Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1980 Sep;29(3):846–852. doi: 10.1128/iai.29.3.846-852.1980

Immune Response in Rabbits to Surface Components of Extracellular and Intracellular Forms of Vaccinia Virus

N Balachandran 1, P Seth 1,*, L N Mohapatra 1
PMCID: PMC551207  PMID: 7000705

Abstract

The development of cellular as well as humoral immune response to extracellular and intracellular forms of vaccinia virus (ECV and ICV, respectively) and their surface antigens were studied in rabbits. Direct lymphocyte cytotoxicity and peripheral blood leukocyte migration inhibition tests were used to measure cell-mediated immune response, while neutralizing and hemagglutination-inhibiting antibodies were assayed for measuring humoral immune response. Direct cytotoxicity of lymphocytes from rabbits immunized with ECV or its surface proteins was demonstrable by day 7 after immunization, and by the end of week 3 it almost declined to pre-immunization levels. Inoculation with ICV or its surface proteins failed to induce lymphocyte cytotoxicity. In contrast, migration inhibition of peripheral blood leukocytes from rabbits immunized with ECV, ICV, or their surface proteins was observed with homologous antigens. However, leukocytes from rabbits immunized with ECV or its surface proteins also showed migration inhibition in the presence of ICV. Similarly, in the humoral immune response, neutralizing antibodies were produced against homologous as well as heterologous forms of virus despite immunization with purified preparations of ECV, ICV, or their surface proteins. Adsorption with purified ICV preparations abolished the neutralizing activity of these antisera against heterologous forms of virus. Hemagglutination-inhibiting antibodies, on the other hand, were produced only after immunization with ECV or its surface proteins. In addition, antibody-dependent cell-mediated cytotoxicity was employed to detect specific antibody response after immunization of rabbits with live virus, ECV, and ICV. Antisera raised against ECV or live virus supported antibody-dependent cell-mediated cytotoxicity, whereas ICV-antiserum failed to do so. The antibody activity present in the former antisera was abolished by absorption with cell membranes from vaccinia-infected cells but not with purified ICV. The data suggest that immunization with inactivated ECV seems to bring about interaction between host immune response (cellular and humoral) and virus-infected cells, which may, perhaps, be necessary for protection against pox virus infection. A similar interaction is unlikely to occur after immunization with inactivated ICV.

