From synapses to immunological memory: The role of sustained T cell stimulation

Current Opinion in Immunology

Volumn 12, Issue 1, 2000, Pages 92-98

  Lanzavecchia, Antonio ^a   Sallusto, Federica ^b  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^b BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOKINE;

ANIMAL CELL; ANTIGEN PRESENTING CELL; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MEMORY CELL; NONHUMAN; REVIEW; SYNAPSE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 0033980716     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(99)00056-4     Document Type: Review

References (70)

1. Monks C.R., Kupfer H., Tamir I., Barlow A., Kupfer A. Selective modulation of protein kinase C-theta during T-cell activation. Nature. 385:1997;83-86.
2. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three dimensional segregation of supramolecular activation clusters in T cells. Nature. 395:1998;82-86. The original description of the immunological synapse in conjugates between T cells and antigen-presenting cells.
3. 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 T cell activation. Science. 285:1999;221-227. A kinetic analysis of the formation of the immunological synapse using T cells and planar membranes.
4. Davis S.J., van der Merwe P.A. The structure and ligand interactions of CD2: implications for T-cell function. Immunol Today. 17:1996;177-187.
5. Shaw A.S., Dustin M.L. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:1997;361-369.
6. 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. 94:1998;667-677.
7. Xavier R., Brennan T., Li Q., McCormack C., Seed B. Membrane compartmentation is required for efficient T cell activation. Immunity. 8:1998;723-732.
8. Montixi C., Langlet C., Bernard A.M., Thimonier J., Dubois C., Wurbel M.A., Chauvin J.P., Pierres M., He H.T. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:1998;5334-5348.
9. Janes P.W., Ley S.C., Magee A.I. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol. 147:1999;447-461.
10. Lanzavecchia A., Iezzi G., Viola A. From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell. 96:1999;1-4. A review on the mechanism of TCR serial triggering.
11. Valitutti S., Muller S., Cella M., Padovan E., Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature. 375:1995;148-151.
12. 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. 181:1995;577-584.
13. Hudrisier D., Kessler B., Valitutti S., Horvath C., Cerottini J.C., Luescher I.F. The efficiency of antigen recognition by CD8+ CTL clones is determined by the frequency of serial TCR engagement. J Immunol. 161:1998;553-562.
14. Itoh Y., Hemmer B., Martin R., Germain R.N. Serial TCR engagement and down-modulation by peptide:MHC molecule ligands: relationship to the quality of individual TCR signaling events. J Immunol. 162:1999;2073-2080.
15. Viola A., Salio M., Tuosto L., Linkert S., Acuto A., Lanzavecchia A. Quantitative contribution of CD4 and CD8 to T cell antigen receptor serial triggering. J Exp Med. 186:1997;1775-1779.
16. Viola A., Linkert S., Lanzavecchia A. A T cell receptor (TCR) antagonist competitively inhibits serial TCR triggering by low-affinity ligands, but does not affect triggering by high-affinity anti-CD3 antibodies. Eur J Immunol. 27:1997;3080-3083.
17. Stotz S.H., Bolliger L., Carbone F.R., Palmer E. T cell receptor (TCR) antagonism without a negative signal: evidence from T cell hybridomas expressing two independent TCRs. J Exp Med. 189:1999;253-264.
18. Dittel B.N., Stefanova I., Germain R.N., Janeway C.A. Jr. Cross, antagonism of a T cell clone expressing two distinct T cell receptors. Immunity. 11:1999;289-298. An interesting study showing a dominant effect of antagonists via recruitment of SHP-1.
19. Davis M.M., Boniface J.J., Reich Z., Lyons D., Hampl J., Arden B., Chien Y. Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol. 16:1998;523-544.
20. Viola A., Lanzavecchia A. T cell activation determined by T cell receptor number and tunable thresholds. Science. 273:1996;104-106.
21. Iezzi G., Karjalainen K., Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity. 8:1998;89-95.
