Structural characterization of recombinant IAV polymerase reveals a stable complex between viral PA-PB1 heterodimer and host RanBP5

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Swale, Christopher ^a,b   Monod, Alexandre ^a,b   Tengo, Laura ^a,b   Labaronne, Alice ^a,b   Garzoni, Frederic ^a,b,c   Bourhis, Jean Marie ^a,b   Cusack, Stephen ^a,b,c   Schoehn, Guy ^a,b   Berger, Imre ^a,b,c,d   Ruigrok, Rob Wh ^a,b   Crepin, Thibaut ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IPO5 PROTEIN, HUMAN; KARYOPHERIN BETA; PROTEIN BINDING; PROTEIN SUBUNIT; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN; VIRUS RNA;

CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INFLUENZA; INFLUENZA A VIRUS; METABOLISM; PROMOTER REGION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; VIROLOGY;

BETA KARYOPHERINS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RNA REPLICASE; RNA, VIRAL; VIRAL PROTEINS;

EID: 84964499223     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24727     Document Type: Article

References (64)

1. Cianci, C., Tiley, L., Krystal, M. Differential activation of the influenza virus polymerase via template RNA binding. J Virol 69, 3995-3999 (1995).
2. Hagen, M., Chung, T. D., Butcher, J. A., Krystal, M. Recombinant influenza virus polymerase: requirement of both 5? and 3? viral ends for endonuclease activity. J Virol 68, 1509-1515 (1994).
3. Tiley, L. S., Hagen, M., Matthews, J. T., Krystal, M. Sequence-specific binding of the influenza virus RNA polymerase to sequences located at the 5? ends of the viral RNAs. J Virol 68, 5108-5116 (1994).
4. 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 23, 847-858 (1981).
5. Reich, S. et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature 516, 361-366, doi: 10.1038/nature14009 (2014).
6. Pflug, A., Guilligay, D., Reich, S., Cusack, S. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516, 355-360, doi: 10.1038/nature14008 (2014).
7. Hengrung, N. et al. Crystal structure of the RNA-dependent RNA polymerase from influenza C virus. Nature 527, 114-117, doi: 10.1038/nature15525 (2015).
8. Mukaigawa, J., Nayak, D. P. Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J Virol 65, 245-253 (1991).
9. Tarendeau, F. et al. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14, 229-233 (2007).
10. Deng, T. et al. Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 80, 11911-11919 (2006).
11. Huet, S. et al. Nuclear import and assembly of influenza A virus RNA polymerase studied in live cells by fluorescence crosscorrelation spectroscopy. J Virol 84, 1254-1264 (2010).
12. 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. J Gen Virol 92, 1859-1869 (2011).
13. Chang, S. et al. Cryo-EM structure of influenza virus RNA polymerase complex at 4.3 A resolution. Mol Cell 57, 925-935, doi: 10.1016/j.molcel.2014.12.031 (2015).
14. Al-Tawfiq, J. A., Zumla, A., Memish, Z. A. Coronaviruses: severe acute respiratory syndrome coronavirus and Middle East respiratory syndrome coronavirus in travelers. Current opinion in infectious diseases 27, 411-417, doi: 10.1097/QCO.000000000 0000089 (2014).
15. Lucas, S., Nelson, A. M. HIV and the spectrum of human disease. The Journal of pathology 235, 229-241, doi: 10.1002/path.4449 (2015).
16. Crepin, T. et al. Polyproteins in structural biology. Curr Opin Struct Biol 32, 139-146, doi: 10.1016/j.sbi.2015.04.007 (2015).
17. Nie, Y., Bellon-Echeverria, I., Trowitzsch, S., Bieniossek, C., Berger, I. Multiprotein complex production in insect cells by using polyproteins. Methods in molecular biology 1091, 131-141, doi: 10.1007/978-1-62703-691-7-8 (2014).
18. Bieniossek, C., Imasaki, T., Takagi, Y., Berger, I. MultiBac: expanding the research toolbox for multiprotein complexes. Trends Biochem Sci 37, 49-57, doi: 10.1016/j.tibs.2011.10.005 (2012).
19. Trowitzsch, S., Bieniossek, C., Nie, Y., Garzoni, F., Berger, I. New baculovirus expression tools for recombinant protein complex production. J Struct Biol 172, 45-54 (2010).
20. Sugiyama, K. et al. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. Embo J 28, 1803-1811 (2009).
21. An, Y., Meresse, P., Mas, P. J., Hart, D. J. CoESPRIT: a library-based construct screening method for identification and expression of soluble protein complexes. PLoS One 6, e16261, doi: 10.1371/journal.pone.0016261 (2011).
22. Guilligay, D. et al. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15, 500-506 (2008).
23. Bieniossek, C., Richmond, T. J., Berger, I. MultiBac: multigene baculovirus-based eukaryotic protein complex production. Current protocols in protein science/editorial board, John E. Coligan .[et al.] Chapter 5, Unit 5 20, doi: 10.1002/0471140864.ps0520s51 (2008).
24. 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 13, 3158-3165 (1994).
25. Crepin, T. et al. Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. J Virol 84, 9096-9104 (2010).
26. Dias, A. et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458, 914-918 (2009).
27. He, X. et al. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454, 1123-1126 (2008).
28. Obayashi, E. et al. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 454, 1127-1131 (2008).
29. Desselberger, U., Racaniello, V. R., Zazra, J. J., Palese, P. The 3? and 5?-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8, 315-328 (1980).
30. Robertson, J. S. 5? and 3? terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Res 6, 3745-3757 (1979).