Full text

PDF
846

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appleyard G., Hapel A. J., Boulter E. A. An antigenic difference between intracellular and extracellular rabbitpox virus. J Gen Virol. 1971 Oct;13(1):9–17. doi: 10.1099/0022-1317-13-1-9. [DOI] [PubMed] [Google Scholar]
  2. Balachandran N., Seth P., Mohapatra L. N. Use of the 51chromium release test to demonstrate antigenic differences between extracellular and intracellular forms of vaccinia virus. J Gen Virol. 1979 Oct;45(1):65–72. doi: 10.1099/0022-1317-45-1-65. [DOI] [PubMed] [Google Scholar]
  3. Boulter E. A., Appleyard G. Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol. 1973;16:86–108. [PubMed] [Google Scholar]
  4. Boulter E. A. Protection against poxviruses. Proc R Soc Med. 1969 Mar 3;62(3):295–297. doi: 10.1177/003591576906200349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boulter E. A., Zwartouw H. T., Titmuss D. H., Maber H. B. The nature of the immune state produced by inactivated vaccinia virus in rabbits. Am J Epidemiol. 1971 Dec;94(6):612–620. doi: 10.1093/oxfordjournals.aje.a121360. [DOI] [PubMed] [Google Scholar]
  6. Brunner K. T., Mauel J., Cerottini J. C., Chapuis B. Quantitative assay of the lytic action of immune lymphoid cells on 51-Cr-labelled allogeneic target cells in vitro; inhibition by isoantibody and by drugs. Immunology. 1968 Feb;14(2):181–196. [PMC free article] [PubMed] [Google Scholar]
  7. Cerottini J. C., Brunner K. T. Cell-mediated cytotoxicity, allograft rejection, and tumor immunity. Adv Immunol. 1974;18:67–132. doi: 10.1016/s0065-2776(08)60308-9. [DOI] [PubMed] [Google Scholar]
  8. Clancy R., Rawls W. E., Jagannath S. Appearanc of cytotoxic cells within the bronchus after local infection with herpes simplex virus. J Immunol. 1977 Sep;119(3):1102–1105. [PubMed] [Google Scholar]
  9. Doherty P. C., Blanden R. V., Zinkernagel R. M. Specificity of virus-immune effector T cells for H-2K or H-2D compatible interactions: implications for H-antigen diversity. Transplant Rev. 1976;29:89–124. doi: 10.1111/j.1600-065x.1976.tb00198.x. [DOI] [PubMed] [Google Scholar]
  10. Ennis F. A. Host defense mechanisms against Herpes simplex virus. I. Control of infection in vitro by senstized spleen cells and antibody. Infect Immun. 1973 Jun;7(6):898–904. doi: 10.1128/iai.7.6.898-904.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ennis F. A., Wells M. Immune control of herpes simplex virus infections. Cancer Res. 1974 May;34(5):1140–1145. [PubMed] [Google Scholar]
  12. Goulmy E., Termijtelen A., Bradley B. A., van Rood J. J. Y-antigen killing by T cells of women is restricted by HLA. Nature. 1977 Apr 7;266(5602):544–545. doi: 10.1038/266544a0. [DOI] [PubMed] [Google Scholar]
  13. Kreth H. W., Wiegand G. Cell-mediated cytotoxicity against measles virus in SSPE. II. Analysis of cytotoxic effector cells. J Immunol. 1977 Jan;118(1):296–301. [PubMed] [Google Scholar]
  14. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  15. Moller-Larsen A., Heron I., Haahr S. Cell-mediated cytotoxicity to herpes-infected cells in humans: dependence on antibodies. Infect Immun. 1977 Apr;16(1):43–47. doi: 10.1128/iai.16.1.43-47.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Møller-Larsen A., Haahr S., Heron I. Lymphocyte-mediated cytotoxicity in humans during revaccination with vaccinia virus. Infect Immun. 1978 Sep;21(3):687–695. doi: 10.1128/iai.21.3.687-695.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Payne L. G., Norrby E. Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles. J Gen Virol. 1976 Jul;32(1):63–72. doi: 10.1099/0022-1317-32-1-63. [DOI] [PubMed] [Google Scholar]
  18. Payne L. Polypeptide composition of extracellular enveloped vaccinia virus. J Virol. 1978 Jul;27(1):28–37. doi: 10.1128/jvi.27.1.28-37.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pearson G. R. In vitro and in vivo investigations on antibody-dependent cellular cytotoxicity. Curr Top Microbiol Immunol. 1978;80:65–96. doi: 10.1007/978-3-642-66956-9_3. [DOI] [PubMed] [Google Scholar]
  20. Perrin L. H., Tishon A., Oldstone M. B. Immunologic injury in measles virus infection. III. Presence and characterization of human cytotoxic lymphocytes. J Immunol. 1977 Jan;118(1):282–290. [PubMed] [Google Scholar]
  21. Perrin L. H., Zinkernagel R. M., Oldstone M. B. Immune response in humans after vaccination with vaccinia virus: generation of a virus-specific cytotoxic activity by human peripheral lymphocytes. J Exp Med. 1977 Oct 1;146(4):949–969. doi: 10.1084/jem.146.4.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Prakash V. J., Norrby E., Payne L. Single radial immunodiffusion test for detecting antibodies against surface antigens of intracellular and extracellular vaccinia virus. J Gen Virol. 1977 Jun;35(3):465–472. doi: 10.1099/0022-1317-35-3-463. [DOI] [PubMed] [Google Scholar]
  23. Shore S. L., Black C. M., Melewicz F. M., Wood P. A., Nahmias A. J. Antibody-dependent cell-mediated cytotoxicity to target cells infected with type 1 and type 2 herpes simplex virus. J Immunol. 1976 Jan;116(1):194–201. [PubMed] [Google Scholar]
  24. Soborg M., Bendixen G. Human lymphocyte migration as a parameter of hypersensitivity. Acta Med Scand. 1967 Feb;181(2):247–256. doi: 10.1111/j.0954-6820.1967.tb07255.x. [DOI] [PubMed] [Google Scholar]
  25. Turner G. S., Squires E. J. Inactivated smallpox vaccine: immunogenicity of inactivated intracellular and extracellular vaccinia virus. J Gen Virol. 1971 Oct;13(1):19–25. doi: 10.1099/0022-1317-13-1-19. [DOI] [PubMed] [Google Scholar]
  26. Tursz T., Fridman W. H., Senik A., Tsapis A., Fellous M. Human virus-infected target cells lacking HLA antigens resist specific T-lymphocyte cytolysis. Nature. 1977 Oct 27;269(5631):806–808. doi: 10.1038/269806a0. [DOI] [PubMed] [Google Scholar]
  27. Wainberg M. A., Markson Y., Weiss D. W., Doljanski F. Cellular immunity against Rous sarcomas of chickens. Preferential reactivity against autochthonous target cells as determined by lymphocyte adherence and cytotoxicity tests in vitro. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3565–3569. doi: 10.1073/pnas.71.9.3565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Weintraub S., Dales S. Biogenesis of poxviruses: genetically controlled modifications of structural and functional components of the plasma membrane. Virology. 1974 Jul;60(1):96–127. doi: 10.1016/0042-6822(74)90369-9. [DOI] [PubMed] [Google Scholar]
  29. Woan M. C., Yip D. M., Tompkins W. A. Autochthonous, allogeneic, and exenogeneic cells as targets for vaccinia immune lymphocyte cytotoxicity. J Immunol. 1978 Jan;120(1):312–316. [PubMed] [Google Scholar]
  30. Zinkernagel R. M., Althage A., Jensen F. C. Cell-mediated immune response to lymphocytic choriomeningitis and vaccinia virus in rats. J Immunol. 1977 Oct;119(4):1242–1247. [PubMed] [Google Scholar]
  31. Zinkernagel R. M., Althage A., Jensen F., Streilein J. W., Duncan W. R. Cell-mediated immunity to viruses in hamsters. Fed Proc. 1978 May 15;37(7):2078–2081. [PubMed] [Google Scholar]
  32. Zinkernagel R. M., Doherty P. C. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature. 1974 Apr 19;248(5450):701–702. doi: 10.1038/248701a0. [DOI] [PubMed] [Google Scholar]
  33. Zinkernagel R. M., Oldstone M. B. Cells that express viral antigens but lack H-2 determinants are not lysed by immune thymus-derived lymphocytes but are lysed by other antiviral immune attack mechanisms. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3666–3670. doi: 10.1073/pnas.73.10.3666. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES