Contribution of Host Intracellular Transport Machineries to Intercellular Movement of Turnip Mosaic Virus

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Agbeci, Maxime ^a   Grangeon, Romain ^a   Nelson, Richard S ^b   Zheng, Huanquan ^c   Laliberté, Jean François ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b PLANT BIOLOGY DIVISION   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; CONCANAMYCIN A; TYRPHOSTIN;

ARTICLE; CELL COMMUNICATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE; GENE EXPRESSION; GENE SILENCING; INFECTION RISK; INTRACELLULAR TRANSPORT; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSPORT HOST; TURNIP YELLOW MOSAIC VIRUS;

ACTIN CYTOSKELETON; ADP-RIBOSYLATION FACTOR 1; ANDROSTADIENES; ANTIFUNGAL AGENTS; ANTIVIRAL AGENTS; BIOLOGICAL TRANSPORT, ACTIVE; BREFELDIN A; ENDOCYTOSIS; ENZYME INHIBITORS; MACROLIDES; MYOSINS; PLANT PROTEINS; TOBACCO; TYMOVIRUS; TYRPHOSTINS; VIRUS REPLICATION;

EID: 84887268882     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003683     Document Type: Article

References (79)

1. Maule AJ, Benitez-Alfonso Y, Faulkner C, (2011) Plasmodesmata- membrane tunnels with attitude. Curr Opin Plant Biol 14: 683-690.
2. Niehl A, Heinlein M, (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248: 75-99.
3. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ, (2010) Plasmodesmata: gateways to local and systemic virus infection. Mol Plant Microbe Interact 23: 1403-1412.
4. Schoelz JE, Harries PA, Nelson RS, (2011) Intracellular transport of plant viruses: finding the door out of the cell. Molecular Plant 4: 813-831.
5. 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.
6. 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.
7. Chen Q, Chen H, Mao Q, Liu Q, Shimizu T, et al. (2012) Tubular structure induced by a plant virus facilitates viral spread in its vector insect. PLoS Pathog 8: e1003032.
8. Pouwels J, Kornet N, van Bers N, Guighelaar T, van Lent J, et al. (2003) Identification of distinct steps during tubule formation by the movement protein of Cowpea mosaic virus. J Gen Virol 84: 3485-3494.
9. Vanlent J, Storms M, Vandermeer F, Wellink J, Goldbach R, (1991) Tubular structures involved in movement of Cowpea mosaic-virus are also formed in infected cowpea protoplasts. J Gen Virol 72: 2615-2623.
10. Kasteel DT, Perbal MC, Boyer JC, Wellink J, Goldbach RW, et al. (1996) The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77: 2857-2864.
11. Wada M, Suetsugu N, (2004) Plant organelle positioning. Curr Opin Plant Biol 7: 626-631.
12. Brandizzi F, Wasteneys GO, (2013) Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J 75: 339-349.
13. Taylor MP, Koyuncu OO, Enquist LW, (2011) Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 9: 427-439.
14. Pena EJ, Heinlein M, (2012) RNA transport during TMV cell-to-cell movement. Front Plant Sci 3: 193.
15. Xu Y, Zhou X, (2012) Role of rice stripe virus NSvc4 in cell-to-cell movement and symptom development in Nicotiana benthamiana. Front Plant Sci 3: 269.
16. Genoves A, Navarro JA, Pallas V, (2010) The intra- and intercellular movement of Melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol Plant Microbe Interact 23: 263-272.
17. Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A, (2010) The Tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397: 56-63.
18. Harries PA, Palanichelvam K, Yu W, Schoelz JE, Nelson RS, (2009) The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149: 1005-1016.
19. Prokhnevsky AI, Peremyslov VV, Dolja VV, (2005) Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79: 14421-14428.
20. Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S, et al. (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15: 2058-2075.
21. Yuan Z, Chen H, Chen Q, Omura T, Xie L, et al. (2011) The early secretory pathway and an actin-myosin VIII motility system are required for plasmodesmatal localization of the NSvc4 protein of Rice stripe virus. Virus Res 159: 62-68.
22. Harries PA, Park JW, Sasaki N, Ballard KD, Maule AJ, 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.
23. Avisar D, Prokhnevsky AI, Dolja VV, (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82: 2836-2843.
24. Wei T, Shimizu T, Omura T, (2008) Endomembranes and myosin mediate assembly into tubules of Pns10 of Rice dwarf virus and intercellular spreading of the virus in cultured insect vector cells. Virology 372: 349-356.
25. Vogel F, Hofius D, Sonnewald U, (2007) Intracellular trafficking of Potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8: 1205-1214.
26. Andika IB, Zheng S, Tan Z, Sun L, Kondo H, et al. (2013) Endoplasmic reticulum export and vesicle formation of the movement protein of Chinese wheat mosaic virus are regulated by two transmembrane domains and depend on the secretory pathway. Virology 435: 493-503.
27. Haupt S, Cowan GH, Ziegler A, Roberts AG, Oparka KJ, et al. (2005) Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 17: 164-181.
28. Lewis JD, Lazarowitz SG, (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A 107: 2491-2496.
29. Pouwels J, Van Der Krogt GN, Van Lent J, Bisseling T, Wellink J, (2002) The cytoskeleton and the secretory pathway are not involved in targeting the cowpea mosaic virus movement protein to the cell periphery. Virology 297: 48-56.
30. Schepetilnikov MV, Solovyev AG, Gorshkova EN, Schiemann J, Prokhnevsky AI, 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.
31. Chung BY, Miller WA, Atkins JF, Firth AE, (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105: 5897-5902.
32. Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA, (2012) Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. Plos Pathogens 8: e1002639.
33. Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ, (1997) Capsid protein and helper Component-Proteinase Function as Potyvirus Cell-to-Cell Movement Proteins. Virology 237: 283-295.
34. Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC, (1994) Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13: 1482-1491.
