tRNA–mRNA mimicry drives translation initiation from a viral IRES (original) (raw)

• Hershey, J.W.B. & Merrick, W.C. Pathway and mechanism of initiation of protein synthesis. In Translational Control of Gene Expression (eds. Sonenberg, N., Hershey, J.W.B. & Mathews, M.B.) 33–88 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 2000).
  Google Scholar
• Stoneley, M. & Willis, A.E. Cellular internal ribosome entry segments: structures, _trans_-acting factors and regulation of gene expression. Oncogene 23, 3200–3207 (2004).
  Article CAS PubMed Google Scholar
• Jackson, R.J. Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans. 33, 1231–1241 (2005).
  Article CAS PubMed Google Scholar
• Schuler, M. et al. Structure of the ribosome-bound cricket paralysis virus IRES RNA. Nat. Struct. Mol. Biol. 13, 1092–1096 (2006).
  Article PubMed Google Scholar
• Spahn, C.M. et al. Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes; the IRES functions as an RNA-based translation factor. Cell 118, 465–475 (2004).
  Article CAS PubMed Google Scholar
• Fukushi, S. et al. Ribosomal protein S5 interacts with the internal ribosomal entry site of hepatitis C virus. J. Biol. Chem. 276, 20824–20826 (2001).
  Article CAS PubMed Google Scholar
• Boehringer, D., Thermann, R., Ostareck-Lederer, A., Lewis, J.D. & Stark, H. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 13, 1695–1706 (2005).
  Article CAS PubMed Google Scholar
• Spahn, C.M. et al. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40S ribosomal subunit. Science 291, 1959–1962 (2001).
  Article CAS PubMed Google Scholar
• Jan, E. Divergent IRES elements in invertebrates. Virus Res. 119, 16–28 (2006).
  Article CAS PubMed Google Scholar
• Pfingsten, J.S., Costantino, D.A. & Kieft, J.S. Conservation and diversity among the three-dimensional folds of the Dicistroviridae intergenic region IRESes. J. Mol. Biol. 370, 856–869 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Costantino, D. & Kieft, J.S. A preformed compact ribosome-binding domain in the cricket paralysis-like virus IRES RNAs. RNA 11, 332–343 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Nishiyama, T. et al. Structural elements in the internal ribosome entry site of Plautia stali intestine virus responsible for binding with ribosomes. Nucleic Acids Res. 31, 2434–2442 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Jan, E. & Sarnow, P. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol. 324, 889–902 (2002).
  Article CAS PubMed Google Scholar
• Kanamori, Y. & Nakashima, N. A tertiary structure model of the internal ribosome entry site (IRES) for methionine-independent initiation of translation. RNA 7, 266–274 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Wilson, J.E., Pestova, T.V., Hellen, C.U. & Sarnow, P. Initiation of protein synthesis from the A site of the ribosome. Cell 102, 511–520 (2000).
  Article CAS PubMed Google Scholar
• Pestova, T.V. & Hellen, C.U. 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 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Sasaki, J. & Nakashima, N. Methionine-independent initiation of translation in the capsid protein of an insect RNA virus. Proc. Natl. Acad. Sci. USA 97, 1512–1515 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Sasaki, J. & Nakashima, N. Translation initiation at the CUU codon is mediated by the internal ribosome entry site of an insect picorna-like virus in vitro. J. Virol. 73, 1219–1226 (1999).
  CAS PubMed PubMed Central Google Scholar
• Jan, E. et al. Initiator Met-tRNA-independent translation mediated by an internal ribosome entry site element in cricket paralysis virus-like insect viruses. Cold Spring Harb. Symp. Quant. Biol. 66, 285–292 (2001).
  Article CAS PubMed Google Scholar
• Thompson, S.R., Gulyas, K.D. & Sarnow, P. Internal initiation in Saccharomyces cerevisiae mediated by an initiator tRNA/eIF2-independent internal ribosome entry site element. Proc. Natl. Acad. Sci. USA 98, 12972–12977 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Wilson, J.E., Powell, M.J., Hoover, S.E. & Sarnow, P. Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites. Mol. Cell. Biol. 20, 4990–4999 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Jan, E., Kinzy, T.G. & Sarnow, P. Divergent tRNA-like element supports initiation, elongation, and termination of protein biosynthesis. Proc. Natl. Acad. Sci. USA 100, 15410–15415 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Pfingsten, J.S., Costantino, D.A. & Kieft, J.S. Structural basis for ribosome recruitment and manipulation by a viral IRES RNA. Science 314, 1450–1454 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Keel, A.Y., Rambo, R.P., Batey, R.T. & Kieft, J.S. A general strategy to solve the phase problem in RNA crystallography. Structure 15, 761–772 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hilbers, C.W., Michiels, P.J. & Heus, H.A. New developments in structure determination of pseudoknots. Biopolymers 48, 137–153 (1998).
  Article CAS PubMed Google Scholar
• Selmer, M. et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935–1942 (2006).
  Article CAS PubMed Google Scholar
• Cabello-Villegas, J., Tworowska, I. & Nikonowicz, E.P. Metal ion stabilization of the U-turn of the A37 N6-dimethylallyl-modified anticodon stem-loop of Escherichia coli tRNAPhe. Biochemistry 43, 55–66 (2004).
  Article CAS PubMed Google Scholar
• Honda, M., Brown, E.A. & Lemon, S.M. Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 2, 955–968 (1996).
  CAS PubMed PubMed Central Google Scholar
• Merino, E.J., Wilkinson, K.A., Coughlan, J.L. & Weeks, K.M. RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127, 4223–4231 (2005).
  Article CAS PubMed Google Scholar
• Wilkinson, K.A., Merino, E.J. & Weeks, K.M. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc. 1, 1610–1616 (2006).
  Article CAS PubMed Google Scholar
• McGarry, K.G., Walker, S.E., Wang, H. & Fredrick, K. 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 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Moazed, D. & Noller, H.F. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342, 142–148 (1989).
  Article CAS PubMed Google Scholar
• Bretscher, M.S. Translocation in protein synthesis: a hybrid structure model. Nature 218, 675–677 (1968).
  Article CAS PubMed Google Scholar
• Yamamoto, H., Nakashima, N., Ikeda, Y. & Uchiumi, T. Binding mode of the first aminoacyl-tRNA in translation initiation mediated by Plautia stali intestine virus internal ribosome entry site. J. Biol. Chem. 282, 7770–7776 (2007).
  Article CAS PubMed Google Scholar
• Blanchard, S.C., Kim, H.D., Gonzalez, R.L., Jr., Puglisi, J.D. & Chu, S. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA 101, 12893–12898 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Munro, J.B., Altman, R.B., O'Connor, N. & Blanchard, S.C. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25, 505–517 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Allen, G.S., Zavialov, A., Gursky, R., Ehrenberg, M. & Frank, J. The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121, 703–712 (2005).
  Article CAS PubMed Google Scholar
• Dorner, S., Brunelle, J.L., Sharma, D. & Green, R. The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nat. Struct. Mol. Biol. 13, 234–241 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Olejniczak, M., Dale, T., Fahlman, R.P. & Uhlenbeck, O.C. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat. Struct. Mol. Biol. 12, 788–793 (2005).
  Article CAS PubMed Google Scholar
• Noller, H.F., Hoang, L. & Fredrick, K. The 30S ribosomal P site: a function of 16S rRNA. FEBS Lett. 579, 855–858 (2005).
  Article CAS PubMed Google Scholar
• Spahn, C.M. et al. Structure of the 80S ribosome from _Saccharomyces cerevisiae_–tRNA-ribosome and subunit-subunit interactions. Cell 107, 373–386 (2001).
  Article CAS PubMed Google Scholar
• Berk, V., Zhang, W., Pai, R.D. & Cate, J.H. Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl. Acad. Sci. USA 103, 15830–15834 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Valle, M. et al. Locking and unlocking of ribosomal motions. Cell 114, 123–134 (2003).
  Article CAS PubMed Google Scholar
• Sharma, D., Southworth, D.R. & Green, R. EF-G-independent reactivity of a pre-translocation-state ribosome complex with the aminoacyl tRNA substrate puromycin supports an intermediate (hybrid) state of tRNA binding. RNA 10, 102–113 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Kristensen, O., Laurberg, M., Liljas, A. & Selmer, M. Is tRNA binding or tRNA mimicry mandatory for translation factors? Curr. Protein Pept. Sci. 3, 133–141 (2002).
  Article CAS PubMed Google Scholar
• Fechter, P., Rudinger-Thirion, J., Florentz, C. & Giege, R. Novel features in the tRNA-like world of plant viral RNAs. Cell. Mol. Life Sci. 58, 1547–1561 (2001).
  Article CAS PubMed Google Scholar
• Moore, S.D. & Sauer, R.T. The tmRNA system for translational surveillance and ribosome rescue. Annu. Rev. Biochem. 76, 101–124 (2007).
  Article CAS PubMed Google Scholar
• Bessho, Y. et al. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc. Natl. Acad. Sci. USA 104, 8293–8298 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
  Article CAS PubMed Google Scholar
• Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948–1954 (2002).
  Article PubMed Google Scholar
• Adams, P.D. et al. Recent developments in the PHENIX software for automated crystallographic structure determination. J. Synchrotron Radiat. 11, 53–55 (2004).
  Article CAS PubMed Google Scholar
• Holton, J. & Alber, T. Automated protein crystal structure determination using ELVES. Proc. Natl. Acad. Sci. USA 101, 1537–1542 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Leslie, A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newslett. Protein Crystallogr No. 26 (1992).
• Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760–763 (1994).
• Terwilliger, T. SOLVE and RESOLVE: automated structure solution, density modification and model building. J. Synchrotron Radiat. 11, 49–52 (2004).
  Article CAS PubMed Google Scholar
• Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A Foundations Crystallogr. 47, 110–119 (1991).
  Article Google Scholar
• Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921 (1998).
  Article CAS PubMed Google Scholar
• Kieft, J.S., Zhou, K., Jubin, R. & Doudna, J.A. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 7, 194–206 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Das, R., Laederach, A., Pearlman, S.M., Herschlag, D. & Altman, R.B. SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA 11, 344–354 (2005).
  Article CAS PubMed PubMed Central Google Scholar