Amino acid substitutions in the non-structural proteins 4A or 4B modulate the induction of autophagy in West Nile virus infected cells independently of the activation of the unfolded protein response

Frontiers in Microbiology

Volumn 5, Issue DEC, 2015, Pages

  Blazquez, Ana Belen ^a   Martín Acebes, Miguel A ^a   Saiz, Juan Carlos ^a  

^a INIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVIVIRUS; WEST NILE VIRUS;

EID: 84930507293     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00797     Document Type: Article

References (43)

1. 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.
2. Ambrose, R.L., and Mackenzie, J.M. (2013). ATF6 signaling is required for efficient West Nile virus replication by promoting cell survival and inhibition of innate immune responses. J Virol 87, 2206-2214. doi: JVI.02097-12 [pii] 10.1128/JVI.02097-12.
3. Bakonyi, T., Gould, E.A., Kolodziejek, J., Weissenbock, H., and Nowotny, N. (2004). Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001: comparison with the South African strain SAAR-1776 and other flaviviruses. Virology 328, 301-310. doi: S0042-6822(04)00525-2 [pii] 10.1016/j.virol.2004.08.005.
4. Beasley, D.W., Li, L., Suderman, M.T., and Barrett, A.D. (2002). Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 296, 17-23. doi: 10.1006/viro.2002.1372 S0042682202913723 [pii].
5. Beatman, E., Oyer, R., Shives, K.D., Hedman, K., Brault, A.C., Tyler, K.L., and David Beckham, J. (2012). West Nile virus growth is independent of autophagy activation. Virology 433, 262-272. doi: S0042-6822(12)00397-2 [pii] 10.1016/j.virol.2012.08.016.
6. Blazquez, A.B., Escribano-Romero, E., Merino-Ramos, T., Saiz, J.C., and Martin-Acebes, M.A. (2013). Infection with Usutu virus induces an autophagic response in mammalian cells. PLoS Negl Trop Dis 7, e2509. doi:10.1371/journal.pntd.0002509 PNTD-D-13-00407 [pii].
7. Blazquez, A.B., Escribano-Romero, E., Merino-Ramos, T., Saiz, J.C., and Martin-Acebes, M.A. (2014). Stress responses in flavivirus-infected cells: activation of unfolded protein response and autophagy. Front Microbiol 5, 266.
8. Blazquez, A.B., and Saiz, J.C. (2010). West Nile virus (WNV) transmission routes in the murine model: intrauterine, by breastfeeding and after cannibal ingestion. Virus Res 151, 240-243.
9. Boyce, M., Bryant, K.F., Jousse, C., Long, K., Harding, H.P., Scheuner, D., Kaufman, R.J., Ma, D., Coen, D.M., Ron, D., and Yuan, J. (2005). A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307, 935-939. doi: 307/5711/935 [pii] 10.1126/science.1101902.
10. Cao, S.S., and Kaufman, R.J. (2013). Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 17, 437-448. doi:10.1517/14728222.2013.756471.
11. Fraser, J.E., Watanabe, S., Wang, C., Chan, W.K., Maher, B., Lopez-Denman, A., Hick, C., Wagstaff, K.M., Mackenzie, J.M., Sexton, P.M., Vasudevan, S.G., and Jans, D.A. (2014). A Nuclear Transport Inhibitor That Modulates the Unfolded Protein Response and Provides In Vivo Protection Against Lethal Dengue virus Infection. J Infect Dis. doi: jiu319 [pii] 10.1093/infdis/jiu319.
12. Gillespie, L.K., Hoenen, A., Morgan, G., and Mackenzie, J.M. (2010). The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J Virol 84, 10438-10447.
13. Green, A.M., Beatty, P.R., Hadjilaou, A., and Harris, E. (2014). Innate immunity to dengue virus infection and subversion of antiviral responses. J Mol Biol 426, 1148-1160. doi: S0022-2836(13)00734-1 [pii] 10.1016/j.jmb.2013.11.023.
14. Hayes, E.B., and Gubler, D.J. (2006). West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu Rev Med 57, 181-194.
