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CD28 and Cd27 Costimulation of Cd8+ T Cells: A Story of Survival

  • Douglas V. Dolfi
  • Peter D. Katsikis
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 590)

Abstract

The role of costimulation in antiviral CD8+ T cells responses is becoming increasingly important as we try to develop adjuvant technologies for therapeutic or vaccine applications. Understanding how costimulation signals work and being able to harness their function to promote robust and protective immune responses is of particular interest. Much of current immunological research is addressing the many costimulatory molecules that are being discovered and characterized in order to elucidate the different mechanisms by which they work. It is becoming clear that multiple costimulation molecules are involved during the different phases of the CD8+ T cell response providing important proliferative and survival signals for these cells. The concept of T cell costimulation has evolved from the initial concept of the single CD28 second signal to an increasingly complex array of costimulation signals that involve multiple members of the B7:CD28 and TNFα/TNFR families. This review will focus on CD28 and CD27 costimulation and examine their involvement in the costimulation of CD8+ T cell responses and the role of such costimulation in the survival of activated, resting, and memory CD8+ T cells. We will also examine the importance of costimulatory-induced survival in antiviral CD8+ T cell responses.

Keywords

Cell Response Costimulatory Molecule Secondary Response CD27 Costimulation Single Positive 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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7. References

  1. 1.
    P. Bretscher and M. Cohn. A theory of self-nonself discrimination. Science 169(950):1042–1049 (1970).PubMedCrossRefGoogle Scholar
  2. 2.
    D.L. Mueller, M.K. Jenkins and R.H. Schwartz. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu Rev Immunol 7:445–480 (1989).PubMedGoogle Scholar
  3. 3.
    F.A. Harding, J.G. McArthur, J.A. Gross, D.H. Raulet and J.P. Allison. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356(6370):607–609 (1992).PubMedCrossRefGoogle Scholar
  4. 4.
    R.J. Greenwald, G.J. Freeman and A.H. Sharpe. The B7 family revisited. Annu Rev Immunol 23:515–548 (2005).PubMedCrossRefGoogle Scholar
  5. 5.
    J.L. Riley and C.H. June. The CD28 family: a T-cell rheostat for therapeutic control of T-cell activation. Blood 105(1):13–21 (2005).PubMedCrossRefGoogle Scholar
  6. 6.
    M. Croft. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol 3(8):609–620 (2003).PubMedCrossRefGoogle Scholar
  7. 7.
    C.A. Janeway Jr. A tale of two T cells. Immunity 8(4):391–394 (1998).PubMedCrossRefGoogle Scholar
  8. 8.
    K. Laky and B.J. Fowlkes. Receptor signals and nuclear events in CD4 and CD8 T cell lineage commitment. Curr Opin Immunol 17(2):116–121 (2005).PubMedCrossRefGoogle Scholar
  9. 9.
    R.N. Germain. T-cell development and the CD4-CD8 lineage decision. Nat Rev Immunol 2(5):309–322 (2002).PubMedCrossRefGoogle Scholar
  10. 10.
    H.Y. Irie, M.S. Mong, A. Itano, M.E. Crooks, D.R. Littman, S.J. Burakoff and E. Robey. The cytoplasmic domain of CD8 beta regulates Lck kinase activation and CD8 T cell development. J Immunol 161(1):183–191 (1998).PubMedGoogle Scholar
  11. 11.
    G. Hernandez-Hoyos, S.J. Sohn, E.V. Rothenberg and J. Alberola-Ila. Lck Activity Controls CD4/CD8 T Cell Lineage Commitment. Immunity 12(3):313 (2000).PubMedCrossRefGoogle Scholar
  12. 12.
    I. Maillard, T. Fang and W.S. Pear. Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu Rev Immunol 23:945–974 (2005).PubMedCrossRefGoogle Scholar
  13. 13.
    H. von Boehmer. Notch in lymphopoiesis and T cell polarization. Nat Immunol 6(7):641–642 (2005).CrossRefGoogle Scholar
  14. 14.
    A. Sambandam, I. Maillard, V.P. Zediak, L. Xu, R.M. Gerstein, J.C. Aster, W.S. Pear and A. Bhandoola. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 6(7):663–670 (2005).PubMedCrossRefGoogle Scholar
  15. 15.
