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. 1981 Feb;31(2):704–711. doi: 10.1128/iai.31.2.704-711.1981

Effect of herpes simplex virus infection on murine antibody-dependent cellular cytotoxicity and natural killer cytotoxicity.

S Kohl, M J Lawman, B T Rouse, D L Cahall
PMCID: PMC351367  PMID: 6260674

Abstract

Mice intraperitoneally inoculated with a sublethal dose of herpes simplex virus (HSV) produced immunoglobulin G antibody-dependent cellular cytotoxicity (ADCC) and radioimmunoassay (RIA) antibody as early as 3 days after infection. There was a rise in natural killer cytotoxicity (NKC) to infected and uninfected target cells 1 to 3 days postinfection mediated by nonadherent peritoneal cells (PC) in mice inoculated with HSV, but also with other substances commonly used in tissue culture media. HSV caused the highest and most consistent increase in NKC. PC-NKC, as ADCC, was inhibited by latex and silica, both macrophage inhibitors. PC-ADCC markedly declined 3 to 8 days after HSV inoculation. This was not due to a soluble or cellular suppressor factor, was not reversed by incubation or trypsin treatment of PC, was not associated with a change in PC Fc receptors, adherence, or acridine orange staining characteristics, and could not be induced by inactivated HSV. In vitro inoculation of PC with HSV similarly caused a reduction in the ability of PC to mediate ADCC to HSV-infected target cells. These data demonstrate the complex stimulatory and inhibitory interactions between virus and host defense mechanisms.

