A sharp T-cell antigen receptor signaling threshold for T-cell proliferation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 35, 2014, Pages

  Au Yeung, Byron B ^a   Zikherman, Julie ^a   Mueller, James L ^a   Ashouri, Judith F ^a   Matloubian, Mehrdad ^a   Cheng, Debra A ^a   Chen, Yiling ^a   Shokat, Kevan M ^a,b   Weiss, Arthur ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; GREEN FLUORESCENT PROTEINS; INTERLEUKIN-2; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84907228126     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413726111     Document Type: Article

References (47)

1. Iezzi G, Karjalainen K, Lanzavecchia A (1998) The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8(1):89-95.
2. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM (2002) Direct observation of ligand recognition by T cells. Nature 419(6909):845-849.
3. Sojka DK, Bruniquel D, Schwartz RH, Singh NJ (2004) IL-2 secretion by CD4 + T cells in vivo is rapid, transient, and influenced by TCR-specific competition. J Immunol 172(10):6136-6143.
4. Huang J, et al. (2013) A single peptide-major histocompatibility complex ligand triggers digital cytokine secretion in CD4(+) T cells. Immunity 39(5):846-857.
5. Kimachi K, Croft M, Grey HM (1997) The minimal number of antigen-major histocompatibility complex class II complexes required for activation of naive and primed T cells. Eur J Immunol 27(12):3310-3317.
6. Viola A, Lanzavecchia A (1996) T cell activation determined by T cell receptor number and tunable thresholds. Science 273(5271):104-106.
7. Bevan MJ, Fink PJ (2001) The CD8 response on autopilot. Nat Immunol 2(5):381-382.
8. van Stipdonk MJ, Lemmens EE, Schoenberger SP (2001) Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2(5):423-429.
9. Wong P, Pamer EG (2001) Cutting edge: Antigen-independent CD8 T cell proliferation. J Immunol 166(10):5864-5868.
10. Schrum AG, Palmer E, Turka LA (2005) Distinct temporal programming of naive CD4+ T cells for cell division versus TCR-dependent death susceptibility by antigen-presenting macrophages. Eur J Immunol 35(2):449-459.
11. Huppa JB, Gleimer M, Sumen C, Davis MM (2003) Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat Immunol 4(8): 749-755.
12. Kaech SM, Ahmed R (2001) Memory CD8+ T cell differentiation: Initial antigen encounter triggers a developmental program in naïve cells. Nat Immunol 2(5):415-422.
13. Obst R, van Santen HM, Mathis D, Benoist C (2005) Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J Exp Med 201(10): 1555-1565.
14. Prlic M, Hernandez-Hoyos G, Bevan MJ (2006) Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J Exp Med 203(9):2135-2143.
15. Bajénoff M, Wurtz O, Guerder S (2002) Repeated antigen exposure is necessary for the differentiation, but not the initial proliferation, of naive CD4(+) T cells. J Immunol 168(4):1723-1729.
16. Gett AV, Sallusto F, Lanzavecchia A, Geginat J (2003) T cell fitness determined by signal strength. Nat Immunol 4(4):355-360.
17. Lee WT, Pasos G, Cecchini L, Mittler JN (2002) Continued antigen stimulation is not required during CD4(+) T cell clonal expansion. J Immunol 168(4):1682-1689.
18. Curtsinger JM, Johnson CM, Mescher MF (2003) CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J Immunol 171(10):5165-5171.
19. Shaulov A, Murali-Krishna K (2008) CD8 T cell expansion and memory differentiation are facilitated by simultaneous and sustained exposure to antigenic and inflammatory milieu. J Immunol 180(2):1131 - 1138.
20. Stock AT, Mueller SN, van Lint AL, Heath WR, Carbone FR (2004) Cutting edge: Prolonged antigen presentation after herpes simplex virus-1 skin infection. J Immunol 173(4):2241-2244.
21. van Stipdonk MJ, et al. (2003) Dynamic programming of CD8+ T lymphocyte responses. Nat Immunol 4(4):361-365.
