Human host factors required for influenza virus replication (original) (raw)

References

1. Palese, P. & Shaw, M. L. in Fields Virology 5th edn, Vol. 2 (eds D. M. Knipe & P. M. Howley) Ch. 47 1647–1689 (Lippincott Williams & Wilkins, 2007)
   Google Scholar
2. Wang, T. T. & Palese, P. Unraveling the mystery of swine influenza virus. Cell 137, 983–985 (2009)
   Article CAS Google Scholar
3. De Clercq, E. Antiviral agents active against influenza A viruses. Nature Rev. Drug Discov. 5, 1015–1025 (2006)
   Article CAS Google Scholar
4. Layne, S. P., Monto, A. S. & Taubenberger, J. K. Pandemic influenza: an inconvenient mutation. Science 323, 1560–1561 (2009)
   Article CAS Google Scholar
5. Brass, A. L. et al. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319, 921–926 (2008)
   Article ADS CAS Google Scholar
6. König, R. et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135, 49–60 (2008)
   Article Google Scholar
7. Zhou, H. et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 4, 495–504 (2008)
   Article CAS Google Scholar
8. Krishnan, M. N. et al. RNA interference screen for human genes associated with West Nile virus infection. Nature 455, 242–245 (2008)
   Article ADS CAS Google Scholar
9. Li, Q. et al. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc. Natl Acad. Sci. USA 10.1073/pnas.0907439106 (27 August 2009)
10. Tai, A. W. et al. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5, 298–307 (2009)
    Article CAS Google Scholar
11. Sessions, O. M. et al. Discovery of insect and human dengue virus host factors. Nature 458, 1047–1050 (2009)
    Article ADS CAS Google Scholar
12. Hao, L. et al. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 454, 890–893 (2008)
    Article ADS CAS Google Scholar
13. 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. 81, 9727–9736 (2007)
    Article CAS Google Scholar
14. König, R. et al. A probability-based approach for the analysis of large-scale RNAi screens. Nature Methods 4, 847–849 (2007)
    Article Google Scholar
15. Sato, S., Fujita, N. & Tsuruo, T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl Acad. Sci. USA 97, 10832–10837 (2000)
    Article ADS CAS Google Scholar
16. Sarbassov, D. D., Guertin, D. A., Ali, S. M. & Sabatini, D. M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098–1101 (2005)
    Article ADS CAS Google Scholar
17. Venkatesan, K. et al. An empirical framework for binary interactome mapping. Nature Methods 6, 83–90 (2009)
    Article CAS Google Scholar
18. Beer, C., Andersen, D. S., Rojek, A. & Pedersen, L. Caveola-dependent endocytic entry of amphotropic murine leukemia virus. J. Virol. 79, 10776–10787 (2005)
    Article CAS Google Scholar
19. McClure, M. O., Sommerfelt, M. A., Marsh, M. & Weiss, R. A. The pH independence of mammalian retrovirus infection. J. Gen. Virol. 71, 767–773 (1990)
    Article CAS Google Scholar
20. Whitney, J. A., Gomez, M., Sheff, D., Kreis, T. E. & Mellman, I. Cytoplasmic coat proteins involved in endosome function. Cell 83, 703–713 (1995)
    Article CAS Google Scholar
21. Aniento, F., Gu, F., Parton, R. G. & Gruenberg, J. An endosomal βCOP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29–41 (1996)
    Article CAS Google Scholar
22. Tscherne, D. M., Manicassamy, B. & Garcia-Sastre, A. An enzymatic virus-like particle assay for sensitive detection of virus entry. J. Virol. Methods 10.1016/j.jviromet.2009.10.020 (29 October 2009)
23. Kutay, U., Bischoff, F. R., Kostka, S., Kraft, R. & Gorlich, D. Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor. Cell 90, 1061–1071 (1997)
    Article CAS Google Scholar
24. Colbran, R. J. Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378, 1–16 (2004)
    Article CAS Google Scholar
25. Sumi, M. et al. The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem. Biophys. Res. Commun. 181, 968–975 (1991)
    Article CAS Google Scholar
26. Chanda, S. K. et al. Genome-scale functional profiling of the mammalian AP-1 signaling pathway. Proc. Natl Acad. Sci. USA 100, 12153–12158 (2003)
    Article ADS CAS Google Scholar
27. Aza-Blanc, P. et al. Identification of modulators of TRAIL-induced apoptosis via RNAi-based phenotypic screening. Mol. Cell 12, 627–637 (2003)
    Article CAS Google Scholar
28. Sui, B. et al. The use of random homozygous gene perturbation to identify novel host-oriented targets for influenza. Virology 387, 473–481 (2009)
    Article CAS Google Scholar
29. Bader, G. D. & Hogue, C. W. An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4, 2 (2003)
    Article Google Scholar

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Acknowledgements

This work was supported in part by National Institutes of Health (NIH) grants U01 AI1074539, U54 AI057158 (Northeast Biodefense Center), HHSN272200900032C, HHSN266200700010C, 1 PO1 AI058113 and 1R21AI083673. S.S. is supported by a fellowship from the German Research Foundation and D.M.T. is supported by NIH fellowship 1F32AI081428. M.B.O. is supported by NIH training grant 1 T32 AI07647 and Mount Sinai Medical Scientist Training Program T32 GM007280. A.I. is supported by a Japan Society for the Promotion of Science Fellowship. The small molecule screen was performed at the National Screening Laboratory for the Regional Centers of Excellence in Biodefense (NSRB), Harvard Medical School, Boston and was supported by NIH grant U54 AI057159. Confocal laser scanning microscopy was performed at the MSSM-Microscopy Shared Resource Facility, supported with funding from NIH-NCI shared resources grant (5R24 CA095823-04), NSF Major Research Instrumentation grant (DBI-9724504) and NIH shared instrumentation grant (1 S10 RR0 9145-01). We thank R. Fouchier for providing influenza A/Netherlands/602/2009 (H1N1) virus.

Author Contributions R.K. and S.S. are equally contributing first authors; M.L.S. and S.K.C. are equally contributing senior authors. R.K., S.S., A.G.-S., J.A.T.Y., P.P., M.L.S. and S.K.C. designed research; R.K., S.S., A.I., H.-H.H., Su.B., S.E.A., J.G.A., D.M.T., M.B.O., Y.L., Q.G., P.D., L.P. and C.S. performed research; R.K., C.S., P.D., B.P.T., L.M. and G.B. performed the screens; A.O. provided siRNAs; R.K., S.S., B.P.T., M.L.S., S.K.C. and P.D. analysed data; Y.Z., G.B., So.B. and T.I. performed bioinformatics analysis; R.K., S.S., A.G.-S., J.A.T.Y., P.P., M.L.S. and S.K.C. co-wrote the manuscript.

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Author notes

1. Renate König, Silke Stertz, Megan L. Shaw and Sumit K. Chanda: These authors contributed equally to this work.

Authors and Affiliations

1. Infectious and Inflammatory Disease Center, Burnham Institute for Medical Research, 10901 North Torrey Pines Road,,
   Renate König, Atsushi Inoue, Paul De Jesus, Lars Pache, Crystal Shih & Sumit K. Chanda
2. Nomis Center for Immunobiology and Microbial Pathogenesis, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road,,
   Suchita Bhattacharyya & John A. T. Young
3. Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA ,
   Shane E. Andrews
4. Department of Microbiology,,
   Silke Stertz, H. -Heinrich Hoffmann, Judith G. Alamares, Donna M. Tscherne, Mila B. Ortigoza, Yuhong Liang, Qinshan Gao, Adolfo García-Sastre, Peter Palese & Megan L. Shaw
5. Department of Medicine, Division of Infectious Diseases,,
   Adolfo García-Sastre & Peter Palese
6. Global Health and Emerging Pathogens Institute, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, New York 10029, USA ,
   Adolfo García-Sastre
7. Genomics Institute of the Novartis Research Foundation, 10675 John J Hopkins Drive, San Diego, California 92121, USA ,
   Yingyao Zhou, Buu P. Tu, Anthony Orth, Ghislain Bonamy & Loren Miraglia
8. Departments of Medicine and Bioengineering, University of California, San Diego, Pharmaceutical Sciences Building, 9500 Gilman Drive, La Jolla, California 92093, USA,
   Sourav Bandyopadhyay & Trey Ideker

