Acrylamide inhibits vaccinia virus through vimentin-independent anti-viral granule formation.
AVGs
VACV
acrylamide
poxvirus
vaccinia
vimentin
Journal
Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
23
03
2021
received:
22
09
2020
accepted:
29
03
2021
pubmed:
2
4
2021
medline:
14
1
2022
entrez:
1
4
2021
Statut:
ppublish
Résumé
The replication and assembly of vaccinia virus (VACV), the prototypic poxvirus, occurs exclusively in the cytoplasm of host cells. While the role of cellular cytoskeletal components in these processes remains poorly understood, vimentin-a type III intermediate filament-has been shown to associate with viral replication sites and to be incorporated into mature VACV virions. Here, we employed chemical and genetic approaches to further investigate the role of vimentin during the VACV lifecycle. The collapse of vimentin filaments, using acrylamide, was found to inhibit VACV infection at the level of genome replication, intermediate- and late-gene expression. However, we found that CRISPR-mediated knockout of vimentin did not impact VACV replication. Combining these tools, we demonstrate that acrylamide treatment results in the formation of anti-viral granules (AVGs) known to mediate translational inhibition of many viruses. We conclude that vimentin is dispensable for poxvirus replication and assembly and that acrylamide, as a potent inducer of AVGs during VACV infection, serves to bolster cell's anti-viral response to poxvirus infection.
Substances chimiques
Antiviral Agents
0
Vimentin
0
Acrylamide
20R035KLCI
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13334Subventions
Organisme : H2020 European Research Council
ID : 649101
Organisme : Medical Research Council
ID : MC_UU_00012/7
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U12266B
Pays : United Kingdom
Informations de copyright
© 2021 The Authors. Cellular Microbiology published by John Wiley & Sons Ltd.
Références
Balzarini, J., & Declercq, E. (1989). The antiviral activity of 9-BETA-D-arabinofuranosyladenine is enhanced by the 2′,3'-dideoxyriboside, the 2′,3'-didehydro-2′,3'-dideoxyriboside and the 3'-azido-2′,3'-dideoxyriboside of 2,6-diaminopurine. Biochemical and Biophysical Research Communications, 159, 61-67.
Bhattacharya, B., Noad, R. J., & Roy, P. (2007). Interaction between bluetongue virus outer capsid protein VP2 and vimentin is necessary for virus egress. Virology Journal, 4, 7.
Bidgood, S. R. (2019). Continued poxvirus research: From foe to friend. Plos Biology, 17(1), e3000124.
Chang, H. W., Watson, J. C., & Jacobs, B. L. (1992). The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein-kinase. Proceedings of the National Academy of Sciences of the United States of America, 89, 4825-4829.
Chang, L., & Goldman, R. D. (2004). Intermediate filaments mediate cytoskeletal crosstalk. Nature Reviews Molecular Cell Biology, 5, 601-613.
Chung, C. S., Chen, C. H., Ho, M. Y., Huang, C. Y., Liao, C. L., & Chang, W. (2006). Vaccinia virus proteome: Identification of proteins in vaccinia virus intracellular mature virion particles. Journal of Virology, 80, 2127-2140.
Condit, R. C., Moussatche, N., & Traktman, P. (2006). In a nutshell: Structure and assembly of the vaccinia virion. Advances in Virus Research, 66, 31.
Cordo, S. M., & Candurra, N. A. (2003). Intermediate filament integrity is required for Junin virus replication. Virus Research, 97, 47-55.
Cudmore, S., Cossart, P., Griffiths, G., & Way, M. (1995). Actin-based motility of vaccinia virus. Nature, 378, 636-638.
Danielsson, F., Peterson, M. K., Araujo, H. C., Lautenschlager, F., & Gad, A. K. B. (2018). Vimentin diversity in health and disease. Cell, 7(10), 147.
