Regulation of vesicular traffic at the T cell immune synapse: Lessons from the primary cilium

Traffic

Volumn 16, Issue 3, 2015, Pages 241-249

  Finetti, Francesca ^a   Onnis, Anna ^a   Baldari, Cosima T ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

Immune synapse; Intraflagellar transport; Primary cilium; TCR recycling; Vesicular traffic

Indexed keywords

T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

CELL FUNCTION; CELL MIGRATION; CELL TRANSPORT; CROSS FERTILIZATION; ENDOSOME; EUKARYOTIC FLAGELLUM; HUMAN; IMMUNE SYSTEM; POLARIZATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; ANIMAL; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; SYNAPSE VESICLE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CILIA; ENDOSOMES; HUMANS; IMMUNOLOGICAL SYNAPSES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SYNAPTIC VESICLES; T-LYMPHOCYTES;

EID: 84923227298     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12241     Document Type: Review

References (69)

1. Fooksman DR, Vardhana S, Vasiliver-Shamis G, Liese J, Blair DA, Waite J, Sacristan C, Victora GD, Zanin-Zhorov A, Dustin ML. Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 2010;28:79-105.
2. Griffiths GM, Tsun A, Stinchcombe JC. The immunological synapse: a focal point for endocytosis and exocytosis. J Cell Biol 2010;189:399-406.
3. Das V, Nal B, Dujeancourt A, Thoulouze MI, Galli T, Roux P, Dautry-Varsat A, Alcover A. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 2004;20:577-588.
4. Linsley PS, Bradshaw J, Greene J, Peach R, Bennett KL, Mittler RS. Intracellular trafficking of CTLA-4 and focal localization towards sites of TCR engagement. Immunity 1996;4:535-543.
5. Vardhana S, Choudhuri K, Varma R, Dustin ML. Essential role of ubiquitin and TSG101 protein in formation and function of the central supramolecular activation cluster. Immunity 2010;32:531-540.
6. Rincon E, Saez de Guinoa J, Gharbi SI, Soriano CO, Carrasco YR, Merida I. Translocation dynamics of sorting nexin 27 in activated T cells. J Cell Sci 2011;124:776-788.
7. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
8. Choudhuri K, Llodra J, Roth EW, Tsai J, Gordo S, Wucherpfennig KW, Kam LC, Stokes DL, Dustin ML. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 2014;507:118-123.
9. Pedersen LB, Rosenbaum JL. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 2008;85:23-61.
10. Finetti F, Paccani SR, Riparbelli MG, Giacomello E, Perinetti G, Pazour GJ, Rosenbaum JL, Baldari CT. Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse. Nat Cell Biol 2009;11:1332-1339.
11. Iezzi G, Karjalainen K, Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 1998;8:89-95.
12. Batista A, Millan J, Mittelbrunn M, Sanchez-Madrid F, Alonso MA. Recruitment of transferrin receptor to immunological synapse in response to TCR engagement. J Immunol 2004;172:6709-6714.
13. Molon B, Gri G, Bettella M, Gomez-Mouton C, Lanzavecchia A, Martinez AC, Manes S, Viola A. T cell costimulation by chemokine receptors. Nat Immunol 2005;6:465-471.
14. Finetti F, Patrussi L, Masi G, Onnis A, Galgano D, Lucherini OM, Pazour GJ, Baldari CT. Specific recycling receptors are targeted to the immune synapse by the intraflagellar transport system. J Cell Sci 2014;127:1924-1937.
15. Munoz P, Mittelbrunn M, de la Fuente H, Perez-Martinez M, Garcia-Perez A, Ariza-Veguillas A, Malavasi F, Zubiaur M, Sanchez-Madrid F, Sancho J. Antigen-induced clustering of surface CD38 and recruitment of intracellular CD38 to the immunologic synapse. Blood 2008;111:3653-3664.
16. Ehrlich LI, Ebert PJ, Krummel MF, Weiss A, Davis MM. Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 2002;17:809-822.
17. Bonello G, Blanchard N, Montoya MC, Aguado E, Langlet C, He HT, Nunez-Cruz S, Malissen M, Sanchez-Madrid F, Olive D, Hivroz C, Collette Y. 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.
18. Dietrich J, Hou X, Wegener AM, Geisler C. CD3 gamma contains a phosphoserine-dependent di-leucine motif involved in down-regulation of the T cell receptor. EMBO J 1994;13:2156-2166.
19. D'Oro U, Vacchio MS, Weissman AM, Ashwell JD. Activation of the Lck tyrosine kinase targets cell surface T cell antigen receptors for lysosomal degradation. Immunity 1997;7:619-628.
20. Lauritsen JP, Christensen MD, Dietrich J, Kastrup J, Odum N, Geisler C. Two distinct pathways exist for down-regulation of the TCR. J Immunol 1998;161:260-267.
21. Dumont C, Blanchard N, Di Bartolo V, Lezot N, Dufour E, Jauliac S, Hivroz C. TCR/CD3 down-modulation and zeta degradation are regulated by ZAP-70. J Immunol 2002;169:1705-1712.
22. Naramura M, Jang IK, Kole H, Huang F, Haines D, Gu H. c-Cbl and Cbl-b regulate T cell responsiveness by promoting ligand-induced TCR down-modulation. Nat Immunol 2002;3:1192-1199.
23. Crotzer VL, Mabardy AS, Weiss A, Brodsky FM. T cell receptor engagement leads to phosphorylation of clathrin heavy chain during receptor internalization. J Exp Med 2004;199:981-991.
24. von Essen M, Menne C, Nielsen BL, Lauritsen JP, Dietrich J, Andersen PS, Karjalainen K, Odum N, Geisler C. The CD3 gamma leucine-based receptor-sorting motif is required for efficient ligand-mediated TCR down-regulation. J Immunol 2002;168:4519-4523.
25. Monjas A, Alcover A, Alarcon B. Engaged and bystander T cell receptors are down-modulated by different endocytotic pathways. J Biol Chem 2004;279:55376-55384.
26. Fernandez-Arenas E, Calleja E, Martinez-Martin N, Gharbi SI, Navajas R, Garcia-Medel N, Penela P, Alcami A, Mayor F Jr, Albar JP, Alarcon B. beta-Arrestin-1 mediates the TCR-triggered re-routing of distal receptors to the immunological synapse by a PKC-mediated mechanism. EMBO J 2014;33:559-577.
27. Liu H, Rhodes M, Wiest DL, Vignali DA. On the dynamics of TCR:CD3 complex cell surface expression and downmodulation. Immunity 2000;13:665-675.
28. Kumar A, Kremer KN, Dominguez D, Tadi M, Hedin KE. Galpha13 and Rho mediate endosomal trafficking of CXCR4 into Rab11+ vesicles upon stromal cell-derived factor-1 stimulation. J Immunol 2011;186:951-958.
29. Lim SN, Bonzelius F, Low SH, Wille H, Weimbs T, Herman GA. Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins. Mol Biol Cell 2001;12:981-995.
30. Kobayashi H, Fukuda M. Arf6, Rab11 and transferrin receptor define distinct populations of recycling endosomes. Commun Integr Biol 2013;6:e25036.
31. Patino-Lopez G, Dong X, Ben-Aissa K, Bernot KM, Itoh T, Fukuda M, Kruhlak MJ, Samelson LE, Shaw S. Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J Biol Chem 2008;283:18323-18330.
32. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 2009;17:712-723.
33. Gomez TS, Billadeau DD. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell 2009;17:699-711.
34. Piotrowski JT, Gomez TS, Schoon RA, Mangalam AK, Billadeau DD. WASH knockout T cells demonstrate defective receptor trafficking, proliferation, and effector function. Mol Cell Biol 2013;33:958-973.
35. Soares H, Henriques R, Sachse M, Ventimiglia L, Alonso MA, Zimmer C, Thoulouze MI, Alcover A. Regulated vesicle fusion generates signaling nanoterritories that control T cell activation at the immunological synapse. J Exp Med 2013;210:2415-2433.
36. Larghi P, Williamson DJ, Carpier JM, Dogniaux S, Chemin K, Bohineust A, Danglot L, Gaus K, Galli T, Hivroz C. VAMP7 controls T cell activation by regulating the recruitment and phosphorylation of vesicular Lat at TCR-activation sites. Nat Immunol 2013;14:723-731.
37. Sharma N, Berbari NF, Yoder BK. Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 2008;85:371-427.
38. Finetti F, Paccani SR, Rosenbaum J, Baldari CT. Intraflagellar transport: a new player at the immune synapse. Trends Immunol 2011;32:139-145.
39. Finetti F, Baldari CT. Compartmentalization of signaling by vesicular trafficking: a shared building design for the immune synapse and the primary cilium. Immunol Rev 2013;25:97-112.
40. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007;129:1201-1213.
41. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK. The primary cilium as a complex signaling center. Curr Biol 2009;19:R526-535.
42. Follit JA, Tuft RA, Fogarty KE, Pazour GJ. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 2006;17:3781-3792.
43. Keady BT, Le YZ, Pazour GJ. IFT20 is required for opsin trafficking and photoreceptor outer segment development. Mol Biol Cell 2011;22:921-930.
44. Nachury MV, Seeley ES, Jin H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 2010;26:59-87.
45. Satir P, Mitchell DR, Jekely G. How did the cilium evolve? Curr Top Dev Biol 2008;85:63-82.
46. Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi SP, Bazan JF, Nachury MV. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 2010;141:1208-1219.
47. Westlake CJ, Baye LM, Nachury MV, Wright KJ, Ervin KE, Phu L, Chalouni C, Beck JS, Kirkpatrick DS, Slusarski DC, Sheffield VC, Scheller RH, Jackson PK. Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc Natl Acad Sci USA 2011;108:2759-2764.
