82
Views
38
CrossRef citations to date
0
Altmetric
Article

Activation of Stress Response Pathways Promotes Formation of Antiviral Granules and Restricts Virus Replication

, , &
Pages 2003-2016 | Received 09 Dec 2013, Accepted 13 Mar 2014, Published online: 20 Mar 2023

REFERENCES

  • Smith GL, Benfield CTO, Maluquer de Motes C, Mazzon M, Ember SWJ, Ferguson BJ, Sumner RP. 2013. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J. Gen. Virol. 94:2367–2392. http://dx.doi.org/10.1099/vir.0.055921-0.
  • Moss B. 2007. Poxviridae: the viruses and their replication, p 2906–2945. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
  • Broyles SS. 2003. Vaccinia virus transcription. J. Gen. Virol. 84:2293–2303. http://dx.doi.org/10.1099/vir.0.18942-0.
  • Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. 2010. Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 107:11513–11518. http://dx.doi.org/10.1073/pnas.1006594107.
  • Yang Z, Reynolds SE, Martens CA, Bruno DP, Porcella SF, Moss B. 2011. Expression profiling of the intermediate and late stages of poxvirus replication. J. Virol. 85:9899–9908. http://dx.doi.org/10.1128/JVI.05446-11.
  • Smith GL, Symons JA, Khanna A, Vanderplasschen A, Alcamí A. 1997. Vaccinia virus immune evasion. Immunol. Rev. 159:137–154. http://dx.doi.org/10.1111/j.1600-065X.1997.tb01012.x.
  • Farrell PJ, Balkow K, Hunt T, Jackson RJ, Trachsel H. 1977. Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis. Cell 11:187–200. http://dx.doi.org/10.1016/0092-8674(77)90330-0.
  • Watson JC, Chang HW, Jacobs BL. 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. http://dx.doi.org/10.1016/0042-6822(91)90768-7.
  • Chang HW, Watson JC, Jacobs BL. 1992. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc. Natl. Acad. Sci. U. S. A. 89:4825–4829. http://dx.doi.org/10.1073/pnas.89.11.4825.
  • Myskiw C, Arsenio J, van Bruggen R, Deschambault Y, Cao J. 2009. Vaccinia virus E3 suppresses expression of diverse cytokines through inhibition of the PKR, NF-kappaB, and IRF3 pathways. J. Virol. 83:6757–6768. http://dx.doi.org/10.1128/JVI.02570-08.
  • Kwon J-A, Rich A. 2005. Biological function of the vaccinia virus Z-DNA-binding protein E3L: gene transactivation and antiapoptotic activity in HeLa cells. Proc. Natl. Acad. Sci. U. S. A. 102:12759–12764. http://dx.doi.org/10.1073/pnas.0506011102.
  • Langland JO, Jacobs BL. 2002. The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology 299:133–141. http://dx.doi.org/10.1006/viro.2002.1479.
  • Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF. 2000. PKR stimulates NF-kappaB irrespective of its kinase function by interacting with the IkappaB kinase complex. Mol. Cell. Biol. 20:4532–4542. http://dx.doi.org/10.1128/MCB.20.13.4532-4542.2000.
  • Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099–1108. http://dx.doi.org/10.1016/S1097-2765(00)00108-8.
  • Srivastava SP, Kumar KU, Kaufman RJ. 1998. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273:2416–2423. http://dx.doi.org/10.1074/jbc.273.4.2416.
  • Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897–904. http://dx.doi.org/10.1016/S1097-2765(00)80330-5.
  • Wek SA, Zhu S, Wek RC. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2 alpha protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497–4506.
  • McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen J-J, Anderson P, Kaufman RJ. 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. J. Biol. Chem. 280:16925–16933. http://dx.doi.org/10.1074/jbc.M412882200.
  • Ron D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110:1383–1388. http://dx.doi.org/10.1172/JCI16784.
  • Kawai T, Fan J, Mazan-Mamczarz K, Gorospe M. 2004. Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol. 24:6773–6787. http://dx.doi.org/10.1128/MCB.24.15.6773-6787.2004.
  • Wek RC, Jiang H-Y, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7–11. http://dx.doi.org/10.1042/BST0340007.
  • Kedersha NL, Gupta M, Li W, Miller I, Anderson P. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147:1431–1442. http://dx.doi.org/10.1083/jcb.147.7.1431.
  • Kedersha N, Anderson P. 2009. Regulation of translation by stress granules and processing bodies. Prog. Mol. Biol. Transl. Sci. 90:155–185. http://dx.doi.org/10.1016/S1877-1173(09)90004-7.
  • Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141–150. http://dx.doi.org/10.1016/j.tibs.2007.12.003.
  • Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257–1268. http://dx.doi.org/10.1083/jcb.151.6.1257.
  • Mazroui R, Sukarieh R, Bordeleau M-E, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I, Pelletier J. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell 17:4212–4219. http://dx.doi.org/10.1091/mbc.E06-04-0318.
