Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9255-9265

  Grangeon, Romain ^a   Agbeci, Maxime ^a   Chen, Jun ^b   Grondin, Gilles ^c   Zheng, Huanquan ^b   Laliberté, Jean Frančois ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COATOMER PROTEIN; COPII COATOMER; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN 6K2;

ARTICLE; CELL STRUCTURE; CHLOROPLAST; CONTROLLED STUDY; CYTOPLASM VESICLE; ENDOPLASMIC RETICULUM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GOLGI COMPLEX; MOLECULAR CLONING; NICOTIANA BENTHAMIANA; NONHUMAN; PERINUCLEAR GLOBULAR STRUCTURE; PLANT CELL; PRIORITY JOURNAL; PROTEIN SECRETION; SECRETORY PATHWAY; TURNIP MOSAIC VIRUS INFECTION; VIRAL PLANT DISEASE; VIRUS CELL INTERACTION; VIRUS ENVELOPE;

ENDOPLASMIC RETICULUM; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; PLANT PROTEINS; POTYVIRUS; PROTEIN TRANSPORT; SECRETORY PATHWAY; TOBACCO;

TURNIP MOSAIC VIRUS;

EID: 84866152585     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01146-12     Document Type: Article

References (62)

1. Amari K, Lerich A, Schmitt-Keichinger C, Dolja VV, Ritzenthaler C. 2011. Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog. 7:e1002327. doi:10.1371/journal.ppat.1002327.
2. Bamunusinghe D, et al. 2009. Analysis of potato virus X replicase and TGBp3 subcellular locations. Virology. 393:272-285.
3. Bamunusinghe D, Seo J-K, Rao ALN. 2011. Subcellular localization and rearrangement of endoplasmic reticulum by brome mosaic virus capsid protein. J. Virol. 85:2953-2963.
4. Batoko H, Zheng HQ, Hawes C, Moore I. 2000. A rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell. 12:2201-2218.
5. Beauchemin C, Boutet N, Laliberté J-F. 2007. Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor iso 4E in planta. J. Virol. 81:775-782.
6. Belov GA, et al. 2007. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 81:558-567.
7. 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. doi:10.1371/journal.ppat.1000216.
8. Belov GA, et al. 2012. Complex dynamic development of poliovirus membranous replication complexes. J. Virol. 86:302-312.
9. Boevink P, et al. 1998. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15:441-447.
10. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. (Oxford). 224:213-232.
11. Carette JE, Stuiver M, Van Lent J, Wellink J, Van Kammen AB. 2000. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J. Virol. 74:6556-6563.
12. Chen J, Stefano G, Brandizzi F, Zheng H. 2011. Arabidopsis RHD3 mediates the generation of the tubular ER network and is required for Golgi distribution and motility in plant cells. J. Cell Sci. 124:2241-2252.
13. Choe SS, Dodd DA, Kirkegaard K. 2005. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virolo. 337:18-29.
14. Cornell CT, Kiosses WB, Harkins S, Whitton JL. 2006. Inhibition of protein trafficking by coxsackievirus b3: multiple viral proteins target a single organelle. J. Virol. 80:6637-6647.
15. Cotton S, et al. 2009. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 83:10460-10471.
16. den Boon JA, Ahlquist P. 2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241-256.
17. Dufresne PJ, et al. 2008. Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology. 374:217-227.
18. Faso C, et al. 2009. A missense mutation in the Arabidopsis COPII coat protein Sec24A induces the formation of clusters of the endoplasmic reticulum and Golgi apparatus. Plant Cell. 21:3655-3671.
19. Fu CY, Johnson JE. 2011. Viral life cycles captured in three-dimensions with electron microscopy tomography. Curr. Opin. Virol. 1:125-133.
20. Harries PA, et al. 2009. Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc. Natl. Acad. Sci. U. S. A. 106:17594-17599.
21. Harries PA, Schoelz JE, Nelson RS. 2010. Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol. Plant Microbe Interact. 23:1381-1393.
22. Haupt S, et al. 2005. Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell. 17:164-181.
23. Hayat MA. 1981. Fixation for electron microscopy. Academic Press, New York, NY.
24. Hsu N-Y, et al. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell. 141:799-811.
25. Huang TS, Wei T, Laliberté J-F, Wang A. 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.
26. Kawakami S, Watanabe Y, Beachy RN. 2004. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U. S. A. 101:6291-6296.
27. Knoops K, et al. 2008. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 6:e226. doi:10.1371/journal.pbio.0060226.
28. Knoops K, et al. 2010. Integrity of the early secretory pathway promotes, but is not required for, severe acute respiratory syndrome coronavirus RNA synthesis and virus-induced remodeling of endoplasmic reticulum membranes. J. Virol. 84:833-846.
