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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.009027-0
2009-08-01
2019-11-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/8/1827.html?itemId=/content/journal/jgv/10.1099/vir.0.009027-0&mimeType=html&fmt=ahah

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, 51, 21–23. Madison, WI: Promega.
  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]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.009027-0
Loading
/content/journal/jgv/10.1099/vir.0.009027-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error