31. Skehel, J. J., Hay, A. J. Nucleotide sequences at the 5? termini of influenza virus RNAs and their transcripts. Nucleic Acids Res 5, 1207-1219 (1978).
32. Brownlee, G. G., Sharps, J. L. The RNA polymerase of influenza a virus is stabilized by interaction with its viral RNA promoter. J Virol 76, 7103-7113 (2002).
33. Tomescu, A. I., Robb, N. C., Hengrung, N., Fodor, E., Kapanidis, A. N. Single-molecule FRET reveals a corkscrew RNA structure for the polymerase-bound influenza virus promoter. Proc Natl Acad Sci USA 111, E3335-3342, doi: 10.1073/pnas.1406056111 (2014).
34. Melen, K. et al. Importin alpha nuclear localization signal binding sites for STAT1, STAT2, and influenza A virus nucleoprotein. J Biol Chem 278, 28193-28200 (2003).
35. Naito, T., Momose, F., Kawaguchi, A., Nagata, K. Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81, 1339-1349, doi: 10.1128/JVI.01917-06 (2007).
36. Portela, A., Digard, P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83, 723-734 (2002).
37. Weber, F., Kochs, G., Gruber, S., Haller, O. A classical bipartite nuclear localization signal on Thogoto and influenza A virus nucleoproteins. Virology 250, 9-18, doi: 10.1006/viro.1998.9329 (1998).
38. 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. J Virol 78, 9144-9153, doi: 10.1128/JVI.78.17.9144-9153.2004 (2004).
39. Rambo, R. P., Tainer, J. A. Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496, 477-481, doi: 10.1038/nature12070 (2013).
40. Kobayashi, J., Matsuura, Y. Structural basis for cell-cycle-dependent nuclear import mediated by the karyopherin Kap121p. J Mol Biol 425, 1852-1868, doi: 10.1016/j.jmb.2013.02.035 (2013).
41. Svergun, D. I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886 (1999).
42. Delaforge, E. et al. Large-Scale Conformational Dynamics Control H5N1 Influenza Polymerase PB2 Binding to Importin alpha. Journal of the American Chemical Society 137, 15122-15134, doi: 10.1021/jacs.5b07765 (2015).
43. Thierry, E. et al. Influenza Polymerase Can Adopt an Alternative Configuration Involving a Radical Repacking of PB2 Domains. Mol Cell 61, 125-137, doi: 10.1016/j.molcel.2015.11.016 (2016).
44. Momose, F. et al. Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277, 45306-45314, doi: 10.1074/jbc.M206822200 (2002).
45. Chase, G. et al. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377, 431-439, doi: 10.1016/j. virol.2008.04.040 (2008).
46. Fitzgerald, D. J. et al. Multiprotein expression strategy for structural biology of eukaryotic complexes. Structure 15, 275-279, doi: 10.1016/j.str.2007.01.016 (2007).
47. Palmberger, D., Rendic, D. SweetBac: Applying MultiBac Technology Towards Flexible Modification of Insect Cell Glycosylation. Methods in molecular biology 1321, 153-169, doi: 10.1007/978-1-4939-2760-9-11 (2015).
48. Iwai, A. et al. Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J Biol Chem 285, 32064-32074, doi: 10.1074/jbc.M110.112458 (2010).
49. 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. J Virol 79, 8669-8674 (2005).
50. Graef, K. M. et al. The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol 84, 8433-8445 (2010).
51. Patel, D., Schultz, L. W., Umland, T. C. Influenza A polymerase subunit PB2 possesses overlapping binding sites for polymerase subunit PB1 and human MAVS proteins. Virus Res 172, 75-80, doi: 10.1016/j.virusres.2012.12.003 (2013).
52. Degut, C., Monod, A., Brachet, F., Crepin, T., Tisne, C. In Vitro/In Vivo Production of tRNA for X-Ray Studies. Methods in molecular biology 1320, 37-57, doi: 10.1007/978-1-4939-2763-0-4 (2016).
53. Price, S. R., Ito, N., Oubridge, C., Avis, J. M., Nagai, K. Crystallization of RNA-protein complexes. I. Methods for the large-scale preparation of RNA suitable for crystallographic studies. J Mol Biol 249, 398-408 (1995).
54. Boulo, S. et al. Human importin alpha and RNA do not compete for binding to influenza A virus nucleoprotein. Virology 409, 84-90 (2011).
55. Chenavas, S. et al. Monomeric nucleoprotein of influenza A virus. PLoS Pathog 9, e1003275, doi: 10.1371/journal.ppat.1003275 (2013).
56. Petoukhov, M. V., Konarev, P. V., Kikhney, A. G., Svergun, D. I. ATSAS 2.1-towards automated and web-supported small-angle scattering data analysis. J. Appl. Crystallogr. 40, s223-s228 (2007).
57. Rambo, R. P., Tainer, J. A. Super-resolution in solution X-ray scattering and its applications to structural systems biology. Annual review of biophysics 42, 415-441, doi: 10.1146/annurev-biophys-083012-130301 (2013).
58. Semenyuk, A. V., Svergun, D. I. GNOM-a program package for small-angle scattering data processing. J. Appl. Crystallogr. 24, 537-540 (1991).
59. Franke, D., Svergun, D. I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346 (2009).
60. Volkov, V. V., Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).
61. Svergun, D., Barberato, C., Koch, M. H. J. CRYSOL-a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates. J. Appl. Crystallogr. 28, 768-773 (1995).
62. Petoukhov, M. V., Svergun, D. I. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophysical journal 89, 1237-1250, doi: 10.1529/biophysj.105.064154 (2005).
63. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612, doi: 10.1002/jcc.20084 (2004).
64. Wong, I., Lohman, T. M. A double-filter method for nitrocellulose-filter binding: application to protein-nucleic acid interactions. Proc Natl Acad Sci USA 90, 5428-5432 (1993).