Host ESCRT Proteins Are Required for Bromovirus RNA Replication Compartment Assembly and Function

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-25

  Diaz, Arturo ^a   Zhang, Jiantao ^b   Ollwerther, Abigail ^a   Wang, Xiaofeng ^b   Ahlquist, Paul ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; SNF7 PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

AGROBACTERIUM; ARTICLE; BROME MOSAIC VIRUS; BROMOVIRUS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENETIC ANALYSIS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MICROSCOPY; NICOTIANA BENTHAMIANA; NONHUMAN; NORTHERN BLOTTING; PHENOTYPE; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; RETROVIRUS; RNA ANALYSIS; RNA REPLICATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; VIRUS ASSEMBLY; VIRUS RELEASE; VIRUS REPLICATION; WESTERN BLOTTING; YEAST; CONFOCAL MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; HOST PARASITE INTERACTION; METABOLISM; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

BROME MOSAIC VIRUS; BROMOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES; TOMATO BUSHY STUNT VIRUS;

BLOTTING, NORTHERN; BLOTTING, WESTERN; BROMOVIRUS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; FLUORESCENT ANTIBODY TECHNIQUE; HOST-PARASITE INTERACTIONS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; RNA, VIRAL; VIRUS REPLICATION;

EID: 84926507804     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004742     Document Type: Article

References (82)

1. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C, Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell. 2005 Feb;97[2]:147–72. 15656780
2. den Boon JA, Diaz A, Ahlquist P, Cytoplasmic viral replication complexes. Cell Host Microbe. 2010 Jul 22;8[1]:77–85. doi: 10.1016/j.chom.2010.06.010 20638644
3. Mackenzie J, Wrapping things up about virus RNA replication. Traffic. 2005 Nov;6[11]:967–77. 16190978
4. Diaz A, Wang X, Ahlquist P, Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc Natl Acad Sci U S A. 2010 Aug 30.
5. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT, Host factors in positive-strand RNA virus genome replication. J Virol. 2003 Aug;77[15]:8181–6. 12857886
6. Panavas T, Serviene E, Brasher J, Nagy PD, Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc Natl Acad Sci U S A. 2005 May 17;102[20]:7326–31. 15883361
7. Barajas D, Jiang Y, Nagy PD, A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog. 2009 Dec;5[12]:e1000705. doi: 10.1371/journal.ppat.1000705 20041173
8. Belov GA, Ehrenfeld E, Involvement of cellular membrane traffic proteins in poliovirus replication. Cell Cycle. 2007 Jan 1;6[1]:36–8. Epub 2007/01/25. eng. 17245115
9. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell. 2010 May 28;141[5]:799–811. Epub 2010/06/01. eng. doi: 10.1016/j.cell.2010.03.050 20510927
10. Heaton NS, Randall G, Multifaceted roles for lipids in viral infection. Trends Microbiol. 2011 Jul;19[7]:368–75. Epub 2011/05/03. eng. doi: 10.1016/j.tim.2011.03.007 21530270
11. Wang X, Diaz A, Hao L, Gancarz B, den Boon JA, Ahlquist P, Intersection of the multivesicular body pathway and lipid homeostasis in RNA replication by a positive-strand RNA virus. Journal of virology. 2011 Jun;85[11]:5494–503. Epub 2011/03/25. eng. doi: 10.1128/JVI.02031-10 21430061
12. Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P, Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 2007 Sep;5[9]:e220. 17696647
13. Haller O, Kochs G, Weber F, The interferon response circuit: induction and suppression by pathogenic viruses. Virology. 2006 Jan 5;344[1]:119–30. 16364743
14. Ahlquist P, Bromovirus RNA replication and transcription. Curr Opin Genet Dev. 1992 Feb;2[1]:71–6. 1378769
15. Janda M, Ahlquist P, RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell. 1993 Mar 26;72[6]:961–70. 8458084
16. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P, Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci U S A. 2003 Dec 23;100[26]:15764–9. 14671320
17. Gancarz BL, Hao L, He Q, Newton MA, Ahlquist P, Systematic identification of novel, essential host genes affecting bromovirus RNA replication. PLoS One. 2011;6[8]:e23988. Epub 2011/09/15. eng. doi: 10.1371/journal.pone.0023988 21915247
18. Sullivan ML, Ahlquist P, A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J Virol. 1999 Apr;73[4]:2622–32. 10074107
19. Restrepo-Hartwig M, Ahlquist P, Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J Virol. 1999 Dec;73[12]:10303–9. 10559348
20. Restrepo-Hartwig MA, Ahlquist P, Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J Virol. 1996 Dec;70[12]:8908–16. 8971020
21. Krol MA, Olson NH, Tate J, Johnson JE, Baker TS, Ahlquist P, RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc Natl Acad Sci U S A. 1999 Nov 23;96[24]:13650–5. 10570127
22. Schwartz M, Chen J, Janda M, Sullivan M, den Boon J, Ahlquist P, A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell. 2002 Mar;9[3]:505–14. 11931759
23. Kim KS, An ultrastructural study of inclusions and disease development in plant cells infected by Cowpea Chlorotic Mottle virus. J Gen Virol. 1977;35:535–43.
24. Francki RIB, The Plant viruses. New York: Plenum Press; 1985.
25. Hatta T, Francki RIB, Cytopathic structures associated with tonoplasts of plant cells infected with cucumber mosaic and tomato aspermy viruses. J Gen Virol. 1981;53:343–6.
26. Hatta T, Bullivant S, Matthews RE, Fine structure of vesicles induced in chloroplasts of Chinese cabbage leaves by infection with turnip yellow mosaic virus. J Gen Virol. 1973 Jul;20[1]:37–50. 4584930
27. Prod'homme D, Le Panse S, Drugeon G, Jupin I, Detection and subcellular localization of the turnip yellow mosaic virus 66K replication protein in infected cells. Virology. 2001 Mar 1;281[1]:88–101. 11222099
28. Burgyan J, Rubino L, Russo M, The 5'-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. J Gen Virol. 1996 Aug;77 (Pt 8):1967–74. 8760449
29. Spuul P, Balistreri G, Hellstrom K, Golubtsov AV, Jokitalo E, Ahola T, Assembly of Alphavirus Replication Complexes from RNA and Protein Components in a Novel Trans-replication System in Mammalian Cells. Journal of virology. 2011 Mar 9. Epub 2011/03/11. Eng.
30. Froshauer S, Kartenbeck J, Helenius A, Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol. 1988 Dec;107(6 Pt 1):2075–86. 2904446
