Structural determinants of an internal ribosome entry site that direct translational reading frame selection

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9366-9382

  Ren, Qian ^a   Au, Hilda H T ^a   Wang, Qing S ^a   Lee, Seonghoon ^a   Jan, Eric ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; GUANINE; URACIL;

AMINO ACID SUBSTITUTION; ANTICODON; ARTICLE; BASE PAIRING; CODING; CONTROLLED STUDY; INTERNAL RIBOSOME ENTRY SITE; MUTAGENESIS; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RNA CONFORMATION; RNA FINGERPRINTING; STRUCTURE ANALYSIS; TRANSLATION INITIATION; VIRUS GENOME;

BASE PAIRING; DICISTROVIRIDAE; HELA CELLS; HUMANS; MUTATION; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOMES; RNA, VIRAL;

EID: 84906266097     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku622     Document Type: Article

References (46)

1. Dinman, J.D. (2012) Control of gene expression by translational recoding. Adv. Protein Chem. Struct. Biol., 86, 129-149.
2. Firth, A.E. and Brierley, I. (2012) Non-canonical translation in RNA viruses. J. Gen. Virol., 93, 1385-1409.
3. Mohr, I., Pe'ery, T. and Mathews, M.B. (2007) In Mathews, MB, Sonenberg, N and Hershey, J (eds). Translational Control in Biology and Medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp.545.
4. Ren, Q., Wang, Q.S., Firth, A.E., Chan, M.M., Gouw, J.W., Guarna, M.M., Foster, L.J., Atkins, J.F. and Jan, E. (2012) Alternative reading frame selection mediated by a tRNA-like domain of an internal ribosome entry site. Proc. Natl. Acad. Sci. U.S.A., 109, E630-E639.
5. Bonning, B.C. and Miller, W.A. (2010) Dicistroviruses. Annu. Rev. Entomol., 55, 129-150.
6. Filbin, M.E. and Kieft, J.S. (2009) Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol., 19, 267-276.
7. Wilson, J.E., Powell, M.J., Hoover, S.E. and Sarnow, P. (2000) Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites. Mol. Cell. Biol., 20, 4990-4999.
8. Wilson, J.E., Pestova, T.V., Hellen, C.U. and Sarnow, P. (2000) Initiation of protein synthesis from the A site of the ribosome. Cell, 102, 511-520.
9. Jan, E. and Sarnow, P. (2002) Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol., 324, 889-902.
10. Nishiyama, T., Yamamoto, H., Shibuya, N., Hatakeyama, Y., Hachimori, A., Uchiumi, T. and Nakashima, N. (2003) Structural elements in the internal ribosome entry site of Plautia stali intestine virus responsible for binding with ribosomes. Nucleic Acids Res., 31, 2434-2442.
11. Costantino, D. and Kieft, J.S. (2005) A preformed compact ribosome-binding domain in the cricket paralysis-like virus IRES RNAs. RNA, 11, 332-343.
12. Pfingsten, J.S., Costantino, D.A. and Kieft, J.S. (2006) Structural basis for ribosome recruitment and manipulation by a viral IRES RNA. Science, 314, 1450-1454.
13. Costantino, D.A., Pfingsten, J.S., Rambo, R.P. and Kieft, J.S. (2008) tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat. Struct. Mol. Biol., 15, 57-64.
14. Schuler, M., Connell, S.R., Lescoute, A., Giesebrecht, J., Dabrowski, M., Schroeer, B., Mielke, T., Penczek, P.A., Westhof, E. and Spahn, C.M. (2006) Structure of the ribosome-bound cricket paralysis virus IRES RNA. Nat. Struct. Mol. Biol., 13, 1092-1096.
15. Fernandez, I.S., Bai, X.C., Murshudov, G., Scheres, S.H. and Ramakrishnan, V. (2014) Initiation of Translation by Cricket Paralysis Virus IRES Requires Its Translocation in the Ribosome. Cell.,157, 823-831
16. Jan, E., Kinzy, T.G. and Sarnow, P. (2003) Divergent tRNA-like element supports initiation, elongation, and termination of protein biosynthesis. Proc. Natl. Acad. Sci. U.S.A., 100, 15410-15415.
17. Pestova, T.V. and Hellen, C.U. (2003) Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev., 17, 181-186.
18. Firth, A.E., Wang, Q.S., Jan, E. and Atkins, J.F. (2009) Bioinformatic evidence for a stem-loop structure 5′-adjacent to the IGR-IRES and for an overlapping gene in the bee paralysis dicistroviruses. Virol. J., 6, 193-200.
19. Sabath, N., Price, N. and Graur, D. (2009) A potentially novel overlapping gene in the genomes of Israeli acute paralysis virus and its relatives. Virol. J., 6, 144-150.
20. Wang, Q.S., Au, H.H. and Jan, E. (2013) Methods for studying IRES-mediated translation of positive-strand RNA viruses. Methods, 59, 167-179.
21. Wilkinson, K.A., Merino, E.J. and Weeks, K.M. (2006) Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc., 1, 1610-1616.
22. Das, R., Laederach, A., Pearlman, S.M., Herschlag, D. and Altman, R.B. (2005) SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA, 11, 344-354.
