Rapid Culling of the CD4+ T Cell Repertoire in the Transition from Effector to Memory

Immunity

Volumn 28, Issue 4, 2008, Pages 533-545

  Williams, Matthew A ^a   Ravkov, Eugene V ^a   Bevan, Michael J ^b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

CELLIMMUNO

Indexed keywords

BIM PROTEIN; T LYMPHOCYTE RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; EFFECTOR CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; LISTERIA; LISTERIOSIS; LONGEVITY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY CELL; MOLECULAR MIMICRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; CRICETINAE; IMMUNOLOGIC MEMORY; INTERFERON TYPE II; INTERLEUKIN-2; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; TUMOR NECROSIS FACTOR-ALPHA; VERO CELLS;

EID: 41549143518     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.02.014     Document Type: Article

References (70)

1. Ahmed R., Salmi A., Butler L.D., Chiller J.M., and Oldstone M.B. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160 (1984) 521-540
2. Bachmann M.F., Wolint P., Walton S., Schwarz K., and Oxenius A. Differential role of IL-2R signaling for CD8+ T cell responses in acute and chronic viral infections. Eur. J. Immunol. 37 (2007) 1502-1512
3. Bitomsky N., Bohm M., and Klempnauer K.H. Transformation suppressor protein Pdcd4 interferes with JNK-mediated phosphorylation of c-Jun and recruitment of the coactivator p300 by c-Jun. Oncogene 23 (2004) 7484-7493
4. Blair D.A., and Lefrancois L. Increased competition for antigen during priming negatively impacts the generation of memory CD4 T cells. Proc. Natl. Acad. Sci. USA 104 (2007) 15045-15050
5. Breitfeld D., Ohl L., Kremmer E., Ellwart J., Sallusto F., Lipp M., and Forster R. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 192 (2000) 1545-1552
6. Chen J., Yusuf I., Andersen H.-M., and Fruman D.A. FOXO transcription factors cooperate with {delta}EF1 to activate growth suppressive genes in B lymphocytes. J. Immunol. 176 (2006) 2711-2721
7. Cheng L.E., Chan F.K., Cado D., and Winoto A. Functional redundancy of the Nur77 and Nor-1 orphan steroid receptors in T-cell apoptosis. EMBO J. 16 (1997) 1865-1875
8. Christian S.L., Lee R.L., McLeod S.J., Burgess A.E., Li A.H.Y., Dang-Lawson M., Lin K.B.L., and Gold M.R. Activation of the Rap GTPases in B lymphocytes modulates B cell antigen receptor-induced activation of Akt but has no effect on MAPK activation. J. Biol. Chem. 278 (2003) 41756-41767
9. Foulds K.E., and Shen H. Clonal competition inhibits the proliferation and differentiation of adoptively transferred TCR transgenic CD4 T cells in response to infection. J. Immunol. 176 (2006) 3037-3043
10. Gett A.V., Sallusto F., Lanzavecchia A., and Geginat J. T cell fitness determined by signal strength. Nat. Immunol. 4 (2003) 355-360
11. Green D.R., Droin N., and Pinkoski M. Activation-induced cell death in T cells. Immunol. Rev. 193 (2003) 70-81
12. Hammarlund E., Lewis M.W., Hansen S.G., Strelow L.I., Nelson J.A., Sexton G.J., Hanifin J.M., and Slifka M.K. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9 (2003) 1131-1137
13. Hand T.W., Morre M., and Kaech S.M. Expression of IL-7 receptor {alpha} is necessary but not sufficient for the formation of memory CD8 T cells during viral infection. Proc. Natl. Acad. Sci. USA 104 (2007) 11730-11735
14. Hataye J., Moon J.J., Khoruts A., Reilly C., and Jenkins M.K. Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 312 (2006) 114-116
15. Hendriks J., Xiao Y., and Borst J. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J. Exp. Med. 198 (2003) 1369-1380
16. Homann D., Teyton L., and Oldstone M.B.A. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7 (2001) 913-919
17. Hughes P.D., Belz G.T., Fortner K.A., Budd R.C., Strasser A., and Bouillet P. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 28 (2008) 197-205
18. Hutcheson J., Scatizzi J.C., Siddiqui A.M., Haines G.K., Wu T., Li Q., Davis L.S., Mohan C., and Perlman H. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity 28 (2008) 206-217
19. Janssen E.M., Lemmens E.E., Wolfe T., Christen U., von Herrath M.G., and Schoenberger S.P. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421 (2003) 852-856
20. Jia S., and Meng A. Tob genes in development and homeostasis. Dev. Dyn. 236 (2007) 913-921
