1932

Abstract

RNA granules are dynamic cellular structures essential for proper gene expression and homeostasis. The two principal types of cytoplasmic RNA granules are stress granules, which contain stalled translation initiation complexes, and processing bodies (P bodies), which concentrate factors involved in mRNA degradation. RNA granules are associated with gene silencing of transcripts; thus, viruses repress RNA granule functions to favor replication. This article discusses the breadth of viral interactions with cytoplasmic RNA granules, focusing on mechanisms that modulate the functions of RNA granules and that typically promote viral replication. Currently, mechanisms for virus manipulation of RNA granules can be loosely grouped into three nonexclusive categories: () cleavage of key RNA granule factors, () regulation of PKR activation, and () co-opting of RNA granule factors for new roles in viral replication. Viral modulation of RNA granules supports productive infection by inhibiting their gene-silencing functions and counteracting their role in linking stress sensing with innate immune activation.

Keyword(s): G3BPP bodiesPKRstress granules

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2014-09-29
2024-04-25
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Literature Cited

  1. Mao YS, Zhang B, Spector DL. 1.  2011. Biogenesis and function of nuclear bodies. Trends Genet. 27:295–306 [Google Scholar]
  2. Caudron-Herger M, Rippe K. 2.  2012. Nuclear architecture by RNA. Curr. Opin. Genet. Dev. 22:179–87 [Google Scholar]
  3. Kedersha N, Anderson P. 3.  2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61–81 [Google Scholar]
  4. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J. 4.  et al. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871–84 [Google Scholar]
  5. Buchan JR, Parker R. 5.  2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36:932–41 [Google Scholar]
  6. Mokas S, Mills JR, Garreau C, Fournier MJ, Robert F. 6.  et al. 2009. Uncoupling stress granule assembly and translation initiation inhibition. Mol. Biol. Cell 20:2673–83 [Google Scholar]
  7. Dang Y, Kedersha N, Low WK, Romo D, Gorospe M. 7.  et al. 2006. Eukaryotic initiation factor 2α–independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281:32870–78 [Google Scholar]
  8. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. 8.  1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2α to the assembly of mammalian stress granules. J. Cell Biol. 147:1431–42 [Google Scholar]
  9. Chang TC, Yamashita A, Chen CYA, Yamashita Y, Zhu W. 9.  et al. 2004. UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant. Genes Dev. 18:2010–23 [Google Scholar]
  10. Shyu AB, Wilkinson MF, van Hoof A. 10.  2008. Messenger RNA regulation: to translate or to degrade. EMBO J. 27:471–81 [Google Scholar]
  11. Anderson P, Kedersha N. 11.  2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141–50 [Google Scholar]
  12. Towers ER, Kelly JJ, Sud R, Gale JE, Dawson SJ. 12.  2011. Caprin-1 is a target of the deafness gene Pou4f3 and is recruited to stress granules in cochlear hair cells in response to ototoxic damage. J. Cell Sci. 124:1145–55 [Google Scholar]
  13. Mangiardi DA, McLaughlin-Williamson K, May KE, Messana EP, Mountain DC, Cotanche DA. 13.  2004. Progression of hair cell ejection and molecular markers of apoptosis in the avian cochlea following gentamicin treatment. J. Comp. Neurol. 475:1–18 [Google Scholar]
  14. Kotani T, Yasuda K, Ota R, Yamashita M. 14.  2013. Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules. J. Cell Biol. 202:1041–55 [Google Scholar]
  15. Weil TT, Parton RM, Herpers B, Soetaert J, Veenendaal T. 15.  et al. 2012. Drosophila patterning is established by differential association of mRNAs with P bodies. Nat. Cell Biol. 14:1305–15 [Google Scholar]
