The ER quality control and ER associated degradation machineries are vital for viral pathogenesis

Frontiers in Plant Science

Volumn 5, Issue MAR, 2014, Pages

  Verchot, Jeanmarie ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Chaperones; ERAD; Plant virus interactome; Ubiquitin proteasome system; Unfolded protein response; Virus host interactions; Virus membrane interactions

Indexed keywords

EID: 84901036991     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00066     Document Type: Review

References (126)

1. Acosta-Alvear, D., Zhou, Y., Blais, A., Tsikitis, M., Lents, N. H., Arias, C., et al. (2007). XBP1 controls diverse cell type-and condition-specific transcriptional regulatory networks. Mol. Cell. 27, 53-66. doi: 10.1016/j.molcel.2007.06.011
2. Ambrose, R. L., and Mackenzie, J. M. (2011). West nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion. J. Virol. 85, 2723-2732. doi: 10.1128/JVI.02050-10
3. An, Y. Q., Lin, R. M., Wang, F. T., Feng, J., Xu, Y. F., and Xu, S. C. (2011). Molecular cloning of a new wheat calreticulin gene TaCRT1 and expression analysis in plant defense responses and abiotic stress resistance. Genet. Mol. Res. 10, 3576-3585. doi: 10.4238/2011.November.10.1
4. Aranda, M. A., Escaler, M., Wang, D., and Maule, A. J. (1996). Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc. Natl. Acad. Sci. U.S.A. 93, 15289-15293. doi: 10.1073/pnas.93.26.15289
5. Ballut, L., Drucker, M., Pugniere, M., Cambon, F., Blanc, S., Roquet, F., et al. (2005). HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities. J. Gen. Virol. 86, 2595-2603. doi: 10.1099/vir.0.81107-0
6. Baluska, F., Samaj, J., Napier, R., and Volkmann, D. (1999). Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J. 19, 481-488. doi: 10.1046/j.1365-313X.1999.00530.x
7. Barajas, D., Li, Z., and Nagy, P. D. (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. doi: 10.1128/JVI.00789-09
8. Barajas, D., and Nagy, P. D. (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. doi: 10.1016/j.virol.2009.11.010
9. Baumberger, N., Tsai, C. H., Lie, M., Havecker, E., and Baulcombe, D. C. (2007). The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609-1614. doi: 10.1016/j.cub.2007.08.039
10. Bayne, E. H., Rakitina, D. V., Morozov, S. Y., and Baulcombe, D. C. (2005). Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J. 44, 471-482. doi: 10.1111/j.1365-313X.2005.02539.x
11. Belaidouni, N., Marchal, C., Benarous, R., and Besnard-Guerin, C. (2007). Involvement of the betaTrCP in the ubiquitination and stability of the HIV-1 Vpu protein. Biochem. Biophys. Res. Commun. 357, 688-693. doi: 10.1016/j.bbrc.2007.03.195
12. Boevink, P., and Oparka, K. J. (2005). Virus-host interactions during movement processes. Plant Physiol. 138, 1815-1821. doi: 10.1104/pp.105.066761
13. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., and Ziegler-Graff, V. (2007). The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615-1621. doi: 10.1016/j.cub.2007.07.061
14. Bour, S., Geleziunas, R., and Wainberg, M. A. (1995). The human immunodeficiency virus type 1 (HIV-1) CD4 receptor and its central role in promotion of HIV-1 infection. Microbiol. Rev. 59, 63-93.
15. Brandizzi, F., Hanton, S., Dasilva, L. L., Boevink, P., Evans, D., Oparka, K., et al. (2003). ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34, 269-281. doi: 10.1046/j.1365-313X.2003.01728.x
16. Camborde, L., Planchais, S., Tournier, V., Jakubiec, A., Drugeon, G., Lacassagne, E., et al. (2010). The ubiquitin-proteasome system regulates the accumulation of turnip yellow mosaic virus RNA-dependent RNA polymerase during viral infection. Plant Cell 22, 3142-3152. doi: 10.1105/tpc.109.072090
17. Carette, J. E., Stuiver, M., Van Lent, J., Wellink, J., and Van Kammen, A. (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. doi: 10.1128/JVI.74.14.6556-6563.2000
18. Castellano, M., and Martelli, G. (1984). Ultrastructure and nature of vesiculated bodies associated with isometric virus-like particles in diseased grapevines. J. Ultrastruct. Res. 89, 56-64. doi: 10.1016/S0022-5320(84)80023-4
19. Chan, S. W., and Egan, P. A. (2005). Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J. 19, 1510-1512.
20. Chen, M. H., Tian, G. W., Gafni, Y., and Citovsky, V. (2005). Effects of calreticulin on viral cell-to-cell movement. Plant Physiol. 138, 1866-1876. doi: 10.1104/pp.105.064386
21. Chenon, M., Camborde, L., Cheminant, S., and Jupin, I. (2012). A viral deubiquitylating enzyme targets viral RNA-dependent RNA polymerase and affects viral infectivity. EMBO J. 31, 741-753. doi: 10.1038/emboj.2011.424
22. Chiu, M. H., Chen, I. H., Baulcombe, D. C., and Tsai, C. H. (2010). The silencing suppressor P25 of potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 11, 641-649. doi: 10.1111/j.1364-3703.2010.00634.x
23. Christensen, A., Svensson, K., Thelin, L., Zhang, W., Tintor, N., Prins, D., et al. (2010). Higher plant calreticulins have acquired specialized functions in Arabidopsis. PLoS ONE 5:e11342. doi: 10.1371/journal.pone.0011342
24. Ciccaglione, A. R., Marcantonio, C., Tritarelli, E., Equestre, M., Vendittelli, F., Costantino, A., et al. (2007). Activation of the ER stress gene gadd153 by hepatitis C virus sensitizes cells to oxidant injury. Virus Res. 126, 128-138. doi: 10.1016/j.virusres.2007.02.006
25. Costa, R. O., Ferreiro, E., Cardoso, S. M., Oliveira, C. R., and Pereira, C. M. (2010). ER stress-mediated apoptotic pathway induced by amyloid-beta peptide requires the presence of functional mitochondria. J. Alzheimers Dis. 20, 625-636. doi: 10.3233/JAD-2010-091369
26. den Boon, J. A., Diaz, A., and Ahlquist, P. (2010). Cytoplasmic viral replication complexes. Cell Host Microbe 8, 77-85. doi: 10.1016/j.chom.2010.06.010
27. Deng, Y., Humbert, S., Liu, J. X., Srivastava, R., Rothstein, S. J., and Howell, S. H. (2011). Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 7247-7252. doi: 10.1073/pnas.1102117108
28. Diaz, A., Wang, X., and Ahlquist, P. (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. doi: 10.1073/pnas.1011105107
29. Diehl, J. A., Fuchs, S. Y., and Koumenis, C. (2011). The cell biology of the unfolded protein response. Gastroenterology 141, 38-41. doi: 10.1053/j.gastro.2011.05.018S0016
30. Drugeon, G., and Jupin, I. (2002). Stability in vitro of the 69K movement protein of turnip yellow mosaic virus is regulated by the ubiquitin-mediated proteasome pathway. J. Gen. Virol. 83, 3187-3197.
31. Dunoyer, P., Ritzenthaler, C., Hemmer, O., Michler, P., and Fritsch, C. (2002). Intracellular localization of the peanut clump virus replication complex in tobacco BY-2 protoplasts containing green fluorescent protein-labeled endoplasmic reticulum or Golgi apparatus. J. Virol. 76, 865-874. doi: 10.1128/JVI.76.2.865-874.2002
32. Estrabaud, E., De Muynck, S., and Asselah, T. (2011). Activation of unfolded protein response and autophagy during HCV infection modulates innate immune response. J. Hepatol. 55, 1150-1153. doi: 10.1016/j.jhep.2011.04.025
33. Evans, J. D., Crown, R. A., Sohn, J. A., and Seeger, C. (2011). West nile virus infection induces depletion of IFNAR1 protein levels. Viral Immunol. 24, 253-263. doi: 10.1089/vim.2010.0126
