1887

Abstract

Virus-specific cytotoxic T lymphocytes (CTLs) are considered to be important in protection against and recovery from viral infections. In this study, several approaches to induce cytotoxicity against bovine herpesvirus 1 (BHV-1) were evaluated. Vaccination of C57BL/6 mice with BHV-1 induced a strong humoral, but no CTL, response, which may be due to downregulation of major histocompatibility complex class I molecules. In contrast, vaccinia virus expressing glycoprotein B (gB) elicited a weaker antibody response, but strong cytotoxicity, in mice. As an approach to inducing both strong humoral and cellular immune responses, a plasmid vector was then used to express gB. Both antibody and CTL responses were induced by the plasmid encoding gB in C57BL/6 and C3H mice, regardless of the type of vector backbone. This demonstrated that DNA immunization induces a broad-based immune response to BHV-1 gB. Interestingly, removal of the membrane anchor, which resulted in secretion of gB from transfected cells, did not result in reduced cytotoxicity. Here, it is shown that, compared with the cell-associated counterpart, plasmid-encoded secreted protein may induce enhanced immune responses in cattle. Therefore, calves were immunized intradermally with pMASIAtgB, a plasmid encoding the secreted form of gB (tgB), using a needle-free injection system. This demonstrated that pMASIAtgB elicited both humoral responses and activated gamma interferon-secreting CD8 CTLs, suggesting that a DNA vaccine expressing tgB induces a CTL response in the natural host of BHV-1.

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2005-04-01
2024-10-08
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References

  1. Baca-Estrada M. E., Snider M., Tikoo S. K., Harland R., Babiuk L. A., van Drunen Littel-van den Hurk S. 1996; Immunogenicity of bovine herpesvirus 1 glycoprotein D in mice: effect of antigen form on the induction of cellular and humoral immune responses. Viral Immunol 9:11–22 [CrossRef]
    [Google Scholar]
  2. Badovinac V. P., Harty J. T. 2000; Intracellular staining for TNF and IFN- γ detects different frequencies of antigen-specific CD8+ T cells. J Immunol Methods 238:107–117 [CrossRef]
    [Google Scholar]
  3. Bangham C. R. M., McMichael A. J. 1990; HIV infection. Why the long latent period?. Nature 348:388 [CrossRef]
    [Google Scholar]
  4. Bevan M. J. 1989; Immunology. Stimulating killer cells. Nature 342:478–479 [CrossRef]
    [Google Scholar]
  5. Braun R., Babiuk L. A., van Drunen Littel-van den Hurk S. 1997; Enhanced immune response to an intradermally delivered DNA vaccine expressing a secreted form of BHV-1 gD. Vaccine Res 6:151–164
    [Google Scholar]
  6. Butz E. A., Bevan M. J. 1998; Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 8:167–175 [CrossRef]
    [Google Scholar]
  7. Byrne K. M., Horohov D. W., Kousoulas K. G. 1995; Glycoprotein B of bovine herpesvirus-1 binds heparin. Virology 209:230–235 [CrossRef]
    [Google Scholar]
  8. Chan S. S. M., McConnell I., Blacklaws B. A. 2002; Generation and characterization of ovine dendritic cells derived from peripheral blood monocytes. Immunology 107:366–372 [CrossRef]
    [Google Scholar]
  9. Corr M., Lee D. J., Carson D. A., Tighe H. 1996; Gene vaccination with naked plasmid DNA: mechanism of CTL priming. J Exp Med 184:1555–1560 [CrossRef]
    [Google Scholar]
  10. Deshpande M. S., Ambagala T. C., Hegde N. R., Hariharan M. J., Navaratnam M., Srikumaran S. 2002; Induction of cytotoxic T-lymphocytes specific for bovine herpesvirus-1 by DNA immunization. Vaccine 20:3744–3751 [CrossRef]
    [Google Scholar]
  11. Doe B., Selby M., Barnett S., Baenziger J., Walker C. M. 1996; Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone marrow-derived cells. Proc Natl Acad Sci U S A 93:8578–8583 [CrossRef]
    [Google Scholar]
  12. Doherty P. C. 1998; Update: the numbers game for virus-specific CD8+ T cells. Science 280:227 [CrossRef]
    [Google Scholar]
  13. Eskra L., Splitter G. A. 1997; Bovine herpesvirus-1 infects activated CD4+ lymphocytes. J Gen Virol 78:2159–2166
    [Google Scholar]
  14. Fitzpatrick D. R., Redmond M. J., Attah-Poku S. K., van Drunen Littel-van den Hurk S., Babiuk L. A., Zamb T. J. 1990; Mapping of 10 epitopes on bovine herpesvirus type 1 glycoproteins gI and gIII. Virology 176:145–157 [CrossRef]
    [Google Scholar]