  16. Costa A, Pazman C, Sinsimer KS, Wong LC, McLeod I. 16.  et al. 2013. Rasputin functions as a positive regulator of Orb in Drosophila oogenesis. PLoS ONE 8:e72864 [Google Scholar]
  17. Bentmann E, Haass C, Dormann D. 17.  2013. Stress granules in neurodegeneration—lessons learnt from TAR DNA binding protein of 43 kDa and fused in sarcoma. FEBS J. 280:4348–70 [Google Scholar]
  18. Vanderweyde T, Youmans K, Liu-Yesucevitz L, Wolozin B. 18.  2013. Role of stress granules and RNA-binding proteins in neurodegeneration: a mini-review. Gerontology 59:524–33 [Google Scholar]
  19. Shelkovnikova TA, Robinson H, Connor-Robson N, Buchman VL. 19.  2013. Recruitment into stress granules prevents irreversible aggregation of FUS protein mislocalized to the cytoplasm. Cell Cycle 12:3194–202 [Google Scholar]
  20. Nakamura T, Furuhashi M, Li P, Cao H, Tuncman G. 20.  et al. 2010. Double-stranded RNA–dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 140:338–48 [Google Scholar]
  21. Yang X, Nath A, Opperman MJ, Chan C. 21.  2010. The double-stranded RNA–dependent protein kinase differentially regulates insulin receptor substrates 1 and 2 in HepG2 cells. Mol. Biol. Cell 21:3449–58 [Google Scholar]
  22. Lu B, Nakamura T, Inouye K, Li J, Tang Y. 22.  et al. 2012. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488:670–74 [Google Scholar]
  23. Taghavi N, Samuel CE. 23.  2012. Protein kinase PKR catalytic activity is required for the PKR-dependent activation of mitogen-activated protein kinases and amplification of interferon β induction following virus infection. Virology 427:208–16 [Google Scholar]
  24. Steele L, Errington F, Prestwich R, Ilett E, Harrington K. 24.  et al. 2011. Pro-inflammatory cytokine/chemokine production by reovirus treated melanoma cells is PKR/NF-κB mediated and supports innate and adaptive anti-tumour immune priming. Mol. Cancer 10:20–33 [Google Scholar]
  25. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E. 25.  et al. 2006. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70:1032–60 [Google Scholar]
  26. Okonski KM, Samuel CE. 26.  2013. Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. J. Virol. 87:756–66 [Google Scholar]
  27. Onomoto K, Jogi M, Yoo JS, Narita R, Morimoto S. 27.  et al. 2012. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS ONE 7:e43031 [Google Scholar]
  28. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. 28.  2012. Large G3BP-induced granules trigger eIF2α phosphorylation. Mol. Biol. Cell 23:3499–510 [Google Scholar]
  29. Dougherty JD, Reineke LC, Lloyd RE. 29.  2014. mRNA decapping enzyme 1a (Dcp1a)-induced translational arrest through PKR activation requires the N-terminal EVH1 domain. J. Biol. Chem. 289:3936–49 [Google Scholar]
  30. Ghosh S, May MJ, Kopp EB. 30.  1998. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225–60 [Google Scholar]
  31. Gil J, Rullas J, Garcia MA, Alcamí J, Esteban M. 31.  2001. The catalytic activity of dsRNA-dependent protein kinase, PKR, is required for NF-κB activation. Oncogene 20:385–94 [Google Scholar]
  32. Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF. 32.  2000. PKR stimulates NF-κB irrespective of its kinase function by interacting with the IκB kinase complex. Mol. Cell. Biol. 20:4532–42 [Google Scholar]
  33. Fung G, Ng CS, Zhang J, Shi J, Wong J. 33.  et al. 2013. Production of a dominant-negative fragment due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS ONE 8:e79546 [Google Scholar]
  34. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S. 34.  et al. 2013. Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J. Virol. 87:9511–22 [Google Scholar]
  35. Hebner CM, Wilson R, Rader J, Bidder M, Laimins LA. 35.  2006. Human papillomaviruses target the double-stranded RNA protein kinase pathway. J. Gen. Virol. 87:3183–93 [Google Scholar]
  36. Langereis MA, Feng Q, van Kuppeveld FJ. 36.  2013. MDA5 localizes to stress granules, but this localization is not required for the induction of type I interferon. J. Virol. 87:6314–25 [Google Scholar]
