Influenza Virus Transcription and Replication

Advances in Virus Research

Volumn 87, Issue , 2013, Pages 113-137

  Martín Benito, Jaime ^a   Ortín, Juan ^a,b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Cryoelectron microscopy; Electron microscopy; Electron tomography; Helical reconstruction; Image processing; Influenza virus; Nucleoprotein; Polymerase; Ribonucleoprotein; RNA replication; RNA transcription; Three dimensional reconstruction

Indexed keywords

EID: 84879569272     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407698-3.00004-1     Document Type: Chapter

References (146)

1. Albertini A.A., Wernimont A.K., Muziol T., Ravelli R.B., Clapier C.R., Schoehn G., et al. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 2006, 313(5785):360-363.
2. Alfonso R., Lutz T., Rodriguez A., Chavez J.P., Rodriguez P., Gutierrez S., et al. CHD6 chromatin remodeler is a negative modulator of influenza virus replication that relocates to inactive chromatin upon infection. Cellular Microbiology 2011, 13(12):1894-1906.
3. Area E., Martín-Benito J., Gastaminza P., Torreira E., Valpuesta J.M., Carrascosa J.L., et al. Three-dimensional structure of the influenza virus RNA polymerase: Localization of subunit domains. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:308-313.
4. Arranz R., Coloma R., Chichón F.J., Conesa J.J., Carrascosa J.L., Valpuesta J.M., et al. The structure of native influenza virion ribonucleoproteins. Science 2012, 338:1634-1637.
5. Baigent S.J., McCauley J.W. Influenza type A in humans, mammals and birds: Determinants of virus virulence, host-range and interspecies transmission. BioEssays 2003, 25(7):657-671.
6. Baudin F., Bach C., Cusack S., Ruigrok R.W. Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. The EMBO Journal 1994, 13(13):3158-3165.
7. Biswas S.K., Boutz P.L., Nayak D.P. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. Journal of Virology 1998, 72(7):5493-5501.
8. Biswas S.K., Nayak D.P. Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1. Journal of Virology 1994, 68:1819-1826.
9. Blaas D., Patzelt E., Keuchler E. Identification of the cap binding protein of influenza virus. Nucleic Acids Research 1982, 10:4803-4812.
10. Boivin S., Hart D.J. Interaction of the influenza A virus polymerase PB2 C-terminal region with importin alpha isoforms provides insights into host adaptation and polymerase assembly. The Journal of Biological Chemistry 2011, 286(12):10439-10448.
11. Boulo S., Akarsu H., Ruigrok R.W., Baudin F. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Research 2007, 124(1-2):12-21.
12. Bouloy M., Plotch S.J., Krug R.M. Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proceedings of the National Academy of Sciences of the United States of America 1978, 75:4886-4890.
13. Brass A.L., Huang I.C., Benita Y., John S.P., Krishnan M.N., Feeley E.M., et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139(7):1243-1254.
14. Bullido R., Gomez-Puertas P., Saiz M.J., Portela A. Influenza A virus NEP (NS2 protein) downregulates RNA synthesis of model template RNAs. Journal of Virology 2001, 75(10):4912-4917.
15. Chase G., Deng T., Fodor E., Leung B.W., Mayer D., Schwemmle M., et al. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 2008, 377(2):431-439.
16. Chen W., Calvo P.A., Malide D., Gibbs J., Schubert U., Bacik I., et al. A novel influenza A virus mitochondrial protein that induces cell death. Nature Medicine 2001, 7(12):1306-1312.
17. Coloma R., Valpuesta J.M., Arranz R., Carrascosa J.L., Ortin J., Martin-Benito J. The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathogens 2009, 5(6):e1000491.
18. Compans R.W., Content J., Duesberg P.H. Structure of the ribonucleoprotein of influenza virus. Journal of Virology 1972, 4:795-800.
19. Crepin T., Dias A., Palencia A., Swale C., Cusack S., Ruigrok R.W. Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. Journal of Virology 2010, 84(18):9096-9104.
20. Deng T., Sharps J., Fodor E., Brownlee G.G. In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. Journal of Virology 2005, 79(13):8669-8674.
21. Deng T., Vreede F.T., Brownlee G.G. Different de novo initiation strategies are used by influenza virus RNA polymerase on its cRNA and viral RNA promoters during viral RNA replication. Journal of Virology 2006, 80(5):2337-2348.
22. Dias A., Bouvier D., Crepin T., McCarthy A.A., Hart D.J., Baudin F., et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009, 458(7240):914-918.
23. Digard P., Blok V.C., Inglis S.C. Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes. Virology 1989, 171(1):162-169.
24. Elton D., Digard P., Tiley L., Ortín J. Structure and function of the influenza virus RNP. Current topics in influenza virology 2005, 1-92. Horizon Scientific Press, Norfolk. Y. Kawaoka (Ed.).
25. Engelhardt O.G., Smith M., Fodor E. Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. Journal of Virology 2005, 79(9):5812-5818.
26. Falcón A.M., Marión R.M., Zürcher T., Gómez P., Portela A., Nieto A., et al. Defective RNA replication and late gene expression in temperature-sensitive (A/Victoria/3/75) influenza viruses expressing deleted forms of NS1 protein. Journal of Virology 2004, 78:3880-3888.
27. Fechter P., Mingay L., Sharps J., Chambers A., Fodor E., Brownlee G.G. Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. The Journal of Biological Chemistry 2003, 278(22):20381-20388.
28. Fislova T., Thomas B., Graef K.M., Fodor E. Association of the influenza virus RNA polymerase subunit PB2 with the host chaperonin CCT. Journal of Virology 2010, 84(17):8691-8699.
29. Flick R., Hobom G. Interaction of influenza virus polymerase with viral RNA in the 'corkscrew' conformation. The Journal of General Virology 1999, 80(Pt. 10):2565-2572.
30. Fodor E., Crow M., Mingay L.J., Deng T., Sharps J., Fechter P., et al. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. Journal of Virology 2002, 76:8989-9001.
31. Fodor E., Pritlove D.C., Brownlee G.G. The influenza virus panhandle is involved in the initiation of transcription. Journal of Virology 1994, 68(6):4092-4096.
32. Fodor E., Smith M. The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. Journal of Virology 2004, 78(17):9144-9153.
33. Gastaminza P., Perales B., Falcón A.M., Ortín J. Influenza virus mutants in the N-terminal region of PB2 protein are affected in virus RNA replication but not transcription. Journal of Virology 2003, 76:5098-5108.
34. Gerritz S.W., Cianci C., Kim S., Pearce B.C., Deminie C., Discotto L., et al. Inhibition of influenza virus replication via small molecules that induce the formation of higher-order nucleoprotein oligomers. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(37):15366-15371.
35. Ghanem A., Mayer D., Chase G., Tegge W., Frank R., Kochs G., et al. Peptide-mediated interference with influenza A virus polymerase. Journal of Virology 2007, 81(14):7801-7804.
36. González S., Ortín J. Characterization of the influenza virus PB1 protein binding to vRNA: Two separate regions of the protein contribute to the interaction domain. Journal of Virology 1999, 73:631-637.
37. González S., Zürcher T., Ortín J. Identification of two separate domains in the influenza virus PB1 protein responsible for interaction with the PB2 and PA subunits: A model for the viral RNA polymerase structure. Nucleic Acids Research 1996, 24:4456-4463.
38. Green T.J., Zhang X., Wertz G.W., Luo M. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 2006, 313(5785):357-360.
39. 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. Nature Structural and Molecular Biology 2008, 15(5):500-506.
40. Hara K., Shiota M., Kido H., Ohtsu Y., Kashiwagi T., Iwahashi J., et al. Influenza virus RNA polymerase PA subunit is a novel serine protease with Ser624 at the active site. Genes to Cells 2001, 6:87-97.
41. Hay A.J., Skehel J.J., McCauley J. Characterization of influenza virus RNA complete transcripts. Virology 1982, 116:517-522.
42. He X., Zhou J., Bartlam M., Zhang R., Ma J., Lou Z., et al. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 2008, 454(7208):1123-1126.
43. Heggeness M.H., Smith P.R., Ulmanen I., Krug R.M., Chopin P.W. Studies on the helical nucleocapsid of influenza virus. Virology 1982, 118:466-470.
44. Hemerka J.N., Wang D., Weng Y., Lu W., Kaushik R.S., Jin J., et al. Detection and characterization of influenza A virus PA-PB2 interaction through a bimolecular fluorescence complementation assay. Journal of Virology 2009, 83(8):3944-3955.
45. Honda A. Role of host protein Ebp1 in influenza virus growth: Intracellular localization of Ebp1 in virus-infected and uninfected cells. Journal of Biotechnology 2008, 133(2):208-212.
46. Honda A., Okamoto T., Ishihama A. Host factor Ebp1: Selective inhibitor of influenza virus transcriptase. Genes to Cells 2007, 12(2):133-142.
47. Honda A., Ueda K., Nagata K., Ishihama A. RNA polymerase of influenza virus: Role of NP in RNA chain elongation. The Journal of Biochemistry (Tokyo) 1988, 104(6):1021-1026.
48. Horimoto T., Kawaoka Y. Influenza: Lessons from past pandemics, warnings from current incidents. Nature Reviews. Microbiology 2005, 3(8):591-600.
49. Hsu M.T., Parvin J.D., Gupta S., Krystal M., Palese P. Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proceedings of the National Academy of Sciences of the United States of America 1987, 84(22):8140-8144.
50. Huang T.S., Palese P., Krystal M. Determination of influenza virus proteins required for genome replication. Journal of Virology 1990, 64(11):5669-5673.
51. Huarte M., Falcon A., Nakaya Y., Ortin J., Garcia-Sastre A., Nieto A. Threonine 157 of influenza virus PA polymerase subunit modulates RNA replication in infectious viruses. Journal of Virology 2003, 77(10):6007-6013.
52. Huarte M., Sanz-Ezquerro J.J., Roncal F., Ortin J., Nieto A. PA subunit from influenza virus polymerase complex interacts with a cellular protein with homology to a family of transcriptional activators. Journal of Virology 2001, 75:8597-8604.
53. Huet S., Avilov S., Ferbitz L., Daigle N., Cusack S., Ellenberg J. Nuclear import and assembly of the influenza A virus RNA polymerase studied in live cells by fluorescence cross correlation spectroscopy. Journal of Virology 2010, 84(3):1254-1264.
54. Hutchinson E.C., Fodor E. Nuclear import of the influenza A virus transcriptional machinery. Vaccine 2012, 30(51):7353-7358.
55. Hutchinson E.C., Orr O.E., Man Liu S., Engelhardt O.G., Fodor E. Characterization of the interaction between the influenza A virus polymerase subunit PB1 and the host nuclear import factor Ran-binding protein 5. The Journal of General Virology 2011, 92(Pt. 8):1859-1869.
56. Jagger B.W., Wise H.M., Kash J.C., Walters K.A., Wills N.M., Xiao Y.L., et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012, 337(6091):199-204.
57. Jennings P.A., Finch J.T., Winter G., Robertson J.S. Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA?. Cell 1983, 34(2):619-627.
58. Jorba N., Area E., Ortin J. Oligomerization of the influenza virus polymerase complex in vivo. The Journal of General Virology 2008, 89(Pt. 2):520-524.
59. Jorba N., Coloma R., Ortin J. Genetic trans-complementation establishes a new model for influenza virus RNA transcription and replication. PLoS Pathogens 2009, 5(5):e1000462.
60. Jorba N., Juarez S., Torreira E., Gastaminza P., Zamarreno N., Albar J.P., et al. Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 2008, 8(10):2077-2088.
61. Karlas A., Machuy N., Shin Y., Pleissner K.P., Artarini A., Heuer D., et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010, 463(7282):818-822.
62. Kawaguchi A., Momose F., Nagata K. Replication-coupled and host factor-mediated encapsidation of the influenza virus genome by viral nucleoprotein. Journal of Virology 2011, 85(13):6197-6204.
63. Klumpp K., Ruigrok R.W., Baudin F. Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. The EMBO Journal 1997, 16(6):1248-1257.
64. Konig R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., et al. Human host factors required for influenza virus replication. Nature 2009, 463(7282):813-817.
65. Kowalinski E., Zubieta C., Wolkerstorfer A., Szolar O.H., Ruigrok R.W., Cusack S. Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) polymerase. PLoS Pathogens 2012, 8(8):e1002831.
66. Kranzusch P., Whelan S. Architecture and regulation of negative-strand viral enzymatic machinery. RNA Biology 2012, 9:941-948.
67. Krug R.M., Broni B.A., Bouloy M. Are the 5'-ends of influenza viral mRNAs synthesized in vivo donated by host mRNAs?. Cell 1979, 18:329-334.
68. 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 Pathogens 2011, 7:e1002397.
69. Lee M.T., Bishop K., Medcalf L., Elton D., Digard P., Tiley L. Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Research 2002, 30(2):429-438.
70. Li X., Palese P. Characterization of the polyadenylation signal of influenza virus RNA. Journal of Virology 1994, 68(2):1245-1249.
71. Li G., Zhang J., Tong X., Liu W., Ye X. Heat shock protein 70 inhibits the activity of Influenza A virus ribonucleoprotein and blocks the replication of virus in vitro and in vivo. PLoS One 2010, 6(2):e16546.
72. Mahy B.W.J. Mutants of influenza virus. Genetics of influenza viruses 1983, 192-253. Springer Verlag, Wien. P. Palese, D.W. Kingsbury (Eds.).
73. Manz B., Brunotte L., Reuther P., Schwemmle M. Adaptive mutations in NEP compensate for defective H5N1 RNA replication in cultured human cells. Nature Communications 2012, 3:802.
74. Marión R.M., Zürcher T., de la Luna S., Ortín J. Influenza virus NS1 protein interacts with viral transcription-replication complexes in vivo. The Journal of General Virology 1997, 78:2447-2451.
75. Marklund J.K., Ye Q., Dong J., Tao Y.J., Krug R.M. Sequence in the influenza a virus nucleoprotein required for viral polymerase binding and RNA synthesis. Journal of Virology 2012, 86(13):7292-7297.
76. Martín-Benito J., Area E., Ortega J., Llorca O., Valpuesta J.M., Carrascosa J.L., et al. Three dimensional reconstruction of a recombinant influenza virus ribonucleoprotein particle. EMBO Reports 2001, 2:313-317.
77. Mayer D., Molawi K., Martinez-Sobrido L., Ghanem A., Thomas S., Baginsky S., et al. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. Journal of Proteome Research 2007, 6(2):672-682.
78. Mena I., Jambrina E., Albo C., Perales B., Ortin J., Arrese M., et al. Mutational analysis of influenza A virus nucleoprotein: Identification of mutations that affect RNA replication. Journal of Virology 1999, 73:1186-1194.
79. Minor P.D., Dimmock N.J. Inhibition of synthesis of influenza virus proteins: Evidence of two host-cell-dependent events during multiplication. Virology 1975, 67(1):114-123.
80. Moeller A., Kirchdoerfer R.N., Potter C.S., Carragher B., Wilson I.A. Organization of the influenza virus replication machinery. Science 2012, 338:1631-1634.
81. Molinari N.A., Ortega-Sanchez I.R., Messonnier M.L., Thompson W.W., Wortley P.M., Weintraub E., et al. The annual impact of seasonal influenza in the US: Measuring disease burden and costs. Vaccine 2007, 25(27):5086-5096.
82. Momose F., Handa H., Nagata K. Identification of host factors that regulate the influenza virus RNA polymerase activity. Biochimie 1996, 78(11-12):1103-1108.
83. Mukaigawa J., Nayak D.P. Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. Journal of Virology 1991, 65:245-253.
84. Murti K.G., Webster R.G., Jones I.M. Localization of RNA polymerases of influenza viral ribonucleoproteins by immunogold labeling. Virology 1988, 164:562-566.
85. Nagata K., Takeuchi K., Ishihama A. In vitro synthesis of influenza viral RNA: Biochemical complementation assay of factors required for influenza virus replication. Journal of Biochemistry 1989, 106(2):205-208.
86. Naito T., Kiyasu Y., Sugiyama K., Kimura A., Nakano R., Matsukage A., et al. An influenza virus replicon system in yeast identified Tat-SF1 as a stimulatory host factor for viral RNA synthesis. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(46):18235-18240.