DeMasi, J., & Traktman, P. (2000). Clustered charge-to-alanine mutagenesis of the vaccinia virus H5 gene: Isolation of a dominant, temperature-sensitive mutant with a profound defect in morphogenesis. Journal of Virology, 74, 2393-2405.
Durham, H. D., Pena, S. D. J., & Carpenter, S. (1983). The neurotoxins 2,5-hexanedione and acrylamide promote aggregation of intermediate filaments in cultured fibroblasts. Muscle & Nerve, 6, 631-637.
Eckert, B. S. (1986). Alteration of the distribution of intermediate filaments in PtK1 cells by acrylamide. 2. Effect on the organization of cytoplasmic organelles. Cell Motility and the Cytoskeleton, 6, 15-24.
Farrell, P. J., Balkow, K., Hunt, T., Jackson, R. J., & Trachsel, H. (1977). Phosphorylation of initiation-factor ELF-2 and control of reticulocyte protein-synthesis. Cell, 11, 187-200.
Fay, N., & Pante, N. (2013). The intermediate filament network protein, vimentin, is required for parvoviral infection. Virology, 444, 181-190.
Galabru, J., & Hovanessian, A. (1987). Autophosphorylation of the protein-kinase dependent on double-stranded-RNA. Journal of Biological Chemistry, 262, 15538-15544.
Guzikowski, A. R., Chen, Y. S., & Zid, B. M. (2019). Stress-induced mRNP granules: Form and function of processing bodies and stress granules. Wiley Interdisciplinary Reviews-RNA, 10(3), e1524.
Harding, H. P., Zhang, Y. H., Bertolotti, A., Zeng, H. Q., & Ron, D. (2000). Perk is essential for translational regulation and cell survival during the unfolded protein response. Molecular Cell, 5, 897-904.
Huttunen, M., & Mercer, J. (2019). Quantitative PCR-based assessment of vaccinia virus RNA and DNA in infected cells. In Vaccinia virus. Methods in molecular biology. New York, NY: Humana.
Ichihashi, Y., Oie, M., & Tsuruhara, T. (1984). Location of DNA-binding proteins and disulfide-linked proteins in vaccinia virus structural elements. Journal of Virology, 50, 929-938.
Issac, T. H. K., Tan, E. L., & Chu, J. J. H. (2014). Proteomic profiling of chikungunya virus-infected human muscle cells: Reveal the role of cytoskeleton network in CHIKV replication. Journal of Proteomics, 108, 445-464.
Ivaska, J., Pallari, H. M., Nevo, J., & Eriksson, J. E. (2007). Novel functions of vimentin in cell adhesion, migration, and signaling. Experimental Cell Research, 313, 2050-2062.
Jackson, R. J., Hellen, C. U. T., & Pestova, T. V. (2010). The mechanism of eukaryotic translation initiation and principles of its regulation. Nature Reviews Molecular Cell Biology, 11, 113-127.
Jiang, L. P., Cao, J., An, Y., Geng, C. Y., Qu, S. X., Jiang, L. J., & Zhong, L. F. (2007). Genotoxicity of acrylamide in human hepatoma G2 (HepG2) cells. Toxicology in Vitro, 21, 1486-1492.
Kilcher, S., Schmidt, F. I., Schneider, C., Kopf, M., Helenius, A., & Mercer, J. (2014). siRNA screen of early poxvirus genes identifies the AAA+ ATPase D5 as the virus genome-uncoating factor. Cell Host & Microbe, 15, 103-112.
Kim, K. H., Park, B., Rhee, D. K., & Pyo, S. (2015). Acrylamide induces senescence in macrophages through a process involving ATF3, ROS, p38/JNK, and a telomerase-independent pathway. Chemical Research in Toxicology, 28, 71-86.
Komoike, Y., & Matsuoka, M. (2016). Endoplasmic reticulum stress-mediated neuronal apoptosis by acrylamide exposure. Toxicology and Applied Pharmacology, 310, 68-77.
