Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler's virus leader protein

Journal of General Virology

Volumn 90, Issue 1, 2009, Pages 177-186

  Ricour, Céline ^a   Delhaye, Sophie ^a   Hato, Stanleyson V ^b   Olenyik, Tamara D ^c   Michel, Bénédicte ^a   van Kuppeveld, Frank J M ^b   Gustin, Kurt E ^c   Michiels, Thomas ^a  

^a DE DUVE INSTITUTE   (Belgium)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; FIREFLY LUCIFERASE; GREEN FLUORESCENT PROTEIN; INTERFERON REGULATORY FACTOR 3; MESSENGER RNA; NUCLEOPORIN 98; SIGNAL PEPTIDE; ZINC FINGER PROTEIN; LUCIFERASE; NUCLEAR PORE COMPLEX PROTEIN 98; NUCLEOPORIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL LINE; CELL NUCLEUS; CONTROLLED STUDY; DIMERIZATION; GENE MUTATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IN SITU HYBRIDIZATION; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; NUCLEAR PORE COMPLEX; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; RNA TRANSPORT; WESTERN BLOTTING; WILD TYPE; ANIMAL; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REPORTER GENE;

MUS; PICORNAVIRIDAE; THEILER'S ENCEPHALOMYELITIS VIRUS;

ANIMALS; DIMERIZATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; INTERFERON REGULATORY FACTOR-3; LUCIFERASES; MICE; NUCLEAR PORE COMPLEX PROTEINS; PHOSPHORYLATION; RNA, MESSENGER; THEILOVIRUS; VIRAL PROTEINS;

EID: 59849121682     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.005678-0     Document Type: Article

References (45)

1. Baida, G., Popko, B., Wollmann, R. L., Stavrou, S., Lin, W., Tretiakova, M., Krausz, T. N. & Roos, R. P. (2008). A subgenomic segment of Theiler's murine encephalomyelitis virus RNA causes demyelination. J Virol 82, 5879-5886.
2. Blevins, M. B., Smith, A. M., Phillips, E. M. & Powers, M. A. (2003). Complex formation among the RNA export proteins Nup98, Rae1/ Gle2, and TAP. J Biol Chem 278, 20979-20988.
3. Brahic, M., Bureau, J. F. & Michiels, T. (2005). The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu Rev Microbiol 59, 279-298.
4. Chakraborty, P., Satterly, N. & Fontoura, B. M. (2006). Nuclear export assays for poly(A) RNAs. Methods 39, 363-369.
5. Chen, H. H., Kong, W. P. & Roos, R. P. (1995). The leader peptide of Theiler's murine encephalomyelitis virus is a zinc-binding protein. J Virol 69, 8076-8078.
6. Daniels, J. B., Pappenheimer, A. M. & Richardson, S. (1952). Observations on encephalomyelitis of mice (DA strain). J Exp Med 96, 517-530.
7. Delhaye, S., van Pesch, V. & Michiels, T. (2004). The leader protein of Theiler's virus interferes with nucleocytoplasmic trafficking of cellular proteins. J Virol 78, 4357-4362.
8. Delhaye, S., Paul, S., Blakqori, G., Minet, M., Weber, F., Staeheli, P. & Michiels, T. (2006). Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci U S A 103, 7835-7840.
9. Faria, P. A., Chakraborty, P., Levay, A., Barber, G. N., Ezelle, H. J., Enninga, J., Arana, C., van Deursen, J. & Fontoura, B. M. (2005). VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol Cell 17, 93-102.
10. Fiette, L., Aubert, C., Muller, U., Huang, S., Aguet, M., Brahic, M. & Bureau, J. F. (1995). Theiler's virus infection of 129Sv mice that lack the interferon α/β or interferon γ receptors. J Exp Med 181, 2069-2076.
11. Fitzgerald, K. A., McWhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., Coyle, A. J., Liao, S. M. & Maniatis, T. (2003). IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4, 491-496.
12. Ghadge, G. D., Ma, L., Sato, S., Kim, J. & Roos, R. P. (1998). A protein critical for a Theiler's virus-induced immune system-mediated demyelinating disease has a cell type-specific antiapoptotic effect and a key role in virus persistence. J Virol 72, 8605-8612.
13. Hato, S. V., Ricour, C., Schulte, B. M., Lanke, K. H., de Bruijni, M., Zoll, J., Melchers, W. J., Michiels, T. & van Kuppeveld, F. J. (2007). The mengovirus leader protein blocks interferon-α/ β gene transcription and inhibits activation of interferon regulatory factor 3. Cell Microbiol 9, 2921-2930.
14. Her, L. S., Lund, E. & Dahlberg, J. E. (1997). Inhibition of Ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus. Science 276, 1845-1848.
15. Jnaoui, K. & Michiels, T. (1998). Adaptation of Theiler's virus to L929 cells: mutations in the putative receptor binding site on the capsid map to neutralization sites and modulate viral persistence. Virology 244, 397-404.
16. Kong, W. P. & Roos, R. P. (1991). Alternative translation initiation site in the DA strain of Theiler's murine encephalomyelitis virus. J Virol 65, 3395-3399.
17. Kong, W. P., Ghadge, G. D. & Roos, R. P. (1994). Involvement of cardiovirus leader in host cell-restricted virus expression. Proc Natl Acad Sci U S A 91, 1796-1800.
18. Kramer, M., Schulte, B. M., Toonen, L. W., Barral, P. M., Fisher, P. B., Lanke, K. H., Galama, J. M., van Kuppeveld, F. J. & Adema, G. J. (2008). Phagocytosis of picornavirus-infected cells induces an RNA-dependent antiviral state in human dendritic cells. J Virol 82, 2930-2937.
19. Lidsky, P. V., Hato, S., Bardina, M. V., Aminev, A. G., Palmenberg, A. C., Sheval, E. V., Polyakov, V. Y., van Kuppeveld, F. J. & Agol, V. I. (2006). Nucleocytoplasmic traffic disorder induced by cardioviruses. J Virol 80, 2705-2717.
20. Lin, R., Heylbroeck, C., Genin, P., Pitha, P. M. & Hiscott, J. (1999a). Essential role of interferon regulatory factor 3 in direct activation of RANTES chemokine transcription. Mol Cell Biol 19, 959-966.
21. Lin, R., Mamane, Y. & Hiscott, J. (1999b). Structural and functional analysis of interferon regulatory factor 3: localization of the transactivation and autoinhibitory domains. Mol Cell Biol 19, 2465-2474.
22. McAllister, A., Tangy, F., Aubert, C. & Brahic, M. (1989). Molecular cloning of the complete genome of Theiler's virus, strain DA, and production of infectious transcripts. Microb Pathog 7, 381-388.
23. Michiels, T., Dejong, V., Rodrigus, R. & Shaw-Jackson, C. (1997). Protein 2A is not required for Theiler's virus replication. J Virol 71, 9549-9556.
24. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M. & Aguet, M. (1994). Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921.
25. Overbergh, L., Giulietti, A., Valckx, D., Decallonne, R., Bouillon, R. & Mathieu, C. (2003). The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression. J Biomol Tech 14, 33-43.
26. Panne, D., Maniatis, T. & Harrison, S. C. (2007). An atomic model of the interferon-β enhanceosome. Cell 129, 1111-1123.
27. Park, N., Katikaneni, P., Skem, T. & Gustin, K. E. (2008). Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J Virol 82, 1647-1655.
28. Paul, S. & Michiels, T. (2006). Cardiovirus leader proteins are functionally interchangeable and have evolved to adapt to virus replication fitness. J Gen Virol 87, 1237-1246.
29. Petro, T. M. (2005). ERK-MAP-kinases differentially regulate expression of IL-23 p19 compared with p40 and IFN-β in Theiler's virus-infected RAW264.7 cells. Immunol Lett 97, 47-53.
30. Porter, F. W., Bochkov, Y. A., Albee, A. J., Wiese, C. & Palmenberg, A. C. (2006). A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc Natl Acad Sci U S A 103, 12417-12422.
31. 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.
32. 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.
33. Rodriguez, M. S., Dargemont, C. & Stutz, F. (2004). Nuclear export of RNA. Biol Cell 96, 639-655.
34. Schafer, S. L., Lin, R., Moore, P. A., Hiscott, J. & Pitha, P. M. (1998). Regulation of type I interferon gene expression by interferon regulatory factor-3. J Biol Chem 273, 2714-2720.
35. Sharma, S., tenOever, B. R., Grandvaux, N., Zhou, G. P., Lin, R. & Hiscott, J. (2003). Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151.
36. Shaw-Jackson, C. & Michiels, T. (1999). Absence of internal ribosome entry site-mediated tissue specificity in the translation of a bicistronic transgene. J Virol 73, 2729-2738.
37. Sommereyns, C., Paul, S., Staeheli, P. & Michiels, T. (2008). IFN-lambda (IFN-λ) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4, e1000017.
38. Theiler, M. & Gard, S. (1940). Encephalomyelitis of mice. I. Characteristics and pathogenesis of the virus. J Exp Med 72, 49-67.
39. van Eyll, O. & Michiels, T. (2002). Non-AUG-initiated internal translation of the L* protein of Theiler's virus and importance of this protein for viral persistence. J Virol 76, 10665-10673.
40. van Pesch, V. & Michiels, T. (2003). Characterization of interferona-α13, a novel constitutive murine interferon-α subtype. J Biol Chem 278, 46321-46328.
41. van Pesch, V., van Eyll, O. & Michiels, T. (2001). The leader protein of Theiler's virus inhibits immediate-early alpha/beta interferon production. J Virol 75, 7811-7817.
42. van Pesch, V., Lanaya, H., Renauld, J. C. & Michiels, T. (2004). Characterization of the murine alpha interferon gene family. J Virol 78, 8219-8228.
43. Yoneyama, M., Suhara, W., Fukuhara, Y., Fukuda, M., Nishida, E. & Fujita, T. (1998). Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J 17, 1087-1095.
44. Zoll, J., Galama, J. M., van Kuppeveld, F. J. & Melchers, W. J. (1996). Mengovirus leader is involved in the inhibition of host cell protein synthesis. J Virol 70, 4948-4952.
45. Zoll, J., Melchers, W. J., Galama, J. M. & van Kuppeveld, F. J. (2002). The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-κB. J Virol 76, 9664-9672.