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Journal of Immunology Research
Volume 2015, Article ID 670437, 18 pages
http://dx.doi.org/10.1155/2015/670437
Review Article

Insights into the Antiviral Immunity against Grass Carp (Ctenopharyngodon idella) Reovirus (GCRV) in Grass Carp

1College of Animal Science and Technology, Northwest A&F University, Yangling 712100, China
2College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China
3Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, China

Received 12 September 2014; Accepted 12 December 2014

Academic Editor: J. Zou

Copyright © 2015 Youliang Rao and Jianguo Su. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Gui and Z. Zhu, “Molecular basis and genetic improvement of economically important traits in aquaculture animals,” Chinese Science Bulletin, vol. 57, no. 15, pp. 1751–1760, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Aoki, J. I. Hikima, S. D. Hwang, and T. S. Jung, “Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts,” Fish & Shellfish Immunology, vol. 35, no. 6, pp. 1689–1702, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. O. Takeuchi and S. Akira, “Pattern recognition receptors and inflammation,” Cell, vol. 140, no. 6, pp. 805–820, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Zou, S. Bird, and C. Secombes, “Antiviral sensing in teleost fish,” Current Pharmaceutical Design, vol. 16, no. 38, pp. 4185–4193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Goubau, S. Deddouche, and C. Reis e Sousa, “Cytosolic Sensing of Viruses,” Immunity, vol. 38, no. 5, pp. 855–869, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Palti, “Toll-like receptors in bony fish: from genomics to function,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1263–1272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. E. R. Verrier, C. Langevin, A. Benmansour, and P. Boudinot, “Early antiviral response and virus-induced genes in fish,” Developmental & Comparative Immunology, vol. 35, no. 12, pp. 1204–1214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. Q. Wang, W. Zeng, C. Liu et al., “Complete genome sequence of a reovirus isolated from grass carp, indicating different genotypes of GCRV in China,” Journal of Virology, vol. 86, no. 22, p. 12466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Fan, L. Shao, and Q. Fang, “Characterization of the nonstructural protein NS80 of grass carp reovirus,” Archives of Virology, vol. 155, no. 11, pp. 1755–1763, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Cheng, Q. Fang, S. Shah, I. C. Atanasov, and Z. Zhou, “Subnanometer-resolution structures of the grass carp reovirus core and virion,” Journal of Molecular Biology, vol. 382, no. 1, pp. 213–222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. F. M. Jaafar, A. E. Goodwin, M. Belhouchet et al., “Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses,” Virology, vol. 373, no. 2, pp. 310–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Ye, Y. Tian, G. Deng, Y. Chi, and X. Jiang, “Complete genomic sequence of a reovirus isolated from grass carp in China,” Virus Research, vol. 163, no. 1, pp. 275–283, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Fan, S. Rao, L. Zeng et al., “Identification and genomic characterization of a novel fish reovirus, Hubei grass carp disease reovirus, isolated in 2009 in China,” Journal of General Virology, vol. 94, no. 10, pp. 2266–2277, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Pei, F. Ke, Z. Chen, and Q. Zhang, “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,” Archives of Virology, vol. 159, no. 9, pp. 2435–2440, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. X. Yan, Y. Wang, L. Xiong, J. Jian, and Z. Wu, “Phylogenetic analysis of newly isolated grass carp reovirus,” SpringerPlus, vol. 3, article 190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. Q. Wan, J. Su, X. Chen, and C. Yang, “Gene-based polymorphisms, genomic organization of interferon-β promoter stimulator 1 (IPS-1) gene and association study with the natural resistance to grass carp reovirus in grass carp Ctenopharyngodon idella,” Developmental and Comparative Immunology, vol. 41, no. 4, pp. 756–765, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Heng, J. Su, T. Huang, J. Dong, and L. Chen, “The polymorphism and haplotype of TLR3 gene in grass carp (Ctenopharyngodon idella) and their associations with susceptibility/resistance to grass carp reovirus,” Fish & Shellfish Immunology, vol. 30, no. 1, pp. 45–50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Chen, J. Su, C. Yang, L. Peng, Q. Wan, and L. Wang, “Functional characterizations of RIG-I to GCRV and viral/bacterial PAMPs in grass carp Ctenopharyngodon idella,” PLoS ONE, vol. 7, no. 7, Article ID e42182, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Rao, J. Su, C. Yang, L. Peng, X. Feng, and Q. Li, “Characterizations of two grass carp Ctenopharyngodon idella HMGB2 genes and potential roles in innate immunity,” Developmental and Comparative Immunology, vol. 41, no. 2, pp. 164–177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Jia, L. Cao, J. Du et al., “Grass carp reovirus induces apoptosis and oxidative stress in grass carp (Ctenopharyngodon idellus) kidney cell line,” Virus Research, vol. 185, pp. 77–81, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Ke, Q. Fang, and Y. Cai, “Characteristics of a novel isolate of grass carp hemorrhagic virus,” Acta Hydrobiologica Sinica, vol. 14, pp. 153–159, 1999 (Chinese). View at Google Scholar
  22. Q. Fang, T. Xiao, Q. Ding, L. Li, H. Zhang, and Z. Zhu, “Virological properties of GCRV991 strain,” Virologica Sinica, vol. 17, no. 2, pp. 178–181, 2002 (Chinese). View at Google Scholar
  23. J. Li, T. Wang, L. Zhou, and H. Xu, “Comparative studies on two isolates of hemorrhagic virus from grass carp,” Journal of Fishery Sciences of China, vol. 5, no. 3, pp. 115–118, 1998 (Chinese). View at Google Scholar
  24. Y. Li, W. Zeng, Q. Wang et al., “Advance in molecular biology of grass carp reovirus,” Progress in Veterinary Medicine, vol. 34, no. 4, pp. 97–103, 2013 (Chinese). View at Google Scholar
  25. C. Zhang, Q. Wang, C. Shi, W. Zeng, Y. Liu, and S. Wu, “Molecular analysis of grass carp reovirus HZ08 genome segments 1–3 and 5–6,” Virus Genes, vol. 41, no. 1, pp. 102–104, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Wang, J. Li, and L. Lu, “Quantitative in vivo and in vitro characterization of co-infection by two genetically distant grass carp reoviruses,” Journal of General Virology, vol. 94, no. 6, pp. 1301–1309, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Jian, Y. Wang, X. Yan, Y. Ding, Z. Wu, and Y. Lu, “Molecular cloning and prokaryotic expression of vp5 gene of grass carp reovirus strain GCRV096,” Virus Genes, vol. 47, no. 3, pp. 483–489, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Yanai, T. Ban, Z. Wang et al., “HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses,” Nature, vol. 462, no. 7269, pp. 99–103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Yanai, T. Ban, and T. Taniguchi, “High-mobility group box family of proteins: ligand and sensor for innate immunity,” Trends in Immunology, vol. 33, no. 12, pp. 633–640, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Rao, J. Su, C. Yang, N. Yan, X. Chen, and X. Feng, “Dynamic localization and the associated translocation mechanism of HMGBs in response to GCRV challenge in CIK cells,” Cellular & Molecular Immunology, 2014. View at Publisher · View at Google Scholar
  31. C. Yang, L. Chen, J. Su, X. Feng, and Y. Rao, “Two novel homologs of high mobility group box 3 gene in grass carp (Ctenopharyngodon idella): potential roles in innate immune responses,” Fish & Shellfish Immunology, vol. 35, no. 5, pp. 1501–1510, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Yang, L. Peng, and J. Su, “Two HMGB1 genes from grass carp Ctenopharyngodon idella mediate immune responses to viral/bacterial PAMPs and GCRV challenge,” Developmental and Comparative Immunology, vol. 39, no. 3, pp. 133–146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Sessa and M. E. Bianchi, “The evolution of high mobility group box (HMGB) chromatin proteins in multicellular animals,” Gene, vol. 387, no. 1-2, pp. 133–140, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Moleri, G. Cappellano, G. Gaudenzi et al., “The HMGB protein gene family in zebrafish: evolution and embryonic expression patterns,” Gene Expression Patterns, vol. 11, no. 1-2, pp. 3–11, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Li, Y. Zhang, Z. Xiang, S. Xiao, F. Yu, and Z. Yu, “High mobility group box 1 can enhance NF-κB activation and act as a pro-inflammatory molecule in the Pacific oyster, Crassostrea gigas,” Fish & Shellfish Immunology, vol. 35, no. 1, pp. 63–70, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Xie, J. W. Hodgkinson, C. Li, N. Kovacevic, and M. Belosevic, “Identification and functional characterization of the goldfish (Carassius auratus L.) high mobility group box 1 (HMGB1) chromatin-binding protein,” Developmental and Comparative Immunology, vol. 44, no. 1, pp. 245–253, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Wang, L. Wang, Y. Guo et al., “A high mobility group box 1 (HMGB1) gene from Chlamys farreri and the DNA-binding ability and pro-inflammatory activity of its recombinant protein,” Fish & Shellfish Immunology, vol. 36, no. 2, pp. 393–400, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Štros, “HMGB proteins: interactions with DNA and chromatin,” Biochimica et Biophysica Acta, vol. 1799, no. 1-2, pp. 101–113, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Chen, X. Jia, X. Huang et al., “Two Litopenaeus vannamei HMGB proteins interact with transcription factors LvSTAT and LvDorsal to activate the promoter of white spot syndrome virus immediate-early gene ie1,” Molecular Immunology, vol. 48, no. 5, pp. 793–799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Yanai, S. Chiba, T. Ban et al., “Suppression of immune responses by nonimmunogenic oligodeoxynucleotides with high affinity for high-mobility group box proteins HMGBs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 28, pp. 11542–11547, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Kumar, T. Kawai, and S. Akira, “Toll-like receptors and innate immunity,” Biochemical and Biophysical Research Communications, vol. 388, no. 4, pp. 621–625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. A. L. Blasius and B. Beutler, “Intracellular toll-like receptors,” Immunity, vol. 32, no. 3, pp. 305–315, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Bonaldi, F. Talamo, P. Scaffidi et al., “Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion,” The EMBO Journal, vol. 22, no. 20, pp. 5551–5560, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Pusterla, F. de Marchis, R. Palumbo, and M. E. Bianchi, “High mobility group B2 is secreted by myeloid cells and has mitogenic and chemoattractant activities similar to high mobility group B1,” Autoimmunity, vol. 42, no. 4, pp. 308–310, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Müller, L. Ronfani, and M. E. Bianchi, “Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function,” Journal of Internal Medicine, vol. 255, no. 3, pp. 332–343, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Zhao, Y. Hu, J. Sun, and L. Sun, “The high mobility group box 1 protein of Sciaenops ocellatus is a secreted cytokine that stimulates macrophage activation,” Developmental & Comparative Immunology, vol. 35, no. 10, pp. 1052–1058, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. D. S. Pedersen, T. Merkle, B. Marktl et al., “Nucleocytoplasmic distribution of the Arabidopsis chromatin-associated HMGB2/3 and HMGB4 proteins,” Plant Physiology, vol. 154, no. 4, pp. 1831–1841, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Kosugi, M. Hasebe, N. Matsumura et al., “Six classes of nuclear localization signals specific to different binding grooves of importinα,” The Journal of Biological Chemistry, vol. 284, no. 1, pp. 478–485, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Zhang, S. Liu, K. V. Rajendran et al., “Pathogen recognition receptors in channel catfish: III phylogeny and expression analysis of toll-like receptors,” Developmental & Comparative Immunology, vol. 40, no. 2, pp. 185–194, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. P. T. Lee, J. Zou, J. W. Holland et al., “Identification and characterisation of TLR18-21 genes in Atlantic salmon (Salmo salar),” Fish & Shellfish Immunology, vol. 41, no. 2, pp. 549–559, 2014. View at Publisher · View at Google Scholar
  51. Y. Zhang and J. Gui, “Molecular regulation of interferon antiviral response in fish,” Developmental and Comparative Immunology, vol. 38, no. 2, pp. 193–202, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Kawai and S. Akira, “The roles of TLRs, RLRs and NLRs in pathogen recognition,” International Immunology, vol. 21, no. 4, pp. 317–337, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Kawai and S. Akira, “Toll-like receptors and their crosstalk with other innate receptors in infection and immunity,” Immunity, vol. 34, no. 5, pp. 637–650, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. K. J. Szretter, M. A. Samuel, S. Gilfillan, A. Fuchs, M. Colonna, and M. S. Diamond, “The immune adaptor molecule SARM modulates tumor necrosis factor alpha production and microglia activation in the brainstem and restricts West Nile virus pathogenesis,” Journal of Virology, vol. 83, no. 18, pp. 9329–9338, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Matsuo, H. Oshiumi, T. Tsujita et al., “Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from Birnaviruses,” The Journal of Immunology, vol. 181, no. 5, pp. 3474–3485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. S. D. Hwang, M. Ohtani, J.