 25 323 7
32. Stinchcombe JC Griffiths GM The role of the secretory immunological synapse in killing by CD8+ CTL Semin. Immunol 2003 15 301 5
33. O'Keefe JP Blaine K Alegre ML Gajewski TF Formation of a central supramolecular activation cluster is not required for activation of naive CD8+ T cells Proc. Natl Acad. Sci. USA 2004 101 9351 6
34. Purbhoo MA Irvine DJ Huppa JB Davis MM T cell killing does not require the formation of a stable mature immunological synapse Nat. Immunol 2004 5 524 30
35. Lee KH Dinner AR Tu C et al The immunological synapse balances T cell receptor signaling and degradation Science 2003 302 1218 22
36. Maldonado RA Irvine DJ Schreiber R Glimcher LH A role for the immunological synapse in lineage commitment of CD4 lymphocytes Nature 2004 431 527 32
37. Depoil D Zaru R Guiraud M et al Immunological synapses are versatile structures enabling selective T cell polarization Immunity 2005 22 185 94
38. Wei X Tromberg BJ Cahalan MD 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 1999 96 8471 6
39. Dustin ML Stop and go traffic to tune T cell responses Immunity 2004 21 305 14
40. Cahalan MD STOP! In the name of positive selection Nat. Immunol 2005 6 126 8
41. Cullinan P Sperling AI Burkhardt JK The distal pole complex: a novel membrane domain distal to the immunological synapse Immunol. Rev 2002 189 111 22
42. Allenspach EJ Cullinan P Tong J et al ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse Immunity 2001 15 739 50
43. Macara IG Parsing the polarity code Nat. Rev. Mol. Cell Biol 2004 5 220 31
44. Ludford-Menting MJ Oliaro J Sacirbegovic F et al A network of PDZ-containing proteins regulates T cell polarity and morphology during migration and immunological synapse formation Immunity 2005 22 737 48
45. Nelson WJ Adaptation of core mechanisms to generate cell polarity Nature 2003 422 766 74
46. Bilder D Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors Genes Dev 2004 18 1909 25
47. Humbert P Russell S Richardson H Dlg, Scribble and Lgl in cell polarity, cell proliferation and cancer Bioessays 2003 25 542 53
48. Ivetic A Ridley AJ Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes Immunology 2004 112 165 76
49. Bilder D Schober M Perrimon N Integrated activity of PDZ protein complexes regulates epithelial polarity Nat. Cell Biol 2003 5 53 8
50. Tanentzapf G Tepass U Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization Nat. Cell Biol 2003 5 46 52
51. Plant PJ Fawcett JP Lin DC et al A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl Nat. Cell Biol 2003 5 301 8
52. Hurd TW Gao L Roh MH Macara IG Margolis B Direct interaction of two polarity complexes implicated in epithelial tight junction assembly Nat. Cell Biol 2003 5 137 42
53. Etienne-Manneville S Hall A Rho GTPases in cell biology Nature 2002 420 629 35
54. Jaffe AB Hall A Cell biology. Smurfing at the leading edge Science 2003 302 1690 91
55. Garrard SM Capaldo CT Gao L Rosen MK Macara IG Tomchick DR Structure of Cdc42 in a complex with the GTPase-binding domain of the cell polarity protein, Par6 EMBO J 2003 22 1125 33
56. Etienne-Manneville S Hall A Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta Cell 2001 106 489 98
57. Joberty G Petersen C Gao L Macara IG The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42 Nat. Cell Biol 2000 2 531 9
58. Etienne-Manneville S Hall A Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity Nature 2003 421 753 6
59. Cantrell DA GTPases and T cell activation Immunol. Rev 2003 192 122 30
60. Giagulli C Scarpini E Ottoboni L et al RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing Immunity 2004 20 25 35
61. Phee H Abraham RT Weiss A Dynamic recruitment of PAK1 to the immunological synapse is mediated by PIX independently of SLP-76 and Vav1 Nat. Immunol 2005 6 608 17
62. Audebert S Navarro C Nourry C et al Mammalian Scribble forms a tight complex with the betaPIX exchange factor Curr. Biol 2004 14 987 95
63. Parnas D Haghighi AP Fetter RD Kim SW Goodman CS Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix Neuron 2001 32 415 24
64. Albertson R Doe CQ Dlg, Scrib and Lgl regulate neuroblast cell size and mitotic spindle asymmetry Nat. Cell Biol 2003 5 166 70
65. Barros CS Phelps CB Brand AH Drosophila nonmuscle myosin II promotes the asymmetric segregation of cell fate determinants by cortical exclusion rather than active transport Dev. Cell 2003 5 829 40
66. Peng CY Manning L Albertson R Doe CQ The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts Nature 2000 408 596 600
67. Faure S Salazar-Fontana LI Semichon M et al ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation Nat. Immunol 2004 5 272 9
