DNA fusion gene vaccination mobilizes effective anti-leukemic cytotoxic T lymphocytes from a tolerized repertoire

European Journal of Immunology

Volumn 38, Issue 8, 2008, Pages 2118-2130

  Rice, Jason ^a   Dossett, Michelle L ^b   Öhlén, Claes ^b   Buchan, Sarah L ^a   Kendall, Timothy J ^a   Dunn, Stuart N ^a   Stevenson, Freda K ^a   Greenberg, Philip D ^b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

T cells; Tolerance; Transgenic mice models; Tumor immunology; Vaccination

Indexed keywords

DNA VACCINE; GAG PROTEIN; GAMMA INTERFERON; LEUKEMIA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TETANUS TOXIN; CANCER VACCINE; EPITOPE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; FRIEND LEUKEMIA VIRUS; FUSION GENE; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; TUMOR IMMUNOLOGY; VACCINE PRODUCTION; ANIMAL; AUTOIMMUNITY; GENE FUSION; GENETICS; IMMUNOLOGY; LIVER; METABOLISM; THYMUS; VACCINATION;

ANIMALS; ARTIFICIAL GENE FUSION; AUTOIMMUNITY; CANCER VACCINES; EPITOPES, T-LYMPHOCYTE; FRIEND MURINE LEUKEMIA VIRUS; GENE PRODUCTS, GAG; IMMUNE TOLERANCE; LEUKEMIA; LIVER; MICE; MICE, TRANSGENIC; T-LYMPHOCYTES, CYTOTOXIC; THYMUS GLAND; VACCINATION; VACCINES, DNA;

EID: 51149114868     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200838213     Document Type: Article

References (55)

