Mechanisms and functional implications of the degradation of host RNA polymerase II in influenza virus infected cells

Virology

Volumn 396, Issue 1, 2010, Pages 125-134

  Vreede, Frank T ^a   Chan, Annie Y ^a   Sharps, Jane ^a   Fodor, Ervin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Gene expression; Influenza virus; RNA polymerase II; RNA dependent RNA polymerase; Transcription; Ubiquitylation

Indexed keywords

MESSENGER RNA; PROTEASOME; RNA POLYMERASE; RNA POLYMERASE II; VIRUS RNA;

ARTICLE; BINDING AFFINITY; CELL FUNCTION; CONTROLLED STUDY; EMBRYO; ENZYME BINDING; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME SUBUNIT; GENE EXPRESSION REGULATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VIRUS; MESSENGER RNA SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA REPLICATION; RNA TRANSCRIPTION; TRANSCRIPTION REGULATION; UBIQUITINATION; VIRUS ENTRY;

CELL LINE; HUMANS; INFLUENZA A VIRUS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

EID: 70649087924     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.10.003     Document Type: Article

References (52)

1. Amorim M.J., and Digard P. Influenza A virus and the cell nucleus. Vaccine 24 44-46 (2006) 6651-6655
2. Amorim M.J., Read E.K., Dalton R.M., Medcalf L., and Digard P. Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8 1 (2007) 1-11
3. Bouloy M., Plotch S.J., and Krug R.M. Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proc. Natl. Acad. Sci. U. S. A. 75 10 (1978) 4886-4890
4. Carr S.M., Carnero E., García-Sastre A., Brownlee G.G., and Fodor E. Characterization of a mitochondrial-targeting signal in the PB2 protein of influenza viruses. Virology 344 2 (2006) 492-508
5. Chan A.Y., Vreede F.T., Smith M., Engelhardt O.G., and Fodor E. Influenza virus inhibits RNA polymerase II elongation. Virology 351 1 (2006) 210-217
6. Chen Z., Li Y., and Krug R.M. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J. 18 8 (1999) 2273-2283
7. Deng T., Sharps J., Fodor E., and 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. J. Virol. 79 13 (2005) 8669-8674
8. Didcock L., Young D.F., Goodbourn S., and Randall R.E. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73 12 (1999) 9928-9933
9. Engelhardt O.G., and Fodor E. Functional association between viral and cellular transcription during influenza virus infection. Rev. Med. Virol. 16 5 (2006) 329-345
10. Engelhardt O.G., Smith M., and Fodor E. Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J. Virol. 79 9 (2005) 5812-5818
11. Fechter P., Mingay L., Sharps J., Chambers A., Fodor E., and Brownlee G.G. Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J. Biol. Chem. 278 22 (2003) 20381-20388
12. Fodor E., Crow M., Mingay L.J., Deng T., Sharps J., Fechter P., and Brownlee G.G. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J. Virol. 76 18 (2002) 8989-9001
13. García-Sastre A., and Biron C.A. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312 5775 (2006) 879-882
14. Goldberg A.L., and St John A.C. Intracellular protein degradation in mammalian and bacterial cells: Part 2. Annu. Rev. Biochem. 45 (1976) 747-803
15. Grimm D., Staeheli P., Hufbauer M., Koerner I., Martinez-Sobrido L., Solorzano A., García-Sastre A., Haller O., and Kochs G. Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc. Natl. Acad. Sci. U. S. A. 104 16 (2007) 6806-6811
16. Hagen M., Chung T.D., Butcher J.A., and Krystal M. Recombinant influenza virus polymerase: requirement of both 5′ and 3′ viral ends for endonuclease activity. J. Virol. 68 3 (1994) 1509-1515
17. Hale B.G., Randall R.E., Ortín J., and Jackson D. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89 Pt. 10 (2008) 2359-2376
18. Hatada E., Hasegawa M., Mukaigawa J., Shimizu K., and Fukuda R. Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. J. Biochem. 105 4 (1989) 537-546
19. Hirose Y., and Manley J.L. RNA polymerase II and the integration of nuclear events. Genes. Dev. 14 12 (2000) 1415-1429
20. Howe K.J. RNA polymerase II conducts a symphony of pre-mRNA processing activities. Biochim. Biophys. Acta. 1577 2 (2002) 308-324
21. Jones E., Kimura H., Vigneron M., Wang Z., Roeder R.G., and Cook P.R. Isolation and characterization of monoclonal antibodies directed against subunits of human RNA polymerases I, II, and III. Exp. Cell. Res. 254 1 (2000) 163-172
22. Krug R.M., Broni B.A., and Bouloy M. Are the 5′ ends of influenza viral mRNAs synthesized in vivo donated by host mRNAs?. Cell 18 2 (1979) 329-334
23. Kuo R.L., and Krug R.M. Influenza a virus polymerase is an integral component of the CPSF30-NS1A protein complex in infected cells. J. Virol. 83 4 (2009) 1611-1616
24. Lamb R.A., and Choppin P.W. Synthesis of influenza virus polypeptides in cells resistant to alpha-amanitin: evidence for the involvement of cellular RNA polymerase II in virus replication. J. Virol. 23 3 (1977) 816-819
25. Lee K.H., and Seong B.L. The position 4 nucleotide at the 3′ end of the influenza virus neuraminidase vRNA is involved in temporal regulation of transcription and replication of neuraminidase RNAs and affects the repertoire of influenza virus surface antigens. J. Gen. Virol. 79 Pt. 8 (1998) 1923-1934
26. Loucaides E.M., von Kirchbach J.C., Foeglein A., Sharps J., Fodor E., and Digard P. Nuclear dynamics of influenza A virus ribonucleoproteins revealed by live-cell imaging studies. Virology (2009) 2009 Sep 8 [Epub ahead of print]
27. Lyles D.S. Cytopathogenesis and inhibition of host gene expression by RNA viruses. Microbiol. Mol. Biol. Rev. 64 4 (2000) 709-724
28. Mark G.E., Taylor J.M., Broni B., and Krug R.M. Nuclear accumulation of influenza viral RNA transcripts and the effects of cycloheximide, actinomycin D, and alpha-amanitin. J. Virol. 29 2 (1979) 744-752
29. Mayer D., Molawi K., Martinez-Sobrido L., Ghanem A., Thomas S., Baginsky S., Grossmann J., García-Sastre A., and Schwemmle M. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome. Res. 6 2 (2007) 672-682
30. Naffakh N., Tomoiu A., Rameix-Welti M.A., and van der Werf S. Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annu. Rev. Microbiol. 62 (2008) 403-424
31. Nemeroff M.E., Barabino S.M., Li Y., Keller W., and Krug R.M. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′end formation of cellular pre-mRNAs. Mol. Cell. 1 7 (1998) 991-1000
32. Palancade B., and Bensaude O. Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation. Eur. J. Biochem. 270 19 (2003) 3859-3870
33. Perez D.R., and Donis R.O. The matrix 1 protein of influenza A virus inhibits the transcriptase activity of a model influenza reporter genome in vivo. Virology 249 1 (1998) 52-61
34. Pichlmair A., and Reis e Sousa C. Innate recognition of viruses. Immunity 27 3 (2007) 370-383
35. Proudfoot N.J., Furger A., and Dye M.J. Integrating mRNA processing with transcription. Cell 108 4 (2002) 501-512
36. Rameix-Welti M.A., Tomoiu A., Dos Santos Afonso E., van der Werf S., and Naffakh N. 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 3 (2009) 1320-1331
37. Ratner J.N., Balasubramanian B., Corden J., Warren S.L., and Bregman D.B. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II. Implications for transcription-coupled DNA repair. J. Biol. Chem. 273 9 (1998) 5184-5189
38. Rodriguez A., Pérez-González A., and Nieto A. Influenza virus infection causes specific degradation of the largest subunit of cellular RNA polymerase II. J. Virol. 81 10 (2007) 5315-5324
39. Rodriguez A., Pérez-González A., Hossain M.J., Chen L.M., Rolling T., Pérez-Breña P., Donis R., Kochs G., and Nieto A. Attenuated strains of influenza A viruses do not induce degradation of RNA polymerase II. J. Virol. (2009) 2009 Aug 19 [Epub ahead of print]
40. Sadler A.J., and Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8 7 (2008) 559-568
41. Salomon R., Franks J., Govorkova E.A., Ilyushina N.A., Yen H.L., Hulse-Post D.J., Humberd J., Trichet M., Rehg J.E., Webby R.J., Webster R.G., and Hoffmann E. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J. Exp. Med. 203 3 (2006) 689-697
42. Shapiro G.I., Gurney Jr. T., and Krug R.M. Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs. J. Virol. 61 3 (1987) 764-773
43. Somesh B.P., Reid J., Liu W.F., Søgaard T.M., Erdjument-Bromage H., Tempst P., and Svejstrup J.Q. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121 6 (2005) 913-923
44. Tumpey T.M., Basler C.F., Aguilar P.V., Zeng H., Solórzano A., Swayne D.E., Cox N.J., Katz J.M., Taubenberger J.K., Palese P., and García-Sastre A. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310 5745 (2005) 77-80
45. Vreede F.T., Jung T.E., and Brownlee G.G. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 78 17 (2004) 9568-9572
46. Watanabe K., Handa H., Mizumoto K., and Nagata K. Mechanism for inhibition of influenza virus RNA polymerase activity by matrix protein. J. Virol. 70 1 (1996) 241-247
47. Watanabe T., Watanabe S., Shinya K., Kim J.H., Hatta M., and Kawaoka Y. Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets. Proc. Natl. Acad. Sci. U. S. A. 106 2 (2009) 588-592
48. Weissman A.M. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell. Biol. 2 3 (2001) 169-178
49. West S., Gromak N., and Proudfoot N.J. Human 5′ -> 3′ exonuclease Xrn2 promotes transcription termination at co-transcriptional cleavage sites. Nature 432 7016 (2004) 522-525
50. Yang L.Y., Jiang H., and Rangel K.M. RNA polymerase II stalled on a DNA template during transcription elongation is ubiquitinated and the ubiquitination facilitates displacement of the elongation complex. Int. J. Oncol. 22 3 (2003) 683-689
51. Ye Z.P., Baylor N.W., and Wagner R.R. Transcription-inhibition and RNA-binding domains of influenza A virus matrix protein mapped with anti-idiotypic antibodies and synthetic peptides. J. Virol. 63 9 (1989) 3586-3594
52. Zvonarjev A.Y., and Ghendon Y.Z. Influence of membrane (M) protein on influenza A virus virion transcriptase activity in vitro and its susceptibility to rimantadine. J. Virol. 33 2 (1980) 583-586