34. Fagone, P., and Jackowski, S. (2009). Membrane phospholipid synthesis and endoplasmic reticulum function. J. Lipid Res. 50, S311-S316. doi: 10.1194/jlr.R800049-JLR200
35. Fusaro, A. F., Correa, R. L., Nakasugi, K., Jackson, C., Kawchuk, L., Vaslin, M. F., et al. (2012). The enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing through AGO1 degradation. Virology 426, 178-187. doi: 10.1016/j.virol.2012.01.026
36. Garcia-Marcos, A., Pacheco, R., Martianez, J., Gonzalez-Jara, P., Diaz-Ruiz, J. R., and Tenllado, F. (2009). Transcriptional changes and oxidative stress associated with the synergistic interaction between potato virus X and potato virus Y and their relationship with symptom expression. Mol. Plant Microbe Interact. 22, 1431-1444. doi: 10.1094/MPMI-22-11-1431
37. Genoves, A., Pallas, V., and Navarro, J. A. (2011). Contribution of topology determinants of a viral movement protein to its membrane association, intracellular traffic, and viral cell-to-cell movement. J. Virol. 85, 7797-7809. doi: 10.1128/JVI.02465-10
38. Guenoune-Gelbart, D., Elbaum, M., Sagi, G., Levy, A., and Epel, B. L. (2008). Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol. Plant Microbe Interact. 21, 335-345. doi: 10.1094/MPMI-21-3-0335
39. Hericourt, F., Blanc, S., Redeker, V., and Jupin, I. (2000). Evidence for phosphorylation and ubiquitinylation of the turnip yellow mosaic virus RNA-dependent RNA polymerase domain expressed in a baculovirus-insect cell system. Biochem. J. 349, 417-425. doi: 10.1042/0264-6021:3490417
40. Iwata, Y., and Koizumi, N. (2012). Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci. 17, 720-727. doi: 10.1016/j.tplants.2012.06.014
41. Jelitto-Van Dooren, E. P., Vidal, S., and Denecke, J. (1999). Anticipating endoplasmic reticulum stress. A novel early response before pathogenesis-related gene induction. Plant Cell 11, 1935-1944. doi: 10.1105/tpc.11.10.1935
42. Jia, X. Y., He, L. H., Jing, R. L., and Li, R. Z. (2009). Calreticulin: conserved protein and diverse functions in plants. Physiol. Plant. 136, 127-138. doi: 10.1111/j.1399-3054.2009.01223.x
43. Jia, X. Y., Xu, C. Y., Jing, R. L., Li, R. Z., Mao, X. G., Wang, J. P., et al. (2008). Molecular cloning and characterization of wheat calreticulin (CRT) gene involved in drought-stressed responses. J. Exp. Bot. 59, 739-751. doi: 10.1093/jxb/erm369
44. Jin, Y., Ma, D., Dong, J., Jin, J., Li, D., Deng, C., et al. (2007). HC-Pro protein of potato virus Y can interact with three Arabidopsis 20S proteasome subunits in planta. J. Virol. 81, 12881-12888. doi: 10.1128/JVI.00913-917
45. Jockusch, H., and Wiegand, C. (2003). Misfolded plant virus proteins: elicitors and targets of ubiquitylation. FEBS Lett. 545, 229-232. doi: 10.1016/S0014-5793(03)00549-0
46. Jouan, L., Chatel-Chaix, L., Melancon, P., Rodrigue-Gervais, I. G., Raymond, V. A., Selliah, S., et al. (2012). Targeted impairment of innate antiviral responses in the liver of chronic hepatitis C patients. J. Hepatol. 56, 70-77. doi: 10.1016/j.jhep.2011.07.017
47. Ju, H. J., Ye, C. M., and Verchot-Lubicz, J. (2008). Mutational analysis of PVX TGBp3 links subcellular accumulation and protein turnover. Virology 375, 103-117. doi: 10.1016/j.virol.2008.01.030.
