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Identification of (-)-epigallocatechin-3-gallate as a potential agent for blocking infection by grass carp reovirus

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Abstract

Grass carp reovirus (GCRV), the representative strain of the species Aquareovirus C, serves as a model for studying the pathogenesis of aquareoviruses. Previously, epigallocatechin gallate (EGCG) was shown to inhibit orthoreovirus infection. The aim of this study was to test its potential in blocking infection by GCRV. We show that adhesion to the CIK (Ctenopharyngodon idellus kidney) cell surface by GCRV particles is inhibited in a dose-dependent manner by EGCG, as well as by a crude extract of green tea. We also evaluated the safety of EGCG and green tea extract using CIK cells, and the results suggest that EGCG is a promising compound that may be developed as a plant-derived small molecular therapeutic agent against grass carp hemorrhagic disease caused by GCRV infection. As the ligand for the 37/67-kDa laminin receptor (LamR), EGCG’s blocking effect on GCRV attachment was associated with the binding potential of GCRV particles to LamR, which was inferred from a VOPBA assay.

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References

  1. Ahne W (1994) Evidence for the early appearance of interleukins and tumor necrosis factor in the phylogenesis of vertebrates. Immunol Today 15:137

    Article  CAS  PubMed  Google Scholar 

  2. Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA (2006) The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 80:9831–9836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bonoli M, Pelillo M, Toschi TG, Lercker G (2003) Analysis of green tea catechins: comparative study between HPLC and HPCE. Food Chem 81:631–638

    Article  CAS  Google Scholar 

  4. Busayarat N, Senapin S, Tonganunt M, Phiwsaiya K, Meemetta W, Unajak S, Jitrapakdee S, Lo C-F, Phongdara A (2011) Shrimp laminin receptor binds with capsid proteins of two additional shrimp RNA viruses YHV and IMNV. Fish Shellfish Immunol 31:66–72

    Article  CAS  PubMed  Google Scholar 

  5. Colpitts CC, Schang LM (2014) A small molecule inhibits virion attachment to heparan sulfate-or sialic acid-containing glycans. J Virol 88:7806–7817

    Article  PubMed  PubMed Central  Google Scholar 

  6. Demeule M, Brossard M, Pagé M, Gingras D, Béliveau R (2000) Matrix metalloproteinase inhibition by green tea catechins. Biochim Biophys Acta 1478:51–60

    Article  CAS  PubMed  Google Scholar 

  7. Fan C, Shao L, Fang Q (2010) Characterization of the nonstructural protein NS80 of grass carp reovirus. Arch Virol 155:1755–1763

    Article  CAS  PubMed  Google Scholar 

  8. Fassina G, Buffa A, Benelli R, Varnier OE, Noonan DM, Albini A (2002) Polyphenolic antioxidant (-)-epigallocatechin-3-gallate from green tea as a candidate anti-HIV agent. Aids 16:939–941

    Article  CAS  PubMed  Google Scholar 

  9. Fauquet CM, Mayo M, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. Academic Press, London

    Google Scholar 

  10. Fujimura Y, Umeda D, Yano S, Maeda-Yamamoto M, Yamada K, Tachibana H (2007) The 67 kDa laminin receptor as a primary determinant of anti-allergic effects of O-methylated EGCG. Biochem Biophys Res Commun 364:79–85

    Article  CAS  PubMed  Google Scholar 

  11. Garbisa S, Biggin S, Cavallarin N, Sartor L, Benelli R, Albini A (1999) Tumor invasion: molecular shears blunted by green tea. Nat Med 5:1216

    Article  CAS  PubMed  Google Scholar 

  12. Garbisa S, Sartor L, Biggin S, Salvato B, Benelli R (2001) Tumor gelatinases and invasion inhibited by the green tea flavanol epigallocatechin-3-gallate. Cancer 91:822–832

    Article  CAS  PubMed  Google Scholar 

  13. Garcia D, Escalante M, Delgado R, Ubeira F, Leiro J (2003) Anthelminthic and antiallergic activities of Mangifera indica L. stem bark components Vimang and mangiferin. Phytother Res 17:1203–1208

    Article  CAS  PubMed  Google Scholar 

  14. Gauczynski S, Peyrin JM, Haïk S, Leucht C, Hundt C, Rieger R, Krasemann S, Deslys JP, Dormont D, Lasmézas CI (2001) The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J 20:5863–5875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. He Y, Xu H, Yang Q, Xu D, Lu L (2011) The use of an in vitro microneutralization assay to evaluate the potential of recombinant VP5 protein as an antigen for vaccinating against Grass carp reovirus. Virol J 8:132–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jiang Y (2009) Hemorrhagic disease of grass carp: status of outbreaks, diagnosis, surveillance, and research. Israeli J Aquac Bamidgeh 61:188–197

    Google Scholar 

  17. Kim M, Kim SY, Lee HW, Shin JS, Kim P, Jung YS, Jeong HS, Hyun JK, Lee CK (2013) Inhibition of influenza virus internalization by (-)-epigallocatechin-3-gallate. Antiviral Res 100:460–472

    Article  CAS  PubMed  Google Scholar 

  18. Leiro J, Arranz J, Parama A, Alvarez M, Sanmartin M (2004) In vitro effects of the polyphenols resveratrol, mangiferin and (–)-epigallocatechin-3-gallate on the scuticociliate fish pathogen Philasterides dicentrarchi. Dis Aquat Organ 59:171–174

    Article  CAS  PubMed  Google Scholar 

  19. Lotito SB, Fraga CG (1998) (+)-Catechin prevents human plasma oxidation. Free Radic Biol Med 24:435–441

    Article  CAS  PubMed  Google Scholar 

  20. Lu L, Xu H, He Y, Li J (2011) Protection of grass carp, Ctenopharyngon idellus (Valenciennes), through oral administration of a subunit vaccine against reovirus. J Fish Dis 34:939–942

    Article  CAS  PubMed  Google Scholar 

  21. Ludwig GV, Kondig JP, Smith JF (1996) A putative receptor for Venezuelan equine encephalitis virus from mosquito cells. J Virol 70:5592–5599

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Lupiani B, Subramanian K, Samal SK (1995) Aquareoviruses. Annual Review of Fish Diseases 5:175–208

    Article  Google Scholar 

  23. Menard S, Castronovo V, Tagliabue E, Sobel ME (1997) New insights into the metastasis-associated 67 kD laminin receptor. J Cell Biochem 67:155–165

    Article  CAS  PubMed  Google Scholar 

  24. Mereles D, Hunstein W (2011) Epigallocatechin-3-gallate (EGCG) for clinical trials: more pitfalls than promises? Int J Mol Sci 12:5592–5603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pei C, Ke F, Chen Z-Y, Zhang Q-Y (2014) Complete genome sequence and comparative analysis of grass carp reovirus strain 109 (GCReV-109) with other grass carp reovirus strains reveals no significant correlation with regional distribution. Arch Virol 159:2435–2440

    Article  CAS  PubMed  Google Scholar 

  26. Rao Y, Su J (2015) Insights into the antiviral immunity against grass carp (Ctenopharyngodon idella) reovirus (GCRV) in grass carp. J Immunol Res 2015:670437

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sheikhzadeh N, Nofouzi K, Delazar A, Oushani AK (2011) Immunomodulatory effects of decaffeinated green tea (Camellia sinensis) on the immune system of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 31:1268–1269

    Article  CAS  PubMed  Google Scholar 

  28. Song J-M, Lee K-H, Seong B-L (2005) Antiviral effect of catechins in green tea on influenza virus. Antiviral Res 68:66–74

    Article  CAS  PubMed  Google Scholar 

  29. Tachibana H, Koga K, Fujimura Y, Yamada K (2004) A receptor for green tea polyphenol EGCG. Nat Struct Mol Biol 11:380–381