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Selected References

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

  1. Austin R. M., Daniels C. A. Inhibition by rheumatoid factor, anti-FC, and staphylococcal protein A of antibody-dependent cell-mediated cytolysis against Herpes simplex virus-infected cells. J Immunol. 1976 Aug;117(2):602–607. [PubMed] [Google Scholar]
  2. Chalon M. P., Milne R. W., Vaerman J. P. Interactions between mouse immunoglobulins and staphylococcal protein A. Scand J Immunol. 1979;9(4):359–364. doi: 10.1111/j.1365-3083.1979.tb03174.x. [DOI] [PubMed] [Google Scholar]
  3. Ching C., Lopez C. Natural killing of herpes simplex virus type 1-infected target cells: normal human responses and influence of antiviral antibody. Infect Immun. 1979 Oct;26(1):49–56. doi: 10.1128/iai.26.1.49-56.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Djeu J. Y., Heinbaugh J. A., Holden H. T., Herberman R. B. Augmentation of mouse natural killer cell activity by interferon and interferon inducers. J Immunol. 1979 Jan;122(1):175–181. [PubMed] [Google Scholar]
  5. Djeu J. Y., Heinbaugh J. A., Holden H. T., Herberman R. B. Role of macrophages in the augementation of mouse natural killer cell activity by poly I:C and interferon. J Immunol. 1979 Jan;122(1):182–188. [PubMed] [Google Scholar]
  6. Evans R. L., Chess L., Levine H., Schlossman S. F. Antibody-dependent cellular cytotoxicity by allosensitized human T cells. J Exp Med. 1978 Feb 1;147(2):605–610. doi: 10.1084/jem.147.2.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gidlund M., Orn A., Wigzell H., Senik A., Gresser I. Enhanced NK cell activity in mice injected with interferon and interferon inducers. Nature. 1978 Jun 29;273(5665):759–761. doi: 10.1038/273759a0. [DOI] [PubMed] [Google Scholar]
  8. Golub S. H., Golightly M. G., Zielske J. V. "NK-like" cytotoxicity of human lymphocytes cultured in media containing fetal bovine serum. Int J Cancer. 1979 Sep 15;24(3):273–283. doi: 10.1002/ijc.2910240302. [DOI] [PubMed] [Google Scholar]
  9. Greenberg S. B., Six H. R., Drake S., Couch R. B. Cell cytotoxicity due to specific influenza antibody production in vitro after recent influenza antigen stimulation. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4622–4626. doi: 10.1073/pnas.76.9.4622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gupta S., Fernandes G., Nair M., Good R. A. Spontaneous and antibody-dependent cell-mediated cytotoxicity by human T cell subpopulations. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5137–5141. doi: 10.1073/pnas.75.10.5137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hayashi K., Kurata T., Morishima T., Nassery T. Analysis of the inhibitory effect of peritoneal macrophages on the spread of herpes simplex virus. Infect Immun. 1980 May;28(2):350–358. doi: 10.1128/iai.28.2.350-358.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kleinerman E. S., Snyderman R., Daniels C. A. Depression of human monocyte chemotaxis by herpes simplex and influenza viruses. J Immunol. 1974 Nov;113(5):1562–1567. [PubMed] [Google Scholar]
  13. Kohl S., Cahall D. L., Walters D. L., Schaffner V. E. Murine antibody-dependent cellular cytotoxicity to herpes simplex virus-infected target cells. J Immunol. 1979 Jul;123(1):25–30. [PubMed] [Google Scholar]
  14. Kohl S., McCoig E. L., Pickering L. K., Walters D. Comparison of cytotoxicity mediated by human monocyte-macrophages and lymphocytes after prolonged in vitro incubation. J Immunol Methods. 1978;24(3-4):345–353. doi: 10.1016/0022-1759(78)90137-0. [DOI] [PubMed] [Google Scholar]
  15. Kohl S., Pickering L. K., Sullivan M. P., Walters D. L. Impaired monocyte-macrophage cytotoxicity in patients with Hodgkin's disease. Clin Immunol Immunopathol. 1980 Apr;15(4):577–585. doi: 10.1016/0090-1229(80)90001-x. [DOI] [PubMed] [Google Scholar]
  16. Kohl S., Starr S. E., oleske J. M., Shore S. L., Ashman R. B., Nahmias A. J. Human monocyte-macrophage-mediated antibody-dependent cytotoxicity to herpes simplex virus-infected cells. J Immunol. 1977 Mar;118(3):729–735. [PubMed] [Google Scholar]
  17. Kronvall G., Grey H. M., Williams R. C., Jr Protein A reactivity with mouse immunoglobulins. Structural relationship between some mouse and human immunoglobulins. J Immunol. 1970 Nov;105(5):1116–1123. [PubMed] [Google Scholar]
  18. Lawman M. J., Rouse B. T., Courtney R. J., Walker R. D. Cell-mediated immunity against herpes simplex induction of cytotoxic T lymphocytes. Infect Immun. 1980 Jan;27(1):133–139. doi: 10.1128/iai.27.1.133-139.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Melewicz F. M., Shore S. L., Ades E. W., Phillips D. J. The mononuclear cell in human blood which mediates antibody-dependent cellular cytotoxicity to virus-infected target cells. II. Identification as a K cell. J Immunol. 1977 Feb;118(2):567–573. [PubMed] [Google Scholar]
  20. Morahan P. S., Morse S. S., McGeorge M. G. Macrophage extrinsic antiviral activity during herpes simplex virus infection. J Gen Virol. 1980 Feb;46(2):291–300. doi: 10.1099/0022-1317-46-2-291. [DOI] [PubMed] [Google Scholar]
  21. Møller-Larsen A., Haahr S., Black F. T. Cellular and humoral immune responses to herpes simplex virus during and after primary gingivostomatitis. Infect Immun. 1978 Nov;22(2):445–451. doi: 10.1128/iai.22.2.445-451.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nahmias A. J., Shore S. L., Kohl S., Starr S. E., Ashman R. B. Immunology of herpes simplex virus infection: relevance to herpes simplex virus vaccines and cervical cancer. Cancer Res. 1976 Feb;36(2 Pt 2):836–844. [PubMed] [Google Scholar]
  23. Oehler J. R., Lindsay L. R., Nunn M. E., Holden H. T., Herberman R. B. Natural cell-mediated cytotoxicity in rats. II. In vivo augmentation of NK-cell activity. Int J Cancer. 1978 Feb 15;21(2):210–220. doi: 10.1002/ijc.2910210213. [DOI] [PubMed] [Google Scholar]
