Generation of unique poliovirus RNA replication organelles

mBio

Volumn 5, Issue 2, 2014, Pages

  Richards, Alexsia L ^a   Soares Martins, Jamária A P ^a   Riddell, Geoffrey T ^a   Jackson, William T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; COAT PROTEIN COMPLEX II; DOUBLE STRANDED RNA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTEGRAL MEMBRANE PROTEIN 3A; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PROTEASOME; PROTEIN GBF1; PROTEIN SEC31; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; AUTOPHAGOSOME; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA REPLICATION; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS GENOME;

HUMANS; INTRACELLULAR MEMBRANES; ORGANELLES; POLIOVIRUS; VIRUS REPLICATION;

EID: 84899744133     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00833-13     Document Type: Article

References (63)

1. Whitton JL, Cornell CT, Feuer R. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776. http://dx.doi.org/10.1038/nrmicro1284.
2. Hope DA, Diamond SE, Kirkegaard K. 1997. Genetic dissection of interaction between poliovirus 3D polymerase and viral protein 3AB. J. Virol. 71:9490-9498.
3. Xiang W, Cuconati A, Hope D, Kirkegaard K, Wimmer E. 1998. Complete protein linkage map of poliovirus P3 proteins: interaction of polymerase 3Dpol with VPg and with genetic variants of 3AB. J. Virol. 72:6732-6741.
4. Bienz K, Egger D, Troxler M, Pasamontes L. 1990. Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region. J. Virol. 64:1156-1163.
5. Seglen PO, Gordon PB. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 79:1889-1892. http://dx.doi.org/10.1073/ pnas.79.6.1889.
6. Richards AL, Jackson WT. 2012. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog. 8:e1003046. doi: 10.1371/journal.ppat.1003046.
7. Jackson WT, Giddings TH, Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156. http://dx.doi.org/ 10.1371/journal.pbio.0030156.
8. Suhy DA, Giddings TH, Jr, Kirkegaard K. 2000. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J. Virol. 74: 8953-8965. http://dx.doi.org/10.1128/JVI.74.19.8953-8965.2000.
9. Belov GA, Nair V, Hansen BT, Hoyt FH, Fischer ER, Ehrenfeld E. 2012. Complex dynamic development of poliovirus membranous replication complexes. J. Virol. 86:302-312. http://dx.doi.org/10.1128/JVI.05937-11.
10. Rust RC, Landmann L, Gosert R, Tang BL, Hong W, Hauri HP, Egger D, Bienz K. 2001. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J. Virol. 75: 9808-9818. http://dx.doi.org/10.1128/JVI.75.20.9808-9818.2001.
11. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R. 2004. Bidirectional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20:87-123. http://dx.doi.org/10.1146/ annurev.cellbio.20.010403.105307.
12. Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzola M, Amherdt M, Schekman R. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895-907. http://dx.doi.org/10.1016/ 0092-8674(94)90138-4.
13. Aridor M, Weissman J, Bannykh S, Nuoffer C, Balch WE. 1998. Cargo selection by the COPII budding machinery during export from the ER. J. Cell Biol. 141:61-70. http://dx.doi.org/10.1083/jcb.141.1.61.
14. Salama NR, Chuang JS, Schekman RW. 1997. Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol. Biol. Cell 8:205-217. http://dx.doi.org/ 10.1091/mbc.8.2.205.
15. Tang BL, Zhang T, Low DY, Wong ET, Horstmann H, Hong W. 2000. Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport. J. Biol. Chem. 275:13597-13604. http://dx.doi.org/ 10.1074/jbc.275.18.13597.
16. Schekman R, Orci L. 1996. Coat proteins and vesicle budding. Science 271:1526-1533. http://dx.doi.org/10.1126/science.271.5255.1526.
17. Trahey M, Oh HS, Cameron CE, Hay JC. 2012. Poliovirus infection transiently increases COPII vesicle budding. J. Virol. 86:9675-9682. http://dx.doi.org/10.1128/JVI.01159-12.
18. Maynell LA, Kirkegaard K, Klymkowsky MW. 1992. Inhibition of poliovirus RNA synthesis by brefeldin A. J. Virol. 66:1985-1994.
19. Niu TK, Pfeifer AC, Lippincott-Schwartz J, Jackson CL. 2005. Dynamics of GBF1, a brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol. Biol. Cell 16:1213-1222. http://dx.doi.org/10.1091/mbc.E04-07-0599.
20. Popoff V, Adolf F, Brügger B, Wieland F. 2011. COPI budding within the Golgi stack. Cold Spring Harb. Perspect. Biol. 3:a005231. http:// dx.doi.org/10.1101/cshperspect.a005231.
