Interaction network linking the human H3N2 influenza A virus genomic RNA segments

Vaccine

Volumn 30, Issue 51, 2012, Pages 7359-7367

  Fournier, Emilie ^a   Moules, Vincent ^b   Essere, Boris ^b   Paillart, Jean Christophe ^a   Sirbat, Jean Daniel ^a   Cavalier, Annie ^c   Rolland, Jean Paul ^c   Thomas, Daniel ^c   Lina, Bruno ^b   Isel, Catherine ^a   Marquet, Roland ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Genome packaging; Influenza A; RNA RNA interactions; Supramolecular complex

Indexed keywords

GENOMIC RNA;

ARTICLE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; IN VITRO STUDY; INFLUENZA VIRUS A H3N2; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; RNA STRUCTURE; SIGNAL TRANSDUCTION; VIRION; VIRUS RELEASE;

ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; IMAGING, THREE-DIMENSIONAL; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; NUCLEOPROTEINS; PROTEIN INTERACTION MAPS; RNA, VIRAL; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84870238129     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.09.079     Document Type: Article

References (48)

1. Neumann G., Noda T., Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 2009, 459(June (7249)):931-939.
2. Horimoto T., Kawaoka Y. Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 2005, 3(August (8)):591-600.
3. 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 Pathog 2009, 5(June (6)):e1000491.
4. 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. Proc Natl Acad Sci USA 1987, 84(November (22)):8140-8144.
5. Palese P., Shaw M. Orthomyxoviridae: the viruses and their replication. Fields virology 2006, 1647-1689. Lippincott, Williams and Wilkins, Philadelphia. D.M. Knipe, P.M. Howley (Eds.).
6. Portela A., Digard P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 2002, 83(April (Pt 4)):723-734.
7. Neumann G., Brownlee G.G., Fodor E., Kawaoka Y. Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 2004, 283:121-143.
8. Compans R.W., Content J., Duesberg P.H. Structure of the ribonucleoprotein of influenza virus. J Virol 1972, 10(October (4)):795-800.
9. Heggeness M.H., Smith P.R., Ulmanen I., Krug R.M., Choppin P.W. Studies on the helical nucleocapsid of influenza virus. Virology 1982, 118(April (2)):466-470.
10. 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. J Gen Virol 1995, 76(April (Pt 4)):1009-1014.
11. Noda T., Kawaoka Y. Structure of influenza virus ribonucleoprotein complexes and their packaging into virions. Rev Med Virol 2010, 20(November (6)):380-391.
12. Boulo S., Akarsu H., Ruigrok R.W., Baudin F. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res 2007, 124(March (1-2)):12-21.
13. 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 1989, 105(April (4)):537-546.
14. McGeoch D., Fellner P., Newton C. Influenza virus genome consists of eight distinct RNA species. Proc Natl Acad Sci USA 1976, 73(September (9)):3045-3049.
15. Enami M., Sharma G., Benham C., Palese P. An influenza virus containing nine different RNA segments. Virology 1991, 185(November (1)):291-298.
16. Nakajima K., Sugiura A. Three-factor cross of influenza virus. Virology 1977, 81(September (2)):486-489.
17. Donald H.B., Isaacs A. Counts of influenza virus particles. J Gen Microbiol 1954, 10(June (3)):457-464.
18. Laver W.G., Downie J.C. Influenza virus recombination. I. Matrix protein markers and segregation during mixed infections. Virology 1976, 70(March (1)):105-117.
19. Lubeck M.D., Palese P., Schulman J.L. Nonrandom association of parental genes in influenza A virus recombinants. Virology 1979, 95(May (1)):269-274.
20. Fujii Y., Goto H., Watanabe T., Yoshida T., Kawaoka Y. Selective incorporation of influenza virus RNA segments into virions. Proc Natl Acad Sci USA 2003, 100(February (4)):2002-2007.
21. Hutchinson E.C., von Kirchbach J.C., Gog J.R., Digard P. Genome packaging in influenza A virus. J Gen Virol 2010, 91(February (Pt 2)):313-328.
22. Dos Santos Afonso E., Escriou N., Leclercq I., van der Werf S., Naffakh N. The generation of recombinant influenza A viruses expressing a PB2 fusion protein requires the conservation of a packaging signal overlapping the coding and noncoding regions at the 5' end of the PB2 segment. Virology 2005, 341(October (1)):34-46.
23. Fujii K., Fujii Y., Noda T., Muramoto Y., Watanabe T., Takada A., et al. Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J Virol 2005, 79(March (6)):3766-3774.
