Protection against lethal vaccinia virus challenge in HLA-A2 transgenic mice by immunization with a single CD8+ T-cell peptide epitope of vaccinia and variola viruses

Journal of Virology

Volumn 78, Issue 13, 2004, Pages 7052-7060

  Snyder, James T ^a   Belyakov, Igor M ^a   Dzutsev, Amiran ^a   Lemonnier, François ^b   Berzofsky, Jay A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A2 ANTIGEN; PEPTIDE; VIRUS VACCINE;

ANIMAL MODEL; ANTIGEN BINDING; ARTICLE; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN; IMMUNIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; POXVIRUS; POXVIRUS INFECTION; PRIORITY JOURNAL; SMALLPOX; SMALLPOX VIRUS; SPLEEN CELL; T LYMPHOCYTE; TRANSGENIC MOUSE; VACCINIA VIRUS; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; EPITOPES, T-LYMPHOCYTE; HLA-A2 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDES; SMALLPOX; SMALLPOX VACCINE; VACCINATION; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 2942652411     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.13.7052-7060.2004     Document Type: Article

References (61)

1. Ahlers, J. D., I. M. Belyakov, and J. A. Berzofsky. 2003. Cytokine, chemokine and costimulatory molecule modulation to enhance efficacy of HIV vaccines. Curr. Mol. Med. 3:285-301.
2. Ahlers, J. D., I. M. Belyakov, S. Matsui, and J. A. Berzofsky. 2001. Mechanisms of cytokine synergy essential for vaccine protection against viral challenge. Int. Immunol. 13:897-908.
3. Ahlers, J. D., I. M. Belyakov, E. K. Thomas, and J. A. Berzofsky. 2001. High affinity T-helper epitope induces complementary helper and APC polarization, increased CTL and protection against viral infection. J. Clin. Investig. 108:1677-1685.
4. Ahlers, J. D., N. Dunlop, D. W. Alling, P. L. Nara, and J. A. Berzofsky. 1997. Cytokine-in-adjuvant steering of the immune response phenotype to HIV-1 vaccine constructs: GM-CSF and TNFα synergize with IL-12 to enhance induction of CTL. J. Immunol. 158:3947-3958.
5. Antoine, G., F. Scheiflinger, F. Dorner, and F. G. Falkner. 1998. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365-396.
6. + cytotoxic T lymphocytes for resistance to mucosalviral transmission in mice and enhancement of resistance by local administration of IL-12. J. Clin. Investig. 102:2072-2081.
7. Belyakov, I. M., and J. A. Berzofsky. 2004. Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 20:247-253.
8. Belyakov, I. M., M. A. Derby, J. D. Ahlers, B. L. Kelsall, P. Earl, B. Moss, W. Strober, and J. A. Berzofsky. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl. Acad. Sci. USA 95:1709-1714.
9. Belyakov, I. M., P. Earl, A. Dzutsev, V. A. Kuznetsov, M. Lemon, L. S. Wyatt, J. T. Snyder, J. D. Ahlers, G. Franchini, B. Moss, and J. A. Berzofsky. 2003. Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc. Natl. Acad. Sci. USA 100:9458-9463.
10. Belyakov, I. M., S. A. Hammond, J. D. Ahlers, G. M. Glenn, and J. A. Berzofsky. 2004. Transcutaneous immunization induces mucosal CTL and protective immunity by migration of primed skin dendritic cells. J. Clin. Investig. 113:998-1007.
11. Belyakov, I. M., Z. Hel, B. Kelsall, V. A. Kuznetsov, J. D. Ahlers, J. Nacsa, D. Watkins, T. M. Allen, A. Sette, J. Altman, R. Woodward, P. Markham, J. D. Clements, G. Franchini, W. Strober, and J. A. Berzofsky. 2001. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat. Med. 7:1320-1326.
12. Belyakov, I. M., B. Moss, W. Strober, and J. A. Berzofsky. 1999. Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity. Proc. Natl. Acad. Sci. USA 96:4512-4517.
13. Belyakov, I. M., J. Wang, R. Koka, J. D. Ahlers, J. T. Snyder, R. Tse, J. Cox, J. S. Gibbs, D. H. Margulies, and J. A. Berzofsky. 2001. Activating CTL precursors to reveal CTL function without skewing the repertoire by in vitro expansion. Eur. J. Immunol. 31:3557-3566.
14. Berzofsky, J. A., J. D. Ahlers, and I. M. Belyakov. 2001. Strategies for designing and optimizing new generation vaccines. Nat. Rev. Immunol. 1:209-219.
15. Berzofsky, J. A., J. D. Ahlers, M. A. Derby, C. D. Pendleton, T. Arichi, and I. M. Belyakov. 1999. Approaches to improve engineered vaccines for human immunodeficiency virus (HIV) and other viruses that cause chronic infections. Immunol. Rev. 170:151-172.
16. Chakrabarti, S., K. Brechling, and B. Moss. 1985. Vaccinia virus expression vector: coexpression of β-galactosidase provides visual screening of recombinant virus plaques. Mol. Cell. Biol. 5:3403-3409.
17. Colella, T. A., T. N. Bullock, L. B. Russell, D. W. Mullins, W. W. Overwijk, C. J. Luckey, R. A. Pierce, N. P. Restifo, and V. H. Engelhard. 2000. Self-tolerance to the murine homologue of a tyrosinase-derived melanoma antigen. Implications for tumor immunotherapy. J. Exp. Med. 191:1221-1232.
18. Drexler, I., C. Staib, W. Kastenmuller, S. Stevanovic, B. Schmidt, F. A. Lemonnier, H. G. Rammensee, D. H. Busch, H. Bernhard, V. Erfle, and G. Sutter. 2003. Identification of vaccinia virus epitope-specific HLA-A*0201- restricted T cells and comparative analysis of smallpox vaccines. Proc. Natl. Acad. Sci. USA 100:217-222.
19. Enghill-Smith, Y., D. Venzon, T. Karpova, J. McNally, J. Nacsa, W.-P. Tsai, E. Tryniszewska, M. Moniuszko, S. J. Snodgrass, J. Parrish, M. G. Lewis, J. A. Berzofsky, I. M. Belyakov, B. Moss, J. Tartaglia, M. Bray, V. Hirsh, H. Golding, and G. Franchini. 2003. Modeling a safer smallpox-vaccination regimen, for human immunodeficiency virus type 1-infected patients, in immunocompromised macaques. J. Infect. Dis. 188:1181-1191.
20. Enserink, M. 2003. Infectious diseases. U. S. monkeypox outbreak traced to Wisconsin pet dealer. Science 300:1639.
21. Firat, H., S. Tourdot, A. Ureta-Vidal, A. Scardino, A. Suhrbier, F. Buseyne, Y. Riviere, O. Danos, M. L. Michel, K. Kosmatopoulos, and F. A. Lemonnier. 2001. Design of a polyepitope construct for the induction of HLA-A0201-restricted HIV 1-specific CTL responses using HLA-A*0201 transgenic, H-2 class I KO mice. Eur. J. Immunol. 31:3064-3074.
22. Gardner, I., N. A. Bowern, and R. V. Blanden. 1974. Cell-mediated cytotoxicity against ectromelia virus-infected target cells. I. Specificity and kinetics. Eur. J. Immunol. 4:63-67.
23. Goebel, S. J., G. P. Johnson, M. E. Perkus, S. W. Davis, J. P. Winslow, and E. Paoletti. 1990. The complete DNA sequence of vaccinia virus. Virology 179:247-266, 517-563.
24. Guidotti, L. G., T. Ishikawa, M. V. Hobbs, B. Matzke, R. Schreiber, and F. V. Chisari. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4:25-36.
25. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. J. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9:1131-1137.
