Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Journal of Virology logoLink to Journal of Virology
. 1995 Mar;69(3):1429–1434. doi: 10.1128/jvi.69.3.1429-1434.1995

Host response to Sendai virus in mice lacking class II major histocompatibility complex glycoproteins.

S Hou 1, X Y Mo 1, L Hyland 1, P C Doherty 1
PMCID: PMC188729  PMID: 7853474

Abstract

The development of Sendai virus-specific cytotoxic T-lymphocyte (CTL) effectors and precursors (CTLp) has been compared for mice that are homozygous (-/-) for a disruption of the H-2I-Ab class II major histocompatibility complex glycoprotein and for normal (+/+) controls. The generation of CD8+ CTLp was not diminished in the -/- mice, though they failed to make virus-specific immunoglobulin G class antibodies. While the cellularity of the regional lymph nodes was decreased, the inflammatory process assayed by bronchoalveolar lavage (BAL) of the pneumonic lung was not modified, and potent CTL effectors were present in BAL populations recovered from both groups at day 10 after infection. There was little effect on virus clearance. Production of interleukin-2 by both freshly isolated BAL inflammatory cells and cultured lymph node cells was greatly diminished, though the -/- mice still made substantial levels of gamma interferon. However, treating the mice with a single dose of a monoclonal antibody to this cytokine, at least some of which is made by CD8+ T cells, did not decrease CTLp frequencies. As found previously with CD4-depleted H-2b mice, the development of Sendai virus-specific CD8+ T-cell-mediated immunity is not compromised by the absence of a concurrent class II major histocompatibility complex-restricted response.

Full Text

The Full Text of this article is available as a PDF (250.5 KB).

