1887

Abstract

Aquareovirus is a genus of viruses in family Reoviridae, subfamily Spinareovirinae, members of which infect fish, shellfish and crustaceans. Grass carp reovirus (GCRV), a genotype 1 reovirus isolated from grass carp, has served as a model strain for investigating aquareovirus–host interactions. Herein, we report a neglected open reading frame (ORF), tentatively named NS12, residing between NS16 and NS31 in segment 7 (S7) of the virus genome. With an additional reading frame, the nucleotide sequence of NS12 partially overlaps with the 3′ expressible nucleotide sequence of NS16. NS12 is not a pseudogene during virus replication, as confirmed in fish cells infected with GCRV and based on amino acid sequence analysis and protein expression pattern. Bioinformatics analysis indicated that NS12 is a transmembrane protein, which was confirmed by its exclusive presence in the membrane-associated fraction of the cell lysate. However, unlike fusion protein NS16, NS12 alone could not induce visible syncytium formation in fish cells. Thus, NS12 is functionally distinct from known aquareovirus membrane-associated protein NS16. NS12-like ORFs (with an AUG or non-AUG initiator codon) are also present in the S7 segment of other aquareoviruses, suggesting that NS12 homologues may be widely distributed in the genus Aquareovirus.

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2019-01-28
2021-10-21
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References

