Viruses and the cellular RNA decay machinery

Wiley Interdisciplinary Reviews: RNA

Volumn 1, Issue 1, 2010, Pages 47-59

  Gaglia, Marta Maria ^a   Glaunsinger, Britt A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; EXORIBONUCLEASE; POLY(A)-SPECIFIC RIBONUCLEASE; POLYADENYLATE SPECIFIC RIBONUCLEASE; RNA BINDING PROTEIN;

ADENYLATION; DEADENYLATION; EUKARYOTE; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA STABILITY; RNA VIRUS; VIRUS GENE; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; POLYADENYLATION; PROTEIN SYNTHESIS; VIRUS;

EUKARYOTA;

ANIMALS; EXORIBONUCLEASES; GENE EXPRESSION REGULATION, VIRAL; HUMANS; MODELS, BIOLOGICAL; POLYADENYLATION; PROTEIN BIOSYNTHESIS; RNA STABILITY; RNA-BINDING PROTEINS; VIRUSES;

EID: 80055066181     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.3     Document Type: Review

References (101)

1. Doma MK, Parker R. RNA quality control in eukaryotes. Cell 2007, 131: 660-668.
2. Goldstrohm AC, Wickens M. Multifunctional deadenylase complexes diversify mRNA control. Nat Rev Mol Cell Biol 2008, 9: 337-344.
3. Parker R, Song H. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 2004, 11: 121-127.
4. ' untranslated region of sindbis virus represses deadenylation of viral transcripts in mosquito and Mammalian cells. J Virol 2008, 82: 880-892.
5. Conrad NK, Steitz JA. A Kaposi's sarcoma virus RNA element that increases the nuclear abundance of intronless transcripts. Embo J 2005, 24: 1831-1841.
6. Conrad NK, Mili S, Marshall EL, Shu MD, Steitz JA. Identification of a rapid mammalian deadenylation-dependent decay pathway and its inhibition by a viral RNA element. Mol Cell 2006, 24: 943-953.
7. Conrad NK, Shu MD, Uyhazi KE, Steitz JA. Mutational analysis of a viral RNA element that counteracts rapid RNA decay by interaction with the polyadenylate tail. Proc Natl Acad Sci U S A 2007, 104: 10412-10417.
8. Beelman CA, Stevens A, Caponigro G, LaGrandeur TE, Hatfield L, et al. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 1996, 382: 642-646.
9. Dunckley T, Parker R. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. Embo J 1999, 18: 5411-5422.
10. Tharun S, He W, Mayes AE, Lennertz P, Beggs JD, et al. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 2000, 404: 515-518.
11. Tharun S, Parker R. Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol Cell 2001, 8: 1075-1083.
12. Bonnerot C, Boeck R, Lapeyre B. The two proteins Pat1p (Mrt1p) and Spb8p interact in vivo, are required for mRNA decay, and are functionally linked to Pab1p. Mol Cell Biol 2000, 20: 5939-5946.
13. Bouveret E, Rigaut G, Shevchenko A, Wilm M, Seraphin B. A Sm-like protein complex that participates in mRNA degradation. Embo J 2000, 19: 1661-1671.
14. Coller JM, Tucker M, Sheth U, Valencia-Sanchez MA, Parker R. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 2001, 7: 1717-1727.
15. Diez J, Ishikawa M, Kaido M, Ahlquist P. Identification and characterization of a host protein required for efficient template selection in viral RNA replication. Proc Natl Acad Sci U S A 2000, 97: 3913-3918.
16. 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.
17. Noueiry AO, Diez J, Falk SP, Chen J, Ahlquist P. Yeast Lsm1p-7p/Pat1p dead-enylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol Cell Biol 2003, 23: 4094-4106.
18. Scheller N, Mina LB, Galao RP, Chari A, Gimenez-Barcons M, et al. 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.
19. Beckham CJ, Light HR, Nissan TA, Ahlquist P, Parker R, et al. Interactions between brome mosaic virus RNAs and cytoplasmic processing bodies. J Virol 2007, 81: 9759-9768.
20. 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.
21. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell 2007, 25: 635-646.
22. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 2005, 169: 871-884.
23. Zheng D, Ezzeddine N, Chen CY, Zhu W, He X, et al. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J Cell Biol 2008, 182: 89-101.
24. ' poly(A) leader. Cell 1987, 50: 163-169.
25. ' poly(A) tracts. Nat Struct Mol Biol 2007, 14: 824-831.
26. Parrish S, Moss B. Characterization of a vaccinia virus mutant with a deletion of the D10R gene encoding a putative negative regulator of gene expression. J Virol 2006, 80: 553-561.
27. 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.
28. Shors T, Keck JG, Moss B. Down regulation of gene expression by the vaccinia virus D10 protein. J Virol 1999, 73: 791-796.
29. Toh EA, Guerry P, Wickner RB. Chromosomal superkiller mutants of Saccharomyces cerevisiae. J Bacteriol 1978, 136: 1002-1007.
30. Cheng CP, Serviene E, Nagy PD. Suppression of viral RNA recombination by a host exoribonuclease. J Virol 2006, 80: 2631-2640.
31. Jaag HM, Nagy PD. Silencing of Nicotiana benthamiana Xrn4p exoribonuclease promotes tombusvirus RNA accumulation and recombination. Virology 2009, 386: 344-352.
