Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1984 May 1;159(5):1322–1337. doi: 10.1084/jem.159.5.1322

Viruses disrupt functions of human lymphocytes. Effects of measles virus and influenza virus on lymphocyte-mediated killing and antibody production

PMCID: PMC2187306  PMID: 6716049

Abstract

We present experimental data that offer, in part, a better understanding of the immunosuppression that accompanies measles virus infection. We note that measles virus "silently" infects human lymphocytes and that the infection does not alter lymphocyte survival in vitro. Yet such infected lymphocytes fail to generate natural killer (NK) cell activity or synthesize immunoglobulins (Ig). Thus, the presence of virus within lymphocytes impairs their specific immune functions in the absence of cytolysis. Influenza virus also infects human lymphocytes. In contrast to measles virus infection of resting lymphocytes in which viral antigen is rarely expressed, influenza virus infection of these cells yields viral antigens expressed in the cytoplasm and on the cell surface. Influenza virus-infected lymphocytes have normal NK cell activity but fail to synthesize IgG or IgM.

Full Text

The Full Text of this article is available as a PDF (994.8 KB).

Selected References

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

  1. BECH V. Measles epidemics in Greenland. Am J Dis Child. 1962 Mar;103:252–253. doi: 10.1001/archpedi.1962.02080020264013. [DOI] [PubMed] [Google Scholar]
  2. BRODY J. A., MCALISTER R. DEPRESSION OF TUBERCULIN SENSITIVITY FOLLOWING MEASLES VACCINATION. Am Rev Respir Dis. 1964 Oct;90:607–611. doi: 10.1164/arrd.1964.90.4.607. [DOI] [PubMed] [Google Scholar]
  3. Bloom B. R., Senik A., Stoner G., Ju G., Nowakowski M., Kano S., Jimenez L. Studies on the interactions between viruses and lymphocytes. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):73–83. doi: 10.1101/sqb.1977.041.01.011. [DOI] [PubMed] [Google Scholar]
  4. Borysiewicz L. K., Morris S., Page J. D., Sissons J. G. Human cytomegalovirus-specific cytotoxic T lymphocytes: requirements for in vitro generation and specificity. Eur J Immunol. 1983 Oct;13(10):804–809. doi: 10.1002/eji.1830131005. [DOI] [PubMed] [Google Scholar]
  5. Casali P., Sissons J. G., Buchmeier M. J., Oldstone M. B. In vitro generation of human cytotoxic lymphocytes by virus. Viral glycoproteins induce nonspecific cell-mediated cytotoxicity without release of interferon. J Exp Med. 1981 Sep 1;154(3):840–855. doi: 10.1084/jem.154.3.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casali P., Sissons J. G., Fujinami R. S., Oldstone M. B. Purification of measles virus glycoproteins and their integration into artificial lipid membranes. J Gen Virol. 1981 May;54(Pt 1):161–171. doi: 10.1099/0022-1317-54-1-161. [DOI] [PubMed] [Google Scholar]
  7. Dahl H. A micro assay for mouse and human interferon. II. Dose-response in different in cell-virus systems. Acta Pathol Microbiol Scand B Microbiol Immunol. 1973 Jun;81(3):359–364. [PubMed] [Google Scholar]
  8. Finkel A., Dent P. B. Abnormalities in lymphocyte proliferation in classical and atypical measles infection. Cell Immunol. 1973 Jan;6(1):41–48. doi: 10.1016/0008-8749(73)90004-x. [DOI] [PubMed] [Google Scholar]
  9. Fireman P., Friday G., Kumate J. Effect of measles vaccine on immunologic responsiveness. Pediatrics. 1969 Feb;43(2):264–272. [PubMed] [Google Scholar]