15. Hetz, C. (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13, 89-102. doi: nrm3270 [pii] 10.1038/nrm3270.
16. Jheng, J.R., Ho, J.Y., and Horng, J.T. (2014). ER stress, autophagy, and RNA viruses. Front Microbiol 5, 388. doi: 10.3389/fmicb.2014.00388.
17. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J 19, 5720-5728.
18. Kaufusi, P.H., Kelley, J.F., Yanagihara, R., and Nerurkar, V.R. (2014). Induction of Endoplasmic Reticulum-Derived Replication-Competent Membrane Structures by West Nile Virus Non-Structural Protein 4B. PLoS One 9, e84040. doi: 10.1371/journal.pone.0084040 PONE-D-13-09922 [pii].
19. Ke, P.Y., and Chen, S.S. (2011). 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.
20. Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J.A., Ahn, H.J., Ait-Mohamed, O., Ait-Si-Ali, S., Akematsu, T., Akira, S., Al-Younes, H.M., Al-Zeer, M.A., Albert, M.L., Albin, R.L., Alegre-Abarrategui, J., Aleo, M.F., Alirezaei, M., Almasan, A., Almonte-Becerril, M., Amano, A., Amaravadi, R., Amarnath, S., Amer, A.O., Andrieu-Abadie, N., Anantharam, V., Ann, D.K., Anoopkumar-Dukie, S., Aoki, H., Apostolova, N., Arancia, G., Aris, J.P., Asanuma, K., Asare, N.Y., Ashida, H., Askanas, V., Askew, D.S., Auberger, P., Baba, M., Backues, S.K., Baehrecke, E.H., Bahr, B.A., Bai, X.Y., Bailly, Y., Baiocchi, R., Baldini, G., Balduini, W., Ballabio, A., Bamber, B.A., Bampton, E.T., Banhegyi, G., Bartholomew, C.R., Bassham, D.C., Bast, R.C., Jr., Batoko, H., Bay, B.H., Beau, I., Bechet, D.M., Begley, T.J., Behl, C., Behrends, C., Bekri, S., Bellaire, B., Bendall, L.J., Benetti, L., Berliocchi, L., Bernardi, H., Bernassola, F., Besteiro, S., Bhatia-Kissova, I., Bi, X., Biard-Piechaczyk, M., Blum, J.S., Boise, L.H., Bonaldo, P., Boone, D.L., Bornhauser, B.C., Bortoluci, K.R., Bossis, I., Bost, F., Bourquin, J.P., Boya, P., Boyer-Guittaut, M., Bozhkov, P.V., Brady, N.R., Brancolini, C., Brech, A., Brenman, J.E., Brennand, A., Bresnick, E.H., Brest, P., Bridges, D., Bristol, M.L., Brookes, P.S., Brown, E.J., Brumell, J.H., et al. (2012). Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544.
21. Kobayashi, S., Orba, Y., Yamaguchi, H., Takahashi, K., Sasaki, M., Hasebe, R., Kimura, T., and Sawa, H. (2014). Autophagy inhibits viral genome replication and gene expression stages in West Nile virus infection. Virus Res 191, 83-91. doi: S0168-1702(14)00282-2 [pii] 10.1016/j.virusres.2014.07.016.
22. Kohno, K., Normington, K., Sambrook, J., Gething, M.J., and Mori, K. (1993). The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol 13, 877-890.
23. Lanciotti, R.S., Roehrig, J.T., Deubel, V., Smith, J., Parker, M., Steele, K., Crise, B., Volpe, K.E., Crabtree, M.B., Scherret, J.H., Hall, R.A., Mackenzie, J.S., Cropp, C.B., Panigrahy, B., Ostlund, E., Schmitt, B., Malkinson, M., Banet, C., Weissman, J., Komar, N., Savage, H.M., Stone, W., Mcnamara, T., and Gubler, D.J. (1999). Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286, 2333-2337.
24. Li J.K., Liang, J.J., Liao, C.L., and Lin, Y.L. (2012). Autophagy is involved in the early step of Japanese encephalitis virus infection. Microbes Infect 14, 159-168. doi: S1286-4579(11)00233-4 [pii] 10.1016/j.micinf.2011.09.001.
25. Martin-Acebes, M.A., Blazquez, A.B., De Oya, N.J., Escribano-Romero, E., Shi, P.Y., and Saiz, J.C. (2013). A single amino acid substitution in the core protein of west nile virus increases resistance to acidotropic compounds. PLoS One 8, e69479. doi: 10.1371/journal.pone.0069479 PONE-D-13-04570 [pii].