  37. Khaperskyy DA, Hatchette TF, McCormick C. 37.  2011. Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J. 26:1629–39 [Google Scholar]
  38. Wasserman T, Katsenelson K, Daniliuc S, Hasin T, Choder M, Aronheim A. 38.  2010. A novel c-Jun N-terminal kinase (JNK)-binding protein WDR62 is recruited to stress granules and mediates a nonclassical JNK activation. Mol. Biol. Cell 21:117–30 [Google Scholar]
  39. Mazroui R, Sukarieh R, Bordeleau ME, Kaufman RJ, Northcote P. 39.  et al. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Mol. Biol. Cell 17:4212–19 [Google Scholar]
  40. Anderson P, Kedersha N. 40.  2009. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10:430–36 [Google Scholar]
  41. Kedersha N, Ivanov P, Anderson P. 41.  2013. Stress granules and cell signaling: more than just a passing phase?. Trends Biochem. Sci. 38:494–506 [Google Scholar]
  42. Loschi M, Leishman CC, Berardone N, Boccaccio GL. 42.  2009. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122:3973–82 [Google Scholar]
  43. Ohn T, Anderson P. 43.  2010. The role of posttranslational modifications in the assembly of stress granules. WIRES RNA 1:486–93 [Google Scholar]
  44. Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. 44.  2008. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10:1224–31 [Google Scholar]
  45. Weber SC, Brangwynne CP. 45.  2012. Getting RNA and protein in phase. Cell 149:1188–91 [Google Scholar]
  46. Kato M, Han TW, Xie S, Shi K, Du X. 46.  et al. 2012. Cell-free formation of RNA granules: Low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–67 [Google Scholar]
  47. Han TW, Kato M, Xie S, Wu LC, Mirzaei H. 47.  et al. 2012. Cell-free formation of RNA granules: Bound RNAs identify features and components of cellular assemblies. Cell 149:768–79 [Google Scholar]
  48. Bentmann E, Neumann M, Tahirovic S, Rodde R, Dormann D, Haass C. 48.  2012. Requirements for stress granule recruitment of fused in sarcoma (FUS) and TAR DNA-binding protein of 43 kDa (TDP-43). J. Biol. Chem. 287:23079–94 [Google Scholar]
  49. Li P, Banjade S, Cheng HC, Kim S, Chen B. 49.  et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336–40 [Google Scholar]
  50. Aulas A, Stabile S, Vande Velde C. 50.  2012. Endogenous TDP-43, but not FUS, contributes to stress granule assembly via G3BP. Mol. Neurodegener. 7:54 [Google Scholar]
  51. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM. 51.  et al. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823–31 [Google Scholar]
  52. Bikkavilli RK, Malbon CC. 52.  2011. Arginine methylation of G3BP1 in response to Wnt3a regulates β-catenin mRNA. J. Cell Sci. 124:2310–20 [Google Scholar]
  53. Dammer EB, Fallini C, Gozal YM, Duong DM, Rossoll W. 53.  et al. 2012. Coaggregation of RNA-binding proteins in a model of TDP-43 proteinopathy with selective RGG motif methylation and a role for RRM1 ubiquitination. PLoS ONE 7:e38658 [Google Scholar]
  54. White JP, Cardenas AM, Marissen WE, Lloyd RE. 54.  2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295–305 [Google Scholar]
  55. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE. 55.  2010. Stable formation of compositionally unique stress granules in virus-infected cells. J. Virol. 84:3654–65 [Google Scholar]
  56. White JP, Lloyd RE. 56.  2011. Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation. J. Virol. 85:12442–54 [Google Scholar]
  57. Borghese F, Michiels T. 57.  2011. The leader protein of cardioviruses inhibits stress granule assembly. J. Virol. 85:9614–22 [Google Scholar]
  58. Khong A, Jan E. 58.  2011. Modulation of stress granules and P bodies during dicistrovirus infection. J. Virol. 85:1439–51 [Google Scholar]
  59. Mok BWY, Song W, Wang P, Tai H, Chen Y. 59.  et al. 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. 86:12695–707 [Google Scholar]