Authors

1. Renate König
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2. Silke Stertz
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3. Yingyao Zhou
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4. Atsushi Inoue
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5. H. -Heinrich Hoffmann
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6. Suchita Bhattacharyya
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7. Judith G. Alamares
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8. Donna M. Tscherne
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9. Mila B. Ortigoza
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10. Yuhong Liang
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11. Qinshan Gao
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12. Shane E. Andrews
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13. Sourav Bandyopadhyay
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14. Paul De Jesus
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15. Buu P. Tu
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16. Lars Pache
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17. Crystal Shih
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18. Anthony Orth
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19. Ghislain Bonamy
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20. Loren Miraglia
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21. Trey Ideker
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22. Adolfo García-Sastre
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23. John A. T. Young
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24. Peter Palese
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25. Megan L. Shaw
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26. Sumit K. Chanda
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Corresponding authors

Correspondence toMegan L. Shaw or Sumit K. Chanda.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Data, Supplementary References, Supplementary Figures S1-S14 with Legends and Legends for Supplementary Tables S1-S13. (PDF 14707 kb)

Supplementary Table 1

Scores of 295 confirmed genes required for influenza virus replication (see Supplementary Information file for full Legend). (XLS 211 kb)

Supplementary Table 2

Overrepresented functional processes and protein domains of proteins required for influenza virus replication (see Supplementary Information file for full Legend). (XLS 60 kb)

Supplementary Table 3

Functional classification of biological processes required for influenza virus replication (see Supplementary Information file for full Legend). (XLS 220 kb)

Supplementary Table 4

Overrepresented functional pathways required for influenza virus replication (see Supplementary Information file for full Legend). (XLS 44 kb)

Supplementary Table 5

References for selected functional categories presented in Table 1 (see Supplementary Information file for full Legend). (XLS 30 kb)

Supplementary Table 6

Binary interactions of the host pathogen interaction map for Figure 1C and Supplementary Figure S4 (see Supplementary Information file for full Legend). (XLS 468 kb)

Supplementary Table 7

Overlap between viral host factors required by different RNA viruses (see Supplementary Information file for full Legend). (XLS 37 kb)

Supplementary Table 8

Biochemical complexes that are required by different RNA viruses (see Supplementary Information file for full Legend). (XLS 172 kb)

Supplementary Table 9

Host proteins confirmed to be required for wild-type influenza virus growth and gene expression (see Supplementary Information file for full Legend). (XLS 161 kb)

Supplementary Table 10

Examination of interferon induction in siRNAtransfected cells (see Supplementary Information file for full Legend). (XLS 52 kb)

Supplementary Table 11

Evaluation of host factors that regulate influenza virus entry (see Supplementary Information file for full Legend). (XLS 33 kb)

Supplementary Table 12

Effects of host factor depletion on expression of an influenza virus mini-genome reporter (see Supplementary Information file for full Legend). (XLS 29 kb)

Supplementary Table 13

Expression levels of host factor after siRNA silencing (see Supplementary Information file for full Legend). (XLS 28 kb)

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König, R., Stertz, S., Zhou, Y. et al. Human host factors required for influenza virus replication.Nature 463, 813–817 (2010). https://doi.org/10.1038/nature08699

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• Received: 24 September 2009
• Accepted: 24 November 2009
• Published: 21 December 2009
• Issue Date: 11 February 2010
• DOI: https://doi.org/10.1038/nature08699