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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.037853-0
2012-04-01
2020-07-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/4/761.html?itemId=/content/journal/jgv/10.1099/vir.0.037853-0&mimeType=html&fmt=ahah

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 Virol83:10384–10394 [CrossRef][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 Biochem139:607–614 [CrossRef][PubMed]
    [Google Scholar]
  3. Belting M.. 2003; Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem Sci28:145–151 [CrossRef][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 Biol8:365–393 [CrossRef][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 Res57:63–79 [CrossRef][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 Res73:81–89 [CrossRef][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 Med3:866–871 [CrossRef][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 Virol81:5518–5526 [CrossRef][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. Nature453:672–676 [CrossRef][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 Virol85:9478–9485 [CrossRef][PubMed]
    [Google Scholar]
  11. Essner J. J., Chen E., Ekker S. C.. 2006; Syndecan-2. Int J Biochem Cell Biol38:152–156 [CrossRef][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. Virology292:162–168 [CrossRef][PubMed]
    [Google Scholar]
  13. Halstead S. B.. 1988; Pathogenesis of dengue: challenges to molecular biology. Science239:476–481 [CrossRef][PubMed]
    [Google Scholar]
  14. Halstead S. B.. 1989; Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. Rev Infect Dis11:Suppl. 4S830–S839 [CrossRef][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 Med146:201–217 [CrossRef][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 Med146:218–229 [CrossRef][PubMed]
    [Google Scholar]
  17. Hilgard P., Stockert R.. 2000; Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology32:1069–1077 [CrossRef][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. Virology257:156–167 [CrossRef][PubMed]
    [Google Scholar]
  19. Igarashi A.. 1979; Characteristics of Aedes albopictus cells persistently infected with dengue viruses. Nature280:690–691 [CrossRef][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. Virology230:300–308 [CrossRef][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 Dis62:343–350[PubMed]
    [Google Scholar]
  22. Kramer K. L., Yost H. J.. 2003; Heparan sulfate core proteins in cell–cell signaling. Annu Rev Genet37:461–484 [CrossRef][PubMed]
    [Google Scholar]
  23. La Russa V. F., Innis B. L.. 1995; Mechanisms of dengue virus-induced bone marrow suppression. Baillieres Clin Haematol8:249–270 [CrossRef][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 Virol76:4901–4911 [CrossRef][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 Immunol144:3183–3186[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 Med166:546–550[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 Virol75:5627–5637 [CrossRef][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 Pathog4:e17 [CrossRef][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. Blood74:1235–1240[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 Rep4:723–728 [CrossRef][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. Blood115:1823–1834 [CrossRef][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 Virol82:8411–8421 [CrossRef][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 Hyg54:503–510[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 Virol75:9187–9200 [CrossRef][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. Virology260:84–88 [CrossRef][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 Hyg1:66–77[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 Virol81:1592–1600 [CrossRef][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 Med197:823–829 [CrossRef][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. Intervirology47:78–86 [CrossRef][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 Med6:816–820 [CrossRef][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 Sci1171:Suppl. 1E42–E47 [CrossRef][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 Virol152:1859–1869 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.037853-0
Loading
/content/journal/jgv/10.1099/vir.0.037853-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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