Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1995 Nov;69(11):6658–6664. doi: 10.1128/jvi.69.11.6658-6664.1995

Role of T-lymphocyte subsets in recovery from respiratory syncytial virus infection in calves.

G Taylor 1, L H Thomas 1, S G Wyld 1, J Furze 1, P Sopp 1, C J Howard 1
PMCID: PMC189575  PMID: 7474075

Abstract

The role of T-cell subsets in respiratory syncytial virus (RSV) infection was investigated by using monoclonal antibodies (MAbs) to selectively deplete gnotobiotic calves of CD4+, CD8+, or WC1+ gamma delta T-cell receptor+ lymphocytes. Injection of these MAbs produced specific reductions of the target cell populations in the circulation and tissues. Ten days after RSV infection, immunoglobulin M (IgM), IgG1, and IgA antibodies were detected in sera and lung washings from control calves. Depletion of CD8+ T cells had no effect on either the serum or local antibody responses to RSV, whereas depletion of CD4+ T cells suppressed the antibody responses in two of three calves. The IgM and IgA responses were significantly increased in the lung washings of calves from which WC1+ T cells were depleted. Depletion of CD4+ or WC1+ T cells caused no significant delay in virus clearance, although an increase in the extent of pneumonic consolidation was observed in anti-CD4-treated calves. Nasopharyngeal excretion of RSV was prolonged in calves depleted of CD8+ T cells, and virus was isolated in high titers from lung washings of these animals 10 days after infection, whereas virus had been cleared from lung washings of all other animals. The delayed virus clearance was associated with an increase in the severity of pneumonic consolidation in three of four of the calves from which CD8+ T cells were depleted. This study shows that CD8+ T cells play a dominant role in the recovery of calves from RSV infection.

Full Text

The Full Text of this article is available as a PDF (311.2 KB).

