The Expanding Functions of Cellular Helicases: The Tombusvirus RNA Replication Enhancer Co-opts the Plant eIF4AIII-Like AtRH2 and the DDX5-Like AtRH5 DEAD-Box RNA Helicases to Promote Viral Asymmetric RNA Replication

English version České info

Genome-wide screens for host factors affecting tombusvirus replication in yeast indicated that subverted cellular RNA helicases likely play major roles in virus replication. Tombusviruses do not code for their own helicases and they might recruit host RNA helicases to aid their replication in infected cells. Accordingly, in this paper, the authors show that the yeast eIF4AIII-like Fal1p and Dbp3p and the orthologous plant AtRH2 and AtRH5 DEAD-box helicases are co-opted by Tomato bushy stunt virus (TBSV) to aid viral replication. The authors find that eIF4AIII-like helicases bind to the replication enhancer element (REN) in the viral (−)RNA and they promote (+)-strand TBSV RNA synthesis in vitro. Data show that eIF4AIII-like helicases are present in the viral replicase complex and they bind to the replication proteins. In addition, the authors show synergistic effect between eIF4AIII-like helicases and the previously identified DDX3-like Ded1p/AtRH20 DEAD box helicases, which bind to a different cis-acting region in the viral (−)RNA, on stimulation of plus-strand synthesis. In summary, the authors find that two different groups of cellular helicases promote TBSV replication via selectively enhancing (+)-strand synthesis through different mechanisms.

Vyšlo v časopise: The Expanding Functions of Cellular Helicases: The Tombusvirus RNA Replication Enhancer Co-opts the Plant eIF4AIII-Like AtRH2 and the DDX5-Like AtRH5 DEAD-Box RNA Helicases to Promote Viral Asymmetric RNA Replication. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004051
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004051

Souhrn

Zdroje

1. NagyPD (2008) Yeast as a model host to explore plant virus-host interactions. Annu Rev Phytopathol 46 : 217–242.

2. den BoonJA, DiazA, AhlquistP (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8 : 77–85.

3. NagyPD, PoganyJ (2012) The dependence of viral RNA replication on co-opted host factors. Nature Reviews Microbiology 10 : 137–149.

4. BelovGA, van KuppeveldFJ (2012) (+)RNA viruses rewire cellular pathways to build replication organelles. Curr Opin Virol 2 : 740–747.

5. NagyPD, PoganyJ (2006) Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344 : 211–220.

6. BrintonMA (2001) Host factors involved in West Nile virus replication. Ann N Y Acad Sci 951 : 207–219.

7. ShiST, LaiMM (2005) Viral and cellular proteins involved in coronavirus replication. Curr Top Microbiol Immunol 287 : 95–131.

8. NagyPD, WangRY, PoganyJ, HafrenA, MakinenK (2011) Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411 : 374–382.

9. BartenschlagerR, CossetFL, LohmannV (2010) Hepatitis C virus replication cycle. Journal of Hepatology 53 : 583–585.

10. NovoaRR, CalderitaG, ArranzR, FontanaJ, GranzowH, et al. (2005) Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97 : 147–172.

11. de CastroIF, VolonteL, RiscoC (2013) Virus factories: biogenesis and structural design. Cell Microbiol 15 : 24–34.

12. LiZ, NagyPD (2011) Diverse roles of host RNA binding proteins in RNA virus replication. RNA Biol 8 : 305–315.

13. OgramSA, FlaneganJB (2011) Non-Templated Functions of Viral RNA in Picornavirus Replication. Curr Opin Virol 1 : 339–346.

14. PanavasT, NagyPD (2003) Yeast as a model host to study replication and recombination of defective interfering RNA of Tomato bushy stunt virus. Virology 314 : 315–325.

15. PanavieneZ, PanavasT, ServaS, NagyPD (2004) Purification of the cucumber necrosis virus replicase from yeast cells: role of coexpressed viral RNA in stimulation of replicase activity. J Virol 78 : 8254–8263.