1. Goldman, J. M., Gale, R. P., Horowitz, M. M., Biggs, J. C., Champlin, R. E., Gluckman, E., Hoffmann, R. G. et al., Bone marrow transplantation for chronic myelogenous leukemia in chronic phase. Increased risk for relapse associated with T-ceLl depletion. Ann. Intern. Med. 1988. 108: 806-814.
2. Gattinoni, L., Powell, D. J., Jr., Rosenberg, S. A. and Restifo, N. P., Adoptive immunotherapy for cancer: Building on success. Nat. Rev. Immunol. 2006. 6: 383-393.
3. Rosenberg, S. A., Yang, J. C. and Restifo, N. P., Cancer immmunotherapy: Moving beyond current vaccines. Nat. Med. 2004. 10: 909-915.
4. Degiovanni, G., Hainaut, P., Lahaye, T., Weynants, P. and Boon, T., Antigens recognized on a melanoma cell line by autologous cytolytic T lymphocytes are also expressed on freshly collected tumor cells. Eur. J. Immunol. 1990. 20: 1865-1868.
5. Coulie, P. G., Karanikas, V., Colau, D., Lurquin, C., Landry, C., Marchand, M., Dorval, T. et al., A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc. Natl. Acad Sci. USA 2001. 98: 10290-10295.
6. Redmond, W. L. and Sherman, L. A., Peripheral tolerance of CD8 T lymphocytes. Immunity 2005. 22: 275-284.
7. Zehn, D. and Bevan, M. J., T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 2006. 25: 261-270.
8. Kyewski, B. and Mein, L., A central role for central tolerance. Annu. Rev. Immunol. 2006. 24: 571-606.
9. Kast, W. M., Levitsky, H. and Marincola, F. M., Synopsis of the 6th Walker's City Colloquium on Cancer Vaccines and Immunotherapy. J. Transl. Med. 2004, 2: 20.
10. Stevenson, F. K., Ottensmeier, C. H., Johnson, P., Zhu, D., Buchan, S. L., McCann, K. J., Roddick, J.S. et al., DNA vaccines to attack cancer. Proc. Natl. Acad. Sci. USA 2004. 101 Suppl 2: 14646-14652.
11. Klinman, D. M., Currie, D., Gursel, I. and Verthelyi, D., Use of CpG oligodeoxynucleotides as immune adjuvants. Immunol. Rev. 2004. 199: 201-216.
12. Spies, B., Hochrein, H., Vabulas, M., Huster, K., Busch, D. H., Schmitz, F., Heit, A. and Wagner, H., Vaccination with plasmid DNA activates dendritic cells via Toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J. Immunol. 2003. 171: 5908-5912.
13. Dupuis, M., Denis-Mize, K., Woo, C., Goldbeck, C., Selby, M. J., Chen, M., Otten, G. R. et al., Distribution of DNA vaccines determines their immunogenicity after intramuscular injection in mice. J. Immunol. 2000. 165: 2850-2858.
14. Buchan, S., Gronevik, E., Mathiesen, I., King, C. A., Stevenson, F. K. and Rice, J., Electroporation as a "prime/boost" strategy for naked DNA vaccination against a tumor antigen. J. Immunol. 2005. 174: 6292-6298.
15. Gurunathan, S., Klinman, D. M. and Seder, R. A., DNA vaccines: Immunoloyy, application, and optimization. Annu. Rev. Immunol. 2000. 18: 927-974.
16. McConkey, S. J., Reece, W. H., Moorthy, V. S., Webster, D., Dunachie, S., Butcher, G., Vuola, J. M. et al., Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med. 2003. 9: 729-735.
17. Widera, G., Austin, M., Rabussay, D., Goldbeck, C., Barnett, S. W., Chen, M., Leung, L. et al., Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J. Immunol. 2000. 164: 4635-4640.
18. Babiuk, S., Baca-Estrada, M. E., Foldvari, M., Storms, M., Rabussay, D., Widera, G. and Babiuk, L. A., Electroporation improves the efficacy of DNA vaccines in large animals. Vaccine 2002. 20: 3399-3408.
19. Tacket, C. O., Roy, M. J., Widera, G., Swain, W. F., Broome, S. and Edelman, R., Phase 1 safety and immune response studies of a DNA vaccine encoding hepatitis B surface antigen delivered by a gene delivery device. Vaccine 1999. 17: 2826-2829.
20. Stevenson, F. K., Rice, J., Ottensmeier, C. H., Thirdborough, S. M. and Zhu, D., DNA fusion gene vaccines against cancer: From the laboratory to the clinic. Immunol. Rev. 2004. 199: 156-180.
21. Rice, J., Ottensmeier, C. H. and Stevenson, F. K., DNA vaccines: Precision tools for activating effective immunity against cancer. Nat. Rev. Cancer 2008. 8: 108-120.
22. Rice, J., Elliott, T., Buchan, S. and Stevenson, F. K., DNA fusion vaccine designed to induce cytotoxic T cell responses against defined peptide motifs: Implications for cancer vaccines. J. Immunol. 2001. 167: 1558-1565.
23. + T cells. J. Immunol. 2006. 177: 6626-66S3.
24. Shedlock, D.J. and Shen, H., Requirement for CD4 Tcell help in generating functional CD8 T cell memory. Science 2003, 300: 337-339.
25. Sun, J. C. and Bevan, M. J., Defective CD8 T cell memory following acute infection without: CD4 T cell help. Science 2003. 300: 339-342.
26. + T lymphocytes. Nature 2003. 421: 852-856.
27. Rice, J., Buchan, S. and Stevenson, F. K., Critical components of a DNA fusion vaccine able to induce protective cytotoxic T cells against a single epitope of a minor antigen. J. Immunol. 2002. 169: 3908-3913.
