1887

Abstract

High mobility group box 1 (HMGB1) protein functions in regulation of transcription, cellular activation and pro-inflammatory responses. However, the potential role of HMGB1 during viral infection has not been investigated. This study attempted to elucidate whether the HMGB1-mediated inflammatory response contributes to the pathogenesis of dengue virus (DENV) infection. Our data showed that HMGB1 was released at low DENV infection levels (m.o.i. of 1) under non-necrotic conditions by human dendritic cells (DCs). When DENV-infected DCs were co-cultured with autologous T cells, there was increased production of HMGB1 by both cell types. HMGB1 regulated tumour necrosis factor alpha, interleukin (IL)-6, IL-8 and alpha interferon secretion in DENV-infected DCs. Additionally, increased HMGB1 production was associated with reduced DENV replication titres in DCs. These results suggest that HMGB1 production influences DENV infection in susceptible hosts.

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2009-08-01
2024-03-28
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References

  1. Abraham E., Arcaroli J., Abraham E., Carmody A., Wang H., Tracey J. K. 2000; HMG-1 as a mediator of acute lung inflammation. J Immunol 165:2950–2954 [CrossRef]
    [Google Scholar]
  2. Andersson U., Wang H., Palmblad K., Aveberger A., Bloom O., Erlandsson-Harris H. 2000; High mobility group 1 protein (HMG-1) stimulates pro-inflammatory cytokine synthesis in human monocytes. J Exp Med 192:565–570 [CrossRef]
    [Google Scholar]
  3. Andersson U., Erlandsson-Harris H., Yang H., Tracey J. K. 2002; HMGB1 as a DNA-binding cytokine. J Leukoc Biol 72:1084–1091
    [Google Scholar]
  4. Avirutnan P., Malasit P., Seliger B., Bhakdi S., Husmann M. 1998; Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 161:6338–6346
    [Google Scholar]
  5. Bianchi M. E., Manfredi A. A. 2007; High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 220:35–46 [CrossRef]
    [Google Scholar]
  6. Chen G., Li J., Qiang X., Czura J. C., Ochani M., Ochani K., Ulloa L., Yang H., Tracey J. K. other authors 2005; Suppression of HMGB1 release by stearoyl lysophosphatidylcholine: an additional mechanism for its therapeutic effects in experimental sepsis. J Lipid Res 46:623–627 [CrossRef]
    [Google Scholar]
  7. Chen L. C., Yeh M. T., Wu N. H., Lin Y. Y., Shyu W. H. 2008; Dengue virus infection induces passive release of high mobility group box 1 protein by epithelial cells. J Infect 56:143–150 [CrossRef]
    [Google Scholar]
  8. Chu J. J., Ng L. M. 2003; The mechanism of cell death during West Nile virus infection is dependent on initial infectious dose. J Gen Virol 84:3305–3314 [CrossRef]
    [Google Scholar]
  9. Czura C. J., Tracey J. K. 2003; Targeting high mobility group box 1 as a late-acting mediator of inflammation. Crit Care Med 31:S46–S50 [CrossRef]
    [Google Scholar]
  10. Czura C. J., Wang H., Tracey J. K. 2001; Dual roles for HMGB1: DNA binding and cytokine. J Endotoxin Res 7:315–321
    [Google Scholar]
  11. Diamond M. S., Harris E. 2001; Interferon inhibits dengue virus infection by preventing translation of viral RNA through a PKR-independent mechanism. Virology 289:297–311 [CrossRef]
    [Google Scholar]
  12. Diamond M. S., Roberts G. T., Edgil D., Lu B., Ernst J., Harris E. 2000; Modulation of dengue virus infection in human cells by alpha, beta, and gamma interferons. J Virol 74:4957–4966 [CrossRef]
    [Google Scholar]
  13. Dumitriu I. E., Baruah P., Valentinis B., Voll E. R., Herrmann M., Nawroth P. P., Arnold B., Bianchi E. M., Manfredi A. A., Rovere-Querini P. 2005; Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 174:7506–7515 [CrossRef]
    [Google Scholar]
  14. El Mezayen R., El Gazzar M. E. R., Seeds C. M., McCall E. C., Dreskin C. S., Nicolls R. M. 2007; Endogenous signals released from necrotic cells augment inflammatory responses to bacterial endotoxin. Immunol Lett 111:36–44 [CrossRef]
    [Google Scholar]
  15. Fan X., Zhang Z. 1994; Increased tumor necrosis factor α production by neutrophils in patients with hepatitis B. J Clin Pathol 47:616–618 [CrossRef]
    [Google Scholar]