  60. Montero H, Rojas M, Arias CF, López S. 60.  2008. Rotavirus infection induces the phosphorylation of eIF2α but prevents the formation of stress granules. J. Virol. 82:1496–504 [Google Scholar]
  61. Smith JA, Schmechel SC, Raghavan A, Abelson M, Reilly C. 61.  et al. 2006. Reovirus induces and benefits from an integrated cellular stress response. J. Virol. 80:2019–33 [Google Scholar]
  62. Qin Q, Hastings C, Miller CL. 62.  2009. Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection. J. Virol. 83:11090–101 [Google Scholar]
  63. Qin Q, Carroll K, Hastings C, Miller CL. 63.  2011. Mammalian orthoreovirus escape from host translational shutoff correlates with stress granule disruption and is independent of eIF2α phosphorylation and PKR. J. Virol. 85:8798–810 [Google Scholar]
  64. Carroll K, Hastings C, Miller CL. 64.  2014. Amino acids 78 and 79 of mammalian orthoreovirus protein μNS are necessary for stress granule localization, core protein λ2 interaction, and de novo virus replication. Virology 448:133–45 [Google Scholar]
  65. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest JP. 65.  et al. 2012. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12:71–85 [Google Scholar]
  66. Paul D, Hoppe S, Saher G, Krijnse-Locker J, Bartenschlager R. 66.  2013. Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J. Virol. 87:10612–27 [Google Scholar]
  67. Raaben M, Groot Koerkamp MJA, Rottier PJM, De Haan CAM. 67.  2007. Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol. 9:2218–29 [Google Scholar]
  68. Sola I, Galán C, Mateos-Gómez PA, Palacio L, Zúñiga S. 68.  et al. 2011. The polypyrimidine tract–binding protein affects coronavirus RNA accumulation levels and relocalizes viral RNAs to novel cytoplasmic domains different from replication-transcription sites. J. Virol. 85:5136–49 [Google Scholar]
  69. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL. 69.  et al. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J. Virol. 84:6720–32 [Google Scholar]
  70. Frolova E, Gorchakov R, Garmashova N, Atasheva S, Vergara LA, Frolov I. 70.  2006. Formation of nsP3-specific protein complexes during Sindbis virus replication. J. Virol. 80:4122–34 [Google Scholar]
  71. Gorchakov R, Garmashova N, Frolova E, Frolov I. 71.  2008. Different types of nsP3-containing protein complexes in Sindbis virus–infected cells. J. Virol. 82:10088–101 [Google Scholar]
  72. Fros JJ, Domeradzka NE, Baggen J, Geertsema C, Flipse J. 72.  et al. 2012. Chikungunya virus nsP3 blocks stress granule assembly by recruitment of G3BP into cytoplasmic foci. J. Virol. 86:10873–79 [Google Scholar]
  73. Atasheva S, Gorchakov R, English R, Frolov I, Frolova E. 73.  2007. Development of Sindbis viruses encoding nsP2/GFP chimeric proteins and their application for studying nsP2 functioning. J. Virol. 81:5046–57 [Google Scholar]
  74. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljeström P. 74.  2005. Importance of eIF2α phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753–63 [Google Scholar]
  75. Panas MD, Varjak M, Lulla A, Eng KE, Merits A. 75.  et al. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol. Biol. Cell 23:4701–12 [Google Scholar]
  76. Matthews JD, Frey TK. 76.  2012. Analysis of subcellular G3BP redistribution during rubella virus infection. J. Gen. Virol. 93:267–74 [Google Scholar]
  77. Emara MM, Brinton MA. 77.  2007. Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. USA 104:9041–46 [Google Scholar]
  78. Emara MM, Liu H, Davis WG, Brinton MA. 78.  2008. Mutation of mapped TIA-1/TIAR binding sites in the 3′ terminal stem-loop of West Nile virus minus-strand RNA in an infectious clone negatively affects genomic RNA amplification. J. Virol. 82:10657–70 [Google Scholar]
  79. Li W, Li Y, Kedersha N, Anderson P, Emara M. 79.  et al. 2002. Cell proteins TIA-1 and TIAR interact with the 3′ stem-loop of the West Nile virus complementary minus-strand RNA and facilitate virus replication. J. Virol. 76:11989–2000 [Google Scholar]