48. Knodler A, Feng S, Zhang J, Zhang X, Das A, Peranen J, Guo W. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc Natl Acad Sci USA 2010;107:6346-6351.
49. Kaplan OI, Doroquez DB, Cevik S, Bowie RV, Clarke L, Sanders AA, Kida K, Rappoport JZ, Sengupta P, Blacque OE. Endocytosis genes facilitate protein and membrane transport in C. elegans sensory cilia. Curr Biol 2012;22:451-460.
50. Wang J, Morita Y, Mazelova J, Deretic D. The Arf GAP ASAP1 provides a platform to regulate Arf4- and Rab11-Rab8-mediated ciliary receptor targeting. EMBO J 2012;31:4057-4071.
51. Babbey CM, Bacallao RL, Dunn KW. Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 2010;299:F495-506.
52. Boehlke C, Bashkurov M, Buescher A, Krick T, John AK, Nitschke R, Walz G, Kuehn EW. Differential role of Rab proteins in ciliary trafficking: Rab23 regulates smoothened levels. J Cell Sci 2010;123:1460-1467.
53. Wright KJ, Baye LM, Olivier-Mason A, Mukhopadhyay S, Sang L, Kwong M, Wang W, Pretorius PR, Sheffield VC, Sengupta P, Slusarski DC, Jackson PK. An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium. Genes Dev 2011;25:2347-2360.
54. Schwarz N, Hardcastle AJ, Cheetham ME. Arl3 and RP2 mediated assembly and traffic of membrane associated cilia proteins. Vision Res 2012;75:2-4.
55. Cevik S, Hori Y, Kaplan OI, Kida K, Toivenon T, Foley-Fisher C, Cottell D, Katada T, Kontani K, Blacque OE. Joubert syndrome Arl13b functions at ciliary membranes and stabilizes protein transport in Caenorhabditis elegans. J Cell Biol 2010;188:953-969.
56. Barral DC, Garg S, Casalou C, Watts GF, Sandoval JL, Ramalho JS, Hsu VW, Brenner MB. Arl13b regulates endocytic recycling traffic. Proc Natl Acad Sci USA 2012;109:21354-21359.
57. Evans RJ, Schwarz N, Nagel-Wolfrum K, Wolfrum U, Hardcastle AJ, Cheetham ME. The retinitis pigmentosa protein RP2 links pericentriolar vesicle transport between the Golgi and the primary cilium. Hum Mol Genet 2010;19:1358-1367.
58. Omori Y, Zhao C, Saras A, Mukhopadhyay S, Kim W, Furukawa T, Sengupta P, Veraksa A, Malicki J. Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat Cell Biol 2008;10:437-444.
59. Kaplan OI, Molla-Herman A, Cevik S, Ghossoub R, Kida K, Kimura Y, Jenkins P, Martens JR, Setou M, Benmerah A, Blacque OE. The AP-1 clathrin adaptor facilitates cilium formation and functions with RAB-8 in C. elegans ciliary membrane transport. J Cell Sci 2010;123:3966-3977.
60. Takiar V, Mistry K, Carmosino M, Schaeren-Wiemers N, Caplan MJ. VIP17/MAL expression modulates epithelial cyst formation and ciliogenesis. Am J Physiol Cell Physiol 2012;303:C862-871.
61. Anton O, Batista A, Millan J, Andres-Delgado L, Puertollano R, Correas I, Alonso MA. An essential role for the MAL protein in targeting Lck to the plasma membrane of human T lymphocytes. J Exp Med 2008;205:3201-3213.
62. Calabia-Linares C, Robles-Valero J, de la Fuente H, Perez-Martinez M, Martin-Cofreces N, Alfonso-Perez M, Gutierrez-Vazquez C, Mittelbrunn M, Ibiza S, Urbano-Olmos FR, Aguado-Ballano C, Sanchez-Sorzano CO, Sanchez-Madrid F, Veiga E. Endosomal clathrin drives actin accumulation at the immunological synapse. J Cell Sci 2011;124:820-830.
63. Gorska MM, Liang Q, Karim Z, Alam R. Uncoordinated 119 protein controls trafficking of Lck via the Rab11 endosome and is critical for immunological synapse formation. J Immunol 2009;183:1675-1684.
64. Martin-Cofreces NB, Baixauli F, Lopez MJ, Gil D, Monjas A, Alarcon B, Sanchez-Madrid F. End-binding protein 1 controls signal propagation from the T cell receptor. EMBO J 2012;31:4140-4152.
65. Chen Y, Wu B, Xu L, Li H, Xia J, Yin W, Li Z, Shi D, Li S, Lin S, Shu X, Pei D. A SNX10/V-ATPase pathway regulates ciliogenesis in vitro and in vivo. Cell Res 2012;22:333-345.
66. Szalinski CM, Labilloy A, Bruns JR, Weisz OA. VAMP7 modulates ciliary biogenesis in kidney cells. PLoS One 2014;9:e86425.
67. Soares H, Lasserre R, Alcover A. Orchestrating cytoskeleton and intracellular vesicle traffic to build functional immunological synapses. Immunol Rev 2013;256:118-132.
68. de la Roche M, Ritter AT, Angus KL, Dinsmore C, Earnshaw CH, Reiter JF, Griffiths GM. Hedgehog signaling controls T cell killing at the immunological synapse. Science 2013;342:1247-1250.
69. Wood CR, Huang K, Diener DR, Rosenbaum JL. The cilium secretes bioactive ectosomes. Curr Biol 2013;23:906-911.