Cap snatching in yeast L-BC double-stranded RNA totivirus

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 23716-23724

  Fujimura, Tsutomu ^a   Esteban, Rosa ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAP STRUCTURE; DOUBLE-STRANDED RNA; VIRUS TRANSFER;

VIRUSES;

RNA;

DOUBLE STRANDED RNA; MAGNESIUM; MANGANESE; MESSENGER RNA; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; CAP SNATCHING; CONTROLLED STUDY; COVALENT BOND; DNA METHYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; RNA CAPPING; RNA SEQUENCE; TOTIVIRUS; TRANSCRIPTION INITIATION; VIRION; VIRUS STRAIN; VIRUS TRANSCRIPTION; VIRUS TRANSMISSION; YEAST;

CAP SNATCHING; CAPPING; DOUBLE-STRANDED RNA; GAG; MRNA; RNA POLYMERASE; RNA VIRUSES; TRANSCRIPTION; YEAST;

AMINO ACID SEQUENCE; BASE SEQUENCE; CATIONS, DIVALENT; DIPHOSPHATES; GENE PRODUCTS, GAG; HISTIDINE; MOLECULAR SEQUENCE DATA; PHENOTYPE; RNA CAPS; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; TOTIVIRUS;

EID: 84882367190     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.490953     Document Type: Article

References (49)