    E.A. Robey and J.A. Bluestone. Notch signaling in lymphocyte development and function. Curr Opin Immunol 16(3):360–366 (2004).PubMedCrossRefGoogle Scholar
  16. 16.
    B. Varnum-Finney, L. Xu, C. Brashem-Stein, C. Nourigat, D. Flowers, S. Bakkour, W.S. Pear and I.D. Bernstein. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med 6(11):1278–1281 (2000).PubMedCrossRefGoogle Scholar
  17. 17.
    D.J. Izon, J.A. Punt, L. Xu, F.G. Karnell, D. Allman, P.S. Myung, N.J. Boerth, J.C. Pui, G.A. Koretzky and W.S. Pear. Notch1 regulates maturation of CD4+ and CD8+ thymocytes by modulating TCR signal strength. Immunity 14(3):253–264 (2001).PubMedCrossRefGoogle Scholar
  18. 18.
    A. de La Coste, E. Six, N. Fazilleau, L. Mascarell, N. Legrand, M.P. Mailhe, A. Cumano, Y. Laabi and A.A. Freitas. In vivo and in absence of a thymus, the enforced expression of the Notch ligands delta-1 or delta-4 promotes T cell development with specific unique effects. J Immunol 174(5):2730–2737 (2005).Google Scholar
  19. 19.
    L.A. Turka, J.A. Ledbetter, K. Lee, C.H. June and C.B. Thompson. CD28 is an inducible T cell surface antigen that transduces a proliferative signal in CD3+ mature thymocytes. J Immunol 144(5):1646–1653 (1990).PubMedGoogle Scholar
  20. 20.
    L.A. Turka, P.S. Linsley, R. d. Paine, G.L. Schieven, G.B. Thompson and J.A. Ledbetter. Signal transduction via CD4, CD8, and CD28 in mature and immature thymocytes: implications for thymic selection. J Immunol 146(5):1428–1436 (1991).PubMedGoogle Scholar
  21. 21.
    J.A. Gross, E. Callas and J.P. Allison. Identification and distribution of the costimulatory receptor CD28 in the mouse. J Immunol 149(2):380–388 (1992).PubMedGoogle Scholar
  22. 22.
    X. Zheng, J.-X. Gao, X. Chang, Y. Wang, Y. Liu, J. Wen, H. Zhang, J. Zhang, Y. Liu and P. Zheng. B7-CD28 interaction promotes proliferation and survival but suppresses differentiation of CD4-CD8-T cells in the thymus. J Immunol 173(4):2253–2261 (2004).PubMedGoogle Scholar
  23. 23.
    J.A. Williams, K.S. Hathcock, D. Klug, Y. Harada, B. Choudhury, J.P. Allison, R. Abe and R.J. Hodes. Regulated costimulation in the thymus is critical for T cell development: dysregulated CD28 costimulation can bypass the pre-TCR checkpoint. J Immunol 175(7):4199–4207 (2005).PubMedGoogle Scholar
  24. 24.
    M.S. Vacchio, J.A. Williams and R.J. Hodes. A novel role for CD28 in thymic selection: elimination of CD28/B7 interactions increases positive selection. Eur J Immunol 35(2):418–427 (2005).PubMedCrossRefGoogle Scholar
  25. 25.
    L. Gravestein, W. van Ewijk, F. Ossendorp and J. Borst. CD27 cooperates with the pre-T cell receptor in the regulation of murine T cell development. J Exp Med 184(2):675–685 (1996).PubMedCrossRefGoogle Scholar
  26. 26.
    K. Tesselaar, Y. Xiao, R. Arens, G.M.W. van Schijndel, D.H. Schuurhuis, R.E. Mebius, J. Borst and R.A.W. van Lier. Expression of the murine CD27 ligand CD70 in vitro and in vivo. J Immunol 170(1):33–40 (2003).PubMedGoogle Scholar
  27. 27.
    J. Hendriks, L.A. Gravestein, K. Tesselaar, R.A. van Lier, T.N. Schumacher and J. Borst. CD27 is required for generation and long-term maintenance of T cell immunity. Nat Immunol 1(5):433–440 (2000).PubMedCrossRefGoogle Scholar
  28. 28.
    S. Stoll, J. Delon, T.M. Brotz and R.N. Germain. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296(5574):1873–1876 (2002).PubMedCrossRefGoogle Scholar
  29. 29.
    T.R. Mempel, S.E. Henrickson and U.H. Von Andrian. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427(6970):154–159 (2004).PubMedCrossRefGoogle Scholar
  30. 30.
    R.L. Lindquist, G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M.L. Dustin and M.C. Nussenzweig. Visualizing dendritic cell networks in vivo. Nat Immunol 5(12):1243–1250 (2004).PubMedCrossRefGoogle Scholar
  31. 31.
    S. Hugues, L. Fetler, L. Bonifaz, J. Helft, F. Amblard and S. Amigorena. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol 5(12):1235–1242 (2004).PubMedCrossRefGoogle Scholar
  32. 32.
    A. Lanzavecchia and F. Sallusto. Lead and follow: the dance of the dendritic cell and T cell. Nat Immunol 5(12):1201–1202 (2004).PubMedCrossRefGoogle Scholar
  33. 33.
    C.H. June, J.A. Ledbetter, M.M. Gillespie, T. Lindsten and C.B. Thompson. T-cell proliferation involving the CD28 pathway is associated with cyclosporine-resistant interleukin 2 gene expression. Mol Cell Biol 7(12):4472–4481 (1987).PubMedGoogle Scholar
  34. 34.
    A.I. Sperling, J.A. Auger, B.D. Ehst, I.C. Rulifson, C.B. Thompson and J.A. Bluestone. CD28/B7 interactions deliver a unique signal to naive T cells that regulates cell survival but not early proliferation. J Immunol 157(9):3909–3917 (1996).PubMedGoogle Scholar
  35. 35.
    S. Kirchhoff, W.W. Muller, M. Li-Weber and P.H. Krammer. Up-regulation of c-FLIPshort and reduction of activation-induced cell death in CD28-costimulated human T cells. Eur J Immunol 30(10):2765–2774 (2000).PubMedCrossRefGoogle Scholar
  36. 36.
    K.A. Frauwirth, J.L. Riley, M.H. Harris, R.V. Parry, J.C. Rathmell, D.R. Plas, R.L. Elstrom, C.H. June and C.B. Thompson. The CD28 signaling pathway regulates glucose metabolism. Immunity 16(6):769–777 (2002).PubMedCrossRefGoogle Scholar
  37. 37.
    C.B. Thompson, T. Lindsten, J.A. Ledbetter, S.L. Kunkel, H.A. Young, S.G. Emerson, J.M. Leiden and C.H. June. CD28 activation pathway regulates the production of multiple T-cell-derived lymphokines/cytokines. PNAS 86(4):1333–1337 (1989).PubMedCrossRefGoogle Scholar
  38. 38.
    O. Acuto and F. Michel. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 3(12):939–951 (2003).PubMedCrossRefGoogle Scholar
  39. 39.
    A.V. Gett, F. Sallusto, A. Lanzavecchia and J. Geginat. T cell fitness determined by signal strength. Nat Immunol 4(4):355–360 (2003).PubMedCrossRefGoogle Scholar
  40. 40.
    A.D. Wells, H. Gudmundsdottir and L.A. Turka. Following the fate of individual T cells throughout activation and clonal expansion: signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J Clin Invest 100(12):3173–3183 (1997).PubMedCrossRefGoogle Scholar
  41. 41.
    H. Gudmundsdottir, A.D. Wells and L.A. Turka. Dynamics and requirements of T Cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J Immunol 162(9):5212–5223 (1999).PubMedGoogle Scholar
  42. 42.
    A. Shahinian, K. Pfeffer, K.P. Lee, T.M. Kundig, K. Kishihara, A. Wakeham, K. Kawai, P.S. Ohashi, C.B. Thompson and T.W. Mak. Differential T cell costimulatory requirements in CD28-deficient mice. Science 261(5121):609–612 (1993).PubMedCrossRefGoogle Scholar
  43. 43.
    T.M. Kundig, A. Shahinian, K. Kawai, H.W. Mittrucker, E. Sebzda, M.F. Bachmann, T.W. Mak and P.S. Ohashi. Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 5(1):41–52 (1996).PubMedCrossRefGoogle Scholar
  44. 44.