  1. Mohd Jaafar F, Goodwin AE, Belhouchet M, Merry G, Fang Q et al. Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses. Virology 2008; 373:310–321 [View Article][PubMed]
    [Google Scholar]
  2. Nibert ML, Duncan R. Bioinformatics of recent aqua- and orthoreovirus isolates from fish: evolutionary gain or loss of FAST and fiber proteins and taxonomic implications. PLoS One 2013; 8:e68607 [View Article][PubMed]
    [Google Scholar]
  3. Zhang F, Guo H, Zhang J, Chen Q, Fang Q. Identification of the caveolae/raft-mediated endocytosis as the primary entry pathway for aquareovirus. Virology 2018; 513:195–207 [View Article][PubMed]
    [Google Scholar]
  4. Wang T, Li J, Lu L. Quantitative in vivo and in vitro characterization of co-infection by two genetically distant grass carp reoviruses. J Gen Virol 2013; 94:1301–1309 [View Article][PubMed]
    [Google Scholar]
  5. Guo H, Chen Q, Yan L, Zhang J, Yan S et al. Identification of a functional motif in the AqRV NS26 protein required for enhancing the fusogenic activity of FAST protein NS16. J Gen Virol 2015; 96:1080–1085 [View Article][PubMed]
    [Google Scholar]
  6. Wang X, Zhang F, Su R, Li X, Chen W et al. Structure of RNA polymerase complex and genome within a dsRNA virus provides insights into the mechanisms of transcription and assembly. Proceedings of the National Academy of Sciences 2018; 115:7344–7349 [View Article]
    [Google Scholar]
  7. Borodavka A, Desselberger U, Patton JT. Genome packaging in multi-segmented dsRNA viruses: distinct mechanisms with similar outcomes. Curr Opin Virol 2018; 33:106–112 [View Article][PubMed]
    [Google Scholar]
  8. Zhang X, Jin L, Fang Q, Hui WH, Zhou ZH. 3.3 A cryo-EM structure of a non enveloped virus reveals a priming mechanism for cell entry. Cell 2010; 141:472–482 [View Article][PubMed]
    [Google Scholar]
  9. Liu W, Wang H, Yu F, Lu L. Grass carp reovirus outer capsid proteins VP5 and VP7 interact in vitro. Arch Virol 2017; 162:2375–2380 [View Article][PubMed]
    [Google Scholar]
  10. Cheng L, Zhu J, Hui WH, Zhang X, Honig B et al. Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. J Mol Biol 2010; 397:852–863 [View Article][PubMed]
    [Google Scholar]
  11. Cheng L, Fang Q, Shah S, Atanasov IC, Zhou ZH. Subnanometer-resolution structures of the grass carp reovirus core and virion. J Mol Biol 2008; 382:213–222 [View Article][PubMed]
    [Google Scholar]
  12. Wang H, Yu F, Li J, Lu L. Laminin receptor is an interacting partner for viral outer capsid protein VP5 in grass carp reovirus infection. Virology 2016; 490:59–68 [View Article][PubMed]
    [Google Scholar]
  13. Zhang J, Guo H, Chen Q, Zhang F, Fang Q. The N-Terminal of aquareovirus NS80 is required for interacting with viral proteins and viral replication. PLoS One 2016; 11:e0148550 [View Article][PubMed]
    [Google Scholar]
  14. Yan L, Zhang J, Guo H, Yan S, Chen Q et al. Aquareovirus NS80 initiates efficient viral replication by retaining core proteins within replication-associated viral inclusion bodies. PLoS One 2015; 10:e0126127 [View Article][PubMed]
    [Google Scholar]
  15. Ciechonska M, Duncan R. Reovirus FAST proteins: virus-encoded cellular fusogens. Trends Microbiol 2014; 22:715–724 [View Article][PubMed]
    [Google Scholar]
  16. Guo H, Sun X, Yan L, Shao L, Fang Q. The NS16 protein of aquareovirus-C is a fusion-associated small transmembrane (FAST) protein, and its activity can be enhanced by the nonstructural protein NS26. Virus Res 2013; 171:129–137 [View Article][PubMed]
    [Google Scholar]
  17. Lu J, Wang H, Zhang Y, Li Y, Lu L. Grass carp reovirus NS26 interacts with cellular lipopolysaccharide-induced tumor necrosis factor-alpha factor, LITAF. Virus Genes 2016; 52:789–796 [View Article][PubMed]
    [Google Scholar]
  18. Racine T, Hurst T, Barry C, Shou J, Kibenge F et al. Aquareovirus effects syncytiogenesis by using a novel member of the FAST protein family translated from a noncanonical translation start site. J Virol 2009; 83:5951–5955 [View Article][PubMed]
    [Google Scholar]
  19. Racine T, Duncan R. Facilitated leaky scanning and atypical ribosome shunting direct downstream translation initiation on the tricistronic S1 mRNA of avian reovirus. Nucleic Acids Res 2010; 38:7260–7272 [View Article][PubMed]
    [Google Scholar]
  20. Racine T, Barry C, Roy K, Dawe SJ, Shmulevitz M et al. Leaky scanning and scanning-independent ribosome migration on the tricistronic S1 mRNA of avian reovirus. J Biol Chem 2007; 282:25613–25622 [View Article][PubMed]
    [Google Scholar]
  21. Firth AE. Mapping overlapping functional elements embedded within the protein-coding regions of RNA viruses. Nucleic Acids Res 2014; 42:12425–12439 [View Article][PubMed]
    [Google Scholar]
  22. He Y, Xu H, Yang Q, Xu D, Lu L. 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 2011; 8:132 [View Article][PubMed]
    [Google Scholar]
  23. Yu F, Wang H, Wang L, Lu L. Orthoreovirus outer-fiber proteins are substrates for SUMO-conjugating enzyme Ubc9. Oncotarget 2016; 7:79814–79827 [View Article][PubMed]
    [Google Scholar]
  24. Guo X, Dong Z, Zhang Y, Li Y, Liu H et al. Proteins in the cocoon of silkworm inhibit the growth of Beauveria bassiana. PLoS One 2016; 11:e0151764 [View Article][PubMed]
    [Google Scholar]
  25. Cross FR. Tying down loose ends in the chlamydomonas genome: functional significance of abundant upstream open reading frames. G3 (Bethesda, Md) 2015; 6:435–446 [View Article][PubMed]
    [Google Scholar]
  26. Key T, Read J, Nibert ML, Duncan R. Piscine reovirus encodes a cytotoxic, non-fusogenic, integral membrane protein and previously unrecognized virion outer-capsid proteins. J Gen Virol 2013; 94:1039–1050 [View Article][PubMed]
    [Google Scholar]
  27. Firth AE, Brierley I. Non-canonical translation in RNA viruses. J Gen Virol 2012; 93:1385–1409 [View Article][PubMed]
    [Google Scholar]
  28. Dietrich MH, Ogden KM, Long JM, Ebenhoch R, Thor A et al. Structural and functional features of the reovirus σ1 tail. J Virol 2018; 92:JVI.00336–00318 [View Article]
    [Google Scholar]
  29. Boehme KW, Hammer K, Tollefson WC, Konopka-Anstadt JL, Kobayashi T et al. Nonstructural protein σ1s mediates reovirus-induced cell cycle arrest and apoptosis. J Virol 2013; 87:12967–12979 [View Article][PubMed]
    [Google Scholar]
  30. Ke F, He LB, Pei C, Zhang QY. Turbot reovirus (SMReV) genome encoding a FAST protein with a non-AUG start site. BMC Genomics 2011; 12:323 [View Article][PubMed]
    [Google Scholar]
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