  • Lloyd RE. 2012. How do viruses interact with stress-associated RNA granules? PLoS Pathog. 8:e1002741. http://dx.doi.org/10.1371/journal.ppat.1002741.
  • Simpson-Holley M, Kedersha N, Dower K, Rubins KH, Anderson P, Hensley LE, Connor JH. 2011. Formation of antiviral cytoplasmic granules during orthopoxvirus infection. J. Virol. 85:1581–1593. http://dx.doi.org/10.1128/JVI.02247-10.
  • Dower K, Rubins KH, Hensley LE, Connor JH. 2011. Development of vaccinia reporter viruses for rapid, high content analysis of viral function at all stages of gene expression. Antiviral Res. 91:72–80. http://dx.doi.org/10.1016/j.antiviral.2011.04.014.
  • Dower K, Filone CM, Hodges EN, Bjornson ZB, Rubins KH, Brown LE, Schaus S, Hensley LE, Connor JH. 2012. Identification of a pyridopyrimidinone inhibitor of orthopoxviruses from a diversity-oriented synthesis library. J. Virol. 86:2632–2640. http://dx.doi.org/10.1128/JVI.05416-11.
  • Van Meerloo J, Kaspers GJL, Cloos J. 2011. Cell sensitivity assays: the MTT assay. Methods Mol. Biol. 731:237–245. http://dx.doi.org/10.1007/978-1-61779-080-5_20.
  • Van de Loosdrecht AA, Beelen RH, Ossenkoppele GJ, Broekhoven MG, Langenhuijsen MM. 1994. A tetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. J. Immunol. Methods 174:311–320. http://dx.doi.org/10.1016/0022-1759(94)90034-5.
  • Santagata S, Mendillo ML, Tang Y, Subramanian A, Perley CC, Roche SP, Wong B, Narayan R, Kwon H, Koeva M, Amon A, Golub TR, Porco JAJr, Whitesell L, Lindquist S. 2013. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 341:1238303. http://dx.doi.org/10.1126/science.1238303.
  • Sodeik B, Griffiths G, Ericsson M, Moss B, Doms RW. 1994. Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65. J. Virol. 68:1103–1114.
  • Grosenbach DW, Jordan R, Hruby DE. 2011. Development of the small-molecule antiviral ST-246 as a smallpox therapeutic. Future Virol. 6:653–671. http://dx.doi.org/10.2217/fvl.11.27.
  • Bonifacino J. 2002. Protein labeling and immunoprecipitation. Curr. Protoc. Cell Biol. 15:7.0.1–7.0.3. http://dx.doi.org/10.1002/0471143030.cb0700s15.
  • David A, Dolan BP, Hickman HD, Knowlton JJ, Clavarino G, Pierre P, Bennink JR, Yewdell JW. 2012. Nuclear translation visualized by ribosome-bound nascent chain puromycylation. J. Cell Biol. 197:45–57. http://dx.doi.org/10.1083/jcb.201112145.
  • Katsafanas GC, Moss B. 2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2:221–228. http://dx.doi.org/10.1016/j.chom.2007.08.005.
  • Breinbauer R, Köhn M. 2003. Azide-alkyne coupling: a powerful reaction for bioconjugate chemistry. Chembiochem 4:1147–1149. http://dx.doi.org/10.1002/cbic.200300705.
  • Wang Q, Chan TR, Hilgraf R, Fokin VV, Sharpless KB, Finn MG. 2003. Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125:3192–3193. http://dx.doi.org/10.1021/ja021381e.
  • Rostovtsev VV, Green LG, Fokin VV, Sharpless KB. 2002. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41:2596–2599. http://dx.doi.org/10.1002/1521-3773(20020715)41:14<2596::AID-ANIE2596>3.0.CO;2-4.
  • Kolb HC, Finn MG, Sharpless KB. 2001. Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. Engl. 40:2004–2021. http://www.renyi.hu/∼stipsicz/Mezo_DECEMBER/click/click.pdf.
  • Bordeleau M-E, Mori A, Oberer M, Lindqvist L, Chard LS, Higa T, Belsham GJ, Wagner G, Tanaka J, Pelletier J. 2006. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat. Chem. Biol. 2:213–220. http://dx.doi.org/10.1038/nchembio776.
  • Kedersha N, Anderson P. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61–81. http://dx.doi.org/10.1016/S0076-6879(07)31005-7.
  • Dales S, Siminovitch L. 1961. The development of vaccinia virus in Earle's L strain cells as examined by electron microscopy. J. Biophys. Biochem. Cytol. 10:475–503. http://dx.doi.org/10.1083/jcb.10.4.475.
  • Tolonen N, Doglio L, Schleich S, Krijnse Locker J. 2001. Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol. Biol. Cell 12:2031–2046. http://dx.doi.org/10.1091/mbc.12.7.2031.
  • Dember LM, Kim ND, Liu KQ, Anderson P. 1996. Individual RNA recognition motifs of TIA-1 and TIAR have different RNA binding specificities. J. Biol. Chem. 271:2783–2788. http://dx.doi.org/10.1074/jbc.271.5.2783.