  80. Katoh H, Okamoto T, Fukuhara T, Kambara H, Morita E. 80.  et al. 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 [Google Scholar]
  81. Pager CT, Schütz S, Abraham TM, Luo G, Sarnow P. 81.  2013. Modulation of hepatitis C virus RNA abundance and virus release by dispersion of processing bodies and enrichment of stress granules. Virology 435:472–84 [Google Scholar]
  82. Ariumi Y, Kuroki M, Kushima Y, Osugi K, Hijikata M. 82.  et al. 2011. Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J. Virol. 85:6882–92 [Google Scholar]
  83. Garaigorta U, Heim MH, Boyd B, Wieland S, Chisari FV. 83.  2012. Hepatitis C virus induces the formation of stress granules whose proteins regulate HCV RNA replication, virus assembly and egress. J. Virol. 86:11043–56 [Google Scholar]
  84. Yi Z, Pan T, Wu X, Song W, Wang S. 84.  et al. 2011. Hepatitis C virus co-opts Ras-GTPase-activating protein–binding protein 1 for its genome replication. J. Virol. 85:6996–7004 [Google Scholar]
  85. Abrahamyan LG, Chatel-Chaix L, Ajamian L, Milev MP, Monette A. 85.  et al. 2010. Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J. Cell Sci. 123:369–83 [Google Scholar]
  86. Thomas MG, Tosar LJM, Desbats MA, Leishman CC, Boccaccio GL. 86.  2009. Mammalian Staufen 1 is recruited to stress granules and impairs their assembly. J. Cell Sci. 122:563–73 [Google Scholar]
  87. Legros S, Boxus M, Gatot JS, Van Lint C, Kruys V. 87.  et al. 2011. The HTLV-1 Tax protein inhibits formation of stress granules by interacting with histone deacetylase 6. Oncogene 30:4050–62 [Google Scholar]
  88. Kwon S, Zhang Y, Matthias P. 88.  2007. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 21:3381–94 [Google Scholar]
  89. Takahashi M, Higuchi M, Makokha GN, Matsuki H, Yoshita M. 89.  et al. 2013. HTLV-1 Tax oncoprotein stimulates ROS production and apoptosis in T cells by interacting with USP10. Blood 122:715–25 [Google Scholar]
  90. Linero FN, Thomas MG, Boccaccio GL, Scolaro LA. 90.  2011. Junin virus infection impairs stress-granule formation in Vero cells treated with arsenite via inhibition of eIF2α phosphorylation. J. Virol. 92:2889–99 [Google Scholar]
  91. Baird NL, York J, Nunberg JH. 91.  2012. Arenavirus infection induces discrete cytosolic structures for RNA replication. J. Virol. 86:11301–10 [Google Scholar]
  92. Pfaller CK, Li Z, George CX, Samuel CE. 92.  2011. Protein kinase PKR and RNA adenosine deaminase ADAR1: new roles for old players as modulators of the interferon response. Curr. Opin. Immunol. 23:573–82 [Google Scholar]
  93. Dinh PX, Beura LK, Das PB, Panda D, Das A, Pattnaik AK. 93.  2013. Induction of stress granule–like structures in vesicular stomatitis virus–infected cells. J. Virol. 87:372–83 [Google Scholar]
  94. Lindquist ME, Mainou BA, Dermody TS, Crowe JE. 94.  2011. Activation of protein kinase R is required for induction of stress granules by respiratory syncytial virus but dispensable for viral replication. Virology 413:103–10 [Google Scholar]
  95. Lindquist ME, Lifland AW, Utley TJ, Santangelo PJ, Crowe JE. 95.  2010. Respiratory syncytial virus induces host RNA stress granules to facilitate viral replication. J. Virol. 84:12274–84 [Google Scholar]
  96. Hanley LL, McGivern DR, Teng MN, Djang R, Collins PL, Fearns R. 96.  2010. Roles of the respiratory syncytial virus trailer region: effects of mutations on genome production and stress granule formation. Virology 406:241–52 [Google Scholar]
  97. Iseni F, Garcin D, Nishio M, Kedersha N, Anderson P, Kolakofsky D. 97.  2002. Sendai virus trailer RNA binds TIAR, a cellular protein involved in virus-induced apoptosis. EMBO J. 21:5141–50 [Google Scholar]
  98. Katsafanas GC, Moss B. 98.  2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2:221–28 [Google Scholar]