35. Dolja VV, Haldeman-Cahill R, Montgomery AE, Vandenbosch KA, Carrington JC, (1995) Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 206: 1007-1016.
36. Carrington JC, Jensen PE, Schaad MC, (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14: 393-400.
37. Rodriguez-Cerezo E, Findlay K, Shaw JG, Lomonossoff GP, Qiu SG, et al. (1997) The coat and cylindrical inclusion proteins of a potyvirus are associated with connections between plant cells. Virology 236: 296-306.
38. Roberts IM, Wang D, Findlay K, Maule AJ, (1998) Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (Cls) show that the Cl protein acts transiently in aiding virus movement. Virology 245: 173-181.
39. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, et al. (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6: e1000962.
40. Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, 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.
41. Wei T, Huang TS, McNeil J, Laliberté J-F, Hong J, et al. (2010) Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J Virol 84: 799-809.
42. Patarroyo C, Laliberté J-F, Zheng H, (2013) Hijack it, Change it: How do Plant Viruses Utilize the Host Secretory Pathway for Efficient Viral Replication and Spread? Front Plant Sci 3: 308.
43. Tse YC, Lam SK, Jiang L, (2007) Enigmatic brefeldin a. Plant Signal Behav 2: 199-202.
44. Gendre D, Oh J, Boutte Y, Best JG, Samuels L, et al. (2011) Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation. Proc Natl Acad Sci U S A 108: 8048-8053.
45. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K, (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
46. Stefano G, Renna L, Chatre L, Hanton SL, Moreau P, et al. (2006) In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J 46: 95-110.
47. Zheng H, Camacho L, Wee E, Batoko H, Legen J, 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.
48. Grangeon R, Agbeci M, Chen J, Grondin G, Zheng H, et al. (2012) Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J Virol 86: 9255-9265.
49. Banbury DN, Oakley JD, Sessions RB, Banting G, (2003) Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. J Biol Chem 278: 12022-12028.
50. Aniento F, Robinson DG, (2005) Testing for endocytosis in plants. Protoplasma 226: 3-11.
51. Boutte Y, Frescatada-Rosa M, Men S, Chow CM, Ebine K, et al. (2010) Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J 29: 546-558.
52. Spiro DJ, Boll W, Kirchhausen T, Wessling-Resnick M, (1996) Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol Biol Cell 7: 355-367.
53. Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, et al. (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microscopy 214: 159-173.
54. Emans N, Zimmermann S, Fischer R, (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell 14: 71-86.
55. Qi X, Kaneda M, Chen J, Geitmann A, Zheng H, (2011) A specific role for Arabidopsis TRAPPII in post-Golgi trafficking that is crucial for cytokinesis and cell polarity. Plant J 68: 234-248.
56. Qi X, Zheng H, (2013) Rab-A1c GTPase defines a population of the trans-golgi network that is sensitive to endosidin1 during cytokinesis in arabidopsis. Mol Plant 6: 847-859.
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. Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, et al. (2004) AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Science 117: 6377-6389.
59. Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, et al. (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19: 1295-1312.
60. Liu J-Z, 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 Physiology 138: 1853-1865.
61. Hofmann C, Niehl A, Sambade A, Steinmetz A, Heinlein M, (2009) Inhibition of tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol 149: 1810-1823.
62. Collings DA, Lill AW, Himmelspach R, Wasteneys GO, (2006) Hypersensitivity to cytoskeletal antagonists demonstrates microtubule-microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytol 170: 275-290.
63. Wang Y-S, Yoo C-M, Blancaflor EB, (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytol 177: 525-536.
64. Eskelin K, Suntio T, Hyvarinen S, Hafren A, Makinen K, (2010) Renilla luciferase-based quantitation of Potato virus A infection initiated with Agrobacterium infiltration of N. benthamiana leaves. J Virol Methods 164: 101-110.
65. Lacorte C, Ribeiro SG, Lohuis D, Goldbach R, Prins M, (2010) Potato virus X and Tobacco mosaic virus-based vectors compatible with the Gateway cloning system. J Virol Methods 164: 7-13.
66. Lindbo JA, (2007) High-efficiency protein expression in plants from agroinfection-compatible Tobacco mosaic virus expression vectors. BMC Biotechnol 7: 52.
67. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
68. Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, 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.
69. Barajas D, Jiang Y, Nagy PD, (2009) A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5: e1000705.
70. Barajas D, Nagy PD, (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.
71. Peremyslov VV, Klocko AL, Fowler JE, Dolja VV, (2012) Arabidopsis myosin XI-K localizes to the motile endomembrane vesicles associated with F-actin. Front Plant Sci 3: 184.
72. Liu C, Nelson RS, (2013) The cell biology of Tobacco mosaic virus replication and movement. Front Plant Sci 4: 12.
73. Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K, et al. (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci U S A 107: 6894-6899.
74. Knoops K, Swett-Tapia C, van den Worm SH, Te Velthuis AJ, Koster AJ, 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.
75. Tilsner J, Oparka KJ, (2012) Missing links?- The connection between replication and movement of plant RNA viruses. Curr Opin Virol 2: 699-705.
76. Thivierge K, Cotton S, Dufresne PJ, Mathieu I, Beauchemin C, 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.
77. Nelson BK, Cai X, Nebenführ A, (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant J 51: 1126-1136.
78. Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC, (2003) Virus-induced gene silencing in plants. Methods 30: 296-303.
79. Gould B, Kramer E, (2007) Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae). Plant Methods 3: 6.