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. 1990 Aug;81(2):218–224. doi: 10.1111/j.1365-2249.1990.tb03321.x

Natural killer cell activity during measles.

D E Griffin 1, B J Ward 1, E Jauregui 1, R T Johnson 1, A Vaisberg 1
PMCID: PMC1535057  PMID: 1696863

Abstract

Natural killer cells are postulated to play an important role in host anti-viral defences. We measured natural killer cell activity in 30 individuals with acute measles (73 +/- 21 lytic units (LU)/10(7) cells) and 16 individuals with other infectious diseases (149 +/- 95 LU) and found it reduced compared with values for adults (375 +/- 70 LU; P less than 0.001) or children (300 +/- 73 LU, P less than 0.01) without infection. Reduced natural killer cell activity was found in measles patients with (84 +/- 30 LU) and without (55 +/- 18 LU) complications and was present for at least 3 weeks after the onset of the rash. Activity was increased by in vitro exposure of cells to interleukin-2. Depressed natural killer cell activity parallels in time the suppression of other parameters of cell-mediated immunity that occurs during measles.

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Selected References

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  1. Aaskov J. G., Fraser J. R., Dalglish D. A. Specific and non-specific immunological changes in epidemic polyarthritis patients. Aust J Exp Biol Med Sci. 1981 Oct;59(Pt 5):599–608. doi: 10.1038/icb.1981.52. [DOI] [PubMed] [Google Scholar]
  2. Beckford A. P., Kaschula R. O., Stephen C. Factors associated with fatal cases of measles. A retrospective autopsy study. S Afr Med J. 1985 Dec 7;68(12):858–863. [PubMed] [Google Scholar]
  3. Benczur M., Petrányl G. G., Pálffy G., Varga M., Tálas M., Kotsy B., Földes I., Hollán S. R. Dysfunction of natural killer cells in multiple sclerosis: a possible pathogenetic factor. Clin Exp Immunol. 1980 Mar;39(3):657–662. [PMC free article] [PubMed] [Google Scholar]
  4. Biron C. A., Welsh R. M. Activation and role of natural killer cells in virus infections. Med Microbiol Immunol. 1982;170(3):155–172. doi: 10.1007/BF02298196. [DOI] [PubMed] [Google Scholar]
  5. Bonavida B., Katz J., Gottlieb M. Mechanism of defective NK cell activity in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. I. Defective trigger on NK cells for NKCF production by target cells, and partial restoration by IL 2. J Immunol. 1986 Aug 15;137(4):1157–1163. [PubMed] [Google Scholar]
  6. Burke D. S., Morill J. C. Levels of interferon in the plasma and cerebrospinal fluid of patients with acute Japanese encephalitis. J Infect Dis. 1987 Apr;155(4):797–799. doi: 10.1093/infdis/155.4.797. [DOI] [PubMed] [Google Scholar]
  7. Caligiuri M., Murray C., Buchwald D., Levine H., Cheney P., Peterson D., Komaroff A. L., Ritz J. Phenotypic and functional deficiency of natural killer cells in patients with chronic fatigue syndrome. J Immunol. 1987 Nov 15;139(10):3306–3313. [PubMed] [Google Scholar]
  8. Casali P., Rice G. P., Oldstone M. B. Viruses disrupt functions of human lymphocytes. Effects of measles virus and influenza virus on lymphocyte-mediated killing and antibody production. J Exp Med. 1984 May 1;159(5):1322–1337. doi: 10.1084/jem.159.5.1322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Cauda R., Tyring S. K., Grossi C. E., Tilden A. B., Hatch K. D., Sams W. M., Jr, Baron S., Whitley R. J. Patients with condyloma acuminatum exhibit decreased interleukin-2 and interferon gamma production and depressed natural killer activity. J Clin Immunol. 1987 Jul;7(4):304–311. doi: 10.1007/BF00915552. [DOI] [PubMed] [Google Scholar]
  11. Dinarello C. A., Dempsey R. A., Allegretta M., LoPreste G., Dainiak N., Parkinson D. R., Mier J. W. Inhibitory effects of elevated temperature on human cytokine production and natural killer activity. Cancer Res. 1986 Dec;46(12 Pt 1):6236–6241. [PubMed] [Google Scholar]
  12. Domzig W., Stadler B. M., Herberman R. B. Interleukin 2 dependence of human natural killer (NK) cell activity. J Immunol. 1983 Apr;130(4):1970–1973. [PubMed] [Google Scholar]
  13. Ferbus D., Saavedra M. C., Levis S., Maiztegui J., Falcoff R. Relation of endogenous interferon and high levels of 2'-5' oligoadenylate synthetase in leukocytes from patients with Argentine hemorrhagic fever. J Infect Dis. 1988 May;157(5):1061–1064. doi: 10.1093/infdis/157.5.1061. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Fontana L., Sirianni M. C., de Sanctis G., Carbonari M., Ensoli B., Aiuti F. Deficiency of natural killer activity, but not of natural killer binding, in patients with lymphoadenopathy syndrome positive for antibodies to HTLV-III. Immunobiology. 1986 Jul;171(4-5):425–435. doi: 10.1016/S0171-2985(86)80074-2. [DOI] [PubMed] [Google Scholar]
  16. GRESSER I., CHANY C. Isolation of measles virus from the washed leucocytic fraction of blood. Proc Soc Exp Biol Med. 1963 Jul;113:695–698. doi: 10.3181/00379727-113-28465. [DOI] [PubMed] [Google Scholar]
  17. Garcia-Peñarrubia P., Koster F. T., Kelley R. O., McDowell T. D., Bankhurst A. D. Antibacterial activity of human natural killer cells. J Exp Med. 1989 Jan 1;169(1):99–113. doi: 10.1084/jem.169.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Godeny E. K., Gauntt C. J. Involvement of natural killer cells in coxsackievirus B3-induced murine myocarditis. J Immunol. 1986 Sep 1;137(5):1695–1702. [PubMed] [Google Scholar]
  19. Graves M., Griffin D. E., Johnson R. T., Hirsch R. L., de Soriano I. L., Roedenbeck S., Vaisberg A. Development of antibody to measles virus polypeptides during complicated and uncomplicated measles virus infections. J Virol. 1984 Feb;49(2):409–412. doi: 10.1128/jvi.49.2.409-412.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Griffin D. E., Hess J. L. Cells with natural killer activity in the cerebrospinal fluid of normal mice and athymic nude mice with acute Sindbis virus encephalitis. J Immunol. 1986 Mar 1;136(5):1841–1845. [PubMed] [Google Scholar]
  21. Griffin D. E., Johnson R. T., Tamashiro V. G., Moench T. R., Jauregui E., Lindo de Soriano I., Vaisberg A. In vitro studies of the role of monocytes in the immunosuppression associated with natural measles virus infections. Clin Immunol Immunopathol. 1987 Dec;45(3):375–383. doi: 10.1016/0090-1229(87)90090-0. [DOI] [PubMed] [Google Scholar]
  22. Griffin D. E., Moench T. R., Johnson R. T., Lindo de Soriano I., Vaisberg A. Peripheral blood mononuclear cells during natural measles virus infection: cell surface phenotypes and evidence for activation. Clin Immunol Immunopathol. 1986 Aug;40(2):305–312. doi: 10.1016/0090-1229(86)90035-8. [DOI] [PubMed] [Google Scholar]
  23. Griffin D. E., Ward B. J., Jauregui E., Johnson R. T., Vaisberg A. Immune activation in measles. N Engl J Med. 1989 Jun 22;320(25):1667–1672. doi: 10.1056/NEJM198906223202506. [DOI] [PubMed] [Google Scholar]
  24. Harris D. T., Cianciolo G. J., Snyderman R., Argov S., Koren H. S. Inhibition of human natural killer cell activity by a synthetic peptide homologous to a conserved region in the retroviral protein, p15E. J Immunol. 1987 Feb 1;138(3):889–894. [PubMed] [Google Scholar]
  25. Herberman R. B., Djeu J., Kay H. D., Ortaldo J. R., Riccardi C., Bonnard G. D., Holden H. T., Fagnani R., Santoni A., Puccetti P. Natural killer cells: characteristics and regulation of activity. Immunol Rev. 1979;44:43–70. doi: 10.1111/j.1600-065x.1979.tb00267.x. [DOI] [PubMed] [Google Scholar]
  26. Hirsch R. L., Griffin D. E., Johnson R. T., Cooper S. J., Lindo de Soriano I., Roedenbeck S., Vaisberg A. Cellular immune responses during complicated and uncomplicated measles virus infections of man. Clin Immunol Immunopathol. 1984 Apr;31(1):1–12. doi: 10.1016/0090-1229(84)90184-3. [DOI] [PubMed] [Google Scholar]
  27. Hirsch R. L., Johnson K. P. The effect of recombinant alpha 2-interferon on defective natural killer cell activity in multiple sclerosis. Neurology. 1985 Apr;35(4):597–600. doi: 10.1212/wnl.35.4.597. [DOI] [PubMed] [Google Scholar]
  28. Hirsch R. L. Natural killer cells appear to play no role in the recovery of mice from Sindbis virus infection. Immunology. 1981 May;43(1):81–89. [PMC free article] [PubMed] [Google Scholar]
  29. Joffe M. I., Rabson A. R. Defective helper factor (LMF) production in patients with acute measles infection. Clin Immunol Immunopathol. 1981 Aug;20(2):215–223. doi: 10.1016/0090-1229(81)90179-3. [DOI] [PubMed] [Google Scholar]
  30. Katz P., Zaytoun A. M., Lee J. H., Jr, Panush R. S., Longley S. Abnormal natural killer cell activity in systemic lupus erythematosus: an intrinsic defect in the lytic event. J Immunol. 1982 Nov;129(5):1966–1971. [PubMed] [Google Scholar]
  31. Katzman M., Lederman M. M. Defective postbinding lysis underlies the impaired natural killer activity in factor VIII-treated, human T lymphotropic virus type III seropositive hemophiliacs. J Clin Invest. 1986 Apr;77(4):1057–1062. doi: 10.1172/JCI112404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kibler R., Lucas D. O., Hicks M. J., Poulos B. T., Jones J. F. Immune function in chronic active Epstein-Barr virus infection. J Clin Immunol. 1985 Jan;5(1):46–54. doi: 10.1007/BF00915168. [DOI] [PubMed] [Google Scholar]
  33. Klein E., Ben-Bassat H., Neumann H., Ralph P., Zeuthen J., Polliack A., Vánky F. Properties of the K562 cell line, derived from a patient with chronic myeloid leukemia. Int J Cancer. 1976 Oct 15;18(4):421–431. doi: 10.1002/ijc.2910180405. [DOI] [PubMed] [Google Scholar]
  34. Klimpel G. R., Herndon D. N., Fons M., Albrecht T., Asuncion M. T., Chin R., Stein M. D. Defective NK cell activity following thermal injury. Clin Exp Immunol. 1986 Nov;66(2):384–392. [PMC free article] [PubMed] [Google Scholar]
  35. Kreth H. W., Wiegand G. Cell-mediated cytotoxicity against measles virus in SSPE. II. Analysis of cytotoxic effector cells. J Immunol. 1977 Jan;118(1):296–301. [PubMed] [Google Scholar]
  36. Kreth H. W., ter Meulen V., Eckert G. Demonstration of HLA restricted killer cells in patients with acute measles. Med Microbiol Immunol. 1979 Jan 24;165(4):203–214. doi: 10.1007/BF02152920. [DOI] [PubMed] [Google Scholar]
  37. Lang N. P., Ortaldo J. R., Bonnard G. D., Herberman R. B. Interferon and prostaglandins: effects on human natural and lectin-induced cytotoxicity. J Natl Cancer Inst. 1982 Aug;69(2):339–343. [PubMed] [Google Scholar]
  38. Levis S. C., Saavedra M. C., Ceccoli C., Falcoff E., Feuillade M. R., Enria D. A., Maiztegui J. I., Falcoff R. Endogenous interferon in Argentine hemorrhagic fever. J Infect Dis. 1984 Mar;149(3):428–433. doi: 10.1093/infdis/149.3.428. [DOI] [PubMed] [Google Scholar]
  39. Lieberman M. M., Ayala E. Active and passive immunity against Pseudomonas aeruginosa with a ribosomal vaccine and antiserum in C3H/HeJ mice. J Immunol. 1983 Jul;131(1):1–3. [PubMed] [Google Scholar]
  40. Luby J. P., Stewart W. E., 2nd, Sulkin S. E., Sanford J. P. Interferon in human infections with St. Louis encephalitis virus. Ann Intern Med. 1969 Oct;71(4):703–709. doi: 10.7326/0003-4819-71-4-703. [DOI] [PubMed] [Google Scholar]
  41. Moench T. R., Griffin D. E., Obriecht C. R., Vaisberg A. J., Johnson R. T. Acute measles in patients with and without neurological involvement: distribution of measles virus antigen and RNA. J Infect Dis. 1988 Aug;158(2):433–442. doi: 10.1093/infdis/158.2.433. [DOI] [PubMed] [Google Scholar]
  42. Morley D. Severe measles in the tropics. I. Br Med J. 1969 Feb 1;1(5639):297–contd. doi: 10.1136/bmj.1.5639.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Müller C., Schernthaner G., Kovarik J., Kalinowska W., Zielinski C. C. Natural killer cell activity and antibody-dependent cellular cytotoxicity in patients under various immunosuppressive regimens. Clin Immunol Immunopathol. 1987 Jul;44(1):12–19. doi: 10.1016/0090-1229(87)90047-x. [DOI] [PubMed] [Google Scholar]
  44. Natuk R. J., Welsh R. M. Accumulation and chemotaxis of natural killer/large granular lymphocytes at sites of virus replication. J Immunol. 1987 Feb 1;138(3):877–883. [PubMed] [Google Scholar]
  45. PETRALLI J. K., MERIGAN T. C., WILBUR J. R. CIRCULATING INTERFERON AFTER MEASLES VACCINATION. N Engl J Med. 1965 Jul 22;273:198–201. doi: 10.1056/NEJM196507222730405. [DOI] [PubMed] [Google Scholar]
  46. Pross H. F., Baines M. G. Studies of human natural killer cells. I. In vivo parameters affecting normal cytotoxic function. Int J Cancer. 1982 Apr 15;29(4):383–390. doi: 10.1002/ijc.2910290404. [DOI] [PubMed] [Google Scholar]
  47. Rager-Zisman B., Bloom B. R. Natural killer cells in resistance to virus-infected cells. Springer Semin Immunopathol. 1982;4(4):397–414. doi: 10.1007/BF02053741. [DOI] [PubMed] [Google Scholar]
  48. Rinaldo C. R., Jr, Ho M., Hamoudi W. H., Gui X. E., DeBiasio R. L. Lymphocyte subsets and natural killer cell responses during cytomegalovirus mononucleosis. Infect Immun. 1983 May;40(2):472–477. doi: 10.1128/iai.40.2.472-477.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Rook A. H., Kehrl J. H., Wakefield L. M., Roberts A. B., Sporn M. B., Burlington D. B., Lane H. C., Fauci A. S. Effects of transforming growth factor beta on the functions of natural killer cells: depressed cytolytic activity and blunting of interferon responsiveness. J Immunol. 1986 May 15;136(10):3916–3920. [PubMed] [Google Scholar]
  50. Shavit Y., Lewis J. W., Terman G. W., Gale R. P., Liebeskind J. C. Opioid peptides mediate the suppressive effect of stress on natural killer cell cytotoxicity. Science. 1984 Jan 13;223(4632):188–190. doi: 10.1126/science.6691146. [DOI] [PubMed] [Google Scholar]
