1887

Abstract

The antiviral activity against dengue virus-2 (DENV-2) of carrageenans reported here has shown a differential susceptibility of C6/36 HT and Vero cells, taken as models of mosquito and mammalian cells, depending on the structural class of polysaccharides: all polysaccharides blocked DENV-2 infection in monkey Vero cells, but only iota-carrageenans were virus inhibitors in mosquito cells. However, iota-carrageenans were less effective in mosquito cells in comparison with mammalian cells with effective concentration 50 % (EC) values in C6/36 HT cells 4.9–17.5-fold higher than in Vero cells, as determined by virus yield reduction assay. The mode of action of iota-carrageenan in both cell types was strikingly different: in Vero cells the inhibitory activity was exerted only at the initiation of the cycle, affecting virion binding, whereas in mosquito cells DENV-2 adsorption was not affected and comparable levels of inhibition were obtained if the compound was added to cells together with the virus, after 8 h of infection or by cell pre-treatment before infection. Furthermore, iota-carrageenans induced a subtle alteration in mosquito cells, detected by cell proliferation and protein synthesis analyses, suggesting that a probable cellular target may be responsible for the refractory state of mosquito cells to DENV-2 infection produced by this class of polysulfates. The failure of iota-carrageenan to block DENV-2 adsorption to mosquito cells appeared to be related to the low presence of adequate heparan sulfate (HS) in C6/36 HT cell surface and is indicative of a differential participation of HS residues for DENV-2 entry in both types of cells.

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2011-06-01
2019-10-20
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References

  1. Avirutnan P. , Zhang L. , Punyadee N. , Manuyakorn A. , Puttikhunt C. , Kasinrerk W. , Malasit P. , Atkinson J. P. , Diamond M. S. . ( 2007; ). Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. . PLoS Pathog 3:, e183. [CrossRef] [PubMed]
    [Google Scholar]
  2. Baeuerle P. A. , Huttner W. B. . ( 1986; ). Chlorate–a potent inhibitor of protein sulfation in intact cells. . Biochem Biophys Res Commun 141:, 870–877. [CrossRef] [PubMed]
    [Google Scholar]
  3. Barth H. , Schnober E. K. , Zhang F. , Linhardt R. J. , Depla E. , Boson B. , Cosset F. L. , Patel A. H. , Blum H. E. , Baumert T. F. . ( 2006; ). Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. . J Virol 80:, 10579–10590. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bishop J. R. , Schuksz M. , Esko J. D. . ( 2007; ). Heparan sulphate proteoglycans fine-tune mammalian physiology. . Nature 446:, 1030–1037. [CrossRef] [PubMed]
    [Google Scholar]
  5. Buck C. B. , Thompson C. D. , Roberts J. N. , Müller M. , Lowy D. R. , Schiller J. T. . ( 2006; ). Carrageenan is a potent inhibitor of papillomavirus infection. . PLoS Pathog 2:, e69. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chee H. Y. , AbuBakar S. . ( 2004; ). Identification of a 48kDa tubulin or tubulin-like C6/36 mosquito cells protein that binds dengue virus 2 using mass spectrometry. . Biochem Biophys Res Commun 320:, 11–17. [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. Damonte E. B. , Matulewicz M. C. , Cerezo A. S. . ( 2004; ). Sulfated seaweed polysaccharides as antiviral agents. . Curr Med Chem 11:, 2399–2419.[PubMed] [CrossRef]
    [Google Scholar]
  9. de S.F-Tischer P. C. , Talarico L. B. , Noseda M. D. , Guimaraes S. M. P. B. , Damonte E. B. , Duarte M. E. R. . ( 2006; ). Chemical structure and antiviral activity of carrageenans from Meristiella gelidium against herpes simplex and dengue virus. . Carbohydr Polym 63:, 459–465. [CrossRef]
    [Google Scholar]
  10. Esko J. D. , Selleck S. B. . ( 2002; ). Order out of chaos: assembly of ligand binding sites in heparan sulfate. . Annu Rev Biochem 71:, 435–471. [CrossRef] [PubMed]
    [Google Scholar]
  11. 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]
  12. Gubler D. J. . ( 2002; ). Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. . Trends Microbiol 10:, 100–103. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hidari K. I. , Takahashi N. , Arihara M. , Nagaoka M. , Morita K. , Suzuki T. . ( 2008; ). Structure and anti-dengue virus activity of sulfated polysaccharide from a marine alga. . Biochem Biophys Res Commun 376:, 91–95. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hilgard P. , Stockert R. . ( 2000; ). Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. . Hepatology 32:, 1069–1077. [CrossRef] [PubMed]
    [Google Scholar]
  15. 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]
  16. Hung J. J. , Hsieh M. T. , Young M. J. , Kao C. L. , King C. C. , Chang W. . ( 2004; ). 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. . J Virol 78:, 378–388. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kuadkitkan A. , Wikan N. , Fongsaran C. , Smith D. R. . ( 2010; ). Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells. . Virology 406:, 149–161. [CrossRef] [PubMed]
    [Google Scholar]
  18. Lee E. , Pavy M. , Young N. , Freeman C. , Lobigs M. . ( 2006; ). Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. . Antiviral Res 69:, 31–38. [CrossRef] [PubMed]
    [Google Scholar]
  19. Lin Y. L. , Lei H. Y. , Lin Y. S. , Yeh T. M. , Chen S. H. , Liu H. S. . ( 2002; ). Heparin inhibits dengue-2 virus infection of five human liver cell lines. . Antiviral Res 56:, 93–96. [CrossRef] [PubMed]
    [Google Scholar]
  20. Marks R. M. , Lu H. , Sundaresan R. , Toida T. , Suzuki A. , Imanari T. , Hernáiz M. J. , Linhardt R. J. . ( 2001; ). Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycan-derived inhibitors. . J Med Chem 44:, 2178–2187. [CrossRef] [PubMed]
    [Google Scholar]
  21. Martínez-Barragán J. J. , del Angel R. M. . ( 2001; ). Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection. . J Virol 75:, 7818–7827. [CrossRef] [PubMed]
    [Google Scholar]
  22. Ono L. , Wollinger W. , Rocco I. M. , Coimbra T. L. , Gorin P. A. , Sierakowski M. R. . ( 2003; ). In vitro and in vivo antiviral properties of sulfated galactomannans against yellow fever virus (BeH111 strain) and dengue 1 virus (Hawaii strain). . Antiviral Res 60:, 201–208. [CrossRef] [PubMed]
    [Google Scholar]
  23. Paingankar M. S. , Gokhale M. D. , Deobagkar D. N. . ( 2010; ). Dengue-2-virus-interacting polypeptides involved in mosquito cell infection. . Arch Virol 155:, 1453–1461. [CrossRef] [PubMed]
    [Google Scholar]
  24. Pujol C. A. , Estevez J. M. , Carlucci M. J. , Ciancia M. , Cerezo A. S. , Damonte E. B. . ( 2002; ). Novel DL-galactan hybrids from the red seaweed Gymnogongrus torulosus are potent inhibitors of herpes simplex virus and dengue virus. . Antivir Chem Chemother 13:, 83–89.[PubMed] [CrossRef]
    [Google Scholar]
  25. Qiu H. , Tang W. , Tong X. , Ding K. , Zuo J. . ( 2007; ). Structure elucidation and sulfated derivatives preparation of two α-d-glucans from Gastrodia elata Bl. and their anti-dengue virus bioactivities. . Carbohydr Res 342:, 2230–2236. [CrossRef] [PubMed]
    [Google Scholar]
  26. Rostand K. S. , Esko J. D. . ( 1997; ). Microbial adherence to and invasion through proteoglycans. . Infect Immun 65:, 1–8.[PubMed]
    [Google Scholar]
  27. Salas-Benito J. , Reyes-Del Valle J. , Salas-Benito M. , Ceballos-Olvera I. , Mosso C. , del Angel R. M. . ( 2007; ). 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. . Am J Trop Med Hyg 77:, 283–290.[PubMed]
    [Google Scholar]
  28. Sessions O. M. , Barrows N. J. , Souza-Neto J. A. , Robinson T. J. , Hershey C. L. , Rodgers M. A. , Ramirez J. L. , Dimopoulos G. , Yang P. L. et al. ( 2009; ). Discovery of insect and human dengue virus host factors. . Nature 458:, 1047–1050. [CrossRef] [PubMed]
    [Google Scholar]
  29. Sinnis P. , Coppi A. , Toida T. , Toyoda H. , Kinoshita-Toyoda A. , Xie J. , Kemp M. M. , Linhardt R. J. . ( 2007; ). Mosquito heparan sulfate and its potential role in malaria infection and transmission. . J Biol Chem 282:, 25376–25384. [CrossRef] [PubMed]
    [Google Scholar]
  30. Spillmann D. . ( 2001; ). Heparan sulfate: anchor for viral intruders?. Biochimie 83:, 811–817. [CrossRef] [PubMed]
    [Google Scholar]
  31. Talarico L. B. , Damonte E. B. . ( 2007; ). Interference in dengue virus adsorption and uncoating by carrageenans. . Virology 363:, 473–485. [CrossRef] [PubMed]
    [Google Scholar]
  32. Talarico L. B. , Pujol C. A. , Zibetti R. G. , Faría P. C. , Noseda M. D. , Duarte M. E. , Damonte E. B. . ( 2005; ). The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell. . Antiviral Res 66:, 103–110. [CrossRef] [PubMed]
    [Google Scholar]
  33. Talarico L. B. , Duarte M. E. , Zibetti R. G. , Noseda M. D. , Damonte E. B. . ( 2007; ). An algal-derived DL-galactan hybrid is an efficient preventing agent for in vitro dengue virus infection. . Planta Med 73:, 1464–1468. [CrossRef] [PubMed]
    [Google Scholar]
  34. Thaisomboonsuk B. K. , Clayson E. T. , Pantuwatana S. , Vaughn D. W. , Endy T. P. . ( 2005; ). Characterization of dengue-2 virus binding to surfaces of mammalian and insect cells. . Am J Trop Med Hyg 72:, 375–383.[PubMed]
    [Google Scholar]
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