22. Viola A., Schroeder S., Sakakibara Y., Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science. 283:1999;680-682. This work shows that CD28 costimulation results in clustering of rafts together with triggered TCRs, resulting in higher levels and more stable tyrosine phosphorylation.
23. Moran M., Miceli M.C. Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity. 9:1998;787-796.
24. Wulfing C., Davis M.M. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science. 282:1998;2266-2269. This work shows that costimulation triggers a cytoskeletal myosin-driven movement that may be important for initiating and sustaining signal transduction. See also [12].
25. Bachmann M.F., Gallimore A., Linkert S., Cerundolo V., Lanzavecchia A., Kopf M., Viola A. Developmental regulation of Lck targeting to the CD8 coreceptor controls signaling in naive and memory T cells. J Exp Med. 189:1999;1521-1530. This work shows that Lck is expressed at high levels at the plasma membrane of memory and activated T cells whereas it is mainly cytosolic in naive T cells. This difference correlates with different responsiveness to antigenic stimulation.
26. Weiss A., Shields R., Newton M., Manger B., Imboden J. Ligand-receptor interactions required for commitment to the activation of the interleukin 2 gene. J Immunol. 138:1987;2169-2176.
27. Timmerman L.A., Clipstone N.A., Ho S.N., Northrop J.P., Crabtree G.R. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature. 383:1996;837-840.
28. Kundig T.M., Shahinian A., Kawai K., Mittrucker H.W., Sebzda E., Bachmann M.F., Mak T.W., Ohashi P.S. Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity. 5:1996;41-52.
29. •] this work demonstrates for the first time a correlation between cell division and T cell polarization.
30. •].
31. Fitzpatrick D.R., Shirley K.M., McDonald L.E., Bielefeldt-Ohmann H., Kay G.F., Kelso A. Distinct methylation of the interferon gamma (IFN-gamma) and interleukin 3 (IL-3) genes in newly activated primary CD8+ T lymphocytes: regional IFN-gamma promoter demethylation and mRNA expression are heritable in CD44(high)CD8+ T cells. J Exp Med. 188:1998;103-117.
32. Agarwal S., Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity. 9:1998;765-775. This work demonstrates changes in chromatin structure correlated with IL-4 and IL-13 gene expression in developing Th2 responses.
33. Iezzi G., Scotet E., Scheidegger D., Lanzavecchia A. The interplay between the duration of TCR and cytokine signalling determines T cell polarization. Eur J Immunol. 29:1999;4092-4101. This work demonstrates that T cell polarization is dependent on a sustained TCR stimulation. Th2 polarization requires simultaneous signaling from the TCR and IL-4 receptor.
34. •], this work illustrates the importance of sustained signaling for T cell polarization.
35. Ho I.C., Hodge M.R., Rooney J.W., Glimcher L.H. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell. 85:1996;973-983.
36. Zheng W., Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell. 89:1997;587-596.
37. Coffman R.L., Reiner S.L. Instruction, selection, or tampering with the odds? Science. 284:1999;1283-1285. A review of the molecular mechanisms leading to lymphocyte polarization.
38. Forster R., Schubel A., Breitfeld D., Kremmer E., Renner-Muller I., Wolf E., Lipp M. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 99:1999;23-33. Demonstration that CCR7 plays a nonredundant role in the migration of DCs and naive T cells to lymph nodes.
39. Sallusto F., Lenig D., Mackay C.R., Lanzavecchia A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med. 187:1998;875-883.
40. Sad S., Mosmann T.R. Single IL-2-secreting precursor CD4 T cells can develop into either Th1 or Th2 cytokine secretion phenotype. J Immunol. 153:1994;3514-3522.
41. Sallusto F., Lenig D., Forster R., Lipp M., Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401:1999;708-712. This work identifies two subsets of human memory T cells, identified on the basis of their homing and effector capacities.
42. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature. 392:1998;245-252. An excellent and comprehensive review of DC biology.
43. Sallusto F., Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 179:1994;1109-1118.
44. Sallusto F., Cella M., Danieli C., Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 182:1995;389-400.