26. Martin-Acebes, M.A., Blazquez, A.B., Jimenez De Oya, N., Escribano-Romero, E., and Saiz, J.C. (2011). West nile virus replication requires Fatty Acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids. PLoS One 6, e24970.
27. Martin-Acebes, M.A., and Saiz, J.C. (2011). A West Nile virus mutant with increased resistance to acid-induced inactivation. J Gen Virol 92, 831-840.
28. Martin-Acebes, M.A., and Saiz, J.C. (2012). West Nile virus: a re-emerging pathogen revisited. World J Virol 1, 51-70.
29. Mclean, J.E., Wudzinska, A., Datan, E., Quaglino, D., and Zakeri, Z. (2012). Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. J Biol Chem 286, 22147-22159. doi: M110.192500 [pii] 10.1074/jbc. M110.192500.
30. Medigeshi, G.R., Lancaster, A.M., Hirsch, A.J., Briese, T., Lipkin, W.I., Defilippis, V., Fruh, K., Mason, P.W., Nikolich-Zugich, J., and Nelson, J.A. (2007). West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81, 10849-10860.
31. Miller, S., Kastner, S., Krijnse-Locker, J., Buhler, S., and Bartenschlager, R. (2007). The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J Biol Chem 282, 8873-8882.
32. Mizushima, N., Levine, B., Cuervo, A.M., and Klionsky, D.J. (2008). Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075.
33. Mohl, B.P., Tedbury, P.R., Griffin, S., and Harris, M. (2012). Hepatitis C virus-induced autophagy is independent of the unfolded protein response. J Virol 86, 10724-10732. doi: JVI.01667-12 [pii] 10.1128/JVI.01667-12.
34. Orvedahl, A., and Levine, B. (2008). Viral evasion of autophagy. Autophagy 4, 280-285.
35. Roosendaal, J., Westaway, E.G., Khromykh, A., and Mackenzie, J.M. (2006). Regulated cleavages at the West Nile virus NS4A-2K-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein. J Virol 80, 4623-4632.
36. Shi, P.Y., Tilgner, M., Lo, M.K., Kent, K.A., and Bernard, K.A. (2002). Infectious cDNA clone of the epidemic west nile virus from New York City. J Virol 76, 5847-5856.
37. Shoji-Kawata, S., Sumpter, R., Leveno, M., Campbell, G.R., Zou, Z., Kinch, L., Wilkins, A.D., Sun, Q., Pallauf, K., Macduff, D., Huerta, C., Virgin, H.W., Helms, J.B., Eerland, R., Tooze, S.A., Xavier, R., Lenschow, D.J., Yamamoto, A., King, D., Lichtarge, O., Grishin, N.V., Spector, S.A., Kaloyanova, D.V., and Levine, B. (2013). Identification of a candidate therapeutic autophagy-inducing peptide. Nature 494, 201-206. doi: nature11866 [pii] 10.1038/nature11866.
38. Sir, D., Chen, W.L., Choi, J., Wakita, T., Yen, T.S., and Ou, J.H. (2008). Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48, 1054-1061.
39. Smithburn, K.C., Hughes, T.P., Burke, A.W., and H., P.J. (1940). A Neurotropic Virus Isolated from the Blood of a Native of Uganda. Am J Trop Med Hyg s1-20, 471-492.
40. Suh, D.H., Kim, M.K., Kim, H.S., Chung, H.H., and Song, Y.S. (2012). Unfolded protein response to autophagy as a promising druggable target for anticancer therapy. Ann N Y Acad Sci 1271, 20-32. doi: 10.1111/j.1749-6632.2012.06739.x.
41. Vandergaast, R., and Fredericksen, B.L. (2012). West Nile Virus (WNV) Replication Is Independent of Autophagy in Mammalian Cells. PLoS One 7, e45800. doi:10.1371/journal.pone.0045800 PONE-D-12-17001 [pii].
42. Wang, J., Kang, R., Huang, H., Xi, X., Wang, B., and Zhao, Z. (2014). Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathwaymediated MAP1LC3B and ATG12 expression. Autophagy 10, 766-784. doi:27954 [pii] 10.4161/auto.27954.
43. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891. doi: S0092-8674(01)00611-0 [pii].