Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1982 Aug;37(2):794–799. doi: 10.1128/iai.37.2.794-799.1982

Influenza A virus-induced polymorphonuclear leukocyte dysfunction.

J S Abramson, D S Lyles, K A Heller, D A Bass
PMCID: PMC347599  PMID: 7118256

Abstract

Previous studies have shown that influenza A virus can activate the polymorphonuclear leukocyte (PMN) respiratory burst and that upon subsequent stimulation of the cell there is depressed metabolic function. We examined the mechanism by which influenza virus causes PMN dysfunction by measuring the effect upon the chemiluminescent activity of cells of varying the type of influenza virus used, the period of time that cells were exposed to virus, and the secondary stimulus that was used. The various types of intact influenza virus elicited different amounts of chemiluminescent activity, but when cells were subsequently stimulated with phorbol myristate acetate, each virus caused equivalent depression of the PMN response. Purified glycoproteins incorporated into a liposome structure similarly stimulated the PMN chemiluminescence, yet did not induce PMN dysfunction. Depressed PMN function was noted after as little as 5 min of incubation of cells with virus and occurred to both receptor-dependent (zymosan, N-formylmethionyl-leucyl-phenylalanine, and phorbol myristate acetate) and -independent (calcium ionophore A23187) stimuli.

Full text

PDF
794

Images in this article

Selected References

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

  1. Abramson J. S., Giebink G. S., Mills E. L., Quie P. G. Polymorphonuclear leukocyte dysfunction during influenza virus infection in chinchillas. J Infect Dis. 1981 Jun;143(6):836–845. doi: 10.1093/infdis/143.6.836. [DOI] [PubMed] [Google Scholar]
  2. Abramson J. S., Mills E. L., Giebink G. S., Quie P. G. Depression of monocyte and polymorphonuclear leukocyte oxidative metabolism and bactericidal capacity by influenza A virus. Infect Immun. 1982 Jan;35(1):350–355. doi: 10.1128/iai.35.1.350-355.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allen R. C., Loose L. D. Phagocytic activation of a luminol-dependent chemiluminescence in rabbit alveolar and peritoneal macrophages. Biochem Biophys Res Commun. 1976 Mar 8;69(1):245–252. doi: 10.1016/s0006-291x(76)80299-9. [DOI] [PubMed] [Google Scholar]
  4. Allen R. C., Stjernholm R. L., Steele R. H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972 May 26;47(4):679–684. doi: 10.1016/0006-291x(72)90545-1. [DOI] [PubMed] [Google Scholar]
  5. Badwey J. A., Karnovsky M. L. Active oxygen species and the functions of phagocytic leukocytes. Annu Rev Biochem. 1980;49:695–726. doi: 10.1146/annurev.bi.49.070180.003403. [DOI] [PubMed] [Google Scholar]
  6. Busse W. W., Sosman J. M. Altered luminol-dependent granulocyte chemiluminescence during an in vitro incubation with an influenza vaccine. Am Rev Respir Dis. 1981 Jun;123(6):654–658. doi: 10.1164/arrd.1981.123.6.654. [DOI] [PubMed] [Google Scholar]
  7. Case G. D., Vanderkooi J. M., Scarpa A. Physical properties of biological membranes determined by the fluorescence of the calcium ionophore A23187. Arch Biochem Biophys. 1974 May;162(1):174–185. doi: 10.1016/0003-9861(74)90116-7. [DOI] [PubMed] [Google Scholar]
  8. Craft A. W., Reid M. M., Low W. T. Effect of virus infections on polymorph function in children. Br Med J. 1976 Jun 26;1(6025):1570–1570. doi: 10.1136/bmj.1.6025.1570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dourmashkin R. R., Tyrrell D. A. Electron microscopic observations on the entry of influenza virus into susceptible cells. J Gen Virol. 1974 Jul;24(1):129–141. doi: 10.1099/0022-1317-24-1-129. [DOI] [PubMed] [Google Scholar]
  10. Fischer J. J., Walker D. H. Invasive pulmonary aspergillosis associated with influenza. JAMA. 1979 Apr 6;241(14):1493–1494. [PubMed] [Google Scholar]
  11. HERS J. F., GOSLINGS W. R., MASUREL N., MULDER J. Death from Asiatic influenza in the Netherlands. Lancet. 1957 Dec 7;273(7006):1164–1165. doi: 10.1016/s0140-6736(57)92066-4. [DOI] [PubMed] [Google Scholar]
  12. Howe C., Lee L. T. Virus-erythrocyte interactions. Adv Virus Res. 1972;17:1–50. doi: 10.1016/S0065-3527(08)60746-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huang R. T., Rott R., Wahn K., Klenk H. D., Kohama T. The function of the neuraminidase in membrane fusion induced by myxoviruses. Virology. 1980 Dec;107(2):313–319. doi: 10.1016/0042-6822(80)90299-8. [DOI] [PubMed] [Google Scholar]
  14. Kleinerman E. S., Snyderman R., Daniels C. A. Depressed monocyte chemotaxis during acute influenza infection. Lancet. 1975 Nov 29;2(7944):1063–1066. doi: 10.1016/s0140-6736(75)90432-8. [DOI] [PubMed] [Google Scholar]
  15. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  16. Larson H. E., Parry R. P., Tyrrell D. A. Impaired polymorphonuclear leucocyte chemotaxis after influenza virus infection. Br J Dis Chest. 1980 Jan;74(1):56–62. [PubMed] [Google Scholar]
