Biochemical signaling pathways for memory T cell recall

Seminars in Immunology

Volumn 21, Issue 2, 2009, Pages 84-91

  Farber, Donna L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Innate immunity; Signal transduction; T cell receptors; T lymphocytes; Transcription factors

Indexed keywords

CD28 ANTIGEN; GAMMA INTERFERON; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; EFFECTOR CELL; GENETIC TRANSCRIPTION; HUMAN; INNATE IMMUNITY; MEMORY T LYMPHOCYTE; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD28; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOLIPASE C GAMMA; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTE SUBSETS; TRANSCRIPTIONAL ACTIVATION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 61949299950     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2009.02.003     Document Type: Review

References (103)

1. Sprent J., and Surh C.D. T cell memory. Annu Rev Immunol 20 (2002) 551-579
2. Surh C.D., and Sprent J. Regulation of naive and memory T-cell homeostasis. Microbes Infect 4 (2002) 51-56
3. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., and Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4 (2003) 1191-1198
4. Tan J.T., Dudl E., LeRoy E., et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 98 (2001) 8732-8737
5. Budd R.C., Cerottini J.C., Horvath C., et al. Distinction of virgin and memory T lymphocytes. Stable acquisition of the Pgp-1 glycoprotein concomitant with antigenic stimulation. J Immunol 138 (1987) 3120-3129
6. + T cells. Immunol 69 (1990) 460-467
7. Slifka M.K., and Whitton J.L. Activated and memory CD8+ T cells can be distinguished by their cytokine profiles and phenotypic markers. J Immunol 164 (2000) 208-216
8. Kaech S.M., Wherry E.J., and Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2 (2002) 251-262
9. Chandok M.R., and Farber D.L. Signaling control of memory T cell generation and function. Semin Immunol 16 (2004) 285-293
10. Araki Y., Fann M., Wersto R., and Weng N.P. Histone acetylation facilitates rapid and robust memory CD8 T cell response through differential expression of effector molecules (eomesodermin and its targets: perforin and granzyme B). J Immunol 180 (2008) 8102-8108
11. Kaech S.M., Hemby S., Kersh E., and Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111 (2002) 837-851
12. Rogers P.R., Dubey C., and Swain S.L. Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J Immunol 164 (2000) 2338-2346
13. Croft M., Bradley L.M., and Swain S.L. Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J Immunol 152 (1994) 2675-2685
14. Dengler T.J., and Pober J.S. Human vascular endothelial cells stimulate memory but not naive CD8+ T cells to differentiate into CTL retaining an early activation phenotype. J Immunol 164 (2000) 5146-5155
15. Zammit D.J., Cauley L.S., Pham Q.M., and Lefrancois L. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22 (2005) 561-570
16. Chandok M.R., Okoye F.I., Ndejembi M.P., and Farber D.L. A biochemical signature for rapid recall of memory CD4 T cells. J Immunol 179 (2007) 3689-3698
17. Damle N.K., Klussman K., Linsley P.S., and Aruffo A. Differential costimulatory effects of adhesion molecules B7, ICAM-1, LFA-3, and VCAM-1 on resting and antigen-primed CD4+ T lymphocytes. J Immunol 148 (1992) 1985-1992
18. Dutton R.W., Bradley L.M., and Swain S.L. T cell memory. Annu Rev Immunol 16 (1998) 201-223
19. Sallusto F., Lenig D., Forster R., Lipp M., and Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions [see comments]. Nature 401 (1999) 708-712
20. Westermann J., Bode U., Sahle A., et al. Naive, effector, and memory T lymphocytes efficiently scan dendritic cells in vivo: contact frequency in T cell zones of secondary lymphoid organs does not depend on LFA-1 expression and facilitates survival of effector T cells. J Immunol 174 (2005) 2517-2524
21. Abraham R.T., and Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol 4 (2004) 301-308
22. Iwashima M., Irving B.A., van Oers N.S., Chan A.C., and Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263 (1994) 1136-1139
23. Chan A.C., Irving B.A., Fraser J.D., and Weiss A. The ζ chain is associated with a tyrosine kinase and upon T-cell antigen receptor stimulation associates with ZAP-70, a 70-kDa tyrosine phosphoprotein. PNAS 88 (1991) 9166-9170
24. Chan A.C., Iwashima M., Turck C.W., and Weiss A. ZAP-70: a 70 kDa protein-tyrosine kinase that associates with the TCR ζ chain. Cell 71 (1992) 649-662
25. Hatada M.H., Lu X., Laird E.R., et al. Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor. Nature 377 (1995) 32-38
26. Jackman J.K., Motto D.G., Sun Q., et al. Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells. J Biol Chem 270 (1995) 7029-7032
27. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., and Samelson L.E. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92 (1998) 83-92
28. Myung P.S., Boerthe N.J., and Koretzky G.A. Adapter proteins in lymphocyte antigen-receptor signaling. Curr Opin Immunol 12 (2000) 256-266
29. Jordan M.S., Singer A.L., and Koretzky G.A. Adaptors as central mediators of signal transduction in immune cells. Nat Immunol 4 (2003) 110-116
30. Finco T.S., Kadlecek T., Zhang W., Samelson L.E., and Weiss A. LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 9 (1998) 617-626
31. Lewis R.S. Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol 19 (2001) 497-521
32. Rincon M. MAP-kinase signaling pathways in T cells. Curr Opin Immunol 13 (2001) 339-345
33. Hardy K., and Chaudhri G. Activation and signal transduction via mitogen-activated protein (MAP) kinases in T lymphocytes. Immunol Cell Biol 75 (1997) 528-545
34. Kuo C.T., and Leiden J.M. Transcriptional regulation of T lymphocyte development and function. Annu Rev Immunol 17 (1999) 149-187
35. Northrop J.P., Ho S.N., Chen L., et al. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369 (1994) 497-502
36. Rawlings D.J., Sommer K., and Moreno-Garcia M.E. The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes. Nat Rev Immunol 6 (2006) 799-812
37. Thome M. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat Rev Immunol 4 (2004) 348-359
38. Weil R., and Israel A. Deciphering the pathway from the TCR to NF-kappaB. Cell Death Differ 13 (2006) 826-833
39. Farber D.L., Acuto O., and Bottomly K. Differential T cell receptor-mediated signaling in naive and memory CD4 T cells. Eur J Immunol 27 (1997) 2094-2101
40. Farber D.L., Luqman M., Acuto O., and Bottomly K. Control of memory CD4 T cell activation: MHC class II molecules on antigen presenting cells and CD4 ligation inhibit memory but not naive CD4 T cells. Immunity 2 (1995) 249-259
41. Hussain S.F., Anderson C.F., and Farber D.L. Differential SLP-76 expression and TCR-mediated signaling in effector and memory CD4 T cells. J Immunol 168 (2002) 1557-1565
42. Hall S.R., Heffernan B.M., Thompson N.T., and Rowan W.C. CD4+ CD45RA+ and CD4+ CD45RO+ T cells differ in their TCR-associated signaling responses. Eur J Immunol 29 (1999) 2098-2106
43. Krishnan S., Warke V.G., Nambiar M.P., Wong H.K., Tsokos G.C., and Farber D.L. Generation and biochemical analysis of human effector CD4 T cells: alterations in tyrosine phosphorylation and loss of CD3ζ expression. Blood 97 (2001) 3851-3859
44. Kersh E.N., Kaech S.M., Onami T.M., et al. TCR signal transduction in antigen-specific memory CD8 T cells. J Immunol 170 (2003) 5455-5463
45. Krutzik P.O., Clutter M.R., and Nolan G.P. Coordinate analysis of murine immune cell surface markers and intracellular phosphoproteins by flow cytometry. J Immunol 175 (2005) 2357-2365
46. Krutzik P.O., Hale M.B., and Nolan G.P. Characterization of the murine immunological signaling network with phosphospecific flow cytometry. J Immunol 175 (2005) 2366-2373
47. Perez O.D., and Nolan G.P. Simultaneous measurement of multiple active kinase states using polychromatic flow cytometry. Nat Biotechnol 20 (2002) 155-162
48. Ahmadzadeh M., Hussain S.F., and Farber D.L. Effector CD4 T cells are biochemically distinct from the memory subset: evidence for long-term persistence of effectors in vivo. J Immunol 163 (1999) 3053-3063
49. Farber D.L. Differential TCR signaling and the generation of memory T cells. J Immunol 160 (1998) 535-539
50. Douglass A.D., and Vale R.D. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121 (2005) 937-950
51. Drevot P., Langlet C., Guo X.J., et al. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J 21 (2002) 1899-1908
52. Watson A.R., and Lee W.T. Differences in signaling molecule organization between naive and memory CD4+ T lymphocytes. J Immunol 173 (2004) 33-41
53. Kenworthy A.K. Have we become overly reliant on lipid rafts? Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9 (2008) 531-535
54. Okoye F.I., Krishnan S., Chandok M.R., Tsokos G.C., and Farber D.L. Proximal signaling control of human effector CD4 T cell function. Clin Immunol 125 (2007) 5-15
55. Song K., Rabin R.L., Hill B.J., et al. Characterization of subsets of CD4+ memory T cells reveals early branched pathways of T cell differentiation in humans. Proc Natl Acad Sci USA 102 (2005) 7916-7921
56. Feinerman O., Veiga J., Dorfman J.R., Germain R.N., and Altan-Bonnet G. Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 321 (2008) 1081-1084
57. London C.A., Lodge M.P., and Abbas A.K. Functional responses and costimulator dependence of memory CD4+ T cells. J Immunol 164 (2000) 265-272
58. Suresh M., Whitmire J.K., Harrington L.E., et al. Role of CD28-B7 interactions in generation and maintenance of CD8 T cell memory. J Immunol 167 (2001) 5565-5573
59. Borowski A.B., Boesteanu A.C., Mueller Y.M., et al. Memory CD8+ T cells require CD28 costimulation. J Immunol 179 (2007) 6494-6503
60. Fuse S., Zhang W., and Usherwood E.J. Control of memory CD8+ T cell differentiation by CD80/CD86-CD28 costimulation and restoration by IL-2 during the recall response. J Immunol 180 (2008) 1148-1157
61. Ndejembi M.P., Teijaro J.R., Patke D.S., et al. Control of memory CD4 T cell recall by the CD28/B7 costimulatory pathway. J Immunol 177 (2006) 7698-7706
62. Sallusto F., Geginat J., and Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22 (2004) 745-763
63. Dienz O., Eaton S.M., Krahl T.J., et al. Accumulation of NFAT mediates IL-2 expression in memory, but not naïve, CD4+ T cells. Proc Natl Acad Sci USA 104 (2007) 7175-7180
64. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
65. Intlekofer A.M., Takemoto N., Wherry E.J., et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6 (2005) 1236-1244
66. Juedes A.E., Rodrigo E., Togher L., Glimcher L.H., and von Herrath M.G. T-bet controls autoaggressive CD8 lymphocyte responses in type 1 diabetes. J Exp Med 199 (2004) 1153-1162
67. Mullen A.C., High F.A., Hutchins A.S., et al. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 292 (2001) 1907-1910
68. Mullen A.C., Hutchins A.S., High F.A., et al. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction. Nat Immunol 3 (2002) 652-658
69. Martins G.A., Hutchins A.S., and Reiner S.L. Transcriptional activators of helper T cell fate are required for establishment but not maintenance of signature cytokine expression. J Immunol 175 (2005) 5981-5985
70. Fann M., Godlove J.M., Catalfamo M., et al. Histone acetylation is associated with differential gene expression in the rapid and robust memory CD8(+) T-cell response. Blood 108 (2006) 3363-3370
71. Corn R.A., Aronica M.A., Zhang F., et al. T cell-intrinsic requirement for NF-kappa B induction in postdifferentiation IFN-gamma production and clonal expansion in a Th1 response. J Immunol 171 (2003) 1816-1824
72. Shin H.M., Minter L.M., Cho O.H., et al. Notch1 augments NF-kappaB activity by facilitating its nuclear retention. EMBO J 25 (2006) 129-138
73. Ahmadzadeh M., Hussain S.F., and Farber D.L. Heterogeneity of the memory CD4 T cell response: persisting effectors and resting memory T cells. J Immunol 166 (2001) 926-935
74. Thome M., and Tschopp J. TCR-induced NF-kappaB activation: a crucial role for Carma1, Bcl10 and MALT1. Trends Immunol 24 (2003) 419-424
75. Sommer K., Guo B., Pomerantz J.L., et al. Phosphorylation of the CARMA1 linker controls NF-kappaB activation. Immunity 23 (2005) 561-574
76. Wille-Reece U., Flynn B.J., Lore K., et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 203 (2006) 1249-1258
77. Wherry E.J., Teichgraber V., Becker T.C., et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 4 (2003) 225-234
78. Kirwan S.E., and Burshtyn D.N. Regulation of natural killer cell activity. Curr Opin Immunol 19 (2007) 46-54
