The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA

Genes and Development

Volumn 23, Issue 3, 2009, Pages 331-334

  Luttermann, Christine ^a   Meyers, Gregor ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Mammalian mRNA translation; Reinitiation; Termination; Translation initiation; TURBS

Indexed keywords

CAPSID PROTEIN; MESSENGER RNA; RNA 18S; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BASE PAIRING; BINDING SITE; CALICIVIRUS; CELL STRAIN BHK; EUKARYOTE; MAMMAL CELL; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; RECOMBINANT PLASMID; RIBOSOME; RNA HYBRIDIZATION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; VACCINIA VIRUS; YEAST CELL;

ANIMALS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; CALICIVIRUS, FELINE; CAPSID PROTEINS; CELL LINE; CRICETINAE; GENES; GENETIC COMPLEMENTATION TEST; MODELS, GENETIC; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; RNA, MESSENGER; RNA, VIRAL; SACCHAROMYCES CEREVISIAE;

CALICIVIRIDAE; EUKARYOTA; MAMMALIA; MIRIDAE;

EID: 59949087959     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.507609     Document Type: Article

References (47)

1. Adhin, M.R. and van Duin, J. 1990. Scanning model for translational reinitiation in eubacteria. J. Mol. Biol. 213: 811-818.
2. Chappell, S.A., Dresios, J., Edelman, G.M., and Mauro, V.P. 2006. Ribosomal shunting mediated by a translational enhancer element that base pairs to 18S rRNA. Proc. Natl. Acad. Sci. 103: 9488-9493.
3. Chaudhry, Y., Nayak, A., Bordeleau, M.E., Tanaka, J., Pelletier, J., Belsham, G.J., Roberts, L.O., and Goodfellow, I.G. 2006. Caliciviruses differ in their functional requirements for eIF4F components. J. Biol. Chem. 281: 25315-25325.
4. Cuesta, R., Xi, Q., and Schneider, R.J. 2001. Preferential translation of adenovirus mRNAs in infected cells. Cold Spring Harb. Symp. Quant. Biol. 66: 259-267.
5. Daughenbaugh, K.F., Fraser, C.S., Hershey, J.W., and Hardy, M.E. 2003. The genome-linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J. 22: 2852-2859.
6. Devereux, J., Haeberli, P., and Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387-395.
7. Dresios, J., Chappell, S.A., Zhou, W., and Mauro, V.P. 2006. An mRNA-rRNA base-pairing mechanism for translation initiation in eukaryotes. Nat. Struct. Mol. Biol. 13: 30-34.
8. Goodfellow, I., Chaudhry, Y., Gioldasi, I., Gerondopoulos, A., Natoni, A., Labrie, L., Laliberte, J.F., and Roberts, L. 2005. Calicivirus translation initiation requires an interaction between VPg and eIF 4 E. EMBO Rep. 6: 968-972.
9. Gould, P.S. and Easton, A.J. 2005. Coupled translation of the respiratory syncytial virus M2 open reading frames requires upstream sequences. J. Biol. Chem. 280: 21972-21980.
10. Gould, P.S. and Easton, A.J. 2007. Coupled translation of the second open reading frame of M2 mRNA is sequence dependent and differs significantly within the subfamily Pneumovirinae. J. Virol. 81: 8488-8496.
11. Green, K.Y., Ando, T., Balayan, M.S., Berke, T., Clarke, I.N., Estes, M.K., Matson, D.O., Nakata, S., Neill, J.D., Studdert, M.J., et al. 2000. Family Caliciviridae.In Virus taxonomy (eds. M.H.V. Regenmortel, et al.), pp. 725-734. Academic Press, New York.
12. Hellen, C.U. and Sarnow, P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes & Dev. 15: 1593-1612.
13. Herbert, T.P., Brierley, I., and Brown, T.D. 1996. Detection of the ORF3 polypeptide of feline calicivirus in infected cells and evidence for its expression from a single, functionally bicistronic, subgenomic mRNA. J. Gen. Virol. 77: 123-127.
14. Horvath, C.M., Williams, M.A., and Lamb, R.A. 1990. Eukaryotic coupled translation of tandem cistrons: Identification of the influenza B virus BM2 polypeptide. EMBO J. 9: 2639-2647.
15. Jacob, W.F., Santer, M., and Dahlberg, A.E. 1987. A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins. Proc. Nat1. Acad. Sci. 84: 4757-4761.
16. Kapp, L.D. and Lorsch, J.R. 2004. The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73: 657-704.
17. Kozak, M. 1987. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell. Biol. 7: 3438-3445.
18. Kozak, M. 1989. The scanning model for translation: An update. J. Cell Biol. 108: 229-241.
19. Kozak, M. 2002. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299: 1-34.
20. Latorre, P., Kolakofsky, D., and Curran, J. 1998. Sendai virus Y proteins are initiated by a ribosomal shunt. Mol. Cell. Biol. 18: 5021-5031.
21. Luttermann, C. and Meyers, G. 2007. A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA. J. Biol. Chem. 282: 7056-7065.
