What counts in the immunological synapse?

Molecular Cell

Volumn 54, Issue 2, 2014, Pages 255-262

  Dustin, Michael L ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR;

ANTIGEN SPECIFICITY; B LYMPHOCYTE; EXOSOME; HELPER CELL; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE COUNT; PLASMA CELL; POSITIVE FEEDBACK; REVIEW; T LYMPHOCYTE;

ANTIGEN PRESENTATION; ASYMMETRIC CELL DIVISION; B-LYMPHOCYTES; CELL MEMBRANE; EXOSOMES; MAJOR HISTOCOMPATIBILITY COMPLEX; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84899138628     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.04.001     Document Type: Review

References (65)

1. Ahmed K.A., Xie Y., Zhang X., Xiang J. Acquired pMHC I complexes greatly enhance CD4(+) Th cell's stimulatory effect on CD8(+) Tcell-mediated diabetes in transgenic RIP-mOVA mice. Cell. Mol. Immunol. 2008, 5:407-415.
2. Aleksic M., Dushek O., Zhang H., Shenderov E., Chen J.L., Cerundolo V., Coombs D., van der Merwe P.A. Dependence of Tcell antigen recognition on Tcell receptor-peptide MHC confinement time. Immunity 2010, 32:163-174.
3. Babbitt B.P., Allen P.M., Matsueda G., Haber E., Unanue E.R. Binding of immunogenic peptides to Ia histocompatibility molecules. Nature 1985, 317:359-361.
4. Batista F.D., Neuberger M.S. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 1998, 8:751-759.
5. Batista F.D., Neuberger M.S. B cells extract and present immobilized antigen: implications for affinity discrimination. EMBO J. 2000, 19:513-520.
6. Batista F.D., Iber D., Neuberger M.S. B cells acquire antigen from target cells after synapse formation. Nature 2001, 411:489-494.
7. Bell G.I. Models for the specific adhesion of cells to cells. Science 1978, 200:618-627.
8. Bjorkman P.J., Saper M.A., Samraoui B., Bennett W.S., Strominger J.L., Wiley D.C. The foreign antigen binding site and Tcell recognition regions of class I histocompatibility antigens. Nature 1987, 329:512-518.
9. Blanchard N., Lankar D., Faure F., Regnault A., Dumont C., Raposo G., Hivroz C. TCR activation of human Tcells induces the production of exosomes bearing the TCR/CD3/zeta complex. J.Immunol. 2002, 168:3235-3241.
10. Boisvert J., Edmondson S., Krummel M.F. Immunological synapse formation licenses CD40-CD40L accumulations at T-APC contact sites. J.Immunol. 2004, 173:3647-3652.
11. Bona C., Robineaux R., Anteunis A., Heuclin C., Astesano A. Transfer of antigen from macrophages to lymphocytes. II. Immunological significance of the transfer of lipopolysaccharide. Immunology 1973, 24:831-840.
12. Carrasco Y.R., Batista F.D. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007, 27:160-171.
13. Chang J.T., Palanivel V.R., Kinjyo I., Schambach F., Intlekofer A.M., Banerjee A., Longworth S.A., Vinup K.E., Mrass P., Oliaro J., et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 2007, 315:1687-1691.
14. Chen Y., Chen J., Xiong Y., Da Q., Xu Y., Jiang X., Tang H. Internalization of CD40 regulates its signal transduction in vascular endothelial cells. Biochem. Biophys. Res. Commun. 2006, 345:106-117.
15. Choudhuri K., Llodrá J., Roth E.W., Tsai J., Gordo S., Wucherpfennig K.W., Kam L.C., Stokes D.L., Dustin M.L. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 2014, 507:118-123.
16. Cormont M., Metón I., Mari M., Monzo P., Keslair F., Gaskin C., McGraw T.E., Le Marchand-Brustel Y. CD2AP/CMS regulates endosome morphology and traffic to the degradative pathway through its interaction with Rab4 and c-Cbl. Traffic 2003, 4:97-112.
17. Davis D.M. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat. Rev. Immunol. 2007, 7:238-243.
18. Davis M.M., Boniface J.J., Reich Z., Lyons D., Hampl J., Arden B., Chien Y. Ligand recognition by alpha beta Tcell receptors. Annu. Rev. Immunol. 1998, 16:523-544.
19. Dustin M.L., Chan A.C. Signaling takes shape in the immune system. Cell 2000, 103:283-294.
20. Dustin M.L., Meyer-Hermann M. Immunology. Antigen feast or famine. Science 2012, 335:408-409.