16. PanavieneZ, PanavasT, NagyPD (2005) Role of an internal and two 3′-terminal RNA elements in assembly of tombusvirus replicase. J Virol 79 : 10608–10618.

17. PoganyJ, WhiteKA, NagyPD (2005) Specific Binding of Tombusvirus Replication Protein p33 to an Internal Replication Element in the Viral RNA Is Essential for Replication. J Virol 79 : 4859–4869.

18. NagyPD, PoganyJ (2008) Multiple roles of viral replication proteins in plant RNA virus replication. Methods Mol Biol 451 : 55–68.

19. PathakKB, PoganyJ, XuK, WhiteKA, NagyPD (2012) Defining the Roles of cis-Acting RNA Elements in Tombusvirus Replicase Assembly In Vitro. J Virol 86 : 156–171.

20. WuB, PoganyJ, NaH, NicholsonBL, NagyPD, et al. (2009) A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Pathog 5: e1000323.

21. WangRY, NagyPD (2008) Tomato bushy stunt virus Co-Opts the RNA-Binding Function of a Host Metabolic Enzyme for Viral Genomic RNA Synthesis. Cell Host Microbe 3 : 178–187.

22. WangRY, StorkJ, PoganyJ, NagyPD (2009) A temperature sensitive mutant of heat shock protein 70 reveals an essential role during the early steps of tombusvirus replication. Virology 394 : 28–38.

23. WangRY, StorkJ, NagyPD (2009) A key role for heat shock protein 70 in the localization and insertion of tombusvirus replication proteins to intracellular membranes. J Virol 83 : 3276–3287.

24. PoganyJ, StorkJ, LiZ, NagyPD (2008) In vitro assembly of the Tomato bushy stunt virus replicase requires the host Heat shock protein 70. Proc Natl Acad Sci U S A 105 : 19956–19961.

25. ServaS, NagyPD (2006) Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J Virol 80 : 2162–2169.

26. LiZ, BarajasD, PanavasT, HerbstDA, NagyPD (2008) Cdc34p Ubiquitin-Conjugating Enzyme Is a Component of the Tombusvirus Replicase Complex and Ubiquitinates p33 Replication Protein. J Virol 82 : 6911–6926.

27. LiZ, PoganyJ, TupmanS, EspositoAM, KinzyTG, et al. (2010) Translation elongation factor 1A facilitates the assembly of the tombusvirus replicase and stimulates minus-strand synthesis. PLoS Pathog 6: e1001175.

28. LiZ, PoganyJ, PanavasT, XuK, EspositoAM, et al. (2009) Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication co-factor. Virology 385 : 245–260.

29. SasvariZ, IzotovaL, KinzyTG, NagyPD (2011) Synergistic Roles of Eukaryotic Translation Elongation Factors 1Bgamma and 1A in Stimulation of Tombusvirus Minus-Strand Synthesis. PLoS Pathog 7: e1002438.

30. KovalevN, PoganyJ, NagyPD (2012) A Co-Opted DEAD-Box RNA Helicase Enhances Tombusvirus Plus-Strand Synthesis. PLoS Pathog 8: e1002537.

31. PathakKB, SasvariZ, NagyPD (2008) The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 379 : 294–305.

32. BarajasD, NagyPD (2010) Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 397 : 358–368.

33. BarajasD, JiangY, NagyPD (2009) A Unique Role for the Host ESCRT Proteins in Replication of Tomato bushy stunt virus. PLoS Pathog 5: e1000705.

34. NagyPD, PoganyJ (2010) Global genomics and proteomics approaches to identify host factors as targets to induce resistance against tomato bushy stunt virus. Adv Virus Res 76 : 123–177.

35. PanavasT, ServieneE, BrasherJ, NagyPD (2005) Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc Natl Acad Sci U S A 102 : 7326–7331.

36. JiangY, ServieneE, GalJ, PanavasT, NagyPD (2006) Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. J Virol 80 : 7394–7404.