  16. Fan X. G., Liu E. W., Li C. Z., Wang C. Z., Luo X. L., Tan M. D., Hu L. G., Zhang Z. 1998; Circulating Th1 and Th2 cytokines in patients with hepatitis C virus infection. Mediators Inflamm 7:295–297 [CrossRef]
    [Google Scholar]
  17. Ho L. J., Wang J. J., Shaio F. M., Kao L. C., Chang M. D., Han W. S., Lai H. J. 2001; Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol 166:1499–1506 [CrossRef]
    [Google Scholar]
  18. Johnson A. J., Roehrig T. J. 1999; New mouse model for dengue virus vaccine testing. J Virol 73:783–786
    [Google Scholar]
  19. Joseph T., Cepica A., Brown L., Ikede B. B., Kibenge S. F. 2004; Mechanism of cell death during infectious salmon anemia virus infection is cell type-specific. J Gen Virol 85:3027–3036 [CrossRef]
    [Google Scholar]
  20. Julkunen I., Sareneva T., Pirhonen J., Ronni T., Melén K., Matikainen S. 2001; Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression. Cytokine Growth Factor Rev 12:171–180 [CrossRef]
    [Google Scholar]
  21. Kawahara K., Setoyama K., Kikuchi K., Biswas K. K., Kamimura R., Iwata M., Ito T., Morimoto Y., Hashiguchi T. other authors 2007; HMGB1 release in co-cultures of porcine endothelial and human T cells. Xenotransplantation 14:636–641 [CrossRef]
    [Google Scholar]
  22. Kurane I. 2007; Dengue hemorrhagic fever with special emphasis on immunopathogenesis. Comp Immunol Microbiol Infect Dis 30:329–340 [CrossRef]
    [Google Scholar]
  23. Kurane I., Innis L. B., Nimmannitya S., Nisalak A., Meager A., Ennis A. F. 1993; High levels of interferon alpha in the sera of children with dengue virus infection. Am J Trop Med Hyg 48:222–229
    [Google Scholar]
  24. Libraty D. H., Pichyangkul S., Ajariyakhajorn C., Endy P. T., Ennis A. F. 2001; Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis. J Virol 75:3501–3508 [CrossRef]
    [Google Scholar]
  25. Libraty D. H., Endy P. T., Houng S. H., Green S., Kalayanarooj S., Suntayakorn S., Chansiriwongs W., Vaughn W. D., Nisalak A. other authors 2002; Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 185:1213–1221 [CrossRef]
    [Google Scholar]
  26. Mantell L. L., Parrish R. W., Ulloa L. 2006; HMGB-1 as a therapeutic target for infectious and inflammatory disorders. Shock 25:4–11
    [Google Scholar]
  27. Messmer D., Yang H., Telusma G., Knoll F., Li J., Messmer B., Tracey J. K., Chiorazzi N. 2004; High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 173:307–313 [CrossRef]
    [Google Scholar]
  28. Miroslav C., Chazot P. L., Coleman S. K., Stephenson F. A. 1995; Using Promega's CytoTox 96 non-radioactive cytotoxicity assay to measure cell death mediated by NMDA receptor subunits. In Promega Notes Magazine 5121–23 Madison, WI: Promega;
    [Google Scholar]
  29. Mollica L., De Marchis F., Spitaleri A., Dallacosta C., Pennacchini D., Zamai M., Agresti A., Trisciuoglio L., Musco G., Bianchi M. E. 2007; Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities. Chem Biol 14:431–441 [CrossRef]
    [Google Scholar]
  30. Muller S., Scaffidi P., Degryse B., Bonaldi T., Ronfani L., Agresti A., Beltrame M., Bianchi E. M. 2001; New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 20:4337–4340 [CrossRef]
    [Google Scholar]
  31. Nightingale Z. D., Patkar C., Rothman L. A. 2008; Viral replication and paracrine effects result in distinct, functional responses of dendritic cells following infection with dengue 2 virus. J Leukoc Biol 84:1028–1038 [CrossRef]
    [Google Scholar]
  32. Nowak P., Barqasho B., Treutiger C. J., Harris H. E., Tracey K. J., Andersson J., Sönnerborg A. 2006; HMGB1 activates replication of latent HIV-1 in a monocytic cell-line, but inhibits HIV-1 replication in primary macrophages. Cytokine 34:17–23 [CrossRef]
    [Google Scholar]
  33. Ombrellino M., Wang H., Ajemian M. S., Talhouk A., Scher L. A., Friedman S. G., Tracey K. J. 1999; Increased serum concentrations of high-mobility-group protein 1 in haemorrhagic shock. Lancet 354:1446–1447 [CrossRef]
    [Google Scholar]
  34. Palmer D. R., Sun P., Celluzzi C., Bisbing J., Pang S., Sun W., Marovich A. M., Burgess T. 2005; Differential effects of dengue virus on infected and bystander dendritic cells. J Virol 79:2432–2439 [CrossRef]
