Loss of tonic T-cell receptor signals alters the generation but not the persistence of CD8+ memory T cells

Blood

Volumn 116, Issue 25, 2010, Pages 5560-5570

  Wiehagen, Karla R ^a   Corbo, Evann ^a   Schmidt, Michelle ^a   Shin, Haina ^b   Wherry, E John ^b,c   Maltzman, Jonathan S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WISTAR INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; PROTEIN SH2; SH2 DOMAIN CONTAINING LEUKOCYTE PROTEIN 76; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

EID: 78650509025     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-292458     Document Type: Article

References (52)

1. Kaech SM, Wherry EJ. Heterogeneity and cellfate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity. 2007;27(3):393-405.
2. Virgin HW, Wherry EJ, Ahmed R. Redefining chronic viral infection. Cell. 2009;138(1):30-50.
3. Williams MA, Bevan MJ. Effector and memory CTL differentiation. Annu Rev Immunol. 2007;25:171-192.
4. Joshi NS, Cui W, Chandele A, et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity. 2007;27(2):281-295. (Pubitemid 47284924)
5. Intlekofer AM, Takemoto N, Wherry EJ, et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol. 2005;6(12):1236-1244.
6. Takemoto N, Intlekofer AM, Northrup JT, Wherry EJ, Reiner SL. Cutting Edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J Immunol. 2006;177(11):7515-7519. (Pubitemid 44846265)
7. Joshi NS, Kaech SM. Effector CD8 T cell development: a balancing act between memory cell potential and terminal differentiation. J Immunol. 2008;180(3):1309-1315.
8. Sarkar S, Kalia V, Haining WN, Konieczny BT, Subramaniam S, Ahmed R. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med. 2008;205(3):625-640. (Pubitemid 351439309)
9. Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity. 1998;8(5):591-599. (Pubitemid 28264750)
10. Kobayashi N, Kondo T, Takata H, Yokota S, Takiguchi M. Functional and phenotypic analysis of human memory CD8+ T cells expressing CXCR3. J Leukoc Biol. 2006;80(2):320-329. (Pubitemid 44835505)
11. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol. 2003;4(12):1191-1198. (Pubitemid 37540688)
12. Schluns KS, Kieper WC, Jameson SC, Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol. 2000;1(5):426-432.
13. Becker TC, Wherry EJ, Boone D, et al. Interleukin 15 is required for proliferative renewal of virusspecific memory CD8 T cells. J Exp Med. 2002;195(12):1541-1548. (Pubitemid 34666068)
14. Goldrath AW, Sivakumar PV, Glaccum M, et al. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med. 2002;195(12):1515-1522. (Pubitemid 34666065)
15. Tan JT, Ernst B, Kieper WC, LeRoy E, Sprent J, Surh CD. Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells. J Exp Med. 2002;195(12):1523-1532. (Pubitemid 34666066)
16. Tanchot C, Lemonnier FA, Perarnau B, Freitas AA, Rocha B. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science. 1997;276(5321):2057-2062. (Pubitemid 27443614)
17. Polic B, Kunkel D, Scheffold A, Rajewsky K. How alpha beta T cells deal with induced TCR alpha ablation. Proc Natl Acad Sci U S A. 2001;98(15):8744- 8749. (Pubitemid 32678098)
18. Murali-Krishna K, Lau LL, Sambhara S, Lemonnier F, Altman J,Ahmed R. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science. 1999;286(5443):1377-1381. (Pubitemid 129516243)
19. Leignadier J, Hardy MP, Cloutier M, Rooney J, Labrecque N. Memory T-lymphocyte survival does not require T-cell receptor expression. Proc Natl Acad Sci U S A. 2008;105(51):20440-20445.
20. Tewari K, Walent J, Svaren J, Zamoyska R, Suresh M. Differential requirement for Lck during primary and memory CD8+ T cell responses. Proc Natl Acad Sci U S A. 2006;103(44):16388-16393. (Pubitemid 44715206)
21. Seddon B, Tomlinson P, Zamoyska R. Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol. 2003;4(7):680-686. (Pubitemid 36874445)
22. Dutton RW, Bradley LM, Swain SL. T cell memory. Annu Rev Immunol. 1998;16:201-223.
23. Yablonski D, Kuhne MR, Kadlecek T, Weiss A. Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell. Science. 1998;281(5375):413-416. (Pubitemid 28340785)
24. Clements JL, Yang B, Ross-Barta SE, et al. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science. 1998;281(5375):416-419. (Pubitemid 28340786)
