1887

Abstract

Cell-mediated immunity is thought to play a decisive role in protecting cats against feline infectious peritonitis (FIP), a progressive and lethal coronavirus disease. In view of the potential of DNA vaccines to induce cell-mediated responses, their efficacy to induce protective immunity in cats was evaluated. The membrane (M) and nucleocapsid (N) proteins were chosen as antigens, because antibodies to the spike (S) protein of FIP virus (FIPV) are known to precipitate pathogenesis. However, vaccination by repeated injections of plasmids encoding these proteins did not protect kittens against challenge infection with FIPV. Also, a prime–boost protocol failed to afford protection, with priming using plasmid DNA and boosting using recombinant vaccinia viruses expressing the same coronavirus proteins. Because of the role of IL-12 in initiating cell-mediated immunity, the effects of co-delivery of plasmids encoding the feline cytokine were studied. Again, IL-12 did not meet expectations – on the contrary, it enhanced susceptibility to FIPV challenge. This study shows that DNA vaccination failed to protect cats against FIP and that IL-12 may yield adverse effects when used as a cytokine adjuvant.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-1-1
2002-01-01
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/1/0830001a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-1-1&mimeType=html&fmt=ahah

References

  1. Addie D. D., Jarrett J. O. 1992; A study of naturally occurring coronavirus infections in kittens. Veterinary Research 130:133–137
    [Google Scholar]
  2. Barlough J. E., Stoddart C. A., Sorresso G. P., Jacobson R. H., Scott F. W. 1984; Experimental inoculation of cats with canine coronavirus and subsequent challenge with feline infectious peritonitis virus. Laboratory Animal Science 34:592–597
    [Google Scholar]
  3. Barlough J. E., Johnson-Lussenburg C. M., Stoddart C. A., Jacobson R. H., Scott F. W. 1985; Experimental inoculation of cats with human coronavirus 229E and subsequent challenge with feline infectious peritonitis virus. Canadian Journal of Comparative Medicine 49:303–307
    [Google Scholar]
  4. Boretti F. S., Leutenegger C. M., Mislin C., Hofmann-Lehmann R., Konig S., Schroff M., Junghans C., Fehr D., Huettner S. W., Habel A., Flynn J. N., Aubert A., Pedersen N. C., Wittig B., Lutz H. 2000; Protection against FIV challenge infection by genetic vaccination using minimalistic DNA constructs for FIV env gene and feline IL-12 expression. AIDS 14:1749–1757
    [Google Scholar]
  5. Chow Y. H., Chiang B. L., Lee Y. L., Chi W. K., Lin W. C., Chen Y. T., Tao M. H. 1998; Development of Th1 and Th2 populations and the nature of immune responses to hepatitis B virus DNA vaccines can be modulated by codelivery of various cytokine genes. Journal of Immunology 160:1320–1329
    [Google Scholar]
  6. Christianson K. K., Ingersoll J. D., Landon R. M., Pfeiffer N. E., Gerber J. D. 1989; Characterization of a temperature-sensitive feline infectious peritonitis coronavirus. Archives of Virology 109:185–196
    [Google Scholar]
  7. Corapi W. V., Olsen C. W., Scott F. W. 1992; Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. Journal of Virology 66:6695–6705
    [Google Scholar]
  8. Fehr D., Holznagel E., Bolla S., Hauser B., Herrewegh A. A. P. M., Horzinek M. C., Lutz H. 1997; Placebo-controlled evaluation of a modified live virus vaccine against feline infectious peritonitis: safety and efficacy under field conditions. Vaccine 15:1101–1109
    [Google Scholar]
  9. Gately M. K., Chizzonite R., Presky D. H. 1997; Measurement of human and mouse interleukin-12. In Current Protocols in Immunology pp. 6.16.1–6.16.15 Edited by Coligan J. E., Kruisbeek A. M., Margulies D. H., Shevach E. M., Strober W. Chichester: John Wiley & Sons;
    [Google Scholar]
  10. Gerber J. D. 1995; Overview of the development of a modified live temperature-sensitive FIP vaccine. Feline Practice 23:62–66
    [Google Scholar]
  11. Gerber J. D., Ingersoll J. D., Gast A. M., Christianson K. K., Selzer N. L., Landon R. M., Pfeiffer N. E., Sharpee R. L., Beckenhauer W. H. 1990; Protection against feline infectious peritonitis by intranasal inoculation of a temperature-sensitive FIPV vaccine. Vaccine 8:536–542