45. Rescigno M., Citterio S., Thery C., Rittig M., Medaglini D., Pozzi G., Amigorena S., Ricciardi-Castagnoli P. Bacteria-induced neo-biosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells. Proc Natl Acad Sci USA. 95:1998;5229-5234. This work shows that live Gram-negative as well as Gram-positive bacteria are potent inducers of DC maturation.
46. Cella M., Salio M., Sakakibara Y., Langen H., Julkunen I., Lanzavecchia A. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med. 189:1999;821-829. This work demonstrates that viral infection and polyI:C induce DC maturation and protection through an autocrine production of type I IFN.
47. Cella M., Scheidegger D., Palmer-Lehmann K., Lane P., Lanzavecchia A., Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med. 184:1996;747-752.
48. Koch F., Stanzl U., Jennewein P., Janke K., Heufler C., Kampgen E., Romani N., Schuler G. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med. 184:1996;741-746.
49. Wong B.R., Josien R., Lee S.Y., Sauter B., Li H., Steinman R.M., Choi Y. TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J Exp Med. 186:1997;2075-2080.
50. Medzhitov R., Janeway C.A. Jr. Innate, immunity: the virtues of a nonclonal system of recognition. Cell. 91:1997;295-298.
51. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 12:1994;991-1045.
52. Cella M., Engering A., Pinet V., Pieters J., Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature. 388:1997;782-787.
53. Pierre P., Turley S.J., Gatti E., Hull M., Meltzer J., Mirza A., Inaba K., Steinman R.M., Mellman I. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature. 388:1997;787-792.
54. Dieu M-C., Vanbervliet B., Vicari A., Bridon J-M., Oldham E., Ait-Yahia S., Briere F., Zlotnik A., Lebecque S., Caux C. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med. 188:1998;373-386.
55. Sallusto F., Schaerli P., Loetscher P., Schaniel C., Lenig D., Mackay C.R., Qin S., Lanzavecchia A. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol. 28:1998;2760-2769.
56. Sozzani S., Allavena P., D'Amico G., Luini W., Bianchi G., Kataura M., Imai T., Yoshie O., Bonecchi R., Mantovani A. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol. 161:1998;1083-1086.
57. Kalinski P., Hilkens C.M., Snijders A., Snijdewint F.G., Kapsenberg M.L. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J Immunol. 159:1997;28-35.
58. Kalinsky P., Hilkens C., Wierenga E., Kapsenberg M. T cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today. 20:1999;561-567. An excellent review illustrating that the same DC type can induce either Th1 or Th2 polarization, following appropriate stimulation.
59. •]) can induce Th2 polarization when appropriately cultured in vitro.
60. Olweus J., Bitmansour A., Warnke R., Thompson P.A., Carballido J., Picker L.J., Lund-Johansen F. Dendritic cell ontogeny: a human dendritic cell lineage of myeloid origin. Proc Natl Acad Sci USA. 94:1997;12551-12556.
61. •] this work characterizes plasmacytoid monocytes as a cell type specialized for the production of type I IFN.
62. •].
63. Ingulli E., Mondino A., Khoruts A., Jenkins M.K. In vivo detection of dendritic cell antigen presentation to CD4(+) T cells. J Exp Med. 185:1997;2133-2141.
64. Inaba K., Turley S., Yamaide F., Iyoda T., Mahnke K., Inaba M., Pack M., Subklewe M., Sauter B., Sheff D.et al. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med. 188:1998;2163-2173.
65. Sallusto F., Lanzavecchia A. Mobilizing dendritic cells for tolerance, priming, and chronic inflammation. J Exp Med. 189:1999;611-614.
66. •] this report demonstrates a coordinate production of inflammatory and lymphoid chemokines in maturing DCs.
67. •].
68. Huang J.F., Yang Y., Sepulveda H., Shi W., Hwang I., Peterson P.A., Jackson M.R., Sprent J., Cai Z. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science. 286:1999;952-954. This work shows that T cells can take up peptide-MHC complexes at the synapse and present them to other T cells initiating a fratricidal response.
69. •].
70. Randolph G.J., Inaba K., Robbiani D.F., Steinman R.M., Muller W.A. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity. 11:1999;753-761. This work demonstrates that a substantial fraction of monocytes that are recruited into inflammatory tissues carry phagocytosed particles to lymph nodes and differentiate into DCs.