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Journal of Tropical Medicine
Volume 2012, Article ID 628475, 13 pages
http://dx.doi.org/10.1155/2012/628475
Review Article

Dengue Virus Entry as Target for Antiviral Therapy

Department of Microbiology and Immunology, Rega Institute for Medical Research, Katholieke Universiteit Leuven, 3000 Leuven, Belgium

Received 26 September 2011; Accepted 10 November 2011

Academic Editor: Jean-Paul Gonzalez

Copyright © 2012 Marijke M. F. Alen and Dominique Schols. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. B. Halstead, “Dengue virus-mosquito interactions,” Annual Review of Entomology, vol. 53, pp. 273–291, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. T. Solomon and M. Mallewa, “Dengue and other emerging flaviviruses,” Journal of Infection, vol. 42, no. 2, pp. 104–115, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. J. G. Rigau-Pérez, G. G. Clark, D. J. Gubler, P. Reiter, E. J. Sanders, and A. V. Vorndam, “Dengue and dengue haemorrhagic fever,” Lancet, vol. 352, no. 9132, pp. 971–977, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. S. B. Halstead, “Dengue,” Lancet, vol. 370, no. 9599, pp. 1644–1652, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. D. J. Gubler, “Dengue and dengue hemorrhagic fever,” Clinical Microbiology Reviews, vol. 11, no. 3, pp. 480–496, 1998. View at Google Scholar · View at Scopus
  6. S. Murrell, S. C. Wu, and M. Butler, “Review of dengue virus and the development of a vaccine,” Biotechnology Advances, vol. 29, no. 2, pp. 239–247, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. S. S. Whitehead, J. E. Blaney, A. P. Durbin, and B. R. Murphy, “Prospects for a dengue virus vaccine,” Nature Reviews Microbiology, vol. 5, no. 7, pp. 518–528, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. R. Takhampunya, S. Ubol, H. S. Houng, C. E. Cameron, and R. Padmanabhan, “Inhibition of dengue virus replication by mycophenolic acid and ribavirin,” Journal of General Virology, vol. 87, no. 7, pp. 1947–1952, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. M. S. Diamond, M. Zachariah, and E. Harris, “Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA,” Virology, vol. 304, no. 2, pp. 211–221, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. L. Chen, Z. Yin, S. B. Lakshminarayana et al., “Inhibition of dengue virus by an ester prodrug of an adenosine analog,” Antimicrobial Agents and Chemotherapy, vol. 54, no. 8, pp. 3255–3261, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. J. M. Crance, N. Scaramozzino, A. Jouan, and D. Garin, “Interferon, ribavirin, 6-azauridine and glycyrrhizin: antiviral compounds active against pathogenic flaviviruses,” Antiviral Research, vol. 58, no. 1, pp. 73–79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Leyssen, E. De Clercq, and J. Neyts, “Perspectives for the treatment of infections with Flaviviridae,” Clinical Microbiology Reviews, vol. 13, no. 1, pp. 67–82, 2000. View at Google Scholar · View at Scopus
  13. A. Takada and Y. Kawaoka, “Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications,” Reviews in Medical Virology, vol. 13, no. 6, pp. 387–398, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. S. C. Kliks, A. Nisalak, W. E. Brandt, L. Wahl, and D. S. Burke, “Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever,” American Journal of Tropical Medicine and Hygiene, vol. 40, no. 4, pp. 444–451, 1989. View at Google Scholar · View at Scopus
  15. A. T. A. Mairuhu, J. Wagenaar, D. P. M. Brandjes, and E. C. M. Van Gorp, “Dengue: an arthropod-borne disease of global importance,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 23, no. 6, pp. 425–433, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. S. J. L. Wu, G. Grouard-Vogel, W. Sun et al., “Human skin Langerhans cells are targets of dengue virus infection,” Nature Medicine, vol. 6, no. 7, pp. 816–820, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. Z. Kou, M. Quinn, H. Chen et al., “Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells,” Journal of Medical Virology, vol. 80, no. 1, pp. 134–146, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. R. J. Kuhn, W. Zhang, M. G. Rossmann et al., “Structure of dengue virus: implications for flavivirus organization, maturation, and fusion,” Cell, vol. 108, no. 5, pp. 717–725, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. E. G. Acosta, V. Castilla, and E. B. Damonte, “Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis,” Journal