87. Naito T., Momose F., Kawaguchi A., Nagata K. Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. Journal of Virology 2007, 81(3):1339-1349.
88. Nath S.T., Nayak D.P. Function of two discrete regions is required for nuclear localization of polymerase basic protein 1 of A/WSN/33 influenza virus (H1N1). Molecular and Cellular Biology 1990, 10(8):4139-4145.
89. Neumann G., Brownlee G.G., Fodor E., Kawaoka Y. Orthomyxovirus replication, transcription, and polyadenylation. Current Topics in Microbiology and Immunology 2004, 283:121-143.
90. Neumann G., Noda T., Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 2009, 459(7249):931-939.
91. Newcomb L.L., Kuo R.L., Ye Q., Jiang Y., Tao Y.J., Krug R.M. Interaction of the influenza a virus nucleocapsid protein with the viral RNA polymerase potentiates unprimed viral RNA replication. Journal of Virology 2009, 83(1):29-36.
92. Ng A.K., Lam M.K., Zhang H., Liu J., Au S.W., Chan P.K., et al. Structural basis for RNA binding and homo-oligomer formation by influenza B virus nucleoprotein. Journal of Virology 2012, 86(12):6758-6767.
93. Ng A.K., Zhang H., Tan K., Li Z., Liu J.H., Chan P.K., et al. Structure of the influenza virus A H5N1 nucleoprotein: Implications for RNA binding, oligomerization, and vaccine design. The FASEB Journal 2008, 22(10):3638-3647.
94. Nieto A., de la Luna S., Bárcena J., Portela A., Ortín J. Complex structure of the nuclear translocation signal of the influenza virus polymerase PA subunit. The Journal of General Virology 1994, 75:29-36.
95. Noble E., Cox A., Deval J., Kim B. Endonuclease substrate selectivity characterized with full-length PA of influenza A virus polymerase. Virology 2012, 433(1):27-34.
96. Obayashi E., Yoshida H., Kawai F., Shibayama N., Kawaguchi A., Nagata K., et al. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 2008, 454(7208):1127-1131.
97. Ortega J., Martín-Benito J., Zürcher T., Valpuesta J.M., Carrascosa J.L., Ortín J. Ultrastructural and functional analyses of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification. Journal of Virology 2000, 74:156-163.
98. Palese P., Shaw M. Orthomyxoviridae: The viruses and their replication. Fields virology 2007, Vol. 1:1647-1689. Lippincott Williams & Wilkins, Philadelphia. 5th ed. D.M. Knipe, P.M. Howley (Eds.).
99. Perales B., de la Luna S., Palacios I., Ortín J. Mutational analysis identifies functional domains in the Influenza A PB2 polymerase subunit. Journal of Virology 1996, 70:1678-1686.
100. Perales B., Sanz-Ezquerro J.J., Gastaminza P., Ortega J., Fernández-Santarén J., Ortín J., et al. The replication activity of influenza virus polymerase is linked to the capacity of the PA subunit to induce proteolysis. Journal of Virology 2000, 74:1307-1312.
101. Pérez D.R., Donis R.O. A 48-amino-acid region of influenza A virus PB1 protein is sufficient for complex formation with PA. Journal of Virology 1995, 69:6932-6939.
102. Perez J.T., Varble A., Sachidanandam R., Zlatev I., Manoharan M., Garcia-Sastre A., et al. Influenza A virus-generated small RNAs regulate the switch from transcription to replication. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(25):11525-11530.
103. Perez J.T., Zlatev I., Aggarwal S., Subramanian S., Sachidanandam R., Kim B., et al. A small-RNA enhancer of viral polymerase activity. Journal of Virology 2012, 86(24):13475-13485.
104. Perez-Gonzalez A., Rodriguez A., Huarte M., Salanueva I.J., Nieto A. hCLE/CGI-99, a human protein that interacts with the influenza virus polymerase, is a mRNA transcription modulator. Journal of Molecular Biology 2006, 362(5):887-900.
105. Plotch S.J., Bouloy M., Ulmanen I., Krug R.M. 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.
106. Poch O., Sauvaget I., Delarue M., Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. The EMBO Journal 1990, 8:3867-3874.
107. Pons M.W., Schulze I.T., Hirst G.K. Isolation and characterization of the ribonucleoprotein of influenza virus. Virology 1969, 39:250-259.
108. Poole E., Elton D., Medcalf L., Digard P. Functional domains of the influenza A virus PB2 protein: Identification of NP- and PB1-binding sites. Virology 2004, 321(1):120-133.
109. Poon L.L.M., Pritlove D.C., Fodor E., Brownlee G.G. 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. Journal of Virology 1999, 73(4):3473-3476.
110. Poon L.L., Pritlove D.C., Sharps J., Brownlee G.G. The RNA polymerase of influenza virus, bound to the 5' end of virion RNA, acts in cis to polyadenylate mRNA. Journal of Virology 1998, 72:8214-8219.
111. Pritlove D.C., Poon L.L., Fodor E., Sharps J., Brownlee G.G. Polyadenylation of influenza virus mRNA transcribed in vitro from model virion RNA templates: Requirement for 5' conserved sequences. Journal of Virology 1998, 72:1280-1286.
112. Rao P., Yuan W., Krug R.M. Crucial role of CA cleavage sites in the cap-snatching mechanism for initiating viral mRNA synthesis. The EMBO Journal 2003, 22(5):1188-1198.
113. Resa-Infante P., Jorba N., Coloma R., Ortín J. The influenza virus RNA synthesis machine: Advances in its structure and function. RNA Biology 2011, 8(2):1-9.
114. Resa-Infante P., Jorba N., Zamarreno N., Fernandez Y., Juarez S., Ortin J. The host-dependent interaction of alpha-importins with influenza PB2 polymerase subunit is required for virus RNA replication. PLoS One 2008, 3(12):e3904.
115. Resa-Infante P., Recuero-Checa M.A., Zamarreño N., Llorca O., Ortín J. Structural and functional characterisation of an influenza virus RNA polymerase-genomic RNA complex. Journal of Virology 2010, 84:10477-10487.
116. Robb N.C., Chase G., Bier K., Vreede F.T., Shaw P.C., Naffakh N., et al. The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. Journal of Virology 2011, 85(10):5228-5231.
117. Robb N.C., Smith M., Vreede F.T., Fodor E. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. The Journal of General Virology 2009, 90(Pt. 6):1398-1407.
118. Robertson J.S., Schubert M., Lazzarini R.A. Polyadenylation sites for influenza mRNA. Journal of Virology 1981, 38:157-163.
119. Rodriguez A., Perez-Gonzalez A., Nieto A. Cellular human CLE/C14orf166 protein interacts with influenza virus polymerase and is required for viral replication. Journal of Virology 2011, 85(22):12062-12066.
120. Rudolph M.G., Kraus I., Dickmanns A., Eickmann M., Garten W., Ficner R. Crystal structure of the borna disease virus nucleoprotein. Structure 2003, 11(10):1219-1226.
121. Ruigrok R.W., Baudin F. Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. The Journal of General Virology 1995, 76:1009-1014.
122. Ruigrok R.W., Crepin T., Hart D.J., Cusack S. Towards an atomic resolution understanding of the influenza virus replication machinery. Current Opinion in Structural Biology 2010, 20(1):104-113.
123. Sanz-Ezquerro J.J., Zürcher T., de la Luna S., Ortin J., Nieto A. The amino-terminal one-third of the influenza virus PA protein is responsible for the induction of proteolysis. Journal of Virology 1996, 70:1905-1911.
124. Shapira S.D., Gat-Viks I., Shum B.O., Dricot A., de Grace M.M., Wu L., et al. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 2009, 139(7):1255-1267.
125. Sugiyama K., Obayashi E., Kawaguchi A., Suzuki Y., Tame J.R., Nagata K., et al. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. The EMBO Journal 2009, 28(12):1803-1811.
126. Tafforeau L., Chantier T., Pradezynski F., Pellet J., Mangeot P.E., Vidalain P.O., et al. Generation and comprehensive analysis of an influenza virus polymerase cellular interaction network. Journal of Virology 2011, 85(24):13010-13018.
127. Tarendeau F., Boudet J., Guilligay D., Mas P.J., Bougault C.M., Boulo S., et al. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nature Structural and Molecular Biology 2007, 14(3):229-233.
128. Tarendeau F., Crepin T., Guilligay D., Ruigrok R.W., Cusack S., Hart D.J. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathogens 2008, 4(8):e1000136.
129. Tiley L.S., Hagen M., Mathews J.T., Krystal M. Sequence-specific binding of the influenza virus RNA polymerase to sequences located at the 5'-end of the viral RNAs. Journal of Virology 1994, 68:5108-5116.
130. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D.A., Chen L.M., et al. A distinct lineage of influenza A virus from bats. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(11):4269-4274.
131. Torreira E., Schoehn G., Fernandez Y., Jorba N., Ruigrok R.W., Cusack S., et al. Three-dimensional model for the isolated recombinant influenza virus polymerase heterotrimer. Nucleic Acids Research 2007, 35(11):3774-3783.
132. Toyoda T., Adyshev D.M., Kobayashi M., Iwata A., Ishihama A. Molecular assembly of the influenza virus RNA polymerase: Determination of the subunit-subunit contact sites. The Journal of General Virology 1996, 77:2149-2157.
133. Turrell L., Lyall J.W., Tiley L.S., Fodor E., Vreede F.T. The role and assembly mechanism of nucleoprotein in influenza A virus ribonucleoprotein complexes. Nature Communications 2013, 4:1591.
134. Ulmanen I., Broni B.A., Krug R.M. The role of two of the influenza virus core P proteins in recognizing cap 1 structures (m7GpppNm) on RNAs and in initiating viral RNA transcription. Proceedings of the National Academy of Sciences of the United States of America 1981, 78:7355-7359.
135. Vreede F.T., Brownlee G.G. Influenza virion-derived viral ribonucleoproteins synthesize both mRNA and cRNA in vitro. Journal of Virology 2007, 81(5):2196-2204.
136. Vreede F.T., Gifford H., Brownlee G.G. Role of initiating nucleoside triphosphate concentrations in the regulation of influenza virus replication and transcription. Journal of Virology 2008, 82(14):6902-6910.
137. Vreede F.T., Jung T.E., Brownlee G.G. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. Journal of Virology 2004, 78(17):9568-9572.
138. Wang Z., Liu X., Zhao Z., Xu C., Zhang K., Chen C., et al. Cyclophilin E functions as a negative regulator to influenza virus replication by impairing the formation of the viral ribonucleoprotein complex. PLoS One 2011, 6(8):e22625.
139. Wang P., Song W., Mok B.W., Zhao P., Qin K., Lai A., et al. Nuclear factor 90 negatively regulates influenza virus replication by interacting with viral nucleoprotein. Journal of Virology 2009, 83(16):7850-7861.
140. Wise H.M., Foeglein A., Sun J., Dalton R.M., Patel S., Howard W., et al. A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. Journal of Virology 2009, 83(16):8021-8031.
141. Wolstenholme A.J., Barrett T., Nichol S.T., Mahy B.W. Influenza virus-specific RNA and protein syntheses in cells infected with temperature-sensitive mutants defective in the genome segment encoding nonstructural proteins. Journal of Virology 1980, 35(1):1-7.
142. Yamanaka K., Ishihama A., Nagata K. Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. The Journal of Biological Chemistry 1990, 265(19):11151-11155.
143. Ye Q., Krug R.M., Tao Y.J. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 2006, 444(7122):1078-1082.
144. 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(7240):909-913.
145. Zhang S., Wang J., Wang Q., Toyoda T. Internal initiation of influenza virus replication of viral RNA and complementary RNA in vitro. The Journal of Biological Chemistry 2010, 285(52):41194-41201.
146. Zürcher T., de la Luna S., Sanz-Ezquerro J.J., Nieto A., Ortín J. Mutational analysis of the influenza virus A/Victoria/3/75 PA protein: Studies of interaction with PB1 protein and identification of a dominant negative mutant. The Journal of General Virology 1996, 77:1745-1749.