Virus-induced translational arrest through 4EBP1/2-dependent decay of 5′-TOP mRNAs restricts viral infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 22, 2015, Pages E2920-E2929

  Hopkins, Kaycie C ^a,c   Tartell, Michael A ^a   Herrmann, Christin ^a   Hackett, Brent A ^a   Taschuk, Frances ^a   Panda, Debasis ^a   Menghani, Sanjay V ^a   Sabin, Leah R ^b   Cherry, Sara ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

5 TOP mRNA; Rift Valley fever virus; RNA decay; RNA granule; Translational arrest

Indexed keywords

ENZYME; INITIATION FACTOR 4E BINDING PROTEIN 1; INTERFERON; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; NUDT16 ENZYME; PROTEIN KINASE R; RIBOSOME PROTEIN; RNA; UNCLASSIFIED DRUG; EIF4EBP1 PROTEIN, HUMAN; INORGANIC PYROPHOSPHATASE; LUCIFERASE; MTOR PROTEIN, HUMAN; NUDT16 PROTEIN, HUMAN; PHOSPHOPROTEIN; PRIMER DNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TARGET OF RAPAMYCIN KINASE;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; RNA TRANSLATION; SIGNAL TRANSDUCTION; TERMINAL OLIGOPYRIMIDINE TRACT; VIRUS REPLICATION; XENOPHAGY; CELL LINE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL MODEL;

ORTHOBUNYAVIRUS; RIFT VALLEY FEVER VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; LINEAR MODELS; LUCIFERASES; PHOSPHOPROTEINS; PROTEIN BIOSYNTHESIS; PYROPHOSPHATASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; RNA 5' TERMINAL OLIGOPYRIMIDINE SEQUENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES;

EID: 84930622945     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418805112     Document Type: Article

References (75)