Selected References

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

  1. Adair J. R. Engineering antibodies for therapy. Immunol Rev. 1992 Dec;130:5–40. doi: 10.1111/j.1600-065x.1992.tb01519.x. [DOI] [PubMed] [Google Scholar]
  2. Allan W., Tabi Z., Cleary A., Doherty P. C. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J Immunol. 1990 May 15;144(10):3980–3986. [PubMed] [Google Scholar]
  3. Alwan W. H., Kozlowska W. J., Openshaw P. J. Distinct types of lung disease caused by functional subsets of antiviral T cells. J Exp Med. 1994 Jan 1;179(1):81–89. doi: 10.1084/jem.179.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Alwan W. H., Record F. M., Openshaw P. J. CD4+ T cells clear virus but augment disease in mice infected with respiratory syncytial virus. Comparison with the effects of CD8+ T cells. Clin Exp Immunol. 1992 Jun;88(3):527–536. doi: 10.1111/j.1365-2249.1992.tb06482.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Born W., Happ M. P., Dallas A., Reardon C., Kubo R., Shinnick T., Brennan P., O'Brien R. Recognition of heat shock proteins and gamma delta cell function. Immunol Today. 1990 Feb;11(2):40–43. doi: 10.1016/0167-5699(90)90015-2. [DOI] [PubMed] [Google Scholar]
  6. Cannon M. J., Openshaw P. J., Askonas B. A. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J Exp Med. 1988 Sep 1;168(3):1163–1168. doi: 10.1084/jem.168.3.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clevers H., MacHugh N. D., Bensaid A., Dunlap S., Baldwin C. L., Kaushal A., Iams K., Howard C. J., Morrison W. I. Identification of a bovine surface antigen uniquely expressed on CD4-CD8- T cell receptor gamma/delta+ T lymphocytes. Eur J Immunol. 1990 Apr;20(4):809–817. doi: 10.1002/eji.1830200415. [DOI] [PubMed] [Google Scholar]
  8. Connors M., Collins P. L., Firestone C. Y., Sotnikov A. V., Waitze A., Davis A. R., Hung P. P., Chanock R. M., Murphy B. R. Cotton rats previously immunized with a chimeric RSV FG glycoprotein develop enhanced pulmonary pathology when infected with RSV, a phenomenon not encountered following immunization with vaccinia--RSV recombinants or RSV. Vaccine. 1992;10(7):475–484. doi: 10.1016/0264-410x(92)90397-3. [DOI] [PubMed] [Google Scholar]
  9. Coutelier J. P. Enhancement of IgG production elicited in mice by treatment with anti-CD8 antibody. Eur J Immunol. 1991 Oct;21(10):2617–2620. doi: 10.1002/eji.1830211046. [DOI] [PubMed] [Google Scholar]
  10. Dennis M. J., Davies D. C., Hoare M. N. A simplified apparatus for the microbiological isolation of calves. Br Vet J. 1976 Nov-Dec;132(6):642–646. doi: 10.1016/s0007-1935(17)34542-6. [DOI] [PubMed] [Google Scholar]
  11. Eichelberger M. C., Wang M. L., Allan W., Webster R. G., Doherty P. C. Influenza virus RNA in the lung and lymphoid tissue of immunologically intact and CD4-depleted mice. J Gen Virol. 1991 Jul;72(Pt 7):1695–1698. doi: 10.1099/0022-1317-72-7-1695. [DOI] [PubMed] [Google Scholar]
  12. Eichelberger M., Allan W., Zijlstra M., Jaenisch R., Doherty P. C. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J Exp Med. 1991 Oct 1;174(4):875–880. doi: 10.1084/jem.174.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Englund J. A., Sullivan C. J., Jordan M. C., Dehner L. P., Vercellotti G. M., Balfour H. H., Jr Respiratory syncytial virus infection in immunocompromised adults. Ann Intern Med. 1988 Aug 1;109(3):203–208. doi: 10.7326/0003-4819-109-3-203. [DOI] [PubMed] [Google Scholar]
  14. Furze J., Wertz G., Lerch R., Taylor G. Antigenic heterogeneity of the attachment protein of bovine respiratory syncytial virus. J Gen Virol. 1994 Feb;75(Pt 2):363–370. doi: 10.1099/0022-1317-75-2-363. [DOI] [PubMed] [Google Scholar]
  15. Graham B. S., Bunton L. A., Rowland J., Wright P. F., Karzon D. T. Respiratory syncytial virus infection in anti-mu-treated mice. J Virol. 1991 Sep;65(9):4936–4942. doi: 10.1128/jvi.65.9.4936-4942.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Graham B. S., Bunton L. A., Wright P. F., Karzon D. T. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J Clin Invest. 1991 Sep;88(3):1026–1033. doi: 10.1172/JCI115362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hall C. B., Powell K. R., MacDonald N. E., Gala C. L., Menegus M. E., Suffin S. C., Cohen H. J. Respiratory syncytial viral infection in children with compromised immune function. N Engl J Med. 1986 Jul 10;315(2):77–81. doi: 10.1056/NEJM198607103150201. [DOI] [PubMed] [Google Scholar]
  18. Harrington R. D., Hooton T. M., Hackman R. C., Storch G. A., Osborne B., Gleaves C. A., Benson A., Meyers J. D. An outbreak of respiratory syncytial virus in a bone marrow transplant center. J Infect Dis. 1992 Jun;165(6):987–993. doi: 10.1093/infdis/165.6.987. [DOI] [PubMed] [Google Scholar]
  19. Hemming V. G., Prince G. A. Respiratory syncytial virus: babies and antibodies. Infect Agents Dis. 1992 Feb;1(1):24–32. [PubMed] [Google Scholar]
  20. Hertz M. I., Englund J. A., Snover D., Bitterman P. B., McGlave P. B. Respiratory syncytial virus-induced acute lung injury in adult patients with bone marrow transplants: a clinical approach and review of the literature. Medicine (Baltimore) 1989 Sep;68(5):269–281. doi: 10.1097/00005792-198909000-00002. [DOI] [PubMed] [Google Scholar]