  99. Katsafanas GC, Moss B. 99.  2004. Vaccinia virus intermediate stage transcription is complemented by Ras-GTPase-activating protein SH3 domain–binding protein (G3BP) and cytoplasmic activation/proliferation–associated protein (p137) individually or as a heterodimer. J. Biol. Chem. 279:52210–17 [Google Scholar]
  100. Zaborowska I, Kellner K, Henry M, Meleady P, Walsh D. 100.  2012. Recruitment of host translation initiation factor eIF4G by the vaccinia virus ssDNA-binding protein I3. Virology 425:11–22 [Google Scholar]
  101. Walsh D, Arias C, Perez C, Halladin D, Escandon M. 101.  et al. 2008. Eukaryotic translation initiation factor 4F architectural alterations accompany translation initiation factor redistribution in poxvirus-infected cells. Mol. Cell. Biol. 28:2648–58 [Google Scholar]
  102. Simpson-Holley M, Kedersha N, Dower K, Rubins KH, Anderson P. 102.  et al. 2011. Formation of antiviral cytoplasmic granules during orthopoxvirus infection. J. Virol. 85:1581–93 [Google Scholar]
  103. Dougherty JD, White JP, Lloyd RE. 103.  2011. Poliovirus-mediated disruption of cytoplasmic processing bodies. J. Virol. 85:64–75 [Google Scholar]
  104. Zheng D, Ezzeddine N, Chen CYA, Zhu W, He X, Shyu AB. 104.  2008. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J. Cell Biol. 182:89–101 [Google Scholar]
  105. Rzeczkowski K, Beuerlein K, Müller H, Dittrich-Breiholz O, Schneider H. 105.  et al. 2011. c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies. J. Cell Biol. 194:581–96 [Google Scholar]
  106. Aizer A, Brody Y, Ler LW, Sonenberg N, Singer RH, Shav-Tal Y. 106.  2008. The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol. Biol. Cell 19:4154–66 [Google Scholar]
  107. Greer AE, Hearing P, Ketner G. 107.  2011. The adenovirus E4 11k protein binds and relocalizes the cytoplasmic P-body component Ddx6 to aggresomes. Virology 417:161–68 [Google Scholar]
  108. Chahar HS, Chen S, Manjunath N. 108.  2013. P-body components LSM1, GW182, DDX3, DDX6 and XRN1 are recruited to WNV replication sites and positively regulate viral replication. Virology 436:1–7 [Google Scholar]
  109. Ward AM, Bidet K, Yinglin A, Ler SG, Hogue K. 109.  et al. 2011. Quantitative mass spectrometry of DENV-2 RNA-interacting proteins reveals that the DEAD-box RNA helicase DDX6 binds the DB1 and DB2 3′ UTR structures. RNA Biol. 8:1173–86 [Google Scholar]
  110. Ernoult-Lange M, Baconnais S, Harper M, Minshall N, Souquere S. 110.  et al. 2012. Multiple binding of repressed mRNAs by the P-body protein Rck/p54. RNA 18:1702–15 [Google Scholar]
  111. Silva PAGC, Pereira CF, Dalebout TJ, Spaan WJM, Bredenbeek PJ. 111.  2010. An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J. Virol. 84:11395–406 [Google Scholar]
  112. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S. 112.  et al. 2008. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579–91 [Google Scholar]
  113. Moon SL, Anderson JR, Kumagai Y, Wilusz CJ, Akira S. 113.  et al. 2012. A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability. RNA 18:2029–40 [Google Scholar]
  114. Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C. 114.  et al. 2012. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86:13486–500 [Google Scholar]
  115. Angus AGN, Dalrymple D, Boulant S, McGivern DR, Clayton RF. 115.  et al. 2010. Requirement of cellular DDX3 for hepatitis C virus replication is unrelated to its interaction with the viral core protein. J. Gen. Virol. 91:122–32 [Google Scholar]
  116. Mamiya N, Worman HJ. 116.  1999. Hepatitis C virus core protein binds to a DEAD box RNA helicase. J. Biol. Chem. 274:15751–56 [Google Scholar]
  117. You LR, Chen CM, Yeh TS, Tsai TY, Mai RT. 117.  et al. 1999. Hepatitis C virus core protein interacts with cellular putative RNA helicase. J. Virol. 73:2841–53 [Google Scholar]
  118. Ariumi Y, Kuroki M, Abe KI, Dansako H, Ikeda M. 118.  et al. 2007. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J. Virol. 81:13922–26 [Google Scholar]
