Biogenesis, assembly and export of viral messenger ribonucleoproteins in the influenza A virus infected cell

RNA Biology

Volumn 10, Issue 8, 2013, Pages 1274-1282

  York, Ashley ^a   Fodor, Ervin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Capping; Influenza virus; MRNP; MRNP export; NXF1; Polyadenylation; RNA polymerase; Splicing; Transcription

Indexed keywords

CLEAVAGE STIMULATION FACTOR; INITIATION FACTOR 4E; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; RNA DIRECTED RNA POLYMERASE; RNA POLYMERASE; SINGLE STRANDED RNA; STRUCTURAL PROTEIN; VIRUS RNA;

ARTICLE; BIOGENESIS; CELL FUNCTION; CELL MEMBRANE; CYTOPLASM; GENETIC TRANSCRIPTION; HERPES SIMPLEX VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA; INFLUENZA VIRUS A; INTRON; MESSENGER RNA SYNTHESIS; NONHUMAN; NUCLEAR EXPORT SIGNAL; POLYADENYLATION; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; VIRION; VIRUS REPLICATION;

EUKARYOTA; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

CAPPING; INFLUENZA VIRUS; MRNP; MRNP EXPORT; NXF1; POLYADENYLATION; RNA POLYMERASE; SPLICING; TRANSCRIPTION;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; INFLUENZA A VIRUS; RIBONUCLEOPROTEINS; RNA TRANSPORT; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84883124285     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.25356     Document Type: Article

References (115)

1. Hieronymus H, Silver PA. A systems view of mRNP biology. Genes Dev 2004; 18:2845-60; PMID:15574591; http://dx.doi.org/10.1101/gad.1256904
2. Moore MJ, Proudfoot NJ. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009; 136:688-700; PMID:19239889; http://dx.doi.org/10.1016/j.cell.2009.02.001
3. Müller-McNicoll M, Neugebauer KM. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet 2013; 14:275-87; PMID:23478349; http://dx.doi.org/10.1038/nrg3434
4. Köhler A, Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 2007; 8:761-73; PMID:17786152; http://dx.doi.org/10.1038/ nrm2255
5. Shandilya J, Roberts SG. The transcription cycle in eukaryotes: from productive initiation to RNA polymerase II recycling. Biochim Biophys Acta 2012; 1819:391-400; PMID:22306664; http://dx.doi.org/10.1016/j.bbagrm.2012.01.010
6. Hoelz A, Debler EW, Blobel G. The structure of the nuclear pore complex. Annu Rev Biochem 2011; 80:613-43; PMID:21495847; http://dx.doi.org/10.1146/ annurev-biochem-060109-151030
7. Strambio-De-Castillia C, Niepel M, Rout MP. The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 2010; 11:490-501; PMID:20571586; http://dx.doi.org/10.1038/nrm2928
8. Cullen BR. Nuclear mRNA export: insights from virology. Trends Biochem Sci 2003; 28:419-24; PMID:12932730; http://dx.doi.org/10.1016/S0968-0004(03) 00142-7
9. Cullen BR. Human immunodeficiency virus: nuclear RNA export unwound. Nature 2005; 433:26-7; PMID:15635396; http://dx.doi.org/10.1038/433026a
10. Sandri-Goldin RM. Viral regulation of mRNA export. J Virol 2004; 78:4389-96; PMID:15078920; http://dx.doi.org/10.1128/JVI.78.9.4389-4396.2004
11. Amorim MJ, Digard P. Influenza A virus and the cell nucleus. Vaccine 2006; 24:6651-5; PMID:16806605; http://dx.doi.org/10.1016/j.vaccine.2006.05.066
12. Engelhardt OG, Fodor E. Functional association between viral and cellular transcription during influenza virus infection. Rev Med Virol 2006; 16:329-45; PMID:16933365; http://dx.doi.org/10.1002/rmv.512
13. Palese P, Shaw ML. Orthomyxoviridae: The Viruses and Their Replication. In: Knipe DM, Howley PM, eds. Fields Virology. Philadelphia: Lippincott Williams and Wilkins, 2007:1647-89.
14. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 2001; 7:1306-12; PMID:11726970; http://dx.doi.org/10.1038/nm1201-1306
15. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012; 337:199-204; PMID:22745253; http://dx.doi.org/10. 1126/science.1222213
16. Muramoto Y, Noda T, Kawakami E, Akkina R, Kawaoka Y. Identification of novel influenza A virus proteins translated from PA mRNA. J Virol 2013; 87:2455-62; PMID:23236060; http://dx.doi.org/10.1128/JVI.02656-12
17. Selman M, Dankar SK, Forbes NE, Jia JJ, Brown EG. Adaptive mutation in influenza A virus non-structural gene is linked to host switching and induces a novel protein by alternative splicing. Emerg Microbes Infec 2012; 1:e42; http://dx.doi.org/10.1038/emi.2012.38
18. Wise HM, Foeglein A, Sun J, Dalton RM, Patel S, Howard W, et al. A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 2009; 83:8021-31; PMID:19494001; http://dx.doi.org/10.1128/JVI.00826-09
19. Wise HM, Hutchinson EC, Jagger BW, Stuart AD, Kang ZH, Robb N, et al. Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathog 2012; 8:e1002998; PMID:23133386; http://dx.doi.org/10.1371/journal.ppat.1002998
20. Resa-Infante P, Jorba N, Coloma R, Ortin J. The influenza virus RNA synthesis machine: advances in its structure and function. RNA Biol 2011; 8:207-15; PMID:21358279; http://dx.doi.org/10.4161/rna.8.2.14513
21. Ruigrok RW, Crépin T, Hart DJ, Cusack S. Towards an atomic resolution understanding of the influenza virus replication machinery. Curr Opin Struct Biol 2010; 20:104-13; PMID:20061134; http://dx.doi.org/10.1016/j.sbi. 2009.12.007
22. Zheng W, Tao YJ. Structure and assembly of the influenza A virus ribonucleoprotein complex. FEBS Lett 2013; 587:1206-14; PMID:23499938; http://dx.doi.org/10.1016/j.febslet.2013.02.048
23. Hutchinson EC, Fodor E. Nuclear import of the influenza A virus transcriptional machinery. Vaccine 2012; 30:7353-8; PMID:22652398; http://dx.doi.org/10.1016/j.vaccine.2012.04.085
24. Fodor E. The RNA polymerase of influenza A virus: mechanisms of viral transcription and replication. Acta Virol 2013; 57:113-22; PMID:23600869; http://dx.doi.org/10.4149/av-2013-02-113
25. Krug RM, Fodor E. The virus genome and its replication. In: Webster RG, Monto AS, Braciale TJ, Lamb RA, eds. Textbook of Influenza 2nd Edition. New York City: John Wiley & Sons, Ltd., 2013:57-66.