  21. Hiromatsu K., Yoshikai Y., Matsuzaki G., Ohga S., Muramori K., Matsumoto K., Bluestone J. A., Nomoto K. A protective role of gamma/delta T cells in primary infection with Listeria monocytogenes in mice. J Exp Med. 1992 Jan 1;175(1):49–56. doi: 10.1084/jem.175.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hoare M. N., Davies D. C., Dennis M. J. The derivation of gnotobiotic calves by a hysterotomy and slaughter technique. Br Vet J. 1976 Jul-Aug;132(4):369–373. doi: 10.1016/s0007-1935(17)34635-3. [DOI] [PubMed] [Google Scholar]
  23. Hou S., Doherty P. C., Zijlstra M., Jaenisch R., Katz J. M. Delayed clearance of Sendai virus in mice lacking class I MHC-restricted CD8+ T cells. J Immunol. 1992 Aug 15;149(4):1319–1325. [PubMed] [Google Scholar]
  24. Howard C. J., Sopp P., Parsons K. R., Finch J. In vivo depletion of BoT4 (CD4) and of non-T4/T8 lymphocyte subsets in cattle with monoclonal antibodies. Eur J Immunol. 1989 Apr;19(4):757–764. doi: 10.1002/eji.1830190428. [DOI] [PubMed] [Google Scholar]
  25. Hyland L., Hou S., Coleclough C., Takimoto T., Doherty P. C. Mice lacking CD8+ T cells develop greater numbers of IgA-producing cells in response to a respiratory virus infection. Virology. 1994 Oct;204(1):234–241. doi: 10.1006/viro.1994.1527. [DOI] [PubMed] [Google Scholar]
  26. Kabelitz D., Bender A., Schondelmaier S., Schoel B., Kaufmann S. H. A large fraction of human peripheral blood gamma/delta + T cells is activated by Mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med. 1990 Mar 1;171(3):667–679. doi: 10.1084/jem.171.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kapikian A. Z., Mitchell R. H., Chanock R. M., Shvedoff R. A., Stewart C. E. An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol. 1969 Apr;89(4):405–421. doi: 10.1093/oxfordjournals.aje.a120954. [DOI] [PubMed] [Google Scholar]
  28. Kast W. M., Bronkhorst A. M., de Waal L. P., Melief C. J. Cooperation between cytotoxic and helper T lymphocytes in protection against lethal Sendai virus infection. Protection by T cells is MHC-restricted and MHC-regulated; a model for MHC-disease associations. J Exp Med. 1986 Sep 1;164(3):723–738. doi: 10.1084/jem.164.3.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kim H. W., Canchola J. G., Brandt C. D., Pyles G., Chanock R. M., Jensen K., Parrott R. H. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol. 1969 Apr;89(4):422–434. doi: 10.1093/oxfordjournals.aje.a120955. [DOI] [PubMed] [Google Scholar]
  30. Leukocyte antigens in cattle, sheep and goats. Proceedings of the First International Workshop on Leukocyte Antigens in Cattle, Sheep and Goats. Hannover, Germany, 25 July 1989. Vet Immunol Immunopathol. 1991 Jan;27(1-3):1–275. [PubMed] [Google Scholar]
  31. Oldham G., Bridger J. C., Howard C. J., Parsons K. R. In vivo role of lymphocyte subpopulations in the control of virus excretion and mucosal antibody responses of cattle infected with rotavirus. J Virol. 1993 Aug;67(8):5012–5019. doi: 10.1128/jvi.67.8.5012-5019.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sciammas R., Johnson R. M., Sperling A. I., Brady W., Linsley P. S., Spear P. G., Fitch F. W., Bluestone J. A. Unique antigen recognition by a herpesvirus-specific TCR-gamma delta cell. J Immunol. 1994 Jun 1;152(11):5392–5397. [PubMed] [Google Scholar]
  33. Sharma R., Woldehiwet Z., Spiller D. G., Warenius H. M. Lymphocyte subpopulations in peripheral blood of lambs experimentally infected with bovine respiratory syncytial virus. Vet Immunol Immunopathol. 1990 Apr;24(4):383–391. doi: 10.1016/0165-2427(90)90008-g. [DOI] [PubMed] [Google Scholar]
  34. Stott E. J., Taylor G., Ball L. A., Anderson K., Young K. K., King A. M., Wertz G. W. Immune and histopathological responses in animals vaccinated with recombinant vaccinia viruses that express individual genes of human respiratory syncytial virus. J Virol. 1987 Dec;61(12):3855–3861. doi: 10.1128/jvi.61.12.3855-3861.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stott E. J., Taylor G. Respiratory syncytial virus. Brief review. Arch Virol. 1985;84(1-2):1–52. doi: 10.1007/BF01310552. [DOI] [PubMed] [Google Scholar]
  36. Taylor G., Stott E. J., Bew M., Fernie B. F., Cote P. J., Collins A. P., Hughes M., Jebbett J. Monoclonal antibodies protect against respiratory syncytial virus infection in mice. Immunology. 1984 May;52(1):137–142. [PMC free article] [PubMed] [Google Scholar]
  37. Taylor G., Stott E. J., Furze J., Ford J., Sopp P. Protective epitopes on the fusion protein of respiratory syncytial virus recognized by murine and bovine monoclonal antibodies. J Gen Virol. 1992 Sep;73(Pt 9):2217–2223. doi: 10.1099/0022-1317-73-9-2217. [DOI] [PubMed] [Google Scholar]
  38. Thomas L. H., Gourlay R. N., Stott E. J., Howard C. J., Bridger J. C. A search for new microorganisms in calf pneumonia by the inoculation of gnotobiotic calves. Res Vet Sci. 1982 Sep;33(2):170–182. doi: 10.1016/S0034-5288(18)32331-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thomas L. H., Stott E. J. Diagnosis of respiratory syncytial virus infection in the bovine respiratory tract by immunofluorescence. Vet Rec. 1981 May 16;108(20):432–435. doi: 10.1136/vr.108.20.432. [DOI] [PubMed] [Google Scholar]
  40. Tonegawa S., Berns A., Bonneville M., Farr A., Ishida I., Ito K., Itohara S., Janeway C. A., Jr, Kanagawa O., Katsuki M. Diversity, development, ligands, and probable functions of gamma delta T cells. Cold Spring Harb Symp Quant Biol. 1989;54(Pt 1):31–44. doi: 10.1101/sqb.1989.054.01.005. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES