1887

Abstract

The present study was aimed at evaluating an underlying mechanism of the antiviral activity of the sulfated galactans (SG) isolated from the red seaweed against white spot syndrome virus (WSSV) infection in haemocytes of the black tiger shrimp . Primary culture of haemocytes from was performed and inoculated with WSSV, after which the cytopathic effect (CPE), cell viability and viral load were determined. Haemocytes treated with WSSV-SG pre-mix showed decreased CPE, viral load and cell mortality from the viral infection. Solid-phase virus-binding assays revealed that SG bound to WSSV in a dose-related manner. Far Western blotting analysis indicated that SG bound to VP 26 and VP 28 proteins of WSSV. In contrast to the native SG, desulfated SG did not reduce CPE and cell mortality, and showed low binding activity with WSSV. The current study suggests that SG from elicits its anti-WSSV activity by binding to viral proteins that are important for the process of viral attachment to the host cells. It is anticipated that the sulfate groups of SG are important for viral binding.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.062919-0
2014-05-01
2019-12-05
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/5/1126.html?itemId=/content/journal/jgv/10.1099/vir.0.062919-0&mimeType=html&fmt=ahah

References

  1. Balasubramanian G. , Sarathi M. , Rajesh Kumar S. , Sahul Hameed A. S. . ( 2007; ). Screening the antiviral activity of Indian medicinal plants against white spot syndrome virus in shrimp. . Aquaculture 263:, 15–19. [CrossRef]
    [Google Scholar]
  2. Betancur-Galvis L. A. , Morales G. E. , Forero J. E. , Roldan J. . ( 2002; ). Cytotoxic and antiviral activities of Colombian medicinal plant extracts of the Euphorbia genus. . Mem Inst Oswaldo Cruz 97:, 541–546. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bridges C. C. , Battle J. R. , Zalups R. K. . ( 2007; ). Transport of thiol-conjugates of inorganic mercury in human retinal pigment epithelial cells. . Toxicol Appl Pharmacol 221:, 251–260. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chaivisuthangkura P. , Tangkhabuanbutra J. , Longyant S. , Sithigorngul W. , Rukpratanporn S. , Menasveta P. , Sithigorngul P. . ( 2004; ). Monoclonal antibodies against a truncated viral envelope protein (VP28) can detect white spot syndrome virus (WSSV) infections in shrimp. . Sci Asia 30:, 359–363. [CrossRef]
    [Google Scholar]
  5. Chaivisuthangkura P. , Phattanapaijitkul P. , Thammapalerd N. , Rukpratanporn S. , Longyant S. , Sithigorngul W. , Sithigorngul P. . ( 2006; ). Production of polyclonal antibodies against recombinant VP26 structural protein of white spot syndrome virus (WSSV). . Sci Asia 32:, 201–204. [CrossRef]
    [Google Scholar]
  6. Chattopadhyay K. , Mateu C. G. , Mandal P. , Pujol C. A. , Damonte E. B. , Ray B. . ( 2007; ). Galactan sulfate of Grateloupia indica: isolation, structural features and antiviral activity. . Phytochemistry 68:, 1428–1435. [CrossRef] [PubMed]
    [Google Scholar]
  7. Chattopadhyay K. , Ghosh T. , Pujol C. A. , Carlucci M. J. , Damonte E. B. , Ray B. . ( 2008; ). Polysaccharides from Gracilaria corticata: sulfation, chemical characterization and anti-HSV activities. . Int J Biol Macromol 43:, 346–351. [CrossRef] [PubMed]
    [Google Scholar]
  8. Chotigeat W. , Tongsupa S. , Supamataya K. , Phongdara A. . ( 2004; ). Effect of fucoidan on disease resistance of black tiger shrimp. . Aquaculture 233:, 23–30. [CrossRef]
    [Google Scholar]
  9. Citarasu T. , Sivaram V. , Immanuel G. , Rout N. , Murugan V. . ( 2006; ). Influence of selected Indian immunostimulant herbs against white spot syndrome virus (WSSV) infection in black tiger shrimp, Penaeus monodon with reference to haematological, biochemical and immunological changes. . Fish Shellfish Immunol 21:, 372–384. [CrossRef] [PubMed]
    [Google Scholar]
  10. Copeland R. , Balasubramaniam A. , Tiwari V. , Zhang F. , Bridges A. , Linhardt R. J. , Shukla D. , Liu J. . ( 2008; ). Using a 3-O-sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1. . Biochemistry 47:, 5774–5783. [CrossRef] [PubMed]
    [Google Scholar]
  11. Cruz-Suãrez L. E. , Tapia-Salazar M. , Nieto-Lopez M. G. , Ricque-Marie D. . ( 2009; ). Use of seaweeds for shrimp nutrition: status and potential. . In The Rising Tide, Proceedings of the Special Session on Sustainable Shrimp Farming, World Aquaculture 2009, pp 147–163. Edited by Browdy C. L. , Jory D. F. . . Baton Rouge, LA:: The World Aquaculture Society;.
    [Google Scholar]
  12. 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]
  13. de Almeida C. L. F. , Falcão H. de S. , Lima G. R. de M. , Montenegro C. de A. , Lira N. S. , de Athayde-Filho P. F. , Rodrigues L. C. , de Souza M. de F. V. , Barbosa-Filho J. M. , Batista L. M. . ( 2011; ). Bioactivities from marine algae of the genus Gracilaria . . Int J Mol Sci 12:, 4550–4573. [CrossRef] [PubMed]
    [Google Scholar]
  14. Edmondson D. G. , Roth S. Y. . ( 2001; ). Identification of protein interactions by far Western analysis. . Curr Protoc Mol Biol 20:, 20.6.[PubMed]
    [Google Scholar]
  15. Escobedo-Bonilla C. M. , Alday-Sanz V. , Wille M. , Sorgeloos P. , Pensaert M. B. , Nauwynck H. J. . ( 2008; ). A review on the morphology, molecular characterization, morphogenesis and pathogenesis of white spot syndrome virus. . J Fish Dis 31:, 1–18. [CrossRef] [PubMed]
    [Google Scholar]
  16. Falshaw R. , Furneaux R. H. . ( 1998; ). Structural analysis of carrageenans from the tetrasporic stages of the red algae, Gigartina lanceata and Gigartina chapmanii . . Carbohydr Res 307:, 325–331. [CrossRef]
    [Google Scholar]
  17. Feng Y. , Press B. , Wandinger-Ness A. . ( 1995; ). Rab 7: an important regulator of late endocytic membrane traffic. . J Cell Biol 131:, 1435–1452. [CrossRef] [PubMed]
    [Google Scholar]
  18. Ghosh T. , Chattopadhyay K. , Marschall M. , Karmakar P. , Mandal P. , Ray B. . ( 2009; ). Focus on antivirally active sulfated polysaccharides: from structure–activity analysis to clinical evaluation. . Glycobiology 19:, 2–15. [CrossRef] [PubMed]
    [Google Scholar]
  19. Gu W. , Yuan J. , Xu G. , Li L. , Liu N. , Zhang C. , Zhang J. , Shi Z. . ( 2007; ). Production and characterization of monoclonal antibodies of shrimp white spot syndrome virus envelope protein VP28. . Virol Sin 22:, 21–25. [CrossRef]
    [Google Scholar]
  20. Hames B. D. . (editor) ( 1998; ). Gel Electrophoresis ofPproteins: aPpractical Approach (The Practical Approach Series vol. 197), , 3rd edn.. Oxford:: Oxford University Press;.
    [Google Scholar]
  21. Hidari K. I. P. J. , 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]
  22. Hou W. Y. , Chen J. C. . ( 2005; ). The immunostimulatory effect of hot-water extract of Gracilaria tenuistipitata on the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus . . Fish Shellfish Immunol 19:, 127–138. [CrossRef] [PubMed]
    [Google Scholar]
  23. Huang Z. J. , Kang S. T. , Leu J. H. , Chen L. L. . ( 2013; ). Endocytic pathway is indicated for white spot syndrome virus (WSSV) entry in shrimp. . Fish Shellfish Immunol 35:, 707–715. [CrossRef] [PubMed]
    [Google Scholar]
  24. Immanuel G. , Sivagnanavelmurugan M. , Marudhupandi T. , Radhakrishnan S. , Palavesam A. . ( 2012; ). The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab). . Fish Shellfish Immunol 32:, 551–564. [CrossRef] [PubMed]
    [Google Scholar]
  25. Jiang Y. , Zhan W. , Wang S. , Xing J. . ( 2006; ). Development of primary shrimp hemocyte cultures of Penaeus chinensis to study white spot syndrome virus (WSSV) infection. . Aquaculture 253:, 114–119. [CrossRef]
    [Google Scholar]
  26. Jose S. , Mohandas A. , Philip R. , Bright Singh I. S. . ( 2010; ). Primary hemocyte culture of Penaeus monodon as an in vitro model for white spot syndrome virus titration, viral and immune related gene expression and cytotoxicity assays. . J Invertebr Pathol 105:, 312–321. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kanjana K. , Radtanatip T. , Asuvapongpatana S. , Withyachumnarnkul B. , Wongprasert K. . ( 2011; ). Solvent extracts of the red seaweed Gracilaria fisheri prevent Vibrio harveyi infections in the black tiger shrimp Penaeus monodon . . Fish Shellfish Immunol 30:, 389–396. [CrossRef] [PubMed]
    [Google Scholar]
  28. Li L. , Xie X. , Yang F. . ( 2005; ). Identification and characterization of a prawn white spot syndrome virus gene that encodes an envelope protein VP31. . Virology 340:, 125–132. [CrossRef] [PubMed]
    [Google Scholar]
  29. Li L. J. , Yuan J. F. , Cai C. A. , Gu W. G. , Shi Z. L. . ( 2006; ). Multiple envelope proteins are involved in white spot syndrome virus (WSSV) infection in crayfish. . Arch Virol 151:, 1309–1317. [CrossRef] [PubMed]
    [Google Scholar]
  30. Maciel J. S. , Chaves L. S. , Souza B. W. S. , Teixeira D. I. A. , Freitas A. L. P. , Feitosa J. P. A. , de Paula R. C. M. . ( 2008; ). Structural characterization of cold extracted fraction of soluble sulfated polysaccharide from red seaweed Gracilaria birdiae . . Carbohydr Polym 71:, 559–565. [CrossRef]
    [Google Scholar]
  31. Matsuhiro B. , Conte A. F. , Damonte E. B. , Kolender A. A. , Matulewicz M. C. , Mejías E. G. , Pujol C. A. , Zúñiga E. A. . ( 2005; ). Structural analysis and antiviral activity of a sulfated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rhodophyta). . Carbohydr Res 340:, 2392–2402. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mazumder S. , Ghosal P. K. , Pujol C. A. , Carlucci M. J. , Damonte E. B. , Ray B. . ( 2002; ). Isolation, chemical investigation and antiviral activity of polysaccharides from Gracilaria corticata (Gracilariaceae, Rhodophyta). . Int J Biol Macromol 31:, 87–95. [CrossRef] [PubMed]
    [Google Scholar]
  33. Otta S. K. . ( 2012; ). Host and virus protein interaction studies in understanding shrimp virus gene function. . Indian J Virol 23:, 184–190. [CrossRef] [PubMed]
    [Google Scholar]
  34. Pereira M. G. , Benevides N. M. , Melo M. R. , Valente A. P. , Melo F. R. , Mourão P. A. . ( 2005; ). Structure and anticoagulant activity of a sulfated galactan from the red alga, Gelidium crinale. Is there a specific structural requirement for the anticoagulant action. ? Carbohydr Res 340:, 2015–2023. [CrossRef] [PubMed]
    [Google Scholar]
  35. Pomin V. H. , Mourão P. A. S. . ( 2008; ). Structure, biology, evolution, and medical importance of sulfated fucans and galactans. . Glycobiology 18:, 1016–1027. [CrossRef] [PubMed]
    [Google Scholar]
  36. Rameshthangam P. , Ramasamy P. . ( 2007; ). Antiviral activity of bis(2-methylheptyl)phthalate isolated from Pongamia pinnata leaves against White Spot Syndrome Virus of Penaeus monodon Fabricius. . Virus Res 126:, 38–44. [CrossRef] [PubMed]
    [Google Scholar]
  37. Rocha J. L. , Guerrelhas A. C. , Teixeira A. K. , Farais F. A. , Teixeira A. P. , de Araujo J. N. . ( 2009; ). Ten years of shrimp genetic improvement in Brazil and recent introduction of specific pathogen free stocks. . In The Rising Tide, Proceedings of the Special Session on Sustainable Shrimp Farming, World Aquaculture 2009, pp 34–45. Edited by Browdy C. L. , Jory D. F. . . Baton Rouge, LA:: The World Aquaculture Society;.
