Interplay between viruses and host mRNA degradation

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 6-7, 2013, Pages 732-741

  Narayanan, Krishna ^a   Makino, Shinji ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Deadenylation; Decapping; Endonuclease; MRNA decay pathways; RNase L; Viruses

Indexed keywords

5' 7 METHYLGUANOSINE; ARGONAUTE PROTEIN; EXORIBONUCLEASE; GUANOSINE DERIVATIVE; INITIATION FACTOR 4E; MESSENGER RNA; POLYADENYLIC ACID; RIBONUCLEASE L; RNA INDUCED SILENCING COMPLEX; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; DOWN REGULATION; ENZYME ACTIVITY; EUKARYOTIC CELL; GENE EXPRESSION; IMMUNE EVASION; LATENT PERIOD; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; RNA DEGRADATION; RNA INTERFERENCE; RNA METABOLISM; RNA STABILITY; RNA VIRUS; VIRUS CELL INTERACTION;

ENDONUCLEASES; EXORIBONUCLEASES; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INFECTION; RNA STABILITY; RNA, MESSENGER; VIRUSES;

EID: 84877821861     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.12.003     Document Type: Review

References (143)

1. Komili S., Silver P.A. Coupling and coordination in gene expression processes: a systems biology view. Nat. Rev. Genet. 2008, 9:38-48.
2. Munchel S.E., Shultzaberger R.K., Takizawa N., Weis K. Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol. Biol. Cell 2011, 22:2787-2795.
3. Sachs A.B. Messenger RNA degradation in eukaryotes. Cell 1993, 74:413-421.
4. Schwanhausser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
5. Behm-Ansmant I., Kashima I., Rehwinkel J., Sauliere J., Wittkopp N., Izaurralde E. mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 2007, 581:2845-2853.
6. Doma M.K., Parker R. RNA quality control in eukaryotes. Cell 2007, 131:660-668.
7. Fasken M.B., Corbett A.H. Process or perish: quality control in mRNA biogenesis. Nat. Struct. Mol. Biol. 2005, 12:482-488.
8. Rehwinkel J., Raes J., Izaurralde E. Nonsense-mediated mRNA decay: target genes and functional diversification of effectors. Trends Biochem. Sci. 2006, 31:639-646.
9. Garneau N.L., Wilusz J., Wilusz C.J. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 2007, 8:113-126.
10. Parker R., Song H. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 2004, 11:121-127.
11. Schoenberg D.R., Maquat L.E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 2012, 13:246-259.
12. Wu X., Brewer G. The regulation of mRNA stability in mammalian cells: 2.0. Gene 2012, 500:10-21.
13. Silverman R.H. Viral encounters with 2', 5'-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 2007, 81:12720-12729.
14. Darnell J.E. Transcription units for mRNA production in eukaryotic cells and their DNA viruses. Prog. Nucleic Acid Res. Mol. Biol. 1979, 22:327-353.
15. Moore M.J., Proudfoot N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009, 136:688-700.
16. Shatkin A.J. Capping of eucaryotic mRNAs. Cell 1976, 9:645-653.
17. Bernstein P., Peltz S.W., Ross J. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol. Cell. Biol. 1989, 9:659-670.
18. Filipowicz W., Furuichi Y., Sierra J.M., Muthukrishnan S., Shatkin A.J., Ochoa S. A protein binding the methylated 5'-terminal sequence, m7GpppN, of eukaryotic messenger RNA. Proc. Natl. Acad. Sci. U. S. A. 1976, 73:1559-1563.
19. Decker C.J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 1993, 7:1632-1643.
20. Chen C.Y., Shyu A.B. Mechanisms of deadenylation-dependent decay. Wiley Interdiscip. Rev. RNA 2010, 2:167-183.
21. Goldstrohm A.C., Wickens M. Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 2008, 9:337-344.
22. Houseley J., LaCava J., Tollervey D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
23. Lykke-Andersen S., Tomecki R., Jensen T.H., Dziembowski A. The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol. 2011, 8:61-66.
24. Liu H., Rodgers N.D., Jiao X., Kiledjian M. The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J. 2002, 21:4699-4708.
25. Wang Z., Kiledjian M. Functional link between the mammalian exosome and mRNA decapping. Cell 2001, 107:751-762.
26. Song M.G., Li Y., Kiledjian M. Multiple mRNA decapping enzymes in mammalian cells. Mol. Cell 2010, 40:423-432.
27. Hsu C.L., Stevens A. Yeast cells lacking 5'→3' exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5' cap structure. Mol. Cell. Biol. 1993, 13:4826-4835.