-I. Hikima et al., “Molecular cloning and characterization of Toll-like receptor 3 in Japanese flounder, Paralichthys olivaceus,” Developmental & Comparative Immunology, vol. 37, no. 1, pp. 87–96, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Seya, M. Matsumoto, T. Ebihara, and H. Oshiumi, “Functional evolution of the TICAM-1 pathway for extrinsic RNA sensing,” Immunological Reviews, vol. 227, no. 1, pp. 44–53, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Su, J. Heng, T. Huang, L. Peng, C. Yang, and Q. Li, “Identification, mRNA expression and genomic structure of TLR22 and its association with GCRV susceptibility/resistance in grass carp (Ctenopharyngodon idella),” Developmental & Comparative Immunology, vol. 36, no. 2, pp. 450–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Su, S. Jang, C. Yang, Y. Wang, and Z. Zhu, “Genomic organization and expression analysis of Toll-like receptor 3 in grass carp (Ctenopharyngodon idella),” Fish & Shellfish Immunology, vol. 27, no. 3, pp. 433–439, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Su, Z. Zhu, Y. Wang, J. Zou, and W. Hu, “Toll-like receptor 3 regulates Mx expression in rare minnow Gobiocypris rarus after viral infection,” Immunogenetics, vol. 60, no. 3-4, pp. 195–205, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. P. E. Phelan, M. T. Mellon, and C. H. Kim, “Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio),” Molecular Immunology, vol. 42, no. 9, pp. 1057–1071, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Fan, S. Chen, Y. Liu et al., “Zebrafish TRIF, a Golgi-localized protein, participates in IFN induction and NF-κB activation,” The Journal of Immunology, vol. 180, no. 8, pp. 5373–5383, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Sullivan, J. H. Postlethwait, C. R. Lage, P. J. Millard, and C. H. Kim, “Evidence for evolving Toll-IL-1 receptor-containing adaptor molecule function in vertebrates,” The Journal of Immunology, vol. 178, no. 7, pp. 4517–4527, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Sun, Y. Zhang, T. Liu, J. Shi, B. Wang, and J. Gui, “Fish MITA serves as a mediator for distinct fish IFN gene activation dependent on IRF3 or IRF7,” The Journal of Immunology, vol. 187, no. 5, pp. 2531–2539, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Yang, Q. Li, J. Su, X. Chen, Y. Wang, and L. Peng, “Identification and functional characterizations of a novel TRIF gene from grass carp (Ctenopharyngodon idella),” Developmental and Comparative Immunology, vol. 41, no. 2, pp. 222–229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Wang, Y. Mu, T. Qian, J. Ao, and X. Chen, “Molecular characterization and expression analysis of Toll-like receptor 1 from large yellow croaker (Pseudosciaena crocea),” Fish & Shellfish Immunology, vol. 35, no. 6, pp. 2046–2050, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. A. H. Meijer, S. F. Gabby Krens, I. A. Medina Rodriguez et al., “Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish,” Molecular Immunology, vol. 40, no. 11, pp. 773–783, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Wei, T. Pan, M. Chang et al., “Cloning and expression of Toll-like receptors 1 and 2 from a teleost fish, the orange-spotted grouper Epinephelus coioides,” Veterinary Immunology and Immunopathology, vol. 141, no. 3-4, pp. 173–182, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Pietretti and G. F. Wiegertjes, “Ligand specificities of Toll-like receptors in fish: indications from infection studies,” Developmental and Comparative Immunology, vol. 43, no. 2, pp. 205–222, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Avunje, M. Oh, and S. Jung, “Impaired TLR2 and TLR7 response in olive flounder infected with viral haemorrhagic septicaemia virus at host susceptible 15°C but high at non-susceptible 20°C,” Fish & Shellfish Immunology, vol. 34, no. 5, pp. 1236–1243, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. M. P. Sepulcre, F. Alcaraz-Pérez, A. López-Muñoz et al., “Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-κB activation,” The Journal of Immunology, vol. 182, no. 4, pp. 1836–1845, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Tsujita, A. Ishii, H. Tsukada, M. Matsumoto, F.-S. Che, and T. Seya, “Fish soluble Toll-like receptor (TLR)5 amplifies human TLR5 response via physical binding to flagellin,” Vaccine, vol. 24, no. 12, pp. 2193–2199, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Tsujita, H. Tsukada, M. Nakao, H. Oshiumi, M. Matsumoto, and T. Seya, “Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Onchorhynchus mikiss),” Journal of Biological Chemistry, vol. 279, no. 47, pp. 48588–48597, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Y. Moon, B. H. Nam, H. J. Kong et al., “Maximal transcriptional activation of piscine soluble Toll-like receptor 5 by the NF-κB subunit p65 and flagellin,” Fish & Shellfish Immunology, vol. 31, no. 6, pp. 881–886, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Chen, T. Wang, T. Tzeng, C. Wang, and D. Wang, “Evidence for positive selection in the TLR9 gene of teleosts,” Fish and Shellfish Immunology, vol. 24, no. 2, pp. 234–242, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. D. B. Iliev, I. Skjæveland, and J. B. Jørgensen, “CpG oligonucleotides bind TLR9 and RRM-containing proteins in Atlantic salmon (Salmo salar),” BMC Immunology, vol. 14, article 12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. D. W. Yeh, Y. Liu, Y. C. Lo et al., “Toll-like receptor 9 and 21 have different ligand recognition profiles and cooperatively mediate activity of CpG-oligodeoxynucleotides in zebrafish,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 51, pp. 20711–20716, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. C. Yang, J. Su, R. Zhang, L. Peng, and Q. Li, “Identification and expression profiles of grass carp Ctenopharyngodon idella tlr7 in responses to double-stranded RNA and virus infection,” Journal of Fish Biology, vol. 80, no. 7, pp. 2605–2622, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Chen, Q. Wang, C. Yang et al., “Identification, expression profiling of a grass carp TLR8 and its inhibition leading to the resistance to reovirus in CIK cells,” Developmental and Comparative Immunology, vol. 41, no. 1, pp. 82–93, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Kawai, S. Sato, K. J. Ishii et al., “Interferon-α induction through toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6,” Nature Immunology, vol. 5, no. 10, pp. 1061–1068, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Su, J. Dong, T. Huang, R. Zhang, C. Yang, and J. Heng, “Myeloid differentiation factor 88 gene is involved in antiviral immunity in grass carp Ctenopharyngodon idella,” Journal of Fish Biology, vol. 78, no. 3, pp. 973–979, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Liu, M. Li, S. Fan et al., “A unique feature of toll/IL-1 receptor domain-containing adaptor protein is partially responsible for lipopolysaccharide insensitivity in zebrafish with a highly conserved function of Myd88,” The Journal of Immunology, vol. 185, no. 6, pp. 3391–3400, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Rebl, H. Rebl, S. Liu, T. Goldammer, and H.-M. Seyfert, “Salmonid Tollip and MyD88 factors can functionally replace their mammalian orthologues in TLR-mediated trout SAA promoter activation,” Developmental & Comparative Immunology, vol. 35, no. 1, pp. 81–87, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. D. B. Iliev, M. Sobhkhez, K. Fremmerlid, and J. B. Jørgensen, “MyD88 interacts with interferon regulatory factor (IRF) 3 and IRF7 in Atlantic salmon (Salmo salar): Transgenic SsMyD88 modulates the IRF-induced type I interferon response and accumulates in aggresomes,” The Journal of Biological Chemistry, vol. 286, no. 49, pp. 42715–42724, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. N. Yan, J. Su, C. Yang et al., “Grass carp SARM1 and its two splice variants negatively regulate IFN-I response and promote cell death upon GCRV infection at different subcellular locations,” Developmental & Comparative Immunology, vol. 48, no. 1, pp. 102–115, 2015. View at Publisher · View at Google Scholar
  86. S. Reikine, J. B. Nguyen, and Y. Modis, “Pattern recognition and signaling mechanisms of RIG-I and MDA5,” Frontiers in Immunology, vol. 5, article 342, 2014. View at Publisher · View at Google Scholar
  87. J. D. Hansen, L. N. Vojtech, and K. J. Laing, “Sensing disease and danger: a survey of vertebrate PRRs and their origins,” Developmental and Comparative Immunology, vol. 35, no. 9, pp. 886–897, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. R. B. Seth, L. Sun, C.-K. Ea, and Z. J. Chen, “Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3,” Cell, vol. 122, no. 5, pp. 669–682, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Ohtani, H. Jun-Ichi, H. Kondo, I. Hirono, J. Tae-Sung, and T. Aoki, “Evolutional conservation of molecular structure and antiviral function of a viral RNA receptor, LGP2, in Japanese flounder, Paralichthys olivaceus,” Journal of Immunology, vol. 185, no. 12, pp. 7507–7517, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Komuro and C. M. Horvath, “RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2,” Journal of Virology, vol. 80, no. 24, pp. 12332–12342, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Runge, K. M. J. Sparrer, C. Lässig et al., “In vivo ligands of MDA5 and RIG-I in measles virus-infected cells,” PLoS Pathogens, vol. 10, no. 4, Article ID e1004081, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. E. Kowalinski, T. Lunardi, A. A. McCarthy et al., “Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA,” Cell, vol. 147, no. 2, pp. 423–435, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. D. W. Leung and G. K. Amarasinghe, “Structural insights into RNA recognition and activation of RIG-I-like receptors,” Current Opinion in Structural Biology, vol. 22, no. 3, pp. 297–303, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. I. C. Berke and Y. Modis, “MDA5 cooperatively forms dimers and ATP-sensitive filaments upon binding double-stranded RNA,” The EMBO Journal, vol. 31, no. 7, pp. 1714–1726, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. B. Wu, A. Peisley, C. Richards et al., “Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5,” Cell, vol. 152, no. 1-2, pp. 276–289, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. K. S. Childs, R. E. Randall, and S. Goodbourn, “LGP2 plays a critical role in sensitizing mda-5 to activation by double-stranded RNA,” PLoS ONE, vol. 8, no. 5, Article ID e64202, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. M. Yoneyama, M. Kikuchi, K. Matsumoto et al., “Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity,” The Journal of Immunology, vol. 175, no. 5, pp. 2851–2858, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Rothenfusser, N. Goutagny, G. DiPerna et al., “The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I,” The Journal of Immunology, vol. 175, no. 8, pp. 5260–5268, 2005. View at Publisher · View at Google Scholar · View at Scopus
  99. Z. Zhu, X. Zhang, G. Wang, and H. Zheng, “The laboratory of genetics and physiology 2: emerging insights into the controversial functions of this RIG-I-like receptor,” BioMed Research International, vol. 2014, Article ID 960190, 7 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. L. Wang, J. Su, C. Yang, Q. Wan, and L. Peng, “Genomic organization, promoter activity of grass carp MDA5 and the association of its polymorphisms with susceptibility/resistance to grass carp reovirus,” Molecular Immunology, vol. 50, no. 4, pp. 236–243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. Q. Wan, J. Su, X. Chen et al., “Genomic sequence comparison, promoter activity, SNP detection of RIG-I gene and association with resistance/susceptibility to grass carp reovirus in grass carp (Ctenopharyngodon idella),” Developmental and Comparative Immunology, vol. 39, no. 4, pp. 333–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. Q. Wan, L. Wang, J. Su, C. Yang, L. Peng, and L. Chen, “Genetic structure, polymorphism identification of LGP2 gene and their relationship with the resistance/susceptibility to GCRV in grass carp, Ctenopharyngodon idella,” Gene, vol. 521, no. 1, pp. 166–175, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Huang, J. Su, J. Heng, J. Dong, R. Zhang, and H. Zhu, “Identification and expression profiling analysis of grass carp Ctenopharyngodon idella LGP2 cDNA,” Fish and Shellfish Immunology, vol. 29, no. 2, pp. 349–355, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. C. Yang, J. Su, T. Huang, R. Zhang, and L. Peng, “Identification of a retinoic acid-inducible gene I from grass carp (Ctenopharyngodon idella) and expression analysis in vivo and in vitro,” Fish & Shellfish Immunology, vol. 30, no. 3, pp. 936–943, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Su, T. Huang, J. Dong, J. Heng, R. Zhang, and L. Peng, “Molecular cloning and immune responsive expression of MDA5 gene, a pivotal member of the RLR gene family from grass carp Ctenopharyngodon idella,” Fish & Shellfish Immunology, vol. 28, no. 4, pp. 712–718, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. K. V. Rajendran, J. Zhang, S. Liu et al., “Pathogen recognition receptors in channel catfish: II. Identification, phylogeny and expression of retinoic acid-inducible gene I (RIG-I)-like receptors (RLRs),” Developmental & Comparative Immunology, vol. 37, no. 3-4, pp. 381–389, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Ohtani, J. I. Hikima, H. Kondo, I. Hirono, T. S. Jung, and T. Aoki, “Characterization and antiviral function of a cytosolic sensor gene, MDA5, in Japanese flounder, Paralichthys olivaceus,” Developmental and Comparative Immunology, vol. 35, no. 5, pp. 554–562, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. R. M. C. Simora, M. Ohtani, J.-I. Hikima et al., “Molecular cloning and antiviral activity of IFN-β promoter stimulator-1 (IPS-1) gene in Japanese flounder, Paralichthys olivaceus,” Fish & Shellfish Immunology, vol. 29, no. 6, pp. 979–986, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Chang, B. Collet, P. Nie et al., “Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in rainbow trout (Oncorhynchus mykiss),” Journal of Virology, vol. 85, no. 16, pp. 8403–8412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. X. Chen, C. Yang, J. Su, Y. Rao, and T. Gu, “LGP2 plays extensive roles in modulating innate immune responses in Ctenopharyngodon idella kidney (CIK) cells,” Developmental & Comparative Immunology, vol. 49, no. 1, pp. 138–148, 2015. View at Publisher · View at Google Scholar
  111. X. Dong, W. Liu, M. Zhao et al., “Classical swine fever virus triggers RIG-I and MDA5-dependent signaling pathway to IRF-3 and NF-κB activation to promote secretion of interferon and inflammatory cytokines in porcine alveolar macrophages,” Virology Journal, vol. 10, article 286, 2013. View at Publisher · View at Google Scholar · View at Scopus
  112. P. Zou, M. Chang, N. Xue et al., “Melanoma differentiation-associated gene 5 in zebrafish provoking higher interferon-promoter activity through signalling enhancing of its shorter splicing variant,” Immunology, vol. 141, no. 2, pp. 192–202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. W. Chen, Y. Hu, P. Zou, S. Ren, P. Nie, and M. Chang, “MAVS splicing variants contribute to the induction of interferon and interferon-stimulated genes mediated by RIG-I-like receptors,” Developmental & Comparative Immunology, vol. 49, no. 1, pp. 19–30, 2014. View at Publisher · View at Google Scholar
