1887

Journal of General Virology header logo

Volume 78, Issue 9

Bovine herpesvirus-1 infects activated CD4+ lymphocytes Free

Abstract

Acute virus infections can induce immune deficiencies, as shown by immunosuppression to a variety of antigens and mitogens. Previously we observed that live bovine herpesvirus-1 (BHV-1) induced considerable lymphocyte death in culture, suggesting that the virus infected one or more cell populations. Our goal was to identify the cells infected by BHV-1 and the mechanism resulting in cell death. ConA activated cells were cultured with BHV-1 and stained with monoclonal antibodies specific for virus envelope glycoproteins (gB, gC and gD) and lymphocyte surface proteins (CD2, CD4 and CD8) and a molecule associated with cells. Two- colour immunofluorescence revealed that virus glycoproteins were preferentially expressed on T lymphocytes of the CD4phenotype. Live virus was required for virus glycoprotein expression, and by 48 h considerable loss of CD4 expression was observed. To confirm virus replication, RNA was isolated from cells, reverse transcribed and amplified using primers to a 342 bp region of immediate- early and early genes (IER2.9/ER2.6) or a 392 bp region of an early gene (gD). Immediate-early/early gene products were detected in CD4 T lymphocytes but not in infectious virions. Lymphocyte apoptosis was observed by 7 h post-infection with increasing levels of cell death at 24–48 h after infection. These findings suggest that the loss of proliferating CD4 T cells during infection or vaccination with modified live vaccines provides the opportunity for secondary infections that commonly occur following BHV-1 infection.

  • Published Online:
© Society for General Microbiology 1997
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-9-2159
1997-09-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/9/9292002.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-9-2159&mimeType=html&fmt=ahah