21. Dustin M.L., Olszowy M.W., Holdorf A.D., Li J., Bromley S., Desai N., Widder P., Rosenberger F., van der Merwe P.A., Allen P.M., Shaw A.S. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell 1998, 94:667-677.
22. Fleire S.J., Goldman J.P., Carrasco Y.R., Weber M., Bray D., Batista F.D. B cell ligand discrimination through a spreading and contraction response. Science 2006, 312:738-741.
23. Govern C.C., Paczosa M.K., Chakraborty A.K., Huseby E.S. Fast on-rates allow short dwell time ligands to activate Tcells. Proc. Natl. Acad. Sci. USA 2010, 107:8724-8729.
24. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse: a molecular machine controlling Tcell activation. Science 1999, 285:221-227.
25. Guy R., Ullrich S.J., Foo-Philips M., Hathcock K.S., Appella E., Hodes R.J. Antigen-specific helper function of cell-free Tcell products bearing TCR V beta 8 determinants. Science 1989, 244:1477-1480.
26. Hawkins E.D., Turner M.L., Wellard C.J., Zhou J.H., Dowling M.R., Hodgkin P.D. Quantal and graded stimulation of B lymphocytes as alternative strategies for regulating adaptive immune responses. Nat. Commun. 2013, 4:2406.
27. Huppa J.B., Axmann M., Mörtelmaier M.A., Lillemeier B.F., Newell E.W., Brameshuber M., Klein L.O., Schütz G.J., Davis M.M. TCR-peptide-MHC interactions insitu show accelerated kinetics and increased affinity. Nature 2010, 463:963-967.
28. Iezzi G., Karjalainen K., Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector Tcells. Immunity 1998, 8:89-95.
29. Johnstone R.M., Adam M., Hammond J.R., Orr L., Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J.Biol. Chem. 1987, 262:9412-9420.
30. Joly E., Hudrisier D. What is trogocytosis and what is its purpose?. Nat. Immunol. 2003, 4:815.
31. Kim S.T., Takeuchi K., Sun Z.Y., Touma M., Castro C.E., Fahmy A., Lang M.J., Wagner G., Reinherz E.L. The alphabeta Tcell receptor is an anisotropic mechanosensor. J.Biol. Chem. 2009, 284:31028-31037.
32. Koguchi Y., Buenafe A.C., Thauland T.J., Gardell J.L., Bivins-Smith E.R., Jacoby D.B., Slifka M.K., Parker D.C. Preformed CD40L is stored in Th1, Th2, Th17, and T follicular helper cells as well as CD4+ 8- thymocytes and invariant NKT cells but not in Treg cells. PLoS ONE 2012, 7:e31296.
33. Kontiainen S., Simpson E., Bohrer E., Beverley P.C., Herzenberg L.A., Fitzpatrick W.C., Vogt P., Torano A., McKenzie I.F., Feldmann M. T-cell lines producing antigen-specific suppressor factor. Nature 1978, 274:477-480.
34. Krangel M.S. Endocytosis and recycling of the T3-T cell receptor complex. The role of T3 phosphorylation. J.Exp. Med. 1987, 165:1141-1159.
35. Krogsgaard M., Li Q.J., Sumen C., Huppa J.B., Huse M., Davis M.M. Agonist/endogenous peptide-MHC heterodimers drive Tcell activation and sensitivity. Nature 2005, 434:238-243.
36. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature 1985, 314:537-539.
37. Lee K.H., Dinner A.R., Tu C., Campi G., Raychaudhuri S., Varma R., Sims T.N., Burack W.R., Wu H., Wang J., et al. The immunological synapse balances Tcell receptor signaling and degradation. Science 2003, 302:1218-1222.
38. Matsui K., Boniface J.J., Steffner P., Reay P.A., Davis M.M. Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 1994, 91:12862-12866.
39. Mittelbrunn M., Gutiérrez-Vázquez C., Villarroya-Beltri C., González S., Sánchez-Cabo F., González M.A., Bernad A., Sánchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from Tcells to antigen-presenting cells. Nat. Commun. 2011, 2:282.
40. Naramura M., Jang I.K., Kole H., Huang F., Haines D., Gu H. c-Cbl and Cbl-b regulate Tcell responsiveness by promoting ligand-induced TCR down-modulation. Nat. Immunol. 2002, 3:1192-1199.
41. O'Donoghue G.P., Pielak R.M., Smoligovets A.A., Lin J.J., Groves J.T. Direct single molecule measurement of TCR triggering by agonist pMHC in living primary Tcells. Elife 2013, 2:e00778.
42. Phan T.G., Green J.A., Gray E.E., Xu Y., Cyster J.G. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 2009, 10:786-793.