  114. S. Lauksund, T. Svingerud, V. Bergan, and B. Robertsen, “Atlantic salmon IPS-1 mediates induction of IFNa1 and activation of NF-κB and localizes to mitochondria,” Developmental and Comparative Immunology, vol. 33, no. 11, pp. 1196–1204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. J. Su, T. Huang, C. Yang, and R. Zhang, “Molecular cloning, characterization and expression analysis of interferon-β promoter stimulator 1 (IPS-1) gene from grass carp Ctenopharyngodon idella,” Fish & Shellfish Immunology, vol. 30, no. 1, pp. 317–323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  116. F. Sun, Y. Zhang, T. Liu et al., “Characterization of fish IRF3 as an IFN-inducible protein reveals evolving regulation of IFN response in vertebrates,” The Journal of Immunology, vol. 185, no. 12, pp. 7573–7582, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. X. Feng, J. Su, C. Yang, N. Yan, Y. Rao, and X. Chen, “Molecular characterizations of grass carp (Ctenopharyngodon idella) TBK1 gene and its roles in regulating IFN-I pathway,” Developmental and Comparative Immunology, vol. 45, no. 2, pp. 278–290, 2014. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Biacchesi, E. Mérour, A. Lamoureux, J. Bernard, and M. Brémont, “Both STING and MAVS fish orthologs contribute to the induction of interferon mediated by RIG-I,” PLoS ONE, vol. 7, no. 10, Article ID e47737, 2012. View at Publisher · View at Google Scholar · View at Scopus
  119. B. Zhong, Y. Yang, S. Li et al., “The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation,” Immunity, vol. 29, no. 4, pp. 538–550, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Ishikawa and G. N. Barber, “STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling,” Nature, vol. 455, no. 7213, pp. 674–678, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. X. Feng, C. Yang, Y. Zhang et al., “Identification, characterization and immunological response analysis of stimulator of interferon gene (STING) from grass carp Ctenopharyngodon idella,” Developmental and Comparative Immunology, vol. 45, no. 1, pp. 163–176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Liu, Y. Meng, Q. Wang, and Z. Sha, “Class II, major histocompatibility complex, transactivator (CIITA) in channel catfish: identification and expression patterns responding to different pathogens,” Molecular Biology Reports, vol. 39, no. 12, pp. 11041–11050, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. J. P. Ting, R. C. Lovering, E. S. Alnemri et al., “The NLR gene family: a standard nomenclature,” Immunity, vol. 28, no. 3, pp. 285–287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. C. B. Moore, D. T. Bergstralh, J. A. Duncan et al., “NLRX1 is a regulator of mitochondrial antiviral immunity,” Nature, vol. 451, no. 7178, pp. 573–577, 2008. View at Publisher · View at Google Scholar · View at Scopus
  125. K. J. Laing, M. K. Purcell, J. R. Winton, and J. D. Hansen, “A genomic view of the NOD-like receptor family in teleost fish: identification of a novel NLR subfamily in zebrafish,” BMC Evolutionary Biology, vol. 8, no. 1, article 42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. W. Chen, Q. Xu, M. Chang, P. Nie, and K. Peng, “Molecular characterization and expression analysis of nuclear oligomerization domain proteins NOD1 and NOD2 in grass carp Ctenopharyngodon idella,” Fish & Shellfish Immunology, vol. 28, no. 1, pp. 18–29, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. L. Chen, Q. Li, J. Su, C. Yang, Y. Li, and Y. Rao, “Trunk kidney of grass carp (Ctenopharyngodon idella) mediates immune responses against GCRV and viral/bacterial PAMPs in vivo and in vitro,” Fish & Shellfish Immunology, vol. 34, no. 3, pp. 909–919, 2013. View at Publisher · View at Google Scholar · View at Scopus
  128. B. Huang, Z. T. Qi, Z. Xu, and P. Nie, “Global characterization of interferon regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution,” BMC Immunology, vol. 11, article 22, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. A. Takaoka, T. Tamura, and T. Taniguchi, “Interferon regulatory factor family of transcription factors and regulation of oncogenesis,” Cancer Science, vol. 99, no. 3, pp. 467–478, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. V. Bergan, Ø. Kileng, B. Sun, and B. Robertsen, “Regulation and function of interferon regulatory factors of Atlantic salmon,” Molecular Immunology, vol. 47, no. 11-12, pp. 2005–2014, 2010. View at Publisher · View at Google Scholar · View at Scopus
  131. C. Yao, X. Huang, Z. Fan, P. Kong, and Z. Wang, “Cloning and expression analysis of interferon regulatory factor (IRF) 3 and 7 in large yellow croaker, Larimichthys crocea,” Fish & Shellfish Immunology, vol. 32, no. 5, pp. 869–878, 2012. View at Publisher · View at Google Scholar · View at Scopus
  132. J. W. Holland, S. Bird, B. Williamson et al., “Molecular characterization of IRF3 and IRF7 in rainbow trout, Oncorhynchus mykiss: functional analysis and transcriptional modulation,” Molecular Immunology, vol. 46, no. 2, pp. 269–285, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. H. Feng, H. Liu, R. Kong et al., “Expression profiles of carp IRF-3/-7 correlate with the up-regulation of RIG-I/MAVS/TRAF3/TBK1, four pivotal molecules in RIG-I signaling pathway,” Fish & Shellfish Immunology, vol. 30, no. 4-5, pp. 1159–1169, 2011. View at Publisher · View at Google Scholar · View at Scopus
  134. Z. Xiang, C. Dong, L. Qi et al., “Characteristics of the interferon regulatory factor pairs zfIRF5/7 and their stimulation expression by ISKNV Infection in zebrafish (Danio rerio),” Developmental and Comparative Immunology, vol. 34, no. 12, pp. 1263–1273, 2010. View at Publisher · View at Google Scholar · View at Scopus
  135. Y. Suzuki, M. Yasuike, H. Kondo, T. Aoki, and I. Hirono, “Molecular cloning and expression analysis of interferon regulatory factor 10 (IRF10) in Japanese flounder, Paralichthys olivaceus,” Fish & Shellfish Immunology, vol. 30, no. 1, pp. 67–76, 2011. View at Publisher · View at Google Scholar · View at Scopus
  136. S. Li, L. Lu, H. Feng et al., “IFN regulatory factor 10 is a negative regulator of the IFN responses in fish,” The Journal of Immunology, vol. 193, no. 3, pp. 1100–1109, 2014. View at Publisher · View at Google Scholar
  137. Q. Xu, M. Chang, F. Xiao, B. Huang, and P. Nie, “The gene and virus-induced expression of IRF-5 in grass carp Ctenopharyngodon idella,” Veterinary Immunology and Immunopathology, vol. 134, no. 3-4, pp. 269–278, 2010. View at Publisher · View at Google Scholar · View at Scopus
  138. A. J. Sadler and B. R. G. Williams, “Interferon-inducible antiviral effectors,” Nature Reviews Immunology, vol. 8, no. 7, pp. 559–568, 2008. View at Publisher · View at Google Scholar · View at Scopus
  139. Z. Qi, P. Nie, C. J. Secombes, and J. Zou, “Intron-containing type I and type III IFN coexist in amphibians: refuting the concept that a retroposition event gave rise to type I IFNs,” The Journal of Immunology, vol. 184, no. 9, pp. 5038–5046, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. L. Peng, C. Yang, and J. Su, “Protective roles of grass carp Ctenopharyngodon idella Mx isoforms against grass carp reovirus,” PLoS ONE, vol. 7, no. 12, Article ID e52142, 2012. View at Publisher · View at Google Scholar · View at Scopus
  141. B. Wang, Y. Zhang, T. Liu, J. Shi, F. Sun, and J. Gui, “Fish viperin exerts a conserved antiviral function through RLR-triggered IFN signaling pathway,” Developmental & Comparative Immunology, vol. 47, no. 1, pp. 140–149, 2014. View at Publisher · View at Google Scholar
  142. C. Langevin, E. Aleksejeva, G. Passoni, N. Palha, J.-P. Levraud, and P. Boudinot, “The antiviral innate immune response in fish: evolution and conservation of the IFN system,” Journal of Molecular Biology, vol. 425, no. 24, pp. 4904–4920, 2013. View at Publisher · View at Google Scholar · View at Scopus