References

  1. Allan E. M., Mosolla P. M. 1980; Scanning electron microscopy of the tracheal epithelium of calves inoculated with bovine herpesvirus 1. Research in Veterinary Science 29:235–237
     [Google Scholar]
  2. Babiuk L. A., Bielefeldt Ohmann H. 1985; Bovine herpesvirus-1 (BHV-1) infection in cattle as a model for viral induced immunosuppression. In Viral Mechanisms of Immune Suppression pp. 99–114 Gilmore N., Wainberg M. A. Edited by New York: Alan R. Liss;
     [Google Scholar]
  3. Baldwin C. L., Teale A. J., Naessen J. G., Goddeeris B. M., MacHugh N. D., Morrison W. I. 1986; Characterization of a subset of bovine T lymphocytes that express BoT4 by monoclonal antibodies and function: similarity to lymphocytes defined by human T4 and murine L3T4. Journal of Immunology 136:4385–4391
     [Google Scholar]
  4. Bielefeldt Ohmann H., Babiuk L. A. 1985a; In vitro and systemic effects of recombinant bovine interferons on natural cytotoxicity in healthy and bovine herpesvirus-1-infected cattle. Journal of Interferon Research 5:551–564
     [Google Scholar]
  5. Bielefeldt Ohmann H., Babiuk L. A. 1985b; Viral-bacterial pneumonia in calves: effect of bovine herpesvirus-1 on immunologic functions. Journal of Infectious Diseases 151:937–947
     [Google Scholar]
  6. Carter J. J., Weinberg A. D., Pollard A., Reeves R., Magnuson J. A., Magnuson N. S. 1989; Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by bovine herpesvirus 1. Journal of Virology 63:1525–1530
     [Google Scholar]
  7. Collins J. K., Butcher A. C., Rioegel C. A. 1985; Immune response to bovine herpesvirus type 1. Virus-specific antibodies in sera from infected animals. Journal of Clinical Microbiology 21:546–552
     [Google Scholar]
  8. Covert J., Splitter G. A. 1995; Detection of cytokine transcriptional profiles from bovine peripheral blood mononuclear cells and CD4+ lymphocytes by RT-PCR. Veterinary Immunology and Immunopathology 49:39–50
     [Google Scholar]
  9. Denis M., Splitter G. A., Thiry E., Pastoret P., Babiuk L. A. 1994; Infectious bovine rhinotracheitis (bovine herpesvirus 1): helper T cells, cytotoxic T cells and NK cells. In Cell Mediated Immunity in Ruminants pp. 157–172 Goddeeris B. M. L., Morrison W. I. Edited by Boca Raton: CRC Press;
     [Google Scholar]
  10. Eskra L., O’Reilly K., Splitter G. A. 1991; The bovine p150/95 molecule (CD11c-/CD18) functions in primary cell-cell interaction. Veterinary Immunology and Immunopathology 29:213–228
     [Google Scholar]
  11. Filion L. G., McGuire R. L., Babiuk L. A. 1981; Nonspecific suppressive effect of bovine herpesvirus type 1 on bovine leukocyte functions. Infection and Immunity 42:106–112
     [Google Scholar]
  12. Fruh K., Ahn K., Djaballah H., Sempé P., van Endert P. M., Tampé R., Peterson P. A., Yang Y. 1995; A viral inhibitor of peptide transporters for antigen presentation. Nature 375:415–418
     [Google Scholar]
  13. Griebel P. J., Qualtiere L., Davis W. C., Gee A., Bielefeldt Ohmann H., Lawman M. J. P., Babiuk L. A. 1987/1988; T lymphocyte population dynamics and function following a primary bovine herpesvirus type-1 infection. Viral Immunology 1:287–304
     [Google Scholar]
  14. Greibel P. J., Bielefeldt Ohmann H., Lawman M. J. P., Babiuk L. A. 1990; The interaction between bovine herpesvirus type 1 and activated bovine T lymphocytes. Journal of General Virology 71:369–377
     [Google Scholar]
  15. Groux H. G., Torpier G., Monté D., Mouton Y., Capron A., Ameisen J. C. 1992; Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. Journal of Experimental Medicine 175:331–340
     [Google Scholar]
  16. Ho D. D., Pomeranthnz R. J., Kaplan J. C. 1987; Pathogenesis of infection with human immunodeficiency virus. New England Journal of Medicine 317:278–286
     [Google Scholar]
  17. Hom R. C., Gopalan S., Finberg R. 1989; Trojan horse lymphocytes : a vesicular stomatitis virus-specific T-cell clone lyses virus by carrying virus. Journal of Virology 63:4157–4164
     [Google Scholar]
  18. Levitskaya J., Corman M., Levitsky V., Imreh S., Steigerwald-Mullen P. M., Klein G., Kurilla M. G., Masucci M. G. 1995; Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685–688
     [Google Scholar]
  19. Ludwig G. V., Letchworth G. J. III 1987; Temporal control of bovine herpesvirus 1 glycoprotein synthesis. Journal of Virology 61:3292–3294
     [Google Scholar]
  20. Mackay C. R., Maddox J. F., Brandon M. R. 1986; Three distinct subpopulations of sheep T lymphocytes. European Journal of Immunology 16:19–25
     [Google Scholar]
  21. Marshall R. L., Rodriguez L. L., Letchworth G. J. III 1986; Characterization of envelope proteins of infectious bovine rhinotracheitis virus (bovine herpesvirus 1) by biochemical and immunological methods. Journal of Virology 57:745–753
     [Google Scholar]
  22. O’Reilly K. L., Splitter G. A. 1989; Monoclonal antibodies to ovine SBU-T8 and SBU-T6 bind analogous molecules on bovine lymphocytes. Immunology 67:178–180
     [Google Scholar]
  23. O’Reilly K. L., Splitter G. A. 1990; Biochemical and functional characterization of 8-10C5 (gp120,90), a novel molecule on the surface of bovine T leukocytes. Immunology 71:434–441
     [Google Scholar]
  24. Pelton B. K., Imrie R. C., Denman A. M. 1977; Susceptibility of human lymphocyte populations to infection by herpes simplex virus. Immunology 32:803–810
     [Google Scholar]
  25. Razvi E. S., Welsh R. M. 1993; Programmed cell death of T lymphocytes during acute viral infection; a mechanism for virus induced immune deficiency. Journal of Virology 67:5754–5765
     [Google Scholar]
  26. Rice G. P. A., Schrier R. D., Oldstone M. B. A. 1984; Cytomegalovirus infects human lymphocytes and monocytes: virus expression is restricted to immediate-early gene products. Proceedings of the National Academy of Sciences, USA 81:6134–6138
     [Google Scholar]
  27. Roizman B., Sears A. E. 1990; Herpes simplex viruses and their replication. In Fields Virology, 2nd edn. p. 1820 Fields B. N., Knipe D. M. Edited by New York: Raven Press;
     [Google Scholar]
  28. Rossi C. R., Kiesel G. K. 1977; Susceptibility of bovine macrophages and tracheal ring cultures to bovine viruses. American Journal of Veterinary Research 38:1705–1708
     [Google Scholar]
  29. Splitter G. A., Eskra L. 1986; Bovine T lymphocyte response to bovine herpesvirus-1 : cell phenotypes, viral recognition and acid-labile interferon production. Veterinary Immunology and Immunopathology 11:235–250
     [Google Scholar]
  30. Takahashi K., Shunro S., Higashi K., Kondo T., Takahashi H., Takahashi M., Yamanishi K. 1989; Predominant CD4 T lymphocyte tropism of human herpesvirus 6-related virus. Journal of Virology 63:3161–3163
     [Google Scholar]
  31. Tropea F., Troiano L., Monti D., Lovato E., Malorni W., Rainaldi G., Mattana P., Viscomi G., Ingletti M. C., Portolani M., Cermelli C., Cossarizza A., Franceschi C. 1995; Sendai virus and herpesvirus type 1 induce apoptosis in human peripheral blood mononuclear cells. Experimental Cell Research 218:63–70
     [Google Scholar]
  32. Uehare T., Miyawaki T., Ohta K., Tamaru Y., Yoko T., Nakamura S. M., Taniguchi N. 1992; Apoptotic cell death of primed CD45RO+ T lymphocytes in Epstein-Barr virus-induced infectious mononucleosis. Blood 80:452–458
     [Google Scholar]
  33. Wirth U. V., Fraefel C., Vogt B., Vlcek C., Paces V., Schwyzer M. 1992; Immediate-early RNA 2.9 and early RNA 2.6 of bovine herpesvirus 1 are 3′ coterminal and encode a putative zinc finger transactivator protein. Journal of Virology 66:2763–2772
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-78-9-2159
Loading
Bovine herpesvirus-1 infects activated CD4+ lymphocytes
J. Gen. Virol. 78, 2159 (1997); https://doi.org/10.1099/0022-1317-78-9-2159
/content/journal/jgv/10.1099/0022-1317-78-9-2159
/content/journal/jgv/10.1099/0022-1317-78-9-2159
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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