Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export

Journal of General Virology

Volumn 91, Issue 5, 2010, Pages 1290-1301

  Read, Eliot K C ^a   Digard, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; MEMBRANE PROTEIN; MESSENGER RNA; NONSTRUCTURAL PROTEIN 1; NXF1 PROTEIN; PROTEIN M1; PROTEIN M2; RNA POLYMERASE II; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; INHIBITION KINETICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA TRANSLATION; SENSITIVITY ANALYSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE; CELL NUCLEUS; DEAD-BOX RNA HELICASES; GENE KNOCKDOWN TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 77951049855     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.018564-0     Document Type: Article

References (55)

1. Amorim, M. J. & Digard, P. (2006). Influenza A virus and the cell nucleus. Vaccine 24, 6651-6655.
2. Amorim, M. J., Read, E. K., Dalton, R. M., Medcalf, L. & Digard, P. (2007). Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8, 1-11. (Pubitemid 44921878)
3. Boyne, J. R., Colgan, K. J. & Whitehouse, A. (2008). Recruitment of the complete hTREX complex is required for Kaposi's sarcoma-associated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog 4, e1000194.
4. Braam, J., Ulmanen, I. & Krug, R. M. (1983). Molecular model of a eucaryotic transcription complex: functions and movements of influenza P proteins during capped RNA-primed transcription. Cell 34, 609-618.
5. Carmody, S. R. & Wente, S. R. (2009). mRNA nuclear export at a glance. J Cell Sci 122, 1933-1937.
6. Carrasco, M., Amorim, M. J. & Digard, P. (2004). Lipid raft-dependent targeting of the influenza A virus nucleoprotein to the apical plasma membrane. Traffic 5, 979-992. (Pubitemid 39534489)
7. Cheng, H., Dufu, K., Lee, C. S., Hsu, J. L., Dias, A. & Reed, R. (2006). Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127, 1389-1400. (Pubitemid 44960410)
8. Clement, J. Q. & Wilkinson, M. F. (2000). Rapid induction of nuclear transcripts and inhibition of intron decay in response to the polymerase II inhibitor DRB. J Mol Biol 299, 1179-1191.
9. Cullen, B. R. (2003). Nuclear mRNA export: insights from virology. Trends Biochem Sci 28, 419-424.
10. Elton, D., Simpson-Holley, M., Archer, K., Medcalf, L., Hallam, R., McCauley, J. & Digard, P. (2001). Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75, 408-419.
11. Engelhardt, O. G., Smith, M. & Fodor, E. (2005). Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J Virol 79, 5812-5818. (Pubitemid 40548249)
12. Erkmann, J. A. & Kutay, U. (2004). Nuclear export of mRNA: from the site of transcription to the cytoplasm. Exp Cell Res 296, 12-20. (Pubitemid 38543207)
13. Fasken, M. B. & Corbett, A. H. (2005). Process or perish: quality control in mRNA biogenesis. Nat Struct Mol Biol 12, 482-488. (Pubitemid 43085877)
14. Fontoura, B. M., Faria, P. A. & Nussenzveig, D. R. (2005). Viral interactions with the nuclear transport machinery: discovering and disrupting pathways. IUBMB Life 57, 65-72. (Pubitemid 40632296)
15. Fraser, N. W., Sehgal, P. B. & Darnell, J. E. (1978). DRB-induced premature termination of late adenovirus transcription. Nature 272, 590-593.
16. Hao, L., Sakurai, A., Watanabe, T., Sorensen, E., Nidom, C. A., Newton, M. A., Ahlquist, P. & Kawaoka, Y. (2008). Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 454, 890-893.
17. Harman, A., Browne, H. & Minson, T. (2002). The transmembrane domain and cytoplasmic tail of herpes simplex virus type 1 glycoprotein H play a role in membrane fusion. J Virol 76, 10708-10716. (Pubitemid 35176187)
18. Hatada, E., Hasegawa, M., Mukaigawa, J., Shimizu, K. & Fukuda, R. (1989). Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. J Biochem 105, 537-546. (Pubitemid 19106773)
19. Hautbergue, G. M., Hung, M. L., Golovanov, A. P., Lian, L. Y. & Wilson, S. A. (2008). Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc Natl Acad Sci U S A 105, 5154-5159.
20. Hautbergue, G. M., Hung, M. L., Walsh, M. J., Snijders, A. P., Chang, C. T., Jones, R., Ponting, C. P., Dickman, M. J. & Wilson, S. A. (2009). UIF, a new mRNA export adaptor that works together with REF/ALY, requires FACT for recruitment to mRNA. Current Biology 19, 1918-1924.
21. Howe, K. J. (2002). RNA polymerase II conducts a symphony of premRNA processing activities. Biochim Biophys Acta 1577, 308-324.
22. Huang, S., Deerinck, T. J., Ellisman, M. H. & Spector, D. L. (1994). In vivo analysis of the stability and transport of nuclear poly(A)+ RNA. J Cell Biol 126, 877-899.
23. Huang, Y., Gattoni, R., Stevenin, J. & Steitz, J. A. (2003). SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 11, 837-843. (Pubitemid 36385134)
24. Hutchinson, E. C., Curran, M. D., Read, E. K., Gog, J. R. & Digard, P. (2008). Mutational analysis of cis-acting RNA signals in segment 7 of influenza A virus. J Virol 82, 11869-11879.
25. Hutten, S. & Kehlenbach, R. H. (2007). CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 17, 193-201. (Pubitemid 46507806)
26. Inglis, S. C. & Mahy, B. W. (1979). Polypeptides specified by the influenza virus genome. 3. Control of synthesis in infected cells. Virology 95, 154-164.
27. Josset, L., Frobert, E. & Rosa-Calatrava, M. (2008). Influenza A replication and host nuclear compartments: many changes and many questions. J Clin Virol 43, 381-390.
28. Lamb, R. A. & Horvath, C. M. (1991). Diversity of coding strategies in influenza viruses. Trends Genet 7, 261-266.
29. Lamb, R. A., Etkind, P. R. & Choppin, P. W. (1978). Evidence for a ninth influenza viral polypeptide. Virology 91, 60-78.
30. Loucaides, E. M., von Kirchbach, J. C., Foeglein, A., Sharps, J., Fodor, E. & Digard, P. (2009). Nuclear dynamics of influenza A virus ribonucleoproteins revealed by live-cell imaging studies. Virology 394, 154-163.
31. Masuda, S., Das, R., Cheng, H., Hurt, E., Dorman, N. & Reed, R. (2005). Recruitment of the human TREX complex to mRNA during splicing. Genes Dev 19, 1512-1517. (Pubitemid 41002995)
32. Mayer, D., Molawi, K., Martinez-Sobrido, L., Ghanem, A., Thomas, S., Baginsky, S., Grossmann, J., Garcia-Sastre, A. & Schwemmle, M. (2007). Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J Proteome Res 6, 672-682. (Pubitemid 46340171)
33. Meignin, C. & Davis, I. (2008). UAP56 RNA helicase is required for axis specification and cytoplasmic mRNA localization in Drosophila. Dev Biol 315, 89-98.
34. Momose, F., Basler, C. F., O'Neill, R. E., Iwamatsu, A., Palese, P. & Nagata, K. (2001). Cellular splicing factor RAF-2p48/NPI-5/BAT1/UAP56 interacts with the influenza virus nucleoprotein and enhances viral RNA synthesis. J Virol 75, 1899-1908. (Pubitemid 32110180)
35. Mullin, A. E., Dalton, R. M., Amorim, M. J., Elton, D. & Digard, P. (2004). Increased amounts of the influenza virus nucleoprotein do not promote higher levels of viral genome replication. J Gen Virol 85, 3689-3698. (Pubitemid 39591876)
36. Neumann, G., Castrucci, M. R. & Kawaoka, Y. (1997). Nuclear import and export of influenza virus nucleoprotein. J Virol 71, 9690-9700. (Pubitemid 27492418)
37. Neumann, G., Brownlee, G. G., Fodor, E. & Kawaoka, Y. (2004). Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 283, 121-143.
38. Nojima, T., Hirose, T., Kimura, H. & Hagiwara, M. (2007). The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export. J Biol Chem 282, 15645-15651. (Pubitemid 47093268)
39. Noton, S. L., Medcalf, E., Fisher, D., Mullin, A. E., Elton, D. & Digard, P. (2007). Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 88, 2280-2290. (Pubitemid 47194226)
40. Rameix-Welti, M. A., Tomoiu, A., Dos Santos Afonso, E., van der Werf, S. & Naffakh, N. (2009). Avian influenza A virus polymerase association with nucleoprotein, but not polymerase assembly, is impaired in human cells during the course of infection. J Virol 83, 1320-1331.
41. Satterly, N., Tsai, P. L., van Deursen, J., Nussenzveig, D. R., Wang, Y., Faria, P. A., Levay, A., Levy, D. E. & Fontoura, B. M. (2007). Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104, 1853-1858. (Pubitemid 46239868)
42. Schneider, J. & Wolff, T. (2009). Nuclear functions of the influenza A and B viruses NS1 proteins: do they play a role in viral mRNA export? Vaccine 27, 6312-6316.
43. Shih, S. R. & Krug, R. M. (1996a). 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 15, 5415-5427.
44. Shih, S. R. & Krug, R. M. (1996b). 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 226, 430-435.
45. Shih, S. R., Nemeroff, M. E. & Krug, R. M. (1995). The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci U S A 92, 6324-6328.
46. Skehel, J. J. (1972). Polypeptide synthesis in influenza virus-infected cells. Virology 49, 23-36.
47. Stamminger, T. (2008). Interactions of human cytomegalovirus proteins with the nuclear transport machinery. Curr Top Microbiol Immunol 325, 167-185.
48. Strasser, K., Masuda, S., Mason, P., Pfannstiel, J., Oppizzi, M., Rodriguez-Navarro, S., Rondon, A. G., Aguilera, A., Struhl, K. & other authors (2002). TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417, 304-308. (Pubitemid 34534714)
49. Tamm, I., Kikuchi, T., Darnell, J. E., Jr & Salditt-Georgieff, M. (1980). Short capped hnRNA precursor chains in HeLa cells: continued synthesis in the presence of 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole. Biochemistry 19, 2743-2748.
50. Tamm, I., Sehgal, P. B., Lamb, R. A. & Goldberg, A. R. (1984). Halogenated ribofuranosylbenzimidazoles. In Antiviral Drugs and Interferon: the Molecular Basis of their Activity, pp. 101-180. Edited by Y. Becker. New York: Martinus Nijhoff.
51. Taniguchi, I. & Ohno, M. (2008). ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol Cell Biol 28, 601-608.
52. Tokunaga, K., Shibuya, T., Ishihama, Y., Tadakuma, H., Ide, M., Yoshida, M., Funatsu, T., Ohshima, Y. & Tani, T. (2006). Nucleocytoplasmic transport of fluorescent mRNA in living mammalian cells: nuclear mRNA export is coupled to ongoing gene transcription. Genes Cells 11, 305-317.
53. Vogel, U., Kunerl, M. & Scholtissek, C. (1994). Influenza A virus late mRNAs are specifically retained in the nucleus in the presence of a methyltransferase or a protein kinase inhibitor. Virology 198, 227-233. (Pubitemid 124018778)
54. Wang, W., Cui, Z. Q., Han, H., Zhang, Z. P., Wei, H. P., Zhou, Y. F., Chen, Z. & Zhang, X. E. (2008). Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res 36, 4913-4928.
55. Whittaker, G., Bui, M. & Helenius, A. (1996). Nuclear trafficking of influenza virus ribonuleoproteins in heterokaryons. J Virol 70, 2743-2756. (Pubitemid 26121888)