26. Harris, N., R. M. Buller, and G. Karupiah. 1995. Gamma interferon-induced, nitric oxide-mediated inhibition of vaccinia virus replication. J. Virol. 69:910-915.
27. Kägi, D., B. Ledermann, K. Bürki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. 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.
28. Kees, U., and R. V. Blanden. 1976. A single genetic element in H-2K affects mouse T-cell antiviral function in poxvirus infection. J. Exp. Med. 143:450-455.
29. Koszinowski, U., and H. Ertl. 1975. Lysis mediated by T cells and restricted by H-2 antigen of target cells infected with vaccinia virus. Nature 255:552-554.
30. Koszinowski, U., and R. Thomssen. 1975. Target cell-dependent T cell-mediated lysis of vaccinia virus-infected cells. Eur. J. Immunol. 5:245-251.
31. Kotwal, G. J., and B. Moss. 1988. Analysis of a large cluster of nonessential genes deleted from a vaccinia virus terminal transposition mutant. Virology 167:524-537.
32. Lane, H. C., J. L. Montagne, and A. S. Fauci. 2001. Bioterrorism: a clear and present danger. Nat. Med. 7:1271-1273.
33. Lane, J. M., F. L. Ruben, J. M. Neff, and J. D. Millar. 1969. Complications of smallpox vaccination, 1968. N. Engl. J. Med. 281:1201-1208.
34. Larkin, M. 2003. Monkeypox spreads as US public-health system plays catch-up. Lancet Infect. Dis. 3:461.
35. Manischewitz, J., L. R. King, N. A. Bleckwenn, J. Shiloach, R. Taffs, M. Merchlinsky, N. Eller, M. G. Mikolajczyk, D. J. Clanton, T. Monath, R. A. Weltzin, D. E. Scott, and H. Golding. 2003. Development of a novel vaccinia-neutralization assay based on reporter-gene expression. J. Infect. Dis. 188:440-448.
36. Mayr, A., V. Hochstein-Mintzel, and H. Stickl. 1987. Origin, properties and use of the attenuated vaccinia strain MVA. Z. Klin. Ther. Infekt. 3:6-14.
37. Mayr, A., H. Stickl, H. K. Muller, K. Danner, and H. Singer. 1978. The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism. Zentbl. Bakteriol. Hyg. Abt 1 Orig. B 167:373-390.
38. Newberg, M. H., D. H. Smith, S. B. Haertel, D. R. Vining, E. Lacy, and V. H. Engelhard. 1996. Importance of MHC class 1 α2 and α3 domains in the recognition of self and non-self MHC molecules. J. Immunol. 156:2473-2480.
39. Nijman, H. W., J. G. A. Houbiers, M. P. M. Vierboom, S. H. van der Burg, J. W. Drijfhout, J. D'Amaro, P. Kenemans, C. J. M. Melief, and W. M. Kast. 1993. Identification of peptide sequences that potentially trigger HLA-A2.1-restricted cytotoxic T lymphocytes. Eur. J. Immunol. 23:1215-1219.
40. Oguiura, N., D. Spehner, and R. Drillien. 1993. Detection of a protein encoded by the vaccinia virus C7L open reading frame and study of its effect on virus multiplication in different cell lines. J. Gen. Virol. 74:1409-1413.
41. Oh, S., J. A. Berzofsky, D. S. Burke, T. A. Waldmann, and L. P. Perera. 2003. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc. Natl. Acad. Sci. USA 100:3392-3397.
42. Okazaki, T., D. C. Pendleton, F. Lemonnier, and J. A. Berzofsky. 2003. Epitope-enhanced conserved HIV-1 peptide protects HLA-A2-transgenic mice against virus expressing HIV-1 antigen. J. Immunol. 171:2548-2555.
43. Parker, K. C., M. A. Bednarek, and J. E. Coligan. 1994. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152:163-175.
44. Parker, K. C., M. A. Bednarek, L. K. Hull, U. Utz, B. Cunningham, H. J. Zweerink, W. E. Biddison, and J. E. Coligan. 1992. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J. Immunol. 149:3580-3587.
45. + T lymphocytes from B2 microglobulin (B2m) HLA-A2.1 monochain transgenic H-2Db B2m double knockout mice. J. Exp. Med. 185:2043-2051.
46. Perkus, M. E., S. J. Goebel, S. W. Davis, G. P. Johnson, K. Limbach, E. K. Norton, and E. Paoletti. 1990. Vaccinia virus host range genes. Virology 179:276-286.
47. Pogue, R. R., J. Eron, J. A. Frelinger, and M. Matsui. 1995. Amino-terminal alteration of the HLA-A*0201-restricted human immunodeficiency virus pol peptide increases complex stability and in vitro immunogenicity. Proc. Natl. Acad. Sci. USA 92:8166-8170.
48. Rosenberg, S. A., J. C. Yang, D. J. Schwartzentruber, P. Hwu, F. M. Marincola, S. L. Topalian, N. P. Restifo, M. E. Dudley, S. L. Schwartz, P. J. Spiess, J. R. Wunderlich, M. R. Parkhurst, Y. Kawakami, C. A. Seipp, J. H. Einhorn, and D. E. White. 1998. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 4:321-327.
49. Rosenthal, S. R., M. Merchlinsky, C. Kleppinger, and K. L. Goldenthal. 2001. Developing new smallpox vaccines. Emerg. Infect. Dis. 7:920-926.
50. Salazar, E., S. Zaremba, P. M. Arlen, K. Y. Tsang, and J. Schlom. 2000. Agonist peptide from a cytotoxic T-lymphocyte epitope of human carcinoembryonic antigen stimulates production of Tcl-type cytokines and increases tyrosine phosphorylation more efficiently than cognate peptide. Int. J. Cancer 85:829-838.
51. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21:235-246.
52. Sarobe, P., C. D. Pendleton, T. Akatsuka, D. Lau, V. H. Engelhard, S. M. Feinstone, and J. A. Berzofsky. 1998. Enhanced in vitro potency and in vivo immunogenicity of a CTL epitope from hepatitis C virus core protein following amino acid replacement at secondary HLA-A2.1 binding positions. J. Clin. Investig. 102:1239-1248.
53. Spies, T., and R. DeMars. 1991. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351:323-324.
54. Stephenson, J. 2003. Monkeypox outbreak a reminder of emerging infections vulnerabilities. JAMA 290:23-24.
55. Sutter, G., and B. Moss. 1992. Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc. Natl. Acad. Sci. USA 89:10847-10851.
56. Sutter, G., and B. Moss. 1995. Novel vaccinia vector derived from the host range restricted and highly attenuated MVA strain of vaccinia virus. Dev. Biol. Stand. 84:195-200.
57. Tartaglia, J., M. E. Perkus, J. Taylor, E. K. Norton, J. C. Audonnet, W. I. Cox, S. W. Davis, J. van der Hoeven, B. Meignier, M. Riviere, et al. 1992. NYVAC: a highly attenuated strain of vaccinia virus. Virology 188:217-232.
58. + T cell responses to newly identified HLA-A*0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J. Exp. Med. 197:927-932.
59. + subjects. Cytometry 39:189-194.
60. Vitiello, A., D. Marchesini, J. Furze, L. A. Sherman, and R. W. Chesnut. 1991. Analysis of the HLA-restricted influenza-specific cytotoxic T lymphocyte response in transgenic mice carrying a chimeric human-mouse class I major histocompatibility complex. J. Exp. Med. 173:1007-1015.
61. Weltzin, R., J. Liu, K. V. Pugachev, G. A. Myers, B. Coughlin, P. S. Blum, R. Nichols, C. Johnson, J. Cruz, J. S. Kennedy, F. A. Ennis, and T. P. Monath. 2003. Clonal vaccinia virus grown in cell culture as a new smallpox vaccine. Nat. Med. 9:1125-1130.