21. Letourneur F, Gaynor EC, Hennecke S, Démollière C, Duden R, Emr SD, Riezman H, Cosson P. 1994. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79: 1199-1207. http://dx.doi.org/10.1016/0092-8674(94)90011-6.
22. Cosson P, Letourneur F. 1994. Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629-1631. http:// dx.doi.org/10.1126/science.8128252.
23. Elazar Z, Orci L, Ostermann J, Amherdt M, Tanigawa G, Rothman JE. 1994. ADP-ribosylation factor and coatomer couple fusion to vesicle budding. J. Cell Biol. 124:415-424. http://dx.doi.org/10.1083/jcb.124.4.415.
24. Manolea F, Claude A, Chun J, Rosas J, Melançon P. 2008. Distinct functions for Arf guanine nucleotide exchange factors at the Golgi complex: GBF1 and BIGs are required for assembly and maintenance of the Golgi stack and trans-Golgi network, respectively. Mol. Biol. Cell 19: 523-535. http://dx.doi.org/10.1091/mbc.E07-04-0394.
25. Belov GA, Fogg MH, Ehrenfeld E. 2005. Poliovirus proteins induce membrane association of GTPase ADP-ribosylation factor. J. Virol. 79: 7207-7216. http://dx.doi.org/10.1128/JVI.79.11.7207-7216.2005.
26. Belov GA, Altan-Bonnet N, Kovtunovych G, Jackson CL, Lippincott-Schwartz J, Ehrenfeld E. 2007. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 81:558-567. http://dx.doi.org/10.1128/JVI.01820-06.
27. Belov GA, Feng Q, Nikovics K, Jackson CL, Ehrenfeld E. 2008. A critical role of a cellular membrane traffic protein in poliovirus RNA replication. PLoS Pathog. 4:e1000216. http://dx.doi.org/10.1371/ journal.ppat.1000216.
28. Belov GA, Ehrenfeld E. 2007. Involvement of cellular membrane traffic proteins in poliovirus replication. Cell Cycle 6:36-38. http://dx.doi.org/ 10.4161/cc.6.1.3683.
29. De Matteis MA, Godi A. 2004. Protein-lipid interactions in membrane trafficking at the Golgi complex. Biochim. Biophys. Acta 1666:264-274. http://dx.doi.org/10.1016/j.bbamem.2004.07.002.
30. Levine TP, Munro S. 2002. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and-independent components. Curr. Biol. 12:695-704. http://dx.doi.org/10.1016/S0960-9822(02)00779-0.
31. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA. 1999. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat. Cell Biol. 1:280-287. http://dx.doi.org/10.1038/12993.
32. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799-811. http://dx.doi.org/10.1016/j.cell.2010.03.050.
33. De Matteis MA, D'Angelo G. 2007. The role of the phosphoinositides at the Golgi complex. Biochem. Soc. Symp. 74:107-116.
34. Ilnytska O, Santiana M, Hsu NY, Du WL, Chen YH, Viktorova EG, Belov G, Brinker A, Storch J, Moore C, Dixon JL, Altan-Bonnet N. 2013. Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication. Cell Host Microbe 14:281-293. http://dx.doi.org/10.1016/j.chom.2013.08.002.
35. Téoulé F, Brisac C, Pelletier I, Vidalain PO, Jégouic S, Mirabelli C, Bessaud M, Combelas N, Autret A, Tangy F, Delpeyroux F, Blondel B. 2013. The Golgi protein ACBD3, an interactor for poliovirus protein 3A, modulates poliovirus replication. J. Virol. 87:11031-11046.
36. Greninger AL, Knudsen GM, Betegon M, Burlingame AL, Derisi JL. 2012. The 3A protein from multiple picornaviruses utilizes the Golgi adaptor protein ACBD3 to recruit PI4KIIIbeta. J. Virol. 86:3605-3616. http://dx.doi.org/10.1128/JVI.06778-11.
37. Schönborn J, Oberstrass J, Breyel E, Tittgen J, Schumacher J, Lukacs N. 1991. Monoclonal antibodies to double-stranded RNA as probes of RNA structure in crude nucleic acid extracts. Nucleic Acids Res. 19:2993-3000. http://dx.doi.org/10.1093/nar/19.11.2993.
38. Agol VI, Paul AV, Wimmer E. 1999. Paradoxes of the replication of picornaviral genomes. Virus Res. 62:129-147. http://dx.doi.org/10.1016/ S0168-1702(99)00037-4.
39. Caliguiri LA, Tamm I. 1968. Action of guanidine on the replication of poliovirus RNA. Virology 35:408-417. http://dx.doi.org/10.1016/0042-6822(68)90219-5.
40. Lama J, Sanz MA, Rodríguez PL. 1995. A role for 3AB protein in poliovirus genome replication. J. Biol. Chem. 270:14430-14438. http:// dx.doi.org/10.1074/jbc.270.24.14430.
41. Strauss DM, Glustrom LW, Wuttke DS. 2003. Towards an understanding of the poliovirus replication complex: the solution structure of the soluble domain of the poliovirus 3A protein. J. Mol. Biol. 330:225-234. http://dx.doi.org/10.1016/S0022-2836(03)00577-1.
