Transient IFN-γ synthesis in the lymph node draining a dermal site loaded with UV-irradiated herpes simplex virus type 1: an NK- and CD3-dependent process regulated by IL-12 but not by IFN-α/β Free

Abstract

Our previous studies have shown that UV-inactivated, non-replicating herpes simplex virus type 1 (UV-HSV-1) triggers early and transient synthesis of IFN-α/β in the mouse regional lymph node when delivered upstream (i.e. in the ear dermis). In this study, it is demonstrated, by use of a quantitative RT–PCR readout assay, that IFN-γ mRNA expression was rapidly and transiently upregulated in draining lymph nodes when UV-HSV-1 was delivered in the ear dermis of C57Bl/6 mice. An increased number of IFN-γ-producing cells was also detected in the lymph node by flow cytometric analysis. Two different subsets of cells, namely DX5 NK cells and CD3ϵ T cells, accounted for this early IFN-γ synthesis. Prompt upregulation of IFN-α and IL-12p40 mRNA was also recorded. We took advantage of IFN-α/β-receptor knockout and wild-type 129 mice to study a potential role of IFN-α/β in the signalling pathway leading to IFN-γ transcription/translation. IFN-γ mRNA upregulation still occurred in IFN-α/β-receptor mice, showing that IFN-α/β was dispensable. The use of IL-12-neutralizing antibodies, prior to UV-HSV-1 delivery, confirmed the major role played by IL-12 in the early/transient IFN-γ burst.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-10-2365
2000-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/10/0812365a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-10-2365&mimeType=html&fmt=ahah

