CD27 stimulation promotes the frequency of IL-7 receptor-expressing memory precursors and prevents il-12-mediated loss of CD8 + T cell memory in the absence of CD4 + T cell help

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 3829-3838

  Dong, Han ^a   Franklin, Nathan A ^a   Roberts, Drew J ^a   Yagita, Hideo ^b   Glennie, Martin J ^c   Bullock, Timothy N J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b JUNTENDO UNIVERSITY   (Japan)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD70 ANTIGEN; DENDRITIC CELL VACCINE; INTERLEUKIN 12; INTERLEUKIN 7 RECEPTOR; VACCINIA VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DENDRITIC CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD27; ANTIGENS, CD70; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS; GENE EXPRESSION REGULATION; IMMUNIZATION; IMMUNOLOGIC MEMORY; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-7; SIGNAL TRANSDUCTION; VACCINIA VIRUS;

EID: 84860317676     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103329     Document Type: Article

References (61)

1. Wherry, E. J., V. Teichgräber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4: 225-234. (Pubitemid 36322131)
2. Chang, J. T., V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, et al. 2007. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315: 1687-1691. (Pubitemid 46515618)
3. Stemberger, C., K. M. Huster, M. Koffler, F. Anderl, M. Schiemann, H. Wagner, and D. H. Busch. 2007. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 27: 985-997. (Pubitemid 50014865)
4. Bannard, O., M. Kraman, and D. T. Fearon. 2009. Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science 323: 505-509.
5. Huster, K. M., V. Busch, M. Schiemann, K. Linkemann, K. M. Kerksiek, H. Wagner, and D. H. Busch. 2004. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc. Natl. Acad. Sci. USA 101: 5610-5615. (Pubitemid 38481204)
6. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198. (Pubitemid 37540688)
7. Joshi, N. S., W. Cui, A. Chandele, H. K. Lee, D. R. Urso, J. Hagman, L. Gapin, and S. M. Kaech. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27: 281-295. (Pubitemid 47284924)
8. Mazzucchelli, R., and S. K. Durum. 2007. Interleukin-7 receptor expression: intelligent design. Nat. Rev. Immunol. 7: 144-154. (Pubitemid 46178275)
9. Pham, N. L., V. P. Badovinac, and J. T. Harty. 2009. A default pathway of memory CD8 T cell differentiation after dendritic cell immunization is deflected by encounter with inflammatory cytokines during antigen-driven proliferation. J. Immunol. 183: 2337-2348.
10. Wilson, D. C., S. Matthews, and G. S. Yap. 2008. IL-12 signaling drives CD8+ T cell IFN-gamma production and differentiation of KLRG1+ effector sub-populations during Toxoplasma gondii infection. J. Immunol. 180: 5935-5945.
11. Rutishauser, R. L., G. A. Martins, S. Kalachikov, A. Chandele, I. A. Parish, E. Meffre, J. Jacob, K. Calame, and S. M. Kaech. 2009. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31: 296-308.
12. Kallies, A., A. Xin, G. T. Belz, and S. L. Nutt. 2009. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 31: 283-295.
13. Intlekofer, A. M., N. Takemoto, C. Kao, A. Banerjee, F. Schambach, J. K. Northrop, H. Shen, E. J. Wherry, and S. L. Reiner. 2007. Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J. Exp. Med. 204: 2015-2021. (Pubitemid 47360863)
14. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300: 339-342. (Pubitemid 36433727)
15. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339. (Pubitemid 36433726)
16. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856. (Pubitemid 36254145)
17. Khanolkar, A., V. P. Badovinac, and J. T. Harty. 2007. CD8 T cell memory development: CD4 T cell help is appreciated. Immunol. Res. 39: 94-104. (Pubitemid 47574900)
18. Williams, M. A., A. J. Tyznik, and M. J. Bevan. 2006. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441: 890-893.
19. Yi, J. S., J. T. Ingram, and A. J. Zajac. 2010. IL-21 deficiency influences CD8 T cell quality and recall responses following an acute viral infection. J. Immunol. 185: 4835-4845.
20. Novy, P., X. Huang, W. J. Leonard, and Y. Yang. 2011. Intrinsic IL-21 signaling is critical for CD8 T cell survival and memory formation in response to vaccinia viral infection. J. Immunol. 186: 2729-2738.
