Secondary memory CD8+ T cells are more protective but slower to acquire a central-memory phenotype

Journal of Experimental Medicine

Volumn 203, Issue 4, 2006, Pages 919-932

  Jabbari, Ali ^a   Harty, John T ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 2; PADGEM PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN FUNCTION; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELL PROTECTION; COCULTURE; CONTROLLED STUDY; CYTOLYSIS; IN VIVO STUDY; LISTERIA MONOCYTOGENES; LYMPH NODE; MEMORY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; L-SELECTIN; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTE SUBSETS;

EID: 33645843343     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052237     Document Type: Article

References (53)

1. Sprent, J., and C.D. Surh. 2002. T cell memory. Annu. Rev. Immunol. 20:551-579.
2. Woodland, D.L. 2004. Jump-starting the immune system: prime-boosting comes of antigene. Trends Immunol. 25:98-104.
3. Masopust, D., V. Vezys, A.L. Marzo, and L. Lefrancois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science. 291:2413-2417.
4. Harty, J.T., and V.P. Badovinac. 2002. Influence of effector molecules on the CD8(+) T cell response to infection. Curr. Opin. Immunol. 14:360-365.
5. Harty, J.T., A.R. Tvinnereim, and D.W. White. 2000. CD8+ T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18:275-308.
6. Badovinac, V.P., B.B. Porter, and J.T. Harty. 2002. Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 3:619-626.
7. Vitetta, E.S., M.T. Berton, C. Burger, M. Kepron, W.T. Lee, and X.M. Yin. 1991. Memory B and T cells. Annu. Rev. Immunol. 9:193-217.
8. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science. 272:54-60.
9. Sprent, J., and D.F. Tough. 1994. Lymphocyte life-span and memory. Science. 265:1395-1400.
10. Homann, D., L. Teyton, and M.B. Oldstone. 2001. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7:913-919.
11. Wherry, E.J., and R. Ahmed. 2004. Memory CD8 T-cell differentiation during viral infection. J. Virol. 78:5535-5545.
12. Weninger, W., N. Manjunath, and U.H. von Andrian. 2002. Migration and differentiation of CD8+ T cells. Immunol. Rev. 186:221-233.
13. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401:708-712.
14. Wherry, E.J., V. Teichgraber, 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.
15. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22:745-763.
16. Roberts, A.D., and D.L. Woodland. 2004. Cutting edge: effector memory CD8+ T cells play a prominent role in recall responses to secondary viral infection in the lung. J. Immunol. 172:6533-6537.
17. Badovinac, V.P., K.A. Messingham, A. Jabbari, J.S. Haring, and J.T. Harty. 2005. Accelerated CD8(+) T-cell memory and prime-boost response after dendritic-cell vaccination. Nat. Med. 11:748-756.
18. Badovinac, V.P., B.B. Porter, and J.T. Harty. 2004. CD8+ T cell contraction is controlled by early inflammation. Nat. Immunol. 5:809-817.
19. Busch, D.H., I.M. Pilip, S. Vijh, and E.G.P. Am. 1998. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity. 8:353-362.
20. Badovinac, V.P., K.A. Messingham, S.E. Hamilton, and J.T. Harty. 2003. Regulation of CD8+ T cells undergoing primary and secondary responses to infection in the same host. J. Immunol. 170:4933-4942.
21. Grayson, J.M., L.E. Harrington, J.G. Lanier, E.J. Wherry, and R. Ahmed. 2002. Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J. Immunol. 169:3760-3770.
22. Roberts, A.D., K.H. Ely, and D.L. Woodland. 2005. Differential contributions of central and effector memory T cells to recall responses. J. Exp. Med. 202:123-133.
23. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
24. Shen, H., J.F. Miller, X. Fan, D. Kolwyck, R. Ahmed, and J.T. Harty. 1998. Compartmentalization of bacterial antigens: differential effects on priming of CD8 T cells and protective immunity. Cell. 92:535-545.
25. Pope, C., S.K. Kim, A. Marzo, D. Masopust, K. Williams, J. Jiang, H. Shen, and L. Lefrancois. 2001. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166:3402-3409.
26. Haring, J.S., G.A. Corbin, and J.T. Harty. 2005. Dynamic regulation of IFN-gamma signaling in antigen-specific CD8+ T cells responding to infection. J. Immunol. 174:6791-6802.
