Human cellular protein nucleoporin hNup98 interacts with influenza A virus NS2/nuclear export protein and overexpression of its GLFG repeat domain can inhibit virus propagation

Journal of General Virology

Volumn 91, Issue 10, 2010, Pages 2474-2484

  Chen, Jingjing ^a,b   Huang, Shengping ^a,b   Chen, Ze ^a,c,d  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c HUNAN NORMAL UNIVERSITY   (China)

^d SHANGHAI INSTITUTE OF BIOLOGICAL PRODUCTS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BINDING PROTEIN; CELL PROTEIN; GLYCYLLEUCYLPHENYLALANYLGLYCINE; NONSTRUCTURAL PROTEIN 2; NUCLEOPORIN 98; UNCLASSIFIED DRUG; NS PROTEIN, INFLUENZA VIRUS; NUCLEAR EXPORT SIGNAL; NUCLEOPORIN; NUP98 PROTEIN, HUMAN; VIRUS PROTEIN;

ARTICLE; DNA LIBRARY; DOWN REGULATION; HUMAN; INFLUENZA VIRUS A; KIDNEY CELL; MAMMAL CELL; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; VIRUS INHIBITION; VIRUS REPLICATION; YEAST; ANIMAL; CELL LINE; CELL NUCLEUS; CHEMISTRY; CONFOCAL MICROSCOPY; DOG; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INFLUENZA VIRUS A H5N1; METABOLISM; NUCLEOLUS; PHYSIOLOGY; PROTEIN ANALYSIS; TWO HYBRID SYSTEM;

ANIMALS; CELL LINE; CELL NUCLEOLUS; CELL NUCLEUS; DOGS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MICROSCOPY, CONFOCAL; NUCLEAR EXPORT SIGNALS; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN INTERACTION MAPPING; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

INFLUENZA A VIRUS; MAMMALIA; ORTHOMYXOVIRIDAE;

EID: 77956795509     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.022681-0     Document Type: Article

References (50)

