Mechanism of initiation site selection promoted by the human rhinovirus 2 internal ribosome entry site

Journal of Virology

Volumn 84, Issue 13, 2010, Pages 6578-6589

  Kaminski, Ann ^a   Pöyry, Tuija A A ^a   Skene, Peter J ^a   Jackson, Richard J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; MESSENGER RNA; NUCLEOTIDE; OLIGODEOXYNUCLEOTIDE; RIBONUCLEASE H;

ARTICLE; BASE PAIRING; HUMAN; HUMAN CELL; HUMAN RHINOVIRUS; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RETICULOCYTE LYSATE; TRANSLATION INITIATION;

CELL EXTRACTS; CODON, INITIATOR; EPITHELIAL CELLS; HELA CELLS; HUMANS; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POINT MUTATION; RETICULOCYTES; RHINOVIRUS; RIBOSOMES; RNA, VIRAL; VIRUS REPLICATION;

HUMAN RHINOVIRUS 2;

EID: 77953306212     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00123-10     Document Type: Article

References (50)

1. Alexander, L., H. H. Lu, and E. Wimmer. 1994. Polioviruses containing picornavirus type 1 and/or type 2 internal ribosomal entry site elements: genetic hybrids and the expression of a foreign gene. Proc. Natl. Acad. Sci. U. S. A. 91:1406-1410.
2. Ali, I. K., L. McKendrick, S. J. Morley, and R. J. Jackson. 2001. Truncated initiation factor eIF4G lacking an eIF4E binding site can support capped mRNA translation. EMBO J. 20:4233-4242.
3. Belsham, G. J. 1992. Dual initiation sites of protein synthesis on foot-and-mouth disease virus RNA are selected following internal entry and scanning of ribosomes in vivo. EMBO J. 11:1105-1110.
4. Borman, A., M. T. Howell, J. G. Patton, and R. J. Jackson. 1993. The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J. Gen. Virol. 74:1775-1788.
5. Borman, A., and R. J. Jackson. 1992. Initiation of translation of human rhinovirus RNA: Mapping the internal ribosome entry site. Virology 188:685-696.
6. Dasso, M. C., and R. J. Jackson. 1989. On the fidelity of mRNA translation in the nuclease-treated rabbit reticulocyte lysate system. Nucleic Acids Res. 17:3129-3144.
7. Gold, L. 1988. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu. Rev. Biochem. 57:199-233.
8. Hellen, C. U. T., T. V. Pestova, and E. Wimmer. 1994. Effect of mutations downstream of the internal ribosome entry site on initiation of poliovirus protein synthesis. J. Virol. 68:6312-6322.
9. Hemmings-Mieszczak, M., and T. Hohn. 1999. A stable hairpin preceded by a short open reading frame promotes nonlinear ribosome migration on a synthetic mRNA leader. RNA 5:1149-1157.
10. Hohn, T., S. Corsten, D. Dominguez, J. Fütterer, D. Kirk, M. Hemmings-Mieszczak, M. Pooggin, N. Schärer-Hernandez, and L. Ryabova. 2001. Shunting is a translation strategy used by plant pararetroviruses (Caulimoviridae). Micron 32:51-57.
11. Hunt, S. L., J. J. Hsuan, N. Totty, and R. J. Jackson. 1999. Unr, a cellular cytoplasmic RNA-binding protein with five cold shock domains, is required for internal initiation of translation of human rhinovirus RNA. Genes Dev. 13:437-448.
12. Hunt, S. L., and R. J. Jackson. 1999. Polypyrimidine-tract binding protein (PTB) is necessary, but not sufficient, for efficient internal initiation of translation of human rhinovirus-2 RNA. RNA 5:344-359.
13. Iizuka, N., M. Kohara, K. Hagino-Yamagishi, S. Abe, T. Komatsu, K. Tago, M. Arita, and A. Nomoto. 1989. Construction of less neurovirulent polioviruses by introducing deletions into the 5′ noncoding sequence of the genome. J. Virol. 63:5354-5363.
14. Ingolia, N. T., S. Ghaemmaghami, J. R. S. Newman, and J. J. Weissman. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218-223.
15. Jackson, R. J., C. U. T. Hellen, and T. V. Pestova. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell. Biol. 10:113-127.
16. Jackson, R. J., and T. Hunt. 1983. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol. 96:50-74.
17. Jackson, R. J., and A. Kaminski. 1995. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1:985-1000.
18. Kaminski, A., G. J. Belsham, and R. J. Jackson. 1994. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J. 13:1673-1681. (Pubitemid 24114719)
19. Kaminski, A., M. T. Howell, and R. J. Jackson. 1990. Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO J. 9:3753-3759. (Pubitemid 20337408)
20. Kozak, M. 1977. Nucleotide sequences of 5′-terminal ribosome-protected initiation regions from two reovirus messages. Nature 269:391-394.
21. Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283-292. (Pubitemid 16048214)
22. Kozak, M. 1991. A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr. 1:111-115.
23. Kozak, M., and A. Shatkin. 1976. Characterization of ribosome-protected fragments from reovirus messenger RNA. J. Biol. Chem. 251:4259-4266.
24. Kozak, M., and A. Shatkin. 1978. Migration of 40S ribosomal subunits on messenger RNA in the presence of edeine. J. Biol. Chem. 253:6568-6577.