1. Shatkin, A. J. (1976) Capping of eucaryotic mRNAs. Cell 9, 645-653
2. Konarska, M. M., Padgett, R. A., and Sharp, P. A. (1984) Recognition of cap structure in splicing in vitro of mRNA precursors. Cell 38, 731-736
3. Wickens, M. P., and Gurdon, J. B. (1983) Post-transcriptional processing of simian virus 40 late transcripts in injected frog oocytes. J. Mol. Biol. 163, 1-26
4. Izaurralde, E., Lewis, J., Gamberi, C., Jarmolowski, A., McGuigan, C., and Mattaj, I. W. (1995) A cap-binding protein complex mediating U snRNA export. Nature 376, 709-712
5. Gingras, A. C., Raught, B., and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963
6. Furuichi, Y., and Shatkin, A. J. (2000) Viral and cellular mRNA capping: past and prospects. Adv. Virus Res. 55, 135-184
7. Venkatesan, S., and Moss, B. (1980) Donor and acceptor specificities of HeLa cell mRNA guanylyltransferase. J. Biol. Chem. 255, 2835-2842
8. Shuman, S. (1995) Capping enzyme in eukaryotic mRNA synthesis. Prog. Nucleic Acid Res. Mol. Biol. 50, 101-129
9. Plotch, S. J., Bouloy, M., Ulmanen, I., and Krug, R. M. (1981) A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23, 847-858
10. Boivin, S., Cusack, S., Ruigrok, R. W., and Hart, D. J. (2010) Influenza A virus polymerase: structural insights into replication and host adaptation mechanisms. J. Biol. Chem. 285, 28411-28417
11. Fujimura, T., and Esteban, R. (2011) Cap-snatching mechanism in yeast L-A double-stranded RNA virus. Proc. Natl. Acad. Sci. U.S.A. 108, 17667-17671
12. Wickner, R. B. (2007) in Fields Virology (Knipe, D. M., and Howley, P. M., eds) 5th Ed., pp. 737-768, Lippincott Williams and Wilkins, Philadelphia, PA
13. Icho, T., and Wickner, R. B (1989) The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames. J. Biol. Chem. 264, 6716-6723
14. Fujimura, T., and Wickner, R. B. (1988) Gene overlap results in a viral protein having an RNA binding domain and a major coat protein domain. Cell 55, 663-671
15. Dinman, J. D., Icho, T., and Wickner, R. B. (1991) A-1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc. Natl. Acad. Sci. U.S.A. 88, 174-178
16. Cheng, R. H., Caston, J. R., Wang, G. J., Gu, F., Smith, T. J., Baker, T. S., Bozarth, R. F., Trus, B. L., Cheng, N., Wickner, R. B., and Steven, A. C. (1994) Fungal virus capsids, cytoplasmic compartments for the replication of double-stranded RNA, formed as icosahedral shells of asymmetric Gag dimers. J. Mol. Biol. 244, 255-258
17. Castón, J. R., Trus, B. L., Booy, F. P., Wickner, R. B., Wall, J. S., and Steven, A. C. (1997) Structure of L-A virus: a specialized compartment for the transcription and replication of double-stranded RNA. J. Cell Biol. 138, 975-985
18. Fujimura, T., Esteban, R., and Wickner, R. B. (1986) In vitro L-A doublestranded RNA synthesis in virus-like particles from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 83, 4433-4437
19. Fujimura, T., and Esteban, R. (2010) Yeast double-stranded RNA virus L-A deliberately synthesizes RNA transcripts with 5-diphosphate. J. Biol. Chem. 285, 22911-22918
20. Park, C. M., Lopinski, J. D., Masuda, J., Tzeng, T. H., and Bruenn, J. A. (1996) A second double-stranded RNA virus from yeast. Virology 216, 451-454
21. Tercero, J. C., and Wickner, R. B. (1992) MAK3 encodes an N-acetyltransferase whose modification of the L-A gag NH2 terminus is necessary for virus particle assembly. J. Biol. Chem. 267, 20277-20281
22. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032
23. Wesolowski, M., and Wickner, R. B. (1984) Two new double-stranded RNAmolecules showing non-Mendelian inheritance and heat inducibility in Saccharomyces cerevisiae. Mol. Cell Biol. 4, 181-1877
24. Blanc, A., Goyer, C., and Sonenberg, N. (1992) The coat protein of the yeast double-stranded RNAvirus L-A attaches covalently to the cap structure of eukaryotic mRNA. Mol. Cell Biol. 12, 3390-3398
25. Blanc, A., Ribas, J. C., Wickner, R. B., and Sonenberg, N. (1994) His-154 is involved in the linkage of the Saccharomyces cerevisiae L-A doublestranded RNA virus Gag protein to the cap structure of mRNAs and is essential for M1 satellite virus expression. Mol. Cell Biol. 14, 2664-2674
26. Minton, A. P. (1983) The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences. Mol. Cell Biochem. 55, 119-140
27. Fujimura, T., and Esteban, R. (2012) Cap snatching of yeast L-A doublestranded RNA virus can operate in trans and requires viral polymerase actively engaging in transcription. J. Biol. Chem. 287, 12797-12804
28. Fujimura, T., and Wickner, R. B. (1992) Interaction of two cis sites with the RNA replicase of the yeast L-A virus. J. Biol. Chem. 267, 2708-2713
29. Wickner, R. B., Icho, T., Fujimura, T., and Widner, W. R. (1991) Expression of yeast L-A double-stranded RNA virus proteins produces derepressed replication: a ski phenocopy. J. Virol. 65, 155-161
30. Wickner, R. B. (1980) Plasmids controlled exclusion of the K2 killer double-stranded RNA plasmid of yeast. Cell 21, 217-226
31. Esteban, R., Fujimura, T., and Wickner, R. B. (1989) Internal and terminal cis-acting sites are necessary for in vitro replication of the L-A doublestranded RNA virus of yeast. EMBO J. 8, 947-954
32. Tipper, D. J., and Bostian, K. A. (1984) Double-stranded ribonucleic acid killer systems in yeasts. Microbiol. Rev. 48, 125-156
33. Naitow, H., Tang, J., Canady, M., Wickner, R. B., and Johnson, J. E. (2002) L-A virus at 3.4-A resolution reveals particle architecture and mRNA decapping mechanism. Nat. Struct. Biol. 9, 725-728
34. Parker, R., and Song, H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11, 121-127
35. Wilusz, C. J., Wormington, M., and Peltz, S. W. (2001) The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2, 237-246
36. Wang, Z., and Kiledjian, M. (2001) Functional link between the mammalian exosome and mRNA decapping. Cell 107, 751-762
37. Liu, H., Rodgers, N. D., Jiao, X., and Kiledjian, M. (2002) The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J. 21, 4699-4708
38. Rodriguez, C. R., Takagi, T., Cho, E. J., and Buratowski, S. (1999) A Saccharomyces cerevisiae RNA 5-triphosphatase related to mRNA capping enzyme. Nucleic Acids Res. 27, 2181-2188
39. Tang, J., Naitow, H., Gardner, N. A., Kolesar, A., Tang, L., Wickner, R. B., and Johnson, J. E. (2005) The structural basis of recognition and removal of cellular mRNA 7-methyl G 'caps' by a viral capsid protein. A unique viral response to host defense. J. Mol. Recognit. 18, 158-168
40. HAkansson, K., Doherty, A. J., Shuman, S., and Wigley, D. B. (1997) X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89, 545-553
41. Chu, C., Das, K., Tyminski, J. R., Bauman, J. D., Guan, R., Qiu, W., Montelione, G. T., Arnold, E., and Shatkin, A. J. (2011) Structure of the guanylyltransferase domain of humanmRNAcapping enzyme. Proc. Natl. Acad. Sci. U.S.A. 108, 10104-10108
42. Shuman, S., and Lima, C. D. (2004) The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr. Opin. Struct. Biol. 14, 757-764
43. Pascal, J. M. (2008)DNAandRNAligases: structural variations and shared mechanisms. Curr. Opin. Struct. Biol. 18, 96-105
44. Ogino, T., Yadav, S. P., and Banerjee, A. K. (2010) Histidine-mediated RNA transfer to GDP for unique mRNA capping by vesicular stomatitis virus RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 107, 3463-3468
45. Huang, Y. L., Hsu, Y. H., Han, Y. T., and Meng, M. (2005) mRNA guanylation catalyzed by the S-adenosylmethionine-dependent guanylyltransferase of bamboo mosaic virus. J. Biol. Chem. 280, 13153-13162
46. Chakravarty, A. K., Subbotin, R., Chait, B. T., and Shuman, S. (2012) RNA ligase RtcB splices 3-phosphate and 5-OH ends via covalent RtcB-(histidinyl)- GMP and polynucleotide-(3)pp(5)G intermediates. Proc. Natl. Acad. Sci. U.S.A. 109, 6072-6077
47. Englert, M., Xia, S., Okada, C., Nakamura, A., Tanavde, V., Yao, M., Eom, S. H., Konigsberg, W. H., Söll, D., and Wang, J. (2012) Structural and mechanistic insights into guanylylation of RNA-splicing ligase RtcB joiningRNAbetween 3-terminal phosphate and 5-OH. Proc. Natl. Acad. Sci. U.S.A. 109, 15235-15240
48. Chakravarty, A. K., Smith, P., and Shuman, S. (2011) Structures of RNA 3-phosphate cyclase bound to ATP reveal the mechanism of nucleotidyl transfer and metal-assisted catalysis. Proc. Natl. Acad. Sci. U.S.A. 108, 21034-21039
49. Chakravarty, A. K., and Shuman, S. (2011) RNA 3-phosphate cyclase (RtcA) catalyzes ligase-like adenylylation of DNA and RNA 5-monophosphate ends. J. Biol. Chem. 286, 4117-4122