    Article  CAS  PubMed  Google Scholar 

  30. Thawonsuwan J, Kiron V, Satoh S, Panigrahi A, Verlhac V (2010) Epigallocatechin-3-gallate (EGCG) affects the antioxidant and immune defense of the rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 36:687–697

    Article  CAS  PubMed  Google Scholar 

  31. Thepparit C, Smith DR (2004) Serotype-specific entry of dengue virus into liver cells: identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 78:12647–12656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tian Y, Ye X, Zhang L, Deng G, Bai Y (2013) Development of a novel candidate subunit vaccine against Grass carp reovirus Guangdong strain (GCRV-GD108). Fish Shellfish Immunol 35:351–356

    Article  CAS  PubMed  Google Scholar 

  33. Umeda D, Yano S, Yamada K, Tachibana H (2008) Green tea polyphenol epigallocatechin-3-gallate signaling pathway through 67-kDa laminin receptor. J Biol Chem 283:3050–3058

    Article  CAS  PubMed  Google Scholar 

  34. Valacchi G, Sticozzi C, Belmonte G, Cervellati F, Demaude J, Chen N, Krol Y, Oresajo C (2015) Vitamin C compound mixtures prevent ozone-induced oxidative damage in human keratinocytes as initial assessment of pollution protection. PLoS One 10:e0131097

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wang H, Shen X, Xu D, Lu L (2013) Lipopolysaccharide-induced TNF-α factor in grass carp (Ctenopharyngodon idella): evidence for its involvement in antiviral innate immunity. Fish Shellfish Immunol 34:538–545

    Article  CAS  PubMed  Google Scholar 

  36. Wang K-S, Kuhn R, Strauss E, Ou S, Strauss J (1992) High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 66:4992–5001

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Wang T, Li J, Lu L (2013) Quantitative in vivo and in vitro characterization of co-infection by two genetically distant grass carp reoviruses. J Gen Virol 94:1301–1309

    Article  CAS  PubMed  Google Scholar 

  38. Xu J, Wang J, Deng F, Hu Z, Wang H (2008) Green tea extract and its major component epigallocatechin gallate inhibits hepatitis B virus in vitro. Antiviral Res 78:242–249

    Article  CAS  PubMed  Google Scholar 

  39. Yang CS, Wang X (2010) Green tea and cancer prevention. Nutr Cancer 62:931–937

    Article  CAS  PubMed  Google Scholar 

  40. Yao K, Yin Y-L, Chu W, Liu Z, Deng D, Li T, Huang R, Zhang J, Tan B, Wang W (2008) Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138:867–872

    CAS  PubMed  Google Scholar 

  41. Zhang L, Luo Q, Fang Q, Wang Y (2010) An improved RT-PCR assay for rapid and sensitive detection of grass carp reovirus. J Virol Methods 169:28–33

    Article  CAS  PubMed  Google Scholar 

  42. Zuo W, Qian H, Xu Y, Du S, Yang X (1986) A cell line derived from the kidney of grass carp. J Fish China 10:11–17

    Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (No. 31372561), the Earmarked Fund for China Agriculture Research System (No. CARS-46-12), and the Program of First-Class Disciplines Project of Shanghai Ocean University.

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Authors and Affiliations

  1. National Pathogen Collection Center for Aquatic Animals, Key Laboratory of Freshwater Fishery Germplasm Resources, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, People’s Republic of China

    Hao Wang, Weisha Liu, Fei Yu & Liqun Lu

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  1. Hao Wang
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  2. Weisha Liu
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  3. Fei Yu
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Correspondence to Liqun Lu.

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Author Hao Wang declares that he has no conflict of interest. Author Weisha Liu declares that she has no conflict of interest. Author Fei Yu declares that he has no conflict of interest. Author Liqun Lu declares that he has no conflict of interest.

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Wang, H., Liu, W., Yu, F. et al. Identification of (-)-epigallocatechin-3-gallate as a potential agent for blocking infection by grass carp reovirus. Arch Virol 161, 1053–1059 (2016). https://doi.org/10.1007/s00705-016-2751-9

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  • DOI: https://doi.org/10.1007/s00705-016-2751-9

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