1887

Abstract

The zebrafish () possesses evolutionarily conserved innate and adaptive immunity as a mammal and has recently become a popular vertebrate model to exploit infection and immunity. Antiviral RNA interference (RNAi) has been illuminated in various model organisms, including , , and mice. However, to date, there is no report on the antiviral RNAi pathway of zebrafish. Here, we have evaluated the possible use of zebrafish to study antiviral RNAi with Sindbis virus (SINV), vesicular stomatitis virus (VSV) and Nodamura virus (NoV). We find that SINVs and NoVs induce the production of virus-derived small interfering RNAs (vsiRNAs), the hallmark of antiviral RNAi, with a preference for a length of 22 nucleotides, after infection of larval zebrafish. Meanwhile, the suppressor of RNAi (VSR) protein, NoV B2, may affect the accumulation of the NoV in zebrafish. Furthermore, taking advantage of the fact that zebrafish argonaute-2 (Ago2) protein is naturally deficient in cleavage compared with that of mammals, we provide evidence that the slicing activity of human Ago2 can virtually inhibit the accumulation of RNA virus after being ectopically expressed in larval zebrafish. Thus, zebrafish may be a unique model organism to study the antiviral RNAi pathway.

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 31770179)
    • Principle Award Recipient: yangli
  • National Natural Science Foundation of China (Award 91640111)
    • Principle Award Recipient: yangli
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001552
2021-01-28
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/3/vir001552.html?itemId=/content/journal/jgv/10.1099/jgv.0.001552&mimeType=html&fmt=ahah

References

  1. Ding S-W, Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007; 130:413–426 [View Article][PubMed]
    [Google Scholar]
  2. Guo Z, Li Y, Ding S-W. Small RNA-based antimicrobial immunity. Nat Rev Immunol 2019; 19:31–44 [View Article][PubMed]
    [Google Scholar]
  3. Berkhout B. RNAi-Mediated antiviral immunity in mammals. Curr Opin Virol 2018; 32:9–14 [View Article][PubMed]
    [Google Scholar]
  4. Maillard PV, van der Veen AG, Poirier EZ, Reis e Sousa C. Slicing and dicing viruses: antiviral RNA interference in mammals. Embo J 2019; 38: [View Article][PubMed]
    [Google Scholar]
  5. Li F, Ding S-W. Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 2006; 60:503–531 [View Article][PubMed]
    [Google Scholar]
  6. Galiana-Arnoux D, Dostert C, Schneemann A, Hoffmann JA, Imler J-L. Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat Immunol 2006; 7:590–597 [View Article][PubMed]
    [Google Scholar]
  7. van Rij RP, Saleh M-C, Berry B, Foo C, Houk A et al. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 2006; 20:2985–2995 [View Article][PubMed]
    [Google Scholar]
  8. Ding SW. RNA-Based antiviral immunity. Nat Rev Immunol 2010; 10:632–644 [View Article][PubMed]
    [Google Scholar]
  9. Li Y, Lu J, Han Y, Fan X, Ding S-W. RNA interference functions as an antiviral immunity mechanism in mammals. Science 2013; 342:231–234 [View Article][PubMed]
    [Google Scholar]
  10. Li Y, Basavappa M, Lu J, Dong S, Cronkite DA et al. Induction and suppression of antiviral RNA interference by influenza A virus in mammalian cells. Nat Microbiol 2016; 2:16250 [View Article][PubMed]
    [Google Scholar]
  11. Qiu Y, Xu Y, Zhang Y, Zhou H, Deng YQ et al. Human virus-derived small RNAs can confer antiviral immunity in mammals. Immunity 2017; 46:e1005992–1004 [View Article][PubMed]
    [Google Scholar]
  12. Xu Y-P, Qiu Y, Zhang B, Chen G, Chen Q et al. Zika virus infection induces RNAi-mediated antiviral immunity in human neural progenitors and brain organoids. Cell Res 2019; 29:265–273 [View Article][PubMed]
    [Google Scholar]
  13. Han Q, Chen G, Wang J, Jee D, Li W-X et al. Mechanism and function of antiviral RNA interference in mice. mBio 2020; 11:e03278-19 [View Article][PubMed]
    [Google Scholar]
  14. Zhang Y, Li Z, Ye Z, Xu Y, Wang B. The activation of antiviral RNA interference not only exists in neural progenitor cells but also in somatic cells in mammals. Emerg Microbes Infect 20201–34
    [Google Scholar]
  15. Maillard PV, Ciaudo C, Marchais A, Li Y, Jay F et al. Antiviral RNA interference in mammalian cells. Science 2013; 342:235–238 [View Article][PubMed]
    [Google Scholar]
  16. Qiu Y, Xu Y-P, Wang M, Miao M, Zhou H et al. Flavivirus induces and antagonizes antiviral RNA interference in both mammals and mosquitoes. Sci Adv 2020; 6:eaax7989 [View Article][PubMed]
    [Google Scholar]
  17. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science 2004; 305:1437–1441 [View Article][PubMed]
    [Google Scholar]
  18. Lieschke GJ, Currie PD. Animal models of human disease: zebrafish swim into view. Nat Rev Genet 2007; 8:353–367 [View Article][PubMed]
    [Google Scholar]
  19. MacRae CA, Peterson RT. Zebrafish as tools for drug discovery. Nat Rev Drug Discov 2015; 14:721–731 [View Article][PubMed]
    [Google Scholar]
  20. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496:498–503 [View Article][PubMed]
    [Google Scholar]
  21. Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA et al. The zebrafish as a model organism to study development of the immune system. Adv Immunol 2003; 81:253–330[PubMed]
    [Google Scholar]
  22. Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 2004; 28:9–28 [View Article][PubMed]
    [Google Scholar]
  23. Van Dycke J, Ny A, Conceicao-Neto N, Maes J, Hosmillo M et al. A robust human norovirus replication model in zebrafish larvae. PLoS Pathog 2019; 15:e1008009 [View Article][PubMed]
    [Google Scholar]
  24. Gabor KA, Goody MF, Mowel WK, Breitbach ME, Gratacap RL et al. Influenza A virus infection in zebrafish recapitulates mammalian infection and sensitivity to anti-influenza drug treatment. Dis Model Mech 2014; 7:1227–1237 [View Article][PubMed]
    [Google Scholar]
  25. Passoni G, Langevin C, Palha N, Mounce BC, Briolat V et al. Imaging of viral neuroinvasion in the zebrafish reveals that Sindbis and Chikungunya viruses favour different entry routes. Dis Model Mech 2017; 10:847–857 [View Article][PubMed]
    [Google Scholar]
  26. Guerra-Varela J, Baz-Martínez M, Da Silva-Álvarez S, Losada AP, Quiroga MI et al. Susceptibility of zebrafish to vesicular stomatitis virus infection. Zebrafish 2018; 15:124–132 [View Article][PubMed]
    [Google Scholar]
  27. Kelly A, Hurlstone AF. The use of RNAi technologies for gene knockdown in zebrafish. Brief Funct Genomics 2011; 10:189–196 [View Article][PubMed]
    [Google Scholar]
  28. Chen GR, Sive H, Bartel DP. A seed mismatch enhances Argonaute2-Catalyzed cleavage and partially rescues severely impaired cleavage found in fish. Mol Cell 2017; 68:1095–1107 [View Article][PubMed]
    [Google Scholar]
  29. Mueller S, Gausson V, Vodovar N, Deddouche S, Troxler L et al. RNAi-Mediated immunity provides strong protection against the negative-strand RNA vesicular stomatitis virus in Drosophila. Proc Natl Acad Sci U S A 2010; 107:19390–19395 [View Article][PubMed]
    [Google Scholar]
  30. Poirier EZ, Goic B, Tomé-Poderti L, Frangeul L, Boussier J et al. Dicer-2-Dependent generation of viral DNA from defective genomes of RNA viruses modulates antiviral immunity in insects. Cell Host Microbe 2018; 23:e358353–365 [View Article][PubMed]
    [Google Scholar]
  31. Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G et al. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 2005; 436:1040–1043 [View Article][PubMed]
    [Google Scholar]
  32. Gammon DB, Ishidate T, Li L, Gu W, Silverman N et al. The antiviral RNA interference response provides resistance to lethal arbovirus infection and vertical transmission in Caenorhabditis elegans. Curr Biol 2017; 27:795–806 [View Article][PubMed]
    [Google Scholar]
  33. Johnson KL, Price BD, Ball LA. Recovery of infectivity from cDNA clones of nodamura virus and identification of small nonstructural proteins. Virology 2003; 305:436–451 [View Article][PubMed]
    [Google Scholar]
  34. Li W-X, Li H, Lu R, Li F, Dus M et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc Natl Acad Sci U S A 2004; 101:1350–1355 [View Article][PubMed]
    [Google Scholar]
  35. Johnson KL, Price BD, Eckerle LD, Ball LA. Nodamura virus nonstructural protein B2 can enhance viral RNA accumulation in both mammalian and insect cells. J Virol 2004; 78:6698–6704 [View Article][PubMed]
    [Google Scholar]
  36. Fenner BJ, Goh W, Kwang J. Sequestration and protection of double-stranded RNA by the betanodavirus B2 protein. J Virol 2006; 80:6822–6833 [View Article][PubMed]
    [Google Scholar]
  37. Fenner BJ, Thiagarajan R, Chua HK, Kwang J. Betanodavirus B2 is an RNA interference antagonist that facilitates intracellular viral RNA accumulation. J Virol 2006; 80:85–94 [View Article][PubMed]
    [Google Scholar]
  38. Maillard PV, Van der Veen AG, Deddouche-Grass S, Rogers NC, Merits A et al. Inactivation of the type I interferon pathway reveals long double-stranded RNA-mediated RNA interference in mammalian cells. Embo J 2016; 35:2505–2518 [View Article][PubMed]
    [Google Scholar]
  39. van der Veen AG, Maillard PV, Schmidt JM, Lee SA, Deddouche-Grass S et al. The RIG-I-like receptor LGP2 inhibits Dicer-dependent processing of long double-stranded RNA and blocks RNA interference in mammalian cells. Embo J 2018; 37: [View Article][PubMed]
    [Google Scholar]
  40. Seo GJ, Kincaid RP, Phanaksri T, Burke JM, Pare JM et al. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 2013; 14:435–445 [View Article][PubMed]
    [Google Scholar]
  41. Tassetto M, Kunitomi M, Andino R. Circulating immune cells mediate a systemic RNAi-based adaptive antiviral response in Drosophila. Cell 2017; 169:e313314–325 [View Article][PubMed]
    [Google Scholar]
  42. Parameswaran P, Sklan E, Wilkins C, Burgon T, Samuel MA et al. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog 2010; 6:e1000764 [View Article][PubMed]
    [Google Scholar]
  43. Donaszi-Ivanov A, Mohorianu I, Dalmay T, Powell PP. Small RNA analysis in Sindbis virus infected human HEK293 cells. PLoS One 2013; 8:e84070 [View Article][PubMed]
    [Google Scholar]
  44. Fenner BJ, Goh W, Kwang J. Dissection of double-stranded RNA binding protein B2 from betanodavirus. J Virol 2007; 81:5449–5459 [View Article][PubMed]
    [Google Scholar]
  45. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004; 15:185–197 [View Article][PubMed]
    [Google Scholar]
  46. Adiliaghdam F, Basavappa M, Saunders TL, Harjanto D, Prior JT et al. A requirement for Argonaute 4 in mammalian antiviral defense. Cell Rep 2020; 30:e16941690–1701 [View Article][PubMed]
    [Google Scholar]
  47. Aliyari R, Wu Q, Li H-W, Wang X-H, Li F et al. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 2008; 4:387–397 [View Article][PubMed]
    [Google Scholar]
  48. Cheloufi S, Dos Santos CO, Chong MMW, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires ago catalysis. Nature 2010; 465:584–U576 [View Article][PubMed]
    [Google Scholar]
  49. Zhang R, Han P, Yang H, Ouyang K, Lee D et al. In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 2013; 498:497–+ [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001552
Loading
/content/journal/jgv/10.1099/jgv.0.001552
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error