  51. Shellam G. R., Allan J. E., Papadimitriou J. M., Bancroft G. J. Increased susceptibility to cytomegalovirus infection in beige mutant mice. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5104–5108. doi: 10.1073/pnas.78.8.5104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Shiozawa S., Yoshikawa N., Iijima K., Negishi K. A sensitive radioimmunoassay for circulating alpha-interferon in the plasma of healthy children and patients with measles virus infection. Clin Exp Immunol. 1988 Sep;73(3):366–369. [PMC free article] [PubMed] [Google Scholar]
  53. Sissons J. G., Colby S. D., Harrison W. O., Oldstone M. B. Cytotoxic lymphocytes generated in vivo with acute measles virus infection. Clin Immunol Immunopathol. 1985 Jan;34(1):60–68. doi: 10.1016/0090-1229(85)90007-8. [DOI] [PubMed] [Google Scholar]
  54. Sissons J. G., Oldstone M. B. Killing of virus-infected cells by cytotoxic lymphocytes. J Infect Dis. 1980 Jul;142(1):114–119. doi: 10.1093/infdis/142.1.114. [DOI] [PubMed] [Google Scholar]
  55. Steinhauer E. H., Doyle A. T., Reed J., Kadish A. S. Defective natural cytotoxicity in patients with cancer: normal number of effector cells but decreased recycling capacity in patients with advanced disease. J Immunol. 1982 Nov;129(5):2255–2259. [PubMed] [Google Scholar]
  56. Tamashiro V. G., Perez H. H., Griffin D. E. Prospective study of the magnitude and duration of changes in tuberculin reactivity during uncomplicated and complicated measles. Pediatr Infect Dis J. 1987 May;6(5):451–454. doi: 10.1097/00006454-198705000-00007. [DOI] [PubMed] [Google Scholar]
  57. Tilles J. G., Balkwill F., Davilla J. 2',5'-Oligoadenylate synthetase and interferon in peripheral blood after rubella, measles, or mumps live virus vaccine. Proc Soc Exp Biol Med. 1987 Oct;186(1):70–74. doi: 10.3181/00379727-186-42586. [DOI] [PubMed] [Google Scholar]
  58. 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]
  59. Volckaert-Vervliet G., Billiau A. Induction of interferon in human lymphoblastoid cells by Sendai and measles viruses. J Gen Virol. 1977 Oct;37(1):199–203. doi: 10.1099/0022-1317-37-1-199. [DOI] [PubMed] [Google Scholar]
  60. WHEELOCK E. F., SIBLEY W. A. CIRCULATING VIRUS, INTERFERON AND ANTIBODY AFTER VACCINATION WITH THE 17-D STRAIN OF YELLOW-FEVER VIRUS. N Engl J Med. 1965 Jul 22;273:194–198. doi: 10.1056/NEJM196507222730404. [DOI] [PubMed] [Google Scholar]
  61. Waltzer W. C., Bachvaroff R. J., Arnold A., Anaise D., Rapaport F. T. Immunological consequence of renal transplantation and immunosuppression. I. Alterations in human natural killer-cell activity. J Clin Immunol. 1985 Mar;5(2):78–83. doi: 10.1007/BF00915004. [DOI] [PubMed] [Google Scholar]
  62. West W. H., Cannon G. B., Kay H. D., Bonnard G. D., Herberman R. B. Natural cytotoxic reactivity of human lymphocytes against a myeloid cell line: characterization of effector cells. J Immunol. 1977 Jan;118(1):355–361. [PubMed] [Google Scholar]
  63. 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]
  64. Witter F., Barouki F., Griffin D., Nadler P., Woods A., Wood D., Lietman P. Biologic response (antiviral) to recombinant human interferon alpha 2a as a function of dose and route of administration in healthy volunteers. Clin Pharmacol Ther. 1987 Nov;42(5):567–575. doi: 10.1038/clpt.1987.198. [DOI] [PubMed] [Google Scholar]
  65. Yamanaka T., Chiba S., Nakao T. Application of microassay technique in cell-mediated immunity to measles virus infection. Tohoku J Exp Med. 1976 Nov;120(3):225–229. doi: 10.1620/tjem.120.225. [DOI] [PubMed] [Google Scholar]

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