Selected References

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

  1. 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]
  2. Ben-Sasson S. Z., Le Gros G., Conrad D. H., Finkelman F. D., Paul W. E. Cross-linking Fc receptors stimulate splenic non-B, non-T cells to secrete interleukin 4 and other lymphokines. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1421–1425. doi: 10.1073/pnas.87.4.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennink J. R., Doherty P. C. Different rules govern help for cytotoxic T cells and B cells. Nature. 1978 Dec 21;276(5690):829–831. doi: 10.1038/276829a0. [DOI] [PubMed] [Google Scholar]
  4. Bodmer H., Obert G., Chan S., Benoist C., Mathis D. Environmental modulation of the autonomy of cytotoxic T lymphocytes. Eur J Immunol. 1993 Jul;23(7):1649–1654. doi: 10.1002/eji.1830230738. [DOI] [PubMed] [Google Scholar]
  5. Cardell S., Merkenschlager M., Bodmer H., Chan S., Cosgrove D., Benoist C., Mathis D. The immune system of mice lacking conventional MHC class II molecules. Adv Immunol. 1994;55:423–440. doi: 10.1016/s0065-2776(08)60515-5. [DOI] [PubMed] [Google Scholar]
  6. Carding S. R., Allan W., McMickle A., Doherty P. C. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med. 1993 Feb 1;177(2):475–482. doi: 10.1084/jem.177.2.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen W. F., Zlotnik A. IL-10: a novel cytotoxic T cell differentiation factor. J Immunol. 1991 Jul 15;147(2):528–534. [PubMed] [Google Scholar]
  8. Croft M. Activation of naive, memory and effector T cells. Curr Opin Immunol. 1994 Jun;6(3):431–437. doi: 10.1016/0952-7915(94)90123-6. [DOI] [PubMed] [Google Scholar]
  9. Doherty P. C., Allan W., Eichelberger M., Carding S. R. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu Rev Immunol. 1992;10:123–151. doi: 10.1146/annurev.iy.10.040192.001011. [DOI] [PubMed] [Google Scholar]
  10. Doherty P. C. Virus infections in mice with targeted gene disruptions. Curr Opin Immunol. 1993 Aug;5(4):479–483. doi: 10.1016/0952-7915(93)90026-o. [DOI] [PubMed] [Google Scholar]
  11. Ewing C., Allan W., Daly K., Hou S., Cole G. A., Doherty P. C., Blackman M. A. Virus-specific CD8+ T-cell responses in mice transgenic for a T-cell receptor beta chain selected at random. J Virol. 1994 May;68(5):3065–3070. doi: 10.1128/jvi.68.5.3065-3070.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fauci A. S. Multifactorial nature of human immunodeficiency virus disease: implications for therapy. Science. 1993 Nov 12;262(5136):1011–1018. doi: 10.1126/science.8235617. [DOI] [PubMed] [Google Scholar]
  13. Finkelman F. D., Katona I. M., Mosmann T. R., Coffman R. L. IFN-gamma regulates the isotypes of Ig secreted during in vivo humoral immune responses. J Immunol. 1988 Feb 15;140(4):1022–1027. [PubMed] [Google Scholar]
  14. Grabstein K. H., Eisenman J., Shanebeck K., Rauch C., Srinivasan S., Fung V., Beers C., Richardson J., Schoenborn M. A., Ahdieh M. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science. 1994 May 13;264(5161):965–968. doi: 10.1126/science.8178155. [DOI] [PubMed] [Google Scholar]
  15. Graham M. B., Dalton D. K., Giltinan D., Braciale V. L., Stewart T. A., Braciale T. J. Response to influenza infection in mice with a targeted disruption in the interferon gamma gene. J Exp Med. 1993 Nov 1;178(5):1725–1732. doi: 10.1084/jem.178.5.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grusby M. J., Johnson R. S., Papaioannou V. E., Glimcher L. H. Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice. Science. 1991 Sep 20;253(5026):1417–1420. doi: 10.1126/science.1910207. [DOI] [PubMed] [Google Scholar]
  17. Hou S., Doherty P. C. Partitioning of responder CD8+ T cells in lymph node and lung of mice with Sendai virus pneumonia by LECAM-1 and CD45RB phenotype. J Immunol. 1993 Jun 15;150(12):5494–5500. [PubMed] [Google Scholar]
  18. 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]
  19. Hou S., Hyland L., Ryan K. W., Portner A., Doherty P. C. Virus-specific CD8+ T-cell memory determined by clonal burst size. Nature. 1994 Jun 23;369(6482):652–654. doi: 10.1038/369652a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Hyland L., Sangster M., Sealy R., Coleclough C. Respiratory virus infection of mice provokes a permanent humoral immune response. J Virol. 1994 Sep;68(9):6083–6086. doi: 10.1128/jvi.68.9.6083-6086.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jennings S. R., Bonneau R. H., Smith P. M., Wolcott R. M., Chervenak R. CD4-positive T lymphocytes are required for the generation of the primary but not the secondary CD8-positive cytolytic T lymphocyte response to herpes simplex virus in C57BL/6 mice. Cell Immunol. 1991 Mar;133(1):234–252. doi: 10.1016/0008-8749(91)90194-g. [DOI] [PubMed] [Google Scholar]
  23. Jones P. D., Ada G. L. Influenza-specific antibody-secreting cells and B cell memory in the murine lung after immunization with wild-type, cold-adapted variant and inactivated influenza viruses. Vaccine. 1987 Sep;5(3):244–248. doi: 10.1016/0264-410x(87)90109-5. [DOI] [PubMed] [Google Scholar]