Komoike, Y., & Matsuoka, M. (2019). In vitro and in vivo studies of oxidative stress responses against acrylamide toxicity in zebrafish. Journal of Hazardous Materials, 365, 430-439.
Liem, J., & Liu, J. (2016). Stress beyond translation: Poxviruses and more. Viruses-Basel, 8(6), 169.
Lin, Y. C. J., & Evans, D. H. (2010). Vaccinia virus particles mix inefficiently, and in a way that would restrict viral recombination, in coinfected cells. Journal of Virology, 84, 2432-2443.
Lowery, J., Kuczmarski, E. R., Herrmann, H., & Goldman, R. D. (2015). Intermediate filaments play a pivotal role in regulating cell architecture and function. Journal of Biological Chemistry, 290, 17145-17153.
Mallardo, M., Schleich, S., & Locker, J. K. (2001). Microtubule-dependent organization of vaccinia virus core-derived early mRNAs into distinct cytoplasmic structures. Molecular Biology of the Cell, 12, 3875-3891.
Manes, N. P., Estep, R. D., Mottaz, H. M., Moore, R. J., Clauss, T. R. W., Monroe, M. E., … Smith, R. D. (2008). Comparative proteomics of human monkeypox and vaccinia intracellular mature and extracellular enveloped virions. Journal of Proteome Research, 7, 960-968.
McCormick, C., & Khaperskyy, D. A. (2017). Translation inhibition and stress granules in the antiviral immune response. Nature Reviews Immunology, 17, 647-660.
McEwen, E., Kedersha, N., Song, B. B., Scheuner, D., Gilks, N., Han, A. P., … Kaufman, R. J. (2005). Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. Journal of Biological Chemistry, 280, 16925-16933.
Mercer, J., & Helenius, A. (2008). Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science, 320, 531-535.
Mercer, J., Knebel, S., Schmidt, F. I., Crouse, J., Burkard, C., & Helenius, A. (2010). Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proceedings of the National Academy of Sciences of the United States of America, 107, 9346-9351.
Mercer, J., Snijder, B., Sacher, R., Burkard, C., Bleck, C. K. E., Stahlberg, H., … Helenius, A. (2012). RNAi screening reveals proteasome- and Cullin3-dependent stages in vaccinia virus infection. Cell Reports, 2, 1036-1047.
Mercer, J., & Traktman, P. (2003). Investigation of structural and functional motifs within the vaccinia virus A14 phosphoprotein, an essential component of the virion membrane. Journal of Virology, 77, 8857-8871.
Mercer, J., & Traktman, P. (2005). Genetic and cell biological characterization of the vaccinia virus A30 and G7 phosphoproteins. Journal of Virology, 79, 7146-7161.
Miller, M. S., & Hertel, L. (2009). Onset of human cytomegalovirus replication in Fibroblasts requires the presence of an intact Vimentin cytoskeleton. Journal of Virology, 83, 7015-7028.
Minin, A. A., & Moldaver, M. V. (2008). Intermediate Vimentin filaments and their role in intracellular organelle distribution. Biochemistry-Moscow, 73, 1453-1466.
Moss, B. (2013). Poxviridae. Fields virology (Vol. 2, 6th ed.). Philadelphia, PA: Lippincott Williams and Wilkins.
Onomoto, K., Yoneyama, M., Fung, G., Kato, H., & Fujita, T. (2014). Antiviral innate immunity and stress granule responses. Trends in Immunology, 35, 420-428.
Piotrowska, J., Hansen, S. J., Park, N., Jamka, K., Sarnow, P., & Gustin, K. E. (2010). Stable formation of compositionally unique stress granules in virus-infected cells. Journal of Virology, 84, 3654-3665.
Ploubidou, A., Moreau, V., Ashman, K., Reckmann, I., Gonzalez, C., & Way, M. (2000). Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO Journal, 19, 3932-3944.
Punjabi, A., & Traktman, P. (2005). Cell biological and functional characterization of the vaccinia virus F10 kinase: Implications for the mechanism of virion morphogenesis. Journal of Virology, 79, 2171-2190.