22. McCormick, C.J., Salim, O., Lambden, P.R., and Clarke, I.N. 2008. Translation termination reinitiation between open reading frame 1 (ORF1) and ORF2 enables capsid expression in a bovine norovirus without the need for production of viral subgenomic RNA. J. Virol. 82: 8917-8921.
23. Meyers, G. 2003. Translation of the minor capsid protein of a calicivirus is initiated by a novel termination-dependent reinitiation mechanism. J. Biol. Chem. 278: 34051-34060.
24. Meyers, G. 2007. Characterization of the sequence element directing translation reinitiation in RNA of the calicivirus rabbit hemorrhagic disease virus. J. Virol. 81: 9623-9632.
25. Park, H.S., Himmelbach, A., Browning, K.S., Hohn, T., and Ryabova, L.A. 2001. A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 106: 723-733.
26. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I., and Hellen, C.U. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. 98: 7029-7036.
27. Pisarev, A.V., Hellen, C.U., and Pestova, T.V. 2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell 131: 286-299.
28. Pisarev, A.V., Kolupaeva, V.G., Yusupov, M.M., Hellen, C.U., and Pestova, T.V. 2008. Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes. EMBO J. 27: 1609-1621.
29. Pöyry, T.A., Kaminski, A., and Jackson, R.J. 2004. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes & Dev. 18: 62-75.
30. Pöyry, T.A., Kaminski, A., Connell, E.J., Fraser, C.S., and Jackson, R.J. 2007. The mechanism of an exceptional case of reinitiation after translation of a long ORF reveals why such events do not generally occur in mammalian mRNA translation. Genes & Dev. 21: 3149-3162.
31. Prasad, B.V., Matson, D.O., and Smith, A.W. 1994. Three-dimensional structure of calicivirus. J. Mol. Biol. 240: 256-264.
32. Rohayem, J., Robel, I., Jager, K., Scheffler, U., and Rudolph, W. 2006. Protein-primed and de novo initiation of RNA synthesis by norovirus 3Dpol. J. Virol. 80: 7060-7069.
33. Ryabova, L.A., Pooggin, M.M., and Hohn, T. 2002. Viral strategies of translation initiation: Ribosomal shunt and reinitiation. Prog. Nucleic Acid Res. Mol. Biol. 72: 1-39.
34. Ryabova, L.A., Pooggin, M.M., and Hohn, T. 2006. Translation reinitiation and leaky scanning in plant viruses. Virus Res. 119: 52-62.
35. Sachs, A.B., Sarnow, P., and Hentze, M.W. 1997. Starting at the beginning, middle, and end: Translation initiation in eukaryotes. Cell 89: 831-838.
36. Sarnow, P., Cevallos, R.C., and Jan, E. 2005. Takeover of host ribosomes by divergent IRES elements. Biochem. Soc. Trans. 33: 1479-1482.
37. Shine, J. and Dalgarno, L. 1975. Determinant of cistron specificity in bacterial ribosomes. Nature 254: 34-38.
38. Sonenberg, N. and Hinnebusch, A.G. 2007. New modes of translational control in development, behavior, and disease. Mol. Cell 28: 721-729.
39. Sosnovtsev, S.V., Sosnovtseva, S.A., and Green, K.Y. 1998. Cleavage of the feline calicivirus capsid precursor is mediated by a virus-encoded proteinase. J. Virol. 72: 3051-3059.
40. Sosnovtsev, S.V., Belliot, G., Chang, K.O., Onwudiwe, O., and Green, K.Y. 2005. Feline calicivirus VP2 is essential for the production of infectious virions. J. Virol. 79: 4012-4024.
41. Szamecz, B., Rutkai, E., Cuchalova, L., Munzarova, V., Herrmannova, A., Nielsen, K.H., Burela, L., Hinnebusch, A.G., and Valasek, L. 2008. eIF3a cooperates with sequences 5' of uORF1 to promote resumption of scanning by post-termination ribosomes for reinitiation on GCN4 mRNA. Genes & Dev. 22: 2414-2425.
42. Thumfart, J.O. and Meyers, G. 2002. Feline calicivirus: Recovery of wild-type and recombinant viruses after transfection of cRNA or cDNA constructs. J. Virol. 76: 6398-6407.
43. Tranque, P., Hu, M.C., Edelman, G.M., and Mauro, V.P. 1998. rRNA complementarity within mRNAs: A possible basis for mRNA-ribosome interactions and translational control. Proc. Natl. Acad. Sci. 95: 12238-12243.
44. Wai, H.H., Vu, L., Oakes, M., and Nomura, M. 2000. Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: Use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo. Nucleic Acids Res. 28: 3524-3534.
45. Wyatt, L.S., Moss, B., and Rozenblatt, S. 1995. Replication- deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells. Virology 210: 202-205.
46. Xi, Q., Cuesta, R., and Schneider, R.J. 2005. Regulation of translation by ribosome shunting through phosphotyrosine- dependent coupling of adenovirus protein 100k to viral mRNAs. J. Virol. 79: 5676-5683.
47. Yueh, A. and Schneider, R.J. 2000. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes & Dev. 14: 414-421.