  17. Lehrer R. I., Cohen L. Receptor-mediated regulation of superoxide production in human neutrophils stimulated by phorbol myristate acetate. J Clin Invest. 1981 Nov;68(5):1314–1320. doi: 10.1172/JCI110378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Loosli C. G. Influenza and the interaction of viruses and bacteria in respiratory infections. Medicine (Baltimore) 1973 Sep;52(5):369–384. doi: 10.1097/00005792-197309000-00001. [DOI] [PubMed] [Google Scholar]
  19. Martin R. R., Couch R. B., Greenberg S. B., Cate T. R., Warr G. A. Effects of infection with influenza virus on the function of polymorphonuclear leukocytes. J Infect Dis. 1981 Sep;144(3):279–280. doi: 10.1093/infdis/144.3.279. [DOI] [PubMed] [Google Scholar]
  20. Mills E. L., Debets-Ossenkopp Y., Verbrugh H. A., Verhoef J. Initiation of the respiratory burst of human neutrophils by influenza virus. Infect Immun. 1981 Jun;32(3):1200–1205. doi: 10.1128/iai.32.3.1200-1205.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mills E. L., Rholl K. S., Quie P. G. Luminol-amplified chemiluminescence: a sensitive method for detecting the carrier state in chronic granulomatous disease. J Clin Microbiol. 1980 Jul;12(1):52–56. doi: 10.1128/jcm.12.1.52-56.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nelson R. D., Mills E. L., Simmons R. L., Quie P. G. Chemiluminescence response of phagocytizing human monocytes. Infect Immun. 1976 Jul;14(1):129–134. doi: 10.1128/iai.14.1.129-134.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oliver J. M. Cell biology of leukocyte abnormalities--membrane and cytoskeletal function in normal and defective cells. A review. Am J Pathol. 1978 Oct;93(1):221–270. [PMC free article] [PubMed] [Google Scholar]
  24. Oxford J. S., McGeoch D. J., Schild G. C., Beare A. S. Analysis of virion RNA segments and polypeptides of influenza A virus recombinants of defined virulence. Nature. 1978 Jun 29;273(5665):778–779. doi: 10.1038/273778a0. [DOI] [PubMed] [Google Scholar]
  25. Rosen H., Klebanoff S. J. Chemiluminescence and superoxide production by myeloperoxidase-deficient leukocytes. J Clin Invest. 1976 Jul;58(1):50–60. doi: 10.1172/JCI108458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ruutu T., Kosunen T. U. Phagocytic activity of neutrophilic leukocytes of A2 influenza patients. Acta Pathol Microbiol Scand B Microbiol Immunol. 1971;79(1):67–72. doi: 10.1111/j.1699-0463.1971.tb00034.x. [DOI] [PubMed] [Google Scholar]
  27. Sawyer W. D. Interaction of influenza virus with leukocytes and its effect on phagocytosis. J Infect Dis. 1969 Jun;119(6):541–556. doi: 10.1093/infdis/119.6.541. [DOI] [PubMed] [Google Scholar]
  28. Scheid A., Choppin P. W. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology. 1974 Feb;57(2):475–490. doi: 10.1016/0042-6822(74)90187-1. [DOI] [PubMed] [Google Scholar]
  29. Schell-Frederick E. Stimulation of the oxidative metabolism of polymorphonuclear leucocytes by the calcium ionophore A23187. FEBS Lett. 1974 Nov 1;48(1):37–40. doi: 10.1016/0014-5793(74)81056-2. [DOI] [PubMed] [Google Scholar]
  30. Stevens P., Winston D. J., Van Dyke K. In vitro evaluation of opsonic and cellular granulocyte function by luminol-dependent chemiluminescence: utility in patients with severe neutropenia and cellular deficiency states. Infect Immun. 1978 Oct;22(1):41–51. doi: 10.1128/iai.22.1.41-51.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Taylor R. N., Dietz T. M., Maxwell K. W., Marcus S. Effect of influenza virus infection on phagocytic and cytopeptic capacities of guinea pig macrophages. Immunol Commun. 1974;3(5):439–455. doi: 10.3109/08820137409061124. [DOI] [PubMed] [Google Scholar]
  32. Van Epps D. E., Brown S. L. Inhibition of formylmethionyl-leucyl-phenylalanine-stimulated neutrophil chemiluminescence by human immunoglobulin A paraproteins. Infect Immun. 1981 Dec;34(3):864–870. doi: 10.1128/iai.34.3.864-870.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Voetman A. A., Weening R. S., Hamers M. N., Meerhof L. J., Bot A. A., Roos D. Phagocytosing human neutrophils inactivate their own granular enzymes. J Clin Invest. 1981 May;67(5):1541–1549. doi: 10.1172/JCI110185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Williams L. T., Snyderman R., Pike M. C., Lefkowitz R. J. Specific receptor sites for chemotactic peptides on human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1204–1208. doi: 10.1073/pnas.74.3.1204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Young L. S., LaForce F. M., Head J. J., Feeley J. C., Bennett J. V. A simultaneous outbreak of meningococcal and influenza infections. N Engl J Med. 1972 Jul 6;287(1):5–9. doi: 10.1056/NEJM197207062870102. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES