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Annual Review of Genetics

Volume 53, 2019

Natural Viruses of Nematodes

Abstract

has long been a laboratory model organism with no known natural pathogens. In the past ten years, however, natural viruses have been isolated from wild-caught (Orsay virus) and its relative (Santeuil virus, Le Blanc virus, and Melnik virus). All are RNA positive-sense viruses related to ; they infect intestinal cells and are horizontally transmitted. The Orsay virus capsid structure has been determined and the virus can be reconstituted by transgenesis of the host. Recent use of the Orsay virus has enabled researchers to identify evolutionarily conserved proviral and antiviral genes that function in nematodes and mammals. These pathways include endocytosis through SID-3 and WASP; a uridylyltransferase that destabilizes viral RNAs by uridylation of their 3′ end; ubiquitin protein modifications and turnover; and the RNA interference pathway, which recognizes and degrades viral RNA.

Keyword(s): Caenorhabditis elegans, Orsay virus, RNA interference, ubiquitin, uridylyltransferase, WASP
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/content/journals/10.1146/annurev-genet-112618-043756
2019-12-03
2024-04-19
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Literature Cited

  1. 1. 
    Aliyari R, Ding SW. 2009. RNA-based viral immunity initiated by the Dicer family of host immune receptors. Immunol. Rev. 227:176–88
     [Google Scholar]
  2. 2. 
    Ashe A, Bélicard T, Le Pen J, Sarkies P, Frézal L et al. 2013. A deletion polymorphism in the Caenorhabditiselegans RIG-I homolog disables viral RNA dicing and antiviral immunity. eLife 2:e00994
     [Google Scholar]
  3. 3. 
    Ashe A, Sarkies P, Le Pen J, Tanguy M, Miska EA 2015. Antiviral RNA interference against Orsay virus is neither systemic nor transgenerational in Caenorhabditiselegans. J. Virol 89:12035–46
     [Google Scholar]
  4. 4. 
    Bakowski MA, Desjardins CA, Smelkinson MG, Dunbar TA, Lopez-Moyado IF et al. 2014. Ubiquitin-mediated response to microsporidia and virus infection in C.elegans. PLOS Pathog 10:e1004200
     [Google Scholar]
  5. 5. 
    Bekal S, Domier LL, Gonfa B, McCoppin NK, Lambert KN, Bhalerao K 2014. A novel flavivirus in the soybean cyst nematode. J. Gen. Virol. 95:1272–80
     [Google Scholar]
  6. 6. 
    Bekal S, Domier LL, Niblack TL, Lambert KN 2011. Discovery and initial analysis of novel viral genomes in the soybean cyst nematode. J. Gen. Virol. 92:1870–79
     [Google Scholar]
  7. 7. 
    Bragard C, Caciagli P, Lemaire O, Lopez-Moya JJ, MacFarlane S et al. 2013. Status and prospects of plant virus control through interference with vector transmission. Annu. Rev. Phytopathol. 51:177–201
     [Google Scholar]
  8. 8. 
    Chen K, Franz CJ, Jiang H, Jiang Y, Wang D 2017. An evolutionarily conserved transcriptional response to viral infection in Caenorhabditis nematodes. BMC Genom 18:303
     [Google Scholar]
  9. 9. 
    Coffman SR, Lu J, Guo X, Zhong J, Jiang H et al. 2017. Caenorhabditiselegans RIG-I homolog mediates antiviral RNA interference downstream of Dicer-dependent biogenesis of viral small interfering RNAs. mBio 8:e00264–17
     [Google Scholar]
  10. 10. 
    Dennis S, Sheth U, Feldman JL, English KA, Priess JR 2012. C.elegans germ cells show temperature and age-dependent expression of Cer1, a Gypsy/Ty3-related retrotransposon. PLOS Pathog 8:e1002591
     [Google Scholar]
  11. 11. 
    Duchaine TF, Wohlschlegel JA, Kennedy S, Bei Y, Conte D Jr. et al. 2006. Functional proteomics reveals the biochemical niche of C.elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124:343–54
     [Google Scholar]
  12. 12. 
    Fan Y, Guo YR, Yuan W, Zhou Y, Holt MV et al. 2017. Structure of a pentameric virion-associated fiber with a potential role in Orsay virus entry to host cells. PLOS Pathog 13:e1006231
     [Google Scholar]
  13. 13. 
    Félix M-A, Ashe A, Piffaretti J, Wu G, Nuez I et al. 2011. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLOS Biol 9:e1000586
     [Google Scholar]
  14. 14. 
    Fenner BJ, Thiagarajan R, Chua HK, Kwang J 2006. Betanodavirus B2 is an RNA interference antagonist that facilitates intracellular viral RNA accumulation. J. Virol. 80:85–94
     [Google Scholar]
  15. 15. 
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditiselegans. Nature 391:806–11
     [Google Scholar]
  16. 16. 
    Franz CJ, Renshaw H, Frézal L, Jiang Y, Félix M-A, Wang D 2014. Orsay, Santeuil and Le Blanc viruses primarily infect intestinal cells in Caenorhabditis nematodes. Virology 448:255–64
     [Google Scholar]
  17. 17. 
    Franz CJ, Zhao G, Félix M-A, Wang D 2012. Complete genome sequence of Le Blanc virus, a third Caenorhabditis nematode-infecting virus. J. Virol. 86:11940
     [Google Scholar]
  18. 18. 
    Frézal L, Jung H, Tahan S, Wang D, Félix M-A 2019. Noda-like RNA viruses infecting Caenorhabditis nematodes: sympatry, diversity and reassortment. J. Virol. In press. https://doi.org/10.1128/JVI.01170-19
    [Crossref]
  19. 19. 
    Gammon DB. 2017. Caenorhabditiselegans as an emerging model for virus-host interactions. J. Virol. 91:e00509–17
     [Google Scholar]
  20. 20. 
    Gammon DB, Ishidate T, Li L, Gu W, Silverman N, Mello CC 2017. The antiviral RNA interference response provides resistance to lethal arbovirus infection and vertical transmission in Caenorhabditiselegans. Curr. Biol 27:795–806
     [Google Scholar]
  21. 21. 
    Guo X, Li WX, Lu R 2012. Silencing of host genes directed by virus-derived short interfering RNAs in Caenorhabditiselegans. J. Virol 86:11645–53
     [Google Scholar]
  22. 22. 
    Guo X, Lu R. 2013. Characterization of virus-encoded RNA interference suppressors in Caenorhabditiselegans. J. Virol 87:5414–23
     [Google Scholar]
  23. 23. 
    Guo X, Zhang R, Wang J, Ding S-W, Lu R 2013. Homologous RIG-I-like helicase proteins direct RNAi-mediated antiviral immunity in C.elegans by distinct mechanisms. PNAS 110:16085–90
     [Google Scholar]
  24. 24. 
    Guo X, Zhang R, Wang J, Lu R 2013. Antiviral RNA silencing initiated in the absence of RDE-4, a double-stranded RNA binding protein, in Caenorhabditiselegans. J. Virol 87:10721–29
     [Google Scholar]
  25. 25. 
    Guo YR, Hryc CF, Jakana J, Jiang H, Wang D et al. 2014. Crystal structure of a nematode-infecting virus. PNAS 111:12781–86
     [Google Scholar]
  26. 26. 
    Guo Z, Li Y, Ding S-W 2019. Small RNA-based antimicrobial immunity. Nat. Rev. Immunol. 19:31–44
     [Google Scholar]
  27. 27. 
    Hunter CP, Winston WM, Molodowitch C, Feinberg EH, Shih J et al. 2006. Systemic RNAi in Caenorhabditiselegans. Cold SpringHarb.. Symp. Quant. Biol 71:95–100
     [Google Scholar]
  28. 28. 
    Huo Y, Shen J, Wu H, Zhang C, Guo L et al. 2016. Widespread 3′-end uridylation in eukaryotic RNA viruses. Sci. Rep. 6:25454
     [Google Scholar]
  29. 29. 
    Jiang H, Chen K, Sandoval LE, Leung C, Wang D 2017. An evolutionarily conserved pathway essential for Orsay virus infection of Caenorhabditiselegans. mBio 8:e00940–17
     [Google Scholar]
  30. 30. 
    Jiang H, Franz CJ, Wang D 2014. Engineering recombinant Orsay virus directly in the metazoan host Caenorhabditiselegans. J. Virol 88:11774–81
     [Google Scholar]
  31. 31. 
    Jiang H, Franz CJ, Wu G, Renshaw H, Zhao G et al. 2014. Orsay virus utilizes ribosomal frameshifting to express a novel protein that is incorporated into virions. Virology 450–451:213–21
     [Google Scholar]
  32. 32. 
    Jose AM, Kim YA, Leal-Ekman S, Hunter CP 2012. Conserved tyrosine kinase promotes the import of silencing RNA into Caenorhabditiselegans cells. PNAS 109:14520–25
     [Google Scholar]
  33. 33. 
    Kim W, Underwood RS, Greenwald I, Shaye DD 2018. OrthoList 2: a new comparative genomic analysis of human and Caenorhabditiselegans genes. Genetics 210:445–61
     [Google Scholar]
  34. 34. 
    Le Pen J, Jiang H, Di Domenico T, Kneuss E, Kosalka J et al. 2018. Terminal uridylyltransferases target RNA viruses as part of the innate immune system. Nat. Struct. Mol. Biol. 25:778–86
     [Google Scholar]
  35. 35. 
    Leyva-Díaz E, Stefanakis N, Carrera I, Glenwinkel L, Wang G et al. 2017. Silencing of repetitive DNA is controlled by a member of an unusual Caenorhabditiselegans gene family. Genetics 207:529–45
     [Google Scholar]
  36. 36. 
    Li H, Li WX, Ding SW 2002. Induction and suppression of RNA silencing by an animal virus. Science 296:1319–21
     [Google Scholar]
  37. 37. 
    Liddicoat BJ, Piskol R, Chalk AM, Ramaswami G, Higuchi M et al. 2015. RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science 349:1115–20
     [Google Scholar]
  38. 38. 
    Lin J, Ye R, Thekke-Veetil T, Staton ME, Arelli PR et al. 2018. A novel picornavirus-like genome from transcriptome sequencing of sugar beet cyst nematode represents a new putative genus. J. Gen. Virol. 99:1418–24
     [Google Scholar]
  39. 39. 
    Long T, Meng F, Lu R 2018. Transgene-assisted genetic screen identifies rsd-6 and novel genes as key components of antiviral RNA interference in Caenorhabditiselegans. J. Virol 92:e00416–18
     [Google Scholar]
  40. 40. 
    Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G et al. 2005. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditiselegans. Nature 436:1040–43
     [Google Scholar]
  41. 41. 
    Lu R, Yigit E, Li W-X, Ding S-W 2009. An RIG-I-like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditiselegans. PLOS Pathog 5:e10000286
     [Google Scholar]
  42. 42. 
    Mahajan K, Mahajan NP. 2015. ACK1/TNK2 tyrosine kinase: molecular signaling and evolving role in cancers. Oncogene 34:4162–67
     [Google Scholar]
  43. 43. 
    Mannion NM, Greenwood SM, Young R, Cox S, Brindle J et al. 2014. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep 9:1482–94
     [Google Scholar]
  44. 44. 
    Mussabekova A, Daeffler L, Imler J-L 2017. Innate and intrinsic antiviral immunity in Drosophila. Cell Mol. Life Sci. 74:2039–54
     [Google Scholar]
  45. 45. 
    Paro S, Imler J-L, Meignin C 2015. Sensing viral RNAs by Dicer/RIG-I like ATPases across species. Curr. Opin. Immunol. 32:106–13
     [Google Scholar]
  46. 46. 
    Rechavi O, Minevich G, Hobert O 2011. Transgenerational inheritance of an acquired small RNA-based antiviral response in C.elegans. Cell 147:1248–56
     [Google Scholar]
  47. 47. 
    Reddy KC, Dror T, Sowa JN, Panek J, Chen K et al. 2017. An intracellular pathogen response pathway promotes proteostasis in C.elegans.Curr. Biol 27:3544–53.e5
     [Google Scholar]
  48. 48. 