28. Tomecki R., Dziembowski A. Novel endoribonucleases as central players in various pathways of eukaryotic RNA metabolism. RNA 2010, 16:1692-1724.
29. Zhu Y., Gao G. ZAP-mediated mRNA degradation. RNA Biol. 2008, 5:65-67.
30. Xuan Y., Liu L., Shen S., Deng H., Gao G. Zinc finger antiviral protein inhibits murine gammaherpesvirus 68 m2 expression and regulates viral latency in cultured cells. J. Virol. 2012, 86:12431-12434.
31. Zhu Y., Wang X., Goff S.P., Gao G. Translational repression precedes and is required for ZAP-mediated mRNA decay. EMBO J. 2012, 31:4236-4246.
32. Chang Y.F., Imam J.S., Wilkinson M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 2007, 76:51-74.
33. Huntzinger E., Kashima I., Fauser M., Sauliere J., Izaurralde E. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 2008, 14:2609-2617.
34. Frischmeyer P.A., van Hoof A., O'Donnell K., Guerrerio A.L., Parker R., Dietz H.C. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 2002, 295:2258-2261.
35. van Hoof A., Frischmeyer P.A., Dietz H.C., Parker R. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 2002, 295:2262-2264.
36. Huntzinger E., Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 2011, 12:99-110.
37. Sheth U., Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003, 300:805-808.
38. Eulalio A., Behm-Ansmant I., Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 2007, 8:9-22.
39. Brengues M., Teixeira D., Parker R. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 2005, 310:486-489.
40. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 2008, 33:141-150.
41. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
42. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M.J., Scheuner D., Kaufman R.J., Golan D.E., Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 2005, 169:871-884.
43. Nallagatla S.R., Toroney R., Bevilacqua P.C. A brilliant disguise for self RNA: 5'-end and internal modifications of primary transcripts suppress elements of innate immunity. RNA Biol. 2008, 5:140-144.
44. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., Reis e Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314:997-1001.
45. Rehwinkel J., Tan C.P., Goubau D., Schulz O., Pichlmair A., Bier K., Robb N., Vreede F., Barclay W., Fodor E., Reis e Sousa C. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010, 140:397-408.
46. Daffis S., Szretter K.J., Schriewer J., Li J., Youn S., Errett J., Lin T.Y., Schneller S., Zust R., Dong H., Thiel V., Sen G.C., Fensterl V., Klimstra W.B., Pierson T.C., Buller R.M., Gale M., Shi P.Y., Diamond M.S. 2'-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 2010, 468:452-456.
47. Zust R., Cervantes-Barragan L., Habjan M., Maier R., Neuman B.W., Ziebuhr J., Szretter K.J., Baker S.C., Barchet W., Diamond M.S., Siddell S.G., Ludewig B., Thiel V. Ribose 2'-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 2011, 12:137-143.
48. Decroly E., Ferron F., Lescar J., Canard B. Conventional and unconventional mechanisms for capping viral mRNA. Nat. Rev. Microbiol. 2012, 10:51-65.
49. Koonin E.V., Moss B. Viruses know more than one way to don a cap. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3283-3284.
50. Fujimura T., Esteban R. Cap-snatching mechanism in yeast L-A double-stranded RNA virus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17667-17671.
51. Naitow H., Tang J., Canady M., Wickner R.B., Johnson J.E. L-A virus at 3.4 A resolution reveals particle architecture and mRNA decapping mechanism. Nat. Struct. Biol. 2002, 9:725-728.
52. Dias A., Bouvier D., Crepin T., McCarthy A.A., Hart D.J., Baudin F., Cusack S., Ruigrok R.W. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009, 458:914-918.
53. Guilligay D., Tarendeau F., Resa-Infante P., Coloma R., Crepin T., Sehr P., Lewis J., Ruigrok R.W., Ortin J., Hart D.J., Cusack S. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol. 2008, 15:500-506.
54. Yuan P., Bartlam M., Lou Z., Chen S., Zhou J., He X., Lv Z., Ge R., Li X., Deng T., Fodor E., Rao Z., Liu Y. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 2009, 458:909-913.
55. Morin B., Coutard B., Lelke M., Ferron F., Kerber R., Jamal S., Frangeul A., Baronti C., Charrel R., de Lamballerie X., Vonrhein C., Lescar J., Bricogne G., Gunther S., Canard B. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog. 2010, 6:e1001038.