  143. O. Haller, P. Staeheli, and G. Kochs, “Interferon-induced Mx proteins in antiviral host defense,” Biochimie, vol. 89, no. 6-7, pp. 812–818, 2007. View at Publisher · View at Google Scholar · View at Scopus
  144. J. A. González-Mariscal, J. B. Gallardo-Gálvez, T. Méndez, M. C. Álvarez, and J. Béjar, “Cloning and characterization of the Mx1, Mx2 and Mx3 promoters from gilthead seabream (Sparus aurata),” Fish & Shellfish Immunology, vol. 38, no. 2, pp. 311–317, 2014. View at Publisher · View at Google Scholar · View at Scopus
  145. P. Staeheli, Y. Yu, R. Grob, and O. Haller, “A double-stranded RNA-inducible fish gene homologous to the murine influenza virus resistance gene Mx,” Molecular and Cellular Biology, vol. 9, no. 7, pp. 3117–3121, 1989. View at Google Scholar · View at Scopus
  146. V. Jensen and B. Robertsen, “Cloning of an Mx cDNA from atlantic halibut (Hippoglossus hippoglossus) and characterization of Mx mRNA expression in response to double-stranded RNA or infectious pancreatic necrosis virus,” Journal of Interferon and Cytokine Research, vol. 20, no. 8, pp. 701–710, 2000. View at Publisher · View at Google Scholar · View at Scopus
  147. G. D. Trobridge, P. P. Chiou, and J.-A. C. Leong, “Cloning of the rainbow trout (Oncorhynchus mykiss) Mx2 and Mx3 cDNAs and characterization of trout Mx protein expression in salmon cells,” Journal of Virology, vol. 71, no. 7, pp. 5304–5311, 1997. View at Google Scholar · View at Scopus
  148. Ø. Kileng, M. I. Brundtland, and B. Robertsen, “Infectious salmon anemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon,” Fish & Shellfish Immunology, vol. 23, no. 2, pp. 378–389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  149. T. P. Røkenes, R. Larsen, and B. Robertsen, “Atlantic salmon ISG15: expression and conjugation to cellular proteins in response to interferon, double-stranded RNA and virus infections,” Molecular Immunology, vol. 44, no. 5, pp. 950–959, 2007. View at Publisher · View at Google Scholar · View at Scopus
  150. C. Furnes, O. Kileng, C. H. Rinaldo, M. Seppola, I. Jensen, and B. Robertsen, “Atlantic cod (Gadus morhua L.) possesses three homologues of ISG15 with different expression kinetics and conjugation properties,” Developmental and Comparative Immunology, vol. 33, no. 12, pp. 1239–1246, 2009. View at Publisher · View at Google Scholar · View at Scopus
  151. B. K. Das, B. Collet, M. Snow, and A. E. Ellis, “Expression kinetics of ISG15 and viral major capsid protein (VP2) in Atlantic cod (Gadus morhua L.) fry following infection with infectious pancreatic necrosis virus (IPNV),” Fish & Shellfish Immunology, vol. 23, no. 4, pp. 825–830, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. W. Wang, M. Zhang, Z. Xiao, and L. Sun, “Cynoglossus semilaevis ISG15: a secreted cytokine-like protein that stimulates antiviral immune response in a LRGG motif-dependent manner,” PLoS ONE, vol. 7, no. 9, Article ID e44884, 2012. View at Publisher · View at Google Scholar · View at Scopus
  153. X. Huang, Y. Huang, J. Cai, S. Wei, Z. Ouyang, and Q. Qin, “Molecular cloning, expression and functional analysis of ISG15 in orange-spotted grouper, Epinephelus coioides,” Fish & Shellfish Immunology, vol. 34, no. 5, pp. 1094–1102, 2013. View at Publisher · View at Google Scholar · View at Scopus
  154. C. Langevin, L. M. van der Aa, A. Houel et al., “Zebrafish ISG15 exerts a strong antiviral activity against RNA and DNA viruses and regulates the interferon response,” Journal of Virology, vol. 87, no. 18, pp. 10025–10036, 2013. View at Publisher · View at Google Scholar · View at Scopus
  155. Y. Zhang, Y. Wang, and J. Gui, “Identification and characterization of two homologues of interferon-stimulated gene ISG15 in crucian carp,” Fish & Shellfish Immunology, vol. 23, no. 1, pp. 52–61, 2007. View at Publisher · View at Google Scholar · View at Scopus
  156. D. Kim, J. Hur, K. Park et al., “Distinct Z-DNA binding mode of a PKR-like protein kinase containing a Z-DNA binding domain (PKZ),” Nucleic Acids Research, vol. 42, no. 9, pp. 5937–5948, 2014. View at Publisher · View at Google Scholar · View at Scopus
  157. S. Rothenburg, N. Deigendesch, M. Dey, T. E. Dever, and L. Tazi, “Double-stranded RNA-activated protein kinase PKR of fishes and amphibians: varying the number of double-stranded RNA binding domains and lineage-specific duplications,” BMC Biology, vol. 6, article 12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  158. P. Yang, C. Wu, W. Li, L. Fan, G. Lin, and C. Hu, “Cloning and functional analysis of PKZ (PKR-like) from grass carp (Ctenopharyngodon idellus),” Fish & Shellfish Immunology, vol. 31, no. 6, pp. 1173–1178, 2011. View at Publisher · View at Google Scholar · View at Scopus
  159. Y. Hu, W. Li, D. Li et al., “Cloning, expression and functional analysis of PKR from grass carp (Ctenopharyngodon idellus),” Fish & Shellfish Immunology, vol. 35, no. 6, pp. 1874–1881, 2013. View at Publisher · View at Google Scholar · View at Scopus
  160. J. Su, Z. Zhu, and Y. Wang, “Molecular cloning, characterization and expression analysis of the PKZ gene in rare minnow Gobiocypris rarus,” Fish & Shellfish Immunology, vol. 25, no. 1-2, pp. 106–113, 2008. View at Publisher · View at Google Scholar · View at Scopus
  161. Y. Zhang and J. Gui, “Identification of two novel interferon-stimulated genes from cultured CAB cells induced by UV-inactivated grass carp hemorrhage virus,” Diseases of Aquatic Organisms, vol. 60, no. 1, pp. 1–9, 2004. View at Publisher · View at Google Scholar · View at Scopus
  162. J. Jiang, Y. Zhang, S. Li, F. Yu, F. Sun, and J. Gui, “Expression regulation and functional characterization of a novel interferon inducible gene Gig2 and its promoter,” Molecular Immunology, vol. 46, no. 15, pp. 3131–3140, 2009. View at Publisher · View at Google Scholar · View at Scopus
  163. F. Sun, Y. Zhang, J. Jiang et al., “Gig1, a novel antiviral effector involved in fish interferon response,” Virology, vol. 448, pp. 322–332, 2014. View at Publisher · View at Google Scholar · View at Scopus
  164. Y. Zhang, T. Liu, J. Jiang et al., “Identification of a novel Gig2 gene family specific to non-amniote vertebrates,” PLoS ONE, vol. 8, no. 4, Article ID e60588, 2013. View at Google Scholar
  165. C. Sun, Y. Liu, Y. Hu et al., “Gig1 and Gig2 homologs (CiGig1 and CiGig2) from grass carp (Ctenopharyngodon idella) display good antiviral activities in an IFN-independent pathway,” Developmental and Comparative Immunology, vol. 41, no. 4, pp. 477–483, 2013. View at Publisher · View at Google Scholar · View at Scopus
  166. C. E. Samuel, “Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral,” Virology, vol. 411, no. 2, pp. 180–193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  167. J. W. Schoggins, S. J. Wilson, M. Panis et al., “A diverse range of gene products are effectors of the type i interferon antiviral response,” Nature, vol. 472, no. 7344, pp. 481–485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  168. C. Yang, J. Su, Q. Li, R. Zhang, and Y. Rao, “Identification and expression profiles of ADAR1 gene, responsible for RNA editing, in responses to dsRNA and GCRV challenge in grass carp (Ctenopharyngodon idella),” Fish & Shellfish Immunology, vol. 33, no. 4, pp. 1042–1049, 2012. View at Publisher · View at Google Scholar · View at Scopus
