Influence of PB2 host-range determinants on the intranuclear mobility of the influenza a virus polymerase

Journal of General Virology

Volumn 92, Issue 7, 2011, Pages 1650-1661

  Foeglein, Ágnes ^a   Loucaides, Eva M ^a   Mura, Manuela ^b   Wise, Helen M ^a   Barclay, Wendy S ^b   Digard, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR FACTOR; PB2 PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FOWL; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLUENZA VIRUS A; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SURFACE CHARGE; TURKEY (REPUBLIC); UNITED KINGDOM; VIRUS STRAIN;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BIRDS; CELL LINE; HOST SPECIFICITY; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; QUAIL; RNA REPLICASE; VIRAL PROTEINS;

AVES; INFLUENZA A VIRUS; MAMMALIA;

EID: 79959307361     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.031492-0     Document Type: Article

References (60)

1. Almond, J. W. (1977). A single gene determines the host range of influenza virus. Nature 270, 617-618.
2. Benfield, C. T., Lyall, J. W., Kochs, G. & Tiley, L. S. (2008). Asparagine 631 variants of the chicken Mx protein do not inhibit influenza virus replication in primary chicken embryo fibroblasts or in vitro surrogate assays. J Virol 82, 7533-7539.
3. Boivin, S. & Hart, D. J. (2011). Interaction of the influenza A virus polymerase PB2 C-terminal region with importin a isoforms provides insights into host adaptation and polymerase assembly. J Biol Chem 286, 10439-10448.
4. Boivin, S., Cusack, S., Ruigrok, R. W. & Hart, D. J. (2010). Influenza A virus polymerase: structural insights into replication and host adaptation mechanisms. J Biol Chem 285, 28411-28417.
5. Bussey, K. A., Bousse, T. L., Desmet, E. A., Kim, B. & Takimoto, T. (2010). PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol 84, 4395-4406.
6. Carrasco, M., Amorim, M. J. & Digard, P. (2004). Lipid raft-dependent targeting of the influenza A virus nucleoprotein to the apical plasma membrane. Traffic 5, 979-992.
7. Chen, G.-W., Chang, S.-C., Mok, C. K., Lo, Y.-L., Kung, Y.-N., Huang, J.-H., Shih, Y.-H., Wang, J.-Y., Chiang, C. & other authors (2006). Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis 12, 1353-1360.
8. de Wit, E., Spronken, M. I. J., Bestebroer, T. M., Rimmelzwaan, G. F., Osterhaus, A. D. M. E. & Fouchier, R. A. M. (2004). Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res 103, 155-161.
9. Engelhardt, O. G., Smith, M. & Fodor, E. (2005). Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J Virol 79, 5812-5818.
10. Fields, S. & Winter, G. (1982). Nucleotide sequences of influenza virus segments 1 and 3 reveal mosaic structure of a small viral RNA segment. Cell 28, 303-313.
11. Finkelstein, D. B., Mukatira, S., Mehta, P. K., Obenauer, J. C., Su, X., Webster, R. G. & Naeve, C. W. (2007). Persistent host markers in pandemic and H5N1 influenza viruses. J Virol 81, 10292-10299.
12. Fodor, E. & Smith, M. (2004). 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.
13. Gabriel, G., Dauber, B., Wolff, T., Planz, O., Klenk, H.-D. & Stech, J. (2005). The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102, 18590-18595.
14. Gabriel, G., Herwig, A. & Klenk, H. D. (2008). Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog 4, e11.
15. Gao, P., Watanabe, S., Ito, T., Goto, H., Wells, K., McGregor, M., Cooley, A. J. & Kawaoka, Y. (1999). Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J Virol 73, 3184-3189.
16. Guilligay, D., Tarendeau, F., Resa-Infante, P., Coloma, R., Crepin, T., Sehr, P., Lewis, J., Ruigrok, R. W. H., Ortín, J. & other authors (2008). The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15, 500-506.
17. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. (2001). Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840-1842.
