#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


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

Souhrn

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.


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.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#