21. Jiang Y., Woronicz J.D., Liu W., and Goeddel D.V. Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science 283 (1999) 543-546
22. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., Gapin L., and Kaech S.M. Inflammation directs memory precursor and short-lived effector CD8+ T cell fates via the graded expression of T-bet transcription factor. Immunity 27 (2007) 281-295
23. Kabashima K., Saji T., Murata T., Nagamachi M., Matsuoka T., Segi E., Tsuboi K., Sugimoto Y., Kobayashi T., Miyachi Y., et al. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J. Clin. Invest. 109 (2002) 883-893
24. Kaech S.M., and Ahmed R. Memory CD8+ T cell differentiation: Initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2 (2001) 415-422
25. 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
26. Kaech S.M., and Wherry E.J. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 27 (2007) 393-405
27. Kester H.A., Blanchetot C., den Hertog J., van der Saag P.T., and van der Burg B. Transforming growth factor-beta -stimulated clone-22 is a member of a family of leucine zipper proteins that can homo- and heterodimerize and has transcriptional repressor activity. J. Biol. Chem. 274 (1999) 27439-27447
28. Klonowski K.D., Williams K.J., Marzo A.L., and Lefrancois L. Cutting edge: IL-7-independent regulation of IL-7 receptor {alpha} expression and memory CD8 T cell development. J. Immunol. 177 (2006) 4247-4251
29. Kroger C.J., and Alexander-Miller M.A. Cutting edge: CD8+ T cell clones possess the potential to differentiate into both high- and low-avidity effector cells. J. Immunol. 179 (2007) 748-751
30. Lanzavecchia A., and Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2 (2002) 982-987
31. Liang H., Samanta S., and Nagarajan L. SSBP2, a candidate tumor suppressor gene, induces growth arrest and differentiation of myeloid leukemia cells. Oncogene 24 (2005) 2625-2634
32. Lin L., Hron J.D., and Peng S.L. Regulation of NF-kappaB, Th Activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21 (2004) 203-213
33. Mamura M., Nakao A., Goto D., Kato M., Saito Y., and Iwamoto I. Ligation of the T cell receptor complex results in phosphorylation of Smad2 in T lymphocytes. Biochem. Biophys. Res. Commun. 268 (2000) 124-127
34. Marrack P., and Kappler J. Control of T cell viability. Annu. Rev. Immunol. 22 (2004) 765-787
35. Mercado R., Vijh S., Allen S.E., Kerksiek K., Pilip I.M., and Pamer E.G. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165 (2000) 6833-6839
36. Metcalfe S.M., Muthukumarana P.A.D.S., Thompson H.L., Haendel M.A., and Lyons G.E. Leukaemia inhibitory factor (LIF) is functionally linked to axotrophin and both LIF and axotrophin are linked to regulatory immune tolerance. FEBS Lett. 579 (2005) 609-614
37. Muto A., Tashiro S., Tsuchiya H., Kume A., Kanno M., Ito E., Yamamoto M., and Igarashi K. Activation of Maf/AP-1 repressor Bach2 by oxidative stress promotes apoptosis and its interaction with promyelocytic leukemia nuclear bodies. J. Biol. Chem. 277 (2002) 20724-20733
38. Myers M.D., Dragone L.L., and Weiss A. Src-like adaptor protein down-regulates T cell receptor (TCR)-CD3 expression by targeting TCR{zeta} for degradation. J. Cell Biol. 170 (2005) 285-294
39. Obst R., van Santen H.-M., Mathis D., and Benoist C. Antigen persistence is required throughout the expansion phase of a CD4+ T cell response. J. Exp. Med. 201 (2005) 1555-1565
40. Onami T.M., Harrington L.E., Williams M.A., Galvan M., Larsen C.P., Pearson T.C., Manjunath N., Baum L.G., Pearce B.D., and Ahmed R. Dynamic regulation of T cell immunity by CD43. J. Immunol. 168 (2002) 6022-6031
41. Oxenius A., Bachmann M.F., Zinkernagel R.M., and Hengartner H. Virus-specific MHC-class II-restricted TCR-transgenic mice: Effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28 (1998) 390-400
42. Parry R.V., Chemnitz J.M., Frauwirth K.A., Lanfranco A.R., Braunstein I., Kobayashi S.V., Linsley P.S., Thompson C.B., and Riley J.L. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell. Biol. 25 (2005) 9543-9553
43. Pearce E.L., and Shen H. Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179 (2007) 2074-2081
44. Pellegrini M., Belz G., Bouillet P., and Strasser A. Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. USA 100 (2003) 14175-14180