1. Akarsu, H., Burmeister, W. P., Petosa, C., Petit, I., Müller, C. W., Ruigrok, R. W. & Baudin, F. (2003). Crystal structure of the M1 protein-binding domain of the influenza A virus nuclear export protein (NEP/NS2). EMBO J 22, 4646-4655.
2. Bayliss, R., Littlewood, T., Strawn, L. A., Wente, S. R. & Stewart, M. (2002). GLFG and FxFG nucleoporins bind to overlapping sites on importin-β. J Biol Chem 277, 50597-50606.
3. Bogerd, H. P., Echarri, A., Ross, T. M. & Cullen, B. R. (1998). Inhibition of human immunodeficiency virus Rev and human T-cell leukemia virus Rex function, but not Mason-Pfizer monkey virus constitutive transport element activity, by a mutant human nucleoporin targeted to Crm1. J Virol 72, 8627-8635.
4. Boulo, S., Akarsu, H., Ruigrok, R. W. & Baudin, F. (2007). Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res 124, 12-21.
5. Boyle, S. M., Ruvolo, V., Gupta, A. K. & Swaminathan, S. (1999). Association with the cellular export receptor CRM 1 mediates function and intracellular localization of Epstein-Barr virus SM protein, a regulator of gene expression. J Virol 73, 6872-6881.
6. Brass, A. L., Huang, I. C., Benita, Y., John, S. P., Krishnan, M. N., Feeley, E. M., Ryan, B. J., Weyer, J. L., van der Weyden, L. & other authors (2009). The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139, 1243-1254.
7. Carmody, S. R. & Wente, S. R. (2009). mRNA nuclear export at a glance. J Cell Sci 122, 1933-1937.
8. Chakraborty, P., Seemann, J., Mishra, R. K., Wei, J. H., Weil, L., Nussenzveig, D. R., Heiber, J., Barber, G. N., Dasso, M. & other authors (2009). Vesicular stomatitis virus inhibits mitotic progression and triggers cell death. EMBO Rep 10, 1154-1160.
9. Chen, I. H., Sciabica, K. S. & Sandri-Goldin, R. M. (2002). ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J Virol 76, 12877-12889.
10. Cros, J. F. & Palese, P. (2003). Trafficking of viral genomic RNA into and out of the nucleus: influenza, Thogoto and Borna disease viruses. Virus Res 95, 3-12.
11. Enninga, J., Levy, D. E., Blobel, G. & Fontoura, B. M. (2002). Role of nucleoporin induction in releasing an mRNA nuclear export block. Science 295, 1523-1525.
12. Floer, M. & Blobel, G. (1999). Putative reaction intermediates in Crm1-mediated nuclear protein export. J Biol Chem 274, 16279-16286.
13. Fritz, C. C., Zapp, M. L. & Green, M. R. (1995). A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature 376, 530-533.
14. Griffis, E. R., Altan, N., Lippincott-Schwartz, J. & Powers, M. A. (2002). Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 13, 1282-1297.
15. Griffis, E. R., Xu, S. & Powers, M. A. (2003). Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol Biol Cell 14, 600-610.
16. Gustin, K. E. (2003). Inhibition of nucleo-cytoplasmic trafficking by RNA viruses: targeting the nuclear pore complex. Virus Res 95, 35-44.
17. Hao, L., Sakurai, A., Watanabe, T., Sorensen, E., Nidom, C. A., Newton, M. A., Ahlquist, P. & Kawaoka, Y. (2008). Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 454, 890-893.
18. Hodel, A. E., Hodel, M. R., Griffis, E. R., Hennig, K. A., Ratner, G. A., Xu, S. & Powers, M. A. (2002). The three-dimensional structure of the autoproteolytic, nuclear pore-targeting domain of the human nucleoporin Nup98. Mol Cell 10, 347-358.
19. Huang, S., Chen, J., Wang, H., Sun, B., Wang, H., Zhang, Z., Zhang, X. & Chen, Z. (2009). Influenza A virus matrix protein 1 interacts with hTFIIIC102-s, a short isoform of the polypeptide 3 subunit of human general transcription factor IIIC. Arch Virol 154, 1101-1110.
20. Iwatsuki-Horimoto, K., Horimoto, T., Fujii, Y. & Kawaoka, Y. (2004). Generation of influenza A virus NS2 (NEP) mutants with an altered nuclear export signal sequence. J Virol 78, 10149-10155.
21. Karlas, A., Machuy, N., Shin, Y., Pleissner, K. P., Artarini, A., Heuer, D., Becker, D., Khalil, H., Ogilvie, L. A. & other authors (2010). Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463, 818-822.
22. Kiss, A., Li, L., Gettemeier, T. & Venkatesh, L. K. (2003). Functional analysis of the interaction of the human immunodeficiency virus type 1 Rev nuclear export signal with its cofactors. Virology 314, 591-600.
23. Kutay, U. & Güttinger, S. (2005). Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol 15, 121-124.