    E.S. Halstead, Y.M. Mueller, J.D. Altman and P.D. Katsikis. In vivo stimulation of CD137 broadens primary antiviral CD8(+) T cell responses. Nat Immunol 3(6):536–541 (2002).PubMedCrossRefGoogle Scholar
  45. 45.
    S.O. Andreasen, J.E. Christensen, O. Marker and A.R. Thomsen. Role of CD40 ligand and CD28 in induction and maintenance of antiviral CD8+ effector T cell responses. J Immunol 164(7):3689–3697 (2000).PubMedGoogle Scholar
  46. 46.
    V.P. Badovinac, B.B. Porter and J.T. Harty. CD8+ T cell contraction is controlled by early inflammation. Nat Immunol 5(8):809 (2004).PubMedCrossRefGoogle Scholar
  47. 47.
    G.A. Corbin and J.T. Harty. Duration of infection and antigen display have minimal influence on the kinetics of the CD4+ T cell response to Listeria monocytogenes infection. J Immunol 173(9):5679–5687 (2004).PubMedGoogle Scholar
  48. 48.
    C. Zimmermann, P. Seiler, P. Lane and R.M. Zinkernagel. Antiviral immune responses in CTLA4 transgenic mice. J Virol 71(3):1802–1807 (1997).PubMedGoogle Scholar
  49. 49.
    M. Kopf, A.J. Coyle, N. Schmitz, M. Barner, A. Oxenius, A. Gallimore, J.C. Gutierrez-Ramos and M.F. Bachmann. Inducible costimulator protein (ICOS) controls T helper cell subset polarization after virus and parasite infection. J Exp Med 192(1):53–61 (2000).PubMedCrossRefGoogle Scholar
  50. 50.
    Y. Liu, R.H. Wenger, M. Zhao and P.J. Nielsen. Distinct costimulatory molecules are required for the induction of effector and memory cytotoxic T lymphocytes. J Exp Med 185(2):251–262 (1997).PubMedCrossRefGoogle Scholar
  51. 51.
    J.K. Whitmire and R. Ahmed. Costimulation in antiviral immunity: differential requirements for CD4(+) and CD8(+) T cell responses. Curr Opin Immunol 12(4):448–455 (2000).PubMedCrossRefGoogle Scholar
  52. 52.
    J. Hendriks, Y. Xiao and J. Borst. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J Exp Med 198(9):1369–1380 (2003).PubMedCrossRefGoogle Scholar
  53. 53.
    A. Yamada, A.D. Salama, M. Sho, N. Najafian, T. Ito, J.P. Forman, R. Kewalramani, S. Sandner, H. Harada, M.R. Clarkson, D.A. Mandelbrot, A.H. Sharpe, H. Oshima, H. Yagita, G. Chalasani, F.G. Lakkis, H. Auchincloss Jr. and M.H. Sayegh. CD70 signaling is critical for CD28-independent CD8+ T cell-mediated alloimmune responses in vivo. J Immunol 174(3):1357–1364 (2005).PubMedGoogle Scholar
  54. 54.
    R. van Lier, J. Borst, T. Vroom, H. Klein, P. Van Mourik, W. Zeijlemaker and C. Melief. Tissue distribution and biochemical and functional properties of Tp55 (CD27), a novel T cell differentiation antigen. J Immunol 139(5):1589–1596 (1987).PubMedGoogle Scholar
  55. 55.
    K. Tesselaar, R. Arens, G.M. van Schijndel, P.A. Baars, M.A. van der Valk, J. Borst, M.H. van Oers and R.A. van Lier. Lethal T cell immunodeficiency induced by chronic costimulation via CD27-CD70 interactions. Nat Immunol 4(1):49–54 (2003).PubMedCrossRefGoogle Scholar
  56. 56.
    R. Arens, K. Tesselaar, P.A. Baars, G.M. van Schijndel, J. Hendriks, S.T. Pals, P. Krimpenfort, J. Borst, M.H. van Oers and R.A. van Lier. Constitutive CD27/CD70 interaction induces expansion of effector-type T cells and results in IFNgammamediated B cell depletion. Immunity 15(5):801–812 (2001).PubMedCrossRefGoogle Scholar
  57. 57.