45. Prlic M., Hernandez-Hoyos G., and Bevan M.J. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J. Exp. Med. 203 (2006) 2135-2143
46. Prlic M., Williams M.A., and Bevan M.J. Requirements for CD8 T-cell priming, memory generation and maintenance. Curr. Opin. Immunol. 19 (2007) 315-319
47. Qiang Y.W., and Rudikoff S. Wnt signaling in B and T lymphocytes. Front. Biosci. 9 (2004) 1000-1010
48. Rees W., Bender J., Teague T.K., Kedl R.M., Crawford F., Marrack P., and Kappler J. An inverse relationship between T cell receptor affinity and antigen dose during CD4+ T cell responses in vivo and in vitro. Proc. Natl. Acad. Sci. USA 96 (1999) 9781-9786
49. Savage P.A., Boniface J.J., and Davis M.M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10 (1999) 485-492
50. Schaerli P., Willimann K., Lang A.B., Lipp M., Loetscher P., and Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192 (2000) 1553-1562
51. Scott K.L., and Plon S.E. CHES1/FOXN3 interacts with Ski-interacting protein and acts as a transcriptional repressor. Gene 359 (2005) 119-126
52. Shedlock D.J., and Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300 (2003) 337-339
53. Shen H., Slifka M.K., Matloubian M., Jensen E.R., Ahmed R., and Miller J.F. Recombinant Listeria monocytogenes as a live vaccine vehicle for the induction of protective anti-viral cell-mediated immunity. Proc. Natl. Acad. Sci. USA 92 (1995) 3987-3991
54. Slifka M.K., and Whitton J.L. Functional avidity maturation of CD8+ T cells without selection of higher affinity TCR. Nat. Immunol. 2 (2001) 711-717
55. Stahl M., Dijkers P.F., Kops G.J.P.L., Lens S.M.A., Coffer P.J., Burgering B.M.T., and Medema R.H. The Forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168 (2002) 5024-5031
56. Sun J.C., and Bevan M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300 (2003) 339-342
57. Sun J.C., Lehar S.M., and Bevan M.J. Augmented IL-7 signaling during viral infection drives greater expansion of effector T cells but does not enhance memory. J. Immunol. 177 (2006) 4458-4463
58. van Stipdonk M.J.B., Hardenberg G., Bijker M.S., Lemmens E.E., Droin N.M., Green D.R., and Schoenberger S.P. Dynamic programming of CD8+ T lymphocyte responses. Nat. Immunol. 4 (2003) 361-365
59. Vietor I., and Huber L.A. Role of TIS7 family of transcriptional regulators in differentiation and regeneration. Differentiation 75 (2007) 891-897
60. Waldmann T.A. The biology of interleukin-2 and interleukin-15: Implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 6 (2006) 595-601
61. Way S.S., Havenar-Daughton C., Kolumam G.A., Orgun N.N., and Murali-Krishna K. IL-12 and type-I IFN synergize for IFN-gamma production by CD4 T cells, whereas neither are required for IFN-gamma production by CD8 T cells after Listeria monocytogenes infection. J. Immunol. 178 (2007) 4498-4505
62. Weant A.E., Michalek R.D., Khan I.U., Holbrook B.C., Willingham M.C., and Grayson J.M. Immunity 28 (2008) 218-230
63. Whitmire J.K., Benning N., and Whitton J.L. Precursor frequency, nonlinear proliferation, and functional maturation of virus-specific CD4+ T cells. J. Immunol. 176 (2006) 3028-3036
64. Williams M.A., and Bevan M.J. Shortening the infectious period does not alter expansion of CD8 T cells but diminishes their capacity to differentiate into memory cells. J. Immunol. 173 (2004) 6694-6702
65. Williams M.A., and Bevan M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25 (2007) 171-192
66. Williams M.A., Tyznik A.J., and Bevan M.J. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441 (2006) 890-893
67. Wojciechowski S., Jordan M.B., Zhu Y., White J., Zajac A.J., and Hildeman D.A. Bim mediates apoptosis of CD127(lo) effector T cells and limits T cell memory. Eur. J. Immunol. 36 (2006) 1694-1706
68. Wojciechowski S., Tripathi P., Bourdeau T., Acero L., Grimes H.L., Katz J.D., Finkelman F.D., and Hildeman D.A. Bim/Bcl-2 balance is critical for maintaining naive and memory T cell homeostasis. J. Exp. Med. 204 (2007) 1665-1675
69. Yamagishi N., Ishihara K., Saito Y., and Hatayama T. Hsp105 family proteins suppress staurosporine-induced apoptosis by inhibiting the translocation of Bax to mitochondria in HeLa cells. Exp. Cell Res. 312 (2006) 3215-3223
70. Zhang J., Xu L.-G., Han K.-J., and Shu H.-B. Identification of a ZU5 and death domain-containing inhibitor of NF-{kappa}B. J. Biol. Chem. 279 (2004) 17819-17825