  169. L. M. van der Aa, L. Jouneau, E. Laplantine, O. Bouchez, L. van Kemenade, and P. Boudinot, “FinTRIMs, fish virus-inducible proteins with E3 ubiquitin ligase activity,” Developmental and Comparative Immunology, vol. 36, no. 2, pp. 433–441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. K. Ozato, D.-M. Shin, T.-H. Chang, and H. C. Morse III, “TRIM family proteins and their emerging roles in innate immunity,” Nature Reviews Immunology, vol. 8, no. 11, pp. 849–860, 2008. View at Publisher · View at Google Scholar · View at Scopus
  171. F. Turrini, A. di Pietro, and E. Vicenzi, “Lentiviral effector pathways of TRIM proteins,” DNA and Cell Biology, vol. 33, no. 4, pp. 191–197, 2014. View at Publisher · View at Google Scholar · View at Scopus
  172. L. M. van der Aa, J.-P. Levraud, M. Yahmi et al., “A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish,” BMC Biology, vol. 7, article 7, 2009. View at Publisher · View at Google Scholar · View at Scopus
  173. G. A. Versteeg, R. Rajsbaum, M. T. Sánchez-Aparicio et al., “The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors,” Immunity, vol. 38, no. 2, pp. 384–398, 2013. View at Publisher · View at Google Scholar · View at Scopus
  174. P. Boudinot, L. M. van der Aa, L. Jouneau et al., “Origin and evolution of TRIM proteins: new insights from the complete TRIM repertoire of zebrafish and pufferfish,” PLoS ONE, vol. 6, no. 7, Article ID e22022, 2011. View at Publisher · View at Google Scholar · View at Scopus
  175. L. Carthagena, A. Bergamaschi, J. M. Luna et al., “Human TRIM gene expression in response to interferons,” PLoS ONE, vol. 4, no. 3, Article ID e4894, 2009. View at Publisher · View at Google Scholar · View at Scopus
  176. B. Gao, Y. Wang, W. Xu, Z. Duan, and S. Xiong, “A 5′ extended IFN-stimulating response element is crucial for IFN-γ-induced tripartite motif 22 expression via interaction with IFN regulatory factor-1,” The Journal of Immunology, vol. 185, no. 4, pp. 2314–2323, 2010. View at Publisher · View at Google Scholar · View at Scopus
  177. K. Asaoka, K. Ikeda, T. Hishinuma, K. Horie-Inoue, S. Takeda, and S. Inoue, “A retrovirus restriction factor TRIM5α is transcriptionally regulated by interferons,” Biochemical and Biophysical Research Communications, vol. 338, no. 4, pp. 1950–1956, 2005. View at Publisher · View at Google Scholar · View at Scopus
  178. M. U. Gack, Y. C. Shin, C.-H. Joo et al., “TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity,” Nature, vol. 446, no. 7138, pp. 916–920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  179. G. D. Manocha, R. Mishra, N. Sharma, K. L. Kumawat, A. Basu, and S. K. Singh, “Regulatory role of TRIM21 in the type-I interferon pathway in Japanese encephalitis virus-infected human microglial cells,” Journal of Neuroinflammation, vol. 11, article 24, 2014. View at Publisher · View at Google Scholar · View at Scopus
  180. C. Wynne, E. Lazzari, S. Smith et al., “TRIM68 negatively regulates IFN-beta production by degrading TRK fused gene, a novel driver of IFN-beta downstream of anti-viral detection systems,” PLoS ONE, vol. 9, no. 7, Article ID e101503, 2014. View at Publisher · View at Google Scholar
  181. J. Yan, Q. Li, A.-P. Mao, M.-M. Hu, and H.-B. Shu, “TRIM4 modulates type I interferon induction and cellular antiviral response by targeting RIG-I for K63-linked ubiquitination,” Journal of Molecular Cell Biology, vol. 6, no. 2, pp. 154–163, 2014. View at Publisher · View at Google Scholar · View at Scopus
  182. T. Kondo, M. Watanabe, and S. Hatakeyama, “TRIM59 interacts with ECSIT and negatively regulates NF-kappaB and IRF-3/7-mediated signal pathways,” Biochemical and Biophysical Research Communications, vol. 422, no. 3, pp. 501–507, 2012. View at Publisher · View at Google Scholar · View at Scopus
  183. J. Zhang, M. Hu, Y. Wang, and H. Shu, “TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination,” The Journal of Biological Chemistry, vol. 287, no. 34, pp. 28646–28655, 2012. View at Publisher · View at Google Scholar · View at Scopus
  184. Q. Xue, Z. Zhou, X. Lei et al., “TRIM38 negatively eegulates TLR3-mediated IFN-β signaling by targeting TRIF for degradation,” PLoS ONE, vol. 7, no. 10, Article ID e46825, 2012. View at Publisher · View at Google Scholar · View at Scopus
  185. W. Zhao, L. Wang, M. Zhang et al., “Tripartite motif-containing protein 38 negatively regulates TLR3/4- and RIG-I-mediated IFN-β production and antiviral response by targeting NAP1,” The Journal of Immunology, vol. 188, no. 11, pp. 5311–5318, 2012. View at Publisher · View at Google Scholar · View at Scopus
  186. W. Zhao, L. Wang, M. Zhang, C. Yuan, and C. Gao, “E3 ubiquitin ligase tripartite motif 38 negatively regulates TLR-mediated immune responses by proteasomal degradation of TNF receptor-associated factor 6 in macrophages,” The Journal of Immunology, vol. 188, no. 6, pp. 2567–2574, 2012. View at Publisher · View at Google Scholar · View at Scopus
  187. B. Zurek, I. Schoultz, A. Neerincx et al., “TRIM27 negatively regulates NOD2 by ubiquitination and proteasomal degradation,” PLoS ONE, vol. 7, no. 7, Article ID e41255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  188. F. Du, J. Su, R. Huang, L. Liao, Z. Zhu, and Y. Wang, “Cloning and preliminary functional studies of the JAM-A gene in grass carp (Ctenopharyngodon idellus),” Fish & Shellfish Immunology, vol. 34, no. 6, pp. 1476–1484, 2013. View at Publisher · View at Google Scholar · View at Scopus
  189. X. Shen, T. Wang, D. Xu, and L. Lu, “Proteomic identification, characterization and expression analysis of Ctenopharyngodon idella VDAC1 upregulated by grass carp reovirus infection,” Fish and Shellfish Immunology, vol. 37, no. 1, pp. 96–107, 2014. View at Publisher · View at Google Scholar · View at Scopus
  190. J. Cai, L. Yang, B. Wang et al., “Identification of a novel N4BP1-like gene from grass carp (Ctenopharyngodon idella) in response to GCRV infection,” Fish & Shellfish Immunology, vol. 36, no. 1, pp. 223–228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  191. H. Wang, X. Shen, D. Xu, and L. Lu, “Lipopolysaccharide-induced TNF-alpha factor in grass carp (Ctenopharyngodon idella): evidence for its involvement in antiviral innate immunity,” Fish & Shellfish Immunology, vol. 34, no. 2, pp. 538–545, 2013. View at Publisher · View at Google Scholar · View at Scopus
  192. L. Wang, N. Shang, H. Feng, Q. Guo, and H. Dai, “Molecular cloning of grass carp (Ctenopharyngodon idellus) T-bet and GATA-3, and their expression profiles with IFN-γ in response to grass carp reovirus (GCRV) infection,” Fish Physiology and Biochemistry, vol. 39, no. 4, pp. 793–805, 2013. View at Publisher · View at Google Scholar · View at Scopus
  193. N. Singh, D. R. Choudhury, A. K. Singh et al., “Comparison of SSR and SNP markers in estimation of genetic diversity and population structure of Indian rice varieties,” PLoS ONE, vol. 8, no. 12, Article ID e84136, 2013. View at Publisher · View at Google Scholar · View at Scopus
  194. M. J. Hayden, T. M. Nguyen, A. Waterman, and K. J. Chalmers, “Multiplex-ready PCR: a new method for multiplexed SSR and SNP genotyping,” BMC Genomics, vol. 9, article 80, 2008. View at Publisher · View at Google Scholar · View at Scopus
  195. W. Ding, L. Cao, and Z. Cao, “The SRAP and SCAR molecular markers for detecting germ degeneration in Ctenopharyngodon idellus,” Acta Hydrobiologica Sinica, vol. 54, no. 3, pp. 475–481, 2008 (Chinese). View at Google Scholar