    T.F. Rowley and A. Al-Shamkhani. Stimulation by soluble CD70 promotes strong primary and secondary CD8+ cytotoxic T cell responses in vivo. J Immunol 172(10):6039–6046 (2004).PubMedGoogle Scholar
  58. 58.
    A. Laouar, V. Haridas, D. Vargas, X. Zhinan, D. Chaplin, R.A. van Lier and N. Manjunath. CD70+ antigen-presenting cells control the proliferation and differentiation of T cells in the intestinal mucosa. Nat Immunol 6(7):698–706 (2005).PubMedCrossRefGoogle Scholar
  59. 59.
    E.M. Bertram, W. Dawicki, B. Sedgmen, J.L. Bramson, D.H. Lynch and T.H. Watts. A switch in costimulation from CD28 to 4-1BB during primary versus secondary CD8 T cell response to influenza in vivo. J Immunol 172(2):981–988 (2004).PubMedGoogle Scholar
  60. 60.
    C.C. Ku, M. Murakami, A. Sakamoto, J. Kappler and P. Marrack. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 288(5466):675–678 (2000).PubMedCrossRefGoogle Scholar
  61. 61.
    X.C. Li, G. Demirci, S. Ferrari-Lacraz, C. Groves, A. Coyle, T.R. Malek and T.B. Strom. IL-15 and IL-2: a matter of life and death for T cells in vivo. Nat Med 7(1):114–118 (2001).PubMedCrossRefGoogle Scholar
  62. 62.
    J.T. Tan, B. Ernst, W.C. Kieper, E. LeRoy, J. Sprent and C.D. Surh. 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 195(12):1523–1532 (2002).PubMedCrossRefGoogle Scholar
  63. 63.
    W.C. Kieper, J.T. Tan, B. Bondi-Boyd, L. Gapin, J. Sprent, R. Ceredig and C.D. Surh. Overexpression of interleukin (IL)-7 Leads to IL-15-independent generation of memory phenotype CD8(+) T cells. J Exp Med 195(12):1533–1539 (2002).PubMedCrossRefGoogle Scholar
  64. 64.
    T.C. Becker, E.J. Wherry, D. Boone, K. Murali-Krishna, R. Antia, A. Ma and R. Ahmed. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J Exp Med 195(12):1541–1548 (2002).PubMedCrossRefGoogle Scholar
  65. 65.
    A.D. Judge, X. Zhang, H. Fujii, C.D. Surh and J. Sprent. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J Exp Med 196(7):935–946 (2002).PubMedCrossRefGoogle Scholar
  66. 66.
    K.S. Schluns and L. Lefrancois. Cytokine control of memory T-cell development and survival. Nat Rev Immunol 3(4):269–279 (2003).PubMedCrossRefGoogle Scholar
  67. 67.
    Y.M. Mueller, V. Makar, P.M. Bojczuk, J. Witek and P.D. Katsikis. IL-15 enhances the function and inhibits CD95/Fas-induced apoptosis of human CD4+ and CD8+ effector-memory T cells. Int Immunol 15(1):49–58 (2003).PubMedCrossRefGoogle Scholar
  68. 68.
    K.S. Schluns, W.C. Kieper, S.C. Jameson and L. Lefrancois. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 1(5):426–432 (2000).PubMedCrossRefGoogle Scholar
  69. 69.
    S. Jaleco, L. Swainson, V. Dardalhon, M. Burjanadze, S. Kinet and N. Taylor. Homeostasis of naive and memory CD4+ T cells: IL-2 and IL-7 differentially regulate the balance between proliferation and Fas-mediated apoptosis. J Immunol 171(1):61–68 (2003).PubMedGoogle Scholar
  70. 70.
    E. Maraskovsky, M. Teepe, P. Morrissey, S. Braddy, R. Miller, D. Lynch and J. Peschon. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J Immunol 157(12):5315–5323 (1996).PubMedGoogle Scholar
  71. 71.
    H. Dooms, E. Kahn, B. Knoechel and A.K. Abbas. IL-2 induces a competitive survival advantage in T lymphocytes. J Immunol 172(10):5973–5979 (2004).PubMedGoogle Scholar
  72. 72.
    S.M. Kaech and R. Ahmed. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2(5):415–422 (2001).PubMedGoogle Scholar
  73. 73.
    M.J. Bevan and P.J. Fink. The CD8 response on autopilot. Nat Immunol 2(5):381–382 (2001).PubMedGoogle Scholar
  74. 74.
