Vaccination with an adenoviral vector encoding the tumor antigen directly linked to invariant chain induces potent CD4+ T-cell-independent CD8+ T-cell-mediated tumor control

European Journal of Immunology

Volumn 39, Issue 10, 2009, Pages 2725-2736

  Sorensen, Maria R ^a   Holst, Peter J ^a   Pircher, Hanspeter ^b   Christensen, Jan P ^a   Thomsen, Allan R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Animal models; Recombinant viral vectors; T cells; Tumor immunology; Vaccination

Indexed keywords

ADENOVIRUS VECTOR; GAMMA INTERFERON; GLYCOPROTEIN; GLYCOPROTEIN 33; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CONTROL; CANCER IMMUNIZATION; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; FLOW CYTOMETRY; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; TRANSGENIC MOUSE; TREATMENT DURATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ADENOVIRIDAE; ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; ANTIGENS, NEOPLASM; ANTIGENS, VIRAL; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL CYCLE; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; GENES, MHC CLASS II; GENETIC VECTORS; GLYCOPROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; LYMPHOCYTIC CHORIOMENINGITIS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; SPLEEN; SURVIVAL ANALYSIS; VACCINES, DNA; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 70350521454     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939543     Document Type: Article

References (40)

1. Bonnet, M. C., Tartaglia, J., Verdier, F., Kourilsky, P., Lindberg, A., Klein, M. and Moingeon, P., Recombinant viruses as a tool for therapeutic vaccination against human cancers. Immunol. Lett. 2000. 74: 11-25.
2. Gajewski, T. F., Meng, Y., Blank, C., Brown, I., Kacha, A., Kline, J. and Harlin, H., Immune resistance orchestrated by the tumor microenvironment. Immunol. Rev. 2006. 213: 131-145.
3. Gajewski, T. F., Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment. Clin. Cancer Res. 2006. 12: 2326S-2330S.
4. Boissonnas, A., Fetler, L., Zeelenberg, I. S., Hugues, S. and Amigorena, S., In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 2007. 204: 345-356.
5. Blohm, U., Potthoff, D., van der Kogel, A. J. and Pircher, A., Solid tumors "melt" from the inside after successful CD8 T cell attack. Eur. J. Immunol. 2006. 36: 468-477.
6. Russell, J. H. and Ley, T. J., Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 2002. 20: 323-370.
7. Kagi, D., Ledermann, B., Burki, K., Zinkernagel, R. M. and Hengartner, H., Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 1996. 14: 207-232.
8. Harrop, R., John, J. and Carroll, M. W., Recombinant viral vectors: Cancer vaccines. Adv. Drug Deliv. Rev. 2006. 58: 931-947.
9. Muruve, D. A., Cotter, M. J., Zaiss, A. K., White, L. R., Liu, Q., Chan, T., Clark, S. A. et al., Helper-Dependent Adenovirus Vectors Elicit Intact Innate but Attenuated Adaptive Host Immune Responses In Vivo. J. Virol. 2004. 78: 5966-5972. (Pubitemid 38661684)
10. Holst, P. J., Sorensen, M. R., Mandrup Jensen, C. M., Orskov, C., Thomsen, A. R. and Christensen, J. P., MHC class II-associated invariant chain linkage of antigen dramatically improves cell-mediated immunity induced by adenovirus vaccines. J. Immunol. 2008. 180: 3339-3346.
11. Holst, P. J., Augmentation of adenovirus induced immune responses. Copenhagen, University of Copenhagen. Thesis/Dissertation. 2008.
12. + T-cell responses. J. Virol. 2008. 82: 11734-11741.
13. Prevost-Blondel, A., Zimmermann, C., Stemmer, C., Kulmburg, P., Rosenthal, F. M. and Pircher, H., Tumor-infiltrating lymphocytes exhibiting high ex vivo cytolytic activity fail to prevent murine melanoma tumor growth in vivo. J. Immunol. 1998. 161: 2187-2194. (Pubitemid 28397028)
14. + T cells from Class II MHC-deficient mice in contact hypersensitivity responses. J. Leukoc. Biol. 2007. 82: 85-92.
15. Hermans, I. F., Silk, J. D., Yang, J., Palmowski, M. J., Gileadi, U., McCarthy, C., Salio, M. et al., The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKT-mediated cytotoxicity against multiple targets in vitro and in vivo. J. Immunol. Methods 2004. 285: 25-40. (Pubitemid 38186583)
16. Oldstone, M. B. A., Nerenberg, M., Southern, P., Price, J. and Lewicki, H., Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: Role of anti-self (virus) immune response. Cell 1991. 65: 319-331. (Pubitemid 121006061)
17. Matter, M., Pavelic, V., Pinschewer, D. D., Mumprecht, S., Eschli, B., Giroglou, T., von, L. D. and Ochsenbein, A. F., Decreased tumor surveillance after adoptive T-cell therapy. Cancer Res. 2007. 67: 7467-7476. (Pubitemid 47206576)
18. zur Hausen, H., Viruses in human cancers. Science 1991. 254: 1167-1173.
