Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity

Traffic

Volumn 8, Issue 1, 2007, Pages 1-11

  Amorim, Maria Joao ^a   Read, Eliot K ^a   Dalton, Rosa M ^a   Medcalf, Liz ^a   Digard, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

amanitin; Actinomycin D; Camptothecin; H7; Leptomycin B; Splicing; Transcription

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; ENZYME INHIBITOR; MESSENGER RNA; PROTEIN HA; PROTEIN M1; PROTEIN NP; PROTEIN NS1; PROTEIN NS2; RNA POLYMERASE II; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RNA STRUCTURE; RNA TRANSCRIPTION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BASE SEQUENCE; CELL LINE; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; DOGS; GENE EXPRESSION; GENES, VIRAL; HUMANS; INFLUENZA A VIRUS; RNA POLYMERASE II; RNA, MESSENGER; RNA, VIRAL;

EID: 33845548158     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2006.00507.x     Document Type: Article

References (66)

1. Herz C, Stavnezer E, Krug R, Gurney T Jr. Influenza virus, an RNA virus, synthesizes its messenger RNA in the nucleus of infected cells. Cell 1981; 26: 391-400.
2. Elton D, Digard P, Tiley L, Ortin J. Structure and function of the influenza virus RNP. In: Kawaoka Y, editor. Influenza Virology: Current Topics. Norfolk: Horizon Scientific Press 2006; 1-36.
3. Barrett T, Wolstenholme AJ, Mahy BW. Transcription and replication of influenza virus RNA. Virology 1979; 98: 211-225.
4. Inglis SC, Mahy BW. Polypeptides specified by the influenza virus genome. 3. Control of synthesis in infected cells. Virology 1979; 95: 154-164.
5. Smith GL, Hay AJ. Replication of the influenza virus genome. Virology 1982; 118: 96-108.
6. Shapiro GI, Gurney T Jr, Krug RM. Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs. J Virol 1987; 61: 764-773.
7. Hatada E, Hasegawa M, Mukaigawa J, Shimizu K, Fukuda R. Control of influenza virus gene expression: Quantitative analysis of each viral RNA species in infected cells. J Biochem (Tokyo) 1989; 105: 537-546.
8. 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: 475-485.
9. 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 U S A 1981; 78: 4170-4174.
10. Kelly DC, Avery RJ, Dimmock NJ. Camptothecin: An inhibitor of influenza virus replication. J Gen Virol 1974; 25: 427-432.
11. Tamm I, Folkers K, Shunk CH, Horsfall FL Jr. Inhibition of influenza virus multiplication by N-glycosides of benzimidazoles-N. J Exp Med 1954; 99: 227-250.
12. Minor PD, Dimmock NJ. Inhibition of synthesis of influenza virus proteins: Evidence of two host-cell-dependent events during multiplication. Virology 1975; 67: 114-123.
13. Barry RD, Ives DR, Cruickshank JG. Participation of deoxyribonucleic acid in the multiplication of influenza virus. Nature 1962; 194: 1139-1140.
14. Barry RD. The effects of actinomycin D and ultraviolet irradiation on the production of fowl plague virus. Virology 1964; 24: 563-569.
15. Spooner LL, Barry RD. Participation of DNA-dependent RNA polymerase II in replication of influenza viruses. Nature 1977; 268: 650-652.
16. Robertson JS, Schubert M, Lazzarini RA. Polyadenylation sites for influenza virus mRNA. J Virol 1981; 38: 157-163.
17. Plotch SJ, Krug RM. Influenza virion transcriptase: Synthesis in vitro of large, polyadenylic acid-containing complementary RNA. J Virol 1977; 21: 24-34.
18. Plotch SJ, Bouloy M, Krug RM. Transfer of 5'-terminal cap of globin mRNA to influenza viral complementary RNA during transcription in vitro. Proc Natl Acad Sci U S A 1979; 76: 1618-1622.
19. Plotch SJ, Bouloy M, Ulmanen I, Krug RM. A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 1981; 23: 847-858.
20. Caton AJ, Robertson JS. Structure of the host-derived sequences present at the 5′ ends of influenza virus mRNA. Nucleic Acids Res 1980; 8: 2591-2603.
21. Skehel JJ. Early polypeptide synthesis in influenza virus-infected cells. Virology 1973; 56: 394-399.
22. Mark GE, Taylor JM, Broni B, Krug RM. Nuclear accumulation of influenza viral RNA transcripts and the effects of cycloheximide, actinomycin D, and alpha-amanitin. J Virol 1979; 29: 744-752.
23. Mahy BW, Barrett T, Briedis DJ, Brownson JM, Wolstenholme AJ. Influence of the host cell on influenza virus replication. Philos Trans R Soc Lond B Biol Sci 1980; 288: 349-357.
24. Kistner O, Muller K, Scholtissek C. Differential phosphorylation of the nucleoprotein of influenza A viruses. J Gen Virol 1989; 70: 2421-2431.
25. Kurokawa M, Ochiai H, Nakajima K, Niwayama S. Inhibitory effect of protein kinase C inhibitor on the replication of influenza type A virus. J Gen Virol 1990; 71: 2149-2155.
26. Vogel U, Kunerl M, Scholtissek C. Influenza A virus late mRNAs are specifically retained in the nucleus in the presence of a methyltransferase or a protein kinase inhibitor. Virology 1994; 198: 227-233.
27. Howe KJ. RNA polymerase II conducts a symphony of pre-mRNA processing activities. Biochim Biophys Acta 2002; 1577: 308-324.
28. Fasken MB, Corbett AH. Process or perish: Quality control in mRNA biogenesis. Nat Struct Mol Biol 2005; 12: 482-488.
29. Krug RM, Morgan MA, Shatkin AJ. Influenza viral mRNA contains internal N6-methyladenosine and 5′-terminal 7-methylguanosine in cap structures. J Virol 1976; 20: 45-53.
30. Bensaude O, Bonnet F, Casse C, Dubois MF, Nguyen VT, Palancade B. Regulated phosphorylation of the RNA polymerase II C-terminal domain (CTD). Biochem Cell Biol 1999; 77: 249-255.
31. Palancade B, Bensaude O. Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation. Eur J Biochem 2003; 270: 3859-3870.
32. Ares M Jr, Proudfoot NJ. The spanish connection: Transcription and mRNA processing get even closer. Cell 2005; 120: 163-166.
33. Chan AY, Vreede FT, Smith M, Engelhardt OG, Fodor E. Influenza virus inhibits RNA polymerase II elongation. Virology 2006; 351: 210-217.
34. 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: 5812-5818.
35. Fraser NW, Sehgal PB, Darnell JE. DRB-induced premature termination of late adenovirus transcription. Nature 1978; 272: 590-593.
36. Tamm I, Kikuchi T, Darnell JE Jr, Salditt-Georgieff M. Short capped hnRNA precursor chains in HeLa cells: Continued synthesis in the presence of 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole. Biochemistry 1980; 19: 2743-2748.
37. Clement JQ, Wilkinson MF. Rapid induction of nuclear transcripts and inhibition of intron decay in response to the polymerase II inhibitor DRB. J Mol Biol 2000; 299: 1179-1191.
38. Mancebo HS, Lee G, Flygare J, Tomassini J, Luu P, Zhu Y, Peng J, Blau C, Hazuda D, Price D, Flores O. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev 1997; 11: 2633-2644.
39. Yamaguchi Y, Wada T, Handa H. Interplay between positive and negative elongation factors: Drawing a new view of DRB. Genes Cells 1998; 3: 9-15.
40. Dubois MF, Nguyen VT, Bellier S, Bensaude O. Inhibitors of transcription such as 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole and isoquinoline sulfonamide derivatives (H-8 and H-7) promote dephosphorylation of the carboxyl-terminal domain of RNA polymerase II largest subunit. J Biol Chem 1994; 269: 13331-13336.
41. Mullin AE, Dalton RM, Amorim MJ, Elton D, Digard P. Increased amounts of the influenza virus nucleoprotein do not promote higher levels of viral genome replication. J Gen Virol 2004; 85: 3689-3698.
42. Dasso MC, Jackson RJ. On the fidelity of mRNA translation in the nuclease-treated rabbit reticulocyte lysate system. Nucleic Acids Res 1989; 17: 3129-3144.
43. Bouloy M, Plotch SJ, Krug RM. Both the 7-methyl and the 2′-O-methyl groups in the cap of mRNA strongly influence its ability to act as primer for influenza virus RNA transcription. Proc Natl Acad Sci U S A 1980; 77: 3952-3956.
44. Hsiang YH, Hertzberg R, Hecht S, Liu LF. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J Biol Chem 1985; 260: 14873-14878.
45. Li TK, Liu LF. Tumor cell death induced by topoisomerase-targeting drugs. Annu Rev Pharmacol Toxicol 2001; 41: 53-77.
46. Perry RP, Kelley DE. Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J Cell Physiol 1970; 76: 127-139.
47. Yankulov K, Yamashita K, Roy R, Egly JM, Bentley DL. The transcriptional elongation inhibitor 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase. J Biol Chem 1995; 270: 23922-23925.
48. Kumahara E, Ebihara T, Saffen D. Protein kinase inhibitor H7 blocks the induction of immediate-early genes zif268 and c-fos by a mechanism unrelated to inhibition of protein kinase C but possibly related to inhibition of phosphorylation of RNA polymerase II. J Biol Chem 1999; 274: 10430-10438.
49. Sidwell RW, Huffman JH, Khare GP, Allen LB, Witkowski JT, Robins RK. Broad-spectrum antiviral activity of Virazole: 1-beta-D-ribofuranosyl-1,2,4-triazole-3-carboxamide. Science 1972; 177: 705-706.
50. Wray SK, Gilbert BE, Knight V. Effect of ribavirin triphosphate on primer generation and elongation during influenza virus transcription in vitro. Antiviral Res 1985; 5: 39-48.
51. Wray SK, Gilbert BE, Noall MW, Knight V. Mode of action of ribavirin: effect of nucleotide pool alterations on influenza virus ribonucleoprotein synthesis. Antiviral Res 1985; 5: 29-37.
52. Nguyen VT, Giannoni F, Dubois MF, Seo SJ, Vigneron M, Kedinger C, Bensaude O. In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res 1996; 24: 2924-2929.
53. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci U S A 1999; 96: 9112-9117.
54. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, McCauley J, Digard P. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 2001; 75: 408-419.
55. Elton D, Amorim MJ, Medcalf L, Digard P. 'Genome gating'; polarised intranuclear trafficking of influenza virus RNPs. Biol Lett 2005; 1: 113-117.
56. Taylor JM, Illmensee R, Litwin S, Herring L, Broni B, Krug RM. Use of specific radioactive probes to study transcription and replication of the influenza virus genome. J Virol 1977; 21: 530-540.
57. Martin K, Helenius A. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 1991; 67: 117-130.
58. Bui M, Wills EG, Helenius A, Whittaker GR. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J Virol 2000; 74: 1781-1786.
59. Hidaka H, Inagaki M, Kawamoto S, Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 1984; 23: 5036-5041.
60. Amorim MJ, Digard P. Influenza A virus and the cell nucleus. Vaccine 2006; 24: 6651-6655.
61. Pinol-Roma S, Dreyfuss G. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science 1991; 253: 312-314.
62. Brennan CM, Gallouzi IE, Steitz JA. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J Cell Biol 2000; 151: 1-14.
63. Bird G, Zorio DA, Bentley DL. RNA polymerase II carboxy-terminal domain phosphorylation is required for cotranscriptional pre-mRNA splicing and 3′-end formation. Mol Cell Biol 2004; 24: 8963-8969.
64. 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 U S A 1995; 92: 6324-6328.
65. Carrasco M, Amorim MJ, Digard P. Lipid raft-dependent targeting of the influenza A virus nucleoprotein to the apical plasma membrane. Traffic 2004; 5: 979-992.
66. Dalton RM, Mullin AE, Amorim MJ, Medcalf E, Tiley LS, Digard P. Temperature sensitive influenza A virus genome replication results from low thermal stability of polymerase-cRNA complexes. Virol J 2006; 3: 58.