References

  1. Ankel H., Capobianchi M. R., Castilletti C., Dianzani F. 1994; Interferon induction by HIV glycoprotein 120: role of the V3 loop. Virology 205:34–43
    [Google Scholar]
  2. Ankel H., Westra D. F., Welling-Wester S., Lebon P. 1998; Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology 251:317–326
    [Google Scholar]
  3. Baudoux P., Carrat C., Besnardeau L., Charley B., Laude H. 1998; Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. Journal of Virology 72:8636–8643
    [Google Scholar]
  4. Belardelli F., Gresser I. 1996; The neglected role of type I interferon in the T-cell response: implications for its clinical use. Immunology Today 17:369–372
    [Google Scholar]
  5. Belkaid Y., Jouin H., Milon G. 1996; A method to recover, enumerate and identify lymphomyeloid cells present in an inflammatory dermal site: a study in laboratory mice. Journal of Immunological Methods 199:5–25
    [Google Scholar]
  6. Biron C. A. 1998; Role of early cytokines, including α and β interferons (IFN-α/β), in innate and adaptive immune responses to viral infections. Seminars in Immunology 10:383–390
    [Google Scholar]
  7. 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. Annual Review of Immunology 17:189–220
    [Google Scholar]
  8. 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 Medicine 5:919–923
    [Google Scholar]
  9. Chomczynski P., Sacchi N. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162:156–159
    [Google Scholar]
  10. Colle J. H., Falanga P. B., Singer M., Hevin B., Milon G. 1997; Quantitation of messenger RNA by competitive RT–PCR: a simplified read out assay. Journal of Immunological Methods 210:175–184
    [Google Scholar]
  11. Cousens L. P., Orange J. S., Su H. C., Biron C. A. 1997; Interferon-α/β inhibition of interleukin 12 and interferon-γ production in vitro and endogenously during viral infection. Proceedings of the National Academy of Sciences, USA 94:634–639
    [Google Scholar]
  12. Cyster J. G. 1999; Chemokines and cell migration in secondary lymphoid organs. Science 286:2098–2102
    [Google Scholar]
  13. Dutton R. W., Bradley L. M., Swain S. L. 1998; T cell memory. Annual Review of Immunology 16:201–223
    [Google Scholar]
  14. Fitzgerald-Bocarsly P. 1993; Human natural interferon-alpha producing cells. Pharmacology and Therapeutics 60:39–62
    [Google Scholar]
  15. Girard J. P., Springer T. A. 1995; High endothelial venules (HEVs): specialized endothelium for lymphocyte migration. Immunology Today 16:449–457
    [Google Scholar]
  16. Gresser I., Guy-Grand D., Maury C., Maunoury M. T. 1981; Interferon induces peripheral lymphadenopathy in mice. Journal of Immunology 127:1569–1575
    [Google Scholar]
  17. Hussell T., Openshaw P. J. M. 1998; Intracellular IFN-γ expression in natural killer cells precedes lung CD8+ T cell recruitment during respiratory syncytial virus infection. Journal of General Virology 79:2593–2601
    [Google Scholar]
  18. Ishikawa R., Biron C. A. 1993; IFN induction and associated changes in splenic leukocyte distribution. Journal of Immunology 150:3713–3727
    [Google Scholar]
  19. Ito Y., Bando H., Komada H., Tsurudome M., Nishio M., Kawano M., Matsumura H., Kusagawa S., Yuasa T., Ohta H., Ikemura M., Watanabe N. 1994; HN proteins of human parainfluenza type 4A virus expressed in cell lines transfected with a cloned cDNA have an ability to induce interferon in mouse spleen cells. Journal of General Virology 75:567–572
    [Google Scholar]
  20. Korngold R., Blank K. J., Murasko D. M. 1983; Effect of interferon on thoracic duct lymphocyte output: induction with either poly I: poly C or vaccinia virus. Journal of Immunology 130:2236–2240
    [Google Scholar]
  21. Kraal G., Mebius R. E. 1997; High endothelial venules: lymphocyte traffic control and controlled traffic. Advances in Immunology 65:347–395
    [Google Scholar]
  22. Leib D. A., Harrison T. E., Laslo K. M., Machalek M. A., Moorman N. J., Virgin H. W. 1999; Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. Journal of Experimental Medicine 189:663–672
    [Google Scholar]
  23. Milone M. C., Fitzgerald-Bocarsly P. 1998; The mannose receptor mediates induction of IFN-alpha in peripheral blood dendritic cells by enveloped RNA and DNA viruses. Journal of Immunology 161:2391–2399
    [Google Scholar]
  24. 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. Science 264:1918–1921
    [Google Scholar]
  25. Orange J. S., Biron C. A. 1996; Characterization of early IL-12, IFN-αβ, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. Journal of Immunology 156:4746–4756
    [Google Scholar]
  26. Riffault S., Eloranta M. L., Carrat C., Sandberg K., Charley B., Alm G. 1996; Herpes simplex virus induces appearance of interferon-α/β-producing cells and partially interferon-α/β-dependent accumulation of leukocytes in murine regional lymph nodes. Journal of Interferon and Cytokine Research 16:1007–1014
    [Google Scholar]
  27. Romani L., Mencacci A., Cenci E., Spaccapelo R., Del Sero G., Nicoletti I., Trinchieri G., Bistoni F., Puccetti P. 1997; Neutrophil production of IL-12 and IL-10 in candidiasis and efficacy of IL-12 therapy in neutropenic mice. Journal of Immunology 158:5349–5356
    [Google Scholar]
  28. Salazar-Mather T. P., Ishikawa R., Biron C. A. 1996; NK cell trafficking and cytokine expression in splenic compartments after IFN induction and viral infection. Journal of Immunology 157:3054–3064
    [Google Scholar]
  29. Salomon B., Cohen J. L., Masurier C., Klatzmann D. 1998; Three populations of mouse lymph node dendritic cells with different origins and dynamics. Journal of Immunology 160:708–717
    [Google Scholar]
  30. Sareneva T., Matikainen S., Kurimoto M., Julkunen I. 1998; Influenza A virus-induced IFN-α/β and IL-18 synergistically enhance IFN-γ gene expression in human T cells. Journal of Immunology 160:6032–6038
    [Google Scholar]
  31. 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. Science 284:1835–1837
    [Google Scholar]
  32. Sinigaglia F., D’Ambrosio D., Panina-Bordignon P., Rogge L. 1999; Regulation of the IL-12/IL-12R axis: a critical step in T-helper cell differentiation and effector function. Immunological Review 170:65–72
    [Google Scholar]
  33. Slifka M. K., Pagarigan R. R., Whitton J. L. 2000; NK markers are expressed on a high percentage of virus-specific CD8+ and CD4+ T cells. Journal of Immunology 164:2009–2015
    [Google Scholar]
  34. Svensson H., Johannisson A., Nikkila T., Alm G. V., Cederblad B. 1996; The cell surface phenotype of human natural interferon-α producing cells as determined by flow cytometry. Scandinavian Journal of Immunology 44:164–172
    [Google Scholar]
  35. Tough D. F., Borrow P., Sprent J. 1996; Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 272:1947–1950
    [Google Scholar]
  36. van den Broek M. F., Muller U., Huang S., Zinkernagel R. M., Aguet M. 1995; Immune defence in mice lacking type I and/or type II interferon receptors. Immunological Review 148:5–18
    [Google Scholar]
  37. van der Korput J. A. G. M., Hilkens J., Kroezen V., Zwarthoff E. C., Trapman J. 1985; Mouse interferon alpha and beta genes are linked at the centromere proximal region of chromosome 4. Journal of General Virology 66:493–502
    [Google Scholar]
  38. Vilček J., Sen G. C. 1996; Interferons and other cytokines. In Fundamental Virology pp 341–365 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  39. Wysocka M., Kubin M., Vieira L. Q., Ozmen L., Garotta G., Scott P., Trinchieri G. 1995; Interleukin-12 is required for interferon-γ production and lethality in lipopolysaccharide-induced shock in mice. European Journal of Immunology 25:672–676
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-10-2365
Loading
/content/journal/jgv/10.1099/0022-1317-81-10-2365
Loading

Data & Media loading...

Most cited Most Cited RSS feed