Immediate Cytotoxicity but Not Degranulation Distinguishes Effector and Memory Subsets of CD8+ T Cells

Journal of Experimental Medicine

Volumn 199, Issue 7, 2004, Pages 925-936

  Wolint, Petra ^a   Betts, Michael R ^b   Koup, Richard A ^b   Oxenius, Annette ^a  

^a ETH ZURICH   (Switzerland)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Central memory; Cytotoxic T cell; Effector memory; Lytic granules; Virus

Indexed keywords

CD8 ANTIGEN; EPITOPE; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; EFFECTOR CELL; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; LYMPH NODE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOCYTOTOXICITY; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL DEGRANULATION; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; IMMUNOLOGIC MEMORY; L-SELECTIN; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTE SUBSETS;

EID: 1842631484     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031799     Document Type: Article

References (35)

1. 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.
2. van Stipdonk, M.J., E.E. Lemmens, and S.P. Schoenberger. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2:423-429.
3. Bachmann, M.F., M. Barner, A. Viola, and M. Kopf. 1999. Distinct kinetics of cytokine production and cytolysis in effector and memory T cells after viral infection. Eur. J. Immunol. 29:291-299.
4. 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.
5. 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.
6. Weninger, W., M.A. Crowley, N. Manjunath, and U.H. von Andrian. 2001. Migratory properties of naive, effector, and memory CD8(+) T cells. J. Exp. Med. 194:953-966.
7. Tussey, L., S. Speller, A. Gallimore, and R. Vessey. 2000. Functionally distinct CD8+ memory T cell subsets in persistent EBV infection are differentiated by migratory receptor expression. Eur. J. Immunol. 30:1823-1829.
8. Unsoeld, H., S. Krautwald, D. Voehringer, U. Kunzendorf, and H. Pircher. 2002. Cutting edge: CCR7+ and CCR7-memory T cells do not differ in immediate effector cell function. J. Immunol. 169:638-641.
9. Ravkov, E.V., C.M. Myrick, and J.D. Altman. 2003. Immediate early effector functions of virus-specific CD8+ CCR7+ memory cells in humans defined by HLA and CC chemokine ligand 19 tetramers. J. Immunol. 170:2461-2468.
10. Kägi, D., B. Ledermann, K. Bürki, P. Seiler, B. Odermatt, K.J. Olsen, E. Podack, R.M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 369:31-37.
11. Schmitz, J.E., M.J. Kuroda, S. Santra, V.G. Sasseville, M.A. Simon, M.A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B.J. Scallon, et al. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 283:857-860.
12. Trapani, J.A., and M.J. Smyth. 2002. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2:735-747.
13. Trambas, C.M., and G.M. Griffiths. 2003. Delivering the kiss of death. Nat. Immunol. 4:399-403.
14. Peters, P.J., J. Borst, V. Oorschot, M. Fukuda, O. Krahenbuhl, J. Tschopp, J.W. Slot, and H.J. Geuze. 1991. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173:1099-1109.
15. Kannan, K., R.M. Stewart, W. Bounds, S.R. Carlsson, M. Fukuda, K.W. Betzing, and R.F. Holcombe. 1996. Lysosome-associated membrane proteins h-LAMP1 (CD107a) and h-LAMP2 (CD107b) are activation-dependent cell surface glycoproteins in human peripheral blood mononuclear cells which mediate cell adhesion to vascular endothelium. Cell. Immunol. 171:10-19.
16. Bossi, G., and G.M. Griffiths. 1999. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5:90-96.
17. Betts, M.R., J.M. Brenchley, D.A. Price, S.C. De Rosa, D.C. Douek, M. Roederer, and R.A. Koup. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods. 281:65-78.
18. Tritel, M., A.M. Stoddard, B.J. Flynn, P.A. Darrah, C.Y. Wu, U. Wille, J.A. Shah, Y. Huang, L. Xu, M.R. Betts, et al. 2003. Prime-boost vaccination with HIV-1 Gag protein and cytosine phosphate guanosine oligodeoxynucleotide, followed by adenovirus, induces sustained and robust humoral and cellular immune responses. J. Immunol. 171:2538-2547.
19. Pircher, H.P., D. Moskophidis, U. Rohrer, K. Bürki, H. Hengartner, and R.M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature. 346:629-633.
20. Oxenius, A., M.F. Bachmann, R.M. Zinkernagel, and H. Hengartner. 1998. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28:390-400.
21. Altman, J.D., P.A. Moss, P.J. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96. (published erratum appears in Science. 1998. 280:1821)
22. Altman, J.D., P.A. Moss, P.J. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96. (published erratum appears in Science. 1998. 280:1821)
23. Bachmann, M.F., A. Oxenius, D.E. Speiser, S. Mariathasan, H. Hengartner, R.M. Zinkernagel, and P.S. Ohashi. 1997. Peptide induced TCR-down regulation predicts agonist/partial agonist properties and strictly correlates with T cell activation. Eur. J. Immunol. 27:2195-2203.
24. Isaaz, S., K. Baetz, K. Olsen, E. Podack, and G.M. Griffiths. 1995. Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway. Eur. J. Immunol. 25:1071-1079.
25. Springer, T.A. 1990. Leucocyte adhesion to cells. Scand. J. Immunol. 32:211-216.
26. Osborn, L. 1990. Leukocyte adhesion to endothelium in inflammation. Cell. 62:3-6.
27. Barber, D.L., E.J. Wherry, and R. Ahmed. 2003. Cutting edge: rapid in vivo killing by memory CD8 T cells. J. Immunol. 171:27-31.
28. Kaech, S.M., S. Hemby, E. Kersh, and R. Ahmed. 2002. Molecular and functional profiling of memory CD8 T cell differentiation. Cell. 111:837-851.
29. Swanson, B.J., M. Murakami, T.C. Mitchell, J. Kappler, and P. Marrack. 2002. RANTES production by memory phenotype T cells is controlled by a posttranscriptional, TCR-dependent process. Immunity. 17:605-615.
30. 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.
31. Byers, A.M., C.C. Kemball, J.M. Moser, and A.E. Lukacher. 2003. Cutting edge: rapid in vivo CTL activity by polyoma virus-specific effector and memory CD8+ T cells. J. Immunol. 171:17-21.
32. Barchet, W., S. Oehen, P. Klenerman, D. Wodarz, G. Bocharov, A.L. Lloyd, M.A. Nowak, H. Hengartner, R.M. Zinkernagel, and S. Ehl. 2000. Direct quantitation of rapid elimination of viral antigen-positive lymphocytes by antiviral CD8(+) T cells in vivo. Eur. J. Immunol. 30:1356-1363.
33. Hermans, I.F., D.S. Ritchie, J. Yang, J.M. Roberts, and F. Ronchese. 2000. CD8+ T cell-dependent elimination of dendritic cells in vivo limits the induction of antitumor immunity. J. Immunol. 164:3095-3101.
34. Medema, J.P., D.H. Schuurhuis, D. Rea, J. van Tongeren, J. de Jong, S.A. Bres, S. Laban, R.E. Toes, M. Toebes, T.N. Schumacher, et al. 2001. Expression of the serpin serine protease inhibitor 6 protects dendritic cells from cytotoxic T lymphocyte-induced apoptosis: differential modulation by T helper type 1 and type 2 cells. J. Exp. Med. 194:657-667.
35. Hirst, C.E., M.S. Buzza, C.H. Bird, H.S. Warren, P.U. Cameron, M. Zhang, P.G. Ashton-Rickardt, and P.I. Bird. 2003. The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency. J. Immunol. 170:805-815.