Baculovirus-infected insect cells expressing peptide-MHC complexes elicit protective antitumor immunity

Journal of Immunology

Volumn 180, Issue 1, 2008, Pages 188-197

  Jordan, Kimberly R ^a   McMahan, Rachel H ^a   Oh, Jason Z ^a   Pipeling, Matthew R ^b   Pardoll, Drew M ^b   Kedl, Ross M ^a   Kappler, John W ^a,c,d   Slansky, Jill E ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BACULOVIRUS VECTOR; CANCER VACCINE; GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE 15; PEPTIDE 39; PEPTIDE AH1; PEPTIDE BETA GALACTOSIDASE; PEPTIDE WMF; UNCLASSIFIED DRUG; H2 ANTIGEN; HISTOCOMPATIBILITY ANTIGEN H 2D(B); HISTOCOMPATIBILITY ANTIGEN H-2D(B); PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; COLON CARCINOMA; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; DRUG EFFICACY; FEMALE; INSECT CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR IMMUNITY; VACCINATION; ANIMAL; BACULOVIRUS; CYTOLOGY; GENETICS; IMMUNOLOGY; INSECT; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NEOPLASM; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; ANTIGENS, CD11C; BACULOVIRIDAE; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; H-2 ANTIGENS; INSECTS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, TRANSGENIC; NEOPLASMS; PEPTIDES; VACCINATION;

EID: 40449115496     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.1.188     Document Type: Article

References (53)