68. Medina E Williams J Klipfell E Zarnescu D Thomas G Le Bivic A Crumbs interacts with moesin and beta(Heavy)-spectrin in the apical membrane skeleton of Drosophila J. Cell Biol 2002 158 941 51
69. Polesello C Payre F Small is beautiful: what flies tell us about ERM protein function in development Trends Cell Biol 2004 14 294 302
70. Hanada T Takeuchi A Sondarva G Chishti AH Protein 4.1-mediated membrane targeting of human discs large in epithelial cells J. Biol. Chem 2003 278 34 445 50
71. Kim E Sheng M PDZ domain proteins of synapses Nat. Rev. Neurosci 2004 5 771 81
72. Husi H Grant SG Isolation of 2000-kDa complexes of N-methyl-D-aspartate receptor and postsynaptic density 95 from mouse brain J. Neurochem 2001 77 281 91
73. Xavier R Rabizadeh S Ishiguro K et al Discs large (Dlg1) complexes in lymphocyte activation J. Cell Biol 2004 166 173 8
74. Round JL Tomassian T Zhang M Patel V Schoenberger SP Miceli MC Dlgh1 coordinates actin polymerization, synaptic T cell receptor and lipid raft aggregation, and effector function in T cells J. Exp. Med 2005 201 419 30
75. Rivas FV O'Keefe JP Alegre ML Gajewski TF Actin cytoskeleton regulates calcium dynamics and NFAT nuclear duration Mol. Cell Biol 2004 24 1628 39
76. Zhou FQ Zhou J Dedhar S Wu YH Snider WD NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC Neuron 2004 42 897 912
77. Jun JE Wilson LE Vinuesa CG et al Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis Immunity 2003 18 751 62
78. Itoh K Sakakibara M Yamasaki S et al Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly J. Immunol 2002 168 541 4
79. Tang P Cheng TP Agnello D et al Cybr, a cytokine-inducible protein that binds cytohesin-1 and regulates its activity Proc. Natl Acad. Sci. USA 2002 99 2625 9
80. Boehm T Hofer S Winklehner P et al Attenuation of cell adhesion in lymphocytes is regulated by CYTIP, a protein which mediates signal complex sequestration EMBO J 2003 22 1014 24
81. Meder D Shevchenko A Simons K Fullekrug J Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells J. Cell Biol 2005 168 303 13
82. Cha B Kenworthy A Murtazina R Donowitz M The lateral mobility of NHE3 on the apical membrane of renal epithelial OK cells is limited by the PDZ domain proteins NHERF1/2, but is dependent on an intact actin cytoskeleton as determined by FRAP J. Cell Sci 2004 117 3353 65
83. Brdickova N Brdicka T Andera L et al Interaction between two adapter proteins, PAG and EBP50: a possible link between membrane rafts and actin cytoskeleton FEBS Lett 2001 507 133 6
84. Millan J Montoya MC Sancho D Sanchez-Madrid F Alonso MA Lipid rafts mediate biosynthetic transport to the T lymphocyte uropod subdomain and are necessary for uropod integrity and function Blood 2002 99 978 84
85. Gomez-Mouton C Abad JL Mira E et al Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization Proc. Natl Acad. Sci. USA 2001 98 9642 7
86. Hanada T Lin L Chandy KG Oh SS Chishti AH Human homologue of the Drosophila discs large tumor suppressor binds to p56lck tyrosine kinase and Shaker type Kv1.3 potassium channel in T lymphocytes J. Biol. Chem 1997 272 26 899 904
87. Ralston KJ Hird SL Zhang X et al The LFA-1-associated molecule PTA-1(CD226) on T cells forms a dynamic molecular complex with protein 4.1G and human discs large J. Biol. Chem 2004 171 121 31
88. Hanada T Lin L Tibaldi EV Reinherz EL Chishti AH GAKIN, a novel kinesin-like protein associates with the human homologue of the Drosophila discs large tumor suppressor in T lymphocytes J. Biol. Chem 2000 275 28 774 84
89. Tibaldi EV Salgia R Reinherz EL CD2 molecules redistribute to the uropod during T cell scanning: implications for cellular activation and immune surveillance Proc. Natl Acad. Sci. USA 2002 99 7582 7
90. Russell S CD46: a complement regulator and pathogen receptor that mediates links between innate and acquired immune function Tissue Antigens 2004 64 111 18
91. Kemper C Chan AC Green JM Brett KA Murphy KM Atkinson JP Activation of human CD4(+) cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype Nature 2003 421 388 92
92. Marie JC Astier AL Rivailler P Rabourdin-Combe C Wild TF Horvat B Linking innate and acquired immunity: divergent role of CD46 cytoplasmic domains in T cell induced inflammation Nat. Immunol 2002 3 659 66
93. Zaffran Y Destaing O Roux A et al CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signal-regulated kinase mitogen-activated protein kinase J. Immunol 2001 167 6780 85
94. Ludford-Menting MJ Thomas SJ Crimeen B et al A functional interaction between CD46 and DLG4: a role for DLG4 in epithelial polarization J. Biol. Chem 2002 277 4477 84