Noncanonical Role for the Host Vps4 AAA+ ATPase ESCRT Protein in the Formation of Replicase

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Replication of positive-stranded RNA viruses depends on recruitment of host proteins and cellular membranes to assemble the viral replicase complexes. Tombusviruses, small RNA viruses of plants, co-opt the cellular ESCRT (endosomal sorting complexes required for transport) proteins to facilitate replicase assembly on the peroxisomal membranes. The authors show a surprising role for the ESCRT-associated Vps4p AAA+ ATPase during tombusvirus replication. They show that Vps4p is recruited to and becomes a permanent member of the replicase complex through its interaction with the viral replication proteins. Also, EM and immuno-EM studies reveal that Vps4p is required for the formation of single-membrane vesicle-like structures, called spherules, which represent the sites of tombusvirus replication. The authors propose that Vps4p and other ESCRT proteins are required for membrane deformation and replicase assembly.

Vyšlo v časopise: Noncanonical Role for the Host Vps4 AAA+ ATPase ESCRT Protein in the Formation of Replicase. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004087
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004087

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Zdroje

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

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

3. HuangYW, HuCC, LinNS, HsuYH (2012) Unusual roles of host metabolic enzymes and housekeeping proteins in plant virus replication. Curr Opin Virol 2: 676–682.

4. ShullaA, RandallG (2012) Hepatitis C virus-host interactions, replication, and viral assembly. Curr Opin Virol 2: 725–732.

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

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

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

8. AhlquistP, NoueiryAO, LeeWM, KushnerDB, DyeBT (2003) Host factors in positive-strand RNA virus genome replication. J Virol 77: 8181–8186.

9. 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.

10. 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 Dev 19: 445–452.

11. 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.

12. KushnerDB, LindenbachBD, GrdzelishviliVZ, NoueiryAO, PaulSM, et al. (2003) Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci U S A 100: 15764–15769.

13. NoueiryAO, AhlquistP (2003) Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annu Rev Phytopathol 41: 77–98.

14. KrishnanMN, NgA, SukumaranB, GilfoyFD, UchilPD, et al. (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455: 242–245.

15. BarajasD, JiangY, NagyPD (2009) A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5: e1000705.

16. DiazA, WangX, AhlquistP (2010) Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc Natl Acad Sci U S A 107: 16291–16296.

17. NeuvonenM, KazlauskasA, MartikainenM, HinkkanenA, AholaT, et al. (2011) SH3 domain-mediated recruitment of host cell amphiphysins by alphavirus nsP3 promotes viral RNA replication. PLoS Pathog 7: e1002383.

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

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

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

21. WhiteKA, NagyPD (2004) Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog Nucleic Acid Res Mol Biol 78: 187–226.

22. 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.

23. 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.

24. ServieneE, ShapkaN, ChengCP, PanavasT, PhuangratB, et al. (2005) Genome-wide screen identifies host genes affecting viral RNA recombination. Proc Natl Acad Sci U S A 102: 10545–10550.

25. ServieneE, JiangY, ChengCP, BakerJ, NagyPD (2006) Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J Virol 80: 1231–1241.

26. 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.

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

28. 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.

29. 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.

30. 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.

31. 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.

32. 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.

33. 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.

34. PoganyJ, NagyPD (2012) p33-Independent Activation of a Truncated p92 RNA-Dependent RNA Polymerase of Tomato Bushy Stunt Virus in Yeast Cell-Free Extract. J Virol 86: 12025–12038.

35. SharmaM, SasvariZ, NagyPD (2011) Inhibition of phospholipid biosynthesis decreases the activity of the tombusvirus replicase and alters the subcellular localization of replication proteins. Virology 415: 141–152.

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

37. SharmaM, SasvariZ, NagyPD (2010) Inhibition of sterol biosynthesis reduces tombusvirus replication in yeast and plants. J Virol 84: 2270–2281.

38. 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.

39. 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.

40. 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.

41. 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.

42. 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.

43. JonczykM, PathakKB, SharmaM, NagyPD (2007) Exploiting alternative subcellular location for replication: tombusvirus replication switches to the endoplasmic reticulum in the absence of peroxisomes. Virology 362: 320–330.

44. 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.

45. PanavasT, HawkinsCM, PanavieneZ, NagyPD (2005) The role of the p33:p33/p92 interaction domain in RNA replication and intracellular localization of p33 and p92 proteins of Cucumber necrosis tombusvirus. Virology 338: 81–95.

46. NagyPD, BarajasD, PoganyJ (2012) Host factors with regulatory roles in tombusvirus replication. Curr Opin Virol 2: 685–692.

47. 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.

48. McCartneyAW, GreenwoodJS, FabianMR, WhiteKA, MullenRT (2005) Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 17: 3513–3531.

49. 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.

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

51. MoritaE, SundquistWI (2004) Retrovirus budding. Annu Rev Cell Dev Biol 20: 395–425.

52. PerlmanM, ReshMD (2006) Identification of an intracellular trafficking and assembly pathway for HIV-1 gag. Traffic 7: 731–745.

53. SlagsvoldT, PattniK, MalerodL, StenmarkH (2006) Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol 16: 317–326.

54. HurleyJH, EmrSD (2006) The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 35: 277–298.

55. KatzmannDJ, OdorizziG, EmrSD (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3: 893–905.

56. BowersK, StevensTH (2005) Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1744: 438–454.

57. HurleyJH, BouraE, CarlsonLA, RozyckiB (2010) Membrane budding. Cell 143: 875–887.

58. WollertT, HurleyJH (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464: 864–869.

59. HurleyJH, HansonPI (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol 11: 556–566.

60. WollertT, YangD, RenX, LeeHH, ImYJ, et al. (2009) The ESCRT machinery at a glance. J Cell Sci 122: 2163–2166.

61. WollertT, WunderC, Lippincott-SchwartzJ, HurleyJH (2009) Membrane scission by the ESCRT-III complex. Nature 458: 172–177.

62. YangD, HurleyJH (2010) Structural role of the Vps4-Vta1 interface in ESCRT-III recycling. Structure 18: 976–984.

63. 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.

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

65. FontanaJ, TzengWP, CalderitaG, Fraile-RamosA, FreyTK, et al. (2007) Novel replication complex architecture in rubella replicon-transfected cells. Cell Microbiol 9: 875–890.

66. RiscoC, Sanmartin-ConesaE, TzengWP, FreyTK, SeyboldV, et al. (2012) Specific, sensitive, high-resolution detection of protein molecules in eukaryotic cells using metal-tagging transmission electron microscopy. Structure 20: 759–766.

67. 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.

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

69. FontanaJ, Lopez-MonteroN, ElliottRM, FernandezJJ, RiscoC (2008) The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell Microbiol 10: 2012–2028.

70. RiscoC, RodriguezJR, Lopez-IglesiasC, CarrascosaJL, EstebanM, et al. (2002) Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76: 1839–1855.

71. DiestraE, FontanaJ, GuichardP, MarcoS, RiscoC (2009) Visualization of proteins in intact cells with a clonable tag for electron microscopy. J Struct Biol 165: 157–168.