26. Paterson D, Fodor E. Emerging roles for the influenza A virus nuclear export protein (NEP). PLoS Pathog 2012; 8:e1003019; PMID:23236273; http://dx.doi.org/10.1371/journal.ppat.1003019
27. Inglis SC, Gething MJ, Brown CM. Relationship between the messenger RNAs transcribed from two overlapping genes of influenza virus. Nucleic Acids Res 1980; 8:3575-89; PMID:7433101; http://dx.doi.org/10.1093/nar/8.16.3575
28. Inglis SC, Barrett T, Brown CM, Almond JW. The smallest genome RNA segment of influenza virus contains two genes that may overlap. Proc Natl Acad Sci USA 1979; 76:3790-4; PMID:291039; http://dx.doi.org/10.1073/pnas.76.8.3790
29. Inglis SC, Brown CM. Spliced and unspliced RNAs encoded by virion RNA segment 7 of influenza virus. Nucleic Acids Res 1981; 9:2727-40; PMID:6169001; http://dx.doi.org/10.1093/nar/9.12.2727
30. Lamb RA, Choppin PW. Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 1981; 112:729-37; PMID:7257188; http://dx.doi.org/10.1016/0042-6822(81)90317-2
31. Lamb RA, Lai CJ, Choppin PW. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc Natl Acad Sci USA 1981; 78:4170-4; PMID:6945577; http://dx.doi.org/10.1073/pnas.78.7.4170
32. Lamb RA, Horvath CM. Diversity of coding strategies in influenza viruses. Trends Genet 1991; 7:261-6; PMID:1771674
33. Lamb RA, Lai CJ. Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for the two overlapping nonstructural proteins of influenza virus. Cell 1980; 21:475-85; PMID:7407920; http://dx.doi.org/10.1016/0092- 8674(80)90484-5
34. Shih SR, Suen PC, Chen YS, Chang SC. A novel spliced transcript of influenza A/WSN/33 virus. Virus Genes 1998; 17:179-83; PMID:9857991; http://dx.doi.org/10.1023/A:1008024909222
35. Rehwinkel J, Reis e Sousa C. RIGorous detection: exposing virus through RNA sensing. Science 2010; 327:284-6; PMID:20075242; http://dx.doi.org/10.1126/ science.1185068
36. García-Sastre A. Induction and evasion of type I interferon responses by influenza viruses. Virus Res 2011; 162:12-8; PMID:22027189; http://dx.doi.org/10.1016/j.virusres.2011.10.017
37. Cook PR. A model for all genomes: the role of transcription factories. J Mol Biol 2010; 395:1-10; PMID:19852969; http://dx.doi.org/10.1016/j.jmb.2009.10. 031
38. Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip Rev RNA 2011; 2:277-98; PMID:21957010; http://dx.doi.org/10.1002/wrna.52
39. Engelhardt OG, Smith M, Fodor E. Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J Virol 2005; 79:5812-8; PMID:15827195; http://dx.doi.org/10.1128/JVI.79.9.5812-5818.2005
40. Biswas SK, Nayak DP. Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1. J Virol 1994; 68:1819-26; PMID:8107244
41. Dias A, Bouvier D, Crépin T, McCarthy AA, Hart DJ, Baudin F, et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009; 458:914-8; PMID:19194459; http://dx.doi.org/10.1038/ nature07745
42. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, et al. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 2008; 15:500-6; PMID:18454157; http://dx.doi.org/10. 1038/nsmb.1421
43. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, et al. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 2009; 458:909-13; PMID:19194458; http://dx.doi.org/10.1038/nature07720
44. 6-methyladenosine and 5′-terminal 7-methylguanosine in cap structures. J Virol 1976; 20:45-53; PMID:1086370
45. Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R. Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 2006; 127:1389-400; PMID:17190602; http://dx.doi.org/10.1016/j.cell.2006.10.044
46. Kelly SM, Corbett AH. Messenger RNA export from the nucleus: a series of molecular wardrobe changes. Traffic 2009; 10:1199-208; PMID:19552647; http://dx.doi.org/10.1111/j.1600-0854.2009.00944.x
47. Reed R, Hurt E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 2002; 108:523-31; PMID:11909523; http://dx.doi.org/10.1016/S0092- 8674(02)00627-X
48. Reed R. Coupling transcription, splicing and mRNA export. Curr Opin Cell Biol 2003; 15:326-31; PMID:12787775; http://dx.doi.org/10.1016/S0955-0674(03) 00048-6
49. Zhou Z, Luo MJ, Straesser K, Katahira J, Hurt E, Reed R. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 2000; 407:401-5; PMID:11014198; http://dx.doi.org/10.1038/35030160
50. Le Hir H, Andersen GR. Structural insights into the exon junction complex. Curr Opin Struct Biol 2008; 18:112-9; PMID:18164611; http://dx.doi.org/10.1016/j.sbi.2007.11.002
51. Hale BG, Randall RE, Ortín J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008; 89:2359-76; PMID:18796704; http://dx.doi.org/10.1099/vir.0.2008/004606-0
52. Robb NC, Fodor E. The accumulation of influenza A virus segment 7 spliced mRNAs is regulated by the NS1 protein. J Gen Virol 2012; 93:113-8; PMID:21918006; http://dx.doi.org/10.1099/vir.0.035485-0
53. Robb NC, Jackson D, Vreede FT, Fodor E. Splicing of influenza A virus NS1 mRNA is independent of the viral NS1 protein. J Gen Virol 2010; 91:2331-40; PMID:20519456; http://dx.doi.org/10.1099/vir.0.022004-0
54. Garaigorta U, Ortín J. Mutation analysis of a recombinant NS replicon shows that influenza virus NS1 protein blocks the splicing and nucleo-cytoplasmic transport of its own viral mRNA. Nucleic Acids Res 2007; 35:4573-82; PMID:17488845; http://dx.doi.org/10.1093/nar/gkm230
55. Smith DB, Inglis SC. Regulated production of an influenza virus spliced mRNA mediated by virus-specific products. EMBO J 1985; 4:2313-9; PMID:3841059
56. Chua MA, Schmid S, Perez JT, Langlois RA, Tenoever BR. Influenza A virus utilizes suboptimal splicing to coordinate the timing of infection. Cell Rep 2013; 3:23-9; PMID:23333274; http://dx.doi.org/10.1016/j.celrep.2012.12.010
57. Proudfoot NJ, Brownlee GG. 3′ non-coding region sequences in eukaryotic messenger RNA. Nature 1976; 263:211-4; PMID:822353; http://dx.doi.org/10.1038/263211a0
58. Proudfoot NJ. Ending the message: poly(A) signals then and now. Genes Dev 2011; 25:1770-82; PMID:21896654; http://dx.doi.org/10.1101/gad.17268411
59. Robertson JS, Schubert M, Lazzarini RA. Polyadenylation sites for influenza virus mRNA. J Virol 1981; 38:157-63; PMID:7241649
60. Fodor E, Pritlove DC, Brownlee GG. The influenza virus panhandle is involved in the initiation of transcription. J Virol 1994; 68:4092-6; PMID:8189550
61. Tiley LS, Hagen M, Matthews JT, Krystal M. Sequencespecific binding of the influenza virus RNA polymerase to sequences located at the 5′ ends of the viral RNAs. J Virol 1994; 68:5108-16; PMID:8035510
62. Poon LL, Pritlove DC, Fodor E, Brownlee GG. Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J Virol 1999; 73:3473-6; PMID:10074205
63. Poon LL, Fodor E, Brownlee GG. Polyuridylated mRNA synthesized by a recombinant influenza virus is defective in nuclear export. J Virol 2000; 74:418-27; PMID:10590131; http://dx.doi.org/10.1128/JVI.74.1.418-427.2000
64. Zheng H, Lee HA, Palese P, García-Sastre A. Influenza A virus RNA polymerase has the ability to stutter at the polyadenylation site of a viral RNA template during RNA replication. J Virol 1999; 73:5240-3; PMID:10233995
65. McCloskey A, Taniguchi I, Shinmyozu K, Ohno M. hnRNP C tetramer measures RNA length to classify RNA polymerase II transcripts for export. Science 2012; 335:1643-6; PMID:22461616; http://dx.doi.org/10.1126/science.1218469
66. Carmody SR, Wente SR. mRNA nuclear export at a glance. J Cell Sci 2009; 122:1933-7; PMID:19494120; http://dx.doi.org/10.1242/jcs.041236
67. Grünwald D, Singer RH, Rout M. Nuclear export dynamics of RNA-protein complexes. Nature 2011; 475:333-41; PMID:21776079; http://dx.doi.org/10.1038/nature10318
68. Mor A, Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol 2010; 12:543-52; PMID:20453848; http://dx.doi.org/10.1038/ncb2056
69. Tutucci E, Stutz F. Keeping mRNPs in check during assembly and nuclear export. Nat Rev Mol Cell Biol 2011; 12:377-84; PMID:21602906; http://dx.doi.org/10.1038/nrm3119
70. Luo MJ, Reed R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc Natl Acad Sci USA 1999; 96:14937-42; PMID:10611316; http://dx.doi.org/10.1073/pnas.96.26.14937
71. Katahira J. mRNA export and the TREX complex. Biochim Biophys Acta 2012; 1819:507-13; PMID:22178508; http://dx.doi.org/10.1016/j.bbagrm.2011.12.001
72. Jani D, Lutz S, Hurt E, Laskey RA, Stewart M, Wickramasinghe VO. Functional and structural characterization of the mammalian TREX-2 complex that links transcription with nuclear messenger RNA export. Nucleic Acids Res 2012; 40:4562-73; PMID:22307388; http://dx.doi.org/10.1093/nar/gks059
73. Ruepp MD, Schümperli D, Barabino SM. mRNA 3′ end processing and more - multiple functions of mammalian cleavage factor I-68. Wiley Interdiscip Rev RNA 2011; 2:79-91; PMID:21956970; http://dx.doi.org/10.1002/ wrna.35
74. Amorim MJ, Read EK, Dalton RM, Medcalf L, Digard P. Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 2007; 8:1-11; PMID:17132145; http://dx.doi.org/10.1111/j.1600-0854.2006.00507.x
75. Wang W, Cui ZQ, Han H, Zhang ZP, Wei HP, Zhou YF, et al. Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res 2008; 36:4913-28; PMID:18653528; http://dx.doi.org/10.1093/nar/gkn475
76. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139:1243-54; PMID:20064371; http://dx.doi.org/10.1016/j.cell.2009.12.017
77. Hao L, Sakurai A, Watanabe T, Sorensen E, Nidom CA, Newton MA, et al. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008; 454:890-3; PMID:18615016; http://dx.doi.org/10.1038/ nature07151
78. Karlas A, Machuy N, Shin Y, Pleissner KP, Artarini A, Heuer D, et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010; 463:818-22; PMID:20081832; http://dx.doi.org/10. 1038/nature08760
79. Shapira SD, Gat-Viks I, Shum BO, Dricot A, de Grace MM, Wu L, et al. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 2009; 139:1255-67; PMID:20064372; http://dx.doi.org/10. 1016/j.cell.2009.12.018
80. Watanabe T, Watanabe S, Kawaoka Y. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 2010; 7:427-39; PMID:20542247; http://dx.doi.org/10.1016/j.chom.2010.05.008
81. Read EK, Digard P. Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export. J Gen Virol 2010; 91:1290-301; PMID:20071484; http://dx.doi.org/10.1099/vir.0.018564-0
82. Gatfield D, Izaurralde E. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J Cell Biol 2002; 159:579-88; PMID:12438415; http://dx.doi.org/10.1083/jcb.200207128
83. Longman D, Johnstone IL, Cáceres JF. The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans. RNA 2003; 9:881-91; PMID:12810921; http://dx.doi.org/10.1261/rna.5420503
84. Bier K, York A, Fodor E. Cellular cap-binding proteins associate with influenza virus mRNAs. J Gen Virol 2011; 92:1627-34; PMID:21402597; http://dx.doi.org/10.1099/vir.0.029231-0
85. Huang Y, Gattoni R, Stévenin J, Steitz JA. SR splicing factors serve as adapter proteins for TAPdependent mRNA export. Mol Cell 2003; 11:837-43; PMID:12667464; http://dx.doi.org/10.1016/S1097-2765(03)00089-3
86. Shih SR, Krug RM. Novel exploitation of a nuclear function by influenza virus: the cellular SF2/ASF splicing factor controls the amount of the essential viral M2 ion channel protein in infected cells. EMBO J 1996; 15:5415-27; PMID:8895585
87. Morita M, Kuba K, Ichikawa A, Nakayama M, Katahira J, Iwamoto R, et al. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 2013; 153:112-25; PMID:23477864; http://dx.doi.org/10.1016/j.cell.2013.02.027
88. Bachi A, Braun IC, Rodrigues JP, Panté N, Ribbeck K, von Kobbe C, et al. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 2000; 6:136-58; PMID:10668806; http://dx.doi.org/10.1017/S1355838200991994
89. Pasquinelli AE, Ernst RK, Lund E, Grimm C, Zapp ML, Rekosh D, et al. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J 1997; 16:7500-10; PMID:9405378; http://dx.doi.org/10.1093/emboj/16.24.7500
90. Hutten S, Kehlenbach RH. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 2007; 17:193-201; PMID:17317185; http://dx.doi.org/10. 1016/j.tcb.2007.02.003
91. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, McCauley J, et al. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 2001; 75:408-19; PMID:11119609; http://dx.doi.org/10.1128/JVI.75.1.408-419.2001
92. Ma K, Roy AM, Whittaker GR. Nuclear export of influenza virus ribonucleoproteins: identification of an export intermediate at the nuclear periphery. Virology 2001; 282:215-20; PMID:11289803; http://dx.doi.org/10.1006/ viro.2001.0833
93. Watanabe K, Takizawa N, Katoh M, Hoshida K, Kobayashi N, Nagata K. Inhibition of nuclear export of ribonucleoprotein complexes of influenza virus by leptomycin B. Virus Res 2001; 77:31-42; PMID:11451485; http://dx.doi.org/10. 1016/S0168-1702(01)00263-5
94. Arts GJ, Fornerod M, Mattaj IW. Identification of a nuclear export receptor for tRNA. Curr Biol 1998; 8:305-14; PMID:9512417; http://dx.doi.org/10. 1016/S0960-9822(98)70130-7
95. Bohnsack MT, Regener K, Schwappach B, Saffrich R, Paraskeva E, Hartmann E, et al. Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm. EMBO J 2002; 21:6205-15; PMID:12426392; http://dx.doi.org/10.1093/emboj/cdf613
96. Calado A, Treichel N, Müller EC, Otto A, Kutay U. Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA. EMBO J 2002; 21:6216-24; PMID:12426393; http://dx.doi.org/10.1093/emboj/cdf620
97. Kutay U, Lipowsky G, Izaurralde E, Bischoff FR, Schwarzmaier P, Hartmann E, et al. Identification of a tRNA-specific nuclear export receptor. Mol Cell 1998; 1:359-69; PMID:9660920; http://dx.doi.org/10.1016/S1097-2765(00)80036-2
98. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004; 303:95-8; PMID:14631048; http://dx.doi.org/10.1126/science.1090599
99. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003; 17:3011-6; PMID:14681208; http://dx.doi.org/10.1101/gad.1158803
100. Schneider J, Wolff T. Nuclear functions of the influenza A and B viruses NS1 proteins: do they play a role in viral mRNA export? Vaccine 2009; 27:6312-6; PMID:19840666; http://dx.doi.org/10.1016/j.vaccine.2009.01.015
101. Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, Faria PA, et al. Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci USA 2007; 104:1853-8; PMID:17267598; http://dx.doi.org/10.1073/pnas.0610977104