37. NagyPD (2011) The roles of host factors in tombusvirus RNA recombination. Adv Virus Res 81 : 63–84.

38. MenduV, ChiuM, BarajasD, LiZ, NagyPD (2010) Cpr1 cyclophilin and Ess1 parvulin prolyl isomerases interact with the tombusvirus replication protein and inhibit viral replication in yeast model host. Virology 406 : 342–351.

39. LinderP (2008) mRNA export: RNP remodeling by DEAD-box proteins. Curr Biol 18: R297–299.

40. LinderP, LaskoP (2006) Bent out of shape: RNA unwinding by the DEAD-box helicase Vasa. Cell 125 : 219–221.

41. CordinO, BanroquesJ, TannerNK, LinderP (2006) The DEAD-box protein family of RNA helicases. Gene 367 : 17–37.

42. RanjiA, Boris-LawrieK (2010) RNA helicases: emerging roles in viral replication and the host innate response. RNA Biol 7 : 775–787.

43. HuangTS, WeiT, LaliberteJF, WangA (2010) A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiol 152 : 255–266.

44. UmateP, TutejaR, TutejaN (2010) Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human. Plant Mol Biol 73 : 449–465.

45. KantP, KantS, GordonM, ShakedR, BarakS (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol 145 : 814–830.

46. DalmayT, HorsefieldR, BraunsteinTH, BaulcombeDC (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20 : 2069–2078.

47. KooninEV, DoljaVV (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28 : 375–430.

48. ZunigaS, SolaI, CruzJLG, EnjuanesL (2009) Role of RNA chaperones in virus replication. Virus Research 139 : 253–266.

49. KovalevN, BarajasD, NagyPD (2012) Similar roles for yeast Dbp2 and Arabidopsis RH20 DEAD-box RNA helicases to Ded1 helicase in tombusvirus plus-strand synthesis. Virology 432 : 470–484.

50. WeaverPL, SunC, ChangTH (1997) Dbp3p, a putative RNA helicase in Saccharomyces cerevisiae, is required for efficient pre-rRNA processing predominantly at site A3. Mol Cell Biol 17 : 1354–1365.

51. GarciaI, AlbringMJ, UhlenbeckOC (2012) Duplex destabilization by four ribosomal DEAD-box proteins. Biochemistry 51 : 10109–10118.

52. AlexandrovA, ColognoriD, SteitzJA (2011) Human eIF4AIII interacts with an eIF4G-like partner, NOM1, revealing an evolutionarily conserved function outside the exon junction complex. Genes Dev 25 : 1078–1090.

53. Shah Nawaz-Ul-RehmanM, Reddisiva PrasanthK, BakerJ, NagyPD (2013) Yeast screens for host factors in positive-strand RNA virus replication based on a library of temperature-sensitive mutants. Methods 59 : 207–216.

54. Shah Nawaz-Ul-RehmanM, Martinez-OchoaN, PascalH, SasvariZ, HerbstC, et al. (2012) Proteome-wide overexpression of host proteins for identification of factors affecting tombusvirus RNA replication: an inhibitory role of protein kinase C. J Virol 86 : 9384–9395.

55. RayD, WhiteKA (2003) An internally located RNA hairpin enhances replication of Tomato bushy stunt virus RNAs. J Virol 77 : 245–257.

56. PanavasT, NagyPD (2003) The RNA replication enhancer element of tombusviruses contains two interchangeable hairpins that are functional during plus-strand synthesis. J Virol 77 : 258–269.

57. PanavasT, NagyPD (2005) Mechanism of stimulation of plus-strand synthesis by an RNA replication enhancer in a tombusvirus. J Virol 79 : 9777–9785.

58. StorkJ, KovalevN, SasvariZ, NagyPD (2011) RNA chaperone activity of the tombusviral p33 replication protein facilitates initiation of RNA synthesis by the viral RdRp in vitro. Virology 409 : 338–347.

59. PanavasT, StorkJ, NagyPD (2006) Use of double-stranded RNA templates by the tombusvirus replicase in vitro: Implications for the mechanism of plus-strand initiation. Virology 352 : 110–120.

60. PanavasT, PoganyJ, NagyPD (2002) Internal initiation by the cucumber necrosis virus RNA-dependent RNA polymerase is facilitated by promoter-like sequences. Virology 296 : 275–287.

61. ChengCP, PoganyJ, NagyPD (2002) Mechanism of DI RNA formation in tombusviruses: dissecting the requirement for primer extension by the tombusvirus RNA dependent RNA polymerase in vitro. Virology 304 : 460–473.

62. NagyPD, PoganyJ (2000) Partial purification and characterization of Cucumber necrosis virus and Tomato bushy stunt virus RNA-dependent RNA polymerases: similarities and differences in template usage between tombusvirus and carmovirus RNA-dependent RNA polymerases. Virology 276 : 279–288.

63. PoganyJ, NagyPD (2008) Authentic replication and recombination of Tomato bushy stunt virus RNA in a cell-free extract from yeast. J Virol 82 : 5967–5980.

64. MonkewichS, LinHX, FabianMR, XuW, NaH, et al. (2005) The p92 polymerase coding region contains an internal RNA element required at an early step in Tombusvirus genome replication. J Virol 79 : 4848–4858.

65. MineA, OkunoT (2012) Composition of plant virus RNA replicase complexes. Curr Opin Virol 2 : 669–675.

66. WuB, GrigullJ, OreMO, MorinS, WhiteKA (2013) Global organization of a positive-strand RNA virus genome. PLoS Pathog 9: e1003363.

67. Rodriguez-GalanO, Garcia-GomezJJ, de la CruzJ (2013) Yeast and human RNA helicases involved in ribosome biogenesis: current status and perspectives. Biochim Biophys Acta 1829 : 775–790.

68. XuR, ZhangS, LuL, CaoH, ZhengC (2013) A genome-wide analysis of the RNA helicase gene family in Solanum lycopersicum. Gene 513 : 128–140.

69. SalonenA, AholaT, KaariainenL (2005) Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285 : 139–173.

70. KaoCC, SinghP, EckerDJ (2001) De novo initiation of viral RNA-dependent RNA synthesis. Virology 287 : 251–260.

71. WangX, AhlquistP (2008) Filling a GAP(DH) in asymmetric viral RNA synthesis. Cell Host Microbe 3 : 124–125.

72. RajendranKS, NagyPD (2003) Characterization of the RNA-binding domains in the replicase proteins of tomato bushy stunt virus. J Virol 77 : 9244–9258.

73. HuangTS, NagyPD (2011) Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant-negative mutant of a host metabolic enzyme, GAPDH, in yeast and plants. J Virol

74. Yasuda-InoueM, KurokiM, AriumiY (2013) Distinct DDX DEAD-box RNA helicases cooperate to modulate the HIV-1 Rev function. Biochem Biophys Res Commun 434 : 803–808.

75. LorgeouxRP, GuoF, LiangC (2012) From promoting to inhibiting: diverse roles of helicases in HIV-1 Replication. Retrovirology 9 : 79.

76. SchroderM (2011) Viruses and the human DEAD-box helicase DDX3: inhibition or exploitation? Biochem Soc Trans 39 : 679–683.

77. NoueiryAO, ChenJ, AhlquistP (2000) A mutant allele of essential, general translation initiation factor DED1 selectively inhibits translation of a viral mRNA. Proc Natl Acad Sci U S A 97 : 12985–12990.

78. BolingerC, SharmaA, SinghD, YuL, Boris-LawrieK (2010) RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions. Nucleic Acids Res 38 : 1686–1696.

79. WatanabeY, OhtakiN, HayashiY, IkutaK, TomonagaK (2009) Autogenous translational regulation of the Borna disease virus negative control factor X from polycistronic mRNA using host RNA helicases. PLoS Pathog 5: e1000654.