23. McGinnis, J.L., Duncan, C.D. and Weeks, K.M. (2009) High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly. Methods Enzymol., 468, 67-89.
24. Au, H.H. and Jan, E. (2012) Insights into factorless translational initiation by the tRNA-like pseudoknot domain of a viral IRES. PLoS ONE, 7, e51477.
25. Dinman, J.D. (2012) Mechanisms and implications of programmed translational frameshifting. Wiley Interdiscip. Rev. RNA, 3, 661-673.
26. Schmeing, T.M., Voorhees, R.M., Kelley, A.C. and Ramakrishnan, V. (2011) How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat. Struct. Mol. Biol., 18, 432-436.
27. McGarry, K.G., Walker, S.E., Wang, H. and Fredrick, K. (2005) Destabilization of the P site codon-anticodon helix results from movement of tRNA into the P/E hybrid state within the ribosome. Mol. Cell, 20, 613-622.
28. Walker, S.E. and Fredrick, K. (2006) Recognition and positioning of mRNA in the ribosome by tRNAs with expanded anticodons. J. Mol. Biol., 360, 599-609.
29. Phelps, S.S., Gaudin, C., Yoshizawa, S., Benitez, C., Fourmy, D. and Joseph, S. (2006) Translocation of a tRNA with an extended anticodon through the ribosome. J. Mol. Biol., 360, 610-622.
30. Pfingsten, J.S., Costantino, D.A. and Kieft, J.S. (2007) Conservation and diversity among the three-dimensional folds of the Dicistroviridae intergenic region IRESes. J. Mol. Biol., 370, 856-869.
31. Hatakeyama, Y., Shibuya, N., Nishiyama, T. and Nakashima, N. (2004) Structural variant of the intergenic internal ribosome entry site elements in dicistroviruses and computational search for their counterparts. RNA, 10, 779-786.
32. Cevallos, R.C. and Sarnow, P. (2005) Factor-independent assembly of elongation-competent ribosomes by an internal ribosome entry site located in an RNA virus that infects penaeid shrimp. J. Virol., 79, 677-683.
33. Jang, C.J. and Jan, E. (2010) Modular domains of the Dicistroviridae intergenic internal ribosome entry site. RNA, 16, 1182-1195.
34. Hertz, M.I. and Thompson, S.R. (2011) In vivo functional analysis of the Dicistroviridae intergenic region internal ribosome entry sites. Nucleic Acids Res., 39, 7276-7288.
35. Jager, G., Nilsson, K. and Bjork, G.R. (2013) The phenotype of many independently isolated +1 frameshift suppressor mutants supports a pivotal role of the P-site in reading frame maintenance. PLoS ONE, 8, e60246.
36. Nasvall, S.J., Nilsson, K. and Bjork, G.R. (2009) The ribosomal grip of the peptidyl-tRNA is critical for reading frame maintenance. J. Mol. Biol., 385, 350-367.
37. Atkins, J.F. and Bjork, G.R. (2009) A gripping tale of ribosomal frameshifting: extragenic suppressors of frameshift mutations spotlight P-site realignment. Microbiol. Mol. Biol. Rev., 73, 178-210.
38. Baril, M. and Brakier-Gingras, L. (2005) Translation of the F protein of hepatitis C virus is initiated at a non-AUG codon in a +1 reading frame relative to the polyprotein. Nucleic Acids Res., 33, 1474-1486.
39. Xu, Z., Choi, J., Yen, T.S., Lu, W., Strohecker, A., Govindarajan, S., Chien, D., Selby, M.J. and Ou, J. (2001) Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J., 20, 3840-3848.
40. Varaklioti, A., Vassilaki, N., Georgopoulou, U. and Mavromara, P. (2002) Alternate translation occurs within the core coding region of the hepatitis C viral genome. J. Biol. Chem., 277, 17713-17721.
41. McMullan, L.K., Grakoui, A., Evans, M.J., Mihalik, K., Puig, M., Branch, A.D., Feinstone, S.M. and Rice, C.M. (2007) Evidence for a functional RNA element in the hepatitis C virus core gene. Proc. Natl. Acad. Sci. U.S.A., 104, 2879-2884.
42. Vassilaki, N., Friebe, P., Meuleman, P., Kallis, S., Kaul, A., Paranhos-Baccala, G., Leroux-Roels, G., Mavromara, P. and Bartenschlager, R. (2008) Role of the hepatitis C virus core+1 open reading frame and core cis-acting RNA elements in viral RNA translation and replication. J. Virol., 82, 11503-11515.
43. Kieft, J.S. (2008) Viral IRES RNA structures and ribosome interactions. Trends Biochem. Sci., 33, 274-283.
44. Qian, Q., Li, J.N., Zhao, H., Hagervall, T.G., Farabaugh, P.J. and Bjork, G.R. (1998) A new model for phenotypic suppression of frameshift mutations by mutant tRNAs. Mol. Cell, 1, 471-482.
45. Farabaugh, P.J., Zhao, H. and Vimaladithan, A. (1993) A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell, 74, 93-103.
46. Sundararajan, A., Michaud, W.A., Qian, Q., Stahl, G. and Farabaugh, P.J. (1999) Near-cognate peptidyl-tRNAs promote +1 programmed translational frameshifting in yeast. Mol. Cell, 4, 1005-1015.