    [Google Scholar]
  12. Gerdts V., Jöns A., Makoschey B., Visser N., Mettenleiter T. C. 1997; Protection of pigs against Aujeszky’s disease by DNA vaccination. Journal of General Virology 78:2139–2146
    [Google Scholar]
  13. Gherardi M. M., Ramirez J. C., Esteban M. 2000; Interleukin-12 (IL-12) enhancement of the cellular immune response against human immunodeficiency virus type 1 env antigen in a DNA prime/vaccinia virus boost vaccine regimen is time and dose dependent: suppressive effects of IL-12 boost are mediated by nitric oxide. Journal of Virology 74:6278–6286
    [Google Scholar]
  14. Haagmans B. L., van Rooij E. M. A., Dubelaar M., Kimman T. G., Horzinek M. C., Schijns V. E. C. J., Bianchi A. T. J. 1999; Vaccination of pigs against pseudorabies virus with plasmid DNA encoding glycoprotein D. Vaccine 17:1264–1271
    [Google Scholar]
  15. Hamajima K., Fukushima J., Bukawa H., Kaneko T., Tsuji T., Asakura Y., Sasaki S., Xin K. Q., Okuda K. 1997; Strong augment effect of IL-12 expression plasmid on the induction of HIV-specific cytotoxic T lymphocyte activity by a peptide vaccine candidate. Clinical Immunology and Immunopathology 83:179–184
    [Google Scholar]
  16. Hanke T., Blanchard T. J., Schneider J., Hannan C. M., Becker M., Gilbert S. C., Hill A. V., Smith G. L., McMichael A. 1998; Enhancement of MHC class I-restricted peptide-specific T cell induction by a DNA prime/MVA boost vaccination regime. Vaccine 16:439–445
    [Google Scholar]
  17. Hartikka J., Sawdey M., Cornefert-Jensen F., Margalith M., Barnhart K., Nolasco M., Vahlsing H. L., Meek J., Marquet M., Hobart P., Norman J., Manthorpe M. 1996; An improved plasmid DNA expression vector for direct injection into skeletal muscle. Human Gene Therapy 7:1205–1217
    [Google Scholar]
  18. Hayashi T., Sasaki N., Ami Y., Fujiwara K. 1983; Role of thymus-dependent lymphocytes and antibodies in feline infectious peritonitis after oral infection. Japanese Journal of Veterinary Science 45:759–766
    [Google Scholar]
  19. Hohdatsu T., Yamada M., Tominaga R., Makino K., Kida K., Koyama H. 1998; Antibody-dependent enhancement of feline infectious peritonitis virus infection in feline alveolar macrophages and human monocyte cell line U937 by serum of cats experimentally or naturally infected with feline coronavirus. Journal of Veterinary Medical Science 60:49–55
    [Google Scholar]
  20. Horvath A. J., Mostowski H. S., Bloom E. T. 1996; IL-12 administered in vivo to young and aged mice. Discrepancy between the effects on tumor growth in vivo and cytotoxic T lymphocyte generation ex vivo : dependence on IFN-γ. International Immunology 8:661–673
    [Google Scholar]
  21. Kida K., Hohdatsu T., Kashimoto-Tokunaga J., Koyama H. 2000; Neutralization of feline infectious peritonitis virus: preparation of monoclonal antibody that shows cell tropism in neutralizing activity after viral absorption into the cells. Archives of Virology 145:1–12
    [Google Scholar]
  22. Kim J. J., Ayyavoo V., Bagarazzi M. L., Chattergoon M. A., Dang K., Wang B., Boyer J. D., Weiner D. B. 1997; In vivo engineering of a cellular immune response by coadministration of IL-12 expression vector with a DNA immunogen. Journal of Immunology 158:816–826
    [Google Scholar]
  23. Kontny U., Kurane I., Ennis F. A. 1988; Gamma interferon augments Fc gamma receptor-mediated dengue virus infection of human monocytic cells. Journal of Virology 62:3928–3933
    [Google Scholar]
  24. Lasarte J. J., Corrales F. J., Casares N., Lopez-Diaz de Cerio A., Qian C., Xie X., Borras-Cuesta F., Prieto J. 1999; Different doses of adenoviral vector expressing IL-12 enhance or depress the immune response to a coadministered antigen: the role of nitric oxide. Journal of Immunology 162:5270–5277
    [Google Scholar]
  25. Laviada M. D., Videgain S. P., Moreno L., Alonso F., Enjuanes L., Escribano J. M. 1990; Expression of swine transmissible gastroenteritis virus envelope antigens on the surface of infected cells: epitopes externally exposed. Virus Research 16:247–254
    [Google Scholar]
  26. Lee K., Overwijk W. W., O’Toole M., Swiniarski H., Restifo N. P., Dorner A. J., Wolf S. F., Sturmhoefel K. 2000; Dose-dependent and schedule-dependent effects of interleukin-12 on antigen-specific CD8 responses. Journal of Interferon and Cytokine Research 20:589–596