19. Holst, P. J., Bartholdy, C., Stryhn, A., Thomsen, A. R. and Christensen, J. P., Rapid and sustained CD4(+) T-cell-independent immunity from adenovirus-encoded vaccine antigens. J. Gen. Virol. 2007. 88: 1708-1716.
20. Steitz, J., Bruck, J., Knop, J. and Tuting, T., Adenovirus-transduced dendritic cells stimulate cellular immunity to melanoma via a CD4(+) T cell-dependent mechanism. Gene Ther. 2001. 8: 1255-1263. (Pubitemid 32780814)
21. Holst, P. J., Bartholdy, C., Stryhn, A., Thomsen, A. R. and Christensen, J. P., Rapid and sustained CD4(+) T-cell-independent immunity from adenovirus-encoded vaccine antigens. J. Gen. Virol. 2007. 88: 1708-1716.
22. Kundig, T. M., Shahinian, A., Kawai, K., Mittrucker, H. W., Sebzda, E., Bachmann, M. F., Mak, T. W. and Ohashi, P. S., Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 1996. 5: 41-52. (Pubitemid 26254783)
23. Hollenbaugh, J. A. and Dutton, R. W., IFN-gamma regulates donor CD8 T cell expansion, migration, and leads to apoptosis of cells of a solid tumor. J. Immunol. 2006. 177: 3004-3011.
24. Kaplan, D. H., Shankaran, V., Dighe, A. S., Stockert, E., Aguet, M., Old, L. J. and Schreiber, R. D., Demonstration of an interferon gamma -dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA 1998. 95: 7556-7561.
25. Dobrzanski, M. J., Reome, J. B. and Dutton, R. W., Immunopotentiating role of IFN-gamma in early and late stages of Type 1 CD8 effector cell-mediated tumor rejection. Clin. Immunol. 2001. 98: 70-84.
26. Rodrigues, E. G., Garofalo, A. S. and Travassos, L. R., Endogenous accumulation of IFN-gamma in IFN-gamma-R(-/-) mice increases resistance to B16F10-Nex2 murine melanoma: a model for direct IFN-gamma anti-tumor cytotoxicity in vitro and in vivo. Cytokines Cell Mol. Ther. 2002. 7: 107-116.
27. Beatty, G. and Paterson, Y., Regulation of tumor growth by IFN in cancer immunotherapy. Immunol. Res. 2001. 24: 201-210.
28. + T Cells. Cancer Res. 2003. 63: 4095-4100.
29. Schroder, K., Hertzog, P. J., Ravasi, T. and Hume, D. A., Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004. 75: 163-189.
30. Peng, L., Krauss, J. C., Plautz, G. E., Mukai, S., Shu, S. and Cohen, P. A., T cell-mediated tumor rejection displays diverse dependence upon perforin and IFN-gamma mechanisms that cannot be predicted from in vitro T cell characteristics. J. Immunol. 2000. 165: 7116-7124. (Pubitemid 32001187)
31. Prévost-Blondel, A., Neuenhahn, M. and Pircher, H., Differential requirement of perforin and IFN- in CD8 T cell-mediated immune responses against B16.F10 melanoma cells expressing a viral antigen. Eur. J. Immunol. 2000. 30: 2507-2515.
32. Hollenbaugh, J. A., Reome, J., Dobrzanski, M. and Dutton, R. W., The rate of the CD8-dependent initial reduction in tumor volume is not limited by contact-dependent perforin, Fas ligand, or TNF-mediated cytolysis. J. Immunol. 2004. 173: 1738-1743. (Pubitemid 38971605)
33. Winter, H., Hu, H. M., Urba, W. J. and Fox, B. A., Tumor regression after adoptive transfer of effector T cells is independent of perforin or Fas ligand (APO-1L/CD95L). J. Immunol. 1999. 163: 4462-4472. (Pubitemid 29474515)
34. Sambhara, S., Switzer, I., Kurichh, A., Miranda, R., Urbanczyk, L., James, O., Underdown, B. et al., Enhanced antibody and cytokine responses to influenza viral antigens in perforin-deficient mice. Cell Immunol. 1998. 187: 13-18. (Pubitemid 28359689)
35. Calzascia, T., Pellegrini, M., Hall, H., Sabbagh, L., Ono, N., Elford, A. R., Mak, T. W. and Ohashi, P. S., TNF-alpha is critical for antitumor but not antiviral T cell immunity in mice. J. Clin. Invest 2007. 117: 3833-3845. (Pubitemid 350224093)
36. Nansen, A., Jensen, T., Christensen, J. P., Andreasen, S. O., Ropke, C., Marker, O. and Thomsen, A. R., Compromised virus control and augmented perforin-mediated immunopathology in IFN-gamma-deficient mice infected with lymphocytic choriomeningitis virus. J. Immunol. 1999. 163: 6114-6122.
37. Diebold, S. S., Cotten, M., Koch, N. and Zenke, M., MHC class II presentation of endogenously expressed antigens by transfected dendritic cells. Gene Ther. 2001. 8: 487-493. (Pubitemid 32266404)
38. Becker, T. C., Noel, R. J., Coats, W. S., Gomez-Foix, A. M., Alam, T., Gerard, R. D. and Newgard, C. B., Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods Cell Biol. 1994. 43: 161-189.
39. Janik, P., Briand, P., Hartmann, N. R. and Hansen, M., The effect of estrone-progesterone treatment on cell proliferation kinetics of hormone-dependent GR mouse mammary tumors. Cancer Res. 1975. 35: 3698-3704.
40. + T cell functionality in virus-infected mice lacking a normal B cell compartment. J. Immunol. 2003. 171: 4733-4741.