Resch, W., Hixson, K. K., Moore, R. J., Lipton, M. S., & Moss, B. (2007). Protein composition of the vaccinia virus mature virion. Virology, 358, 233-247.
Rietdorf, J., Ploubidou, A., Reckmann, I., Holmstrom, A., Frischknecht, F., Zettl, M., … Way, M. (2001). Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nature Cell Biology, 3, 992-1000.
Risco, C., Rodriguez, J. R., Lopez-Iglesias, C., Carrascosa, J. L., Esteban, M., & Rodriguez, D. (2002). Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. Journal of Virology, 76, 1839-1855.
Rizopoulos, Z., Balistreri, G., Kilcher, S., Martin, C. K., Syedbasha, M., Helenius, A., & Mercer, J. (2015). Vaccinia virus infection requires maturation of macropinosomes. Traffic, 16, 814-831.
Rozelle, D. K., Filone, C. M., Kedersha, N., & Connor, J. H. (2014). Activation of stress response pathways promotes formation of antiviral granules and restricts virus replication. Molecular and Cellular Biology, 34, 2003-2016.
Schmidt, F. I., Bleck, C. K. E., Helenius, A., & Mercer, J. (2011). Vaccinia extracellular virions enter cells by macropinocytosis and acid-activated membrane rupture. EMBO Journal, 30, 3647-3661.
Schmidt, F. I., Bleck, C. K. E., Reh, L., Novy, K., Wollscheid, B., Helenius, A., … Mercer, J. (2013). Vaccinia virus entry is followed by core activation and proteasome-mediated release of the immunomodulatory effector VH1 from lateral bodies. Cell Reports, 4, 464-476.
Sidwell, R. W., Dixon, G. J., Sellers, S. M., & Schabel, F. M. (1968). In vivo antiviral properties of biologically active compounds. 2. Studies with influenza and vaccinia viruses. Applied Microbiology, 16, 370.
Simpson-Holley, M., Kedersha, N., Dower, K., Rubins, K. H., Anderson, P., Hensley, L. E., & Connor, J. H. (2011). Formation of antiviral cytoplasmic granules during Orthopoxvirus infection. Journal of Virology, 85, 1581-1593.
Smith, G. L., & Law, M. (2004). The exit of vaccinia virus from infected cells. Virus Research, 106, 189-197.
Styers, M. L., Salazar, G., Love, R., Peden, A. A., Kowalczyk, A. P., & Faundez, V. (2004). The endo-lysosomal sorting machinery interacts with the intermediate filament cytoskeleton. Molecular Biology of the Cell, 15, 5369-5382.
Szajner, P., Weisberg, A. S., & Moss, B. (2004). Physical and functional interactions between vaccinia virus F10 protein kinase and virion assembly proteins A30 and G7. Journal of Virology, 78, 266-274.
Tolonen, N., Doglio, L., Schleich, S., & Locker, J. K. (2001). Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Molecular Biology of the Cell, 12, 2031-2046.
Wang, Q., Zhang, X. L., Han, Y. L., Wang, X. L., & Gao, G. X. (2016). M2BP inhibits HIV-1 virion production in a vimentin filaments-dependent manner. Scientific Reports, 6(1), 32736.
Ward, B. M., & Moss, B. (2001). Vaccinia virus intracellular movement is associated with microtubules and independent of Actin tails. Journal of Virology, 75, 11651-11663.
Watson, J. C., Chang, H. W., & Jacobs, B. L. (1991). Characterization of a vaccinia virus-encoded double-stranded RNA-binding protein that may be involved in inhibition of the double-stranded RNA-dependent protein-kinase. Virology, 185, 206-216.
Yakimovich, A., Huttunen, M., Zehnder, B., Coulter, L. J., Gould, V., Schneider, C., … Mercer, J. (2017). Inhibition of poxvirus gene expression and genome replication by Bisbenzimide derivatives. Journal of Virology, 91(18), e00838.