    [Google Scholar]
  27. Leutenegger C. M., Boretti F. S., Mislin C. N., Flynn J. N., Schroff M., Habel A., Junghans C., Koenig-Merediz S. A., Sigrist B., Aubert A., Pedersen N. C., Wittig B., Lutz H. 2000; Immunization of cats against feline immunodeficiency virus (FIV) infection by using minimalistic immunogenic defined gene expression vector vaccines expressing FIV gp140 alone or with feline interleukin-12 (IL-12), IL-16, or a CpG motif. Journal of Virology 74:10447–10457
    [Google Scholar]
  28. Loeffler D. G., Ott R. L., Evermann J. F., Ali R., Alexander J. E. 1978; The incidence of naturally occurring antibodies against feline infectious peritonitis in selected cat populations. Feline Practice 8:43–47
    [Google Scholar]
  29. McArdle F., Tennant B., Bennett M., Kelly D. F., Gaskell C. J., Gaskell R. M. 1995; Independent evaluation of a modified live FIPV vaccine under experimental conditions. Feline Practice 23:67–72
    [Google Scholar]
  30. Manickan E., Rouse R. J., Yu Z., Wire W. S., Rouse B. T. 1995; Genetic immunization against herpes simplex virus. Protection is mediated by CD4+ T lymphocytes. Journal of Immunology 155:259–265
    [Google Scholar]
  31. Mortola E., Endo Y., Mizuno T., Ohno K., Watari T., Tsujimoto H., Hasegawa A. 1998; Effect of interleukin-12 and interleukin-10 on the virus replication and apoptosis in T-cells infected with feline immunodeficiency virus. Journal of Veterinary Medical Science 60:1181–1185
    [Google Scholar]
  32. Okada E., Sasaki S., Ishii N., Aoki I., Yasuda T., Nishioka K., Fukushima J., Miyazaki J., Wahren B., Okuda K. R. 1997; Intranasal immunization of a DNA vaccine with IL-12- and granulocyte-macrophage colony-stimulating factor (GM-CSF)-expressing plasmids in liposomes induces strong mucosal and cell-mediated immune responses against HIV-1 antigens. Journal of Immunology 159:3638–3647
    [Google Scholar]
  33. Olsen C. W., Corapi W. V., Ngichabe C. K., Baines J. D., Scott F. W. 1992; Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. Journal of Virology 66:956–965
    [Google Scholar]
  34. Orange J. S., Wolf S. F., Biron C. A. 1994; Effects of IL-12 on the response and susceptibility to experimental viral infections. Journal of Immunology 152:1253–1264
    [Google Scholar]
  35. Pedersen N. C. 1976a; Feline infectious peritonitis: something old, something new. Feline Practice 6:42–51
    [Google Scholar]
  36. Pedersen N. C. 1976b; Serologic studies of naturally occurring feline infectious peritonitis. American Journal of Veterinary Research 37:1149–1453
    [Google Scholar]
  37. Pedersen N. C., Black J. W. 1983; Attempted immunization of cats against feline infectious peritonitis using avirulent live virus or sublethal amounts of virulent virus. American Journal of Veterinary Research 44:229–234
    [Google Scholar]
  38. Pedersen N. C., Floyd K. 1985; Experimental studies with three new strains of feline infectious peritonitis virus: FIPV-UCD2, FIPV-UCD3, and FIPV-UCD4. Compendium Continuing Education in Practical Veterinary 7:1001–1011
    [Google Scholar]
  39. Puddu P., Fantuzzi L., Borghi P., Varano B., Rainaldi G., Guillemard E., Malorni W., Nicaise P., Wolf S. F., Belardelli F., Gessani S. 1997; IL-12 induces IFN-γ expression and secretion in mouse peritoneal macrophages. Journal of Immunology 159:3490–3497
    [Google Scholar]
  40. Roman M., Martin-Orozco E., Goodman J. S., Nguyen M. D., Sato Y., Ronaghy A., Kornbluth R. S., Richman D. D., Carson D. A., Raz E. 1997; Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nature Medicine 3:849–854
    [Google Scholar]
  41. Sato Y., Roman M., Tighe H., Lee D., Corr M., Nguyen M. D., Silverman G. J., Lotz M., Carson D. A., Raz E. 1996; Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273:352–354
    [Google Scholar]
  42. Schijns V. E., Wierda C. M., Vahlenkamp T. W., Horzinek M. C. 1997; Molecular cloning of cat interleukin-12. Immunogenetics 45:462–463
    [Google Scholar]
  43. Schneider J., Gilbert S. C., Blanchard T. J., Hanke T., Robson K. J., Hannan C. M., Becker M., Sinden R., Smith G. L., Hill A. V. S. 1998; Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nature Medicine 4:397–402