31. Raghow RS, Grace TD, Filshie BK, Bartley W, Dalgarno L, Ross River virus replication in cultured mosquito and mammalian cells: virus growth and correlated ultrastructural changes. J Gen Virol. 1973 Oct;21:109–22. 4357368
32. Gruenberg J, Stenmark H, The biogenesis of multivesicular endosomes. Nature reviews Molecular cell biology. 2004 Apr;5[4]:317–23. Epub 2004/04/09. eng. 15071556
33. Henne WM, Buchkovich NJ, Emr SD, The ESCRT pathway. Dev Cell. 2011 Jul 19;21[1]:77–91. Epub 2011/07/19. eng. doi: 10.1016/j.devcel.2011.05.015 21763610
34. Hurley JH, ESCRT complexes and the biogenesis of multivesicular bodies. Curr Opin Cell Biol. 2008 Feb;20[1]:4–11. Epub 2008/01/29. eng. doi: 10.1016/j.ceb.2007.12.002 18222686
35. Hurley JH, Hanson PI, Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nature reviews Molecular cell biology. 2010 Aug;11[8]:556–66. Epub 2010/07/01. eng. doi: 10.1038/nrm2937 20588296
36. Wollert T, Hurley JH, Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature. 2010 Apr 8;464(7290):864–9. Epub 2010/03/23. eng. doi: 10.1038/nature08849 20305637
37. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH, Membrane scission by the ESCRT-III complex. Nature. 2009 Mar 12;458(7235):172–7. Epub 2009/02/24. eng. doi: 10.1038/nature07836 19234443
38. Wollert T, Yang D, Ren X, Lee HH, Im YJ, Hurley JH, The ESCRT machinery at a glance. Journal of cell science. 2009 Jul 1;122(Pt 13):2163–6. Epub 2009/06/19. eng. doi: 10.1242/jcs.029884 19535731
39. Hurley JH, Emr SD, The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct. 2006;35:277–98. Epub 2006/05/13. eng. 16689637
40. Saksena S, Wahlman J, Teis D, Johnson AE, Emr SD, Functional reconstitution of ESCRT-III assembly and disassembly. Cell. 2009 Jan 9;136[1]:97–109. Epub 2009/01/13. eng. doi: 10.1016/j.cell.2008.11.013 19135892
41. Alonso YAM, Teis D, Assembly and disassembly of the ESCRT-III membrane scission complex. FEBS letters. 2011 Sep 9. Epub 2011/10/01. Eng.
42. Saksena S, Emr SD, ESCRTs and human disease. Biochem Soc Trans. 2009 Feb;37(Pt 1):167–72. Epub 2009/01/16. eng. doi: 10.1042/BST0370167 19143624
43. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, Sundquist WI, ESCRT-III protein requirements for HIV-1 budding. Cell host & microbe. 2011 Mar 17;9[3]:235–42. Epub 2011/03/15. eng.
44. Morita E, Sundquist WI, Retrovirus budding. Annual review of cell and developmental biology. 2004;20:395–425. Epub 2004/10/12. eng. 15473846
45. Bieniasz PD, The cell biology of HIV-1 virion genesis. Cell Host Microbe. 2009 Jun 18;5[6]:550–8. doi: 10.1016/j.chom.2009.05.015 19527882
46. Watanabe T, Sorensen EM, Naito A, Schott M, Kim S, Ahlquist P, Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proceedings of the National Academy of Sciences of the United States of America. 2007 Jun 12;104[24]:10205–10. Epub 2007/06/07. eng. 17551004
47. Ahlquist P, Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol. 2006 May;4[5]:371–82. 16582931
48. Barajas D, Martin IF, Pogany J, Risco C, Nagy PD, Noncanonical Role for the Host Vps4 AAA+ ATPase ESCRT Protein in the Formation of Tomato Bushy Stunt Virus Replicase. PLoS Pathog. 2014 Apr;10[4]:e1004087. doi: 10.1371/journal.ppat.1004087 24763736
49. Diaz A, Gallei A, Ahlquist P, Bromovirus RNA Replication Compartment Formation Requires Concerted Action of 1a's Self-Interacting RNA Capping and Helicase Domains. Journal of virology. 2012 Jan;86[2]:821–34. Epub 2011/11/18. eng. doi: 10.1128/JVI.05684-11 22090102
50. Liu L, Westler WM, den Boon JA, Wang X, Diaz A, Steinberg HA, et al. An Amphipathic alpha-Helix Controls Multiple Roles of Brome Mosaic Virus Protein 1a in RNA Replication Complex Assembly and Function. PLoS Pathog. 2009 Mar;5[3]:e1000351. doi: 10.1371/journal.ppat.1000351 19325881
51. Schwartz M, Chen J, Lee WM, Janda M, Ahlquist P, Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11263–8. 15280537
52. Zhang J, Diaz A, Mao L, Ahlquist P, Wang X, Host acyl coenzyme A binding protein regulates replication complex assembly and activity of a positive-strand RNA virus. Journal of virology. 2012 May;86[9]:5110–21. Epub 2012/02/22. eng. doi: 10.1128/JVI.06701-11 22345450
53. Babst M, Wendland B, Estepa EJ, Emr SD, The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. The EMBO journal. 1998 Jun 1;17[11]:2982–93. Epub 1998/06/26. eng. 9606181
54. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD, Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell. 2002 Aug;3[2]:283–9. Epub 2002/08/27. eng. 12194858
55. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD, Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell. 2002 Aug;3[2]:271–82. Epub 2002/08/27. eng. 12194857
