1887

Abstract

Dengue virus (DENV) causes fever and severe haemorrhagic symptoms in humans. The DEN2 16681 strain, derived from a dengue haemorrhagic fever patient, has been widely used in studies related to DENV pathogenesis, such as mouse and non-human primate haemorrhagic models and human vascular endothelial-cell permeability. To clarify the entry mechanism of the 16681 strain, we characterized a novel cell receptor for this strain. Our two major findings were as follows: firstly, the SDC2 membrane protein was an effective DEN2 16681 receptor in a cloned K562 cell line. Secondly, a heparan sulfate (HS) glycochain (of four glycochains in SDC2) is the specific binding site of DENV and seems to be involved in tissue-culture adaptation. Our findings present an entry mechanism that could be implicated for DENV adaptation and HS-mediated DENV infection.

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2012-04-01
2024-03-28
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References

  1. Añez G., Men R., Eckels K. H., Lai C. J. 2009; Passage of dengue virus type 4 vaccine candidates in fetal rhesus lung cells selects heparin-sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques. J Virol 83:10384–10394 [View Article][PubMed]
    [Google Scholar]
  2. Aoki C., Hidari K. I., Itonori S., Yamada A., Takahashi N., Kasama T., Hasebe F., Islam M. A., Hatano K. other authors 2006; Identification and characterization of carbohydrate molecules in mammalian cells recognized by dengue virus type 2. J Biochem 139:607–614 [View Article][PubMed]
    [Google Scholar]
  3. Belting M. 2003; Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem Sci 28:145–151 [View Article][PubMed]
    [Google Scholar]
  4. Bernfield M., Kokenyesi R., Kato M., Hinkes M. T., Spring J., Gallo R. L., Lose E. J. 1992; Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 8:365–393 [View Article][PubMed]
    [Google Scholar]
  5. Bielefeldt-Ohmann H. 1998; Analysis of antibody-independent binding of dengue viruses and dengue virus envelope protein to human myelomonocytic cells and B lymphocytes. Virus Res 57:63–79 [View Article][PubMed]
    [Google Scholar]
  6. Bielefeldt-Ohmann H., Meyer M., Fitzpatrick D. R., Mackenzie J. S. 2001; Dengue virus binding to human leukocyte cell lines: receptor usage differs between cell types and virus strains. Virus Res 73:81–89 [View Article][PubMed]
    [Google Scholar]
  7. Chen Y., Maguire T., Hileman R. E., Fromm J. R., Esko J. D., Linhardt R. J., Marks R. M. 1997; Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3:866–871 [View Article][PubMed]
    [Google Scholar]
  8. Chen H. C., Hofman F. M., Kung J. T., Lin Y. D., Wu-Hsieh B. A. 2007; Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 81:5518–5526 [View Article][PubMed]
    [Google Scholar]
  9. Chen S. T., Lin Y. L., Huang M. T., Wu M. F., Cheng S. C., Lei H. Y., Lee C. K., Chiou T. W., Wong C. H., Hsieh S. L. 2008; CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453:672–676 [View Article][PubMed]
    [Google Scholar]
  10. Dalrymple N., Mackow E. R. 2011; Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors. J Virol 85:9478–9485 [View Article][PubMed]
    [Google Scholar]
  11. Essner J. J., Chen E., Ekker S. C. 2006; Syndecan-2. Int J Biochem Cell Biol 38:152–156 [View Article][PubMed]
    [Google Scholar]
  12. Germi R., Crance J. M., Garin D., Guimet J., Lortat-Jacob H., Ruigrok R. W., Zarski J. P., Drouet E. 2002; Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 292:162–168 [View Article][PubMed]
    [Google Scholar]
  13. Halstead S. B. 1988; Pathogenesis of dengue: challenges to molecular biology. Science 239:476–481 [View Article][PubMed]
    [Google Scholar]
  14. Halstead S. B. 1989; Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. Rev Infect Dis 11:Suppl. 4S830–S839 [View Article][PubMed]
    [Google Scholar]
  15. Halstead S. B., O’Rourke E. J. 1977; Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146:201–217 [View Article][PubMed]
    [Google Scholar]
  16. Halstead S. B., O’Rourke E. J., Allison A. C. 1977; Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection. J Exp Med 146:218–229 [View Article][PubMed]
    [Google Scholar]
  17. Hilgard P., Stockert R. 2000; Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32:1069–1077 [View Article][PubMed]
    [Google Scholar]
  18. Hung S. L., Lee P. L., Chen H. W., Chen L. K., Kao C. L., King C. C. 1999; Analysis of the steps involved in dengue virus entry into host cells. Virology 257:156–167 [View Article][PubMed]
    [Google Scholar]
  19. Igarashi A. 1979; Characteristics of Aedes albopictus cells persistently infected with dengue viruses. Nature 280:690–691 [View Article][PubMed]
    [Google Scholar]
  20. Kinney R. M., Butrapet S., Chang G. J., Tsuchiya K. R., Roehrig J. T., Bhamarapravati N., Gubler D. J. 1997; Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230:300–308 [View Article][PubMed]
    [Google Scholar]
  21. Kinoshita H., Mathenge E. G., Hung N. T., Huong V. T., Kumatori A., Yu F., Parquet M. C., Inoue S., Matias R. R. other authors 2009; Isolation and characterization of two phenotypically distinct dengue type-2 virus isolates from the same dengue hemorrhagic fever patient. Jpn J Infect Dis 62:343–350[PubMed]
    [Google Scholar]
  22. Kramer K. L., Yost H. J. 2003; Heparan sulfate core proteins in cell–cell signaling. Annu Rev Genet 37:461–484 [View Article][PubMed]
    [Google Scholar]
  23. La Russa V. F., Innis B. L. 1995; Mechanisms of dengue virus-induced bone marrow suppression. Baillieres Clin Haematol 8:249–270 [View Article][PubMed]
    [Google Scholar]
  24. Lee E., Lobigs M. 2002; Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus. J Virol 76:4901–4911 [View Article][PubMed]
    [Google Scholar]
  25. Littaua R., Kurane I., Ennis F. A. 1990; Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J Immunol 144:3183–3186[PubMed]
    [Google Scholar]
  26. Lozzio B. B., Lozzio C. B., Bamberger E. G., Feliu A. S. 1981; A multipotential leukemia cell line (K-562) of human origin. Proc Soc Exp Biol Med 166:546–550[PubMed] [CrossRef]
    [Google Scholar]
  27. Mandl C. W., Kroschewski H., Allison S. L., Kofler R., Holzmann H., Meixner T., Heinz F. X. 2001; Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J Virol 75:5627–5637 [View Article][PubMed]
    [Google Scholar]
  28. Miller J. L., de Wet B. J., Martinez-Pomares L., Radcliffe C. M., Dwek R. A., Rudd P. M., Gordon S. 2008; The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 4:e17 [View Article][PubMed]
    [Google Scholar]
  29. Nakao S., Lai C. J., Young N. S. 1989; Dengue virus, a flavivirus, propagates in human bone marrow progenitors and hematopoietic cell lines. Blood 74:1235–1240[PubMed]
    [Google Scholar]
  30. Navarro-Sanchez E., Altmeyer R., Amara A., Schwartz O., Fieschi F., Virelizier J. L., Arenzana-Seisdedos F., Desprès P. 2003; Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4:723–728 [View Article][PubMed]
    [Google Scholar]
  31. Onlamoon N., Noisakran S., Hsiao H. M., Duncan A., Villinger F., Ansari A. A., Perng G. C. 2010; Dengue virus-induced hemorrhage in a nonhuman primate model. Blood 115:1823–1834 [View Article][PubMed]
    [Google Scholar]
  32. Prestwood T. R., Prigozhin D. M., Sharar K. L., Zellweger R. M., Shresta S. 2008; A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 82:8411–8421 [View Article][PubMed]
    [Google Scholar]
  33. Rothwell S. W., Putnak R., La Russa V. F. 1996; Dengue-2 virus infection of human bone marrow: characterization of dengue-2 antigen-positive stromal cells. Am J Trop Med Hyg 54:503–510[PubMed]
    [Google Scholar]
  34. Saphire A. C., Bobardt M. D., Zhang Z., David G., Gallay P. A. 2001; Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J Virol 75:9187–9200 [View Article][PubMed]
    [Google Scholar]
  35. Schlesinger J. J., Chapman S. E. 1999; Influence of the human high-affinity IgG receptor FcγRI (CD64) on residual infectivity of neutralized dengue virus. Virology 260:84–88 [View Article][PubMed]
    [Google Scholar]
  36. Schlesinger W., Frankel J. W. 1952; Adaptation of the New Guinea B strain of dengue virus to suckling and to adult Swiss mice; a study in viral variation. Am J Trop Med Hyg 1:66–77[PubMed]
    [Google Scholar]
  37. Srikiatkhachorn A., Ajariyakhajorn C., Endy T. P., Kalayanarooj S., Libraty D. H., Green S., Ennis F. A., Rothman A. L. 2007; Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic fever. J Virol 81:1592–1600 [View Article][PubMed]
    [Google Scholar]
  38. Tassaneetrithep B., Burgess T. H., Granelli-Piperno A., Trumpfheller C., Finke J., Sun W., Eller M. A., Pattanapanyasat K., Sarasombath S. other authors 2003; DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197:823–829 [View Article][PubMed]
    [Google Scholar]
  39. 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 [View Article][PubMed]
    [Google Scholar]
  40. Wu S. J., Grouard-Vogel G., Sun W., Mascola J. R., Brachtel E., Putvatana R., Louder M. K., Filgueira L., Marovich M. A. other authors 2000; Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6:816–820 [View Article][PubMed]
    [Google Scholar]
  41. Wu-Hsieh B. A., Yen Y. T., Chen H. C. 2009; Dengue hemorrhage in a mouse model. Ann N Y Acad Sci 1171:Suppl. 1E42–E47 [View Article][PubMed]
    [Google Scholar]
  42. Yu F., Hasebe F., Inoue S., Mathenge E. G., Morita K. 2007; Identification and characterization of RNA-dependent RNA polymerase activity in recombinant Japanese encephalitis virus NS5 protein. Arch Virol 152:1859–1869 [View Article][PubMed]
    [Google Scholar]
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