The adenovirus VA RNA-derived miRNAs are not essential for lytic virus growth in tissue culture cells

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 4802-4812

  Kamel, Wael ^a   Segerman, Bo ^b   Öberg, Daniel ^a   Punga, Tanel ^a   Akusjärvi, Göran ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b NATIONAL VETERINARY INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; DICER; DNA DIRECTED RNA POLYMERASE III; MICRORNA; PROTEIN KINASE R; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS ASSOCIATED RNA I; VIRUS RNA;

ADENOVIRUS; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA BINDING; TISSUE CULTURE CELL; VIROGENESIS; VIRUS RECOMBINANT;

ADENOVIRUSES, HUMAN; BASE SEQUENCE; EIF-2 KINASE; GENETIC VECTORS; HEK293 CELLS; HELA CELLS; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; RNA, VIRAL; RNA-INDUCED SILENCING COMPLEX;

EID: 84876146243     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt172     Document Type: Article

References (39)

1. Thimmappaya, B., Weinberger, C., Schneider, R.J. and Shenk, T. (1982) Adenovirus VAI RNA is required for efficient translation of viral mRNAs at late times after infection. Cell, 31, 543-551.
2. Maran, A. and Mathews, M.B. (1988) Characterization of the double-stranded RNA implicated in the inhibition of protein synthesis in cells infected with a mutant adenovirus defective for VA RNA. Virology, 164, 106-113.
3. Mathews, M.B. and Shenk, T. (1991) Adenovirus virus-associated RNA and translation control. J. Virol., 65, 5657-5662.
4. Andersson, M.G., Haasnoot, P.C., Xu, N., Berenjian, S., Berkhout, B. and Akusjarvi, G. (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol., 79, 9556-9565.
5. Aparicio, O., Razquin, N., Zaratiegui, M., Narvaiza, I. and Fortes, P. (2006) Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol., 80, 1376-1384.
6. Lu, S. and Cullen, B.R. (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J. Virol., 78, 12868-12876.
7. Sano, M., Kato, Y. and Taira, K. (2006) Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett., 580, 1553-1564.
8. Xu, N., Gkountela, S., Saeed, K. and Akusjarvi, G. (2009) The 5-end heterogeneity of adenovirus virus-associated RNAI contributes to the asymmetric guide strand incorporation into the RNA-induced silencing complex. Nucleic Acids Res., 37, 6950-6959.
9. Bennasser, Y., Chable-Bessia, C., Triboulet, R., Gibbings, D., Gwizdek, C., Dargemont, C., Kremer, E.J., Voinnet, O. and Benkirane, M. (2011) Competition for XPO5 binding between Dicer mRNA, pre-miRNA and viral RNA regulates human Dicer levels. Nat. Struct. Mol. Biol., 18, 323-327.
10. Xu, N., Segerman, B., Zhou, X. and Akusjarvi, G. (2007) Adenovirus virus-associated RNAII-derived small RNAs are efficiently incorporated into the RNA-induced silencing complex and associate with polyribosomes. J. Virol., 81, 10540-10549.
11. Aparicio, O., Carnero, E., Abad, X., Razquin, N., Guruceaga, E., Segura, V. and Fortes, P. (2010) Adenovirus VA RNA-derived miRNAs target cellular genes involved in cell growth, gene expression and DNA repair. Nucleic Acids Res., 38, 750-763.
12. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
13. Chekulaeva, M. and Filipowicz, W. (2009) Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol., 21, 452-460.
14. He, T.C., Zhou, S., da Costa, L.T., Yu, J., Kinzler, K.W. and Vogelstein, B. (1998) A simplified system for generating recombinant adenoviruses. Proc. Natl Acad. Sci. USA, 95, 2509-2514.
15. Luo, J., Deng, Z.L., Luo, X., Tang, N., Song, W.X., Chen, J., Sharff, K.A., Luu, H.H., Haydon, R.C., Kinzler, K.W. et al. (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc., 2, 1236-1247.
16. Bhat, R.A. and Thimmappaya, B. (1984) Adenovirus mutants with DNA sequence perturbations in the intragenic promoter of VAI RNA gene allow the enhanced transcription of VAII RNA gene in HeLa cells. Nucleic Acids Res., 12, 7377-7388.