  24. Kast W. M., Roux L., Curren J., Blom H. J., Voordouw A. C., Meloen R. H., Kolakofsky D., Melief C. J. Protection against lethal Sendai virus infection by in vivo priming of virus-specific cytotoxic T lymphocytes with a free synthetic peptide. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2283–2287. doi: 10.1073/pnas.88.6.2283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kelso A., Troutt A. B., Maraskovsky E., Gough N. M., Morris L., Pech M. H., Thomson J. A. Heterogeneity in lymphokine profiles of CD4+ and CD8+ T cells and clones activated in vivo and in vitro. Immunol Rev. 1991 Oct;123:85–114. doi: 10.1111/j.1600-065x.1991.tb00607.x. [DOI] [PubMed] [Google Scholar]
  26. Kos F. J., Müllbacher A. Induction of primary anti-viral cytotoxic T cells by in vitro stimulation with short synthetic peptide and interleukin-7. Eur J Immunol. 1992 Dec;22(12):3183–3185. doi: 10.1002/eji.1830221224. [DOI] [PubMed] [Google Scholar]
  27. Le Gros G., Erard F. Non-cytotoxic, IL-4, IL-5, IL-10 producing CD8+ T cells: their activation and effector functions. Curr Opin Immunol. 1994 Jun;6(3):453–457. doi: 10.1016/0952-7915(94)90127-9. [DOI] [PubMed] [Google Scholar]
  28. Locksley R. M., Heinzel F. P., Holaday B. J., Mutha S. S., Reiner S. L., Sadick M. D. Induction of Th1 and Th2 CD4+ subsets during murine Leishmania major infection. Res Immunol. 1991 Jan;142(1):28–32. doi: 10.1016/0923-2494(91)90007-6. [DOI] [PubMed] [Google Scholar]
  29. Locksley R. M., Reiner S. L., Hatam F., Littman D. R., Killeen N. Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice. Science. 1993 Sep 10;261(5127):1448–1451. doi: 10.1126/science.8367726. [DOI] [PubMed] [Google Scholar]
  30. Moskophidis D., Cobbold S. P., Waldmann H., Lehmann-Grube F. Mechanism of recovery from acute virus infection: treatment of lymphocytic choriomeningitis virus-infected mice with monoclonal antibodies reveals that Lyt-2+ T lymphocytes mediate clearance of virus and regulate the antiviral antibody response. J Virol. 1987 Jun;61(6):1867–1874. doi: 10.1128/jvi.61.6.1867-1874.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mosmann T. R., Coffman R. L. Heterogeneity of cytokine secretion patterns and functions of helper T cells. Adv Immunol. 1989;46:111–147. doi: 10.1016/s0065-2776(08)60652-5. [DOI] [PubMed] [Google Scholar]
  32. Nash A. A., Jayasuriya A., Phelan J., Cobbold S. P., Waldmann H., Prospero T. Different roles for L3T4+ and Lyt 2+ T cell subsets in the control of an acute herpes simplex virus infection of the skin and nervous system. J Gen Virol. 1987 Mar;68(Pt 3):825–833. doi: 10.1099/0022-1317-68-3-825. [DOI] [PubMed] [Google Scholar]
  33. Owen J. A., Allouche M., Doherty P. C. Limiting dilution analysis of the specificity of influenza-immune cytotoxic T cells. Cell Immunol. 1982 Feb;67(1):49–59. doi: 10.1016/0008-8749(82)90198-8. [DOI] [PubMed] [Google Scholar]
  34. Palladino G., Scherle P. A., Gerhard W. Activity of CD4+ T-cell clones of type 1 and type 2 in generation of influenza virus-specific cytotoxic responses in vitro. J Virol. 1991 Nov;65(11):6071–6076. doi: 10.1128/jvi.65.11.6071-6076.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sarawar S. R., Carding S. R., Allan W., McMickle A., Fujihashi K., Kiyono H., McGhee J. R., Doherty P. C. Cytokine profiles of bronchoalveolar lavage cells from mice with influenza pneumonia: consequences of CD4+ and CD8+ T cell depletion. Reg Immunol. 1993 May-Aug;5(3-4):142–150. [PubMed] [Google Scholar]
  36. Sarawar S. R., Doherty P. C. Concurrent production of interleukin-2, interleukin-10, and gamma interferon in the regional lymph nodes of mice with influenza pneumonia. J Virol. 1994 May;68(5):3112–3119. doi: 10.1128/jvi.68.5.3112-3119.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sarawar S. R., Sangster M., Coffman R. L., Doherty P. C. Administration of anti-IFN-gamma antibody to beta 2-microglobulin-deficient mice delays influenza virus clearance but does not switch the response to a T helper cell 2 phenotype. J Immunol. 1994 Aug 1;153(3):1246–1253. [PubMed] [Google Scholar]
  38. Schrader J. W., Moyer C., Ziltener H. J., Reinisch C. L. Release of the cytokines colony-stimulating factor-1, granulocyte-macrophage colony-stimulating factor, and IL-6 by cloned murine vascular smooth muscle cells. J Immunol. 1991 Jun 1;146(11):3799–3808. [PubMed] [Google Scholar]
  39. Zinkernagel R. M., Doherty P. C. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness. Adv Immunol. 1979;27:51–177. doi: 10.1016/s0065-2776(08)60262-x. [DOI] [PubMed] [Google Scholar]
  40. Zlotnik A., Godfrey D. I., Fischer M., Suda T. Cytokine production by mature and immature CD4-CD8- T cells. Alpha beta-T cell receptor+ CD4-CD8- T cells produce IL-4. J Immunol. 1992 Aug 15;149(4):1211–1215. [PubMed] [Google Scholar]

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

RESOURCES