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
2019-10-18
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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. [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 Biochem 139:, 607–614. [CrossRef] [PubMed]
    [Google Scholar]
  3. Belting M. . ( 2003; ). Heparan sulfate proteoglycan as a plasma membrane carrier. . Trends Biochem Sci 28:, 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 Biol 8:, 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 Res 57:, 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 Res 73:, 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 Med 3:, 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 Virol 81:, 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. . Nature 453:, 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 Virol 85:, 9478–9485. [CrossRef] [PubMed]
    [Google Scholar]
  11. Essner J. J. , Chen E. , Ekker S. C. . ( 2006; ). Syndecan-2. . Int J Biochem Cell Biol 38:, 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. . Virology 292:, 162–168. [CrossRef] [PubMed]
    [Google Scholar]
  13. Halstead S. B. . ( 1988; ). Pathogenesis of dengue: challenges to molecular biology. . Science 239:, 476–481. [CrossRef] [PubMed]
    [Google Scholar]
  14. Halstead S. B. . ( 1989; ). Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. . Rev Infect Dis 11: (Suppl. 4), S830–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 Med 146:, 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 Med 146:, 218–229. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hilgard P. , Stockert R. . ( 2000; ). Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. . Hepatology 32:, 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. . Virology 257:, 156–167. [CrossRef] [PubMed]
    [Google Scholar]
  19. Igarashi A. . ( 1979; ). Characteristics of Aedes albopictus cells persistently infected with dengue viruses. . Nature 280:, 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. . Virology 230:, 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 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. [CrossRef] [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. [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 Virol 76:, 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 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. [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 Pathog 4:, 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. . 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. [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. . Blood 115:, 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 Virol 82:, 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 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. [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. . Virology 260:, 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 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. [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 Med 197:, 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. . Intervirology 47:, 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 Med 6:, 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 Sci 1171: (Suppl. 1), E42–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 Virol 152:, 1859–1869. [CrossRef] [PubMed]
    [Google Scholar]
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