of General Virology, vol. 89, no. 2, pp. 474–484, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. H. M. Van Der Schaar, M. J. Rust, Chen et al., “Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells,” PLoS Pathogens, vol. 4, no. 12, Article ID e1000244, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. J. J. H. Chu and M. L. Ng, “Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway,” Journal of Virology, vol. 78, no. 19, pp. 10543–10555, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. M. Nawa, T. Takasaki, K. I. Yamada, I. Kurane, and T. Akatsuka, “Interference in Japanese encephalitis virus infection of Vero cells by a cationic amphiphilic drug, chlorpromazine,” Journal of General Virology, vol. 84, no. 7, pp. 1737–1741, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. E. G. Acosta, V. Castilla, and E. B. Damonte, “Alternative infectious entry pathways for dengue virus serotypes into mammalian cells,” Cellular Microbiology, vol. 11, no. 10, pp. 1533–1549, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. Y. Modis, S. Ogata, D. Clements, and S. C. Harrison, “Structure of the dengue virus envelope protein after membrane fusion,” Nature, vol. 427, no. 6972, pp. 313–319, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. K. Stiasny, R. Fritz, K. Pangerl, and F. X. Heinz, “Molecular mechanisms of flavivirus membrane fusion,” Amino Acids, vol. 41, no. 5, pp. 1159–1163, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. Y. Zhang, W. Zhang, S. Ogata et al., “Conformational changes of the flavivirus E glycoprotein,” Structure, vol. 12, no. 9, pp. 1607–1618, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. C. S. S. Martín, C. Y. Liu, and M. Kielian, “Dealing with low pH: entry and exit of alphaviruses and flaviviruses,” Trends in Microbiology, vol. 17, no. 11, pp. 514–521, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. Y. Chen, T. Maguire, R. E. Hileman et al., “Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate,” Nature Medicine, vol. 3, no. 8, pp. 866–871, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Germi, J. M. Crance, D. Garin et al., “Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus,” Virology, vol. 292, no. 1, pp. 162–168, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. J. J. Martínez-Barragán and R. M. Del Angel, “Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection,” Journal of Virology, vol. 75, no. 17, pp. 7818–7827, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Wichit, A. Jittmittraphap, K. I. Hidari et al., “Dengue virus type 2 recognizes the carbohydrate moiety of neutral glycosphingolipids in mammalian and mosquito cells,” Microbiology and Immunology, vol. 55, no. 2, pp. 135–140, 2011. View at Publisher · View at Google Scholar · View at PubMed
  32. Y. C. Chen, S. Y. Wang, and C. C. King, “Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism,” Journal of Virology, vol. 73, no. 4, pp. 2650–2657, 1999. View at Google Scholar · View at Scopus
  33. J. Reyes-Del Valle, S. Chávez-Salinas, F. Medina, and R. M. Del Angel, “Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells,” Journal of Virology, vol. 79, no. 8, pp. 4557–4567, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. E. Navarro-Sanchez, R. Altmeyer, A. Amara et al., “Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses,” EMBO Reports, vol. 4, no. 7, pp. 723–728, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. B. Tassaneetrithep, T. H. Burgess, A. Granelli-Piperno et al., “DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells,” Journal of Experimental Medicine, vol. 197, no. 7, pp. 823–829, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. J. L. Miller, B. J. M. DeWet, L. Martinez-Pomares et al., “The mannose receptor mediates dengue virus infection of macrophages,” PLoS Pathogens, vol. 4, no. 2, article e17, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. S. T. Chen, Y. L. Lin, M. T. Huang et al., “CLEC5A is critical for dengue-virus-induced lethal disease,” Nature, vol. 453, no. 7195, pp. 672–676, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. P. Hilgard and R. Stockert, “Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes,” Hepatology, vol. 32, no. 5, pp. 1069–1077, 2000. View at Google Scholar · View at Scopus
  39. Y. L. Lin, H. Y. Lei, Y. S. Lin, T. M. Yeh, S. H. Chen, and H. S. Liu, “Heparin inhibits dengue-2 virus infection of five human liver cell lines,” Antiviral Research, vol. 56, no. 1, pp. 93–96, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Jindadamrongwech, C. Thepparit, and D. R. Smith, “Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2,” Archives of Virology, vol. 149, no. 5, pp. 915–927, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. C. Thepparit and D. R. Smith, “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,” Journal of Virology, vol. 78, no. 22, pp. 12647–12656, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. J. L. Zhang, J. L. Wang, N. Gao, Z. T. Chen, Y. P. Tian, and J. An, “Up-regulated expression of β3 integrin induced by dengue virus serotype 2 infection associated with virus entry into human dermal microvascular endothelial cells,” Biochemical and Biophysical Research Communications, vol. 356, no. 3, pp. 763–768, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. L. Hung, P. L. Lee, H. W. Chen, L. K. Chen, C. L. Kao, and C. C. King, “Analysis of the steps involved in dengue virus entry into host cells,” Virology, vol. 257, no. 1, pp. 156–167, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. C. Aoki, K. I. P. J. Hidari, S. Itonori et al., “Identification and characterization of carbohydrate molecules in mammalian cells recognized by dengue virus type 2,” Journal of Biochemistry, vol. 139, no. 3, pp. 607–614, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. P. Sakoonwatanyoo, V. Boonsanay, and D. R. Smith, “Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein,” Intervirology, vol. 49, no. 3, pp. 161–172, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. J. S. Salas-Benito and R. M. Del Angel, “Identification of two surface proteins from C6/36 cells that bind dengue type 4 virus,” Journal of Virology, vol. 71, no. 10, pp. 7246–7252, 1997. View at Google Scholar · View at Scopus
  47. J. Salas-Benito, J. R. D. Valle, M. Salas-Benito, I. Ceballos-Olvera, C. Mosso, and R. M. Del Angel, “Evidence that the 45-kD glycoprotein, part of a putative dengue virus receptor complex in the mosquito cell line C6/36, is a heat-shock-related protein,” American Journal of Tropical Medicine and Hygiene, vol. 77, no. 2, pp. 283–290, 2007. View at Google Scholar · View at Scopus
  48. A. Kuadkitkan, N. Wikan, C. Fongsaran, and D. R. Smith, “Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells,” Virology, vol. 406, no. 1, pp. 149–161, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. J. M. Costin, E. Jenwitheesuk, S. M. Lok et al., “Structural optimization and de novo design of dengue virus entry inhibitory peptides,” PLoS Neglected Tropical Diseases, vol. 4, no. 6, article no. e721, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. Y. M. Hrobowski, R. F. Garry, and S. F. Michael, “Peptide inhibitors of dengue virus and West Nile virus infectivity,” Virology Journal, vol. 2, article 49, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. Q. Y. Wang, S. J. Patel, E. Vangrevelinghe et al., “A small-molecule dengue virus entry inhibitor,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 5, pp. 1823–1831, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. J. M. Yang, Y. F. Chen, Y. Y. Tu, K. R. Yen, and Y. L. Yang, “Combinatorial computational approaches to identify tetracycline derivatives as flavivirus inhibitors,” PLoS One, vol. 2, no. 5, article no. e428, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. S. J. F. Kaptein, T. De Burghgraeve, M. Froeyen et al., “A derivate of the antibiotic doxorubicin is a selective inhibitor of dengue and yellow fever virus replication in vitro,” Antimicrobial Agents and Chemotherapy, vol. 54, no. 12, pp. 5269–5280, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. M. K. Poh, A. Yip, S. Zhang et al., “A small molecule fusion inhibitor of dengue virus,” Antiviral Research, vol. 84, no. 3, pp. 260–266, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. K. Whitby, T. C. Pierson, B. Geiss et al., “Castanospermine, a potent inhibitor of dengue virus infection in vitro and in vivo,” Journal of Virology, vol. 79, no. 14, pp. 8698–8706, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. M. P. Courageot, M. P. Frenkiel, C. Duarte Dos Santos, V. Deubel, and P. Desprès, “α-Glucosidase inhibitors reduce dengue virus production by affecting the initial steps of virion morphogenesis in the endoplasmic reticulum,” Journal of Virology, vol. 74, no. 1, pp. 564–572, 2000. View at Google Scholar · View at Scopus
  57. S. F. Wu, C. J. Lee, C. L. Liao, R. A. Dwek, N. Zitzmann, and Y. L. Lin, “Antiviral effects of an iminosugar derivative on flavivirus infections,” Journal of Virology, vol. 76, no. 8, pp. 3596–3604, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. P. H. Liang, W. C. Cheng, Y. L. Lee et al., “Novel five-membered iminocyclitol derivatives as selective and potent glycosidase inhibitors: new structures for antivirals and osteoarthritis,” ChemBioChem, vol. 7, no. 1, pp. 165–173, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. B. Gu, P. Mason, L. Wang et al., “Antiviral profiles of novel iminocyclitol compounds against bovine viral diarrhea virus, West Nile virus, dengue virus and hepatitis B virus,” Antiviral Chemistry and Chemotherapy, vol. 18, no. 1, pp. 49–59, 2007. View at Google Scholar · View at Scopus
  60. J. Chang, L. Wang, D. Ma et al., “Novel imino sugar derivatives demonstrate potent antiviral activity against flavivirusesv,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 4, pp. 1501–1508, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. M. M. F. Alen, S. J. F. Kaptein, T. De Burghgraeve, J. Balzarini, J. Neyts, and D. Schols, “Antiviral activity of carbohydrate-binding agents and the role of DC-SIGN in dengue virus infection,” Virology, vol. 387, no. 1, pp. 67–75, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. M. M.F. Alen, T. de Burghgraeve, S. J.F. Kaptein, J. Balzarini, J. Neyts, and D. Schols, “Broad Antiviral activity of Carbohydrate-binding agents against the four serotypes of dengue virus in monocyte-derived dendritic cells,” PLoS One, vol. 6, no. 6, article e21658, 2011. View at Publisher · View at Google Scholar · View at PubMed
  63. E. Lee, M. Pavy, N. Young, C. Freeman, and M. Lobigs, “Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses,” Antiviral Research, vol. 69, no. 1, pp. 31–38, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. K. I. P. J. Hidari, N. Takahashi, M. Arihara, M. Nagaoka, K. Morita, and T. Suzuki, “Structure and anti-dengue virus activity of sulfated polysaccharide from a marine alga,” Biochemical and Biophysical Research Communications, vol. 376, no. 1, pp. 91–95, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. L. Ono, W. Wollinger, I. M. Rocco, T. L. M. Coimbra, P. A. J. Gorin, and M. R. Sierakowski, “In vitro and in vivo antiviral properties of sulfated galactomannans against yellow fever virus (BeH111 strain) and dengue 1 virus (Hawaii strain),” Antiviral Research, vol. 60, no. 3, pp. 201–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. L. B. Talarico, C. A. Pujol, R. G. M. Zibetti et al., “The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell,” Antiviral Research, vol. 66, no. 2-3, pp. 103–110, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. L. B. Talarico and E. B. Damonte, “Interference in dengue virus adsorption and uncoating by carrageenans,” Virology, vol. 363, no. 2, pp. 473–485, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. H. Qiu, W. Tang, X. Tong, K. Ding, and J. Zuo, “Structure elucidation and sulfated derivatives preparation of two α-d-glucans from Gastrodia elata Bl. and their anti-dengue virus bioactivities,” Carbohydrate Research, vol. 342, no. 15, pp. 2230–2236, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. C. R. Rees, J. M. Costin, R. C. Fink et al., “In vitro inhibition of dengue virus entry by p-sulfoxy-cinnamic acid and structurally related combinatorial chemistries,” Antiviral Research, vol. 80, no. 2, pp. 135–142, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. S. B. Halstead, E. J. O'Rourke, and A. C. Allison, “Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection,” Journal of Experimental Medicine, vol. 146, no. 1, pp. 218–229, 1977. View at Google Scholar · View at Scopus
  71. A. P. Durbin, M. J. Vargas, K. Wanionek et al., “Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever,” Virology, vol. 376, no. 2, pp. 429–435, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. C. C. Daughaday, W. E. Brandt, J. M. McCown, and P. K. Russell, “Evidence for two mechanisms of dengue virus infection of adherent human monocytes: trypsin-sensitive virus receptors and trypsin-resistant immune complex receptors,” Infection and Immunity, vol. 32, no. 2, pp. 469–473, 1981. View at Google Scholar · View at Scopus
  73. S. Taweechaisupapong, S. Sriurairatana, S. Angsubhakorn et al., “Langerhans cell density and serological changes following intradermal immunisation of mice with dengue 2 virus,” Journal of Medical Microbiology, vol. 45, no. 2, pp. 138–145, 1996. View at Google Scholar · View at Scopus
  74. M. Marovich, G. Grouard-Vogel, M. Louder et al., “Human dendritic cells as targets of dengue virus infection,” Journal of Investigative Dermatology Symposium Proceedings, vol. 6, no. 3, pp. 219–224, 2001. View at Google Scholar · View at Scopus
  75. D. H. Libraty, S. Pichyangkul, C. Ajariyakhajorn, T. P. Endy, and F. A. Ennis, “Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis,” Journal of Virology, vol. 75, no. 8, pp. 3501–3508, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. L. J. Ho, J. J. Wang, M. F. Shaio et al., “Infection of human dendritic cells by Dengue virus causes cell maturation and cytokine production,” Journal of Immunology, vol. 166, no. 3, pp. 1499–1506, 2001. View at Google Scholar · View at Scopus
  77. P. Y. Lozach, L. Burleigh, I. Staropoli et al., “Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals,” Journal of Biological Chemistry, vol. 280, no. 25, pp. 23698–23708, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. D. A. Mitchell, A. J. Fadden, and K. Drickamer, “A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands,” Journal of Biological Chemistry, vol. 276, no. 31, pp. 28939–28945, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. H. Feinberg, D. A. Mitchell, K. Drickamer, and W. I. Weis, “Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR,” Science, vol. 294, no. 5549, pp. 2163–2166, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. B. J. Appelmelk, I. Van Die, S. J. Van Vliet, C. M. J. E. Vandenbroucke-Grauls, T. B. H. Geijtenbeek, and Y. Van Kooyk, “Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells,” Journal of Immunology, vol. 170, no. 4, pp. 1635–1639, 2003. View at Google Scholar · View at Scopus
  81. T. B. H. Geijtenbeek, D. S. Kwon, R. Torensma et al., “DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells,” Cell, vol. 100, no. 5, pp. 587–597, 2000. View at Google Scholar · View at Scopus
  82. S. Pöhlmann, J. Zhang, F. Baribaud et al., “Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR,” Journal of Virology, vol. 77, no. 7, pp. 4070–4080, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Marzi, P. Möller, S. L. Hanna et al., “Analysis of the interaction of Ebola virus glycoprotein with DC-SIGN (dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin) and its homologue DC-SIGNR,” Journal of Infectious Diseases, vol. 196, no. 2, pp. S237–S246, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. Y. Van Kooyk and T. B. H. Geijtenbeek, “DC-SIGN: escape mechanism for pathogens,” Nature Reviews Immunology, vol. 3, no. 9, pp. 697–709, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. J. Banchereau and R. M. Steinman, “Dendritic cells and the control of immunity,” Nature, vol. 392, no. 6673, pp. 245–252, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. Y. C. Chen and S. Y. Wang, “Activation of terminally differentiated human monocytes/macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide,” Journal of Virology, vol. 76, no. 19, pp. 9877–9887, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. A. A. Watson, A. A. Lebedev, B. A. Hall et al., “Structural flexibility of the macrophage dengue virus receptor CLEC5A: implications for ligand binding and signaling,” Journal of Biological Chemistry, vol. 286, no. 27, pp. 24208–24218, 2011. View at Publisher · View at Google Scholar · View at PubMed
  88. Y. L. Lin, C. C. Liu, H. Y. Lei et al., “Infection of five human liver cell lines by dengue-2 virus,” Journal of Medical Virology, vol. 60, no. 4, pp. 425–431, 2000. View at Publisher · View at Google Scholar · View at Scopus
  89. S. L. Seneviratne, G. N. Malavige, and H. J. de Silva, “Pathogenesis of liver involvement during dengue viral infections,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 100, no. 7, pp. 608–614, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. C. Thepparit, W. Phoolcharoen, L. Suksanpaisan, and D. R. Smith, “Internalization and propagation of the dengue virus in human hepatoma (HepG2) cells,” Intervirology, vol. 47, no. 2, pp. 78–86, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. S. Wati, M. L. Soo, P. Zilm et al., “Dengue virus infection induces upregulation of GRP78, which acts to chaperone viral antigen production,” Journal of Virology, vol. 83, no. 24, pp. 12871–12880, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. S. Pöhlmann, E. J. Soilleux, F. Baribaud et al., “DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2670–2675, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  93. A. A. Bashirova, T. B. H. Geijtenbeek, G. C. F. Van Duijnhoven et al., “A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection,” Journal of Experimental Medicine, vol. 193, no. 6, pp. 671–678, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. C. W. Davis, H. Y. Nguyen, S. L. Hanna, M. D. Sánchez, R. W. Doms, and T. C. Pierson, “West nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection,” Journal of Virology, vol. 80, no. 3, pp. 1290–1301, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. P. Avirutnan, P. Malasit, B. Seliger, S. Bhakdi, and M. Husmann, “Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis,” Journal of Immunology, vol. 161, no. 11, pp. 6338–6346, 1998. View at Google Scholar · View at Scopus
  96. T. Hase, P. L. Summers, and K. H. Eckels, “Flavivirus entry into cultured mosquito cells and human peripheral blood monocytes,” Archives of Virology, vol. 104, no. 1-2, pp. 129–143, 1989. View at Google Scholar · View at Scopus
  97. V. B. Randolph and V. Stollar, “Low pH-induced cell fusion in flavivirus-infected Aedes albopictus cell cultures,” Journal of General Virology, vol. 71, no. 8, pp. 1845–1850, 1990. View at Google Scholar · View at Scopus
  98. R. F. Mercado-Curiel, H. A. Esquinca-Avilés, R. Tovar, Á. Díaz-Badillo, M. Camacho-Nuez, and M. D. L. Muñoz, “The four serotypes of dengue recognize the same putative receptors in Aedes aegypti midgut and Ae. albopictus cells,” BMC Microbiology, vol. 6, article no. 85, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  99. R. Perera, M. Khaliq, and R. J. Kuhn, “Closing the door on flaviviruses: entry as a target for antiviral drug design,” Antiviral Research, vol. 80, no. 1, pp. 11–22, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  100. Y. Modis, S. Ogata, D. Clements, and S. C. Harrison, “A ligand-binding pocket in the dengue virus envelope glycoprotein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 6986–6991, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. F. A. Rey, F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison, “The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution,” Nature, vol. 375, no. 6529, pp. 291–298, 1995. View at Google Scholar · View at Scopus
  102. W. D. Crill and J. T. Roehrig, “Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to vero cells,” Journal of Virology, vol. 75, no. 16, pp. 7769–7773, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  103. R. Rajamanonmani, C. Nkenfou, P. Clancy et al., “On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes,” Journal of General Virology, vol. 90, no. 4, pp. 799–809, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  104. J. H. Scherret, J. S. Mackenzie, A. A. Khromykh, and R. A. Hall, “Biological significance of glycosylation of the envelope protein of Kunjin virus,” Annals of the New York Academy of Sciences, vol. 951, pp. 361–363, 2001. View at Google Scholar · View at Scopus
  105. J. A. Mondotte, P. Y. Lozach, A. Amara, and A. V. Gamarnik, “Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation,” Journal of Virology, vol. 81, no. 13, pp. 7136–7148, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  106. E. Pokidysheva, Y. Zhang, A. J. Battisti et al., “Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN,” Cell, vol. 124, no. 3, pp. 485–493, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  107. D. J. Vigerust and V. L. Shepherd, “Virus glycosylation: role in virulence and immune interactions,” Trends in Microbiology, vol. 15, no. 5, pp. 211–218, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  108. A. J. Johnson, F. Guirakhoo, and J. T. Roehrig, “The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites,” Virology, vol. 203, no. 2, pp. 241–249, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  109. K. Hacker, L. White, and A. M. de Silva, “N-linked glycans on dengue viruses grown in mammalian and insect cells,” Journal of General Virology, vol. 90, no. 9, pp. 2097–2106, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  110. E. Lee, S. K. Leang, A. Davidson, and M. Lobigs, “Both E protein glycans adversely affect dengue virus infectivity but are beneficial for virion release,” Journal of Virology, vol. 84, no. 10, pp. 5171–5180, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. F. Guirakhoo, A. R. Hunt, J. G. Lewis, and J. T. Roehrig, “Selection and partial characterization of dengue 2 virus mutants that induce fusion at elevated pH,” Virology, vol. 194, no. 1, pp. 219–223, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. E. Lee, R. C. Weir, and L. Dalgarno, “Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein,” Virology, vol. 232, no. 2, pp. 281–290, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. J. E. Bryant, A. E. Calvert, K. Mesesan et al., “Glycosylation of the dengue 2 virus E protein at N67 is critical for virus growth in vitro but not for growth in intrathoracically inoculated Aedes aegypti mosquitoes,” Virology, vol. 366, no. 2, pp. 415–423, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. K. M. Rogers and M. Heise, “Modulation of cellular tropism and innate antiviral response by viral glycans,” Journal of Innate Immunity, vol. 1, no. 5, pp. 405–412, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  115. W. B. Klimstra, E. M. Nangle, M. S. Smith, A. D. Yurochko, and K. D. Ryman, “DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses,” Journal of Virology, vol. 77, no. 22, pp. 12022–12032, 2003. View at Publisher · View at Google Scholar · View at Scopus
  116. C. O. Nicholson, J. M. Costin, D. K. Rowe et al., “Viral entry inhibitors block dengue antibody-dependent enhancement in vitro,” Antiviral Research, vol. 89, no. 1, pp. 71–74, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. A. C. Sayce, J. L. Miller, and N. Zitzmann, “Targeting a host process as an antiviral approach against dengue virus,” Trends in Microbiology, vol. 18, no. 7, pp. 323–330, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  118. A. Mehta, S. Ouzounov, R. Jordan et al., “Imino sugars that are less toxic but more potent as antivirals, in vitro, compared with N-n-nonyl DNJ,” Antiviral Chemistry and Chemotherapy, vol. 13, no. 5, pp. 299–304, 2002. View at Google Scholar · View at Scopus
  119. W. Schul, W. Liu, H. Y. Xu, M. Flamand, and S. G. Vasudevan, “A dengue fever viremia model in mice shows reduction in viral replication and suppression of the inflammatory response after treatment with antiviral drugs,” Journal of Infectious Diseases, vol. 195, no. 5, pp. 665–674, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  120. J. Chang, W. Schul, T. D. Butters et al., “Combination of α-glucosidase inhibitor and ribavirin for the treatment of dengue virus infection in vitro and in vivo,” Antiviral Research, vol. 89, no. 1, pp. 26–34, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. N. Shibuya, I. J. Goldstein, E. J. Van Damme, and W. J. Peumans, “Binding properties of a mannose-specific lectin from the snowdrop (Galanthus nivalis) bulb,” Journal of Biological Chemistry, vol. 263, no. 2, pp. 728–734, 1988. View at Google Scholar · View at Scopus
  122. H. Kaku, E. J. M. Van Damme, W. J. Peumans, and I. J. Goldstein, “Carbohydrate-binding specificity of the daffodil (Narcissus pseudonarcissus) and amaryllis (Hippeastrum hybr.) bulb lectins,” Archives of Biochemistry and Biophysics, vol. 279, no. 2, pp. 298–304, 1990. View at Publisher · View at Google Scholar · View at Scopus
  123. N. Shibuya, I. J. Goldstein, J. A. Shafer, W. J. Peumans, and W. F. Broekaert, “Carbohydrate binding properties of the stinging nettle (Urtica dioica) rhizome lectin,” Archives of Biochemistry and Biophysics, vol. 249, no. 1, pp. 215–224, 1986. View at Google Scholar · View at Scopus
  124. J. J. Hung, M. T. Hsieh, M. J. Young, C. L. Kao, C. C. King, and W. Chang, “An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells,” Journal of Virology, vol. 78, no. 1, pp. 378–388, 2004. View at Publisher · View at Google Scholar · View at Scopus
  125. R. M. Marks, H. Lu, R. Sundaresan et al., “Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycan-derived inhibitors,” Journal of Medicinal Chemistry, vol. 44, no. 13, pp. 2178–2187, 2001. View at Publisher · View at Google Scholar · View at Scopus
  126. C. A. Pujol, J. M. Estevez, M. J. Carlucci, M. Ciancia, A. S. Cerezo, and E. B. Damonte, “Novel DL-galactan hybrids from the red seaweed Gymnogongrus torulosus are potent inhibitors of herpes simplex virus and dengue virus,” Antiviral Chemistry and Chemotherapy, vol. 13, no. 2, pp. 83–89, 2002. View at Google Scholar · View at Scopus
  127. X. K. Tong, H. Qiu, X. Zhang et al., “WSS45, a sulfated α-D-glucan, strongly interferes with Dengue 2 virus infection in vitro,” Acta Pharmacologica Sinica, vol. 31, no. 5, pp. 585–592, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus