Nuclear factor NF45 interacts with viral proteins of infectious bursal disease virus and inhibits viral replication

Journal of Virology

Volumn 84, Issue 20, 2010, Pages 10592-10605

  Stricker, Ruth L O ^a   Behrens, Sven Erik ^b   Mundt, Egbert ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; INTERLEUKIN ENHANCER BINDING FACTOR 2; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CYTOPLASM; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA VIRUS; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; BASE SEQUENCE; CELL LINE; CERCOPITHECUS AETHIOPS; CHICKENS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; DNA PRIMERS; HOST-PATHOGEN INTERACTIONS; INFECTIOUS BURSAL DISEASE VIRUS; KARYOPHERINS; NUCLEAR FACTOR 45 PROTEIN; RABBITS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA INTERFERENCE; RNA, SMALL INTERFERING; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

INFECTIOUS BURSAL DISEASE VIRUS; MIRIDAE; RNA VIRUSES;

EID: 77957200286     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02506-09     Document Type: Article

References (62)

1. Agbottah, E. T., C. Traviss, J. McArdle, S. Karki, G. C. St Laurent 3rd, and A. Kumar. 2007. Nuclear factor 90 (NF90) targeted to TAR RNA inhibits transcriptional activation of HIV. Retrovirology 4:41.
2. Barber, G. N. 2009. The NFAR's (nuclear factors associated with dsRNA): evolutionarily conserved members of the dsRNA binding protein family. RNA Biol. 6:35-39.
3. Birghan, C., E. Mundt, and A. E. Gorbalenya. 2000. A non-canonical lon proteinase lacking the ATPase domain employs the ser-Lys catalytic dyad to exercise broad control over the life cycle of a double-stranded RNA virus. EMBO J. 19:114-123.
4. Corthésy, B., and P. N. Kao. 1994. Purification by DNA affinity chromatography of two polypeptides that contact the NF-AT DNA binding site in the interleukin 2 promoter. J. Biol. Chem. 269:20682-20690.
5. Cosgrove, A. S. 1962. An apparently new disease of chickens: avian nephrosis. Avian Dis. 6:385-389.
6. Da Costa, B., C. Chevalier, C. Henry, J. C. Huet, S. Petit, J. Lepault, H. Boot, and B. Delmas. 2002. The capsid of infectious bursal disease virus contains several small peptides arising from the maturation process of pVP2. J. Virol. 76:2393-2402. (Pubitemid 34150707)
7. Delmas, B., F. S. B. Kibenge, J. C. Leong, E. Mundt, V. N. Vakharia, and J. L. Wu. 2005. Birnaviridae, p. 561-569. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and A. L. Ball (ed.), Virus taxonomy, Academic Press, London, England.
8. Diaz, M. O., S. Ziemin, M. M. Le Beau, P. Pitha, S. D. Smith, R. R. Chilcote, and J. D. Rowley. 1988. Homozygous deletion of the alpha- and beta 1-interferon genes in human leukemia and derived cell lines. Proc. Natl. Acad. Sci. U. S. A. 85:5259-5263.
9. Dobos, P., B. J. Hill, R. Hallett, D. T. Kells, H. Becht, and D. Teninges. 1979. Biophysical and biochemical characterization of five animal viruses with bisegmented double-stranded RNA genomes. J. Virol. 32:593-605. (Pubitemid 10188774)
10. Granzow, H., C. Birghan, T. C. Mettenleiter, J. Beyer, B. Köllner, and E. Mundt. 1997. A second form of infectious bursal disease virus-associated tubule contains VP4. J. Virol. 71:8879-8885. (Pubitemid 27446476)
11. Guan, D., N. Altan-Bonnet, A. M. Parrott, C. J. Arrigo, Q. Li, M. Khaleduzzaman, H. Li, C. G. Lee, T. Pe'ery, and M. B. Mathews. 2008. Nuclear factor 45 (NF45) is a regulatory subunit of complexes with NF90/110 involved in mitotic control. Mol. Cell. Biol. 28:4629-4641.
12. Himly, M., D. N. Foster, I. Bottoli, J. S. Iacovoni, and P. K. Vogt. 1998. The DF-chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248:295-304.
13. Icard, A. H., H. S. Sellers, and E. Mundt. 2008. Detection of infectious bursal disease virus isolates with unknown antigenic properties by reverse genetics. Avian Dis. 52:590-598.
14. Irigoyen, N., D. Garriga, A. Navarro, N. Verdaguer, J. F. Rodríguez, and J. R. Castón. 2009. Autoproteolytic activity derived from the infectious bursal disease virus capsid protein. J. Biol. Chem. 284:8064-8072.
15. Isken, O., M. Baroth, C. W. Grassmann, S. Weinlich, D. H. Ostareck, A. Ostareck-Lederer, and S. E. Behrens. 2007. Nuclear factors are involved in hepatitis C virus RNA replication. RNA 13:1675-1692.
16. Isken, O., C. W. Grassmann, R. T. Sarisky, M. Kann, S. Zhang, F. Grosse, P. N. Kao, and S. E. Behrens. 2003. Members of the NF90/NFAR protein group are involved in the life cycle of a positive-strand RNA virus. EMBO J. 22:5655-5665.
17. Isken, O., C. W. Grassmann, H. Yu, and S. E. Behrens. 2004. Complex signals in the genomic 3′ nontranslated region of bovine viral diarrhea virus coordinate translation and replication of the viral RNA. RNA 10:1637-1652.
18. Kao, P. N., L. Chen, G. Brock, J. Ng, J. Kenny, A. J. Smith, and B. Corthésy. 1994. Cloning and expression of cyclosporin A- and FK506-sensitive nuclear factor of activated T-cells: NF45 and NF90. J. Biol. Chem. 269:20691-20699.
19. Klopfleisch, R., O. Werner, E. Mundt, T. Harder, and J. P. Teifke. 2006. Neurotropism of highly pathogenic avian influenza virus /chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columbia livia f. domestica). Vet. Pathol. 43:463-470.
20. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
21. Kuwano, Y., H. H. Kim, K. Abdelmohsen, R. Pullmann, Jr., J. L. Martindale, X. Yang, and M. Gorospe. 2008. MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28:4562-4575.
22. Kuwano, Y., R. Pullmann, Jr., B. S. Marasa, K. Abdelmohsen, E. K. Lee, X. Yang, J. L. Martindale, M. Zhan, and M. Gorospe. 2010. NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res. 38:225-238.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head for bacteriophage T4. Nature 227:680-685.
24. Langland, J. O., P. N. Kao, and B. L. Jacobs. 1999. Nuclear factor-90 of activated T-cells: a double-stranded RNA-binding protein and substrate for the double-stranded RNA-dependent protein kinase, PKR. Biochemistry 38:6361-6368.
25. Lejal, N., B. Da Costa, J.-C. Huet, and B. Delmas. 2000. Role of Ser-652 and Lys-692 in the protease activity of infectious bursal disease virus VP4 and identification of its substrate cleavage sites. J. Gen. Virol. 81:983-992.
26. Letzel, T., E. Mundt, and A. E. Gorbalenya. 2007. Evidence for functional significance of the permuted C motif in Co2+-stimulated RNA-dependent RNA polymerase of infectious bursal disease virus. J. Gen. Virol. 88:2824-2833.
27. Liao, H. J., R. Kobayashi, and M. B. Mathews. 1998. Activities of adenovirus virus-associated RNAs: purification and characterization of RNA binding proteins. Proc. Natl. Acad. Sci. U. S. A. 95:8514-8519.
28. Lombardo, E., A. Maraver, I. Espinosa, A. Fernández-Arias, and J. F. Rodriguez. 2000. VP5, the nonstructural polypeptide of infectious bursal disease virus, accumulates within the host plasma membrane and induces cell lysis. Virology 277:345-357.
29. Luque, D., I. Saugar, M. T. Rejas, J. L. Carrascosa, J. F. Rodríguez, and J. R. Castón. 2009. Infectious bursal disease virus: ribonucleoprotein complexes of a double-stranded RNA virus. J. Mol. Biol. 386:891-901.
30. Ma, K., A. M. Roy, and G. R. Whittaker. 2001. Nuclear export of influenza virus ribonucleoproteins: identification of an export intermediate at the nuclear periphery. Virology 282:215-220.
31. Maraver, A., A. Oña, F. Abaitua, D. González, R. Clemente, J. A. Ruiz-Díaz, J. R. Castón, F. Pazos, and J. F. Rodriguez. 2003. The oligomerization domain of VP3, the scaffolding protein of infectious bursal disease virus, plays a critical role in capsid assembly. J. Virol. 77:6438-6449.
32. Merrill, M. K., and M. Gromeier. 2006. The double-stranded RNA binding protein 76:NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site. J. Virol. 80:6936-6942.
33. Mundt, E., J. Beyer, and H. Müller. 1995. Identification of a novel viral protein in infectious bursal disease virus-infected cells. J. Gen. Virol. 76: 437-443.
34. Mundt, E., B. Köllner, and D. Kretzschmar. 1997. VP5 of infectious bursal disease virus is not essential for viral replication in cell culture. J. Virol. 71:5647-5651. (Pubitemid 27258247)
35. Mundt, E., and V. N. Vakharia. 1996. Synthetic transcripts of double-stranded Birnavirus genome are infectious. Proc. Natl. Acad. Sci. U. S. A. 93:11131-11136.
36. Nie, Y., L. Ding, P. N. Kao, R. Braun, and J. H. Yang. 2005. ADAR1 interacts with NF90 through double-stranded RNA and regulates NF90-mediated gene expression independently of RNA editing. Mol. Cell. Biol. 25:6956-6963.
37. Oña, A., D. Luque, F. Abaitua, A. Maraver, J. R. Castón, and J. F. Rodríguez. 2004. The C-terminal domain of the pVP2 precursor is essential for the interaction between VP2 and VP3, the capsid polypeptides of infectious bursal disease virus. Virology 322:135-142.
38. Parker, L. M., I. Fierro-Monti, and M. B. Mathews. 2001. Nuclear factor 90 is a substrate and regulator of the eukaryotic initiation factor 2 kinase double-stranded RNA-activated protein kinase. J. Biol. Chem. 276:32522-32530.
39. Pfeifer, I., R. Elsby, M. Fernandez, P. A. Faria, D. R. Nussenzveig, I. S. Lossos, B. M. Fontoura, W. D. Martin, and G. N. Barber. 2008. NFAR-1 and -2 modulate translation and are required for efficient host defense. Proc. Natl. Acad. Sci. U. S. A. 105:4173-4178.
40. Ranpura, S. A., U. Deshmukh, and P. P. Reddi. 2008. NF45 and NF90 in murine seminiferous epithelium: potential role in SP-10 gene transcription. J. Androl. 29:186-197.
41. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Epidemiol. 27:493-497.
42. Sakamoto, S., K. Aoki, T. Higuchi, H. Todaka, K. Morisawa, N. Tamaki, E. Hatano, A. Fukushima, T. Taniguchi, and Y. Agata. 2009. The NF90-NF45 complex functions as a negative regulator in the microRNA processing pathway. Mol. Cell. Biol. 29:3754-3769.
43. Saunders, L. R., D. J. Perkins, S. Balachandran, R. Michaels, R. Ford, A. Mayeda, and G. N. Barber. 2001. Characterization of two evolutionarily conserved, alternatively spliced nuclear phosphoproteins, NFAR-1 and -2, that function in mRNA processing and interact with the double-stranded RNA-dependent protein kinase, PKR. J. Biol. Chem. 276:32300-32312.
44. Shaw, J. P., P. J. Utz, D. B. Durand, J. J. Toole, E. A. Emmel, and G. R. Crabtree. 1988. Identification of a putative regulator of early T cell activation genes. Science 241:202-205.
45. Shi, L., W. R. Godfrey, J. Lin, G. Zhao, and P. N. Kao. 2007. NF90 regulates inducible IL-2 gene expression in T cells. J. Exp. Med. 204:971-977.
46. Shi, L., D. Qiu, G. Zhao, B. Corthesy, S. Lees-Miller, W. H. Reeves, and P. N. Kao. 2007. Dynamic binding of Ku80, Ku70 and NF90 to the IL-2 promoter in vivo in activated T-cells. Nucleic Acids Res. 35:2302-2310.
47. Shi, L., G. Zhao, D. Qiu, W. R. Godfrey, H. Vogel, T. A. Rando, H. Hu, P. N. Kao. 2005. NF90 regulates cell cycle exit and terminal myogenic differentiation by direct binding to the 3′-untranslated region of MyoD and p21WAF1/CIP1 mRNAs. J. Biol. Chem. 280:18981-18989.
48. Shim, J., H. Lim, R. Yates, and M. Karin. 2002. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell 10:1331-1344. (Pubitemid 36050875)
49. Shin, H. J., S. S. Kim, Y. H. Cho, S. G. Lee, and H. M. Rho. 2002. Host cell proteins binding to the encapsidation signal epsilon in hepatitis B virus RNA. Arch. Virol. 147:471-491.
50. Snyder, D. B., D. P. Lana, P. K. Savage, F. S. Yancey, S. A. Mengel, and W. W. Marquardt. 1988. Differentiation of infectious bursal disease virus directly from infected tissues with neutralizing monoclonal antibodies: evidence of a major antigenic shift in recent field isolates. Avian Dis. 32:535-539.
51. Spies, U., H. Müller, and H. Becht. 1989. Nucleotide sequence of infectious bursal disease virus genome segment A delineates two major open reading frames. Nucleic Acids Res. 17:7982. (Pubitemid 19251958)
52. Tacken, M. G., B. P. Peeters, A. A. Thomas, P. J. Rottier, and H. J. Boot. 2002. Infectious bursal disease virus capsid protein VP3 interacts both with VP1, the RNA-dependent RNA polymerase, and with viral double-stranded RNA. J. Virol. 76:11301-11311.
53. Ting, N. S., P. N. Kao, D. W. Chan, L. G. Lintott, and S. P. Lees-Miller. 1998. DNA-dependent protein kinase interacts with antigen receptor response element binding proteins NF90 and NF45. J. Biol. Chem. 273:2136-2145.
54. Tran, H., M. Schilling, C. Wirbelauer, D. Hess, and Y. Nagamine. 2004. Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Mol. Cell 13:101-111.
55. Von Einem, U. I., A. E. Gorbalenya, H. Schirrmeier, S. E. Behrens, T. Letzel, and E. Mundt. 2004. VP1 of infectious bursal disease virus is an RNA-dependent RNA polymerase. J. Gen. Virol. 85:2221-2229.
56. Vumbaca, F., K. N. Phoenix, D. Rodriguez-Pinto, D. K. Han, and K. P. Claffey. 2008. Double-stranded RNA-binding protein regulates vascular endothelial growth factor mRNA stability, translation, and breast cancer angiogenesis. Mol. Cell. Biol. 28:772-783.
57. Wang, P., W. Song, B. W. Mok, P. Zhao, K. Qin, A. Lai, G. J. Smith, J. Zhang, T. Lin, Y. Guan, and H. Chen. 2009. Nuclear factor 90 negatively regulates influenza virus replication by interacting with viral nucleoprotein. J. Virol. 83:7850-7861.
58. Xu, Y. H., and G. A. Grabowski. 1999. Molecular cloning and characterization of a translational inhibitory protein that binds to coding sequences of human acid beta-glucosidase and other mRNAs. Mol. Genet. Metab. 68: 441-454.
59. Xu, Y. H., C. Busald, and G. A. Grabowski. 2000. Reconstitution of TCP80/NF90 translation inhibition activity in insect cells. Mol. Genet. Metab. 70: 106-115.
60. Yao, K., and V. N. Vakharia. 2001. Induction of apoptosis in vitro by the 17-kDa nonstructural protein of infectious bursal disease virus: possible role in viral pathogenesis. Virology 285:50-58.
61. Yaseen, N. R., A. L. Maizel, F. Wang, and S. Sharma. 1993. Comparative analysis of NFAT (nuclear factor of activated T cells) complex in human T and B lymphocytes. J. Biol. Chem. 268:14285-14293.
62. Yewdell, J. W., E. Frank, and W. Gerhard. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. J. Immunol. 126:1814-1819.