29. Laliberté J-F, Sanfaçon H. 2010. Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 48:69-91.
30. Langenberg WG. 1991. Cylindrical inclusion bodies of wheat streak mosaic virus and three other potyviruses only self-assemble in mixed infections. J. Gen. Virol. 72:493-497.
31. Lee SC, Wu CH, Wang CW. 2010. Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic. 11:912-930.
32. Lee WM, Ahlquist P. 2003. Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positivestr and RNA virus RNA replication protein. J. Virol. 77:12819-12828.
33. Lerich A, Langhans M, Sturm S, Robinson DG. 2011. Is the 6 kDa tobacco etch viral protein a bona fide ERES marker? J. Exp. Bot. 62:5013-5023.
34. Limpens RW, et al. 2011. The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments. mBio 2(5):e00166 -11. doi:10.1128/mBio.00166-11.
35. Liu JZ, Blancaflor EB, Nelson RS. 2005. The tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol. 138:1853-1865.
36. Marti L, Fornaciari S, Renna L, Stefano G, Brandizzi F. 2010. COPIImediated traffic in plants. Trends Plant Sci. 15:522-528.
37. Moffat K, et al. 2007. Inhibition of the secretory pathway by foot-and mouth disease virus 2BC protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J. Virol. 81:1129-1139.
38. Nakano RT, et al. 2009. GNOM-LIKE1/ERMO1 and SEC24a/ERMO2 are required for maintenance of endoplasmic reticulum morphology in Arabidopsis thaliana. Plant Cell. 21:3672-3685.
39. Nebenfuhr A, et al. 1999. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121:1127-1142.
40. Nebenfuhr A, Ritzenthaler C, Robinson DG. 2002. Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130:1102-1108.
41. Nelson BK, Cai X, Nebenfuhr A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51:1126-1136.
42. Netherton CL, Wileman T. 2011. Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr. Opin. Virol. 1:381-387.
43. Phillipson BA, et al. 2001. Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell. 13:2005-2020.
44. Ritzenthaler C. 2011. Parallels and distinctions in the direct cell-to-cell spread of the plant and animal viruses. Curr. Opin. Virol. 1:403-409.
45. Ritzenthaler C, et al. 2002. Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76:8808-8819.
46. Runions J, Brach T, Kuhner S, Hawes C. 2006. Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J. Exp. Bot. 57:43-50.
47. Saint-Jore CM, et al. 2002. Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29:661-678.
48. Schaad MC, Jensen PE, Carrington JC. 1997. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 16:4049-4059.
49. Schepetilnikov MV, et al. 2008. Intracellular targeting of a hordeiviral membrane-spanning movement protein: sequence requirements and involvement of an unconventional mechanism. J. Virol. 82:1284-1293.
50. Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. 2010. Inhibition of cellular protein secretion by Norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 5: e13130. doi:10.1371/journal.pone.0013130.
51. Sparkes IA, Ketelaar T, De Ruijter NCA, Hawes C. 2009. Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic. 10:567-571.
52. 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.
53. Thivierge K, et al. 2008. Eukaryotic elongation factor 1A interacts with Turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology. 377:216-225.
54. Tilsner J, et al. 2012. The TGB1 movement protein of potato virus X reorganizes actin and endomembranes into the X-Body, a viral replication factory. Plant Physiol. 158:1359-1370.
55. Verchot J. 2011. Wrapping membranes around plant virus infection. Curr. Opin. Virol. 1:388-395.
56. Wei T, et al. 2010. Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 84:799-809.
57. Wei T, Wang A. 2008. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI-and COPII-dependent manner. J. Virol. 82:12252-12264.
58. Welsch S, et al. 2009. Composition and three-dimensional architecture of the Dengue virus replication and assembly sites. Cell Host Microbe. 5:365-375.
59. Wessels E, et al. 2006. A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1. Dev. Cell. 11:191-201.
60. Wolk B, Buchele B, Moradpour D, Rice CM. 2008. A dynamic view of hepatitis C virus replication complexes. J. Virol. 82:10519-10531.
61. Zheng H, et al. 2005. A Rab-E GTPase mutant acts downstream of the Rab-D subclass in biosynthetic membrane traffic to the plasma membrane in tobacco leaf epidermis. Plant Cell. 17:2020-2036.
62. Zheng H, Kunst L, Hawes C, Moore I. 2004. A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J. 37:398-414.