Time-resolved visualisation of nearly-native influenza A virus progeny ribonucleoproteins and their individual components in live infected cells

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Avilov, Sergiy ^a,e   Magnus, Julie ^b,c,d   Cusack, Stephen ^a   Naffakh, Nadia ^b,c,d  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b Sorbonne Paris Cité   (France)

^c Institut Pasteur   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HYBRID PROTEIN; PB2 PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VIRUS NUCLEOPROTEIN; VIRUS PROTEIN; VIRUS RIBONUCLEOPROTEIN; VIRUS RNA; GREEN FLUORESCENT PROTEIN;

ARTICLE; CELL LABELING; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; GENETIC CODE; INFLUENZA A; INFLUENZA A VIRUS; NONHUMAN; PROGENY; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS ENTRY; VIRUS RECOMBINANT; VIRUS STRAIN; ANIMAL; CELL LINE; CELL MEMBRANE; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; PROTEIN TRANSPORT; SPECTROFLUOROMETRY;

ANIMALS; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; GREEN FLUORESCENT PROTEINS; HUMANS; INFLUENZA A VIRUS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RIBONUCLEOPROTEINS; SPECTROMETRY, FLUORESCENCE;

EID: 84962329056     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149986     Document Type: Article

References (53)

1. Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza A viruses. Currenttopics in microbiology and immunology. 2014; 385:359-75. Epub 2014/07/06. doi: 10.1007/82 2014 396 PMID: 24990620.
2. Schrauwen EJ, Fouchier RA. Host adaptation and transmission of influenza A viruses in mammals. Emerging microbes & infections. 2014; 3(2):e9. Epub 2014/02/01. doi: 10.1038/emi.2014.9 PMID: 26038511; PubMed Central PMCID: PMC3944123.
3. Arranz R, Coloma R, Chichon FJ, Conesa JJ, Carrascosa JL, Valpuesta JM, et al. The Structure of Native Influenza Virion Ribonucleoproteins. Science. 2012; 338(6114):1634-7. doi: 10.1126/science.1228172 PMID: 23180776.
4. Moeller A, Kirchdoerfer RN, Potter CS, Carragher B, Wilson IA. Organization of the Influenza Virus Replication Machinery. Science. 2012; 338(6114):1631-4. doi: 10.1126/science.1227270 PMID: 23180774.
5. Ortin J, Martin-Benito J. The RNA synthesis machinery of negative-stranded RNA viruses. Virology. 2015; 479-480:532-44. Epub 2015/04/01. doi: 10.1016/j.virol.2015.03.018 PMID: 25824479.
6. Hutchinson EC, Fodor E. Transport of the influenza virus genome from nucleus to nucleus. Viruses. 2013; 5(10):2424-46. Epub 2013/10/10. doi: 10.3390/v5102424 PMID: 24104053; PubMed Central PMCID: PMC3814596.
7. Elton D, Medcalf L, Bishop K, Harrison D, Digard P. Identification of Amino Acid Residues of Influenza Virus Nucleoprotein Essential for RNA Binding. J Virol. 1999; 73(9):7357-67. PMID: 10438825.
8. Ng AK-L, Zhang H, Tan K, Li Z, Liu J-h, Chan PK-S, et al. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. The FASEB Journal. 2008; 22(10):3638-47. doi: 10.1096/fj.08-112110 PMID: 18614582.
9. Chan WH, Ng AK, Robb NC, Lam MK, Chan PK, Au SW, et al. Functional analysis of the influenza virus H5N1 nucleoprotein tail loop reveals amino acids that are crucial for oligomerization and ribonucleoprotein activities. J Virol. 2010; 84(14):7337-45. Epub 2010/05/14. doi: 10.1128/JVI.02474-09 PMID: 20463064; PubMed Central PMCID: PMC2898228.
