1887

Abstract

Inactivated influenza A virus and fixed, virus-infected cells induce type 1 interferon (IFN-α/β) production in murine splenocytes. In this study, we have explored the nature of the virus–spleen cell interaction that leads to IFN-α/β induction and the reason for the poor response to some virus strains. IFN-α/β induction by horse serum-sensitive, but not -resistant, strains of influenza virus was inhibited in the presence of horse serum, indicating that binding of the virus to sialylated cell receptors is a necessary step in the induction process. Furthermore, influenza viruses A/PR/8/34 (H1N1) and A/WS/33 (H1N1), which were poor inducers of IFN-α/β in spleen cells, were shown to have a more active neuraminidase than strains that induced higher IFN levels, and IFN-α/β induction by A/PR/8/34 (H1N1) and A/WS/33 (H1N1) was restored in the presence of a neuraminidase inhibitor. Growth of virus in different cell types altered the level of IFN-α/β induced in spleen cells by particular virus strains, suggesting that the nature of the carbohydrate moieties on the viral glycoproteins may also influence IFN-α/β induction in this system. Consistent with this notion, treatment of egg-grown virus with periodate to oxidize viral carbohydrate greatly reduced its capacity for IFN-α/β induction. Furthermore, induction of IFN-α/β was inhibited in the presence of the saccharides yeast mannan and laminarin. Together these findings indicate: (i) a requirement for interaction of the virus with sialylated receptors on the IFN-producing cell; (ii) an influence of viral carbohydrate on the response; and (iii) possible involvement of a lectin-like receptor on the IFN-producing cell in the induction of IFN-α/β or in regulation of this response.

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2003-01-01
2020-09-27
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References

  1. Anders E. M., Scalzo A. A., Rogers G. N., White D. O.. 1986; Relationship between mitogenic activity of influenza viruses and the receptor-binding specificity of their hemagglutinin molecules. J Virol60:476–482
    [Google Scholar]
  2. Anders E. M., Hartley C. A., Jackson D. C.. 1990; Bovine and mouse serum β inhibitors of influenza A viruses are mannose-binding lectins. Proc Natl Acad Sci U S A87:4485–4489
    [Google Scholar]
  3. Anders E. M., Hartley C. A., Reading P. C., Ezekowitz R. A.. 1994; Complement-dependent neutralization of influenza virus by a serum mannose-binding lectin. J Gen Virol75:615–622
    [Google Scholar]
  4. Asselin-Paturel C., Boonstra A., Dalod M.. 8 other authors 2001; Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nature Immunol2:1144–1150
    [Google Scholar]
  5. Biron C. A., Nguyen K. B., Pien G. C., Cousens L. P., Salazar-Mather T. P.. 1999; Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol17:189–220
    [Google Scholar]
  6. Bjorck P.. 2001; Isolation and characterization of plasmacytoid dendritic cells from Flt3 ligand and granulocyte–macrophage colony-stimulating factor-treated mice. Blood98:3520–3526
    [Google Scholar]
  7. Bogdan C.. 2000; The function of type I interferons in antimicrobial immunity. Curr Opin Immunol12:419–424
    [Google Scholar]
  8. Caton A. J., Brownlee G. G., Yewdell J. W., Gerhard W.. 1982; The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell31:417–427
    [Google Scholar]
  9. Cella M., Jarrossay D., Facchetti F., Alebardi O., Nakajima H., Lanzavecchia A., Colonna M.. 1999; Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nature Med5:919–923
    [Google Scholar]
  10. Charley B., Laude H.. 1988; Induction of α interferon by transmissible gastroenteritis coronavirus: role of transmembrane glycoprotein E1. J Virol62:8–11
    [Google Scholar]
  11. Charley B., Lavenant L., Delmas B.. 1991; Glycosylation is required for coronavirus TGEV to induce an efficient production of IFNα by blood mononuclear cells. Scand J Immunol33:435–440
    [Google Scholar]
  12. Crecelius D. M., Deom C. M., Schulze I. T.. 1984; Biological properties of a hemagglutinin mutant of influenza virus selected by host cells. Virology139:164–177