  119. Yu SF, Lujan P, Jackson DL, Emerman M, Linial ML. 119.  2011. The DEAD-box RNA helicase DDX6 is required for efficient encapsidation of a retroviral genome. PLoS Pathog. 7:e1002303 [Google Scholar]
  120. Scheller N, Mina LB, Galão RP, Chari A, Giménez-Barcons M. 120.  et al. 2009. Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates. Proc. Natl. Acad. Sci. USA 106:13517–22 [Google Scholar]
  121. Jangra RK, Yi M, Lemon SM. 121.  2010. DDX6 (Rck/p54) is required for efficient hepatitis C virus replication but not for internal ribosome entry site–directed translation. J. Virol. 84:6810–24 [Google Scholar]
  122. Berezhna SY, Supekova L, Sever MJ, Schultz PG, Deniz AA. 122.  2011. Dual regulation of hepatitis C viral RNA by cellular RNAi requires partitioning of Ago2 to lipid droplets and P-bodies. RNA 17:1831–45 [Google Scholar]
  123. Huys A, Thibault PA, Wilson JA. 123.  2013. Modulation of hepatitis C virus RNA accumulation and translation by DDX6 and miR-122 are mediated by separate mechanisms. PLoS ONE 8:e67437 [Google Scholar]
  124. Roberts APE, Lewis AP, Jopling CL. 124.  2011. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res. 39:7716–29 [Google Scholar]
  125. Pérez-Vilaró G, Scheller N, Saludes V, Díez J. 125.  2012. Hepatitis C virus infection alters P-body composition but is independent of P-body granules. J. Virol. 86:8740–49 [Google Scholar]
  126. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT. 126.  2008. Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc. Natl. Acad. Sci. USA 105:19294–99 [Google Scholar]
  127. Mir MA, Panganiban AT. 127.  2008. A protein that replaces the entire cellular eIF4F complex. EMBO J. 27:3129–39 [Google Scholar]
  128. Noueiry AO, Díez J, Falk SP, Chen J, Ahlquist P. 128.  2003. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol. Cell. Biol. 23:4094–106 [Google Scholar]
  129. Beckham CJ, Light HR, Nissan TA, Ahlquist P, Parker R, Noueiry A. 129.  2007. Interactions between brome mosaic virus RNAs and cytoplasmic processing bodies. J. Virol. 81:9759–68 [Google Scholar]
  130. Wang X, Lee WM, Watanabe T, Schwartz M, Janda M, Ahlquist P. 130.  2005. Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J. Virol. 79:13747–58 [Google Scholar]
  131. Yasuda-Inoue M, Kuroki M, Ariumi Y. 131.  2013. DDX3 RNA helicase is required for HIV-1 Tat function. Biochem. Biophys. Res. Commun. 441:607–11 [Google Scholar]
  132. Izumi T, Burdick R, Shigemi M, Plisov S, Hu WS, Pathak VK. 132.  2013. Mov10 and APOBEC3G localization to processing bodies is not required for virion incorporation and antiviral activity. J. Virol. 87:11047–62 [Google Scholar]
  133. Phalora PK, Sherer NM, Wolinsky SM, Swanson CM, Malim MH. 133.  2012. HIV-1 replication and APOBEC3 antiviral activity are not regulated by P bodies. J. Virol. 86:11712–24 [Google Scholar]
  134. Lu C, Contreras X, Peterlin BM. 134.  2011. P bodies inhibit retrotransposition of endogenous intracisternal A particles. J. Virol. 85:6244–51 [Google Scholar]
  135. Lu C, Luo Z, Jäger S, Krogan NJ, Peterlin BM. 135.  2012. Moloney leukemia virus type 10 inhibits reverse transcription and retrotransposition of intracisternal A particles. J. Virol. 86:10517–23 [Google Scholar]
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Supplemental Material

    Virus-induced stress granules () forming in cells infected with coxsackievirus B3 that produces dsRed fluorescent protein as a marker of robust replication. HEK cells are expressing Tia1-GFP () as a marker for stress granules, which translocates from the nucleus to cytoplasm as infection initiates. Expression of Tia1-GFP makes the cells more prone to stress granule formation, which generally delays or inhibits coxsackievirus B3 replication. In other infected cells, stress granules shrink or disperse after they appear, or they persist as residual pseudo–stress granules that no longer contain stalled translation complexes.

  • Article Type: Review Article
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