1887

Abstract

Newcastle disease virus (NDV) is a member of subfamily and can infect most species of birds causing severe economic losses. The current control measure is vaccination, but infections cannot be completely prevented. It remains a constant threat to the poultry industry and new control measures are urgently needed. This study demonstrates that sulfated polysaccharides (sCVPSs) were potent inhibitors of NDV, with 50 % inhibitory concentrations (IC) ranging from 62.55 to 76.31 µg ml in Baby hamster kidney fibroblasts clone 21 (BHK-21) and from 101.57 to 125.90 µg ml in chicken embryo fibroblasts (CEF). sCVPS is more effective than heparan sulfate (HS; as a positive control) with IC values of 99.28 µg ml in BHK-21 and 118.79 µg ml in CEF. sCVPSs and HS exhibit anti-NDV activity by prevention of the early stages of viral life. The mechanism of action study indicated that virus adsorption in BHK-21, and both virus adsorption and penetration in CEF were inhibited by sCVPSs. When the number of viruses was increased to an m.o.i. of 0.1 in the immunofluorescence study and to an m.o.i. of 1 in the fluorescent quantitative PCR study, viral infection was also significantly suppressed; the antiviral activity of sCVPSs was independent of the m.o.i. sCVPSs also prevented the cell-to-cell spread of NDV. tests carried out on specific pathogen-free (SPF) chickens showed that sCVPSs also inhibited virus multiplication in heart, liver, spleen, lung and kidney. These results indicated that sCVPSs perform more effectively than HS as antiviral agents against NDV, and can be further examined for their potential as an alternative control measure for NDV infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.054270-0
2013-10-01
2019-09-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/10/2164.html?itemId=/content/journal/jgv/10.1099/vir.0.054270-0&mimeType=html&fmt=ahah