80. MorohashiK, SaharaH, WatashiK, IwabataK, SunokiT, et al. (2011) Cyclosporin a associated helicase-like protein facilitates the association of hepatitis C virus RNA polymerase with its cellular cyclophilin B. PLoS One 6: e18285.

81. LawrenceP, RiederE (2009) Identification of RNA helicase A as a new host factor in the replication cycle of foot-and-mouth disease virus. J Virol 83 : 11356–11366.

82. GohPY, TanYJ, LimSP, TanYH, LimSG, et al. (2004) Cellular RNA helicase p68 relocalization and interaction with the hepatitis C virus (HCV) NS5B protein and the potential role of p68 in HCV RNA replication. J Virol 78 : 5288–5298.

83. UpadhyayA, DixitU, ManvarD, ChaturvediN, PandeyVN (2013) Affinity capture and identification of host cell factors associated with hepatitis C virus (+) strand subgenomic RNA. Mol Cell Proteomics 12 : 1539–1552.

84. Gimenez-BarconsM, Alves-RodriguesI, JungfleischJ, Van WynsberghePM, AhlquistP, et al. (2013) The cellular decapping activators LSm1, Pat1, and Dhh1 control the ratio of subgenomic to genomic Flock House virus RNAs. J Virol 87 : 6192–6200.

85. WangH, KimS, RyuWS (2009) DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. J Virol 83 : 5815–5824.

86. XuZ, HobmanTC (2012) The helicase activity of DDX56 is required for its role in assembly of infectious West Nile virus particles. Virology 433 : 226–235.

87. JongJE, ParkJ, KimS, SeoT (2010) Kaposi's sarcoma-associated herpesvirus viral protein kinase interacts with RNA helicase a and regulates host gene expression. J Microbiol 48 : 206–212.

88. YeP, LiuS, ZhuY, ChenG, GaoG (2010) DEXH-Box protein DHX30 is required for optimal function of the zinc-finger antiviral protein. Protein Cell 1 : 956–964.

89. SumpterRJr, LooYM, FoyE, LiK, YoneyamaM, et al. (2005) Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79 : 2689–2699.

90. FullamA, SchroderM (2013) DExD/H-box RNA helicases as mediators of anti-viral innate immunity and essential host factors for viral replication. Biochim Biophys Acta 1829 : 854–865.

91. LiZ, VizeacoumarFJ, BahrS, LiJ, WarringerJ, et al. (2011) Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat Biotechnol 29 : 361–367.

92. JankeC, MagieraMM, RathfelderN, TaxisC, ReberS, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21 : 947–962.

93. KovalevN, NagyPD (2013) Cyclophilin A binds to the viral RNA and replication proteins resulting in inhibition of tombusviral replicase assembly. J Virol 87(24): 13330–42.

94. BarajasD, LiZ, NagyPD (2009) The Nedd4-type Rsp5p ubiquitin ligase inhibits tombusvirus replication by regulating degradation of the p92 replication protein and decreasing the activity of the tombusvirus replicase. J Virol 83 : 11751–11764.

95. ChengCP, JaagHM, JonczykM, ServieneE, NagyPD (2007) Expression of the Arabidopsis Xrn4p 5′-3′ exoribonuclease facilitates degradation of tombusvirus RNA and promotes rapid emergence of viral variants in plants. Virology 368 : 238–248.

96. RajendranKS, PoganyJ, NagyPD (2002) Comparison of turnip crinkle virus RNA-dependent RNA polymerase preparations expressed in Escherichia coli or derived from infected plants. J Virol 76 : 1707–1717.

97. PanavasT, PoganyJ, NagyPD (2002) Analysis of minimal promoter sequences for plus-strand synthesis by the Cucumber necrosis virus RNA-dependent RNA polymerase. Virology 296 : 263–274.

98. JiangY, LiZ, NagyPD (2010) Nucleolin/Nsr1p binds to the 3′ noncoding region of the tombusvirus RNA and inhibits replication. Virology 396 : 10–20.