    [Google Scholar]
  13. De Clercq E.. 1981; Interferon induction by polynucleotides, modified polynucleotides, and polycarboxylates. Methods Enzymol78:227–236
    [Google Scholar]
  14. Deom C. M., Schulze I. T.. 1985; Oligosaccharide composition of an influenza virus hemagglutinin with host-determined binding properties. J Biol Chem260:14771–14774
    [Google Scholar]
  15. Dzionek A., Sohma Y., Nagafune J.. 14 other authors 2001; BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon α/β induction. J Exp Med194:1823–1834
    [Google Scholar]
  16. Feldman S. B., Ferraro M., Zheng H. M., Patel N., Gould-Fogerite S., Fitzgerald-Bocarsly P.. 1994; Viral induction of low frequency interferon-α producing cells. Virology204:1–7
    [Google Scholar]
  17. Figdor C. G., van Kooyk Y., Adema G. J.. 2002; C-type lectin receptors on dendritic cells and Langerhans cells. Nature Rev Immunol2:77–84
    [Google Scholar]
  18. Fitzgerald-Bocarsly P.. 1993; Human natural interferon-α producing cells. Pharmacol & Ther60:39–62
    [Google Scholar]
  19. Gallucci S., Lolkema M., Matzinger P.. 1999; Natural adjuvants: endogenous activators of dendritic cells. Nature Med5:1249–1255
    [Google Scholar]
  20. Gambaryan A. S., Marinina V. P., Tuzikov A. B., Bovin N. V., Rudneva I. A., Sinitsyn B. V., Shilov A. A., Matrosovich M. N.. 1998; Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs. Virology247:170–177
    [Google Scholar]
  21. Geijtenbeek T. B., Kwon D. S., Torensma R.. 9 other authors 2000; DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell100:587–597
    [Google Scholar]
  22. Hemmi H., Takeuchi O., Kawai T.. 8 other authors 2000; A Toll-like receptor recognizes bacterial DNA. Nature408:740–745
    [Google Scholar]
  23. Hemmi H., Kaisho T., Takeuchi O.. 7 other authors 2002; Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nature Immunol3:196–200
    [Google Scholar]
  24. Isaacs A., Lindenmann J.. 1957; Virus interference. I. The interferon. Proc R Soc Lond Ser B Biol Sci147:258–268
    [Google Scholar]
  25. Ito Y.. 1994; Induction of interferon by virus glycoprotein(s) in lymphoid cells through interaction with the cellular receptors via lectin-like action: an alternative interferon induction mechanism. Arch Virol138:187–198
    [Google Scholar]
  26. Ito Y., Nishiyama Y., Shimokata K., Nagata I., Takeyama H., Kunii A.. 1978; The mechanism of interferon induction in mouse spleen cells stimulated with HVJ. Virology88:128–137
    [Google Scholar]
  27. Ito T., Amakawa R., Kaisho T.. 7 other authors 2002; Interferon-α and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J Exp Med195:1507–1512
    [Google Scholar]
  28. Jacobs B. L., Langland J. O.. 1996; When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology219:339–349
    [Google Scholar]
  29. Kadowaki N., Ho S., Antonenko S., Maleyft R. W., Kastelein R. A., Bazan F., Liu Y. J.. 2001; Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J Exp Med194:863–869
    [Google Scholar]
  30. Kaverin N. V., Webster R. G.. 1995; Impairment of multicycle influenza virus growth in Vero (WHO) cells by loss of trypsin activity. J Virol69:2700–2703
    [Google Scholar]
  31. Krug A., Rothenfusser S., Hornung V., Jahrsdorfer B., Blackwell S., Ballas Z. K., Endres S., Krieg A. M., Hartmann G.. 2001; Identification of CpG oligonucleotide sequences with high induction of IFN-α/β in plasmacytoid dendritic cells. Eur J Immunol31:2154–2163
    [Google Scholar]
  32. Laude H., Gelfi J., Lavenant L., Charley B.. 1992; Single amino acid changes in the viral glycoprotein M affect induction of α interferon by the coronavirus transmissible gastroenteritis virus. J Virol66:743–749
    [Google Scholar]
  33. Le Bon A., Schiavoni G., D'Agostino G., Gresser I., Belardelli F., Tough D. F.. 2001; Type 1 interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo . Immunity14:461–470
    [Google Scholar]
  34. Luft T., Pang K. C., Thomas E., Hertzog P., Hart D. N., Trapani J., Cebon J.. 1998; Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol161:1947–1953
    [Google Scholar]
  35. Markwell M. A., Portner A., Schwartz A. L.. 1985; An alternative route of infection for viruses: entry by means of the asialoglycoprotein receptor of a Sendai virus mutant lacking its attachment protein. Proc Natl Acad Sci U S A82:978–982
    [Google Scholar]
  36. Medzhitov R., Janeway C. Jr. 2000; Innate immune recognition: mechanisms and pathways. Immunol Rev173:89–97
    [Google Scholar]
  37. Mosmann T.. 1983; Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods65:55–63
    [Google Scholar]
  38. Muller U., Steinhoff U., Reis L. F., Hemmi S., Pavlovic J., Zinkernagel R. M., Aguet M.. 1994; Functional role of type I and type II interferons in antiviral defense. Science264:1918–1921
    [Google Scholar]
  39. Nakamura K., Compans R. W.. 1979; Host cell- and virus strain-dependent differences in oligosaccharides of hemagglutinin glycoproteins of influenza A viruses. Virology95:8–23
    [Google Scholar]
  40. Nakano H., Yanagita M., Gunn M. D.. 2001; CD11c+ B220+ Gr-1+ cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med194:1171–1178
    [Google Scholar]
  41. Nigou J., Zelle-Rieser C., Gilleron M., Thurnher M., Puzo G.. 2001; Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J Immunol166:7477–7485
    [Google Scholar]
  42. O'Keeffe M., Hochrein H., Vremec D.. 10 other authors 2002; Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8+ dendritic cells only after microbial stimulus. J Exp Med196:1307–1319
    [Google Scholar]
  43. Raymond F. L., Caton A. J., Cox N. J., Kendal A. P., Brownlee G. G.. 1983; Antigenicity and evolution amongst recent influenza viruses of H1N1 subtype. Nucleic Acids Res11:7191–7203
    [Google Scholar]
  44. Reading P. C., Morey L. S., Crouch E. C., Anders E. M.. 1997; Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J Virol71:8204–8212
    [Google Scholar]
  45. Reading P. C., Miller J. L., Anders E. M.. 2000; Involvement of the mannose receptor in infection of macrophages by influenza virus. J Virol74:5190–5197
    [Google Scholar]
  46. Rogers G. N., Pritchett T. J., Lane J. L., Paulson J. C.. 1983; Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology131:394–408
    [Google Scholar]
  47. Rudd P. M., Wormald M. R., Harvey D. J., Devasahayam M., McAlister M. S., Brown M. H., Davis S. J., Barclay A. N., Dwek R. A.. 1999; Oligosaccharide analysis and molecular modeling of soluble forms of glycoproteins belonging to the Ly-6, scavenger receptor, and immunoglobulin superfamilies expressed in Chinese hamster ovary cells. Glycobiology9:443–458
    [Google Scholar]
  48. Sawyer W.. 1969; Interaction of influenza virus with leukocytes and its effect on phagocytosis. J Infect Dis119:541–556
    [Google Scholar]
  49. Sedmak J. J., Grossberg S. E.. 1973; Comparative enzyme kinetics of influenza neuraminidases with the synthetic substrate methoxyphenylneuraminic acid. Virology56:658–661
    [Google Scholar]
  50. Siegal F. P., Kadowaki N., Shodell M., Fitzgerald-Bocarsly P. A., Shah K., Ho S., Antonenko S., Liu Y. J.. 1999; The nature of the principal type 1 interferon-producing cells in human blood. Science284:1835–1837
    [Google Scholar]
  51. Stray S. J., Cummings R. D., Air G. M.. 2000; Influenza virus infection of desialylated cells. Glycobiology10:649–658
    [Google Scholar]
  52. Takeda K., Akira S.. 2001; Roles of Toll-like receptors in innate immune responses. Genes Cells6:733–742
    [Google Scholar]
  53. Ward A. C., de Koning-Ward T. F.. 1995; Changes in the hemagglutinin gene of the neurovirulent influenza virus strain A/NWS/33. Virus Genes10:179–183
    [Google Scholar]
  54. Weis W., Brown J. H., Cusack S., Paulson J. C., Skehel J. J., Wiley D. C.. 1988; Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature333:426–431
    [Google Scholar]
  55. Wilson I. A., Skehel J. J., Wiley D. C.. 1981; Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature289:366–373
    [Google Scholar]
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