79. Lantz O., and Bendelac A. An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med 180 (1994) 1097-1106
80. Bendelac A., Savage P.B., and Teyton L. The biology of NKT cells. Annu Rev Immunol 25 (2007) 297-336
81. Berg R.E., Crossley E., Murray S., and Forman J. Memory CD8+ T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J Exp Med 198 (2003) 1583-1593
82. Kambayashi T., Assarsson E., Lukacher A.E., Ljunggren H.G., and Jensen P.E. Memory CD8+ T cells provide an early source of IFN-gamma. J Immunol 170 (2003) 2399-2408
83. Hu J., and August A. Naive and innate memory phenotype CD4+ T cells have different requirements for active Itk for their development. J Immunol 180 (2008) 6544-6552
84. Nagarajan N.A., and Kronenberg M. Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J Immunol 178 (2007) 2706-2713
85. Tyznik A.J., Tupin E., Nagarajan N.A., Her M.J., Benedict C.A., and Kronenberg M. Cutting edge: the mechanism of invariant NKT cell responses to viral danger signals. J Immunol 181 (2008) 4452-4456
86. Way S.S., and Wilson C.B. Cutting edge: immunity and IFN-gamma production during Listeria monocytogenes infection in the absence of T-bet. J Immunol 173 (2004) 5918-5922
87. Tato C.M., Mason N., Artis D., et al. Opposing roles of NF-kappaB family members in the regulation of NK cell proliferation and production of IFN-gamma. Int Immunol 18 (2006) 505-513
88. Tato C.M., Villarino A., Caamano J.H., Boothby M., and Hunter C.A. Inhibition of NF-kappa B activity in T and NK cells results in defective effector cell expansion and production of IFN-gamma required for resistance to Toxoplasma gondii. J Immunol 170 (2003) 3139-3146
89. Gross O., Grupp C., Steinberg C., et al. Multiple ITAM-coupled NK-cell receptors engage the Bcl10/Malt1 complex via Carma1 for NF-kappaB and MAPK activation to selectively control cytokine production. Blood 112 (2008) 2421-2428
90. Hara H., Ishihara C., Takeuchi A., et al. Cell type-specific regulation of ITAM-mediated NF-kappaB activation by the adaptors, CARMA1 and CARD9. J Immunol 181 (2008) 918-930
91. Broderick L., Brooks S.P., Takita H., Baer A.N., Bernstein J.M., and Bankert R.B. IL-12 reverses anergy to T cell receptor triggering in human lung tumor-associated memory T cells. Clin Immunol 118 (2006) 159-169
92. Valenzuela J., Schmidt C., and Mescher M. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J Immunol 169 (2002) 6842-6849
93. Liao X.C., and Littman D.R. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 3 (1995) 757-769
94. Atherly L.O., Lucas J.A., Felices M., Yin C.C., Reiner S.L., and Berg L.J. The Tec family tyrosine kinases Itk and Rlk regulate the development of conventional CD8+ T cells. Immunity 25 (2006) 79-91
95. Hu J., Sahu N., Walsh E., and August A. Memory phenotype CD8+ T cells with innate function selectively develop in the absence of active Itk. Eur J Immunol 37 (2007) 2892-2899
96. Broussard C., Fleischacker C., Horai R., et al. Altered development of CD8+ T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 25 (2006) 93-104
97. Schwartzberg P.L., Finkelstein L.D., and Readinger J.A. TEC-family kinases: regulators of T-helper-cell differentiation. Nat Rev Immunol 5 (2005) 284-295
98. Schoenborn J.R., and Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 96 (2007) 41-101
99. Fitzpatrick D.R., Shirley K.M., and Kelso A. Cutting edge: stable epigenetic inheritance of regional IFN-gamma promoter demethylation in CD44highCD8+ T lymphocytes. J Immunol 162 (1999) 5053-5057
100. Fitzpatrick D.R., Shirley K.M., McDonald L.E., Bielefeldt-Ohmann H., Kay G.F., and 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
101. Avni O., Lee D., Macian F., Szabo S.J., Glimcher L.H., and Rao A. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 3 (2002) 643-651
102. Chang S., and Aune T.M. Histone hyperacetylated domains across the Ifng gene region in natural killer cells and T cells. Proc Natl Acad Sci USA 102 (2005) 17095-17100
103. Tato C.M., Martins G.A., High F.A., DiCioccio C.B., Reiner S.L., and Hunter C.A. Cutting edge: innate production of IFN-gamma by NK cells is independent of epigenetic modification of the IFN-gamma promoter. J Immunol 173 (2004) 1514-1517