  196. L. Xue, J. Wei, H. Yu, and H. Qian, “Progress in fish genetic markers,” Journal of Zhejiang Ocean University, vol. 23, no. 3, pp. 240–243, 2004 (Chinese). View at Google Scholar
  197. J. Yang, P. Zhang, Q. Wei, G. Zou, and G. Yang, “Construction of a sequence-known marker linkage map of silover carp and the marker synteny comparsion between silver carp and grass carp,” Periodical of Ocean University of China, vol. 42, no. 7-8, pp. 76–81, 2012 (Chinese). View at Google Scholar
  198. D. S. Portnoy and E. J. Heist, “Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs,” Journal of Fish Biology, vol. 80, no. 5, pp. 1120–1140, 2012. View at Publisher · View at Google Scholar · View at Scopus
  199. C. Li, H. Liu, R. Huang et al., “Inentification of type I microsatellite markers and their polymorphism in grass carp (Ctenopharyngodon idellus),” Acta Hydrobiologica Sinica, vol. 35, no. 4, pp. 681–687, 2011 (Chinese). View at Google Scholar
  200. H. Lian, M. Shi, F. Du et al., “Cloning and characterization of (AG)-microsatellites in grass carp (Ctenopharyngodon idellus),” Acta Hydrobiologica Sinica, vol. 36, no. 1, pp. 29–34, 2012 (Chinese). View at Google Scholar
  201. D. van Inghelandt, A. E. Melchinger, C. Lebreton, and B. Stich, “Population structure and genetic diversity in a commercial maize breeding program assessed with SSR and SNP markers,” Theoretical and Applied Genetics, vol. 120, no. 7, pp. 1289–1299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  202. L. Zhang, Q. Luo, Q. Fang, and Y. Wang, “An improved RT-PCR assay for rapid and sensitive detection of grass carp reovirus,” Journal of Virological Methods, vol. 169, no. 1, pp. 28–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  203. Q. Zhang, Y. Yan, J. Shen et al., “Development of a reverse transcription loop-mediated isothermal amplification assay for rapid detection of grass carp reovirus,” Journal of Virological Methods, vol. 187, no. 2, pp. 384–389, 2013. View at Publisher · View at Google Scholar · View at Scopus
  204. C. Chen, X. Sun, L. Liao et al., “Antigenic analysis of grass carp reovirus using single-chain variable fragment antibody against IgM from Ctenopharyngodon idella,” Science China Life Sciences, vol. 56, no. 1, pp. 59–65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  205. Y. He, Y. Jiang, and L. Lu, “Serodiagnosis of grass carp reovirus infection in grass carp Ctenopharyngodon idella by a novel Western blot technique,” Journal of Virological Methods, vol. 194, no. 1-2, pp. 14–20, 2013. View at Publisher · View at Google Scholar · View at Scopus
  206. J. Hongli, Z. Lifeng, F. Zhenzhen et al., “Detection of grass carp reovirus (GCRV) with monoclonal antibodies,” Archives of Virology, vol. 159, no. 4, pp. 649–655, 2014. View at Publisher · View at Google Scholar · View at Scopus
  207. A. K. Dhar, S. K. Manna, and F. C. T. Allnutt, “Viral vaccines for farmed finfish,” VirusDisease, vol. 25, no. 1, pp. 1–17, 2014. View at Publisher · View at Google Scholar · View at Scopus
  208. G. Hao, J. Shen, and X. Pan, “The current development of nucleic acid vaccine and its application in fish,” Journal of Dalian Fisheries University, vol. 22, no. 2, pp. 142–148, 2007 (Chinese). View at Google Scholar
  209. S. Xu, H. Li, G. Deng, and L. Jiang, “The preparation and immune effect of attenuated live vaccine obtained through cell culture for hemorrhage of grass carp,” Journal of Fishery Sciences of China, vol. 18, no. 2, pp. 111–117, 1994 (Chinese). View at Google Scholar
  210. X. Yang and W. Zou, “Inactivated vaccine obtained through cell culture for hemorrhage of grass carp (Ctenopharyngodon idella): the srability of vaccine and influence of adjuvants and booster immuniation on the immune response,” Acta Hydrobiologica Sinica, vol. 27, no. 1, pp. 46–52, 1993 (Chinese). View at Google Scholar
  211. L. Shao, X. Sun, and Q. Fang, “Antibodies against outer-capsid proteins of grass carp reovirus expressed in E. coli are capable of neutralizing viral infectivity,” Virology Journal, vol. 8, article 347, 2011. View at Publisher · View at Google Scholar · View at Scopus
  212. Y. Tian, X. Ye, L. Zhang, G. Deng, and Y. Bai, “Development of a novel candidate subunit vaccine against Grass carp reovirus Guangdong strain (GCRV-GD108),” Fish & Shellfish Immunology, vol. 35, no. 2, pp. 351–356, 2013. View at Publisher · View at Google Scholar · View at Scopus
  213. J. Heppell and H. L. Davis, “Application of DNA vaccine technology to aquaculture,” Advanced Drug Delivery Reviews, vol. 43, no. 1, pp. 29–43, 2000. View at Publisher · View at Google Scholar · View at Scopus
  214. Y. Zhou, Y. Fan, and L. Zeng, “Construction of a recombinant eukaryotic vector for a grass carp reovirus VP6 gene and its expression in vitro and in vivo,” Indian Journal of Virology, vol. 25, no. 1, pp. 69–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  215. B. Zhu, G. Liu, Y. Gong, F. Ling, and G. Wang, “Protective immunity of grass carp immunized with DNA vaccine encoding the vp7 gene of grass carp reovirus using carbon nanotubes as a carrier molecule,” Fish & Shellfish Immunology, vol. 42, no. 2, pp. 325–334, 2015. View at Publisher · View at Google Scholar
  216. G. Cao, L. Liu, R. Xue et al., “Evaluation of immune efficacy of GCRV vp6 DNA vaccine,” Journal of Fishery Sciences of China, vol. 19, no. 5, pp. 841–847, 2012 (Chinese). View at Publisher · View at Google Scholar
  217. X. Li, L. Yang, S. Jiang, M. Fu, J. Huang, and S. Jiang, “Identification and expression analysis of Dicer2 in black tiger shrimp (Penaeus monodon) responses to immune challenges,” Fish & Shellfish Immunology, vol. 35, no. 1, pp. 1–8, 2013. View at Publisher · View at Google Scholar · View at Scopus
  218. S. Guo, J. Li, and L. Lu, “Molecular pathogenesis of grass carp reovirus and novel antiviral strategies,” Fishery Modernization, vol. 37, no. 1, pp. 37–42, 2010 (Chinese). View at Google Scholar
  219. X. Shen, D. Xu, J. Li, and L. Lu, “Molecular cloning and immune responsive expression of a ribonuclease III orthologue involved in RNA interference, dicer, in grass carp Ctenopharyngodon idella,” Journal of Fish Biology, vol. 83, no. 5, pp. 1234–1248, 2013. View at Publisher · View at Google Scholar · View at Scopus
  220. S. Guo, D. Xu, H. Xu, T. Wang, J. Li, and L. Lu, “Suppression of RNA interference pathway in vitro by grass carp reovirus,” Virologica Sinica, vol. 27, no. 2, pp. 109–119, 2012. View at Publisher · View at Google Scholar · View at Scopus
  221. B. Li, Y. Fan, Y. Li, J. Xu, Y. Zhou, and L. Zeng, “Highly efficient inhibition on replication of grass carp reovirus mediated by chemically synthesized small interfering RNAs,” Chinese Journal of Virology, vol. 25, no. 5, pp. 388–394, 2009 (Chinese). View at Google Scholar · View at Scopus
  222. C. Lupini, M. Cecchinato, A. Scagliarini, R. Graziani, and E. Catelli, “In vitro antiviral activity of chestnut and quebracho woods extracts against avian reovirus and metapneumovirus,” Research in Veterinary Science, vol. 87, no. 3, pp. 482–487, 2009. View at Publisher · View at Google Scholar · View at Scopus
  223. L. L. Hermann and K. M. Coombs, “Inhibition of reovirus by Mycophenolic acid is associated with the M1 genome segment,” Journal of Virology, vol. 78, no. 12, pp. 6171–6179, 2004. View at Publisher · View at Google Scholar · View at Scopus