    [Google Scholar]
  44. Scott F. W., Corapi W. V., Olsen C. W. 1995; Independent evaluation of a modified live FIPV vaccine under experimental conditions. Feline Practice 23:74–76
    [Google Scholar]
  45. Sin J. I., Kim J. J., Arnold R. L., Shroff K. E., McCallus D., Pachuk C., McElhiney S. P., Wolf M. W., Pompa-de Bruin S., Higgins T. J., Ciccarelli R. B., Weiner D. B. 1999a; IL-12 gene as a DNA vaccine adjuvant in a herpes mouse model: IL-12 enhances Th1-type CD4+ T cell-mediated protective immunity against herpes simplex virus-2 challenge. Journal of Immunology 162:2912–2921
    [Google Scholar]
  46. Sin J. I., Kim J. J., Boyer J. D., Ciccarelli R. B., Higgins T. J., Weiner D. B. 1999b; In vivo modulation of vaccine-induced immune responses toward a Th1 phenotype increases potency and vaccine effectiveness in a herpes simplex virus type 2 mouse model. Journal of Virology 73:501–509
    [Google Scholar]
  47. Stoddart C. A., Barlough J. E., Baldwin C. A., Scott F. W. 1988; Attempted immunisation of cats against feline infectious peritonitis using canine coronavirus. Research in Veterinary Science 45:383–388
    [Google Scholar]
  48. Tan J., Yang N. S., Turner J. G., Niu G. L., Maassab H. F., Sun J., Herlocher M. L., Chang A. E., Yu H. 1999; Interleukin-12 cDNA skin transfection potentiates human papillomavirus E6 DNA vaccine-induced antitumor immune response. Cancer Gene Therapy 6:331–339
    [Google Scholar]
  49. Tsuji T., Hamajima K., Fukushima J., Xin K. Q., Ishii N., Aoki I., Ishigatsubo Y., Tani K., Kawamoto S., Nitta Y., Miyazaki J., Koff W. C., Okubo T., Okuda K. 1997; Enhancement of cell-mediated immunity against HIV-1 induced by coinoculation of plasmid-encoded HIV-1 antigen with plasmid expressing IL-12. Journal of Immunology 158:4008–4013
    [Google Scholar]
  50. van Rooij E. M., Haagmans B. L., Glansbeek H. L., de Visser Y. E., de Bruin M. G., Boersma W., Bianchi A. T. 2000; A DNA vaccine coding for glycoprotein B of pseudorabies virus induces cell-mediated immunity in pigs and reduces virus excretion early after infection. Veterinary Immunology and Immunopathology 74:121–136
    [Google Scholar]
  51. Vennema H., de Groot R. J., Harbour D. A., Dalderup M., Gruffydd-Jones T., Horzinek M. C., Spaan W. J. 1990; Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. Journal of Virology 64:1407–1409
    [Google Scholar]
  52. Vennema H., de Groot R. J., Harbour D. A., Horzinek M. C., Spaan W. J. 1991; Primary structure of the membrane and nucleocapsid protein genes of feline infectious peritonitis virus and immunogenicity of recombinant vaccinia viruses in kittens. Virology 181:327–335
    [Google Scholar]
  53. Vennema H., Poland A., Foley J., Pedersen N. C. 1998; Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology 243:150–157
    [Google Scholar]
  54. Wasmoen T. L., Kadakia N. P., Unfer R. C., Fickbohm B. L., Cook C. P., Chu H. J., Acree W. M. 1995; Protection of cats from infectious peritonitis by vaccination with a recombinant raccoon poxvirus expressing the nucleocapsid gene of feline infectious peritonitis virus. Advances in Experimental Medicine and Biology 280:221–228
    [Google Scholar]
  55. Weiss R. C., Scott F. W. 1981; Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comparative Immunology, Microbiology and Infectious Diseases 4:175–189
    [Google Scholar]
  56. Woods R. D., Pedersen N. C. 1979; Cross-protection studies between feline infectious peritonitis and porcine transmissible gastroenteritis viruses. Veterinary Microbiology 4:11–16
    [Google Scholar]
  57. Woods R. D., Wesley R. D., Kapke P. A. 1988; Neutralization of porcine transmissible gastroenteritis virus by complement-dependent monoclonal antibodies. American Journal of Veterinary Research 49:300–304
    [Google Scholar]
  58. Yokoyama M., Hassett D. E., Zhang J., Whitton J. L. 1997; DNA immunization can stimulate florid local inflammation, and the antiviral immunity induced varies depending on injection site. Vaccine 15:553–560
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-1-1
Loading
/content/journal/jgv/10.1099/0022-1317-83-1-1
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error