  • Katoh H, Okamoto T, Fukuhara T, Kambara H, Morita E, Mori Y, Kamitani W, Matsuura Y. 2013. Japanese encephalitis virus core protein inhibits stress granule formation through an interaction with caprin-1 and facilitates viral propagation. J. Virol. 87:489–502. http://dx.doi.org/10.1128/JVI.02186-12.
  • Smith JA, Schmechel SC, Raghavan A, Abelson M, Reilly C, Katze MG, Kaufman RJ, Bohjanen PR, Schiff LA. 2006. Reovirus induces and benefits from an integrated cellular stress response. J. Virol. 80:2019–2033. http://dx.doi.org/10.1128/JVI.80.4.2019-2033.2006.
  • White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295–305. http://dx.doi.org/10.1016/j.chom.2007.08.006.
  • White SD, Jacobs BL. 2012. The amino terminus of the vaccinia virus E3 protein is necessary to inhibit the interferon response. J. Virol. 86:5895–5904. http://dx.doi.org/10.1128/JVI.06889-11.
  • Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D. 2003. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22:1180–1187. http://dx.doi.org/10.1093/emboj/cdg112.
  • Kufe DW, Munroe D, Herrick D, Egan E, Spriggs D. 1984. Effects of 1-beta-D-arabinofuranosylcytosine incorporation on eukaryotic DNA template function. Mol. Pharmacol. 26:128–134.
  • Prins C, Cresawn SG, Condit RC. 2004. An isatin-beta-thiosemicarbazone-resistant vaccinia virus containing a mutation in the second largest subunit of the viral RNA polymerase is defective in transcription elongation. J. Biol. Chem. 279:44858–44871. http://dx.doi.org/10.1074/jbc.M408167200.
  • Moss B, Rosenblum EN, Katz E, Grimley PM. 1969. Rifampicin: a specific inhibitor of vaccinia virus assembly. Nature 224:1280–1284. http://dx.doi.org/10.1038/2241280a0.
  • Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, Rippen S, Barone L, Burns C, Rhodes G, Tohan S, Huggins JW, Baker RO, Buller RLM, Touchette E, Waller K, Schriewer J, Neyts J, DeClercq E, Jones K, Hruby D, Jordan R. 2005. An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus challenge. J. Virol. 79:13139–13149. http://dx.doi.org/10.1128/JVI.79.20.13139-13149.2005.
  • Antman KH. 2001. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist 6(Suppl 2):1–2. http://dx.doi.org/10.1634/theoncologist.6-suppl_2-1.
  • Cutler EG, Bradford EH. 1878. Action of iron, cod-liver oil, and arsenic on the globular richness of the blood. Am. J. Med. Sci. 75:74–84.
  • Anderson P, Kedersha N. 2006. RNA granules. J. Cell Biol. 172:803–808. http://dx.doi.org/10.1083/jcb.200512082.
  • Panas MD, Varjak M, Lulla A, Eng KE, Merits A, Karlsson Hedestam GB, McInerney GM. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol. Biol. Cell 23:4701–4712. http://dx.doi.org/10.1091/mbc.E12-08-0619.
  • Fros JJ, Domeradzka NE, Baggen J, Geertsema C, Flipse J, Vlak JM, Pijlman GP. 2012. Chikungunya virus nsP3 blocks stress granule assembly by recruitment of G3BP into cytoplasmic foci. J. Virol. 86:10873–10879. http://dx.doi.org/10.1128/JVI.01506-12.
  • White JP, Lloyd RE. 2011. Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation. J. Virol. 85:12442–12454. http://dx.doi.org/10.1128/JVI.05888-11.
  • Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE. 2010. Stable formation of compositionally unique stress granules in virus-infected cells. J. Virol. 84:3654–3665. http://dx.doi.org/10.1128/JVI.01320-09.
  • Mok BW-Y, Song W, Wang P, Tai H, Chen Y, Zheng M, Wen X, Lau S-Y, Wu WL, Matsumoto K, Yuen K-Y, Chen H. 2012. The NS1 protein of influenza A virus interacts with cellular processing bodies and stress granules through RNA-associated protein 55 (RAP55) during virus infection. J. Virol. 86:12695–12707. http://dx.doi.org/10.1128/JVI.00647-12.
  • Onomoto K, Jogi M, Yoo J-S, Narita R, Morimoto S, Takemura A, Sambhara S, Kawaguchi A, Osari S, Nagata K, Matsumiya T, Namiki H, Yoneyama M, Fujita T. 2012. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 7:e43031. http://dx.doi.org/10.1371/journal.pone.0043031.
  • Filone CM, Caballero IS, Dower K, Mendillo ML, Cowley GS, Santagata S, Rozelle DK, Yen J, Rubins KH, Hacohen N, Root DE, Hensley LE, Connor J. 2014. The master regulator of the cellular stress response (HSF1) is critical for orthopoxvirus infection. PLoS Pathog. 10:e1003904. http://dx.doi.org/10.1371/journal.ppat.1003904.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.