56. Reguera J., Weber F., Cusack S. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog. 2010, 6:e1001101.
57. Mir M.A., Duran W.A., Hjelle B.L., Ye C., Panganiban A.T. Storage of cellular 5' mRNA caps in P bodies for viral cap-snatching. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19294-19299.
58. Fujimura T., Esteban R. Cap snatching of yeast L-A double-stranded RNA virus can operate in trans and requires viral polymerase actively engaging in transcription. J. Biol. Chem. 2012, 287:12797-12804.
59. Martinez-Salas E., Pacheco A., Serrano P., Fernandez N. New insights into internal ribosome entry site elements relevant for viral gene expression. J. Gen. Virol. 2008, 89:611-626.
60. Balvay L., Soto Rifo R., Ricci E.P., Decimo D., Ohlmann T. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta 2009, 1789:542-557.
61. Ford L.P., Wilusz J. 3'-Terminal RNA structures and poly(U) tracts inhibit initiation by a 3'→5' exonuclease in vitro. Nucleic Acids Res. 1999, 27:1159-1167.
62. Brinton M.A., Fernandez A.V., Dispoto J.H. The 3'-nucleotides of flavivirus genomic RNA form a conserved secondary structure. Virology 1986, 153:113-121.
63. Geerts-Dimitriadou C., Lu Y.Y., Geertsema C., Goldbach R., Kormelink R. Analysis of the Tomato spotted wilt virus ambisense S RNA-encoded hairpin structure in translation. PLoS One 2012, 7:e31013.
64. Meyer B.J., Southern P.J. Concurrent sequence analysis of 5' and 3' RNA termini by intramolecular circularization reveals 5' nontemplated bases and 3' terminal heterogeneity for lymphocytic choriomeningitis virus mRNAs. J. Virol. 1993, 67:2621-2627.
65. Eberle A.B., Stalder L., Mathys H., Orozco R.Z., Muhlemann O. Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PLoS Biol. 2008, 6:e92.
66. Hogg J.R., Goff S.P. Upf1 senses 3'UTR length to potentiate mRNA decay. Cell 2010, 143:379-389.
67. Weil J.E., Hadjithomas M., Beemon K.L. Structural characterization of the Rous sarcoma virus RNA stability element. J. Virol. 2009, 83:2119-2129.
68. Han J.Q., Townsend H.L., Jha B.K., Paranjape J.M., Silverman R.H., Barton D.J. A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. J. Virol. 2007, 81:5561-5572.
69. Townsend H.L., Jha B.K., Han J.Q., Maluf N.K., Silverman R.H., Barton D.J. A viral RNA competitively inhibits the antiviral endoribonuclease domain of RNase L. RNA 2008, 14:1026-1036.
70. Washenberger C.L., Han J.Q., Kechris K.J., Jha B.K., Silverman R.H., Barton D.J. Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res. 2007, 130:85-95.
71. Han J.Q., Barton D.J. Activation and evasion of the antiviral 2'-5' oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA 2002, 8:512-525.
72. Abdelmohsen K., Gorospe M. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip. Rev. RNA 2010, 1:214-229.
73. Harris D., Zhang Z., Chaubey B., Pandey V.N. Identification of cellular factors associated with the 3'-nontranslated region of the hepatitis C virus genome. Mol. Cell. Proteomics 2006, 5:1006-1018.
74. Sokoloski K.J., Dickson A.M., Chaskey E.L., Garneau N.L., Wilusz C.J., Wilusz J. Sindbis virus usurps the cellular HuR protein to stabilize its transcripts and promote productive infections in mammalian and mosquito cells. Cell Host Microbe 2010, 8:196-207.
75. Korf M., Jarczak D., Beger C., Manns M.P., Kruger M. Inhibition of hepatitis C virus translation and subgenomic replication by siRNAs directed against highly conserved HCV sequence and cellular HCV cofactors. J. Hepatol. 2005, 43:225-234.
76. Rivas-Aravena A., Ramdohr P., Vallejos M., Valiente-Echeverria F., Dormoy-Raclet V., Rodriguez F., Pino K., Holzmann C., Huidobro-Toro J.P., Gallouzi I.E., Lopez-Lastra M. The Elav-like protein HuR exerts translational control of viral internal ribosome entry sites. Virology 2009, 392:178-185.
77. Garneau N.L., Sokoloski K.J., Opyrchal M., Neff C.P., Wilusz C.J., Wilusz J. The 3' untranslated region of sindbis virus represses deadenylation of viral transcripts in mosquito and Mammalian cells. J. Virol. 2008, 82:880-892.
78. Makeyev A.V., Liebhaber S.A. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 2002, 8:265-278.
79. Fukushi S., Okada M., Kageyama T., Hoshino F.B., Nagai K., Katayama K. Interaction of poly(rC)-binding protein 2 with the 5'-terminal stem loop of the hepatitis C-virus genome. Virus Res. 2001, 73:67-79.
80. Ogram S.A., Spear A., Sharma N., Flanegan J.B. The 5'CL-PCBP RNP complex, 3' poly(A) tail and 2A(pro) are required for optimal translation of poliovirus RNA. Virology 2010, 397:14-22.
81. Spear A., Sharma N., Flanegan J.B. Protein-RNA tethering: the role of poly(C) binding protein 2 in poliovirus RNA replication. Virology 2008, 374:280-291.
82. Wang L., Jeng K.S., Lai M.M. Poly(C)-binding protein 2 interacts with sequences required for viral replication in the hepatitis C virus (HCV) 5' untranslated region and directs HCV RNA replication through circularizing the viral genome. J. Virol. 2011, 85:7954-7964.
83. Palusa S., Ndaluka C., Bowen R.A., Wilusz C.J., Wilusz J. The 3' untranslated region of the rabies virus glycoprotein mRNA specifically interacts with cellular PCBP2 protein and promotes transcript stability. PLoS One 2012, 7:e33561.
84. Dougherty J.D., White J.P., Lloyd R.E. Poliovirus-mediated disruption of cytoplasmic processing bodies. J. Virol. 2011, 85:64-75.
85. Kuyumcu-Martinez N.M., Joachims M., Lloyd R.E. Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J. Virol. 2002, 76:2062-2074.
86. White J.P., Cardenas A.M., Marissen W.E., Lloyd R.E. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2007, 2:295-305.
87. Emara M.M., Brinton M.A. 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. U. S. A. 2007, 104:9041-9046.
88. Mocquet V., Neusiedler J., Rende F., Cluet D., Robin J.P., Terme J.M., Duc Dodon M., Wittmann J., Morris C., Le Hir H., Ciminale V., Jalinot P. The human T-lymphotropic virus type 1 tax protein inhibits nonsense-mediated mRNA decay by interacting with INT6/EIF3E and UPF1. J. Virol. 2012, 86:7530-7543.
89. Marshall E.E., Bierle C.J., Brune W., Geballe A.P. Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J. Virol. 2009, 83:4112-4120.
90. Sanchez R., Mohr I. Inhibition of cellular 2'-5' oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 2007, 81:3455-3464.
91. Maitra R.K., McMillan N.A., Desai S., McSwiggen J., Hovanessian A.G., Sen G., Williams B.R., Silverman R.H. HIV-1 TAR RNA has an intrinsic ability to activate interferon-inducible enzymes. Virology 1994, 204:823-827.
92. Schroder H.C., Ugarkovic D., Wenger R., Reuter P., Okamoto T., Muller W.E. Binding of Tat protein to TAR region of human immunodeficiency virus type 1 blocks TAR-mediated activation of (2'-5')oligoadenylate synthetase. AIDS Res. Hum. Retroviruses 1990, 6:659-672.
93. SenGupta D.N., Silverman R.H. Activation of interferon-regulated, dsRNA-dependent enzymes by human immunodeficiency virus-1 leader RNA. Nucleic Acids Res. 1989, 17:969-978.
94. Zhao L., Jha B.K., Wu A., Elliott R., Ziebuhr J., Gorbalenya A.E., Silverman R.H., Weiss S.R. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 2012, 11:607-616.
95. Zhao L., Rose K.M., Elliott R., Van Rooijen N., Weiss S.R. Cell-type-specific type I interferon antagonism influences organ tropism of murine coronavirus. J. Virol. 2011, 85:10058-10068.
96. McLennan A.G. Decapitation: poxvirus makes RNA lose its head. Trends Biochem. Sci. 2007, 32:297-299.
97. Parrish S., Moss B. Characterization of a second vaccinia virus mRNA-decapping enzyme conserved in poxviruses. J. Virol. 2007, 81:12973-12978.
98. Parrish S., Resch W., Moss B. Vaccinia virus D10 protein has mRNA decapping activity, providing a mechanism for control of host and viral gene expression. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2139-2144.
99. Glaunsinger B.A., Ganem D.E. Messenger RNA turnover and its regulation in herpesviral infection. Adv. Virus Res. 2006, 66:337-394.
100. Elgadi M.M., Hayes C.E., Smiley J.R. The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts. J. Virol. 1999, 73:7153-7164.
101. Kwong A.D., Frenkel N. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:1926-1930.
102. Oroskar A.A., Read G.S. Control of mRNA stability by the virion host shutoff function of herpes simplex virus. J. Virol. 1989, 63:1897-1906.
103. Doepker R.C., Hsu W.L., Saffran H.A., Smiley J.R. Herpes simplex virus virion host shutoff protein is stimulated by translation initiation factors eIF4B and eIF4H. J. Virol. 2004, 78:4684-4699.
104. Page H.G., Read G.S. The virion host shutoff endonuclease (UL41) of herpes simplex virus interacts with the cellular cap-binding complex eIF4F. J. Virol. 2010, 84:6886-6890.
105. Shiflett L.A., Read G.S. mRNA decay during herpes simplex virus (HSV) infections: mutations that affect translation of an mRNA influence the sites at which it is cleaved by the HSV virion host shutoff (Vhs) protein. J. Virol. 2013, 87:94-109.
106. Buisson M., Geoui T., Flot D., Tarbouriech N., Ressing M.E., Wiertz E.J., Burmeister W.P. A bridge crosses the active-site canyon of the Epstein-Barr virus nuclease with DNase and RNase activities. J. Mol. Biol. 2009, 391:717-728.
107. Glaunsinger B., Chavez L., Ganem D. The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable. J. Virol. 2005, 79:7396-7401.
108. Rowe M., Glaunsinger B., van Leeuwen D., Zuo J., Sweetman D., Ganem D., Middeldorp J., Wiertz E.J., Ressing M.E. Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3366-3371.
109. Covarrubias S., Gaglia M.M., Kumar G.R., Wong W., Jackson A.O., Glaunsinger B.A. Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. PLoS Pathog. 2011, 7:e1002339.
110. Gaglia M.M., Covarrubias S., Wong W., Glaunsinger B.A. A common strategy for host RNA degradation by divergent viruses. J. Virol. 2012, 86:9527-9530.
111. Kumar G.R., Glaunsinger B.A. Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol. Cell. Biol. 2010, 30:4996-5008.
112. Lee Y.J., Glaunsinger B.A. Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol. 2009, 7:e1000107.
113. Kamitani W., Narayanan K., Huang C., Lokugamage K., Ikegami T., Ito N., Kubo H., Makino S. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12885-12890.
114. Narayanan K., Huang C., Lokugamage K., Kamitani W., Ikegami T., Tseng C.T., Makino S. Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J. Virol. 2008, 82:4471-4479.
115. Huang C., Lokugamage K.G., Rozovics J.M., Narayanan K., Semler B.L., Makino S. SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog. 2011, 7:e1002433.
116. Kamitani W., Huang C., Narayanan K., Lokugamage K.G., Makino S. A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat. Struct. Mol. Biol. 2009, 16:1134-1140.
117. Lokugamage K.G., Narayanan K., Huang C., Makino S. SARS coronavirus nsp1 protein is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation. J. Virol. 2012, 86:13598-13608.
118. Hastie K.M., Kimberlin C.R., Zandonatti M.A., MacRae I.J., Saphire E.O. Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3' to 5' exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2396-2401.
119. Qi X., Lan S., Wang W., Schelde L.M., Dong H., Wallat G.D., Ly H., Liang Y., Dong C. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 2010, 468:779-783.
120. Tang J., Naitow H., Gardner N.A., Kolesar A., Tang L., Wickner R.B., Johnson J.E. The structural basis of recognition and removal of cellular mRNA 7-methyl G 'caps' by a viral capsid protein: a unique viral response to host defense. J. Mol. Recognit. 2005, 18:158-168.
121. Bergman N., Moraes K.C., Anderson J.R., Zaric B., Kambach C., Schneider R.J., Wilusz C.J., Wilusz J. Lsm proteins bind and stabilize RNAs containing 5' poly(A) tracts. Nat. Struct. Mol. Biol. 2007, 14:824-831.
122. Galao R.P., Chari A., Alves-Rodrigues I., Lobao D., Mas A., Kambach C., Fischer U., Diez J. LSm1-7 complexes bind to specific sites in viral RNA genomes and regulate their translation and replication. RNA 2010, 16:817-827.