  15. Franco M. A., Lefevre P., Willems P., Tosser G., Lintermanns P., Cohen J. 1994; Identification of cytotoxic T cell epitopes on the VP3 and VP6 rotavirus proteins. J Gen Virol 75:589–596 [CrossRef]
    [Google Scholar]
  16. Fu T. M., Ulmer J. B., Caulfield M. J., Deck R. R., Friedman A., Wang S., Liu X., Donnelly J. J., Liu M. A. 1997; Priming of cytotoxic T lymphocytes by DNA vaccines: requirement for professional antigen presenting cells and evidence for antigen transfer from myocytes. Mol Med 3:362–371
    [Google Scholar]
  17. Fuller A. O., Lee W.-C. 1992; Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. J Virol 66:5002–5012
    [Google Scholar]
  18. Griebel P. J., Ohmann H. B., Lawman M. J. P., Babiuk L. A. 1990; The interaction between bovine herpesvirus type 1 and activated bovine T lymphocytes. J Gen Virol 71:369–377 [CrossRef]
    [Google Scholar]
  19. Hariharan M. J., Nataraj C., Srikumaran S. 1993; Down regulation of murine MHC class I expression by bovine herpesvirus 1. Viral Immunol 6:273–284 [CrossRef]
    [Google Scholar]
  20. Iwasaki A., Stiernholm B. J., Chan A. K., Berinstein N. L., Barber B. H. 1997; Enhanced CTL responses mediated by plasmid DNA immunogens encoding costimulatory molecules and cytokines. J Immunol 158:4591–4601
    [Google Scholar]
  21. Kostense S., Ogg G. S., Manting E. H. & 8 other authors; 2001; High viral burden in the presence of major HIV-specific CD8+ T cell expansions: evidence for impaired CTL effector function. Eur J Immunol 31:677–686 [CrossRef]
    [Google Scholar]
  22. Krieg A. M., Wu T., Weeratna R., Efler S. M., Love-Homan L., Yang L., Yi A.-K., Short D., Davis H. L. 1998; Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc Natl Acad Sci U S A 95:12631–12636 [CrossRef]
    [Google Scholar]
  23. Kühn J. E., Kramer M. D., Willenbacher W., Wieland U., Lorentzen E. U., Braun R. W. 1990; Identification of herpes simplex virus type 1 glycoproteins interacting with the cell surface. J Virol 64:2491–2497
    [Google Scholar]
  24. Lewis P. J., van Drunen Littel-van den Hurk S., Babiuk L. A. 1999; Altering the cellular location of an antigen expressed by a DNA-based vaccine modulates the immune response. J Virol 73:10214–10223
    [Google Scholar]
  25. Li Y., van Drunen Littel-van den Hurk S., Liang X., Babiuk L. A. 1996; Production and characterization of bovine herpesvirus 1 glycoprotein B ectodomain derivatives in an hsp70A gene promoter-based expression system. Arch Virol 141:2019–2029 [CrossRef]
    [Google Scholar]
  26. Li Y., van Drunen Littel-van den Hurk S., Liang X., Babiuk L. A. 1997; Functional analysis of the transmembrane anchor region of bovine herpesvirus 1 glycoprotein gB. Virology 228:39–54 [CrossRef]
    [Google Scholar]
  27. Madin S. H., York C. J., McKercher D. G. 1956; Isolation of the infectious bovine rhinotracheitis virus. Science 124:721–722 [CrossRef]
    [Google Scholar]
  28. Miethke A., Keil G. M., Weiland F., Mettenleiter T. C. 1995; Unidirectional complementation between glycoprotein B homologues of pseudorabies virus and bovine herpesvirus 1 is determined by the carboxy-terminal part of the molecule. J Gen Virol 76:1623–1635 [CrossRef]
    [Google Scholar]
  29. Mikloska Z., Cunningham A. L. 1998; Herpes simplex virus type 1 glycoproteins gB, gC and gD are major targets for CD4 T-lymphocyte cytotoxicity in HLA-DR expressing human epidermal keratinocytes. J Gen Virol 79:353–361
    [Google Scholar]
  30. Misra V., Blumenthal R. M., Babiuk L. A. 1981; Proteins specified by bovine herpesvirus 1 (infectious bovine rhinotracheitis virus). J Virol 40:367–378
    [Google Scholar]
  31. Murali-Krishna K., Altman J. D., Suresh M., Sourdive D. J., Zajac A. J., Miller J. D., Slansky J., Ahmed R. 1998; Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177–187 [CrossRef]
    [Google Scholar]
  32. Nataraj C., Eidmann S., Hariharan M. J., Sur J. H., Perry G. A., Srikumaran S. 1997; Bovine herpesvirus 1 downregulates the expression of bovine MHC class I molecules. Viral Immunol 10:21–34 [CrossRef]
    [Google Scholar]
  33. Paliard X., Doe B., Selby M. J., Hartog K., Lee A. Y., Burke R. L., Walker C. M. 2001; Induction of herpes simplex virus gB-specific cytotoxic T lymphocytes in TAP1-deficient mice by genetic immunization but not HSV infection. Virology 282:56–64 [CrossRef]
    [Google Scholar]