    Reddy KC, Dror T, Underwood RS, Osman GA, Elder CR et al. 2019. Antagonistic paralogs control a switch between growth and pathogen resistance in C.elegans. PLOS Pathog 15:e1007528
     [Google Scholar]
  49. 49. 
    Reich DP, Tyc KM, Bass BL 2018. C.elegans ADARs antagonize silencing of cellular dsRNAs by the antiviral RNAi pathway. Genes Dev 32:271–82
     [Google Scholar]
  50. 50. 
    Ruark CL, Gardner M, Mitchum MG, Davis EL, Sit TL 2018. Novel RNA viruses within plant parasitic cyst nematodes. PLOS ONE 13:e0193881
     [Google Scholar]
  51. 51. 
    Sandoval LE, Jiang H, Wang D 2019. The dietary restriction-like gene drl-1, which encodes a putative serine/threonine kinase, is essential for Orsay virus infection in Caenorhabditiselegans. J. Virol 93:e01400–18
     [Google Scholar]
  52. 52. 
    Sarkies P, Ashe A, Le Pen J, McKie MA, Miska EA 2013. Competition between virus-derived and endogenous small RNAs regulates gene expression in Caenorhabditiselegans. Genome Res 23:1258–70
     [Google Scholar]
  53. 53. 
    Schott DH, Cureton DK, Whelan SP, Hunter CP 2005. An antiviral role for the RNA interference machinery in Caenorhabditiselegans. PNAS 102:18420–24
     [Google Scholar]
  54. 54. 
    Schulenburg H, Félix M-A. 2017. The natural biotic environment of Caenorhabditiselegans. Genetics 206:55–86
     [Google Scholar]
  55. 55. 
    Shi M, Lin XD, Tian JH, Chen LJ, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:539–43
     [Google Scholar]
  56. 56. 
    Shirayama M, Stanney W 3rd, Gu W, Seth M, Mello CC 2014. The Vasa homolog RDE-12 engages target mRNA and multiple Argonaute proteins to promote RNAi in C.elegans. . Curr. Biol 24:845–51
     [Google Scholar]
  57. 57. 
    Sijen T, Steiner FA, Thijssen KL, Plasterk RH 2007. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315:244–47
     [Google Scholar]
  58. 58. 
    Sterken MG, Snoek LB, Bosman KJ, Daamen J, Riksen JA et al. 2014. A heritable antiviral RNAi response limits Orsay virus infection in Caenorhabditiselegans N2. PLOS ONE 9:e89760
     [Google Scholar]
  59. 59. 
    Tanguy M, Veron L, Stempor P, Ahringer J, Sarkies P, Miska EA 2017. An alternative STAT signaling pathway acts in viral immunity in Caenorhabditiselegans. mBio 8:e00924–17
     [Google Scholar]
  60. 60. 
    Troemel ER, Félix M-A, Whiteman NK, Barrière A, Ausubel FM 2008. Microsporidia are natural intracellular parasites of the nematode C.elegans. PLOS Biol 6:e309
     [Google Scholar]
  61. 61. 
    Tsai HY, Chen CC, Conte D Jr., Moresco JJ, Chaves DA et al. 2015. A ribonuclease coordinates siRNA amplification and mRNA cleavage during RNAi. Cell 160:407–19
     [Google Scholar]
  62. 62. 
    Yokoyama N, Lougheed J, Miller WT 2005. Phosphorylation of WASP by the Cdc42-associated kinase ACK1: dual hydroxyamino acid specificity in a tyrosine kinase. J. Biol. Chem. 280:42219–26
     [Google Scholar]
  63. 63. 
    Yuan W, Zhou Y, Fan Y, Tao YJ, Zhong W 2018. Orsay δ protein is required for nonlytic viral egress. J. Virol. 92:e00745–18
     [Google Scholar]
  64. 64. 
    Zigackova D, Vanacova S. 2018. The role of 3′ end uridylation in RNA metabolism and cellular physiology. Philos. Trans. R. Soc. B 373:20180171
     [Google Scholar]
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Natural Viruses of Caenorhabditis Nematodes
Annual Review of Genetics 53, 313 (2019); https://doi.org/10.1146/annurev-genet-112618-043756
/content/journals/10.1146/annurev-genet-112618-043756
/content/journals/10.1146/annurev-genet-112618-043756
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