    [Google Scholar]
  35. Pang T., Cardosa J. M., Guzman G. M. 2007; Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever–dengue shock syndrome (DHF/DSS). Immunol Cell Biol 85:43–45 [CrossRef]
    [Google Scholar]
  36. Parrish W., Ulloa L. 2007; High-mobility group box-1 isoforms as potential therapeutic targets in sepsis. Methods Mol Biol 361:145–162
    [Google Scholar]
  37. Pisetsky D. S., Erlandsson-Harris H., Andersson U. 2008; High-mobility group box protein 1 (HMGB1): an alarmin mediating the pathogenesis of rheumatic disease. Arthritis Res Ther 10:209–219 [CrossRef]
    [Google Scholar]
  38. Sadon N., Delers A., Jarman G. R., Klungthong C., Nisalak A., Gibbons V. R., Vassilev V. 2008; A new quantitative RT-PCR method for sensitive detection of dengue virus in serum samples. J Virol Methods 153:1–6 [CrossRef]
    [Google Scholar]
  39. Sallusto F., Lanzavecchia A. 2000; Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol Rev 177:134–140 [CrossRef]
    [Google Scholar]
  40. Sha Y., Zmijewski J., Xu Z., Abraham E. 2008; HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 180:2531–2537 [CrossRef]
    [Google Scholar]
  41. Shresta S., Kyle L. J., Snider M. H., Basavapatna M., Beatty R. P., Harris E. 2004; Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J Virol 78:2701–2710 [CrossRef]
    [Google Scholar]
  42. Sundén-Cullberg J., Norrby-Teglund A., Rouhiainen A., Rauvala H., Herman G., Tracey K. J., Lee M. L., Andersson J., Tokics L., Treutiger C. J. 2005; Persistent elevation of high mobility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock. Crit Care Med 33:564–573 [CrossRef]
    [Google Scholar]
  43. Ueno H., Matsuda T., Hashimoto S., Amaya F., Kitamura Y., Tanaka M., Kobayashi A., Maruyama I., Yamada S. other authors 2004; Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med 170:1310–1316 [CrossRef]
    [Google Scholar]
  44. Ulloa L., Ochani M., Yang H., Tanovic M., Halperin D., Yang R., Czura J. C., Fink P. M., Tracey J. K. 2002; Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proc Natl Acad Sci U S A 99:12351–12356 [CrossRef]
    [Google Scholar]
  45. Vaughn D. W., Green S., Kalayanarooj S., Innis B. L., Nimmannitya S., Suntayakorn S., Endy T. P., Raengsakulrach B., Rothman A. L. other authors 2000; Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181:2–9 [CrossRef]
    [Google Scholar]
  46. Wang H., Bloom O., Zhang M., Vishnubhakat J. M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S. other authors 1999a; HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248–251 [CrossRef]
    [Google Scholar]
  47. Wang H., Vishnubhakat J. M., Bloom O., Zhang M., Ombrellino M., Sama A., Tracey K. J. 1999b; Proinflammatory cytokines (tumor necrosis factor and interleukin 1) stimulate release of high mobility group protein-1 by pituicytes. Surgery 126:389–392 [CrossRef]
    [Google Scholar]
  48. Wang H., Ward F. M., Fan G. X., Sama E. A., Li W. 2006; Potential role of high mobility group box 1 in viral infectious diseases. Viral Immunol 19:3–9 [CrossRef]
    [Google Scholar]
  49. Wati S., Li P., Burrell J. C., Carr M. J. 2007; Dengue virus (DV) replication in monocyte-derived macrophages is not affected by tumor necrosis factor alpha (TNF), and DV infection induces altered responsiveness to TNF-stimulation. J Virol 81:10161–10171 [CrossRef]
    [Google Scholar]
  50. Yang H., Wang H., Tracey J. K. 2001; HMG-1 rediscovered as a cytokine. Shock 15:247–253 [CrossRef]
    [Google Scholar]
  51. Yang H., Ochani M., Li J., Qiang X., Tanovic M., Harris H. E., Susarla S. M., Ulloa L., Wang H. other authors 2004; Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci U S A 101:296–301 [CrossRef]
    [Google Scholar]
  52. Yang D., Chen Q., Yang H., Tracey J. K., Bustin M., Oppenheim J. J. 2007; High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 81:59–66
    [Google Scholar]
  53. Yin K., Gribbin E., Wang H. 2005; Interferon- γ inhibition attenuates lethality after cecal ligation and puncture in rats: implication of high mobility group box 1. Shock 24:396–401 [CrossRef]
    [Google Scholar]
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