1. Diamond MS, Farzan M (2013) The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13(1):46-57.
2. Kaufman RJ (1999) Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: A new role for an old actor. Proc Natl Acad Sci USA 96(21):11693-11695.
3. Wek RC, Jiang HY, Anthony TG (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34(Pt 1):7-11.
4. Lancaster AM, Jan E, Sarnow P (2006) Initiation factor-independent translation mediated by the hepatitis C virus internal ribosome entry site. RNA 12(5):894-902.
5. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6(4):318-327.
6. Keene JD (2007) RNA regulons: Coordination of post-transcriptional events. Nat Rev Genet 8(7):533-543.
7. Wang Y, et al. (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 99(9):5860-5865.
8. Marzluff WF, Wagner EJ, Duronio RJ (2008) Metabolism and regulation of canonical histone mRNAs: Life without a poly(A) tail. Nat Rev Genet 9(11):843-854.
9. Ikegami T, et al. (2009) Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog 5(2):e1000287.
10. Billecocq A, et al. (2004) NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J Virol 78(18):9798-9806.
11. Mir MA, Sheema S, Haseeb A, Haque A (2010) Hantavirus nucleocapsid protein has distinct m7G cap- and RNA-binding sites. J Biol Chem 285(15):11357-11368.
12. Patterson JLJ, Holloway B, Kolakofsky D (1984) La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol 52(1):215-222.
13. Reguera J, Weber F, Cusack S (2010) Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog 6(9):e1001101.
14. Simons JF, Pettersson RF (1991) Host-derived 5′ ends and overlapping complementary 3′ ends of the two mRNAs transcribed from the ambisense S segment of Uukuniemi virus. J Virol 65(9):4741-4748.
15. Daffis S, et al. (2010) 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468(7322):452-456.
16. Hopkins KC, et al. (2013) A genome-wide RNAi screen reveals that mRNA decapping restricts bunyaviral replication by limiting the pools of Dcp2-accessible targets for cap-snatching. Genes Dev 27(13):1511-1525.
17. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT (2008) Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci USA 105(49):19294-19299.
18. Meyuhas O (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267(21):6321-6330.
19. Jefferies HB, Reinhard C, Kozma SC, Thomas G (1994) Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc Natl Acad Sci USA 91(10):4441-4445.
20. Iadevaia V, Caldarola S, Tino E, Amaldi F, Loreni F (2008) All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5′-terminal oligopyrimidine (TOP) mRNAs. RNA 14(9):1730-1736.
21. Avni D, Biberman Y, Meyuhas O (1997) The 5′ terminal oligopyrimidine tract confers translational control on TOP mRNAs in a cell type- and sequence context-dependent manner. Nucleic Acids Res 25(5):995-1001.
22. Tang H, et al. (2001) Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol Cell Biol 21(24):8671-8683.
23. Thoreen CC, et al. (2012) A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485(7396):109-113.
24. Colina R, et al. (2008) Translational control of the innate immune response through IRF-7. Nature 452(7185):323-328.
25. Damgaard CK, Lykke-Andersen J (2011) Translational coregulation of 5′TOP mRNAs by TIA-1 and TIAR. Genes Dev 25(19):2057-2068.
26. Thomas MG, Loschi M, Desbats MA, Boccaccio GL (2011) RNA granules: The good, the bad and the ugly. Cell Signal 23(2):324-334.
27. Brennan B, Welch SR, Elliott RM (2014) The consequences of reconfiguring the ambisense S genome segment of Rift Valley fever virus on viral replication in mammalian and mosquito cells and for genome packaging. PLoS Pathog 10(2):e1003922.
28. Sharova LV, et al. (2009) Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 16(1):45-58.
29. Moy RH, et al. (2014) Antiviral autophagy restricts Rift Valley fever virus infection and is conserved from flies to mammals. Immunity 40(1):51-65.
30. Constantinou C, Elia A, Clemens MJ (2008) Activation of p53 stimulates proteasome-dependent truncation of eIF4E-binding protein 1 (4E-BP1). Biol Cell 100(5):279-289.
31. Elia A, Constantinou C, Clemens MJ (2008) Effects of protein phosphorylation on ubiquitination and stability of the translational inhibitor protein 4E-BP1. Oncogene 27(6):811-822.
32. Mohr I, Sonenberg N (2012) Host translation at the nexus of infection and immunity. Cell Host Microbe 12(4):470-483.
33. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R (2005) Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11(4):371-382.
34. Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E (2007) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 27(11):3970-3981.
35. Kedersha N, et al. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169(6):871-884.
36. Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25(5):635-646.
37. Emara MM, et al. (2012) Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem Biophys Res Commun 423(4):763-769.
38. Dougherty JD, White JP, Lloyd RE (2011) Poliovirus-mediated disruption of cytoplasmic processing bodies. J Virol 85(1):64-75.
39. Kedersha N, et al. (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151(6):1257-1268.
40. van Dijk E, et al. (2002) Human Dcp2: A catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21(24):6915-6924.
41. Song M-G, Li Y, Kiledjian M (2010) Multiple mRNA decapping enzymes in mammalian cells. Mol Cell 40(3):423-432.
42. Li Y, Song MG, Kiledjian M (2008) Transcript-specific decapping and regulated stability by the human Dcp2 decapping protein. Mol Cell Biol 28(3):939-948.
43. Li Y, Dai J, Song M, Fitzgerald-Bocarsly P, Kiledjian M (2012) Dcp2 decapping protein modulates mRNA stability of the critical interferon regulatory factor (IRF) IRF-7. Mol Cell Biol 32(6):1164-1172.
44. Li Y, Song M, Kiledjian M (2011) Differential utilization of decapping enzymes in mammalian mRNA decay pathways. RNA 17(3):419-428.
45. Tritschler F, et al. (2009) DCP1 forms asymmetric trimers to assemble into active mRNA decapping complexes in metazoa. Proc Natl Acad Sci USA 106(51):21591-21596.
46. Bouloy M, Pardigon N, Vialat P, Gerbaud S, Girard M (1990) Characterization of the 5′ and 3′ ends of viral messenger RNAs isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology 175(1):50-58.
47. Hirsch CA, Hiatt HH (1966) Turnover of liver ribosomes in fed and in fasted rats. J Biol Chem 241(24):5936-5940.
48. Lam YW, Lamond AI, Mann M, Andersen JS (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 17(9):749-760.
49. Jouffe C, et al. (2013) The circadian clock coordinates ribosome biogenesis. PLoS Biol 11(1):e1001455.
50. Huch S, Nissan T (2014) Interrelations between translation and general mRNA degradation in yeast. Wiley Interdiscip Rev RNA 5(6):747-763.
51. Won S, Ikegami T, Peters CJ, Makino S (2007) NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol 81(24):13335-13345.
52. Chawla-Sarkar M, et al. (2003) Apoptosis and interferons: Role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8(3):237-249.
53. Gil J, Esteban M (2000) Induction of apoptosis by the dsRNA-dependent protein kinase (PKR): Mechanism of action. Apoptosis 5(2):107-114.
54. Moon SL, Barnhart MD, Wilusz J (2012) Inhibition and avoidance of mRNA degradation by RNA viruses. Curr Opin Microbiol 15(4):500-505.
55. Reineke LC, Lloyd RE (2013) Diversion of stress granules and P-bodies during viral infection. Virology 436(2):255-267.
56. Emara MM, Brinton MA (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(21):9041-9046.
57. Chahar HS, Chen S, Manjunath N (2013) P-body components LSM1, GW182, DDX3, DDX6 and XRN1 are recruited to WNV replication sites and positively regulate viral replication. Virology 436(1):1-7.
58. Pager CT, Schütz S, Abraham TM, Luo G, Sarnow P (2013) Modulation of hepatitis C virus RNA abundance and virus release by dispersion of processing bodies and enrichment of stress granules. Virology 435(2):472-484.
59. Kwong AD, Kruper JA, Frenkel N (1988) Herpes simplex virus virion host shutoff function. J Virol 62(3):912-921.
60. Rowe M, et al. (2007) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci USA 104(9):3366-3371.
61. Glaunsinger B, Ganem D (2004) Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol Cell 13(5):713-723.
62. Kamitani W, et al. (2006) Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci USA 103(34):12885-12890.
63. Cheng E, Mir MA (2012) Signatures of host mRNA 5′ terminus for efficient hantavirus cap snatching. J Virol 86(18):10173-10185.
64. Ptushkina M, et al. (1998) Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20. EMBO J 17(16):4798-4808.
65. Mir MA, Panganiban AT (2008) A protein that replaces the entire cellular eIF4F complex. EMBO J 27(23):3129-3139.
66. Tsalikis J, Croitoru DO, Philpott DJ, Girardin SE (2013) Nutrient sensing and metabolic stress pathways in innate immunity. Cell Microbiol 15(10):1632-1641.
67. Brunton J, Steele S, Ziehr B, Moorman N, Kawula T (2013) Feeding uninvited guests: mTOR and AMPK set the table for intracellular pathogens. PLoS Pathog 9(10):e1003552.
68. Carpenter S, Ricci EP, Mercier BC, Moore MJ, Fitzgerald KA (2014) Post-transcriptional regulation of gene expression in innate immunity. Nat Rev Immunol 14(6):361-376.
69. Morita M, et al. (2013) mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation. Cell Metab 18(5):698-711.
70. Moser TS, Jones RG, Thompson CB, Coyne CB, Cherry S (2010) A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog 6(6):e1000954.
71. Petersen J, et al. (2014) The major cellular sterol regulatory pathway is required for Andes virus infection. PLoS Pathog 10(2):e1003911.
72. Filone CM, et al. (2010) Rift valley fever virus infection of human cells and insect hosts is promoted by protein kinase C epsilon. PLoS One 5(11):e15483.
73. Rose PP, et al. (2011) Natural resistance-associated macrophage protein is a cellular receptor for sindbis virus in both insect and mammalian hosts. Cell Host Microbe 10(2):97-104.
74. Cherry S, et al. (2005) Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev 19(4):445-452.
75. Xu J, et al. (2012) Transcriptional pausing controls a rapid antiviral innate immune response in Drosophila. Cell Host Microbe 12(4):531-543.