32. Domingo E. Virus evolution. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., eds. Fields Virology. 5th ed. Philadelphia: Lippincott Williams and Wilkins; 2007; 389-421.
33. Esteban R, Vega L, Fujimura T. 20S RNA narnavirus defies the antiviral activity of SKI1/XRN1 in Saccharomyces cerevisiae. J Biol Chem 2008, 283: 25812-25820.
34. Murray KE, Roberts AW, Barton DJ. Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 2001, 7: 1126-1141.
35. ' cloverleaf of uncapped poliovirus mRNA function during de novo assembly of polysomes. J Virol 2008, 82: 5835-5846.
36. '-nontranslated regions. Virus Res 1997, 51: 213-229.
37. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, et al. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 2008, 4: 579-591.
38. Schmid M, Jensen TH. The exosome: a multipurpose RNA-decay machine. Trends Biochem Sci 2008, 33: 501-510.
39. Gao G, Guo X, Goff SP. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 2002, 297: 1703-1706.
40. Bick MJ, Carroll JW, Gao G, Goff SP, Rice CM, et al. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J Virol 2003, 77: 11555-11562.
41. Muller S, Moller P, Bick MJ, Wurr S, Becker S, et al. Inhibition of filovirus replication by the zinc finger antiviral protein. J Virol 2007, 81: 2391-2400.
42. Guo X, Ma J, Sun J, Gao G. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc Natl Acad Sci U S A 2007, 104: 151-156.
43. Guo X, Carroll JW, Macdonald MR, Goff SP, Gao G, et al. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J Virol 2004, 78: 12781-12787.
44. Glaunsinger B, Ganem D. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol Cell 2004, 13: 713-723.
45. Kwong AD, 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.
46. Lee YJ, Glaunsinger BA. Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol 2009, 7: e1000107.
47. Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T, et al. 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.
48. Tohya Y, Narayanan K, Kamitani W, Huang C, Lokugamage K, et al. Suppression of host gene expression by nsp1 proteins of group 2 bat coronaviruses. J Virol 2009, 83: 5282-5288.
49. Muhlemann O, Eberle AB, Stalder L, Zamudio R. Recognition and elimination of nonsense mRNA. Biochim Biophys Acta 2008, 1779: 538-549.
50. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 2009, 16: 49-55.
51. 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.
52. Isken O, Maquat LE. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 2007, 21: 1833-1856.
53. Zhang J, Sun X, Qian Y, LaDuca JP, Maquat LE, et al. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol Cell Biol 1998, 18: 5272-5283.
54. Zhang J, Sun X, Qian Y, Maquat LE. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 1998, 4: 801-815.
55. ' untranslated region. PLoS Biol 2008, 6: e92.
56. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE, et al. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. Embo J 2008, 27: 736-747.
57. Singh G, Rebbapragada I, Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 2008, 6: e111.
58. ' end. Nucleic Acids Res 2005, 33: 825-837.
59. ' UTR sequence stabilizes termination codons in the unspliced RNA of Rous sarcoma virus. RNA 2006, 12: 102-110.
60. Weil JE, Hadjithomas M, Beemon KL. Structural characterization of the Rous sarcoma virus RNA stability element. J Virol 2009, 83: 2119-2129.
61. Kuhn RJ. Togaviridiae: the viruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., eds. Fields Virology. 5th ed. Philadelphia: Lippincott Williams and Wilkins; 2007; 1002-1022.
62. Lai MC, Perlman S, Anderson LJ. Coronaviridiae. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., eds. Fields Virology. 5th ed. Philadephia: Lippincott Williams and Wilkins; 2007; 1305-1335.
63. Ganem D. Kaposi's Sarcoma-associated herpesvirus. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., eds. Fields Virology. 5th ed. Philadelphia: Lippincott Williams and Wilkins; 2007; 2847-2888.
64. Ajamian L, Abrahamyan L, Milev M, Ivanov PV, Kulozik AE, et al. Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation. RNA 2008, 14: 914-927.
65. Endo Y, Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 1987, 262: 8128-8130.
66. Hudak KA, Wang P, Tumer NE. A novel mechanism for inhibition of translation by pokeweed antiviral protein: depurination of the capped RNA template. RNA 2000, 6: 369-380.
67. Irvin JD. Purification and partial characterization of the antiviral protein from Phytolacca americana which inhibits eukaryotic protein synthesis. Arch Biochem Biophys 1975, 169: 522-528.
68. Zarling JM, Moran PA, Haffar O, Diegel M, Myers DE, et al. Inhibition of HIV-1 replication in seropositive patients' CD4+ T-cells by pokeweed antiviral protein-monoclonal antibody conjugates. Int J Immunopharmacol 1991, 13(Suppl 1): 63-68.
69. Parikh BA, Tumer NE. Antiviral activity of ribosome inactivating proteins in medicine. Mini Rev Med Chem 2004, 4: 523-543.
70. Tumer NE, Hwang DJ, Bonness M. C-terminal deletion mutant of pokeweed antiviral protein inhibits viral infection but does not depurinate host ribosomes. Proc Natl Acad Sci U S A 1997, 94: 3866-3871.
71. Gandhi R, Manzoor M, Hudak KA. Depurination of Brome mosaic virus RNA3 in vivo results in translation-dependent accelerated degradation of the viral RNA. J Biol Chem 2008, 283: 32218-32228.
72. Doma MK, Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006, 440: 561-564.
73. Mansouri S, Choudhary G, Sarzala PM, Ratner L, Hudak KA, et al. Suppression of human T-cell leukemia virus I gene expression by pokeweed antiviral protein. J Biol Chem 2009, 284: 31453-31462.
74. Park SW, Prithiviraj B, Vepachedu R, Vivanco JM. Isolation and purification of ribosome-inactivating proteins. Methods Mol Biol 2006, 318: 335-347.
75. '-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 2007, 81: 12720-12729.
76. Malathi K, Dong B, Gale M Jr, Silverman RH. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 2007, 448: 816-819.
77. '-oligoadenylate-dependent RNase L. Embo J 1997, 16: 6355-6363.
78. Sawicki DL, Silverman RH, Williams BR, Sawicki SG. Alphavirus minus-strand synthesis and persistence in mouse embryo fibroblasts derived from mice lacking RNase L and protein kinase R. J Virol 2003, 77: 1801-1811.
79. Flodstrom-Tullberg M, Hultcrantz M, Stotland A, Maday A, Tsai D, et al. RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J Immunol 2005, 174: 1171-1177.
80. Lombardi VC, Ruscetti FW, Das Gupta J, Pfost MA, Hagen KS, et al. Detection of an infectious retrovirus, XMRV, in blood cells of patients with chronic fatigue syndrome. Science 2009, 326: 585-589.
81. Urisman A, Molinaro RJ, Fischer N, Plummer SJ Casey G, et al. Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog 2006, 2: e25.
82. Ireland DD, Stohlman SA, Hinton DR, Kapil P, Silverman RH, et al. RNase L mediated protection from virus induced demyelination. PLoS Pathog 2009, 5: e1000602.
83. Hale BG, Randall RE, Ortin J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008, 89: 2359-2376.
84. ' oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci U S A 2006, 103: 7100-7105.
85. Bolinger C, Boris-Lawrie K. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 2009, 6: 8.
86. Rice AP, Roberts WK, Kerr IM. 2-5A accumulates to high levels in interferon-treated, vaccinia virus-infected cells in the absence of any inhibition of virus replication. J Virol 1984, 50: 220-228.
87. ' oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA 2002, 8: 512-525.
88. Han JQ, Townsend HL, Jha BK, Paranjape JM, Silverman RH, et al. A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. J Virol 2007, 81: 5561-5572.
89. Townsend HL, Jha BK, Han JQ, Maluf NK, Silverman RH, et al. A viral RNA competitively inhibits the antiviral endoribonuclease domain of RNase L. RNA 2008, 14: 1026-1036.
90. Smith JA, Schmechel SC, Williams BR, Silverman RH, Schiff LA, et al. Involvement of the interferon-regulated antiviral proteins PKR and RNase L in reovirus-induced shutoff of cellular translation. J Virol 2005, 79: 2240-2250.
91. ' oligoadenylate/RNase L/RNase L inhibitor pathway regulates both MyoD mRNA stability and muscle cell differentiation. Mol Cell Biol 2000, 20: 4959-4969.
92. Khabar KS, Siddiqui YM, al-Zoghaibi F, al-Haj L, Dhalla M, et al. RNase L mediates transient control of the interferon response through modulation of the double-stranded RNA-dependent protein kinase PKR. J Biol Chem 2003, 278: 20124-20132.
93. Li XL, Blackford JA, Judge CS, Liu M, Xiao W, et al. RNase-L-dependent destabilization of interferon-induced mRNAs. A role for the 2-5A system in attenuation of the interferon response. J Biol Chem 2000, 275: 8880-8888.
94. Schmechel S, Chute M, Skinner P, Anderson R, Schiff L, et al. Preferential translation of reovirus mRNA by a sigma3-dependent mechanism. Virology 1997, 232: 62-73.
95. ')oligoadenylate and activation of an endoribonuclease in interferon-treated HeLa cells infected with reovirus. J Virol 1982, 42: 1039-1045.
96. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. Embo J 1998, 17: 3351-3362.
97. '-end processing machinery. Embo J 1999, 18: 2273-2283.
98. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009, 458: 914-918.
99. Kamitani W, Huang C, Narayanan K, Lokugamage KG, Makino S. A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat Struct Mol Biol 2009, 16: 1134-1140.
100. Lai MC, Peng TY, Tarn WY. Functional interplay between viral and cellular SR proteins in control of post-transcriptional gene regulation. FEBS J 2009, 276: 1517-1526.
101. McCormick C, Ganem D. The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 2005, 307: 739-741.