21. Bourgeois, C., B. Rocha, and C. Tanchot. 2002. A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science 297: 2060-2063.
22. Kennedy, R., and E. Celis. 2006. T helper lymphocytes rescue CTL from activation-induced cell death. J. Immunol. 177: 2862-2872. (Pubitemid 44277801)
23. Schoenberger, S. P. 2009. T cell memory. Semin. Immunol. 21: 51-52.
24. Ahonen, C. L., C. L. Doxsee, S. M. McGurran, T. R. Riter, W. F. Wade, R. J. Barth, J. P. Vasilakos, R. J. Noelle, and R. M. Kedl. 2004. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J. Exp. Med. 199: 775-784. (Pubitemid 38375197)
25. Bullock, T. N., and H. Yagita. 2005. Induction of CD70 on dendritic cells through CD40 or TLR stimulation contributes to the development of CD8+ T cell responses in the absence of CD4+ T cells. J. Immunol. 174: 710-717. (Pubitemid 40094264)
26. Taraban, V. Y., T. F. Rowley, and A. Al-Shamkhani. 2004. Cutting edge: a critical role for CD70 in CD8 T cell priming by CD40-licensed APCs. J. Immunol. 173: 6542-6546. (Pubitemid 39541037)
27. Sanchez, P. J., J. A. McWilliams, C. Haluszczak, H. Yagita, and R. M. Kedl. 2007. Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J. Immunol. 178: 1564-1572. (Pubitemid 46154627)
28. Nolte, M. A., R. W. van Olffen, K. P. van Gisbergen, and R. A. van Lier. 2009. Timing and tuning of CD27-CD70 interactions: the impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol. Rev. 229: 216-231.
29. Taraban, V. Y., T. F. Rowley, D. F. Tough, and A. Al-Shamkhani. 2006. Requirement for CD70 in CD4+ Th cell-dependent and innate receptor-mediated CD8+ T cell priming. J. Immunol. 177: 2969-2975. (Pubitemid 44277812)
30. Dolfi, D. V., A. C. Boesteanu, C. Petrovas, D. Xia, E. A. Butz, and P. D. Katsikis. 2008. Late signals from CD27 prevent Fas-dependent apoptosis of primary CD8+ T cells. J. Immunol. 180: 2912-2921.
31. Hendriks, J., L. A. Gravestein, K. Tesselaar, R. A. van Lier, T. N. Schumacher, and J. Borst. 2000. CD27 is required for generation and long-term maintenance of T cell immunity. Nat. Immunol. 1: 433-440.
32. Roberts, D. J., N. A. Franklin, L. M. Kingeter, H. Yagita, A. L. Tutt, M. J. Glennie, and T. N. Bullock. 2010. Control of established melanoma by CD27 stimulation is associated with enhanced effector function and persistence, and reduced PD-1 expression of tumor infiltrating CD8(+) T cells. J. Immunother. 33: 769-779.
33. Oshima, H., H. Nakano, C. Nohara, T. Kobata, A. Nakajima, N. A. Jenkins, D. J. Gilbert, N. G. Copeland, T. Muto, H. Yagita, and K. Okumura. 1998. Characterization of murine CD70 by molecular cloning and mAb. Int. Immunol. 10: 517-526. (Pubitemid 28182109)
34. Bullock, T. N. J., T. A. Colella, and V. H. Engelhard. 2000. The density of peptides displayed by dendritic cells affects immune responses to human tyrosinase and gp100 in HLA-A2 transgenic mice. J. Immunol. 164: 2354-2361. (Pubitemid 30115462)
35. Novy, P., M. Quigley, X. Huang, and Y. Yang. 2007. CD4 T cells are required for CD8 T cell survival during both primary and memory recall responses. J. Immunol. 179: 8243-8251.
36. Fuse, S., C. Y. Tsai, M. J. Molloy, S. R. Allie, W. Zhang, H. Yagita, and E. J. Usherwood. 2009. Recall responses by helpless memory CD8+ T cells are restricted by the up-regulation of PD-1. J. Immunol. 182: 4244-4254.
37. Obar, J. J., and L. Lefrançois. 2010. Memory CD8+ T cell differentiation. Ann. N. Y. Acad. Sci. 1183: 251-266.
38. Mitchell, D. M., E. V. Ravkov, and M. A. Williams. 2010. Distinct roles for IL-2 and IL-15 in the differentiation and survival of CD8+ effector and memory T cells. J. Immunol. 184: 6719-6730.
39. Hand, T. W., M. Morre, and S. M. Kaech. 2007. 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: 11730-11735. (Pubitemid 47175081)
40. Sun, J. C., S. M. Lehar, and M. J. Bevan. 2006. Augmented IL-7 signaling during viral infection drives greater expansion of effector T cells but does not enhance memory. J. Immunol. 177: 4458-4463. (Pubitemid 44469775)
41. Peperzak, V., Y. Xiao, E. A. Veraar, and J. Borst. 2010. CD27 sustains survival of CTLs in virus-infected nonlymphoid tissue in mice by inducing autocrine IL-2 production. J. Clin. Invest. 120: 168-178.
42. Kalia, V., S. Sarkar, S. Subramaniam, W. N. Haining, K. A. Smith, and R. Ahmed. 2010. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ T cells favors terminal-effector differentiation in vivo. Immunity 32: 91-103.