    K. Murali-Krishna, J.D. Altman, M. Suresh, D.J. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky and R. Ahmed. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8(2):177–187 (1998).PubMedCrossRefGoogle Scholar
  75. 75.
    S. Hou, L. Hyland, K.W. Ryan, A. Portner and P.C. Doherty. Virus-specific CD8+ T-cell memory determined by clonal burst size. Nature 369(6482):652–654 (1994).PubMedCrossRefGoogle Scholar
  76. 76.
    N. Manjunath, P. Shankar, J. Wan, W. Weninger, M.A. Crowley, K. Hieshima, T.A. Springer, X. Fan, H. Shen, J. Lieberman and U.H. von Andrian. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J Clin Invest 108(6):871–878 (2001).PubMedCrossRefGoogle Scholar
  77. 77.
    D.L. Woodland and M.A. Blackman. Vaccine development: baring the ‘dirty little secret’. Nat Med 11(7):715 (2005).PubMedCrossRefGoogle Scholar
  78. 78.
    A. Wiesmann, R.L. Phillips, M. Mojica, L.J. Pierce, A.E. Searles, G.J. Spangrude and I. Lemischka. Expression of CD27 on murine hematopoietic stem and progenitor cells. Immunity 12(2):193–199 (2000).PubMedCrossRefGoogle Scholar
  79. 79.
    K. Tesselaar, L. Gravestein, G. van Schijndel, J. Borst and R. van Lier. Characterization of murine CD70, the ligand of the TNF receptor family member CD27. J Immunol 159(10):4959–4965 (1997).PubMedGoogle Scholar
  80. 80.
    R. de Jong, W. Loenen, M. Brouwer, L. van Emmerik, E. de Vries, J. Borst and R. van Lier. Regulation of expression of CD27, a T cell-specific member of a novel family of membrane receptors. J Immunol 146(8):2488–2494 (1991).PubMedGoogle Scholar
  81. 81.
    M. Bowman, M. Crimmins, J. Yetz-Aldape, R. Kriz, K. Kelleher and S. Herrmann. The cloning of CD70 and its identification as the ligand for CD27. J Immunol 152(4):1756–1761 (1994).PubMedGoogle Scholar
  82. 82.
    L.E. Gamadia, E.M. M. van Leeuwen, E.B.M. Remmerswaal, S.-L. Yong, S. Surachno, P.M.E. Wertheim-van Dillen, I.J.M. ten Berge and R.A.W. van Lier. The size and phenotype of virus-specific T cell populations is determined by repetitive antigenic stimulation and environmental cytokines. J Immunol 172(10):6107–6114 (2004).PubMedGoogle Scholar
  83. 83.
    B. Jamieson and R. Ahmed. T cell memory. Long-term persistence of virus-specific cytotoxic T cells. J Exp Med 169(6):1993–2005 (1989).PubMedCrossRefGoogle Scholar
  84. 84.
    V. Appay, P.R. Dunbar, M. Callan, P. Klenerman, G.M. Gillespie, L. Papagno, G.S. Ogg, A. King, F. Lechner, C.A. Spina, S. Little, D.V. Havlir, D.D. Richman, N. Gruener, G. Pape, A. Waters, P. Easterbrook, M. Salio, V. Cerundolo, A.J. McMichael and S.L. Rowland-Jones. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 8(4):379–385 (2002).PubMedCrossRefGoogle Scholar
  85. 85.
    F. Sallusto and A. Lanzavecchia. Exploring pathways for memory T cell generation. J Clin Invest 108(6):805–806 (2001).PubMedCrossRefGoogle Scholar
  86. 86.
    M.J. van Stipdonk, E.E. Lemmens and S.P. Schoenberger. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2(5):423–429 (2001).PubMedGoogle Scholar
  87. 87.
    A.L. Marzo, K.D. Klonowski, A. Le Bon, P. Borrow, D.F. Tough and L. Lefrancois. Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nat Immunol 6(8):793–799 (2005).PubMedCrossRefGoogle Scholar
  88. 88.
    M.A. Williams and M.J. Bevan. T cell memory: fixed or flexible? Nat Immunol 6(8):752 (2005).PubMedCrossRefGoogle Scholar
  89. 89.