28. Rice, J., Buchan, S., Dewchand, H., Simpson, E. and Stevenson, F. K., DNA fusion vaccines induce targeted epitope-specific CTLs against minor histocompatibility antigens from a normal or tolerized repertoire. J. Immunol. 2004. 173: 4492-4499.
29. Rice, J., Dunn, S., Piper, K., Buchan, S. L., Moss, P. A. and Stevenson, F. K., DNA fusion vaccines induce epitope-specific cytotoxic CDB(+) T cells against human leukemia-associated minor histocompatibility antigens. Cancer Res. 2006. 66: 5436-5442.
30. + helper T lymphocytes recognize distinct Friend murine leukemia virus-encoded antigens. J. Exp. Med. 1989. 169: 457-467.
31. Chen, W., Qin, H., Chesebro, B. and Cheever, M. A., Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J. Virol. 1996. 70: 7773-7782.
32. + T cells or CTL immunotherapy of tumors expressing the antigen. J. Immunol. 2001. 166: 2863-2870.
33. Ohlen, C., Kalos, M., Cheng, L. E., Shur, A. C., Hong, D. J., Carson, B. D., Kokot, N. C. et al., CD8(+) T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J. Exp. Med. 2002. 195: 1407-1418.
34. Starr, T. K., Jameson, S. C. and Hogquist, K. A., Positive and negative selection of T cells. Annu. Rev. Immunol. 2003. 21: 139-176.
35. Morgan, D. J., Kreuwel, H. T., Fleck, S., Levitsky, H. I., Pardoll, D. M. and Sherman, L. A., Activation of low avidity CTL specific for a self epitope results in tumor rejection but not autoimmunity. J. Immunol. 1998. 160: 643-651.
36. + T cells in tumor-bearing mice. J. Immunol. 2005. 174: 2563-2572.
37. Kundig, T. M., Kalberer, C. P., Hengartner, H. and Zinkernagel, R. M., Vaccination with two different vaccinia recombinant viruses: Long-term inhibition of secondary vaccination. Vaccine 1993. 11: 1154-1158.
38. Bos, R., van Duikeren, S., van Hall, T., Lauwen, M. M., Parrington, M., Berinstein, N. L., McNeil, B. et al., Characterization of antigen-specific immune responses induced by canarypox virus vaccines. J. Immunol. 2007. 179: 6115-6122.
39. Smith, C. L., Mirza, F., Pasquetto, V., Tscharke, D. C., Palmowski, M. J., Dunbar, P. R., Sette, A. et al., Immunodominance of poxviral-specific CTL in a human trial of recombinant-modified vaccinia Ankara. J. Immunol. 2005. 175: 8431-8437.
40. + T cells for use in adoptive immunotherapy of established tumors. Nat. Med. 2006. 12: 335-341.
41. Ossendorp, F., Mengede, E., Camps, M., Filius, R. and Melief, C. J., Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J. Exp. Med. 1998. 187: 693-702.
42. Heiser, A., Maurice, M. A., Yancey, D. R., Wu, N. Z., Dahm, P., Pruitt, S. K., Boczkowski, D. et al., Induction of polyclonal prostate cancer-specific CTL using dendritic cells transfected with amplified tumor RNA. J. Immunol. 2001. 166: 2953-2960.
43. + T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl. Acad. Sci. USA 2002. 99: 16168-16173.
44. Palmowski, M. J., Choi, E. M., Hermans, I. F., Gilbert, S. C., Chen, J. L., Gileadi, U., Salio, M. et al., Competition between CTL narrows the immune response induced by prime-boost vaccination protocols. J. Immunol. 2002. 168: 4391-4398.
45. Yewdell, J. W. and Bennink, J. R., Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 1999. 17: 51-88.
46. + T-cell-based cancer vaccines. Adv. Cancer Res. 2006. 95: 203-247.
47. Limmer, A., Sacher, T., Alferink, J., Kretschmar, M., Schonrich, G., Nichterlein, T., Arnold, B. and Hammerling, G. J., Failure to induce organ-specific autoimmunity by breaking of tolerance: Importance of the microenvironment. Eur. J. Immunol. 1998. 28: 2395-2406.
48. + T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J. Immunol. 2000. 165: 6047-6055.
49. Lang, K. S., Georgiev, P., Recher, M., Navarini, A. A., Bergthaler, A., Heikenwalder,M., Harris, N. L. et al., Immunoprivileged status of the liver is controlled by Toll-like receptor 3 signaling. J. Clin. Invest. 2006. 116: 2456-2463.
50. - T cells. Tumor eradication does not require participation of cytotoxic T cells. J. Exp. Med. 1985. 161: 1122-1134.
51. Panina-Bordignon, P., Tan, A., Termijtelen, A., Demotz, S., Corradin, G. and Lanzavecchia, A., Universally immunogenic T cell epitopes: Promiscuous binding to human MHC class II and promiscuous recognition by T cells. Eur. J. Immunol. 1989. 19: 2237-2242.
52. b epitope is encoded by a novel mouse Y chromosome gene. Nat. Genet. 1996. 14: 474-478.
53. Chen, W., Yewdell, J. W., Levine, R. L. and Bennink, J. R., Modification of cysteine residues in vitro and in vivo affects the immunogenicity and antigenicity of major histocompatibility complex class I-restricted viral determinants. J. Exp. Med. 1999. 189: 1757-1764.
54. Berlioz, C. and Darlix, J. L., An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. J. Virol. 1995. 69: 2214-2222.
55. Prats, A. C., De Billy, G., Wang, P. and Darlix, J. L., CUG initiation codon used for the synthesis of a cell surface antigen coded by the murine leukemia virus. J. Mol. Biol. 1989. 205: 363-372.