48. Kawakami, S., Watanabe, Y., and Beachy, R. N. (2004). Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U.S.A. 101, 6291-6296. doi: 10.1073/pnas.0401221101
49. Ke, P. Y., and Chen, S. S. (2011a). Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J. Clin. Invest. 121, 37-56. doi: 10.1172/JCI41474
50. Ke, P. Y., and Chen, S. S. (2011b). Autophagy: a novel guardian of HCV against innate immune response. Autophagy 7, 533-535. doi: 10.4161/auto.7.5.14732
51. Laporte, C., Vetter, G., Loudes, A. M., Robinson, D. G., Hillmer, S., Stussi-Garaud, C., 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. doi: 10.1105/tpc.013896
52. Li, L., Wang, L., Xiao, R., Zhu, G., Li, Y., Liu, C., et al. (2012). The invasion of tobacco mosaic virus RNA induces endoplasmic reticulum stress-related autophagy in HeLa cells. Biosci. Rep. 32, 171-186. doi: 10.1042/BSR20110069
53. Li, S., Ye, L., Yu, X., Xu, B., Li, K., Zhu, X., et al. (2009). Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 391, 257-264. doi: 10.1016/j.virol.2009.06.039
54. Li, Z., Barajas, D., Panavas, T., Herbst, D. A., and Nagy, P. D. (2008). Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J. Virol. 82, 6911-6926. doi: 10.1128/JVI.00702-08
55. Liu, L., Cui, F., Li, Q., Yin, B., Zhang, H., Lin, B., et al. (2011). The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res. 21, 957-969. doi: 10.1038/cr.2010.181
56. Liu, Y., Schiff, M., Czymmek, K., Talloczy, Z., Levine, B., and Dinesh-Kumar, S. P. (2005). Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567-577. doi: 10.1016/j.cell.2005.03.007
57. Mai, B., and Breeden, L. (1997). Xbp1, a stress-induced transcriptional repressor of the Saccharomyces cerevisiae Swi4/Mbp1 family. Mol. Cell. Biol. 17, 6491-6501.
58. Malim, M. H., and Emerman, M. (2008). HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe 3, 388-398. doi: 10.1016/j.chom.2008.04.008
59. Martelli, G. P., Adams, M. J., Kreuze, J. F., and Dolja, V. V. (2007). Family flexiviridae: a case study in virion and genome plasticity. Annu. Rev. Phytopathol. 45, 73-100. doi: 10.1146/annurev.phyto.45.062806.094401
60. Martinez-Gil, L., Johnson, A. E., and Mingarro, I. (2010). Membrane insertion and biogenesis of the turnip crinkle virus p9 movement protein. J. Virol. 84, 5520-5527. doi: 10.1128/JVI.00125-10
61. Martinez-Gil, L., Sauri, A., Vilar, M., Pallas, V., and Mingarro, I. (2007). Membrane insertion and topology of the p7B movement protein of melon necrotic spot virus (MNSV). Virology 367, 348-357. doi: 10.1016/j.virol.2007.06.006
62. Mas, P., and Beachy, R. N. (1999). 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. 147, 945-958. doi: 10.1083/jcb.147.5.945
63. Matsukawa, M., Shibata, Y., Ohtsu, M., Mizutani, A., Mori, H., Wang, P., et al. (2013). Nicotiana benthamiana calreticulin 3a is required for the ethylene-mediated production of phytoalexins and disease resistance against oomycete pathogen Phytophthora infestans. Mol. Plant Microbe Interact. 26, 880-892. doi: 10.1094/MPMI-12-12-0301-R
64. Melcher, U. (2000). The '30K' superfamily of viral movement proteins. J. Gen. Virol. 81, 257-266.
65. Meusser, B., Hirsch, C., Jarosch, E., and Sommer, T. (2005). ERAD: the long road to destruction. Nat. Cell Biol. 7, 766-772. doi: 10.1038/ncb0805-766
66. Miura, K., and Hasegawa, P. M. (2010). Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol. 20, 223-232. doi: 10.1016/j.tcb.2010.01.007
67. Moreno, A. A., Mukhtar, M. S., Blanco, F., Boatwright, J. L., Moreno, I., Jordan, M. R., et al. (2012). IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS ONE 7:e31944. doi: 10.1371/journal.pone.0031944
68. Moreno, A. A., and Orellana, A. (2011). The physiological role of the unfolded protein response in plants. Biol. Res. 44, 75-80. doi: 10.4067/S0716-97602011000100010
69. Muller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., et al. (2005). Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17, 149-163. doi: 10.1105/tpc.104.026625
70. Mutwil, M., Obro, J., Willats, W. G., and Persson, S. (2008). GeneCAT-novel webtools that combine BLAST and co-expression analyses. Nucleic Acids Res. 36, W320-W326. doi: 10.1093/nar/gkn292
71. Nagy, P. D., Wang, R. Y., Pogany, J., Hafren, A., and Makinen, K. (2011). Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411, 374-382. doi: 10.1016/j.virol.2010.12.061
72. Nekrutenko, A., and He, J. (2006). Functionality of unspliced XBP1 is required to explain evolution of overlapping reading frames. Trends Genet. 22, 645-648. doi: 10.1016/j.tig.2006.09.012
73. Netherton, C., Moffat, K., Brooks, E., and Wileman, T. (2007). A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv. Virus Res. 70, 101-182. doi: 10.1016/S0065-3527(07)70004-0
74. Niehl, A., Pena, E. J., Amari, K., and Heinlein, M. (2013). Microtubules in viral replication and transport. Plant J. 75, 290-308. doi: 10.1111/tpj.12134
75. Nomaguchi, M., Fujita, M., and Adachi, A. (2008). Role of HIV-1 Vpu protein for virus spread and pathogenesis. Microbes Infect. 10, 960-967. doi: 10.1016/j.micinf.2008.07.006
76. Noueiry, A. O., and Ahlquist, P. (2003). Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annu. Rev. Phytopathol. 41, 77-98. doi: 10.1146/annurev.phyto.41.052002.095717
77. Paradkar, P. N., Ooi, E. E., Hanson, B. J., Gubler, D. J., and Vasudevan, S. G. (2011). Unfolded protein response (UPR) gene expression during antibody-dependent enhanced infection of cultured monocytes correlates with dengue disease severity. Biosci. Rep. 31, 221-230. doi: 10.1042/BSR20100078BSR20100078
78. Parmar, V. M., and Schroder, M. (2012). Sensing endoplasmic reticulum stress. Adv. Exp. Med. Biol. 738, 153-168. doi: 10.1007/978-1-4614-1680-7_10
79. Pazhouhandeh, M., Dieterle, M., Marrocco, K., Lechner, E., Berry, B., Brault, V., et al. (2006). F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc. Natl. Acad. Sci. U.S.A. 103, 1994-1999. doi: 10.1073/pnas.0510784103
80. Pena, J., and Harris, E. (2011). Dengue virus modulates the unfolded protein response in a time-dependent manner. J. Biol. Chem. 286, 14226-14236. doi: 10.1074/jbc.M111.222703
81. Pena, J., and Harris, E. (2012). Early dengue virus protein synthesis induces extensive rearrangement of the endoplasmic reticulum independent of the UPR and SREBP-2 pathway. PLoS ONE 7:e38202. doi: 10.1371/journal.pone.0038202
82. Peremyslov, V. V., Pan, Y. W., and Dolja, V. V. (2004). Movement protein of a closterovirus is a type III integral transmembrane protein localized to the endoplasmic reticulum. J. Virol. 78, 3704-3709. doi: 10.1128/JVI.78.7.3704-3709.2004
83. Persson, S., Rosenquist, M., Svensson, K., Galvao, R., Boss, W. F., and Sommarin, M. (2003). Phylogenetic analyses and expression studies reveal two distinct groups of calreticulin isoforms in higher plants. Plant Physiol. 133, 1385-1396. doi: 10.1104/pp.103.024943
84. Reichel, C., and Beachy, R. N. (2000). Degradation of tobacco mosaic virus movement protein by the 26S proteasome. J. Virol. 74, 3330-3337. doi: 10.1128/JVI.74.7.3330-3337.2000
85. Ribeiro, D., Foresti, O., Denecke, J., Wellink, J., Goldbach, R., and Kormelink, R. J. (2008). Tomato spotted wilt virus glycoproteins induce the formation of endoplasmic reticulum-and Golgi-derived pleomorphic membrane structures in plant cells. J. Gen. Virol. 89, 1811-1818. doi: 10.1099/vir.0.2008/001164-1160
86. Richards, A. L., and Jackson, W. T. (2012). Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog. 8:e1003046. doi: 10.1371/journal.ppat.1003046
87. Richards, A. L., and Jackson, W. T. (2013). How positive-strand RNA viruses benefit from autophagosome maturation. J. Virol. 87, 9966-9972. doi: 10.1128/JVI.00460-13
88. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., et al. (2002). Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76, 8808-8819. doi: 10.1128/JVI.76.17.8808-8819.2002
89. Sahana, N., Kaur, H., Basavaraj, Tena, F., Jain, R. K., Palukaitis, P., et al. (2012). Inhibition of the host proteasome facilitates papaya ringspot virus accumulation and proteosomal catalytic activity is modulated by viral factor HcPro. PLoS ONE 7:e52546. doi: 10.1371/journal.pone.0052546
90. Sambade, A., Brandner, K., Hofmann, C., Seemanpillai, M., Mutterer, J., and Heinlein, M. (2008). Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9, 2073-2088. doi: 10.1111/j.1600-0854.2008.00824.x
91. Sauri, A., Saksena, S., Salgado, J., Johnson, A.E., and Mingarro, I. (2005). Double-spanning plant viral movement protein integration into the endoplasmic reticulum membrane is signal recognition particle-dependent, translocon-mediated, and concerted. J. Biol. Chem. 280, 25907-25912. doi: 10.1074/jbc.M412476200
92. Shen, W., Yan, P., Gao, L., Pan, X., Wu, J., and Zhou, P. (2010). Helper component-proteinase (HC-Pro) protein of papaya ringspot virus interacts with papaya calreticulin. Mol. Plant Pathol. 11, 335-346. doi: 10.1111/j.1364-3703.2009.00606.x
93. Shi, J., and Luo, H. (2012). Interplay between the cellular autophagy machinery and positive-stranded RNA viruses. Acta Biochim. Biophys. Sin. (Shanghai) 44, 375-384. doi: 10.1093/abbs/gms010
94. Shiboleth, Y. M., Haronsky, E., Leibman, D., Arazi, T., Wassenegger, M., Whitham, S. A., et al. (2007). The conserved FRNK box in HC-Pro, a plant viral suppressor of gene silencing, is required for small RNA binding and mediates symptom development. J. Virol. 81, 13135-13148. doi: 10.1128/JVI.01031-07
95. Shinohara, Y., Imajo, K., Yoneda, M., Tomeno, W., Ogawa, Y., Kirikoshi, H., et al. (2013). Unfolded protein response pathways regulate hepatitis C virus replication via modulation of autophagy. Biochem. Biophys. Res. Commun. 432, 326-332. doi: 10.1016/j.bbrc.2013.01.103
96. Sir, D., Liang, C., Chen, W. L., Jung, J. U., and Ou, J. H. (2008). Perturbation of autophagic pathway by hepatitis C virus. Autophagy 4, 830-831.
97. Slepak, T. I., Tang, M., Slepak, V. Z., and Lai, K. (2007). Involvement of endoplasmic reticulum stress in a novel classic galactosemia model. Mol. Genet. Metab. 92, 78-87. doi: 10.1016/j.ymgme.2007.06.005
98. Smalle, J., and Vierstra, R. D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590. doi: 10.1146/annurev.arplant.55.031903.141801
99. Tardif, K. D., Waris, G., and Siddiqui, A. (2005). Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol 13, 159-163. doi: 10.1016/j.tim.2005.02.004
100. Taylor, M. P., and Jackson, W. T. (2009). Viruses and arrested autophagosome development. Autophagy 5, 870-871.
101. Thelin, L., Mutwil, M., Sommarin, M., and Persson, S. (2011). Diverging functions among calreticulin isoforms in higher plants. Plant Signal. Behav. 6, 905-910. doi: 10.4161/psb.6.6.15339
102. Tilsner, J., Amari, K., and Torrance, L. (2011). Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248, 39-60. doi: 10.1007/s00709-010-0217-6
103. Tilsner, J., Cowan, G. H., Roberts, A. G., Chapman, S. N., Ziegler, A., Savenkov, E., et al. (2010). Plasmodesmal targeting and intercellular movement of potato mop-top pomovirus is mediated by a membrane anchored tyrosine-based motif on the lumenal side of the endoplasmic reticulum and the C-terminal transmembrane domain in the TGB3 movement protein. Virology 402, 41-51. doi: 10.1016/j.virol.2010.03.008
104. Turner, K. A., Sit, T. L., Callaway, A. S., Allen, N. S., and Lommel, S. A. (2004). Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 320, 276-290. doi: 10.1016/j.virol.2003.12.006
105. Urade, R. (2007). Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J. 274, 1152-1171. doi: 10.1111/j.1742-4658.2007.05664.x
106. Urade, R. (2009). The endoplasmic reticulum stress signaling pathways in plants. Biofactors 35, 326-331. doi: 10.1002/biof.45
107. Usadel, B., Obayashi, T., Mutwil, M., Giorgi, F. M., Bassel, G. W., Tanimoto, M., et al. (2009). Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ. 32, 1633-1651. doi: 10.1111/j.1365-3040.2009.02040.x
108. Verchot-Lubicz, J., Torrance, L., Solovyev, A. G., Morozov, S. Y., Jackson, A. O., and Gilmer, D. (2010). Varied movement strategies employed by triple gene block-encoding viruses. Mol. Plant Microbe Interact. 23, 1231-1247. doi: 10.1094/MPMI-04-10-0086
109. Verchot, J. (2011). Wrapping membranes around plant virus infection. Curr. Opin. Virol. 1, 388-395. doi: 10.1016/j.coviro.2011.09.009
110. Verchot, J. (2012). Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Front. Plant Sci. 3:275. doi: 10.3389/fpls.2012.00275
111. Vierstra, R. D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397. doi: 10.1038/nrm2688
112. Vilar, M., Sauri, A., Monne, M., Marcos, J. F., Von Heijne, G., Perez-Paya, E., et al. (2002). Insertion and topology of a plant viral movement protein in the endoplasmic reticulum membrane. J. Biol. Chem. 277, 23447-23452. doi: 10.1074/jbc.M202935200
113. Wahyu Indra Duwi, F., Lee, S. Y., and Lee, K. O. (2013). The unfolded protein response in plants: a fundamental adaptive cellular response to internal and external stresses. J. Proteomics 93, 356-368. doi: 10.1016/j.jprot.2013.04.023
114. Wei, T., Huang, T. S., Mcneil, J., Laliberte, J. F., Hong, J., Nelson, R. S., et al. (2010). Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 84, 799-809. doi: 10.1128/JVI.01824-09
115. Wei, T., and 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. doi: 10.1128/JVI.01329-08
116. Wright, K. M., Wood, N. T., Roberts, A. G., Chapman, S., Boevink, P., Mackenzie, K. M., et al. (2007). Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8, 21-31. doi: 10.1111/j.1600-0854.2006.00510.x
117. Wyatt, S. E., Tsou, P. L., and Robertson, D. (2002). Expression of the high capacity calcium-binding domain of calreticulin increases bioavailable calcium stores in plants. Transgenic Res. 11, 1-10. doi: 10.1023/A:1013917701701
118. Xu, C., Bailly-Maitre, B., and Reed, J. C. (2005). Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115, 2656-2664. doi: 10.1172/JCI26373
119. Yap, Y. K., Duangjit, J., and Panyim, S. (2009). N-terminal of papaya ringspot virus type-W (PRSV-W) helper component proteinase (HC-Pro) is essential for PRSV systemic infection in zucchini. Virus Genes 38, 461-467. doi: 10.1007/s11262-009-0348-z
120. Ye, C., and Verchot, J. (2011). Role of unfolded protein response in plant virus infection. Plant Signal. Behav. 6, 1212-1215. doi: 10.4161/psb.6.8.16048
121. Ye, C. M., Chen, S., Payton, M., Dickman, M. B., and Verchot, J. (2013). TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death. Mol. Plant Pathol. 14, 241-255. doi:10.1111/mpp.12000
122. Yu, C. Y., Hsu, Y. W., Liao, C. L., and Lin, Y. L. (2006). Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J. Virol. 80, 11868-11880. doi: 10.1128/JVI.00879-06
123. Yue, X., Wang, H., Zhao, F., Liu, S., Wu, J., Ren, W., et al. (2012). Hepatitis B virus-induced calreticulin protein is involved in IFN resistance. J. Immunol. 189, 279-286. doi:10.4049/jimmunol.1103405
124. Zavaliev, R., Levy, A., Gera, A., and Epel, B. L. (2013). Subcellular dynamics and role of Arabidopsis beta-1,3-glucanases in cell-to-cell movement of tobamoviruses. Mol. Plant Microbe Interact. 26, 1016-1030. doi: 10.1094/MPMI-03-13-0062-R
125. Zhao, L., and Ackerman, S. L. (2006). Endoplasmic reticulum stress in health and disease. Curr. Opin. Cell Biol. 18, 444-452. doi: 10.1016/j.ceb.2006.06.005
126. Zheng, Y., Gao, B., Ye, L., Kong, L., Jing, W., Yang, X., et al. (2005). Hepatitis C virus non-structural protein NS4B can modulate an unfolded protein response. J. Microbiol. 43, 529-536.