    V.P. Badovinac and J.T. Harty. Memory lanes. Nat Immunol 4(3):212–213 (2003).PubMedCrossRefGoogle Scholar
  90. 90.
    E.J. Wherry, V. Teichgraber, T.C. Becker, D. Masopust, S.M. Kaech, R. Antia, U.H. von Andrian and R. Ahmed. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 4(3):225–234 (2003).PubMedCrossRefGoogle Scholar
  91. 91.
    S.M. Kaech, J.T. Tan, E.J. Wherry, B.T. Konieczny, C.D. Surh and R. Ahmed. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4(12):1191–1198 (2003).PubMedCrossRefGoogle Scholar
  92. 92.
    C.M. Smith, N.S. Wilson, J. Waithman, J.A. Villadangos, F.R. Carbone, W.R. Heath and G.T. Belz. Cognate CD4(+) T cell licensing of dendritic cells in CD8(+) T cell immunity. Nat Immunol 5(11):1143–1148 (2004).PubMedCrossRefGoogle Scholar
  93. 93.
    G.T. Belz, H. Liu, S. Andreansky, P.C. Doherty and P.G. Stevenson. Absence of a functional defect in CD8+ T cells during primary murine gammaherpesvirus-68 infection of I-Ab-/- mice. J Gen Virol 84(2):337–341 (2003).PubMedCrossRefGoogle Scholar
  94. 94.
    M.J. Bevan. Helping the CD8(+) T-cell response. Nat Rev Immunol 4(8):595–602 (2004).PubMedCrossRefGoogle Scholar
  95. 95.
    A.L. Marzo, V. Vezys, K.D. Klonowski, S.-J. Lee, G. Muralimohan, M. Moore, D.F. Tough and L. Lefrancois. Fully functional memory CD8 T cells in the absence of CD4 T cells. J Immunol 173(2):969–975 (2004).PubMedGoogle Scholar
  96. 96.
    D.J. Shedlock and H. Shen. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300(5617):337–339 (2003).PubMedCrossRefGoogle Scholar
  97. 97.
    J.C. Sun and M.J. Bevan. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300(5617):339–342 (2003).PubMedCrossRefGoogle Scholar
  98. 98.
    J.C. Sun, M.A. Williams and M.J. Bevan. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 5(9):927–933 (2004).PubMedCrossRefGoogle Scholar
  99. 99.
    S. Jung, D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, E.G. Pamer, D.R. Littman and R.A. Lang. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17(2):211–220 (2002).PubMedCrossRefGoogle Scholar
  100. 100.
    D.J. Zammit, L.S. Cauley, Q.M. Pham and L. Lefrancois. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22(5):561–570 (2005).PubMedCrossRefGoogle Scholar
  101. 101.
    M. Suresh, J.K. Whitmire, L.E. Harrington, C.P. Larsen, T.C. Pearson, J.D. Altman and R. Ahmed. Role of CD28-B7 interactions in generation and maintenance of CD8 T cell memory. J Immunol 167(10):5565–5573 (2001).PubMedGoogle Scholar
  102. 102.
    H.-W. Mittrucker, M. Kursar, A. Kohler, R. Hurwitz and S.H.E. Kaufmann. Role of CD28 for the generation and expansion of antigen-specific CD8+ T lymphocytes during infection with Listeria monocytogenes. J Immunol 167(10):5620–5627 (2001).PubMedGoogle Scholar
  103. 103.
    J. Hendriks, Y. Xiao, J.W.A. Rossen, K.F. van der Sluijs, K. Sugamura, N. Ishii and J. Borst. During viral infection of the respiratory tract, CD27, 4-1BB, and OX40 collectively determine formation of CD8+ memory T cells and their capacity for secondary expansion. J Immunol 175(3):1665–1676 (2005).PubMedGoogle Scholar
  104. 104.
    J.E. Moyron-Quiroz, J. Rangel-Moreno, K. Kusser, L. Hartson, F. Sprague, S. Goodrich, D.L. Woodland, F.E. Lund and T.D. Randall. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med 10(9):927–934 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Douglas V. Dolfi
    • 1
  • Peter D. Katsikis
    • 1
  1. 1.Department of Microbiology and ImmunologyDrexel University College of MedicinePhiladelphiaUSA

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