  10. Fireman P., Friday G., Kumate J. Effect of measles vaccine on immunologic responsiveness. Pediatrics. 1969 Feb;43(2):264–272. [PubMed] [Google Scholar]
  11. Galama J. M., Ubels-Postma J., Vos A., Lucas C. J. Measles virus inhibits acquisition of lymphocyte functions but not established effector functions. Cell Immunol. 1980 Mar 15;50(2):405–415. doi: 10.1016/0008-8749(80)90294-4. [DOI] [PubMed] [Google Scholar]
  12. Hirsch R. L., Mokhtarian F., Griffin D. E., Brooks B. R., Hess J., Johnson R. T. Measles virus vaccination of measles seropositive individuals suppresses lymphocyte proliferation and chemotactic factor production. Clin Immunol Immunopathol. 1981 Dec;21(3):341–350. doi: 10.1016/0090-1229(81)90223-3. [DOI] [PubMed] [Google Scholar]
  13. Horta-Barbosa L., Hamilton R., Wittig B., Fuccillo D. A., Sever J. L., Vernon M. L. Subacute sclerosing panencephalitis: isolation of suppressed measles virus from lymph node biopsies. Science. 1971 Aug 27;173(3999):840–841. doi: 10.1126/science.173.3999.840. [DOI] [PubMed] [Google Scholar]
  14. Huddlestone J. R., Lampert P. W., Oldstone M. B. Virus-lymphocyte interactions: infection of Tg and Tm subsets by measles virus. Clin Immunol Immunopathol. 1980 Mar;15(3):502–509. doi: 10.1016/0090-1229(80)90062-8. [DOI] [PubMed] [Google Scholar]
  15. Härfast B., Huddlestone J. R., Casali P., Merigan T. C., Oldstone M. B. Interferon acts directly on human B lymphocytes to modulate immunoglobulin synthesis. J Immunol. 1981 Nov;127(5):2146–2150. [PubMed] [Google Scholar]
  16. Jacobson S., McFarland H. F. Measles virus persistence in human lymphocytes: a role for virus-induced interferon. J Gen Virol. 1982 Dec;63(2):351–357. doi: 10.1099/0022-1317-63-2-351. [DOI] [PubMed] [Google Scholar]
  17. Joseph B. S., Lampert P. W., Oldstone M. B. Replication and persistence of measles virus in defined subpopulations of human leukocytes. J Virol. 1975 Dec;16(6):1638–1649. doi: 10.1128/jvi.16.6.1638-1649.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kantor F. S. Infection, anergy and cell-mediated immunity. N Engl J Med. 1975 Mar 20;292(12):629–634. doi: 10.1056/NEJM197503202921210. [DOI] [PubMed] [Google Scholar]
  19. MELLMAN W. J., WETTON R. Depression of the tuberculin reaction by attenuated measles virus vaccine. J Lab Clin Med. 1963 Mar;61:453–458. [PubMed] [Google Scholar]
  20. Notkins A. L., Mergenhagen S. E., Howard R. J. Effect of virus infections on the function of the immune system. Annu Rev Microbiol. 1970;24:525–538. doi: 10.1146/annurev.mi.24.100170.002521. [DOI] [PubMed] [Google Scholar]
  21. Oldstone M. B., Fujinami R. S., Tishon A., Finney D., Powell H. C., Lampert P. W. Mapping of the major histocompatibility complex and viral antigens on the plasma membrane of a measles virus-infected cell. Virology. 1983 Jun;127(2):426–437. doi: 10.1016/0042-6822(83)90155-1. [DOI] [PubMed] [Google Scholar]
  22. Oldstone M. B., Sinha Y. N., Blount P., Tishon A., Rodriguez M., von Wedel R., Lampert P. W. Virus-induced alterations in homeostasis: alteration in differentiated functions of infected cells in vivo. Science. 1982 Dec 10;218(4577):1125–1127. doi: 10.1126/science.7146898. [DOI] [PubMed] [Google Scholar]
  23. Osunkoya B. O., Cooke A. R., Ayeni O., Adejumo T. A. Studies on leukocyte cultures in measles. I. Lymphocyte transformation and giant cell formation in leukocyte cultures from clinical cases of measles. Arch Gesamte Virusforsch. 1974;44(4):313–322. [PubMed] [Google Scholar]
  24. Pelton B. K., Imrie R. C., Denman A. M. Susceptibility of human lymphocyte populations to infection by herpes simplex virus. Immunology. 1977 May;32(5):803–810. [PMC free article] [PubMed] [Google Scholar]
  25. Perussia B., Starr S., Abraham S., Fanning V., Trinchieri G. Human natural killer cells analyzed by B73.1, a monoclonal antibody blocking Fc receptor functions. I. Characterization of the lymphocyte subset reactive with B73.1. J Immunol. 1983 May;130(5):2133–2141. [PubMed] [Google Scholar]
  26. Rice G. P., Casali P., Oldstone M. B. A new solid-phase enzyme-linked immunosorbent assay for specific antibodies to measles virus. J Infect Dis. 1983 Jun;147(6):1055–1059. doi: 10.1093/infdis/147.6.1055. [DOI] [PubMed] [Google Scholar]
  27. Robbins S. J., Wrzos H., Kline A. L., Tenser R. B., Rapp F. Rescue of a cytopathic paramyxovirus from peripheral blood leukocytes in subacute sclerosing panencephalitis. J Infect Dis. 1981 Mar;143(3):396–403. doi: 10.1093/infdis/143.3.396. [DOI] [PubMed] [Google Scholar]
  28. STARR S., BERKOVICH S. EFFECTS OF MEASLES, GAMMA-GLOBULIN-MODIFIED MEASLES AND VACCINE MEASLES ON THE TUBERCULIN TEST. N Engl J Med. 1964 Feb 20;270:386–391. doi: 10.1056/NEJM196402202700802. [DOI] [PubMed] [Google Scholar]
  29. Sullivan J. L., Barry D. W., Lucas S. J., Albrecht P. Measles infection of human mononuclear cells. I. Acute infection of peripheral blood lymphocytes and monocytes. J Exp Med. 1975 Sep 1;142(3):773–784. doi: 10.1084/jem.142.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Valdirmarsson H., Agnarsdottir G., Lachmann P. J. Measles virus receptor on human T lymphocytes. Nature. 1975 Jun 12;255(5509):554–556. doi: 10.1038/255554a0. [DOI] [PubMed] [Google Scholar]
  31. Wheelock E. F., Toy S. T. Participation of lymphocytes in viral infections. Adv Immunol. 1973;16:123–184. doi: 10.1016/s0065-2776(08)60297-7. [DOI] [PubMed] [Google Scholar]
  32. White R. G., Boyd J. F. The effect of measles on the thymus and other lymphoid tissues. Clin Exp Immunol. 1973 Mar;13(3):343–357. [PMC free article] [PubMed] [Google Scholar]
  33. Whittle H. C., Bradley-Moore A., Fleming A., Greenwood B. M. Effects of measles on the immune response of Nigerian children. Arch Dis Child. 1973 Oct;48(10):753–756. doi: 10.1136/adc.48.10.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Whittle H. C., Dossetor J., Oduloju A., Bryceson A. D., Greenwood B. M. Cell-mediated immunity during natural measles infection. J Clin Invest. 1978 Sep;62(3):678–684. doi: 10.1172/JCI109175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wilson A. B., Planterose D. N., Nagington J., Park J. R., Barry R. D., Coombs R. R. Influenza A antigens on human lymphocytes in vitro and probably in vivo. Nature. 1976 Feb 19;259(5544):582–584. doi: 10.1038/259582a0. [DOI] [PubMed] [Google Scholar]
  36. Woodruff J. F., Woodruff J. J. T lymphocyte interaction with viruses and virus-infected tissues. Prog Med Virol. 1975;19:120–160. [PubMed] [Google Scholar]
  37. Wrzos H., Kulczycki J., Laskowski Z., Matacz D., Brzosko W. J. Detection of measles virus antigen(s) in peripheral lymphocytes from patients with subacute sclerosing panencephalitis. Arch Virol. 1979;60(3-4):291–297. doi: 10.1007/BF01317500. [DOI] [PubMed] [Google Scholar]
  38. Zweiman B., Pappagianis D., Maibach H., Hildreth E. A. Effect of measles immunization on tuberculin hypersensitivity and in vitro lymphocyte reactivity. Int Arch Allergy Appl Immunol. 1971;40(6):834–841. doi: 10.1159/000230466. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES