Inefficient splicing of segment 7 and 8 mRNAs is an inherent property of influenza virus A/Brevig Mission/1918/1 (H1N1) that causes elevated expression of NS1 protein

Virology

Volumn 422, Issue 1, 2012, Pages 46-58

  Backström Winquist, Ellenor ^a,b   Abdurahman, Samir ^b   Tranell, Anna ^b   Lindström, Sofia ^b   Tingsborg, Susanne ^b   Schwartz, Stefan ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

ASF SF2; Influenza; NS1; Polyadenylation; Spanish flu; Splicing; SR proteins; SRp30c; SRp40

Indexed keywords

NONSTRUCTURAL PROTEIN 1; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC POLYMORPHISM; HUMAN; HUMAN CELL; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA SPLICING; RNA STRUCTURE; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; GENES, VIRAL; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; PLASMIDS; RNA SPLICING; RNA, MESSENGER; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 82355190150     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.10.004     Document Type: Article

References (59)

1. Aragon T., de la Luna S., Novoa I., Carrasco L., Ortin J., Nieto A. Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol. Cell. Biol. 2000, 20:6259-6268.
2. Basler C.F., Aguilar P.V. Progress in identifying virulence determinants of the 1918 H1N1 and the Southeast Asian H5N1 influenza A viruses. Antiviral Res. 2008, 79:166-178.
3. Basler C.F., Reid A.H., Dybing J.K., Janczewski T.A., Fanning T.G., Zheng H., Salvatore M., Perdue M.L., Swayne D.E., Garcia-Sastre A., Palese P., Taubenberger J.K. Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2746-2751.
4. Billharz R., Zeng H., Proll S.C., Korth M.J., Lederer S., Albrecht R., Goodman A.G., Rosenzweig E., Tumpey T.M., Garcia-Sastre A., Katze M.G. The NS1 protein of the 1918 pandemic influenza virus blocks host interferon and lipid metabolism pathways. J. Virol. 2009, 83:10557-10570.
5. Blencowe B.J. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 2000, 25:106-110.
6. C, Centers for disease control, prevention Isolation of avian influenza A (H5N1) from humans - Hong Kong, May-December, 1997. Morbid. Mortal. Weekly Rep. 1997, 46:1204-1207.
7. Cartegni L., Chew S.L., Krainer A.R. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 2002, 3:285-298.
8. Cartegni L., Wang J., Zhu Z., Zhang M.Q., Krainer A.R. ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 2003, 31:3568-3571.
9. Cazalla D., Zhu J., Manche L., Huber E., Krainer A.R., Caceres J.F. Nuclear export and retention signals in the RS domain of SR proteins. Mol. Cell. Biol. 2002, 22:6871-6882.
10. Cheung T.K., Guan Y., Ng S.S., Chen H., Wong C.H., Peiris J.S., Poon L.L. Generation of recombinant influenza A virus without M2 ion-channel protein by introduction of a point mutation at the 5' end of the viral intron. J. Gen. Virol. 2005, 86:1447-1454.
11. Collier B., Öberg D., Zhao X., Schwartz S. Specific inactivation of inhibitory sequences in the 5' end of the human papillomavirus type 16 L1 open reading frame results in production of high levels of L1 protein in human epithelial cells. J. Virol. 2002, 76:2739-2752.
12. de la Grange P., Gratadou L., Delord M., Dutertre M., Auboeuf D. Splicing factor and exon profiling across human tissues. Nucleic Acids Res. 2010, 38:2825-2838.
13. de Wit E., Fouchier R.A. Emerging influenza. J. Clin. Virol. 2008, 41:1-6.
14. Fackenthal J.D., Godley L.A. Aberrant RNA splicing and its functional consequences in cancer cells. Dis. Model. Mech. 2008, 1:37-42.
15. Fay J., Kelehan P., Lambkin H., Schwartz S. Increased expression of cellular RNA-binding proteins in HPV-induced neoplasia and cervical cancer. J. Med. Virol. 2009, 81:897-907.
16. Fortes P., Beloso A., Ortin J. Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J. 1994, 13:704-712.
17. Fortes P., Lamond A.I., Ortin J. Influenza virus NS1 protein alters the subnuclear localization of cellular splicing components. J. Gen. Virol. 1995, 76(Pt 4):1001-1007.
18. Garaigorta U., Ortin 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, 35:4573-4582.
19. Graveley B.R. Sorting out the complexity of SR protein functions. RNA 2000, 6:1197-1211.
20. Grosso A.R., Gomes A.Q., Barbosa-Morais N.L., Caldeira S., Thorne N.P., Grech G., von Lindern M., Carmo-Fonseca M. Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res. 2008, 36:4823-4832.
21. Gultyaev A.P., Heus H.A., Olsthoorn R.C. An RNA conformational shift in recent H5N1 influenza A viruses. Bioinformatics 2007, 23:272-276.
22. Hale B.G., Randall R.E., Ortin J., Jackson D. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 2008, 89:2359-2376.
23. Hatada E., Takizawa T., Fukuda R. Specific binding of influenza A virus NS1 protein to the minus-sense RNA. J. Gen. Virol. 1992, 73:17-25.
24. Huang Y., Steitz J.A. Splicing factors SRp20 and 9 G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 2001, 7:899-905.
25. Jackson D., Lamb R.A. The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J. Gen. Virol. 2008, 89:3097-3101.
26. Johansson C., Zhao H., Bajak E., Granberg F., Pettersson U., Svensson C. Impact of the interaction between adenovirus E1A and CtBP on host cell gene expression. Virus Res. 2005, 113:51-63.
27. Kalthoff D., Globig A., Beer M. (Highly pathogenic) avian influenza as a zoonotic agent. Vet. Microbiol. 2010, 140:237-245.
28. Karlas A., Machuy N., Shin Y., Pleissner K.P., Artarini A., Heuer D., Becker D., Khalil H., Ogilvie L.A., Hess S., Maurer A.P., Muller E., Wolff T., Rudel T., Meyer T.F. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010, 463:818-822.
29. Lamb R.A., Lai C.-H. Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for the two overlapping nonstructural proteins of infeluenza virus. Cell 1980, 21:475-485.
30. Lamb R.A., Lai C.H., Choppin P.W. 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.
31. Lamb R.A., Lai C.J. Spliced and unspliced messenger RNAs synthesized from cloned influenza virus M DNA in an SV40 vector: expression of the influenza virus membrane protein (M1). Virology 1982, 123:237-256.
32. Lee C.-W., Jung K., Jadhao S.J., Suarez D.L. Evaluation of chicken-origin (DF-1) and quail-origin (QT-6) fibroblast cell lines for replication of avian influenza viruses. J. Virol. Meth. 2008, 153:22-28.
33. Long J.C., Caceres J.F. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 2009, 417:15-27.
34. Lu Y., Qian X.Y., Krug R.M. The influenza virus NS1 protein: a novel inhibitor of pre-mRNA splicing. Genes Dev. 1994, 8:1817-1828.
35. Moscovici C., Moscovici M.G., Jimenez H., Lai M.M., Hayman M.J., Vogt P.K. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell 1977, 11:95-103.
36. Muraki Y., Furukawa T., Kohno Y., Matsuzaki Y., Takashita E., Sugawara K., Hongo S. Influenza C virus NS1 protein upregulates the splicing of viral mRNAs. J. Virol. 2010, 84:1957-1966.
37. Nemeroff M.E., Barabino S.M., Li Y., Keller W., 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 1998, 1:991-1000.
38. Nemeroff M.E., Utans U., Kramer A., Krug R.M. Identification of cis-acting intron and exon regions in influenza virus NS1 mRNA that inhibit splicing and cause the formation of aberrantly sedimenting presplicing complexes. Mol. Cell. Biol. 1992, 12:962-970.
39. Neumann G., Kawaoka Y. Reverse genetics of influenza virus. Virology 2001, 287:243-250.
40. Neumann G., Watanabe T., Kawaoka Y. Plasmid-driven formation of influenza virus-like particles. J. Virol. 2000, 74:547-551.
41. O'Neil R.E., Talon J., Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J. 1998, 17:288-296.
42. Palese P., Shaw M. Orthomyxoviridae: the viruses and their replication. Fields Virology 2006, 1647-1689. Lippincott Williams & Wilkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley (Eds.).
43. Reid A.H., Fanning T.G., Janczewski T.A., McCall S., Taubenberger J.K. Characterization of the 1918 "Spanish" influenza virus matrix gene segment. J. Virol. 2002, 76:10717-10723.
44. Reid A.H., Taubenberger J.K., Fanning T.G. Evidence of an absence: the genetic origins of the 1918 pandemic influenza virus. Nat. Rev. Microbiol. 2004, 2:909-914.
45. Rimmelzwaan G.F., Nieuwkoop N.J., de Mutsert G., Boon A.C., Kuiken T., Fouchier R.A., Osterhaus A.D. Attachment of infectious influenza A viruses of various subtypes to live mammalian and avian cells as measured by flow cytometry. Virus Res. 2007, 129:175-181.
46. Robb N.C., Fodor E. The accumulation of influenza A virus segment 7 mRNAs is regulated by the NS1 protein. J. Gen. Virol. 2011, 10.1099/vir.0.0354585-0.
47. Robb N.C., Jackson D., Vreede F.T., Fodor E. Splicing of influenza A virus NS1 mRNA is independent of the viral NS1 protein. J. Gen. Virol. 2010, 91:2331-2340.
48. Shepard P.J., Hertel K.J. The SR protein family. Genome Biol. 2009, 10:242.
49. Shih S.R., Krug R.M. 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, 15:5415-5427.
50. Shih S.R., Nemeroff M.E., Krug R.M. 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.
51. Somberg M., Li X., Johansson C., Orru B., Chang R., Rush M., Fay J., Ryan F., Schwartz S. SRp30c activates human papillomavirus type 16 L1 mRNA expression via a bimodal mechanism. J. Gen. Virol. 2011, 92:2411-2421.
52. Taubenberger J.K. The origin and virulence of the 1918 "Spanish" influenza virus. Proc. Am. Philos. Soc. 2006, 150:86-112.
53. Tranell A., Fenyö E.M., Schwartz S. Serine- and arginine-rich proteins 55 and 75 (SRp55 and SRp75) induce production of HIV-1 vpr mRNA by inhibiting the 5'-splice site of exon 3. J. Biol. Chem. 2010, 285:31537-31547.
54. Tumpey T.M., Basler C.F., Aguilar P.V., Zeng H., Solorzano A., Swayne D.E., Cox N.J., Katz J.M., Taubenberger J.K., Palese P., Garcia-Sastre A. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 2005, 310:77-80.
55. Valcarcel J., Portela A., Ortin J. Regulated M1 mRNA splicing in influenza virus-infected cells. J. Gen. Virol. 1991, 72(Pt 6):1301-1308.
56. Wolschek M., Samm E., Seper H., Sturlan S., Kuznetsova I., Schwager C., Khassidov A., Kittel C., Muster T., Egorov A., Bergmann M. Establishment of a chimeric, replication-deficient influenza A virus vector by modulation of splicing efficiency. J. Virol. 2011, 85:2469-2473.
57. Xu X., Subbarao Cox N.J., Guo Y. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 1999, 261:15-19.
58. Zhao X., Rush M., Schwartz S. Identification of an hnRNP A1 dependent splicing silencer in the HPV-16 L1 coding region that prevents premature expression of the late L1 gene. J. Virol. 2004, 78:10888-10905.
59. Zhong X.Y., Wang P., Han J., Rosenfeld M.G., Fu X.D. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 2009, 35:1-10.