24. Lim, R. Y., Ullman, K. S. & Fahrenkrog, B. (2008). Biology and biophysics of the nuclear pore complex and its components. Int Rev Cell Mol Biol 267, 299-342.
25. Lommer, B. S. & Luo, M. (2002). Structural plasticity in influenza virus protein NS2 (NEP). J Biol Chem 277, 7108-7117.
26. Nayak, D. P., Hui, E. K. & Barman, S. (2004). Assembly and budding of influenza virus. Virus Res 106, 147-165.
27. Neumann, G., Hughes, M. T. & Kawaoka, Y. (2000). Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO J 19, 6751-6758.
28. Neville, M., Stutz, F., Lee, L., Davis, L. I. & Rosbash, M. (1997). The importin-b family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr Biol 7, 767-775.
29. Oka, M., Asally, M., Yasuda, Y., Ogawa, Y., Tachibana, T. & Yoneda, Y. (2010). The mobile FG nucleoporin Nup98 is a cofactor for Crm1-dependent protein export. Mol Biol Cell 21, 1885-1896.
30. O'Neill, R. E., Talon, J. & Palese, P. (1998). The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J 17, 288-296.
31. Otero, G. C., Harris, M. E., Donello, J. E. & Hope, T. J. (1998). Leptomycin B inhibits equine infectious anemia virus Rev and feline immunodeficiency virus Rev function but not the function of the hepatitis B virus post-transcriptional regulatory element. J Virol 72, 7593-7597.
32. Park, N., Katikaneni, P., Skern, T. & Gustin, K. E. (2007). Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J Virol 82, 1647-1655.
33. Pemberton, L. F. & Paschal, B. M. (2005). Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6, 187-198.
34. Powers, M. A., Forbes, D. J., Dahlberg, J. E. & Lund, E. (1997). The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways. J Cell Biol 136, 241-250.
35. Pritchard, C. E., Fornerod, M., Kasper, L. H. & van Deursen, J. M. (1999). RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J Cell Biol 145, 237-254.
36. Radu, A., Moore, M. S. & Blobel, G. (1995a). The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81, 215-222.
37. Radu, A., Blobel, G. & Moore, M. S. (1995b). Identification of a protein complex that is required for nuclear protein import and mediates docking of import substrate to distinct nucleoporins. Proc Natl Acad Sci U S A 92, 1769-1773.
38. Reed, L. J. & Muench, H. (1938). A simple method of estimating fifty per cent endpoints. Am J Hyg 27, 493-497.
39. Ricour, C., Delhaye, S., Hato, S. V., Olenyik, T. D., Michel, B., van Kuppeveld, F. J., Gustin, K. E. & Michiels, T. (2009). Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler's virus leader protein. J Gen Virol 90, 177-186.
40. Sanz-Ezquerro, J. J., de la Luna, S., Ort́n, J. & Nieto, A. (1995). Individual expression of influenza virus PA protein induces degradation of coexpressed proteins. J Virol 69, 2420-2426.
41. Satterly, N., Tsai, P. L., van Deursen, J., Nussenzveig, D. R., Wang, Y., Faria, P. A., Levay, A., Levy, D. E. & Fontoura, B. M. (2007). Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104, 1853-1858.
42. Stutz, F., Izaurralde, E., Mattaj, I. W. & Rosbash, M. (1996). A role for nucleoporin FG repeat domains in export of human immunodeficiency virus type 1 Rev protein and RNA from the nucleus. Mol Cell Biol 16, 7144-7150.
43. Terry, L. J. & Wente, S. R. (2007). Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J Cell Biol 178, 1121-1132.
44. Terry, L. J. & Wente, S. R. (2009). Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot Cell 8, 1814-1827.
45. Tran, E. J. & Wente, S. R. (2006). Dynamic nuclear pore complexes: life on the edge. Cell 125, 1041-1053.
46. Turner, J. G. & Sullivan, D. M. (2008). CRM1-mediated nuclear export of proteins and drug resistance in cancer. Curr Med Chem 15, 2648-2655.
47. Weis, K. (2002). Nucleocytoplasmic transport: cargo trafficking across the border. Curr Opin Cell Biol 14, 328-335.
48. Yasuda, J., Nakada, S., Kato, A., Toyoda, T. & Ishihama, A. (1993). Molecular assembly of influenza virus: association of the NS2 protein with virion matrix. Virology 196, 249-255.
49. Zheng, L., Wang, F., Yang, Z., Chen, J., Chang, H. & Chen, Z. (2009). A single immunization with HA DNA vaccine by electroporation induces early protection against H5N1 avian influenza virus challenge in mice. BMC Infect Dis 9, 17.
50. Zolotukhin, A. S. & Felber, B. K. (1999). Nucleoporins Nup98 and Nup214 participate in nuclear export of human immunodeficiency virus type 1 Rev. J Virol 73, 120-127.