18. Herfst, S., Chutinimitkul, S., Ye, J., de Wit, E., Munster, V. J., Schrauwen, E. J. A., Bestebroer, T. M., Jonges, M., Meijer, A. & other authors (2010). Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission. J Virol 84, 3752-3758.
19. Howard, W., Hayman, A., Lackenby, A., Whiteley, A., Londt, B., Banks, J., McCauley, J. W. & Barclay, W. S. (2007). Development of a reverse genetics system enabling the rescue of recombinant avian influenza virus A/Turkey/England/50-92/91 (H5N1). Avian Dis 51 (Suppl.), 393-395.
20. Jagger, B. W., Memoli, M. J., Sheng, Z.-M., Qi, L., Hrabal, R. J., Allen, G. L., Dugan, V. G., Wang, R., Digard, P. & other authors (2010). The PB2-E627K mutation attenuates viruses containing the 2009 H1N1 influenza pandemic polymerase. mBio 1, e00067-10.
21. Josset, L., Frobert, E. & Rosa-Calatrava, M. (2008). Influenza A replication and host nuclear compartments: many changes and many questions. J Clin Virol 43, 381-390.
22. Kuzuhara, T., Kise, D., Yoshida, H., Horita, T., Murazaki, Y., Nishimura, A., Echigo, N., Utsunomiya, H. & Tsuge, H. (2009). Structural basis of the influenza A virus RNA polymerase PB2 RNAbinding domain containing the pathogenicity-determinant lysine 627 residue. J Biol Chem 284, 6855-6860.
23. Labadie, K., Dos Santos Afonso, E., Rameix-Welti, M.-A., van der Werf, S. & Naffakh, N. (2007). Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology 362, 271-282.
24. Le, Q. M., Sakai-Tagawa, Y., Ozawa, M., Ito, M. & Kawaoka, Y. (2009). Selection of H5N1 influenza virus PB2 during replication in humans. J Virol 83, 5278-5281.
25. Lee, M. T. M., Bishop, K., Medcalf, L., Elton, D., Digard, P. & Tiley, L. S. (2002). Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res 30, 429-438.
26. Lee, M.-T. M., Klumpp, K., Digard, P. & Tiley, L. S. (2003). Activation of influenza virus RNA polymerase by the 59 and 39 terminal duplex of genomic RNA. Nucleic Acids Res 31, 1624-1632.
27. Li, Z., Chen, H., Jiao, P., Deng, G., Tian, G., Li, Y., Hoffmann, E., Webster, R. G., Matsuoka, Y. & Yu, K. (2005). Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79, 12058-12064.
28. Li, J., Ishaq, M., Prudence, M., Xi, X., Hu, T., Liu, Q. & Guo, D. (2009). Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. Virus Res 144, 123-129.
29. Loucaides, E. M., von Kirchbach, J. C., Foeglein, A., Sharps, J., Fodor, E. & Digard, P. (2009). Nuclear dynamics of influenza A virus ribonucleoproteins revealed by live-cell imaging studies. Virology 394, 154-163.
30. Massin, P., van der Werf, S. & Naffakh, N. (2001). Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J Virol 75, 5398-5404.
31. Massin, P., Kuntz-Simon, G., Barbezange, C., Deblanc, C., Oger, A., Marquet-Blouin, E., Bougeard, S., van der Werf, S. & Jestin, V. (2010). Temperature sensitivity on growth and/or replication of H1N1, H1N2 andH3N2 influenza A viruses isolated from pigs and birds in mammalian cells. Vet Microbiol 142, 232-241.
32. Mehle, A. & Doudna, J. A. (2008). An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe 4, 111-122.
33. Mehle, A. & Doudna, J. A. (2009). Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A 106, 21312-21316.
34. Miotto, O., Heiny, A., Tan, T. W., August, J. T. & Brusic, V. (2008). Identification of human-to-human transmissibility factors in PB2 proteins of influenza A by large-scale mutual information analysis. BMC Bioinformatics 9 (Suppl. 1), S18.
35. Moncorge ́, O., Mura, M. & Barclay, W. S. (2010). Evidence for avian and human host cell factors that affect the activity of influenza virus polymerase. J Virol 84, 9978-9986.
36. Mukaigawa, J. & Nayak, D. P. (1991). Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J Virol 65, 245-253.
37. Mullin, A. E., Dalton, R. M., Amorim, M. J., Elton, D. & Digard, P. (2004). Increased amounts of the influenza virus nucleoprotein do not promote higher levels of viral genome replication. J Gen Virol 85, 3689-3698.
38. Munster, V. J., de Wit, E., van Riel, D., Beyer, W. E. P., Rimmelzwaan, G. F., Osterhaus, A. D. M. E., Kuiken, T. & Fouchier, R. A. M. (2007). The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 196, 258-265.
39. Naffakh, N., Massin, P., Escriou, N., Crescenzo-Chaigne, B. & van der Werf, S. (2000). Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J Gen Virol 81, 1283-1291.
40. Naffakh, N., Tomoiu, A., Rameix-Welti, M.-A. & van der Werf, S. (2008). Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annu Rev Microbiol 62, 403-424.
41. Neumann, G., Brownlee, G. G., Fodor, E. & Kawaoka, Y. (2004). Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 283, 121-143.
42. Phair, R. D. & Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
43. Poole, E., Elton, D., Medcalf, L. & Digard, P. (2004). Functional domains of the influenza A virus PB2 protein: identification of NP- and PB1-binding sites. Virology 321, 120-133.
44. Portela, A. & Digard, P. (2002). The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83, 723-734.
45. Rameix-Welti, M.-A., Tomoiu, A., Dos Santos Afonso, E., van der Werf, S. & Naffakh, N. (2009). 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, 1320-1331.
46. Resa-Infante, P., Jorba, N., Zamarren ̃ o, N., Ferna ́ ndez, Y., Jua ́ rez, S. & Ort́n, J. (2008). The host-dependent interaction of alpha-importins with influenza PB2 polymerase subunit is required for virus RNA replication. PLoS ONE 3, e3904.
47. Schnitzler, S. U. & Schnitzler, P. (2009). An update on swine-origin influenza virus A/H1N1: a review. Virus Genes 39, 279-292.
48. Shinya, K., Watanabe, S., Ito, T., Kasai, N. & Kawaoka, Y. (2007). Adaptation of an H7N7 equine influenza A virus in mice. J Gen Virol 88, 547-553.
49. Steel, J., Lowen, A. C., Mubareka, S. & Palese, P. (2009). Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5, e1000252.
50. Subbarao, E. K., London, W. & Murphy, B. R. (1993). A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67, 1761-1764.
51. Sugiyama, K., Obayashi, E., Kawaguchi, A., Suzuki, Y., Tame, J. R., Nagata, K. & Park, S. Y. (2009). Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J 28, 1803-1811.
52. Tarendeau, F., Boudet, J., Guilligay, D., Mas, P. J., Bougault, C. M., Boulo, S., Baudin, F., Ruigrok, R. W. H., Daigle, N. & other authors (2007). Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14, 229-233.
53. Tarendeau, F., Crepin, T., Guilligay, D., Ruigrok, R. W. H., Cusack, S. & Hart, D. J. (2008). Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4, e1000136.
54. Taubenberger, J. K. & Kash, J. C. (2010). Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7, 440-451.
55. Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. & Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiol Rev 56, 152-179.
56. Wise, H. M., Foeglein, A., Sun, J., Dalton, R. M., Patel, S., Howard, W., Anderson, E. C., Barclay, W. S. & Digard, P. (2009). A complicated message: identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 83, 8021-8031.
57. Wood, G. W., McCauley, J. W., Bashiruddin, J. B. & Alexander, D. J. (1993). Deduced amino acid sequences at the haemagglutinin cleavage site of avian influenza A viruses of H5 and H7 subtypes. Arch Virol 130, 209-217.
58. Yamada, S., Hatta, M., Staker, B. L., Watanabe, S., Imai, M., Shinya, K., Sakai-Tagawa, Y., Ito, M., Ozawa, M. & other authors (2010). Biological and structural characterization of a host-adapting amino acid in influenza virus. PLoS Pathog 6, e1001034.
59. Yao, Y., Mingay, L. J., McCauley, J. W. & Barclay, W. S. (2001). Sequences in influenza A virus PB2 protein that determine productive infection for an avian influenza virus in mouse and human cell lines. J Virol 75, 5410-5415.
60. Zhu, H., Wang, J., Wang, P., Song, W., Zheng, Z., Chen, R., Guo, K., Zhang, T., Peiris, J. S. M. & Chen, H. (2010). Substitution of lysine at 627 position in PB2 protein does not change virulence of the 2009 pandemic H1N1 virus in mice. Virology 401, 1-5.