25. Kuge, S., N. Kawamura, and A. Nomoto. 1989. Genetic variation occurring on the genome of an in vitro insertion mutant of poliovirus type 1. J. Virol. 63:1069-1075. (Pubitemid 19061346)
26. Kuge, S., N. Kawamura, and A. Nomoto. 1989. Strong inclination towards transition mutation in nucleotide substitutions by poliovirus replicase. J. Mol. Biol. 207:175-182.
27. Kuge, S., and A. Nomoto. 1987. Construction of viable deletion and insertion mutants of the Sabin strain of type 1 poliovirus: function of the 5′ noncoding sequence in viral replication. J. Virol. 61:1478-1487. (Pubitemid 17069737)
28. Lazarowitz, S. G., and H. D. Robertson. 1977. Initiator regions from the small size class of reovirus messenger RNA protected by rabbit reticulocyte ribosomes. J. Biol. Chem. 252:7842-7849.
29. 125Ilabelled rabbit globin messenger RNA. J. Mol. Biol. 106:37-53.
30. Legon, S., P. Model, and H. D. Robertson. 1977. Interaction of rabbit reticulocyte ribosomes with bacteriophage f1 mRNA and of Escherichia coli ribosomes with rabbit globin mRNA. Proc. Natl. Acad. Sci. U. S. A. 74:2692-2696.
31. Lomakin, I. V., C. U. T. Hellen, and T. V. Pestova. 2000. Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus is required for internal initiation of translation. Mol. Cell. Biol. 20:6019-6029.
32. Meerovitch, K., R. Nicholson, and N. Sonenberg. 1991. In vitro mutational analysis of cis-acting RNA translational elements within the poliovirus type 2 5′ untranslated region. J. Virol. 65:5895-5901.
33. Nicholson, R., J. Pelletier, S.-Y. Le, and N. Sonenberg. 1991. Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies. J. Virol. 65:5886-5894.
34. Nivinskas, R., N. Malys, V. Klausa, R. Vaiskunaite, and E. Gineikiene. 1999. Post-transcriptional control of bacteriophage T4 gene 25 expression: mRNA secondary structure that enhances translational initiation. J. Mol. Biol. 288:291-304.
35. Palmenberg, A. C., D. Spiro, R. Kuzmickas, S. Wang, A. Djikeng, J. A. Rathe, C. M. Frase-Liggett, and S. B. Liggett. 2009. Sequencing and analysis of all known human rhinovirus genomes reveal structure and evolution. Science 324:55-59.
36. Pause, A., N. Méthot, Y. Svitkin, W. C. Merrick, and N. Sonenberg. 1994. Dominant negative mutants of mammalian translation initiation factor eIF4A define a critical role for eIF4F in cap-dependent and cap-independent initiation of translation. EMBO J. 13:1205-1215. (Pubitemid 24074727)
37. Pelletier, J., M. E. Flynn, G. Kaplan, V. Racaniello, and N. Sonenberg. 1988. Mutational analysis of upstream AUG codons of poliovirus RNA. J. Virol. 62:4486-4492. (Pubitemid 19006109)
38. Pestova, T. V., S. I. Borukhov, and C. U. T. Hellen. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394:854-859.
39. Pestova, T. V., C. U. T. Hellen, and E. Wimmer. 1994. A conserved AUG triplet in the 5′ nontranslated region of poliovirus can function as an initiation codon in vitro and in vivo. Virology 204:729-737.
40. Pestova, T. V., and V. Kolupaeva. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16:2906-2922.
41. Pestova, T. V., I. N. Shatsky, S. P. Fletcher, R. J. Jackson, and C. U. T. Hellen. 1998. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 12:67-83. (Pubitemid 28083659)
42. Pilipenko, E. V., A. P. Gmyl, S. V. Maslova, Y. V. Svitkin, A. N. Sinyakov, and V. I. Agol. 1992. Prokaryotic-like cis elements in the cap-independent internal initiation of translation on picornavirus RNA. Cell 68:119-131.
43. Pisarev, A. V., C. U. T. Hellen, and T. V. Pestova. 2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell 131:286-299.
44. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Sangar, D. V., S. E. Newton, D. J. Rowlands, and B. E. Clarke. 1987. All foot and mouth disease virus serotypes initiate protein synthesis at two separate AUGs. Nucleic Acids Res. 15:3305-3315.
46. Siridechadilok, B., C. S. Fraser, R. J. Hall, J. A. Doudna, and E. Nogales. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310:1513-1515.
47. Unbehaun, A., S. I. Borukhov, C. U. T. Hellen, and T. V. Pestova. 2004. Release of initiation factors from 48S complexes during ribosomal subunit joining and the link between establishment of codon-anticodon base-pairing and hydrolysis of eIF2-bound GTP. Genes Dev. 18:3078-3093.
48. Wolin, S. L., and P. Walter. 1988. Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J. 7:3559-3569.
49. Yueh, A., and R. J. Schneider. 1996. Selective translation initiation by ribosome jumping in adenovirus-infected and heat-shocked cells. Genes Dev. 10:1557-1567. (Pubitemid 26262062)
50. Yueh, A., and R. J. Schneider. 2000. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes Dev. 14:414-421. (Pubitemid 30131887)