Antigen delivered by anthrax lethal toxin induces the development of memory CD8+ T cells that can be rapidly boosted and display effector functions

Infection and Immunity

Volumn 76, Issue 3, 2008, Pages 1214-1222

  Shaw, Christine A ^a   Starnbach, Michael N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; CD8 ANTIGEN; HYBRID PROTEIN; L SELECTIN; LFN ANTIGEN FUSION PROTEIN; PROTEIN LFN; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL TOXIN; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 7 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; BACILLUS ANTHRACIS; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY; EFFECTOR CELL; IN VIVO STUDY; INTRACELLULAR TRANSPORT; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VACCINATION; VACCINE PRODUCTION; ANIMAL; BACTERIAL COUNT; BAGG ALBINO MOUSE; CHEMISTRY; CYTOTOXICITY TEST; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MICROBIOLOGY; SPLEEN; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CD8-POSITIVE T-LYMPHOCYTES; COLONY COUNT, MICROBIAL; CYTOTOXICITY TESTS, IMMUNOLOGIC; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; INTERFERON TYPE II; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; L-SELECTIN; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; RECOMBINANT FUSION PROTEINS; SPLEEN; T-LYMPHOCYTE SUBSETS;

EID: 40749151913     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01208-07     Document Type: Article

References (44)

1. Abrami, L., S. Liu, P. Cosson, S. H. Leppla, and F. G. van der Goot. 2003. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 160:321-328.
2. Arora, N., and S. H. Leppla. 1993. Residues 1-254 of anthrax toxin lethal factor are sufficient to cause cellular uptake of fused polypeptides. J. Biol. Chem. 268:3334-3341.
3. + T cell subsets identified by expression of IL-7 receptor alpha and CD62L. J. Immunol. 175: 4686-4696.
4. + T cell generation after acute infection. J. Immunol. 179:53-63.
5. + T-cell memory and prime-boost response after dendritic-cell vaccination. Nat. Med. 11:748-756.
6. + cells. Infect. Immun. 66: 4696-4699.
7. Ballard, J. D., R. J. Collier, and M. N. Starnbach. 1996. Anthrax toxin-mediated delivery of a cytotoxic T-cell epitope in vivo. Proc. Natl. Acad. Sci. USA 93:12531-12534.
8. Ballard, J. D., A. M. Doling, K. Beauregard, R. J. Collier, and M. N. Starnbach. 1998. Anthrax toxin-mediated delivery in vivo and in vitro of a cytotoxic T-lymphocyte epitope from ovalbumin. Infect. Immun. 66:615-619.
9. Blaustein, R. O., T. M. Koehler, R. J. Collier, and A. Finkelstein. 1989. Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers. Proc. Natl. Acad. Sci. USA 86:2209-2213.
10. Bradley, K. A., J. Mogridge, M. Mourez, R. J. Collier, and J. A. Young. 2001. Identification of the cellular receptor for anthrax toxin. Nature 414:225-229.
11. Doling, A. M., J. D. Ballard, H. Shen, K. M. Krishna, R. Ahmed, R. J. Collier, and M. N. Starnbach. 1999. Cytotoxic T-lymphocyte epitopes fused to anthrax toxin induce protective antiviral immunity. Infect. Immun. 67: 3290-3296.
12. Goletz, T. J., K. R. Klimpel, N. Arora, S. H. Leppla, J. M. Keith, and J. A. Berzofsky. 1997. Targeting HIV proteins to the major histocompatibility complex class I processing pathway with a novel gp120-anthrax toxin fusion protein. Proc. Natl. Acad. Sci. USA 94:12059-12064.
13. Guermonprez, P., J. Valladeau, L. Zitvogel, C. Thery, and S. Amigorena. 2002. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20:621-667.
14. + T cell response. Immunity 25:19-29.
15. + T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18:275-308.
16. + memory T cell subsets. Proc. Natl. Acad. Sci. USA 101:5610-5615.
17. + central memory T cells into protective Listeria-specific effector memory T cells. Eur. J. Immunol. 36:1453-1464.
18. Huster, K. M., C. Stemberger, and D. H. Busch. 2006. Protective immunity towards intracellular pathogens. Curr. Opin. Immunol. 18:458-464.
19. Jabbari, A., and J. T. Harty. 2006. The generation and modulation of antigen-specific memory CD8 T cell responses. J. Leukoc. Biol. 80:16-23.
20. + T cells are more protective but slower to acquire a central-memory phenotype. J. Exp. Med. 203:919-932.
21. 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.
22. 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.
23. 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.
24. Koehler, T. M., and R. J. Collier. 1991. Anthrax toxin protective antigen: low-pH-induced hydrophobicity and channel formation in liposomes. Mol. Microbiol. 5:1501-1506.
25. + memory T lymphocyte precursors following peptide immunization. J. Immunol. 175:4400-4407.
26. Lu, Y., R. Friedman, N. Kushner, A. Doling, L. Thomas, N. Touzjian, M. Starnbach, and J. Lieberman. 2000. Genetically modified anthrax lethal toxin safely delivers whole HIV protein antigens into the cytosol to induce T cell immunity. Proc. Natl. Acad. Sci. USA 97:8027-8032.
27. Masopust, D., S. J. Ha, V. Vezys, and R. Ahmed. 2006. Stimulation history dictates memory CD8 T cell phenotype: implications for prime-boost vaccination. J. Immunol. 177:831-839.
28. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrancois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417.
29. McEvers, K., M. Elrefaei, P. Norris, S. Deeks, J. Martin, Y. Lu, and H. Cao. 2005. Modified anthrax fusion proteins deliver HIV antigens through MHC class I and II pathways. Vaccine 23:4128-4135.
30. Milne, J. C., and R. J. Collier. 1993. pH-dependent permeabilization of the plasma membrane of mammalian cells by anthrax protective antigen. Mol. Microbiol. 10:647-653.
31. Milne, J. C., D. Furlong, P. C. Hanna, J. S. Wall, and R. J. Collier. 1994. Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J. Biol. Chem. 269:20607-20612.
32. Mogridge, J., K. Cunningham, and R. J. Collier. 2002. Stoichiometry of anthrax toxin complexes. Biochemistry 41:1079-1082.
33. Mourez, M. 2004. Anthrax toxins. Rev. Physiol. Biochem. Pharmacol. 152: 135-164.
34. Pamer, E., and P. Cresswell. 1998. Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323-358.
35. 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.
36. 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.
37. Schluns, K. S., and L. Lefrancois. 2003. Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 3:269-279.
38. Scobie, H. M., G. J. Rainey, K. A. Bradley, and J. A. Young. 2003. Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc. Natl. Acad. Sci. USA 100:5170-5174.
39. Seder, R. A., and A. V. Hill. 2000. Vaccines against intracellular infections requiring cellular immunity. Nature 406:793-798.
40. 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.
41. Simsova, M., P. Sebo, and C. Leclerc. 2004. The adenylate cyclase toxin from Bordetella pertussis - a novel promising vehicle for antigen delivery to dendritic cells. Int. J. Med. Microbiol. 293:571-576.
42. 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.
43. + T cells. J. Exp. Med. 199:925-936.
44. Woodland, D. L. 2004. Jump-starting the immune system: prime-boosting comes of age. Trends Immunol. 25:98-104.