Skip to main content

Advertisement

Log in

Identification of a potential transcriptional regulator encoded by grass carp reovirus

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Many transcription factors are encoded by DNA viruses and retroviruses due to their regulatory roles in gene expression in the host cell. However, no transcriptional regulator has been identified in any reovirus. Here, a non-structural protein, NS31, encoded by grass carp reovirus genomic segment S7 was characterized. The NS31 protein is predicted to contain a helix-turn-helix (HTH)-like domain and a C-terminal acidic α-helix motif. In yeast, a fusion protein composed of the Gal4-BD domain and NS31 (BD-NS31) was able to activate the expression of reporter genes (Gal1/MEL1 promoter) without the Gal4-AD domain. We also found that NS31 activated the reporter genes in a BD-dependent manner, and both the C- and N-termini contribute to the activation function of NS31. Furthermore, NS31 homologues from other aquareoviruses were also shown to possess a similar transcriptional activation function in yeast. Thus, the aquareovirus NS31 protein appears to act as a transcriptional regulatory protein, the first one identified in a member of the family Reoviridae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Ahn JH, Chiou CJ, Hayward GS (1998) Evaluation and mapping of the DNA binding and oligomerization domains of the IE2 regulatory protein of human cytomegalovirus using yeast one and two hybrid interaction assays. Gene 210:25

    Article  CAS  PubMed  Google Scholar 

  2. Attoui H, Fang Q, Mohd JF, Cantaloube JF, Biagini P, De MP, De LX (2002) Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae). J Gen Virol 83:1941–1951

    Article  CAS  PubMed  Google Scholar 

  3. Bussiere LD, Choudhury P, Bellaire B, Miller CL (2017) Characterization of a replicating mammalian orthoreovirus with tetracysteine tagged μNS for live cell visualization of viral factories. J Virol 91

  4. Cheng L, Fang Q, Shah S, Atanasov IC, Zhou ZH (2008) Subnanometer-resolution structures of the grass carp reovirus core and virion. J Mol Biol 382:213–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cheng L, Zhu J, Hui WH, Zhang X, Honig B, Fang Q, Zhou ZH (2010) Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. J Mol Biol 397:852–863

    Article  CAS  PubMed  Google Scholar 

  6. Chung KM, Song OK, Jang SK (1997) Hepatitis C virus nonstructural protein 5A contains potential transcriptional activator domains. Mol Cells 7:661–667

    CAS  PubMed  Google Scholar 

  7. Ciechonska M, Duncan R (2014) Reovirus FAST proteins: virus-encoded cellular fusogens. Trends Microbiol 22:715–724

    Article  CAS  PubMed  Google Scholar 

  8. Dayalan Naidu S, Kostov RV, Dinkova-Kostova AT (2015) Transcription factors Hsf1 and Nrf2 engage in crosstalk for cytoprotection. Trends Pharmacol Sci 36:6–14

    Article  CAS  PubMed  Google Scholar 

  9. Fan Y, Rao S, Zeng L, Ma J, Zhou Y, Xu J, Zhang H (2013) Identification and genomic characterization of a novel fish reovirus, Hubei grass carp disease reovirus, isolated in 2009 in China. J Gen Virol 94:2266–2277

    Article  CAS  PubMed  Google Scholar 

  10. Fang Q, Shah S, Liang Y, Zhou (2005) 3D reconstruction and capsid protein characterization of grass carp reovirus. Science in China 48:593–600

    Article  CAS  PubMed  Google Scholar 

  11. Fang Q, Ke LH (1989) Growth characteristics and high titer culture of grass carp hemorrhage virus (GCHV)-873 in vitro. Virol Sin

  12. Fang Q, Seng EK, Ding QQ, Zhang LL (2008) Characterization of infectious particles of grass carp reovirus by treatment with proteases. Adv Virol 153:675–682

    CAS  Google Scholar 

  13. Fonseca GJ, Cohen MJ, Mymryk JS (2014) Adenovirus E1A recruits the human Paf1 complex to enhance transcriptional elongation. J Virol 88:5630–5637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gaudray G, Gachon F, Basbous J, Biard-Piechaczyk M, Devaux C, Mesnard JM (2002) The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J Virol 76:12813–12822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Guo H, Sun X, Yan L, Shao L, Fang Q (2013) 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 171:129–137

    Article  CAS  PubMed  Google Scholar 

  16. Guo H, Chen Q, Yan L, Zhang J, Yan S, Zhang F, Fang Q (2015) Identification of a functional motif in the AqRV NS26 protein required for enhancing the fusogenic activity of FAST protein NS16. J Gen Virol 96:1080–1085

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hollenberg SM, Evans RM (1988) Multiple and cooperative trans-activation domains of the human glucocorticoid receptor. Cell 55:899

    Article  CAS  PubMed  Google Scholar 

  19. Yan L, Liu H, Li X, Fang Q (2014) The VP2 protein of grass carp reovirus (GCRV) expressed in a baculovirus exhibits RNA polymerase activity. Virol Sin 29:86–93

    Article  CAS  PubMed  Google Scholar 

  20. Jayaram H, Estes MK, Prasad BV (2004) Emerging themes in rotavirus cell entry, genome organization, transcription and replication. Virus Res 101:67–81

    Article  CAS  PubMed  Google Scholar 

  21. Kato N, Lan KH, Ononita SK, Yoshida H, Shiratori Y, Omata M (1997) Hepatitis C virus nonstructural region 5A protein is a potent transcriptional activator. J Virol 71:8856–8859

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Ke F, He LB, Zhang QY (2013) Nonstructural protein NS80 is crucial in recruiting viral components to form aquareoviral factories. PLoS One 8:e63737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lin C, Sun X, Ling S, Qin F (2011) Functional investigation of grass carp reovirus nonstructural protein NS80. Virology Journal 8:168

    Article  CAS  Google Scholar 

  24. Ling S, Chao F, Maj E, Qin F (2010) Molecular characterization of nonstructural protein NS38 of grass carp reovirus. Virologica Sinica 25:123–129

    Article  CAS  Google Scholar 

  25. Liu W, Wang H, Yu F, Lu L (2017) Grass carp reovirus outer capsid proteins VP5 and VP7 interact in vitro. Adv Virol 162:2375–2380

    CAS  Google Scholar 

  26. Lu J, Wang H, Zhang Y, Li Y, Lu L (2016) Grass carp reovirus NS26 interacts with cellular lipopolysaccharide-induced tumor necrosis factor-alpha factor, LITAF. Virus Genes 52:789–796

    Article  CAS  PubMed  Google Scholar 

  27. Lukhovitskaya NI, Solovieva AD, Boddeti SK, Thaduri S, Solovyev AG, Savenkov EI (2013) An RNA virus-encoded zinc-finger protein acts as a plant transcription factor and induces a regulator of cell size and proliferation in two tobacco species. Plant Cell 25:960–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Maqbool MA, Imache MR, Higgs MR, Carmouse S, Pawlotsky JM, Lerat H (2013) Regulation of hepatitis C virus replication by nuclear translocation of nonstructural 5A protein and transcriptional activation of host genes. J Virol 87:5523–5539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mohd-Jaafar F, Goodwin AM, Merry G, Fang Q, Cantaloube J, Biagini P, De-Micco P, Mertens P, Attoui H (2008) Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses. Virology 373:310

    Article  CAS  PubMed  Google Scholar 

  30. Newman JA, Rodrigues C, Lewis RJ (2013) Molecular basis of the activity of SinR protein, the master regulator of biofilm formation in Bacillus subtilis. J Biol Chem 288:10766–10778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pei C, Ke F, Chen ZY, Zhang QY (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. Adv Virol 159:2435–2440

    CAS  Google Scholar 

  32. Rosales R, Harris N, Ahn BY, Moss B (1994) Purification and identification of a vaccinia virus-encoded intermediate stage promoter-specific transcription factor that has homology to eukaryotic transcription factor SII (TFIIS) and an additional role as a viral RNA polymerase subunit. J Biol Chem 269:14260

    CAS  PubMed  Google Scholar 

  33. Ruden DM (1992) Activating regions of yeast transcription factors must have both acidic and hydrophobic amino acids. Chromosoma 101:342–348

    Article  CAS  PubMed  Google Scholar 

  34. Schumacher MA, Chinnam NB, Cuthbert B, Tonthat NK, Whitfill T (2015) Structures of regulatory machinery reveal novel molecular mechanisms controlling B. subtilis nitrogen homeostasis. Genes Dev 29:451–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang H, Yu F, Li J, Lu L (2016) Laminin receptor is an interacting partner for viral outer capsid protein VP5 in grass carp reovirus infection. Virology 490:59–68

    Article  CAS  PubMed  Google Scholar 

  36. Wang Q, Zeng W, Liu C, Zhang C, Wang Y, Shi C, Wu S (2012) Complete genome sequence of a reovirus isolated from Grass Carp, indicating different genotypes of GCRV in China. J Virol 86:12466

    Article  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. Wang X, Zhang F, Su R, Li X, Chen W, Chen Q, Yang T, Wang J, Liu H, Fang Q, Cheng L (2018) Structure of RNA polymerase complex and genome within a dsRNA virus provides insights into the mechanisms of transcription and assembly. Proc Natl Acad Sci 115:7344–7349

    Article  CAS  PubMed  Google Scholar 

  39. Weigel T, Solomaier T, Peuker A, Pathapati T, Wolff MW, Reichl U (2014) A flow-through chromatography process for influenza A and B virus purification. J Virol Methods 207:45–53

    Article  CAS  PubMed  Google Scholar 

  40. Xiaoming Fang (2013) High-resolution 3D structures reveal the biological functions of reoviruses. Virol Sin 28:318–325

    Article  CAS  Google Scholar 

  41. Yan L, Guo H, Sun X, Shao L, Fang Q (2012) Characterization of grass carp reovirus minor core protein VP4. Virol J 9:89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Yan L, Zhang J, Guo H, Yan S, Chen Q, Zhang F, Fang Q (2015) Aquareovirus NS80 initiates efficient viral replication by retaining core proteins within replication-associated viral inclusion bodies. PLoS One 10:e0126127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yan S, Zhang J, Guo H, Yan L, Chen Q, Zhang F, Fang Q (2015) VP5 autocleavage is required for efficient infection by in vitro-recoated aquareovirus particles. J Gen Virol 96:1795–1800

    Article  CAS  PubMed  Google Scholar 

  44. Yang X, Baliji S, Buchmann RC, Wang H, Lindbo JA, Sunter G, Bisaro DM (2007) Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J Virol 81:11972–11981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yang Z, Moss B (2009) Interaction of the vaccinia virus RNA polymerase-associated 94-kilodalton protein with the early transcription factor. J Virol 83:12018–12026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Yu EM, Zhang HF, Li ZF, Wang GJ, Wu HK, Xie J, Yu DG, Xia Y, Zhang K, Gong WB (2017) Proteomic signature of muscle fibre hyperplasia in response to faba bean intake in grass carp. Sci Rep 7:45950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhang J, Guo H, Chen Q, Zhang F, Fang Q (2016) The N-terminal of aquareovirus NS80 is required for interacting with viral proteins and viral replication. PLoS One 11:e0148550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhang X, Jin L, Fang Q, Hui WH, Zhou ZH (2010) 3.3 Å Cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 141:472–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Funding for this research was provided by the National Natural Science Foundation of China (No. 31672690) and the Earmarked Fund for China Agriculture Research System (No. CARS-45-19).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liqun Lu.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical approval

Animal were handled in accordance with the Guidelines on the Care and Use of Animals for Scientific Purposes provided by the Institutional Animal Care and Use Committee (IACUC) of Shanghai Ocean University (No. SHOU-09-007), Shanghai, China.

Additional information

Handling Editor: Chan-Shing Lin.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, F., Wang, H., Wang, L. et al. Identification of a potential transcriptional regulator encoded by grass carp reovirus. Arch Virol 164, 1393–1404 (2019). https://doi.org/10.1007/s00705-019-04204-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-019-04204-1

Navigation