References

  1. Aguilar H. C. , Lee B. . ( 2011; ). Emerging paramyxoviruses: molecular mechanisms and antiviral strategies. . Expert Rev Mol Med 13:, e6. [CrossRef] [PubMed]
    [Google Scholar]
  2. Antoine T. E. , Mishra Y. K. , Trigilio J. , Tiwari V. , Adelung R. , Shukla D. . ( 2012; ). Prophylactic, therapeutic and neutralizing effects of zinc oxide tetrapod structures against herpes simplex virus type-2 infection. . Antiviral Res 96:, 363–375. [CrossRef] [PubMed]
    [Google Scholar]
  3. Baba M. , Nakajima M. , Schols D. , Pauwels R. , Balzarini J. , De Clercq E. . ( 1988; ). Pentosan polysulfate, a sulfated oligosaccharide, is a potent and selective anti-HIV agent in vitro. . Antiviral Res 9:, 335–343. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bhella D. , Ralph A. , Murphy L. B. , Yeo R. P. . ( 2002; ). Significant differences in nucleocapsid morphology within the Paramyxoviridae. . J Gen Virol 83:, 1831–1839.[PubMed]
    [Google Scholar]
  5. Bourgeois C. , Bour J. B. , Lidholt K. , Gauthray C. , Pothier P. . ( 1998; ). Heparin-like structures on respiratory syncytial virus are involved in its infectivity in vitro. . J Virol 72:, 7221–7227.[PubMed]
    [Google Scholar]
  6. Connaris H. , Takimoto T. , Russell R. , Crennell S. , Moustafa I. , Portner A. , Taylor G. . ( 2002; ). Probing the sialic acid binding site of the hemagglutinin-neuraminidase of Newcastle disease virus: identification of key amino acids involved in cell binding, catalysis, and fusion. . J Virol 76:, 1816–1824. [CrossRef] [PubMed]
    [Google Scholar]
  7. Crennell S. , Takimoto T. , Portner A. , Taylor G. . ( 2000; ). Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. . Nat Struct Biol 7:, 1068–1074. [CrossRef] [PubMed]
    [Google Scholar]
  8. Damonte E. , Neyts J. , Pujol C. A. , Snoeck R. , Andrei G. , Ikeda S. , Witvrouw M. , Reymen D. , Haines H. . & other authors ( 1994; ). Antiviral activity of a sulphated polysaccharide from the red seaweed Nothogenia fastigiata . . Biochem Pharmacol 47:, 2187–2192. [CrossRef] [PubMed]
    [Google Scholar]
  9. Damonte E. B. , Matulewicz M. C. , Cerezo A. S. . ( 2004; ). Sulfated seaweed polysaccharides as antiviral agents. . Curr Med Chem 11:, 2399–2419. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dodgson K. S. , Price R. G. . ( 1962; ). A note on the determination of the ester sulphate content of sulphated polysaccharides. . Biochem J 84:, 106–110.[PubMed]
    [Google Scholar]
  11. Dortmans J. C. , Rottier P. J. M. , Koch G. , Peeters B. P. . ( 2011; ). Passaging of a Newcastle disease virus pigeon variant in chickens results in selection of viruses with mutations in the polymerase complex enhancing virus replication and virulence. . J Gen Virol 92:, 336–345. [CrossRef] [PubMed]
    [Google Scholar]
  12. Elizondo-Gonzalez R. , Cruz-Suarez L. E. , Ricque-Marie D. , Mendoza-Gamboa E. , Rodriguez-Padilla C. , Trejo-Avila L. M. . ( 2012; ). In vitro characterization of the antiviral activity of fucoidan from Cladosiphon okamuranus against Newcastle Disease Virus. . Virol J 9:, 307. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gerber P. , Dutcher J. D. , Adams E. V. , Sherman J. H. . ( 1958; ). Protective effect of seaweed extracts for chicken embryos infected with influenza B or mumps virus. . Proc Soc Exp Biol Med 99:, 590–593. [CrossRef] [PubMed]
    [Google Scholar]
  14. González M. E. , Alarcón B. , Carrasco L. . ( 1987; ). Polysaccharides as antiviral agents: antiviral activity of carrageenan. . Antimicrob Agents Chemother 31:, 1388–1393. [CrossRef] [PubMed]
    [Google Scholar]
  15. Han S. Q. , Yoshida D. , Kanamoto T. , Nakashima H. , Uryu T. , Yoshida T. . ( 2010; ). Sulfated oligosaccharide cluster with polylysine core scaffold as a new anti-HIV dendrimer. . Carbohydr Polym 80:, 1111–1115. [CrossRef]
    [Google Scholar]