56. Wemmer M, Azmi I, West M, Davies B, Katzmann D, Odorizzi G, Bro1 binding to Snf7 regulates ESCRT-III membrane scission activity in yeast. The Journal of cell biology. 2011 Jan 24;192[2]:295–306. Epub 2011/01/26. eng. doi: 10.1083/jcb.201007018 21263029
57. Davies BA, Azmi IF, Payne J, Shestakova A, Horazdovsky BF, Babst M, et al. Coordination of substrate binding and ATP hydrolysis in Vps4-mediated ESCRT-III disassembly. Mol Biol Cell. 2010 Oct 1;21[19]:3396–408. doi: 10.1091/mbc.E10-06-0512 20702581
58. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, et al. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev. 2005 Dec 1;19[23]:2816–26. Epub 2005/12/03. eng. 16322557
59. Mas P, Beachy RN, Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J Cell Biol. 1999 Nov 29;147[5]:945–58. 10579716
60. Harrison BD, Kubo S., Robinson D.J., Hutcheson A.M., The multiplication cycle of tobacco rattle virus in tobacco mesophyll protoplasts. Journal of General Virology. 1976;33:237–48.
61. Meng B, Lever AM, Wrapping up the bad news: HIV assembly and release. Retrovirology. 2013;10:5. Epub 2013/01/12. eng. doi: 10.1186/1742-4690-10-5 23305486
62. Teis D, Saksena S, Emr SD, SnapShot: the ESCRT machinery. Cell. 2009 Apr 3;137[1]:182–e1. Epub 2009/04/07. eng. doi: 10.1016/j.cell.2009.03.027 19345195
63. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM, Dynamics of ESCRT protein recruitment during retroviral assembly. Nat Cell Biol. 2011 Apr;13[4]:394–401. Epub 2011/03/12. eng. doi: 10.1038/ncb2207 21394083
64. Adell MA, Vogel GF, Pakdel M, Muller M, Lindner H, Hess MW, et al. Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol. 2014 Apr 7.
65. Lee WM, Ahlquist P, Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J Virol. 2003 Dec;77[23]:12819–28. 14610203
66. Nikko E, Andre B, Split-ubiquitin two-hybrid assay to analyze protein-protein interactions at the endosome: application to Saccharomyces cerevisiae Bro1 interacting with ESCRT complexes, the Doa4 ubiquitin hydrolase, and the Rsp5 ubiquitin ligase. Eukaryotic cell. 2007 Aug;6[8]:1266–77. 17513562
67. Richter CM, West M, Odorizzi G, Doa4 function in ILV budding is restricted through its interaction with the Vps20 subunit of ESCRT-III. J Cell Sci. 2013 Apr 15;126(Pt 8):1881–90. doi: 10.1242/jcs.122499 23444383
68. Amerik AY, Nowak J, Swaminathan S, Hochstrasser M, The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol Biol Cell. 2000 Oct;11[10]:3365–80. 11029042
69. Carlson LA, Briggs JA, Glass B, Riches JD, Simon MN, Johnson MC, et al. Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis. Cell host & microbe. 2008 Dec 11;4[6]:592–9. Epub 2008/12/10. eng.
70. Hanson PI, Roth R, Lin Y, Heuser JE, Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. The Journal of cell biology. 2008 Jan 28;180[2]:389–402. Epub 2008/01/23. eng. doi: 10.1083/jcb.200707031 18209100
71. Votteler J, Sundquist WI, Virus budding and the ESCRT pathway. Cell host & microbe. 2013 Sep 11;14[3]:232–41. Epub 2013/09/17. eng.
72. West M, Zurek N, Hoenger A, Voeltz GK, A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. The Journal of cell biology. 2011 Apr 18;193[2]:333–46. Epub 2011/04/20. eng. doi: 10.1083/jcb.201011039 21502358
73. Boucrot E, Pick A, Camdere G, Liska N, Evergren E, McMahon HT, et al. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell. 2012 Mar 30;149[1]:124–36. Epub 2012/04/03. eng. doi: 10.1016/j.cell.2012.01.047 22464325
74. Curtis MD, Grossniklaus U, A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 2003 Oct;133[2]:462–9. Epub 2003/10/14. eng. 14555774
75. Janda M, Ahlquist P, Brome mosaic virus RNA replication protein 1a dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc Natl Acad Sci U S A. 1998 Mar 3;95[5]:2227–32. 9482867
76. Sullivan ML, Ahlquist P, A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. Journal of virology. 1999 Apr;73[4]:2622–32. Epub 1999/03/12. eng. 10074107
77. Lindbo JA, TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 2007 Dec;145[4]:1232–40. Epub 2007/08/28. eng. 17720752
78. Liu Y, Schiff M, Dinesh-Kumar SP, Virus-induced gene silencing in tomato. Plant J. 2002 Sep;31[6]:777–86. Epub 2002/09/11. eng. 12220268
79. Bendahmane A, Querci M, Kanyuka K, Baulcombe DC, Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J. 2000 Jan;21[1]:73–81. Epub 2000/01/29. eng. 10652152
80. Wang X, Lee WM, Watanabe T, Schwartz M, Janda M, Ahlquist P, Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J Virol. 2005 Nov;79[21]:13747–58. 16227294
81. Chen J, Ahlquist P, Brome mosaic virus polymerase-like protein 2a is directed to the endoplasmic reticulum by helicase-like viral protein 1a. J Virol. 2000 May;74[9]:4310–8. 10756046
82. den Boon JA, Chen J, Ahlquist P, Identification of sequences in Brome mosaic virus replicase protein 1a that mediate association with endoplasmic reticulum membranes. J Virol. 2001 Dec;75[24]:12370–81. 11711627