17. Xu, N. and Akusjarvi, G. (2011) Characterization of RISC-associated adenoviral small RNAs. Methods Mol. Biol., 721, 183-198.
18. Pall, G.S. and Hamilton, A.J. (2008) Improved northern blot method for enhanced detection of small RNA. Nat. Protoc., 3, 1077-1084.
19. Fallaux, F.J., Kranenburg, O., Cramer, S.J., Houweling, A., Van Ormondt, H., Hoeben, R.C. and Van Der Eb, A.J. (1996) Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum. Gene Ther., 7, 215-222.
20. Fowlkes, D.M. and Shenk, T. (1980) Transcriptional control regions of the adenovirus VAI RNA gene. Cell, 22, 405-413.
21. Svensson, C. and Akusjarvi, G. (1984) Adenovirus VA RNAI: a positive regulator of mRNA translation. Mol. Cell. Biol., 4, 736-742.
22. Guilfoyle, R. and Weinmann, R. (1981) Control region for adenovirus VA RNA transcription. Proc. Natl Acad. Sci. USA, 78, 3378-3382.
23. Soderlund, H., Pettersson, U., Vennstrom, B., Philipson, L. and Mathews, M.B. (1976) A new species of virus-coded low molecular weight RNA from cells infected with adenovirus type 2. Cell, 7, 585-593.
24. Vennstrom, B., Pettersson, U. and Philipson, L. (1978) Two initiation sites for adenovirus 5.5S RNA. Nucleic Acids Res., 5, 195-204.
25. Thimmappaya, B., Jones, N. and Shenk, T. (1979) A mutation which alters initiation of transcription by RNA polymerase III on the Ad5 chromosome. Cell, 18, 947-954.
26. Wahid, A.M., Coventry, V.K. and Conn, G.L. (2008) Systematic deletion of the adenovirus-associated RNAI terminal stem reveals a surprisingly active RNA inhibitor of double-stranded RNA-activated protein kinase. J. Biol. Chem., 283, 17485-17493.
27. Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z., Aronin, N. and Zamore, P.D. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell, 115, 199-208.
28. Khvorova, A., Reynolds, A. and Jayasena, S.D. (2003) Functional siRNAs and miRNAs exhibit strand bias. Cell, 115, 209-216.
29. Robertson, H.D. and Mathews, M.B. (1996) The regulation of the protein kinase PKR by RNA. Biochimie, 78, 909-914.
30. McKenna, S.A., Lindhout, D.A., Shimoike, T., Aitken, C.E. and Puglisi, J.D. (2007) Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR. J. Mol. Biol., 372, 103-113.
31. Svensson, C. and Akusjarvi, G. (1986) Defective RNA splicing in the absence of adenovirus-associated RNAI. Proc. Natl Acad. Sci. USA, 83, 4690-4694.
32. Gantier, M.P., McCoy, C.E., Rusinova, I., Saulep, D., Wang, D., Xu, D., Irving, A.T., Behlke, M.A., Hertzog, P.J., Mackay, F. et al. (2011) Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res., 39, 5692-5703.
33. Gwizdek, C., Ossareh-Nazari, B., Brownawell, A.M., Evers, S., Macara, I.G. and Dargemont, C. (2004) Minihelix-containing RNAs mediate exportin-5-dependent nuclear export of the double-stranded RNA-binding protein ILF3. J. Biol. Chem., 279, 884-891.
34. Sullivan, C.S., Grundhoff, A.T., Tevethia, S., Pipas, J.M. and Ganem, D. (2005) SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature, 435, 682-686.
35. Buck, A.H., Perot, J., Chisholm, M.A., Kumar, D.S., Tuddenham, L., Cognat, V., Marcinowski, L., Dolken, L. and Pfeffer, S. (2010) Post-transcriptional regulation of miR-27 in murine cytomegalovirus infection. RNA, 16, 307-315.
36. Yanagawa-Matsuda, A., Kitamura, T., Higashino, F., Yamano, S., Totsuka, Y. and Shindoh, M. (2012) E1A expression might be controlled by miR-214 in cells with low adenovirus productivity. Virus Res., 170, 85-90.
37. Benhamed, M., Herbig, U., Ye, T., Dejean, A. and Bischof, O. (2012) Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat. Cell Biol., 14, 266-275.
38. Garnett, C.T., Talekar, G., Mahr, J.A., Huang, W., Zhang, Y., Ornelles, D.A. and Gooding, L.R. (2009) Latent species C adenoviruses in human tonsil tissues. J. Virol., 83, 2417-2428.
39. Cai, X. and Cullen, B.R. (2006) Transcriptional origin of Kaposi's sarcoma-associated herpesvirus microRNAs. J. Virol., 80, 2234-2242.