25. Pivniouk V, Tsitsikov E, Swinton P, Rathbun G, Alt FW, Geha RS. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell. 1998;94(2):229-238. (Pubitemid 28348010)
26. Maltzman JS, Kovoor L, Clements JL, Koretzky GA. Conditional deletion reveals a cell-autonomous requirement of SLP-76 for thymocyte selection. J Exp Med. 2005;202(7):893-900. (Pubitemid 41396889)
27. Bushar ND, Corbo E, Schmidt M, Maltzman JS, Farber DL. Ablation of SLP-76 signaling after T cell priming generates memory CD4 T cells impaired in steady-state and cytokine-driven homeostasis. Proc Natl Acad Sci U S A. 2010;107(2):827-831.
28. Srinivas S, Watanabe T, Lin CS, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4. (Pubitemid 38883775)
29. Ruzankina Y, Pinzon-Guzman C, Asare A, et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell. 2007;1(1):113-126. (Pubitemid 46865802)
30. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol. 2003;77(8):4911-4927. (Pubitemid 36402840)
31. Sprent J, Surh CD. T cell memory. Annu Rev Immunol. 2002;20:551-579.
32. Seddon B, Zamoyska R. TCR signals mediated by Src family kinases are essential for the survival of naive T cells. J Immunol. 2002;169(6):2997-3005. (Pubitemid 35013142)
33. Labrecque N, Whitfield LS, Obst R, Waltzinger C, Benoist C, Mathis D. How much TCR does a T cell need? Immunity. 2001;15(1):71-82. (Pubitemid 32728321)
34. Surh CD, Boyman O, Purton JF, Sprent J. Homeostasis of memory T cells. Immunol Rev. 2006;211:154-163.
35. Goldrath AW, Bogatzki LY, Bevan MJ. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med. 2000;192(4):557-564.
36. Carrio R, Rolle CE, Malek TR. Non-redundant role for IL-7R signaling for the survival of CD8+ memory T cells. Eur J Immunol. 2007;37(11):3078-3088. (Pubitemid 350131287)
37. Osborne LC, Dhanji S, Snow JW, et al. Impaired CD8 T cell memory and CD4 T cell primary responses in IL-7R alpha mutant mice. J Exp Med. 2007;204(3):619-631. (Pubitemid 46457084)
38. Sarkar S, Teichgraber V, Kalia V, et al. Strength of stimulus and clonal competition impact the rate of memory CD8 T cell differentiation. J Immunol. 2007;179(10):6704-6714.
39. Surh CD, Sprent J. Homeostasis of naive and memory T cells. Immunity. 2008;29(6):848-862.
40. Cao MY, Davidson D, Yu J, Latour S, Veillette A. Clnk, a novel SLP-76-related adaptor molecule expressed in cytokine-stimulated hemopoietic cells. J Exp Med. 1999;190(10):1527-1534.
41. Bouneaud C, Garcia Z, Kourilsky P, Pannetier C. Lineage relationships, homeostasis, and recall capacities of central- and effector-memory CD8 T cells in vivo. J Exp Med. 2005;201(4):579-590. (Pubitemid 40289548)
42. Wherry EJ, Ahmed R. Memory CD8 T-cell differentiation during viral infection. J Virol. 2004;78(11):5535-5545. (Pubitemid 38661640)
43. Wherry EJ, Teichgraber V, Becker TC, et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol. 2003;4(3):225-234. (Pubitemid 36322131)
44. Badovinac VP, Haring JS, Harty JT. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity. 2007;26(6):827-841.
45. Obar JJ, Lefrancois L. Memory CD8+ T cell differentiation. Ann N Y Acad Sci. 2010;1183:251-266.
46. Smith-Garvin JE, Burns JC, Gohil M, et al. T-cell receptor signals direct the composition and function of the memory CD8+ T-cell pool. Blood. 2010;116(25):5548-5559.
47. Shin H, Blackburn SD, Blattman JN, Wherry EJ. Viral antigen and extensive division maintain virus-specific CD8 T cells during chronic infection. J Exp Med. 2007;204(4):941-949. (Pubitemid 46631621)
48. Haring JS, Badovinac VP, Harty JT. Inflaming the CD8+ T cell response. Immunity. 2006;25(1):19-29.
49. Rao RR, Li Q, Odunsi K, Shrikant PA. The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and eomesodermin. Immunity. 2010;32(1):67-78.
50. Intlekofer AM, Takemoto N, Kao C, et al. Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J Exp Med. 2007;204(9):2015-2021. (Pubitemid 47360863)
51. Araki K, Turner AP, Shaffer VO, et al. mTOR regulates memory CD8 T-cell differentiation. Nature. 2009;460(7251):108-112.
52. Hwang ES, Szabo SJ, Schwartzberg PL, Glimcher LH. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science. 2005;307(5708):430-433.