22. Zehn D, King C, Bevan MJ, Palmer E (2012) TCR signaling requirements for activating T cells and for generating memory. Cell Mol Life Sci 69(10):1565-1575.
23. Baldwin TA, Hogquist KA (2007) Transcriptional analysis of clonal deletion in vivo. J Immunol 179(2):837-844.
24. Winoto A, Littman DR (2002) Nuclear hormone receptors in T lymphocytes. Cell 109 (Suppl):S57-S66.
25. Moran AE, et al. (2011) T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med 208(6): 1279-1289.
26. Zikherman J, Parameswaran R, Weiss A (2012) Endogenous antigen tunes the responsiveness of naive B cells but not T cells. Nature 489(7414):160-164.
27. Au-Yeung BB, et al. (2010) A genetically selective inhibitor demonstrates a function for the kinase Zap70 in regulatory T cells independent of its catalytic activity. Nat Immunol 11(12):1085-1092.
28. Levin SE, Zhang C, Kadlecek TA, Shokat KM, Weiss A (2008) Inhibition of ZAP-70 kinase activity via an analog-sensitive allele blocks T cell receptor and CD28 superagonist signaling. J Biol Chem 283(22):15419-15430.
29. Wang H, et al. (2010) ZAP-70: An essential kinase in T-cell signaling. Cold Spring Harb Perspect Biol 2(5):a002279.
30. Kadlecek TA, et al. (1998) Differential requirements for ZAP-70 in TCR signaling and T cell development. J Immunol 161(9):4688-4694.
31. Corish P, Tyler-Smith C (1999) Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng 12(12):1035-1040.
32. Lourido S, et al. (2013) Optimizing small molecule inhibitors of calcium-dependent protein kinase 1 to prevent infection by Toxoplasma gondii. J Med Chem 56(7): 3068-3077.
33. Au-Yeung BB, et al. (2014) Quantitative and temporal requirements revealed for Zap70 catalytic activity during T cell development. Nat Immunol 15(7):687-694.
34. Barnden MJ, Allison J, Heath WR, Carbone FR (1998) Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol 76(1):34-40.
35. Oxenius A, Bachmann MF, Zinkernagel RM, Hengartner H (1998) Virus-specific MHCclass II-restricted TCR-transgenic mice: Effects on humoral and cellular immune responses after viral infection. Eur J Immunol 28(1):390-400.
36. Guy CS, et al. (2013) Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat Immunol 14(3):262-270.
37. Holst J, et al. (2008) Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat Immunol 9(6): 658-666.
38. Itoh Y, Germain RN (1997) Single cell analysis reveals regulated hierarchical T cell antigen receptor signaling thresholds and intraclonal heterogeneity for individual cytokine responses of CD4+ T cells. J Exp Med 186(5):757-766.
39. Zehn D, Lee SY, Bevan MJ (2009) Complete but curtailed T-cell response to very lowaffinity antigen. Nature 458(7235):211-214.
40. Daniels MA, et al. (2006) Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444(7120):724-729.
41. Siggs OM, et al. (2007) Opposing functions of the T cell receptor kinase ZAP-70 in immunity and tolerance differentially titrate in response to nucleotide substitutions. Immunity 27(6):912-926.
42. Whitmire JK, Ahmed R (2000) Costimulation in antiviral immunity: Differential requirements for CD4(+) and CD8(+) T cell responses. Curr Opin Immunol 12(4):448-455.
43. Mempel TR, Henrickson SE, Von Andrian UH (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427(6970):154-159.
44. Butler TC, Kardar M, Chakraborty AK (2013) Quorum sensing allows T cells to discriminate between self and nonself. Proc Natl Acad Sci USA 110(29):11833-11838.
45. Faroudi M, Zaru R, Paulet P, Müller S, Valitutti S (2003) Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J Immunol 171(3):1128-1132.
46. Friedl P, Gunzer M (2001) Interaction of T cells with APCs: The serial encounter model. Trends Immunol 22(4):187-191.
47. Rachmilewitz J, Lanzavecchia A (2002) A temporal and spatial summation model for T-cell activation: Signal integration and antigen decoding. Trends Immunol 23(12): 592-595.