43. Obar, J. J., M. J. Molloy, E. R. Jellison, T. A. Stoklasek, W. Zhang, E. J. Usherwood, and L. Lefrançois. 2010. CD4+ T cell regulation of CD25 expression controls development of short-lived effector CD8+ T cells in primary and secondary responses. Proc. Natl. Acad. Sci. USA 107: 193-198.
44. Valenzuela, J., C. Schmidt, and M. Mescher. 2002. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J. Immunol. 169: 6842-6849. (Pubitemid 36899269)
45. Pearce, E. L., and H. Shen. 2007. Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179: 2074-2081.
46. Feau, S., R. Arens, S. Togher, and S. P. Schoenberger. 2011. Autocrine IL-2 is required for secondary population expansion of CD8(+) memory T cells. Nat. Immunol. 12: 908-913.
47. Cui, W., N. S. Joshi, A. Jiang, and S. M. Kaech. 2009. Effects of signal 3 during CD8 T cell priming: bystander production of IL-12 enhances effector T cell expansion but promotes terminal differentiation. Vaccine 27: 2177-2187.
48. Keppler, S. J., K. Theil, S. Vucikuja, and P. Aichele. 2009. Effector T-cell differentiation during viral and bacterial infections: role of direct IL-12 signals for cell fate decision of CD8(+) T cells. Eur. J. Immunol. 39: 1774-1783.
49. Afkarian, M., J. R. Sedy, J. Yang, N. G. Jacobson, N. Cereb, S. Y. Yang, T. L. Murphy, and K. M. Murphy. 2002. T-bet is a STAT1-induced regulator of IL-12R expression in naive CD4+ T cells. Nat. Immunol. 3: 549-557. (Pubitemid 34662307)
50. Liao, W., J. X. Lin, and W. J. Leonard. 2011. IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr. Opin. Immunol. 23: 598-604.
51. van Oosterwijk, M. F., H. Juwana, R. Arens, K. Tesselaar, M. H. van Oers, E. Eldering, and R. A. van Lier. 2007. CD27-CD70 interactions sensitise naive CD4+ T cells for IL-12-induced Th1 cell development. Int. Immunol. 19: 713-718. (Pubitemid 47078715)
52. Takemoto, N., A. M. Intlekofer, J. T. Northrup, E. J. Wherry, and S. L. Reiner. 2006. Cutting edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J. Immunol. 177: 7515-7519. (Pubitemid 44846265)
53. van Gisbergen, K. P., P. L. Klarenbeek, N. A. Kragten, P. P. Unger, M. B. Nieuwenhuis, F. M. Wensveen, A. ten Brinke, P. P. Tak, E. Eldering, M. A. Nolte, and R. A. van Lier. 2011. The costimulatory molecule CD27 maintains clonally diverse CD8(+) T cell responses of low antigen affinity to protect against viral variants. Immunity 35: 97-108.
54. Fuse, S., S. Bellfy, H. Yagita, and E. J. Usherwood. 2007. CD8+ T cell dysfunction and increase in murine gammaherpesvirus latent viral burden in the absence of 4-1BB ligand. J. Immunol. 178: 5227-5236. (Pubitemid 46595307)
55. Chandele, A., N. S. Joshi, J. Zhu, W. E. Paul, W. J. Leonard, and S. M. Kaech. 2008. Formation of IL-7Ralphahigh and IL-7Ralphalow CD8 T cells during infection is regulated by the opposing functions of GABPalpha and Gfi-1. J. Immunol. 180: 5309-5319.
56. Kerdiles, Y. M., D. R. Beisner, R. Tinoco, A. S. Dejean, D. H. Castrillon, R. A. DePinho, and S. M. Hedrick. 2009. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10: 176-184.
57. Feng, X., H. Wang, H. Takata, T. J. Day, J. Willen, and H. Hu. 2011. Transcription factor Foxp1 exerts essential cell-intrinsic regulation of the quiescence of naive T cells. Nat. Immunol. 12: 544-550.
58. Grenningloh, R., T. S. Tai, N. Frahm, T. C. Hongo, A. T. Chicoine, C. Brander, D. E. Kaufmann, and I. C. Ho. 2011. Ets-1 maintains IL-7 receptor expression in peripheral T cells. J. Immunol. 186: 969-976.
59. Carr, J. M., M. J. Carrasco, J. E. Thaventhiran, P. J. Bambrough, M. Kraman, A. D. Edwards, A. Al-Shamkhani, and D. T. Fearon. 2006. CD27 mediates interleukin-2-independent clonal expansion of the CD8+ T cell without effector differentiation. Proc. Natl. Acad. Sci. USA 103: 19454-19459. (Pubitemid 46026052)
60. Pellegrini, M., T. Calzascia, A. R. Elford, A. Shahinian, A. E. Lin, D. Dissanayake, S. Dhanji, L. T. Nguyen, M. A. Gronski, M. Morre, et al. 2009. Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat. Med. 15: 528-536.
61. Pellegrini, M., T. Calzascia, J. G. Toe, S. P. Preston, A. E. Lin, A. R. Elford, A. Shahinian, P. A. Lang, K. S. Lang, M. Morre, et al. 2011. IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144: 601-613.