  16. Harden E. A. , Falshaw R. , Carnachan S. M. , Kern E. R. , Prichard M. N. . ( 2009; ). Virucidal activity of polysaccharide extracts from four algal species against herpes simplex virus. . Antiviral Res 83:, 282–289. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hasui M. , Matsuda M. , Okutani K. , Shigeta S. . ( 1995; ). In vitro antiviral activities of sulfated polysaccharides from a marine microalga (Cochlodinium polykrikoides) against human immunodeficiency virus and other enveloped viruses. . Int J Biol Macromol 17:, 293–297. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hayashi T. , Hayashi K. , Maeda M. , Kojima I. . ( 1996; ). Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis . . J Nat Prod 59:, 83–87. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hosoya M. , Balzarini J. , Shigeta S. , De Clercq E. . ( 1991; ). Differential inhibitory effects of sulfated polysaccharides and polymers on the replication of various myxoviruses and retroviruses, depending on the composition of the target amino acid sequences of the viral envelope glycoproteins. . Antimicrob Agents Chemother 35:, 2515–2520. [CrossRef] [PubMed]
    [Google Scholar]
  20. Huang X. Y. , Wang D. Y. , Hu Y. L. , Lu Y. , Guo Z. H. , Kong X. F. , Sun J. L. . ( 2008; ). Effect of sulfated astragalus polysaccharide on cellular infectivity of infectious bursal disease virus. . Int J Biol Macromol 42:, 166–171. [CrossRef] [PubMed]
    [Google Scholar]
  21. 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]
  22. Liu J. , Thorp S. C. . ( 2002; ). Cell surface heparan sulfate and its roles in assisting viral infections. . Med Res Rev 22:, 1–25. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lu Y. , Wang D. , Hu Y. , Huang X. , Wang J. . ( 2008; ). Sulfated modification of epimedium polysaccharide and effects of the modifiers on cellular infectivity of IBDV. . Carbohydr Polym 71:, 180–186. [CrossRef]
    [Google Scholar]
  24. Mahon P. J. , Mirza A. M. , Iorio R. M. . ( 2011; ). Role of the two sialic acid binding sites on the Newcastle disease virus HN protein in triggering the interaction with the F protein required for the promotion of fusion. . J Virol 85:, 12079–12082. [CrossRef] [PubMed]
    [Google Scholar]
  25. Mastromarino P. , Petruzziello R. , Macchia S. , Rieti S. , Nicoletti R. , Orsi N. . ( 1997; ). Antiviral activity of natural and semisynthetic polysaccharides on the early steps of rubella virus infection. . J Antimicrob Chemother 39:, 339–345. [CrossRef] [PubMed]
    [Google Scholar]
  26. Miller P. J. , Decanini E. L. , Afonso C. L. . ( 2010; ). Newcastle disease: evolution of genotypes and the related diagnostic challenges. . Infect Genet Evol 10:, 26–35. [CrossRef] [PubMed]
    [Google Scholar]
  27. Nguyen T. L. , Chen J. , Hu Y. , Wang D. , Fan Y. , Wang J. , Abula S. , Zhang J. , Qin T. . & other authors ( 2012; ). In vitro antiviral activity of sulfated Auricularia auricula polysaccharides. . Carbohydr Polym 90:, 1254–1258. [CrossRef] [PubMed]
    [Google Scholar]
  28. Nyberg K. , Ekblad M. , Bergström T. , Freeman C. , Parish C. R. , Ferro V. , Trybala E. . ( 2004; ). The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. . Antiviral Res 63:, 15–24. [CrossRef] [PubMed]
    [Google Scholar]
  29. Porotto M. , Salah Z. , DeVito I. , Talekar A. , Palmer S. G. , Xu R. , Wilson I. A. , Moscona A. . ( 2012; ). The second receptor binding site of the globular head of the Newcastle disease virus hemagglutinin-neuraminidase activates the stalk of multiple paramyxovirus receptor binding proteins to trigger fusion. . J Virol 86:, 5730–5741. [CrossRef] [PubMed]
    [Google Scholar]
  30. Pourianfar H. R. , Poh C. L. , Fecondo J. , Grollo L. . ( 2012; ). In vitro evaluation of the antiviral activity of heparan sulfate mimetic compounds against Enterovirus 71. . Virus Res 169:, 22–29. [CrossRef] [PubMed]
    [Google Scholar]
  31. Pujol C. A. , Carlucci M. J. , Matulewicz M. C. , Damonte E. B. . ( 2007; ). Natural sulfated polysaccharides for the prevention and control of viral infections. . Top Heterocycl Chem 11:, 259–281. [CrossRef]
    [Google Scholar]