123. Mas A., Alves-Rodrigues I., Noueiry A., Ahlquist P., Diez J. Host deadenylation-dependent mRNA decapping factors are required for a key step in brome mosaic virus RNA replication. J. Virol. 2006, 80:246-251.
124. Noueiry A.O., Diez J., Falk S.P., Chen J., Ahlquist P. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol. Cell. Biol. 2003, 23:4094-4106.
125. Scheller N., Mina L.B., Galao R.P., Chari A., Gimenez-Barcons M., Noueiry A., Fischer U., Meyerhans A., Diez J. Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13517-13522.
126. Ahn B.Y., Jones E.V., Moss B. Identification of the vaccinia virus gene encoding an 18-kilodalton subunit of RNA polymerase and demonstration of a 5' poly(A) leader on its early transcript. J. Virol. 1990, 64:3019-3024.
127. Ahn B.Y., Moss B. Capped poly(A) leaders of variable lengths at the 5' ends of vaccinia virus late mRNAs. J. Virol. 1989, 63:226-232.
128. Jangra R.K., Yi M., Lemon S.M. DDX6 (Rck/p54) is required for efficient hepatitis C virus replication but not for internal ribosome entry site-directed translation. J. Virol. 2010, 84:6810-6824.
129. Machlin E.S., Sarnow P., Sagan S.M. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3193-3198.
130. Shimakami T., Yamane D., Jangra R.K., Kempf B.J., Spaniel C., Barton D.J., Lemon S.M. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:941-946.
131. Garaigorta U., Heim M.H., Boyd B., Wieland S., Chisari F.V. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J. Virol. 2012, 86:11043-11056.
132. Pijlman G.P., Funk A., Kondratieva N., Leung J., Torres S., van der Aa L., Liu W.J., Palmenberg A.C., Shi P.Y., Hall R.A., Khromykh A.A. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 2008, 4:579-591.
133. Silva P.A., Pereira C.F., Dalebout T.J., Spaan W.J., Bredenbeek P.J. An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J. Virol. 2010, 84:11395-11406.
134. Moon S.L., Anderson J.R., Kumagai Y., Wilusz C.J., Akira S., Khromykh A.A., Wilusz J. A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability. RNA 2012, 18:2029-2040.
135. Schuessler A., Funk A., Lazear H.M., Cooper D.A., Torres S., Daffis S., Jha B.K., Kumagai Y., Takeuchi O., Hertzog P., Silverman R., Akira S., Barton D.J., Diamond M.S., Khromykh A.A. West Nile virus noncoding subgenomic RNA contributes to viral evasion of the type I interferon-mediated antiviral response. J. Virol. 2012, 86:5708-5718.
136. Beliakova-Bethell N., Beckham C., Giddings T.H., Winey M., Parker R., Sandmeyer S. Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components. RNA 2006, 12:94-101.
137. Dutko J.A., Kenny A.E., Gamache E.R., Curcio M.J. 5' to 3' mRNA decay factors colocalize with Ty1 gag and human APOBEC3G and promote Ty1 retrotransposition. J. Virol. 2010, 84:5052-5066.
138. Furuichi Y., Morgan M., Muthukrishnan S., Shatkin A.J. Reovirus messenger RNA contains a methylated, blocked 5'-terminal structure: m-7G(5')ppp(5')G-MpCp. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:362-366.
139. Furuichi Y., Muthukrishnan S., Shatkin A.J. 5'-Terminal m-7G(5')ppp(5')G-m-p in vivo: identification in reovirus genome RNA. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:742-745.
140. Furuichi Y., Shatkin A.J. Viral and cellular mRNA capping: past and prospects. Adv. Virus Res. 2000, 55:135-184.
141. Toh E.A., Guerry P., Wickner R.B. Chromosomal superkiller mutants of Saccharomyces cerevisiae. J. Bacteriol. 1978, 136:1002-1007.
142. Wei C.M., Moss B. Methylated nucleotides block 5'-terminus of vaccinia virus messenger RNA. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:318-322.
143. Benarroch D., Egloff M.P., Mulard L., Guerreiro C., Romette J.L., Canard B. A structural basis for the inhibition of the NS5 dengue virus mRNA 2'-O-methyltransferase domain by ribavirin 5'-triphosphate. J. Biol. Chem. 2004, 279:35638-35643.