27. Marzo, A.L., K.D. Klonowski, A.L. Bon, P. Borrow, D.F. Tough, and L. Lefrancois. 2005. Initial T cell frequency dictates memory CD8(+) T cell lineage commitment. Nat. Immunol. 6:793-799.
28. Hogquist, K.A., S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell. 76:17-27.
29. Murali-Krishna, K., L.L. Lau, S. Sambhara, F. Lemonnier, J. Altman, and R. Ahmed. 1999. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science. 286:1377-1381.
30. Lau, L.L., B.D. Jamieson, T. Somasundaram, and R. Ahmed. 1994. Cytotoxic T-cell memory without antigen. Nature. 369:648-652.
31. Becker, T.C., E.J. Wherry, D. Boone, K. Murali-Krishna, R. Antia, A. Ma, and R. Ahmed. 2002. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J. Exp. Med. 195:1541-1548.
32. Tan, J.T., B. Ernst, W.C. Kieper, E. LeRoy, J. Sprent, and C.D. Surh. 2002. 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. 195:1523-1532.
33. Goldrath, A.W., P.V. Sivakumar, M. Glaccum, M.K. Kennedy, M.J. Bevan, C. Benoist, D. Mathis, and E.A. Butz. 2002. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 195:1515-1522.
34. Schluns, K.S., K.D. Klonowski, and L. Lefrancois. 2004. Transregulation of memory CD8 T-cell proliferation by IL-15Ralpha+ bone marrow-derived cells. Blood. 103:988-994.
35. Sandau, M.M., K.S. Schluns, L. Lefrancois, and S.C. Jameson. 2004. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15Ralpha by the same cells. J. Immunol. 173:6537-6541.
36. Ochsenbein, A.F., U. Karrer, P. Klenerman, A. Althantigene, A. Ciurea, H. Shen, J.F. Miller, J.L. Whitton, H. Hengartner, and R.M. Zinkernantigenel. 1999. A comparison of T cell memory against the same antigen induced by virus versus intracellular bacteria. Proc. Natl. Acad. Sci. USA. 96:9293-9298.
37. Corbin, G.A., and J.T. Harty. 2004. Duration of infection and antigen display have minimal influence on the kinetics of the CD4+ T cell response to Listeria monocytogenes infection. J. Immunol. 173:5679-5687.
38. Slifka, M.K., and J.L. Whitton. 2001. Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat. Immunol. 2:711-717.
39. Messingham, K.A., V.P. Badovinac, and J.T. Harty. 2003. Deficient anti-listerial immunity in the absence of perforin can be restored by increasing memory CD8+ T cell numbers. J. Immunol. 171:4254-4262.
40. Shresta, S., C.T. Pham, D.A. Thomas, T.A. Graubert, and T.J. Ley. 1998. How do cytotoxic lymphocytes kill their targets? Curr. Opin. Immunol. 10:581-587.
41. Wolint, P., M.R. Betts, R.A. Koup, and A. Oxenius. 2004. Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J. Exp. Med. 199:925-936.
42. Kedl, R.M., W.A. Rees, D.A. Hildeman, B. Schaefer, T. Mitchell, J. Kappler, and P. Marrack. 2000. T cells compete for access to antigen-bearing antigen-presenting cells. J. Exp. Med. 192:1105-1113.
43. Jacob, J., and D. Baltimore. 1999. Modelling T-cell memory by genetic marking of memory T cells in vivo. Nature. 399:593-597.
44. Opferman, J.T., B.T. Ober, and P.G. Ashton-Rickardt. 1999. Linear differentiation of cytotoxic effectors into memory T lymphocytes. Science. 283:1745-1748.
45. Leclercq, G., and J. Plum. 1996. Thymic and extrathymic T cell development. Leukemia. 10:1853-1859.
46. Kaech, S.M., and R. Ahmed. 2001. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2:415-422.
47. Ogoshi, M., A. Takashima, and R.S. Taylor. 1997. Mechanisms regulating telomerase activity in murine T cells. J. Immunol. 158:622-628.
48. Weng, N.P., K.S. Hathcock, and R.J. Hodes. 1998. Regulation of telomere length and telomerase in T and B cells: a mechanism for maintaining replicative potential. Immunity. 9:151-157.
49. Kaech, S.M., E.J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-262.
50. Tvinnereim, A.R., S.E. Hamilton, and J.T. Harty. 2002. CD8(+)-T-cell response to secreted and nonsecreted antigens delivered by recombinant Listeria monocytogenes during secondary infection. Infect. Immun. 70:153-162.
51. Harty, J.T., and M.J. Bevan. 1995. Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity. 3:109-117.
52. Badovinac, V.P., A.R. Tvinnereim, and J.T. Harty. 2000. Regulation of antigen-specific CD8+ T cell homeostasis by perforin and interferon-gamma. Science. 290:1354-1358.
53. Badovinac, V.P., and J.T. Harty. 2000. Intracellular staining for TNF and IFN-gamma detects different frequencies of antigen-specific CD8(+) T cells. J. Immunol. Methods. 238:107-117.