24. Liang Y., Hong Y., Parslow T.G. cis-Acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J Virol 2005, 79(August (16)):10348-10355.
25. Marsh G.A., Hatami R., Palese P. Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J Virol 2007, 81(September (18)):9727-9736.
26. Muramoto Y., Takada A., Fujii K., Noda T., Iwatsuki-Horimoto K., Watanabe S., et al. Hierarchy among viral RNA (vRNA) segments in their role in vRNA incorporation into influenza A virions. J Virol 2006, 80(March (5)):2318-2325.
27. Watanabe T., Watanabe S., Noda T., Fujii Y., Kawaoka Y. Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J Virol 2003, 77(October (19)):10575-10583.
28. Ozawa M., Fujii K., Muramoto Y., Yamada S., Yamayoshi S., Takada A., et al. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J Virol 2007, 81(January (1)):30-41.
29. Ozawa M., Maeda J., Iwatsuki-Horimoto K., Watanabe S., Goto H., Horimoto T., et al. Nucleotide sequence requirements at the 5' end of the influenza A virus M RNA segment for efficient virus replication. J Virol 2009, 83(April (7)):3384-3388.
30. Fujii K., Ozawa M., Iwatsuki-Horimoto K., Horimoto T., Kawaoka Y. Incorporation of influenza A virus genome segments does not absolutely require wild-type sequences. J Gen Virol 2009, 90(July (Pt 7)):1734-1740.
31. Gog J.R., Afonso Edos S., Dalton R.M., Leclercq I., Tiley L., Elton D., et al. Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res 2007, 35(6):1897-1907.
32. Marsh G.A., Rabadán R., Levine A.J., Palese P. Highly conserved regions of influenza a virus polymerase gene segments are critical for efficient viral RNA packaging. J Virol 2008, 82(February (5)):2295-2304.
33. Hutchinson E.C., Curran M.D., Read E.K., Gog J.R., Digard P. Mutational analysis of cis-acting RNA signals in segment 7 of influenza A virus. J Virol 2008, 82(December 23):11869-11879.
34. Hutchinson E.C., Wise H.M., Kudryavtseva K., Curran M.D., Digard P. Characterisation of influenza A viruses with mutations in segment 5 packaging signals. Vaccine 2009, 27(October (45)):6270-6275.
35. Harris A., Cardone G., Winkler D.C., Heymann J.B., Brecher M., White J.M., et al. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci USA 2006, 103(December (50)):19123-19127.
36. Noda T., Sagara H., Yen A., Takada A., Kida H., Cheng R.H., et al. Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 2006, 439(January (7075)):490-492.
37. Calder L.J., Wasilewski S., Berriman J.A., Rosenthal P.B. Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci USA 2010, 107(June (23)):10685-10690.
38. Fournier E., Moules V., Essere B., Paillart J.C., Sirbat J.D., Isel C., et al. A supramolecular assembly formed by influenza A virus genomic RNA segments. Nucleic Acids Res 2012, 40(March (5)):2197-2209.
39. Liang Y., Huang T., Ly H., Parslow T.G., Liang Y. Mutational analyses of packaging signals in influenza virus PA, PB1, and PB2 genomic RNA segments. J Virol 2008, 82(December (1)):229-236.
40. Paillart J.C., Shehu-Xhilaga M., Marquet R., Mak J. Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2004, 2(June (6)):461-472.
41. Skripkin E., Paillart J.C., Marquet R., Ehresmann B., Ehresmann C. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc Natl Acad Sci USA 1994, 91(May (11)):4945-4949.
42. Ye Q., Krug R.M., Tao Y.J. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 2006, 444(December (7122)):1078-1082.
43. 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. FASEB J 2008, 22(October (10)):3638-3647.
44. 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. EMBO J 1994, 13(July (13)):3158-3165.
45. Yamanaka K., Ishihama A., Nagata K. Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J Biol Chem 1990, 265(July (19)):11151-11155.
46. Chen L.M., Davis C.T., Zhou H., Cox N.J., Donis R.O. Genetic compatibility and virulence of reassortants derived from contemporary avian H5N1 and human H3N2 influenza A viruses. PLoS Pathog 2008, 4(May (5)):e1000072.
47. Li C., Hatta M., Nidom C.A., Muramoto Y., Watanabe S., Neumann G., et al. Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proc Natl Acad Sci USA 2010, 107(March (10)):4687-4692.
48. Li C., Hatta M., Watanabe S., Neumann G., Kawaoka Y. Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J Virol 2008, 82(December (23)):11880-11888.