1887

Abstract

We have recently proposed that amphisomes act as a site for translation and replication of dengue virus (DENV)-2 and that DENV-2 entry and replication are linked through an ongoing association with membranes of an endosomal–autophagosomal lineage. In this report, we present the results of an investigation into the interaction between DENV-3 and the autophagy machinery. Critically, treatment with the lysosomal fusion inhibitor -asparagine differentiated the interaction of DENV-3 from that of DENV-2. Inhibition of fusion of autophagosomes and amphisomes with lysosomes resulted in decreased DENV-3 production, implying a role for the autophagolysosome in the DENV-3 life cycle. Evidence based upon the co-localization of LC3 and cathepsin D with double stranded RNA and NS1 protein, as assessed by confocal microscopy, support a model in which DENV-3 interacts with both amphisomes and autophagolysosomes. These results demonstrate that the interactions between DENV and the host cell autophagy machinery are complex and may be determined in part by virus-encoded factors.

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2009-05-01
2019-11-13
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References

  1. Acosta, E. G., Castilla, V. & Damonte, E. B. ( 2008; ). Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol 89, 474–484.[CrossRef]
    [Google Scholar]
  2. Bampton, E. T., Goemans, C. G., Niranjan, D., Mizushima, N. & Tolkovsky, A. M. ( 2005; ). The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 1, 23–36.[CrossRef]
    [Google Scholar]
  3. Clyde, K., Kyle, J. L. & Harris, E. ( 2006; ). Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J Virol 80, 11418–11431.[CrossRef]
    [Google Scholar]
  4. Dunn, W. A., Jr ( 1990a; ). Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J Cell Biol 110, 1923–1933.[CrossRef]
    [Google Scholar]
  5. Dunn, W. A., Jr ( 1990b; ). Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J Cell Biol 110, 1935–1945.[CrossRef]
    [Google Scholar]
  6. Eskelinen, E. L. ( 2005; ). Maturation of autophagic vacuoles in mammalian cells. Autophagy 1, 1–10.[CrossRef]
    [Google Scholar]
  7. Eskelinen, E. L., Illert, A. L., Tanaka, Y., Schwarzmann, G., Blanz, J., Von Figura, K. & Saftig, P. ( 2002; ). Role of LAMP-2 in lysosome biogenesis and autophagy. Mol Biol Cell 13, 3355–3368.[CrossRef]
    [Google Scholar]
  8. Espert, L., Codogno, P. & Biard-Piechaczyk, M. ( 2007; ). Involvement of autophagy in viral infections: antiviral function and subversion by viruses. J Mol Med 85, 811–823.[CrossRef]
    [Google Scholar]
  9. Gordon, P. B. & Seglen, P. O. ( 1988; ). Prelysosomal convergence of autophagic and endocytic pathways. Biochem Biophys Res Commun 151, 40–47.[CrossRef]
    [Google Scholar]
  10. Guzman, M. G. & Kouri, G. ( 2002; ). Dengue: an update. Lancet Infect Dis 2, 33–42.[CrossRef]
    [Google Scholar]
  11. Halstead, S. B. ( 1988; ). Pathogenesis of dengue: challenges to molecular biology. Science 239, 476–481.[CrossRef]
    [Google Scholar]
  12. Heinz, F. X., Stiasny, K. & Allison, S. L. ( 2004; ). The entry machinery of flaviviruses. Arch Virol Suppl 18, 133–137.
    [Google Scholar]
  13. Holmes, E. C. & Twiddy, S. S. ( 2003; ). The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3, 19–28.[CrossRef]
    [Google Scholar]
  14. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y. & Yoshimori, T. ( 2000; ). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19, 5720–5728.[CrossRef]
    [Google Scholar]
  15. Kihara, A., Kabeya, Y., Ohsumi, Y. & Yoshimori, T. ( 2001; ). Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2, 330–335.[CrossRef]
    [Google Scholar]
  16. Kimura, S., Noda, T. & Yoshimori, T. ( 2007; ). Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452–460.[CrossRef]
    [Google Scholar]
  17. Ko, K. K., Igarashi, A. & Fukai, K. ( 1979; ). Electron microscopic observations on Aedes albopictus cells infected with dengue viruses. Arch Virol 62, 41–52.[CrossRef]
    [Google Scholar]
  18. Krishnan, M. N., Sukumaran, B., Pal, U., Agaisse, H., Murray, J. L., Hodge, T. W. & Fikrig, E. ( 2007; ). Rab 5 is required for the cellular entry of dengue and West Nile viruses. J Virol 81, 4881–4885.[CrossRef]
    [Google Scholar]
  19. Lee, H. K. & Iwasaki, A. ( 2008; ). Autophagy and antiviral immunity. Curr Opin Immunol 20, 23–29.[CrossRef]
    [Google Scholar]
  20. Lee, Y. R., Lei, H. Y., Liu, M. T., Wang, J. R., Chen, S. H., Jiang-Shieh, Y. F., Lin, Y. S., Yeh, T. M., Liu, C. C. & Liu, H. S. ( 2008; ). Autophagic machinery activated by dengue virus enhances virus replication. Virology 374, 240–248.[CrossRef]
    [Google Scholar]
  21. Lerena, C., Calligaris, S. D. & Colombo, M. I. ( 2008; ). Autophagy: for better or for worse, in good times or in bad times. Curr Mol Med 8, 92–101.[CrossRef]
    [Google Scholar]
  22. Levine, B. & Klionsky, D. J. ( 2004; ). Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6, 463–477.[CrossRef]
    [Google Scholar]
  23. Malavige, G. N., Fernando, S., Fernando, D. J. & Seneviratne, S. L. ( 2004; ). Dengue viral infections. Postgrad Med J 80, 588–601.[CrossRef]
    [Google Scholar]
  24. Meijer, A. J. & Codogno, P. ( 2006; ). Signalling and autophagy regulation in health, aging and disease. Mol Aspects Med 27, 411–425.[CrossRef]
    [Google Scholar]
  25. Miller, S. & Krijnse-Locker, J. ( 2008; ). Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6, 363–374.[CrossRef]
    [Google Scholar]
  26. Mizushima, N. & Yoshimori, T. ( 2007; ). How to interpret LC3 immunoblotting. Autophagy 3, 542–545.[CrossRef]
    [Google Scholar]
  27. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M. D., Klionsky, D. J., Ohsumi, M. & Ohsumi, Y. ( 1998; ). A protein conjugation system essential for autophagy. Nature 395, 395–398.[CrossRef]
    [Google Scholar]
  28. Mizushima, N., Yoshimori, T. & Ohsumi, Y. ( 2002; ). Mouse Apg10 as an Apg12-conjugating enzyme: analysis by the conjugation-mediated yeast two-hybrid method. FEBS Lett 532, 450–454.[CrossRef]
    [Google Scholar]
  29. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. ( 2008; ). Autophagy fights disease through cellular self-digestion. Nature 451, 1069–1075.[CrossRef]
    [Google Scholar]
  30. Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. ( 2004; ). Structure of the dengue virus envelope protein after membrane fusion. Nature 427, 313–319.[CrossRef]
    [Google Scholar]
  31. Mukhopadhyay, S., Kuhn, R. J. & Rossmann, M. G. ( 2005; ). A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3, 13–22.[CrossRef]
    [Google Scholar]
  32. Noda, T. & Ohsumi, Y. ( 1998; ). Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273, 3963–3966.[CrossRef]
    [Google Scholar]
  33. Ohsumi, Y. ( 2001; ). Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2, 211–216.[CrossRef]
    [Google Scholar]
  34. Panyasrivanit, M., Khakpoor, A., Wikan, N. & Smith, D. R. ( 2009; ). Co-localization of constituents of the dengue virus translation and replication machinery with amphisomes. J Gen Virol 90, 448–456.[CrossRef]
    [Google Scholar]
  35. Puttikhunt, C., Kasinrerk, W., Srisa-ad, S., Duangchinda, T., Silakate, W., Moonsom, S., Sittisombut, N. & Malasit, P. ( 2003; ). Production of anti-dengue NS1 monoclonal antibodies by DNA immunization. J Virol Methods 109, 55–61.[CrossRef]
    [Google Scholar]
  36. Salonen, A., Ahola, T. & Kääriäinen, L. ( 2005; ). Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285, 139–173.
    [Google Scholar]
  37. Seglen, P. O. & Gordon, P. B. ( 1982; ). 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79, 1889–1892.[CrossRef]
    [Google Scholar]
  38. Seglen, P. O., Berg, T. O., Blankson, H., Fengsrud, M., Holen, I. & Strømhaug, P. E. ( 1996; ). Structural aspects of autophagy. Adv Exp Med Biol 389, 103–111.
    [Google Scholar]
  39. Seneviratne, S. L., Malavige, G. N. & de Silva, H. J. ( 2006; ). Pathogenesis of liver involvement during dengue viral infections. Trans R Soc Trop Med Hyg 100, 608–614.[CrossRef]
    [Google Scholar]
  40. Sithisarn, P., Suksanpaisan, L., Thepparit, C. & Smith, D. R. ( 2003; ). Behavior of the dengue virus in solution. J Med Virol 71, 532–539.[CrossRef]
    [Google Scholar]
  41. Suksanpaisan, L., Cabrera-Hernandez, A. & Smith, D. R. ( 2007; ). Infection of human primary hepatocytes with dengue virus serotype 2. J Med Virol 79, 300–307.[CrossRef]
    [Google Scholar]
  42. Taylor, P. R., Gordon, S. & Martinez-Pomares, L. ( 2005; ). The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol 26, 104–110.[CrossRef]
    [Google Scholar]
  43. Thepparit, C. & Smith, D. R. ( 2004; ). Serotype-specific entry of dengue virus into liver cells: identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 78, 12647–12656.[CrossRef]
    [Google Scholar]
  44. Thepparit, C., Phoolcharoen, W., Suksanpaisan, L. & Smith, D. R. ( 2004; ). Internalization and propagation of the dengue virus in human hepatoma (HepG2) cells. Intervirology 47, 78–86.[CrossRef]
    [Google Scholar]
  45. van der Schaar, H. M., Rust, M. J., Waarts, B. L., van der Ende-Metselaar, H., Kuhn, R. J., Wilschut, J., Zhuang, X. & Smit, J. M. ( 2007; ). Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J Virol 81, 12019–12028.[CrossRef]
    [Google Scholar]
  46. Xie, Z. & Klionsky, D. J. ( 2007; ). Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9, 1102–1109.[CrossRef]
    [Google Scholar]
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