43. Quah B.J., Barlow V.P., McPhun V., Matthaei K.I., Hulett M.D., Parish C.R. Bystander B cells rapidly acquire antigen receptors from activated B cells by membrane transfer. Proc. Natl. Acad. Sci. USA 2008, 105:4259-4264.
44. Reinherz E.L., Tan K., Tang L., Kern P., Liu J., Xiong Y., Hussey R.E., Smolyar A., Hare B., Zhang R., et al. The crystal structure of a Tcell receptor in complex with peptide and MHC class II. Science 1999, 286:1913-1921.
45. Skokos D., Le Panse S., Villa I., Rousselle J.C., Peronet R., David B., Namane A., Mécheri S. Mast cell-dependent B and T lymphocyte activation is mediated by the secretion of immunologically active exosomes. J.Immunol. 2001, 166:868-876.
46. Soubeyran P., Kowanetz K., Szymkiewicz I., Langdon W.Y., Dikic I. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 2002, 416:183-187.
47. Stinchcombe J.C., Bossi G., Booth S., Griffiths G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 2001, 15:751-761.
48. Szöllósi J., Horejsí V., Bene L., Angelisová P., Damjanovich S. Supramolecular complexes of MHC class I, MHC class II, CD20, and tetraspan molecules (CD53, CD81, and CD82) at the surface of a B cell line JY. J.Immunol. 1996, 157:2939-2946.
49. Thaunat O., Batista F.D. Daughter B cells are not created equal: asymmetric segregation of antigen during B cell division. Cell Cycle 2012, 11:2219-2220.
50. Thaunat O., Granja A.G., Barral P., Filby A., Montaner B., Collinson L., Martinez-Martin N., Harwood N.E., Bruckbauer A., Batista F.D. Asymmetric segregation of polarized antigen on B cell division shapes presentation capacity. Science 2012, 335:475-479.
51. Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biology Rep. 2011, 3:15.
52. Tolentino T.P., Wu J., Zarnitsyna V.I., Fang Y., Dustin M.L., Zhu C. Measuring diffusion and binding kinetics by contact area FRAP. Biophys. J. 2008, 95:920-930.
53. Trombetta E.S., Mellman I. Cell biology of antigen processing invitro and invivo. Annu. Rev. Immunol. 2005, 23:975-1028.
54. Tubo N.J., Pagán A.J., Taylor J.J., Nelson R.W., Linehan J.L., Ertelt J.M., Huseby E.S., Way S.S., Jenkins M.K. Single naive CD4+ Tcells from a diverse repertoire produce different effector cell types during infection. Cell 2013, 153:785-796.
55. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
56. Valitutti S., Müller 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.
57. Valitutti S., Müller S., Salio M., Lanzavecchia A. Degradation of Tcell receptor (TCR)-CD3-zeta complexes after antigenic stimulation. J.Exp. Med. 1997, 185:1859-1864.
58. 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.
59. Velazquez C., DiPaolo R., Unanue E.R. Quantitation of lysozyme peptides bound to class II MHC molecules indicates very large differences in levels of presentation. J.Immunol. 2001, 166:5488-5494.
60. Victora G.D., Nussenzweig M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30:429-457.
61. Victora G.D., Schwickert T.A., Fooksman D.R., Kamphorst A.O., Meyer-Hermann M., Dustin M.L., Nussenzweig M.C. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 2010, 143:592-605.
62. Wang J., Lim K., Smolyar A., Teng M., Liu J., Tse A.G., Liu J., Hussey R.E., Chishti Y., Thomson C.T., et al. Atomic structure of an alphabeta Tcell receptor (TCR) heterodimer in complex with an anti-TCR fab fragment derived from a mitogenic antibody. EMBO J. 1998, 17:10-26.
63. Weiss A., Littman D.R. Signal transduction by lymphocyte antigen receptors. Cell 1994, 76:263-274.
64. Xie J., Huppa J.B., Newell E.W., Huang J., Ebert P.J., Li Q.J., Davis M.M. Photocrosslinkable pMHC monomers stain Tcells specifically and cause ligand-bound TCRs to be 'preferentially' transported to the cSMAC. Nat. Immunol. 2012, 13:674-680.
65. Yachi P.P., Lotz C., Ampudia J., Gascoigne N.R. T cell activation enhancement by endogenous pMHC acts for both weak and strong agonists but varies with differentiation state. J.Exp. Med. 2007, 204:2747-2757.