Is Required for High Efficiency Viral Replication

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Viruses often can highly efficiently utilize the host system to make huge amounts of viral proteins for their replication; however, which host factors are needed by the viruses are largely unknown. We analyzed about one hundred Drosophila mutants and found that the pelo mutation in Drosophila inhibited Drosophila C virus (DCV) replication. We found pelo is specifically required for high efficiency synthesis of proteins of a number of viruses, suggesting that inhibition of pelo may mediate a general antiviral activity. We proposed that the function of pelo in quality control of protein synthesis is required for high efficiency viral protein synthesis. Our study presented here identifies a new host factor, pelo, that is specifically required for effective viral replication and it may be a new potential therapeutic target for broad-spectrum antiviral therapy.

Vyšlo v časopise: Is Required for High Efficiency Viral Replication. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004034
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004034

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Zdroje

1. OldstoneMB (1996) Principles of viral pathogenesis. Cell 87: 799–801.

2. BeutlerB, EidenschenkC, CrozatK, ImlerJL, TakeuchiO, et al. (2007) Genetic analysis of resistance to viral infection. Nature reviews Immunology 7: 753–766.

3. PichlmairA, Reis e SousaC (2007) Innate recognition of viruses. Immunity 27: 370–383.

4. YanN, ChenZJ (2012) Intrinsic antiviral immunity. Nature immunology 13: 214–222.

5. LemaitreB, HoffmannJ (2007) The host defense of Drosophila melanogaster. Annual review of immunology 25: 697–743.

6. FerrandonD, ImlerJL, HetruC, HoffmannJA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nature reviews Immunology 7: 862–874.

7. KempC, ImlerJL (2009) Antiviral immunity in drosophila. Current opinion in immunology 21: 3–9.

8. SabinLR, HannaSL, CherryS (2010) Innate antiviral immunity in Drosophila. Current opinion in immunology 22: 4–9.

9. WangXH, AliyariR, LiWX, LiHW, KimK, et al. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452–454.

10. SalehMC, TassettoM, van RijRP, GoicB, GaussonV, et al. (2009) Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458: 346–350.

11. DingSW, VoinnetO (2007) Antiviral immunity directed by small RNAs. Cell 130: 413–426.

12. LiH, LiWX, DingSW (2002) Induction and suppression of RNA silencing by an animal virus. Science 296: 1319–1321.

13. van RijRP, SalehMC, BerryB, FooC, HoukA, et al. (2006) The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes & development 20: 2985–2995.

14. NayakA, BerryB, TassettoM, KunitomiM, AcevedoA, et al. (2010) Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nature structural & molecular biology 17: 547–554.

15. DostertC, JouanguyE, IrvingP, TroxlerL, Galiana-ArnouxD, et al. (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nature immunology 6: 946–953.

16. DeddoucheS, MattN, BuddA, MuellerS, KempC, et al. (2008) The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nature immunology 9: 1425–1432.

17. ZambonRA, NandakumarM, VakhariaVN, WuLP (2005) The Toll pathway is important for an antiviral response in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 102: 7257–7262.

18. CostaA, JanE, SarnowP, SchneiderD (2009) The Imd pathway is involved in antiviral immune responses in Drosophila. PloS one 4: e7436.

19. ShellyS, LukinovaN, BambinaS, BermanA, CherryS (2009) Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 30: 588–598.

20. NakamotoM, MoyRH, XuJ, BambinaS, YasunagaA, et al. (2012) Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity 36: 658–667.

21. PirieNW (1946) The viruses. Annual review of biochemistry 15: 573–592.

22. CherryS, PerrimonN (2004) Entry is a rate-limiting step for viral infection in a Drosophila melanogaster model of pathogenesis. Nature immunology 5: 81–87.

23. CherryS, DoukasT, ArmknechtS, WhelanS, WangH, et al. (2005) Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes & development 19: 445–452.

24. CherryS, KunteA, WangH, CoyneC, RawsonRB, et al. (2006) COPI activity coupled with fatty acid biosynthesis is required for viral replication. PLoS pathogens 2: e102.

25. BushellM, SarnowP (2002) Hijacking the translation apparatus by RNA viruses. The Journal of cell biology 158: 395–399.

26. DeverTE, GreenR (2012) The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harbor perspectives in biology 4: a013706.

27. ShoemakerCJ, EylerDE, GreenR (2010) Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330: 369–372.

28. van den ElzenAM, HenriJ, LazarN, GasME, DurandD, et al. (2010) Dissection of Dom34-Hbs1 reveals independent functions in two RNA quality control pathways. Nature structural & molecular biology 17: 1446–1452.

29. DomaMK, ParkerR (2006) Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440: 561–564.

30. KurohaK, AkamatsuM, DimitrovaL, ItoT, KatoY, et al. (2010) Receptor for activated C kinase 1 stimulates nascent polypeptide-dependent translation arrest. EMBO reports 11: 956–961.

31. TsuboiT, KurohaK, KudoK, MakinoS, InoueE, et al. (2012) Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Molecular cell 46: 518–529.

32. PisarevaVP, SkabkinMA, HellenCU, PestovaTV, PisarevAV (2011) Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes. The EMBO journal 30: 1804–1817.

33. IzawaT, TsuboiT, KurohaK, InadaT, NishikawaS, et al. (2012) Roles of dom34:hbs1 in nonstop protein clearance from translocators for normal organelle protein influx. Cell reports 2: 447–453.

34. LeeHH, KimYS, KimKH, HeoI, KimSK, et al. (2007) Structural and functional insights into Dom34, a key component of no-go mRNA decay. Molecular cell 27: 938–950.

35. GrailleM, ChailletM, van TilbeurghH (2008) Structure of yeast Dom34: a protein related to translation termination factor Erf1 and involved in No-Go decay. The Journal of biological chemistry 283: 7145–7154.

36. DavisL, EngebrechtJ (1998) Yeast dom34 mutants are defective in multiple developmental pathways and exhibit decreased levels of polyribosomes. Genetics 149: 45–56.

37. BhattacharyaA, McIntoshKB, WillisIM, WarnerJR (2010) Why Dom34 stimulates growth of cells with defects of 40S ribosomal subunit biosynthesis. Molecular and cellular biology 30: 5562–5571.

38. EberhartCG, WassermanSA (1995) The pelota locus encodes a protein required for meiotic cell division: an analysis of G2/M arrest in Drosophila spermatogenesis. Development 121: 3477–3486.

39. XiR, DoanC, LiuD, XieT (2005) Pelota controls self-renewal of germline stem cells by repressing a Bam-independent differentiation pathway. Development 132: 5365–5374.

40. AdhamIM, SallamMA, StedingG, KorabiowskaM, BrinckU, et al. (2003) Disruption of the pelota gene causes early embryonic lethality and defects in cell cycle progression. Molecular and cellular biology 23: 1470–1476.

41. ReavyB, MooreNF (1983) Cell-free translation of Drosophila C virus RNA: identification of a virus protease activity involved in capsid protein synthesis and further studies on in vitro processing of cricket paralysis virus specified proteins. Archives of virology 76: 101–115.

42. JoussetFX, BergoinM, RevetB (1977) Characterization of the Drosophila C virus. The Journal of general virology 34: 269–283.

43. KingLA, MooreNF (1988) Evidence for the presence of a genome-linked protein in two insect picornaviruses, cricket paralysis and DrosophilaC viruses. FEMS Microbiology Letters 50: 41–44.

44. Lautie-HarivelN, Thomas-OrillardM (1990) Location of Drosophila C virus target organs in Drosophila host population by an immunofluorescence technique. Biology of the cell/under the auspices of the European Cell Biology Organization 69: 35–39.

45. TeixeiraL, FerreiraA, AshburnerM (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS biology 6: e2.

46. Fields BN, Knipe DM, Howley PM (2007) Fields virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins.

47. JohnsonKN, ChristianPD (1999) Molecular characterization of Drosophila C virus isolates. Journal of invertebrate pathology 73: 248–254.

48. JohnsonKN, ChristianPD (1998) The novel genome organization of the insect picorna-like virus Drosophila C virus suggests this virus belongs to a previously undescribed virus family. The Journal of general virology 79(Pt 1): 191–203.

49. MasekT, ValasekL, PospisekM (2011) Polysome analysis and RNA purification from sucrose gradients. Methods in molecular biology 703: 293–309.

50. Carr-SchmidA, PfundC, CraigEA, KinzyTG (2002) Novel G-protein complex whose requirement is linked to the translational status of the cell. Molecular and cellular biology 22: 2564–2574.

51. JohanssonM, BouakazE, LovmarM, EhrenbergM (2008) The kinetics of ribosomal peptidyl transfer revisited. Molecular cell 30: 589–598.

52. KempC, MuellerS, GotoA, BarbierV, ParoS, et al. (2013) Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. Journal of immunology 190: 650–658.

53. StrunkBS, NovakMN, YoungCL, KarbsteinK (2012) A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150: 111–121.

54. BeckerT, ArmacheJP, JaraschA, AngerAM, VillaE, et al. (2011) Structure of the no-go mRNA decay complex Dom34-Hbs1 bound to a stalled 80S ribosome. Nature structural & molecular biology 18: 715–720.

55. TzouP, MeisterM, LemaitreB (2002) Methods for studying infection and immunity in Drosophila. Methods in Microbiology 31: 507–529.

56. ReedLJ, MuenchH (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27: 493–497.

57. RogersSL, RogersGC (2008) Culture of Drosophila S2 cells and their use for RNAi-mediated loss-of-function studies and immunofluorescence microscopy. Nature protocols 3: 606–611.