10. Tarus B, Bakowiez O, Chenavas S, Duchemin L, Estrozi LF, Bourdieu C, et al. Oligomerization paths of the nucleoprotein of influenza A virus. Biochimie. 2012; 94(3):776-85. doi: 10.1016/j.biochi.2011.11.009 PMID: 22155087.
11. Turrell L, Lyall JW, Tiley LS, Fodor E, Vreede FT. The role and assembly mechanism of nucleoprotein in influenza A virus ribonucleoprotein complexes. Nat Commun. 2013; 4:1591. doi: 10.1038/ncomms2589 PMID: 23481399.
12. Turrell L, Hutchinson EC, Vreede FT, Fodor E. Regulation of influenza A virus nucleoprotein oligomerization by phosphorylation. J Virol. 2015; 89(2):1452-5. Epub 2014/10/31. doi: 10.1128/JVI.02332-14 PMID: 25355893; PubMed Central PMCID: PMC4300657.
13. Mondal A, Potts GK, Dawson AR, Coon JJ, Mehle A. Phosphorylation at the homotypic interface regulates nucleoprotein oligomerization and assembly of the influenza virus replication machinery. PLoS pathogens. 2015; 11(4):e1004826. Epub 2015/04/14. doi: 10.1371/journal.ppat.1004826 PMID: 25867750; PubMed Central PMCID: PMC4395114.
14. Gui X, Li R, Zhang X, Shen C, Yu H, Guo X, et al. An important amino acid in nucleoprotein contributes to influenza A virus replication by interacting with polymerase PB2. Virology. 2014; 464-465C:11-20. Epub 2014/07/22. doi: 10.1016/j.virol.2014.06.033 PMID: 25043584.
15. Verhelst J, Parthoens E, Schepens B, Fiers W, Saelens X. Interferon-Inducible Protein Mx1 Inhibits Influenza Virus by Interfering with Functional Viral Ribonucleoprotein Complex Assembly. J Virol. 2012; 86(24):13445-55. doi: 10.1128/jvi.01682-12 PMID: 23015724.
16. Mehle A, Doudna JA. An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe. 2008; 4(2):111-22. Epub 2008/08/12. doi: 10.1016/j.chom.2008.06.007 PMID: 18692771; PubMed Central PMCID: PMC2597520.
17. Rameix-Welti M-A, Tomoiu A, Dos Santos Afonso E, van der Werf S, 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. 2009; 83(3):1320-31. doi: 10.1128/jvi.00977-08 PMID: 19019950.
18. Ng AK, Chan WH, Choi ST, Lam MK, Lau KF, Chan PK, et al. Influenza polymerase activity correlates with the strength of interaction between nucleoprotein and PB2 through the host-specific residue K/E627. PLoS ONE. 2012; 7(5):e36415. Epub 2012/05/10. doi: 10.1371/journal.pone.0036415 PMID: 22570712; PubMed Central PMCID: PMC3343083.
19. Cauldwell AV, Moncorge O, Barclay WS. Unstable Polymerase-Nucleoprotein Interaction Is Not Responsible for Avian Influenza Virus Polymerase Restriction in Human Cells. J Virol. 2013; 87(2):1278-84. doi: 10.1128/jvi.02597-12 PMID: 23115299.
20. Paterson D, te Velthuis AJ, Vreede FT, Fodor E. Host restriction of influenza virus polymerase activity by PB2 627E is diminished on short viral templates in a nucleoprotein-independent manner. J Virol. 2014; 88(1):339-44. Epub 2013/10/25. doi: 10.1128/JVI.02022-13 PMID: 24155385; PubMed Central PMCID: PMC3911742.
21. 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(9):5812-8. doi: 10.1128/jvi.79.9.5812-5818.2005 PMID: 15827195.
22. Vreede FT, Chan AY, Sharps J, Fodor E. Mechanisms and functional implications of the degradation of host RNA polymerase II in influenza virus infected cells. Virology. 2009; 396(1):125-34. doi: 10.1016/j.virol.2009.10.003 PMID: 19875144.
23. Takizawa N, Watanabe K, Nouno K, Kobayashi N, Nagata K. Association of functional influenza viral proteins and RNAswith nuclear chromatin and sub-chromatin structure. Microbes and Infection. 2006; 8(3):823-33. doi: 10.1016/j.micinf.2005.10.005 PMID: 16513387.