102. Salvatore M, Basler CF, Parisien JP, Horvath CM, Bourmakina S, Zheng H, et al. Effects of influenza A virus NS1 protein on protein expression: the NS1 protein enhances translation and is not required for shutoff of host protein synthesis. J Virol 2002; 76:1206-12; PMID:11773396; http://dx.doi.org/10.1128/ JVI.76.3.1206-1212.2002
103. Burgui I, Yángüez E, Sonenberg N, Nieto A. Influenza virus mRNA translation revisited: is the eIF4E capbinding factor required for viral mRNA translation? J Virol 2007; 81:12427-38; PMID:17855553; http://dx.doi.org/ 10.1128/JVI.01105-07
104. Shih SR, Krug RM. Surprising function of the three influenza viral polymerase proteins: selective protection of viral mRNAs against the cap-snatching reaction catalyzed by the same polymerase proteins. Virology 1996; 226:430-5; PMID:8955065; http://dx.doi.org/10.1006/viro.1996.0673
105. Shih SR, Nemeroff ME, Krug RM. The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci USA 1995; 92:6324-8; PMID:7541537; http://dx.doi.org/10.1073/ pnas.92.14.6324
106. Bradel-Tretheway BG, Mattiacio JL, Krasnoselsky A, Stevenson C, Purdy D, Dewhurst S, et al. Comprehensive proteomic analysis of influenza virus polymerase complex reveals a novel association with mitochondrial proteins and RNA polymerase accessory factors. J Virol 2011; 85:8569-81; PMID:21715506; http://dx.doi.org/10.1128/JVI.00496-11
107. Jorba N, Juarez S, Torreira E, Gastaminza P, Zamarreño N, Albar JP, et al. Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 2008; 8:2077-88; PMID:18491320; http://dx.doi.org/10.1002/pmic.200700508
108. Landeras-Bueno S, Jorba N, Pérez-Cidoncha M, Ortín J. The splicing factor proline-glutamine rich (SFPQ/PSF) is involved in influenza virus transcription. PLoS Pathog 2011; 7:e1002397; PMID:22114566; http://dx.doi.org/10.1371/journal.ppat.1002397
109. Momose F, Basler CF, O'Neill RE, Iwamatsu A, Palese P, Nagata K. Cellular splicing factor RAF-2p48/NPI-5/BAT1/UAP56 interacts with the influenza virus nucleoprotein and enhances viral RNA synthesis. J Virol 2001; 75:1899-908; PMID:11160689; http://dx.doi.org/10.1128/JVI.75.4.1899-1908.2001
110. Chen IH, Sciabica KS, Sandri-Goldin RM. ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J Virol 2002; 76:12877-89; PMID:12438613; http://dx.doi.org/10.1128/JVI.76.24.12877-12889.2002
111. Lischka P, Toth Z, Thomas M, Mueller R, Stamminger T. The UL69 transactivator protein of human cytomegalovirus interacts with DEXD/H-Box RNA helicase UAP56 to promote cytoplasmic accumulation of unspliced RNA. Mol Cell Biol 2006; 26:1631-43; PMID:16478985; http://dx.doi.org/10.1128/MCB.26.5.1631- 1643.2006
112. Toth Z, Stamminger T. The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export. Front Biosci 2008; 13:2939-49; PMID:17981767; http://dx.doi.org/10.2741/2899
113. Baltz AG, Munschauer M, Schwanhäusser B, Vasile A, Murakawa Y, Schueler M, et al. The mRNAbound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012; 46:674-90; PMID:22681889; http://dx.doi.org/10.1016/j.molcel.2012.05.021
114. Schmidt C, Kramer K, Urlaub H. Investigation of protein-RNA interactions by mass spectrometry - Techniques and applications. J Proteomics 2012; 75:3478-94; PMID:22575267; http://dx.doi.org/10.1016/j.jprot.2012.04.030
115. Weil TT, Parton RM, Davis I. Making the message clear: visualizing mRNA localization. Trends Cell Biol 2010; 20:380-90; PMID:20444605; http://dx.doi.org/10.1016/j.tcb.2010.03.006