  32. Ravindra P. V. , Tiwari A. K. , Ratta B. , Bais M. V. , Chaturvedi U. , Palia S. K. , Sharma B. , Chauhan R. S. . ( 2009; ). Time course of Newcastle disease virus-induced apoptotic pathways. . Virus Res 144:, 350–354. [CrossRef] [PubMed]
    [Google Scholar]
  33. Reed L. J. , Muench H. . ( 1938; ). A simple method of estimating fifty percent endpoints. . Am J Hyg 27:, 493–497.
    [Google Scholar]
  34. Song X. , Xu J. , Yin Z. Q. , Jia R. Y. , Cheng A. C. , Deng Y. X. , C. , Liang X. X. , Wang Y. . & other authors ( 2013a; ). Effects of polysaccharide from Chuanminshen violaceum on immune response of Newcastle disease vaccine in chicken. . Acta Sci Vet 41: 1104
    [Google Scholar]
  35. Song X. , Yin Z. , Li L. , Cheng A. , Jia R. , Xu J. , Wang Y. , Yao X. , Lv C. , Zhao X. . ( 2013b; ). Antiviral activity of sulfated Chuanminshen violaceum polysaccharide against duck enteritis virus in vitro. . Antiviral Res 98:, 344–351. [CrossRef] [PubMed]
    [Google Scholar]
  36. Talarico L. B. , Damonte E. B. . ( 2007; ). Interference in dengue virus adsorption and uncoating by carrageenans. . Virology 363:, 473–485. [CrossRef] [PubMed]
    [Google Scholar]
  37. Wang D. Y. , Guo Z. H. , Ma X. , Hu Y. L. , Huang X. Y. , Fan Y. P. , Yang S. J. , Guo L. . ( 2010a; ). Effects of sulfated lentinan on cellular infectivity of avian infectious bronchitis virus. . Carbohydr Polym 79:, 461–465. [CrossRef]
    [Google Scholar]
  38. Wang J. , Hu Y. , Wang D. , Zhang F. , Zhao X. , Abula S. , Fan Y. , Guo L. . ( 2010b; ). Lycium barbarum polysaccharide inhibits the infectivity of Newcastle disease virus to chicken embryo fibroblast. . Int J Biol Macromol 46:, 212–216. [CrossRef] [PubMed]
    [Google Scholar]
  39. Wang W. , Zhang P. , Hao C. , Zhang X. E. , Cui Z. Q. , Guan H. S. . ( 2011; ). In vitro inhibitory effect of carrageenan oligosaccharide on influenza A H1N1 virus. . Antiviral Res 92:, 237–246. [CrossRef] [PubMed]
    [Google Scholar]
  40. Wijesekara I. , Pangestuti R. , Kim S. K. . ( 2011; ). Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. . Carbohydr Polym 84:, 14–21. [CrossRef]
    [Google Scholar]
  41. Witvrouw M. , Schols D. , Andrei G. , Snoeck R. , Hosoya M. , Pauwels R. , Balzarini J. , De Clercq E. . ( 1991; ). Antiviral activity of low-MW dextran sulphate (derived from dextran MW 1000) compared to dextran sulphate samples of higher MW. . Antivir Chem Chemother 2:, 171–179.[CrossRef]
    [Google Scholar]
  42. Witvrouw M. , Este J. , Mateu M. , Reymen D. , Andrei G. , Snoeck R. , Ikeda S. , Pauwels R. , Bianchini N. . & other authors ( 1994; ). Activity of a sulfated polysaccharide extracted from the red seaweed Aghardhiella tenera against human immunodeficiency virus and other enveloped viruses. . Antivir Chem Chemother 5:, 297–303.[CrossRef]
    [Google Scholar]
  43. Zaitsev V. , von Itzstein M. , Groves D. , Kiefel M. , Takimoto T. , Portner A. , Taylor G. . ( 2004; ). Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. . J Virol 78:, 3733–3741. [CrossRef] [PubMed]
    [Google Scholar]
  44. Zhang R. , Pu J. , Su J. , Zhao J. , Wang X. , Zhang S. , Li X. , Zhang G. . ( 2010; ). Phylogenetic characterization of Newcastle disease virus isolated in the mainland of China during 2001–2009. . Vet Microbiol 141:, 246–257. [CrossRef] [PubMed]
    [Google Scholar]
  45. Zhang S. , Wang X. , Zhao C. , Liu D. , Hu Y. , Zhao J. , Zhang G. . ( 2011; ). Phylogenetic and pathotypical analysis of two virulent Newcastle disease viruses isolated from domestic ducks in China. . PLoS ONE 6:, e25000. [CrossRef] [PubMed]
    [Google Scholar]
  46. Zhao X. N. , Hu Y. L. , Wang D. Y. , Guo L. W. , Yang S. J. , Fan Y. P. , Zhao B. K. , Wang Y. L. , Abula S. . ( 2011; ). Optimization of sulfated modification conditions of tremella polysaccharide and effects of modifiers on cellular infectivity of NDV. . Int J Biol Macromol 49:, 44–49. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.054270-0
Loading
/content/journal/jgv/10.1099/vir.0.054270-0
Loading

Data & Media loading...

Most Cited This Month

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