24. 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):672-82. doi: 10.1021/pr060432u PMID: 17269724.
25. Moisy D, Avilov SV, Jacob Y, Laoide BM, Ge X, Baudin F, et al. HMGB1 Protein Binds to Influenza Virus Nucleoprotein and Promotes Viral Replication. J Virol. 2012; 86(17):9122-33. doi: 10.1128/jvi.00789-12 PMID: 22696656.
26. Chase GP, Rameix-Welti M-A, Zvirbliene A, Zvirblis G, Götz V, Wolff T, et al. Influenza Virus Ribonucleoprotein Complexes Gain Preferential Access to Cellular Export Machinery through Chromatin Targeting. PLoS Pathog. 2011; 7(9):e1002187. doi: 10.1371/journal.ppat.1002187 PMID: 21909257.
27. Eisfeld AJ, Kawakami E, Watanabe T, Neumann G, Kawaoka Y. RAB11A is essential for transport of the influenza virus genome to the plasma membrane. J Virol. 2011; 85(13):6117-26. Epub 2011/04/29. doi: 10.1128/JVI.00378-11 PMID: 21525351; PubMed Central PMCID: PMC3126513.
28. Momose F, Sekimoto T, Ohkura T, Jo S, Kawaguchi A, Nagata K, et al. Apical Transport of Influenza A Virus Ribonucleoprotein Requires Rab11-positive Recycling Endosome. PLoS ONE. 2011; 6(6): e21123. doi: 10.1371/journal.pone.0021123 PMID: 21731653.
29. Amorim MJ, Bruce EA, Read EK, Foeglein A, Mahen R, Stuart AD, et al. ARab11-andmicrotubule-dependent mechanism for cytoplasmic transport of influenza Avirus viral RNA. J Virol. 2011; 85(9):4143-56. Epub 2011/02/11. doi: 10.1128/JVI.02606-10 PMID: 21307188; PubMed Central PMCID: PMC3126276.
30. Cabantous S, Terwilliger TC, Waldo GS. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nature Biotechnology. 2005; 23(1):102-7. doi: 10.1038/nbt1044 PMID: 15580262.
31. Cabantous S, Waldo GS. In vivo and in vitro protein solubility assays using split GFP. Nature Methods. 2006; 3(10):845-54. doi: 10.1038/nmeth932 PMID: 16990817.
32. Avilov SV, Moisy D, Naffakh N, Cusack S. Influenza Avirus progeny vRNP trafficking in live infected cells studied with the virus-encoded fluorescently tagged PB2 protein. Vaccine. 2012;(0:). doi: 10.1016/j.vaccine.2012.09.077 PMID: 23063830.
33. Avilov SV, Moisy D, Munier S, Schraidt O, Naffakh N, Cusack S. Replication-competent influenza A virus that encodes a split-green fluorescent protein-tagged PB2 polymerase subunit allows live-cell imaging of the virus life cycle. J Virol. 2012; 86(3):1433-48. Epub 2011/11/25. doi: 10.1128/JVI.05820-11 PMID: 22114331; PubMed Central PMCID: PMC3264389.
34. Lakdawala SS, Wu Y, Wawrzusin P, Kabat J, Broadbent AJ, Lamirande EW, et al. Influenza a virus assembly intermediates fuse in the cytoplasm. PLoS Pathog. 2014; 10(3):e1003971. Epub 2014/03/08. doi: 10.1371/journal.ppat.1003971 PMID: 24603687; PubMed Central PMCID: PMC3946384.
35. Gerlich D, Beaudouin J, Gebhard M, Ellenberg J, Eils R. Four-dimensional imaging and quantitative reconstruction to analyse complex spatiotemporal processes in live cells. Nat Cell Biol. 2001; 3(9):852-5. PMID: 11533667.
36. Keppler A, Ellenberg J. Chromophore-assisted laser inactivation of alpha-and gamma-tubulin SNAP-tag fusion proteins inside living cells. ACS Chem Biol. 2009; 4(2):127-38. Epub 2009/02/05. doi: 10.1021/cb800298u PMID: 19191588.
37. Riedl J, Flynn KC, Raducanu A, Gartner F, Beck G, Bosl M, et al. Lifeact mice for studying F-actin dynamics. Nat Methods. 2010; 7(3):168-9. Epub 2010/03/03. doi: 10.1038/nmeth0310-168 PMID: 20195247.
38. Matrosovich M, Matrosovich T, Garten W, Klenk HD. New low-viscosity overlay medium for viral plaque assays. Virology Journal. 2006; 3. doi: 10.1186/1743-422x-3-63 PMID: 16945126.
39. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006; 3(12):995-1000. Epub 2006/10/31. doi: 10.1038/nmeth947 PMID: 17072308.
40. Huet S, Avilov SV, Ferbitz L, Daigle N, Cusack S, Ellenberg J. Nuclear Import and Assembly of Influenza A Virus RNA Polymerase Studied in Live Cells by Fluorescence Cross-Correlation Spectroscopy. J Virol. 2010; 84(3):1254-64. doi: 10.1128/jvi.01533-09 PMID: 19906916.
41. Goldman RD, Swedlow J.R., Spector D.L. Live Cell Imaging. 2ed. New-York: Cold Spring Harbor Laboratory Press; 2010. 736 p.
42. Loucaides EM, von Kirchbach JC, Foeglein A, Sharps J, Fodor E, Digard P. Nuclear dynamics of influenza A virus ribonucleoproteins revealed by live-cell imaging studies. Virology. 2009; 394(1):154-63. Epub 2009/09/12. doi: 10.1016/j.virol.2009.08.015 PMID: 19744689; PubMed Central PMCID: PMC2771073.
43. Noda T, Kawaoka Y. Structure of influenza virus ribonucleoprotein complexes and their packaging into virions. Reviews in medical virology. 2010; 20(6):380-91. Epub 2010/09/21. doi: 10.1002/rmv.666 PMID: 20853340.
44. Chan WH, Ng AKL, Robb NC, Lam MKH, Chan PKS, Au SWN, et al. Functional Analysis of the Influenza Virus H5N1 Nucleoprotein Tail Loop Reveals Amino Acids That Are Crucial for Oligomerization and Ribonucleoprotein Activities. J Virol. 2010; 84(14):7337-45. doi: 10.1128/Jvi.02474-09 PMID: 20463064.
45. Chenavas S, Estrozi LF, Slama-Schwok A, Delmas B, Di Primo C, Baudin F, et al. Monomeric Nucleoprotein of Influenza A Virus. PLoS Pathog. 2013; 9(3):e1003275. doi: 10.1371/journal.ppat.1003275 PMID: 23555270.
46. Schwille P, Haupts U, Maiti S, Webb WW. Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one- and two-photon excitation. Biophys J. 1999; 77(4):2251-65. PMID: 10512844.
47. Kim SA, Heinze KG, Schwille P. Fluorescence correlation spectroscopy in living cells. Nat Methods. 2007; 4(11):963-73. PMID: 17971781.
48. Digman MA, Brown CM, Sengupta P, Wiseman PW, Horwitz AR, Gratton E. Measuring Fast Dynamics in Solutions and Cells with a Laser Scanning Microscope. Biophysical Journal. 2005; 89(2):1317-27. doi: 10.1529/biophysj.105.062836 PMID: 15908582.
49. Amorim MJ, Kao RY, Digard P. Nucleozin targets cytoplasmic trafficking of viral ribonucleoprotein-Rab11 complexes in influenza A virus infection. J Virol. 2013; 87(8):4694-703. Epub 2013/02/15. doi: 10.1128/JVI.03123-12 PMID: 23408618; PubMed Central PMCID: PMC3624347.
50. Biswas SK, Boutz PL, Nayak DP. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. J Virol. 1998; 72(7):5493-501. Epub 1998/06/17. PMID: 9621005; PubMed Central PMCID: PMC110190.
51. Labadie K, Dos Santos Afonso E, Rameix-Welti MA, van der Werf S, Naffakh N. Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology. 2007; 362(2):271-82. PMID: 17270230.
52. Marklund JK, Ye Q, Dong J, Tao YJ, Krug RM. Sequence in the Influenza A Virus Nucleoprotein Required for Viral Polymerase Binding and RNA Synthesis. J Virol. 2012; 86(13):7292-7. doi: 10.1128/jvi.00014-12 PMID: 22532672.
53. Chou Y HN, Gao Q, Palese P, Singer R, Lionnet T. Colocalization of Different Influenza Viral RNA Segments in the Cytoplasm before Viral Budding as Shown by Single-molecule Sensitivity FISH Analysis. PLoS Pathogens. 2013; 9(5). doi: 10.1371/journal.ppat.1003358 PMID: 23671419.