42. Xiang W, Cuconati A, Paul AV, Cao X, Wimmer E. 1995. Molecular dissection of the multifunctional poliovirus RNA-binding protein 3AB. RNA 1:892-904.
43. Tanida I. 2011. Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14:2201-2214. http://dx.doi.org/ 10.1089/ars.2010.3482.
44. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728. http://dx.doi.org/10.1093/emboj/ 19.21.5720.
45. Taylor MP, Kirkegaard K. 2007. Modification of cellular autophagy protein LC3 by poliovirus. J. Virol. 81:12543-12553. http://dx.doi.org/ 10.1128/JVI.00755-07.
46. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y. 2000. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 151:263-276. http://dx.doi.org/10.1083/jcb.151.2.263.
47. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, Balduini W, Ballabio A, Bamber BA, Bampton ET, Banhegyi G, Bartholomew CR, Bassham DC, et al. 2012. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544.
48. Chun J, Shapovalova Z, Dejgaard SY, Presley JF, Melançon P. 2008. Characterization of class I and II ADP-ribosylation factors (Arfs) in live cells: GDP-bound class II Arfs associate with the ER-Golgi intermediate compartment independently of GBF1. Mol. Biol. Cell 19:3488-3500. http://dx.doi.org/10.1091/mbc.E08-04-0373.
49. Wessels E, Duijsings D, Lanke KH, van Dooren SH, Jackson CL, Melchers WJ, van Kuppeveld FJ. 2006. Effects of picornavirus 3A proteins on protein transport and GBF1-dependent COP-I recruitment. J. Virol. 80:11852-11860. http://dx.doi.org/10.1128/JVI.01225-06.
50. Rothman JE. 1996. The protein machinery of vesicle budding and fusion. Protein Sci. 5:185-194.
51. Peter F, Plutner H, Zhu H, Kreis TE, Balch WE. 1993. Beta-COP is essential for transport of protein from the endoplasmic reticulum to the Golgi in vitro. J. Cell Biol. 122:1155-1167. http://dx.doi.org/10.1083/ jcb.122.6.1155.
52. Han YH, Moon HJ, You BR, Park WH. 2009. The effect of MG132, a proteasome inhibitor on HeLa cells in relation to cell growth, reactive oxygen species and GSH. Oncol. Rep. 22:215-221.
53. Schnellmann RG, Williams SW. 1998. Proteases in renal cell death: calpains mediate cell death produced by diverse toxicants. Ren. Fail. 20: 679-686. http://dx.doi.org/10.3109/08860229809045162.
54. Quiner CA, Jackson WT. 2010. Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A. Virology 407: 185-195. http://dx.doi.org/10.1016/j.virol.2010.08.012.
55. Bolten R, Egger D, Gosert R, Schaub G, Landmann L, Bienz K. 1998. Intracellular localization of poliovirus plus-and minus-strand RNA visualized by strand-specific fluorescent in situ hybridization. J. Virol. 72: 8578-8585.
56. Szul T, Garcia-Mata R, Brandon E, Shestopal S, Alvarez C, Sztul E. 2005. Dissection of membrane dynamics of the ARF-guanine nucleotide exchange factor GBF1. Traffic 6:374-385. http://dx.doi.org/10.1111/ j.1600-0854.2005.00282.x.
57. Presley JF, Ward TH, Pfeifer AC, Siggia ED, Phair RD, Lippincott-Schwartz J. 2002. Dissection of COPI and Arf1 dynamics in vivo and role in Golgi membrane transport. Nature 417:187-193. http://dx.doi.org/ 10.1038/417187a.
58. Alvarez C, Garcia-Mata R, Brandon E, Sztul E. 2003. COPI recruitment is modulated by a Rab1b-dependent mechanism. Mol. Biol. Cell 14: 2116-2127. http://dx.doi.org/10.1091/mbc.E02-09-0625.
59. Belov GA, Kovtunovych G, Jackson CL, Ehrenfeld E. 2010. Poliovirus replication requires the N-terminus but not the catalytic Sec7 domain of ArfGEF GBF1. Cell. Microbiol. 12:1463-1479. http://dx.doi.org/10.1111/ j.1462-5822.2010.01482.x.
60. Wong K, Meyers ddR, Cantley LC. 1997. Meyers d, Cantley LC. Subcellular locations of phosphatidylinositol 4-kinase isoforms. J. Biol. Chem. 272:13236-13241. http://dx.doi.org/10.1074/jbc.272.20.13236.
61. Fan J, Liu J, Culty M, Papadopoulos V. 2010. Acyl-coenzyme A binding domain containing 3 (ACBD3; PAP7; GCP60): an emerging signaling molecule. Prog. Lipid Res. 49:218-234.
62. Beske O, Reichelt M, Taylor MP, Kirkegaard K, Andino R. 2007. Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J. Cell Sci. 120: 3207-3218. http://dx.doi.org/10.1242/jcs.03483.
63. Hawes P, Netherton CL, Mueller M, Wileman T, Monaghan P. 2007. Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells. J. Microsc. 226:182-189. http://dx.doi.org/10.1111/ j.1365-2818.2007.01767.x.