1. Smith, G. E., M. D. Summers, and M. J. Fraser. 1983. Production of human β interferon in insect cells infected with a baculovirus expression vector. Mol. Cell. Biol. 3: 2156-2165.
2. Buonaguro, L., M. L. Tornesello, M. Tagliamonte, R. C. Gallo, L. X. Wang, R. Kamin-Lewis, S. Abdelwahab, G. K. Lewis, and F. M. Buonaguro. 2006. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol. 80: 9134-9143.
3. He, Y., J. Li, S. Heck, S. Lustigman, and S. Jiang. 2006. Antigenic and immunogenic characterization of recombinant baculovirus-expressed severe acute respiratory syndrome coronavirus spike protein: implication for vaccine design. J. Virol. 80: 5757-5767.
4. Herniou, E. A., J. A. Olszewski, J. S. Cory, and D. R. O'Reilly. 2003. The genome sequence and evolution of baculoviruses. Annu. Rev. Entomol. 48: 211-234.
5. Altmann, F., E. Staudacher, I. B. Wilson, and L. Marz. 1999. Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj. J. 16: 109-123.
6. Grabherr, R., W. Ernst, O. Doblhoff-Dier, M. Sara, and H. Katinger. 1997. Expression of foreign proteins on the surface of Autographa californica nuclear polyhedrosis virus. BioTechniques 22: 730-735.
7. Tami, C., A. Peralta, R. Barbieri, A. Berinstein, E. Carrillo, and O. Taboga. 2004. Immunological properties of FMDV-gP64 fusion proteins expressed on SF9 cell and baculovirus surfaces. Vaccine 23: 840-845.
8. Lindley, K. M., J. L. Su, P. K. Hodges, G. B. Wisely, R. K. Bledsoe, J. P. Condreay, D. A. Winegar, J. T. Hutchins, and T. A. Kost. 2000. Production of monoclonal antibodies using recombinant baculovirus displaying gp64-fusion proteins. J. Immunol. Methods 234: 123-135.
9. Hofmann, C., V. Sandig, G. Jennings, M. Rudolph, P. Schlag, and M. Strauss. 1995. Efficient gene transfer into human hepatocytes by baculovirus vectors. Proc. Natl. Acad. Sci. USA 92: 10099-10103.
10. Carbonell, L. F., M. J. Klowden, and L. K. Miller. 1985. Baculovirus-mediated expression of bacterial genes in dipteran and mammalian cells. J. Virol. 56: 153-160.
11. Boyce, F. M., and N. L. Bucher. 1996. Baculovirus-mediated gene transfer into mammalian cells. Proc. Natl. Acad. Sci. USA 93: 2348-2352.
12. Groner, A., R. R. Granados, and J. P. Burand. 1984. Interaction of Autographa californica nuclear polyhedrosis virus with two nonpermissive cell lines. Intervirology 21: 203-209.
13. Facciabene, A., L. Aurisicchio, and N. La Monica. 2004. Baculovirus vectors elicit antigen-specific immune responses in mice. J. Virol. 78: 8663-8672.
14. Gronowski, A. M., D. M. Hilbert, K. C. Sheehan, G. Garotta, and R. D. Schreiber. 1999. Baculovirus stimulates antiviral effects in mammalian cells. J. Virol. 73: 9944-9951.
15. Hervas-Stubbs, S., P. Rueda, L. Lopez, and C. Leclerc. 2007. Insect baculoviruses strongly potentiate adaptive immune responses by inducing type I IFN. J. Immunol. 178: 2361-2369.
16. Hofmann, C., and M. Strauss. 1998. Baculovirus-mediated gene transfer in the presence of human serum or blood facilitated by inhibition of the complement system. Gene Ther. 5: 531-536.
17. Barsoum, J. 1999. Concentration of recombinant baculovirus by cation-exchange chromatography. BioTechniques 26: 834-836.
18. Bae, J. E., G. G. Schurig, and T. E. Toth. 2002. Mice immune responses to Brucella abortus heat shock proteins: use of baculovirus recombinant-expressing whole insect cells, purified Brucella abortus recombinant proteins, and a vaccinia virus recombinant as immunogens. Vet. Microbiol. 88: 189-202.
19. Kappler, J., J. White, H. Kozono, J. Clements, and P. Marrack. 1994. Binding of a soluble αβ T-cell receptor to superantigen/major histocompatibility complex ligands. Proc. Natl. Acad. Sci. USA 91: 8462-8466.
20. Kozono, H., J. White, J. Clements, P. Marrack, and J. Kappler. 1994. Production of soluble MHC class II proteins with covalently bound single peptides. Nature 369: 151-154.
21. Wang, Y., A. Rubtsov, R. Heiser, J. White, F. Crawford, P. Marrack, and J. W. Kappler. 2005. Using a baculovirus display library to identify MHC class I mimotopes. Proc. Natl. Acad. Sci. USA 102: 2476-2481.
22. Crawford, F., E. Huseby, J. White, P. Marrack, and J. W. Kappler. 2004. Mimotopes for alloreactive and conventional T cells in a peptide-MHC display library. PLoS Biol. 2: 523-533.
23. Crawford, F., K. R. Jordan, B. Stadinski, Y. Wang, E. Huseby, P. Marrack, J. E. Slansky, and J. W. Kappler. 2006. Use of baculovirus MHC/peptide display libraries to characterize T-cell receptor ligands. Immunol. Rev. 210: 156-170.
24. Purcell, A. W., J. McCluskey, and J. Rossjohn. 2007. More than one reason to rethink the use of peptides in vaccine design. Nat. Rev. Drug Discov. 6: 404-414.
25. McMahan, R. H., and J. E. Slansky. 2007. Mobilizing the low-avidity T cell repertoire to kill tumors. Semin. Cancer Biol. 17: 317-329.
26. Huang, A. Y., P. H. Gulden, A. S. Woods, M. C. Thomas, C. D. Tong, W. Wang, V. H. Engelhard, G. Pasternack, R. Cotter, D. Hunt, D. M. Pardoll, and E. M. Jaffee. 1996. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc. Natl. Acad. Sci. USA 93: 9730-9735.
27. McMahan, R. H., J. A. McWilliams, K. R. Jordan, S. W. Dow, D. B. Wilson, and J. E. Slansky. 2006. Relating TCR-peptide-MHC affinity to immunogenicity for the design of tumor vaccines. J. Clin. Invest. 116: 2543-2551.
28. Slansky, J. E., F. M. Rattis, L. F. Boyd, T. Fahmy, E. M. Jaffee, J. P. Schneck, D. H. Margulies, and D. M. Pardoll. 2000. Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. Immunity 13: 529-538.
29. Corbett, T. H., D. P. Griswold, Jr., B. J. Roberts, J. C. Peckham, and F. M. Schabel, Jr. 1977. Evaluation of single agents and combinations of chemotherapeutic agents in mouse colon carcinomas. Cancer 40: 2660-2680.
30. Kedl, R. M., B. C. Schaefer, J. W. Kappler, and P. Marrack. 2002. T cells down-modulate peptide-MHC complexes on APCs in vivo. Nat. Immunol. 3: 27-32.
31. Berg, L. J., B. Fazekas de St Groth, F. Ivars, C. C. Goodnow, S. Gilfillan, H. J. Garchon, and M. M. Davis. 1988. Expression of T-cell receptor α-chain genes in transgenic mice. Mol. Cell. Biol. 8: 5459-5469.
32. Boublik, Y., P. Di Bonito, and I. M. Jones. 1995. Eukaryotic virus display: engineering the major surface glycoprotein of the Autographa californica nuclear polyhedrosis virus (AcNPV) for the presentation of foreign proteins on the virus surface. Biotechnology 13: 1079-1084.
33. Overwijk, W. W., D. R. Surman, K. Tsung, and N. P. Restifo. 1997. Identification of a Kb-restricted CTL epitope of β-galactosidase: potential use in development of immunization protocols for "self" antigens. Methods 12: 117-123.
34. Spivak, J. L., L. S. Avedissian, J. H. Pierce, D. Williams, W. D. Hankins, and R. A. Jensen. 1996. Isolation of the full-length murine erythropoietin receptor using a baculovirus expression system. Blood 87: 926-937.
35. Springer, T. A. 1998. Immunoprecipitation. In Current Protocols in Immunology, Vol. 2. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. John Wiley & Sons, Hoboken, NJ, pp. 8.3.1- 8.3.11.
36. Andre, F., N. Chaput, N. E. Schartz, C. Flament, N. Aubert, J. Bernard, F. Lemonnier, G. Raposo, B. Escudier, D. H. Hsu, et al. 2004. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J. Immunol. 172: 2126-2136.
37. Zehn, D., and M. J. Bevan. 2006. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 25: 261-270.
38. Wang, R. F., and H. Y. Wang. 2002. Enhancement of antitumor immunity by prolonging antigen presentation on dendritic cells. Nat. Biotechnol. 20: 149-154.
39. + T cells persist in vivo following induction of peripheral tolerance. J. Immunol. 160: 4719-4729.
40. Kedl, R. M., W. A. Rees, D. A. Hildeman, B. Schaefer, T. Mitchell, J. Kappler, and P. Marrack. 2000. T cells compete for access to antigen-bearing antigen-presenting cells. J. Exp. Med. 192: 1105-1113.
41. + dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192: 1685-1696.
42. Pinilla, C., V. Rubio-Godoy, V. Dutoit, P. Guillaume, R. Simon, Y. Zhao, R. A. Houghten, J. C. Cerottini, P. Romero, and D. Valmori. 2001. Combinatorial peptide libraries as an alternative approach to the identification of ligands for tumor-reactive cytolytic T lymphocytes. Cancer Res. 61: 5153-5160.
43. Elliott, S. L., S. Pye, T. Le, L. Mateo, J. Cox, L. Macdonald, A. A. Scalzo, C. A. Forbes, and A. Suhrbier. 1999. Peptide based cytotoxic T-cell vaccines; delivery of multiple epitopes, help, memory and problems. Vaccine 17: 2009-2019.
44. Baker, B. M., S. J. Gagnon, W. E. Biddison, and D. C. Wiley. 2000. Conversion of a T cell antagonist into an agonist by repairing a defect in the TCR/peptide/ MHC interface: implications for TCR signaling. Immunity 13: 475-484.
45. + T-cell responses to the tumorspecific antigen NY-ESO-1. J. Immunother. 28: 252-257.
46. + T cells following peptide vaccination. J. Immunol. 176: 6340-6346.
47. Chen, W., J. W. Yewdell, R. L. Levine, and J. R. Bennink. 1999. 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. 189: 1757-1764.
48. Cawthon, A. G., H. Lu, and M. A. Alexander-Miller. 2001. Peptide requirement for CTL activation reflects the sensitivity to CD3 engagement: correlation with CD8αβ versus CD8αα expression. J. Immunol. 167: 2577-2584.
49. Hamad, A. R., A. Srikrishnan, P. Mirmonsef, C. P. Broeren, C. H. June, D. Pardoll, and J. P. Schneck. 2001. Lack of coreceptor allows survival of chronically stimulated double-negative α/β T cells: implications for autoimmunity. J. Exp. Med. 193: 1113-1121.
50. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
51. Sanchez, P. J., J. A. McWilliams, C. Haluszczak, H. Yagita, and R. M. Kedl. 2007. Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J. Immunol. 178: 1564-1572.
52. Santambrogio, L., A. K. Sato, G. J. Carven, S. L. Belyanskaya, J. L. Strominger, and L. J. Stern. 1999. Extracellular antigen processing and presentation by immature dendritic cells. Proc. Natl. Acad. Sci. USA 96: 15056-15061.
53. Stubbs, A. C., K. S. Martin, C. Coeshott, S. V. Skaates, D. R. Kuritzkes, D. Bellgrau, A. Franzusoff, R. C. Duke, and C. C. Wilson. 2001. Whole recombinant yeast vaccine activates dendritic cells and elicits protective cell-mediated immunity. Nat. Med. 7: 625-629.