    [Google Scholar]
  38. Sahul Hameed A. S. , Parameswaran V. , Syed Musthaq S. , Sudhakaran R. , Balasubramanian G. , Yoganandhan K. . ( 2005; ). A simple PCR procedure to detect white spot syndrome virus (WSSV) of shrimp, Penaeus monodon (Fabricious). . Aquacult Int 13:, 441–450. [CrossRef]
    [Google Scholar]
  39. Sarathi M. , Simon M. C. , Venkatesan C. , Hameed A. S. S. . ( 2008; ). Oral administration of bacterially expressed VP28dsRNA to protect Penaeus monodon from white spot syndrome virus. . Mar Biotechnol (NY) 10:, 242–249. [CrossRef] [PubMed]
    [Google Scholar]
  40. Sirirustananun N. , Chen J. C. , Lin Y. C. , Yeh S. T. , Liou C. H. , Chen L. L. , Sim S. S. , Chiew S. L. . ( 2011; ). Dietary administration of a Gracilaria tenuistipitata extract enhances the immune response and resistance against Vibrio alginolyticus and white spot syndrome virus in the white shrimp Litopenaeus vannamei . . Fish Shellfish Immunol 31:, 848–855. [CrossRef] [PubMed]
    [Google Scholar]
  41. Sritunyalucksana K. , Wannapapho W. , Lo C. F. , Flegel T. W. . ( 2006; ). PmRab7 is a VP28-binding protein involved in white spot syndrome virus infection in shrimp. . J Virol 80:, 10734–10742. [CrossRef] [PubMed]
    [Google Scholar]
  42. Sudhakaran R. , Mekata T. , Kono T. , Inada M. , Okugawa S. , Yoshimine M. , Yoshida T. , Sakai M. , Itami T. . ( 2011; ). Double-stranded RNA-mediated silencing of the white spot syndrome virus VP28 gene in kuruma shrimp, Marsupenaeus japonicas . . Aquacult Res 42:, 1153–1162. [CrossRef]
    [Google Scholar]
  43. Sudheer N. S. , Philip R. , Bright Singh I. S. . ( 2012; ). Anti-white spot syndrome virus activity of Ceriops tagal aqueous extract in giant tiger shrimp Penaeus monodon . . Arch Virol 157:, 1665–1675. [CrossRef] [PubMed]
    [Google Scholar]
  44. Syed Musthaq S. , Yoganandhan K. , Sudhakaran R. , Rajesh Kumar S. , Sahul Hameed A. S. . ( 2006; ). Neutralization of white spot syndrome virus of shrimp by antiserum raised against recombinant VP28. . Aquaculture 253:, 98–104. [CrossRef]
    [Google Scholar]
  45. Talarico L. B. , Zibetti R. G. M. , Faria P. C. S. , Scolaro L. A. , Duarte M. E. R. , Noseda M. D. , Pujol C. A. , Damonte E. B. . ( 2004; ). Anti-herpes simplex virus activity of sulfated galactans from the red seaweeds Gymnogongrus griffithsiae and Cryptonemia crenulata . . Int J Biol Macromol 34:, 63–71. [CrossRef] [PubMed]
    [Google Scholar]
  46. Tsai J. M. , Wang H. C. , Leu J. H. , Wang A. H. J. , Zhuang Y. , Walker P. J. , Kou G. H. , Lo C. F. . ( 2006; ). Identification of the nucleocapsid, tegument, and envelope proteins of the shrimp white spot syndrome virus virion. . J Virol 80:, 3021–3029. [CrossRef] [PubMed]
    [Google Scholar]
  47. Wang C. H. , Lo C. F. , Leu J. H. , Chou C. M. , Yeh P. Y. , Chou H. Y. , Tung M. C. , Chang C. F. , Su M. S. , Kou G. H. . ( 1995; ). Purification and genomic analysis of baculovirus associated with white spot syndrome (WSBV) of Penaeus monodon . . Dis Aquat Organ 23:, 239–242. [CrossRef]
    [Google Scholar]
  48. Witvrouw M. , De Clercq E. . ( 1997; ). Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. . Gen Pharmacol 29:, 497–511. [CrossRef] [PubMed]
    [Google Scholar]
  49. Witvrouw M. , Este J. A. , Mateu M. Q. , Reymen D. , Andrei G. , Snoeck R. , Ikeda S. , Pauwels R. , Bianchini N. V. . & 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]
  50. Wongprasert K. , Rudtanatip T. , Praiboon J. . ( 2014; ). Immunostimulatory activity of sulfated galactans isolated from the red seaweed Gracilaria fisheri and development of resistance against white spot syndrome virus (WSSV) in shrimp. . Fish Shellfish Immunol 36:, 52–60. [CrossRef] [PubMed]
    [Google Scholar]
  51. Xie X. , Yang F. . ( 2005; ). Interaction of white spot syndrome virus VP26 protein with actin. . Virology 336:, 93–99. [CrossRef] [PubMed]
    [Google Scholar]
  52. Yi G. , Wang Z. , Qi Y. , Yao L. , Qian J. , Hu L. . ( 2004; ). Vp28 of shrimp white spot syndrome virus is involved in the attachment and penetration into shrimp cells. . J Biochem Mol Biol 37:, 726–734. [CrossRef] [PubMed]
    [Google Scholar]
  53. Zhou Q. , Xu L. , Li H. , Qi Y. P. , Yang F. . ( 2009; ). Four major envelope proteins of white spot syndrome virus bind to form a complex. . J Virol 83:, 4709–4712. [CrossRef] [PubMed]
    [Google Scholar]
  54. Zhu F. , Zhang X. . ( 2011; ). The antiviral vp28-siRNA expressed in bacteria protects shrimp against white spot syndrome virus (WSSV). . Aquaculture 319:, 311–314. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.062919-0
Loading
/content/journal/jgv/10.1099/vir.0.062919-0
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