  34. Pontarollo R. A., Babiuk L. A., Hecker R., van Drunen Littel-van den Hurk S. 2002; Augmentation of cellular immune responses to bovine herpesvirus-1 glycoprotein D by vaccination with CpG-enhanced plasmid vectors. J Gen Virol 83:2973–2981
    [Google Scholar]
  35. Raggo C., Habermehl M., Babiuk L. A., Griebel P. 2000; The in vivo effects of recombinant bovine herpesvirus-1 expressing bovine interferon- γ . J Gen Virol 81:2665–2673
    [Google Scholar]
  36. Smith P. M., Zhang Y., Jennings S. R., O'Callaghan D. J. 1998; Characterization of the cytolytic T-lymphocyte response to a candidate vaccine strain of equine herpesvirus 1 in CBA mice. J Virol 72:5366–5372
    [Google Scholar]
  37. Torres C. A., Iwasaki A., Barber B. H., Robinson H. L. 1997; Differential dependence on target site tissue for gene gun and intramuscular DNA immunizations. J Immunol 158:4529–4532
    [Google Scholar]
  38. Townsend A. R. M., Rothbard J., Gotch F. M., Bahadur G., Wraith D., McMichael A. J. 1986; The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44:959–968 [CrossRef]
    [Google Scholar]
  39. Truong M.-J., Darcissac E. C. A., Hermann E., Dewulf J., Capron A., Bahr G. M. 1999; Interleukin-16 inhibits human immunodeficiency virus type 1 entry and replication in macrophages and in dendritic cells. J Virol 73:7008–7013
    [Google Scholar]
  40. Ulmer J. B., Deck R. R., DeWitt C. M., Donnelly J. J., Liu M. A. 1996; Generation of MHC class I-restricted cytotoxic T lymphocytes by expression of a viral protein in muscle cells: antigen presentation by non-muscle cells. Immunology 89:59–67 [CrossRef]
    [Google Scholar]
  41. van Drunen Littel-van den Hurk S., van den Hurk J. V., Gilchrist J. E., Misra V., Babiuk L. A. 1984; Interactions of monoclonal antibodies and bovine herpesvirus type 1 (BHV-1) glycoproteins: characterization of their biochemical and immunological properties. Virology 135:466–479 [CrossRef]
    [Google Scholar]
  42. van Drunen Littel-van den Hurk S., van den Hurk J. V., Babiuk L. A. 1985; Topographical analysis of bovine herpesvirus type-1 glycoproteins: use of monoclonal antibodies to identify and characterize functional epitopes. Virology 144:216–227 [CrossRef]
    [Google Scholar]
  43. van Drunen Littel-van den Hurk S., Zamb T., Babiuk L. A. 1989; Synthesis, cellular location, and immunogenicity of bovine herpesvirus 1 glycoproteins gI and gIII expressed by recombinant vaccinia virus. J Virol 63:2159–2168
    [Google Scholar]
  44. van Drunen Littel-van den Hurk S., Gifford G. A., Babiuk L. A. 1990; Epitope specificity of the protective immune response induced by individual bovine herpesvirus-1 glycoproteins. Vaccine 8:358–368 [CrossRef]
    [Google Scholar]
  45. van Drunen Littel-van den Hurk S., Braun R. P., Lewis P. J., Karvonen B. C., Baca-Estrada M. E., Snider M., McCartney D., Watts T., Babiuk L. A. 1998; Intradermal immunization with a bovine herpesvirus-1 DNA vaccine induces protective immunity in cattle. J Gen Virol 79:831–839
    [Google Scholar]
  46. Vasilakos J. P., Michael J. G. 1993; Herpes simplex virus class I-restricted peptide induces cytotoxic T lymphocytes in vivo independent of CD4+ T cells. J Immunol 150:2346–2355
    [Google Scholar]
  47. Whetstone C. A., Miller J. M., Seal B. S., Bello L. J., Lawrence W. C. 1992; Latency and reactivation of a thymidine kinase-negative bovine herpesvirus 1 deletion mutant. Arch Virol 122:207–214 [CrossRef]
    [Google Scholar]
  48. Witmer L. A., Rosenthal K. L., Graham F. L., Friedman H. M., Yee A., Johnson D. C. 1990; Cytotoxic T lymphocytes specific for herpes simplex virus (HSV) studied using adenovirus vectors expressing HSV glycoproteins. J Gen Virol 71:387–396 [CrossRef]
    [Google Scholar]
  49. Wyler R., Engels M., Schwyzer M. 1989; Infectious bovine rhinotracheitis/vulvovaginitis (BHV1). In Herpesvirus Diseases of Cattle, Horses, and Pigs pp  1–72 Edited by Wittmann G. Boston: Kluwer;
    [Google Scholar]
  50. Yates W. D. G. 1982; A review of infectious bovine rhinotracheitis, shipping fever pneumonia and viral–bacterial synergism in respiratory disease of cattle. Can J Comp Med 46:225–263
    [Google Scholar]
  51. Zatechka D. S. Jr, Hegde N. R., Hariharan K., Srikumaran S. 1999; Identification of murine cytotoxic T-lymphocyte epitopes of bovine herpesvirus 1. Vaccine 17:686–694 [CrossRef]
    [Google Scholar]
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