  24. Pfizenmaier K., Jung H., Starzinski-Powitz A., Röllinghoff M., Wagner H. The role of T cells in anti-herpes simplex virus immunity. I. Induction of antigen-specific cytotoxic T lymphocytes. J Immunol. 1977 Sep;119(3):939–944. [PubMed] [Google Scholar]
  25. Pfizenmaier K., Starzinski-Powitz A., Röllinghoff M., Falks D., Wagner H. T-cell-mediated cytotoxicity against herpes simplex virus-infected target cells. Nature. 1977 Feb 17;265(5595):630–632. doi: 10.1038/265630a0. [DOI] [PubMed] [Google Scholar]
  26. Piontek G. E., Weltzin R., Tompkins W. A. Enhanced cytotoxicity of mouse natural killer cells for vaccinia and herpes virus-infected targets. J Reticuloendothel Soc. 1980 Feb;27(2):175–188. [PubMed] [Google Scholar]
  27. Quinnan G. V., Manischewitz J. E. The role of natural killer cells and antibody-dependent cell-mediated cytotoxicity during murine cytomegalovirus infection. J Exp Med. 1979 Dec 1;150(6):1549–1554. doi: 10.1084/jem.150.6.1549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rager-Zisman B., Allison A. C. Mechanism of immunologic resistance to herpes simplex virus 1 (HSV-1) infection. J Immunol. 1976 Jan;116(1):35–40. [PubMed] [Google Scholar]
  29. Rager-Zisman B., Bloom B. R. Immunological destruction of herpes simplex virus I infected cells. Nature. 1974 Oct 11;251(5475):542–543. doi: 10.1038/251542a0. [DOI] [PubMed] [Google Scholar]
  30. Ramshaw I. A. Lysis of herpesvirus-infected cells by immune spleen cells. Infect Immun. 1975 Apr;11(4):767–769. doi: 10.1128/iai.11.4.767-769.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Richie E. R., Culbert S. J., Sullivan M. P., van Eys J. Complement receptor-positive, sheep erythrocyte receptor-negative lymphoblasts in childhood acute lymphocytic leukemia. Cancer Res. 1978 Nov;38(11 Pt 1):3616–3620. [PubMed] [Google Scholar]
  32. Roberts N. J., Jr, Steigbigel R. T. Effect of in vitro virus infection on response of human monocytes and lymphocytes to mitogen stimulation. J Immunol. 1978 Sep;121(3):1052–1058. [PubMed] [Google Scholar]
  33. Santoli D., Trinchieri G., Koprowski H. Cell-mediated cytotoxicity against virus-infected target cells in humans. II. Interferon induction and activation of natural killer cells. J Immunol. 1978 Aug;121(2):532–538. [PubMed] [Google Scholar]
  34. Santoli D., Trinchieri G., Lief F. S. Cell-mediated cytotoxicity against virus-infected target cells in humans. I. Characterization of the effector lymphocyte. J Immunol. 1978 Aug;121(2):526–531. [PubMed] [Google Scholar]
  35. Shaw S., Pichler W. J., Nelson D. L. Fc receptors on human T-lymphocytes. III. Characterization of subpopulations involved in cell-mediated lympholysis and antibody-dependent cellular cytotoxicity. J Immunol. 1979 Feb;122(2):599–604. [PubMed] [Google Scholar]
  36. 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]
  37. Shore S. L., Cromeans T. L., Romano T. J. Immune destruction of virus-infected cells early in the infectious cycle. Nature. 1976 Aug 19;262(5570):695–696. doi: 10.1038/262695a0. [DOI] [PubMed] [Google Scholar]
  38. Shore S. L., Nahmias A. J., Starr S. E., Wood P. A., McFarlin D. E. Detection of cell-dependent cytotoxic antibody to cells infected with herpes simplex virus. Nature. 1974 Sep 27;251(5473):350–352. doi: 10.1038/251350a0. [DOI] [PubMed] [Google Scholar]
  39. Tagliabue A., Mantovani A., Kilgallen M., Herberman R. B., McCoy J. L. Natural cytotoxicity of mouse monocytes and macrophages. J Immunol. 1979 Jun;122(6):2363–2370. [PubMed] [Google Scholar]
  40. Tracey D. E. The requirement for macrophages in the augmentation of natural killer cell activity by BCG. J Immunol. 1979 Aug;123(2):840–845. [PubMed] [Google Scholar]
  41. Tracey D. E., Wolfe S. A., Durdik J. M., Henney C. S. BCG-induced murine effector cells. I. Cytolytic activity in peritoneal exudates: an early response to BCG. J Immunol. 1977 Sep;119(3):1145–1151. [PubMed] [Google Scholar]
  42. Trinchieri G., Santoli D. Anti-viral activity induced by culturing lymphocytes with tumor-derived or virus-transformed cells. Enhancement of human natural killer cell activity by interferon and antagonistic inhibition of susceptibility of target cells to lysis. J Exp Med. 1978 May 1;147(5):1314–1333. doi: 10.1084/jem.147.5.1314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Trinchieri G., Santoli D., Koprowski H. Spontaneous cell-mediated cytotoxicity in humans: role of interferon and immunoglobulins. J Immunol. 1978 Jun;120(6):1849–1855. [PubMed] [Google Scholar]
  44. Welsh R. M., Jr Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. I. Characterization of natural killer cell induction. J Exp Med. 1978 Jul 1;148(1):163–181. doi: 10.1084/jem.148.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Welsh R. M., Jr, Zinkernagel R. M., Hallenbeck L. A. Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. II. "Specificities" of the natural killer cells. J Immunol. 1979 Feb;122(2):475–481. [PubMed] [Google Scholar]
  46. Welsh R. M., Jr, Zinkernagel R. M. Heterospecific cytotoxic cell activity induced during the first three days of acute lymphocytic choriomeningitis virus infection in mice. Nature. 1977 Aug 18;268(5621):646–648. doi: 10.1038/268646a0. [DOI] [PubMed] [Google Scholar]
  47. Wilkinson P. C. Leukocyte locomotion and chemotaxis: effects of bacteria and viruses. Rev Infect Dis. 1980 Mar-Apr;2(2):293–318. doi: 10.1093/clinids/2.2.293. [DOI] [PubMed] [Google Scholar]
  48. Wolfe S. A., Tracey D. E., Henney C. S. BCG-induced murine effector cells. II. Characterization of natural killer cells in peritoneal exudates. J Immunol. 1977 Sep;119(3):1152–1158. [PubMed] [Google Scholar]
  49. de Vries J. E., Mendelsohn J., Bont W. S. Requirement for monocytes in the spontaneous cytotoxic effects of human lymphocytes against non-lymphoid target cells. Nature. 1980 Feb 7;283(5747):574–576. doi: 10.1038/283574a0. [DOI] [PubMed] [Google Scholar]

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