Accuracy mechanism of eukaryotic ribosome translocation

  • 1.

    Ortiz, P. A., Ulloque, R., Kihara, G. K., Zheng, H. & Kinzy, T. G. Translation elongation factor 2 anticodon mimicry domain mutants affect fidelity and diphtheria toxin resistance. J. Biol. Chem. 281, 32639–32648 (2006).

    CAS 
    Article 

    Google Scholar 

  • 2.

    Waas, W. F., Druzina, Z., Hanan, M. & Schimmel, P. Role of a tRNA base modification and its precursors in frameshifting in eukaryotes. J. Biol. Chem. 282, 26026–26034 (2007).

    CAS 
    Article 

    Google Scholar 

  • 3.

    Noller, H. F., Lancaster, L., Mohan, S. & Zhou, J. Ribosome structural dynamics in translocation: yet another functional role for ribosomal RNA. Q. Rev. Biophys. 50, e12 (2017).

    Article 

    Google Scholar 

  • 4.

    Murray, J. et al. Structural characterization of ribosome recruitment and translocation by type IV IRES. Elife 5, e13567 (2016).

  • 5.

    Jørgensen, R., Merrill, A. R. & Andersen, G. R. The life and death of translation elongation factor 2. Biochem. Soc. Trans. 34, 1–6 (2006).

    Article 

    Google Scholar 

  • 6.

    Flis, J. et al. tRNA translocation by the eukaryotic 80S ribosome and the impact of GTP hydrolysis. Cell Rep. 25, 2676–2688.e7 (2018).

    CAS 
    Article 

    Google Scholar 

  • 7.

    Pellegrino, S. et al. Structural insights into the role of diphthamide on elongation factor 2 in mRNA reading-frame maintenance. J. Mol. Biol. 430, 2677–2687 (2018).

    CAS 
    Article 

    Google Scholar 

  • 8.

    Spahn, C. M. et al. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 23, 1008–1019 (2004).

    CAS 
    Article 

    Google Scholar 

  • 9.

    Taylor, D. J. et al. Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. EMBO J. 26, 2421–2431 (2007).

    CAS 
    Article 

    Google Scholar 

  • 10.

    Voorhees, R. M., Fernández, I. S., Scheres, S. H. W. & Hegde, R. S. Structure of the mammalian ribosome–Sec61 complex to 3.4 Å resolution. Cell 157, 1632–1643 (2014).

    CAS 
    Article 

    Google Scholar 

  • 11.

    Bhatt, P. R. et al. Structural basis of ribosomal frameshifting during translation of the SARS-CoV-2 RNA genome. Science 372, 1306–1313 (2021).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 12.

    Gavrilova, L. P., Koteliansky, V. E. & Spirin, A. S. Ribosomal protein S12 and ‘non-enzymatic’ translocation. FEBS Lett. 45, 324–328 (1974).

    CAS 
    Article 

    Google Scholar 

  • 13.

    Ogle, J. M. et al. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897–902 (2001).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 14.

    Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. A new understanding of the decoding principle on the ribosome. Nature 484, 256–259 (2012).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 15.

    Liu, S. et al. Diphthamide modification on eukaryotic elongation factor 2 is needed to assure fidelity of mRNA translation and mouse development. Proc. Natl Acad. Sci. USA 109, 13817–13822 (2012).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 16.

    Ulyanov, N. B. & James, T. L. RNA structural motifs that entail hydrogen bonds involving sugar-phosphate backbone atoms of RNA. New J. Chem. 34, 910–917 (2010).

    CAS 
    Article 

    Google Scholar 

  • 17.

    Khade, P. K. & Joseph, S. Messenger RNA interactions in the decoding center control the rate of translocation. Nat. Struct. Mol. Biol. 18, 1300–1302 (2011).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Prokhorova, I. et al. Aminoglycoside interactions and impacts on the eukaryotic ribosome. Proc. Natl Acad. Sci. USA 114, E10899–E10908 (2017).

    CAS 
    Article 

    Google Scholar 

  • 19.

    Stanley, R. E., Blaha, G., Grodzicki, R. L., Strickler, M. D. & Steitz, T. A. The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70S ribosome. Nat. Struct. Mol. Biol. 17, 289–293 (2010).

    CAS 
    Article 

    Google Scholar 

  • 20.

    Peske, F., Savelsbergh, A., Katunin, V. I., Rodnina, M. V. & Wintermeyer, W. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J. Mol. Biol. 343, 1183–1194 (2004).

    CAS 
    Article 

    Google Scholar 

  • 21.

    Rosselló-Tortella, M. et al. Epigenetic loss of the transfer RNA-modifying enzyme TYW2 induces ribosome frameshifts in colon cancer. Proc. Natl Acad. Sci. USA 117, 20785–20793 (2020).

    Article 

    Google Scholar 

  • 22.

    Carlson, B. A. et al. Transfer RNA modification status influences retroviral ribosomal frameshifting. Virology 255, 2–8 (1999).

    CAS 
    Article 

    Google Scholar 

  • 23.

    Moazed, D. & Noller, H. F. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342, 142–148 (1989).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 24.

    Cornish, P. V., Ermolenko, D. N., Noller, H. F. & Ha, T. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30, 578–588 (2008).

    CAS 
    Article 

    Google Scholar 

  • 25.

    Salsi, E., Farah, E. & Ermolenko, D. N. EF-G activation by phosphate analogs. J. Mol. Biol. 428, 2248–2258 (2016).

    CAS 
    Article 

    Google Scholar 

  • 26.

    Susorov, D. et al. Eukaryotic translation elongation factor 2 (eEF2) catalyzes reverse translocation of the eukaryotic ribosome. J. Biol. Chem. 293, 5220–5229 (2018).

    CAS 
    Article 

    Google Scholar 

  • 27.

    Chen, C. et al. Elongation factor G initiates translocation through a power stroke. Proc. Natl Acad. Sci. USA 113, 7515–7520 (2016).

    CAS 
    Article 

    Google Scholar 

  • 28.

    Belardinelli, R. et al. Choreography of molecular movements during ribosome progression along mRNA. Nat. Struct. Mol. Biol. 23, 342–348 (2016).

    CAS 
    Article 

    Google Scholar 

  • 29.

    Ben-Shem, A., Jenner, L., Yusupova, G. & Yusupov, M. Crystal structure of the eukaryotic ribosome. Science 330, 1203–1209 (2010).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 30.

    Jørgensen, R., Carr-Schmid, A., Ortiz, P. A., Kinzy, T. G. & Andersen, G. R. Purification and crystallization of the yeast elongation factor eEF2. Acta Crystallogr. D Biol. Crystallogr. 58, 712–715 (2002).

    Article 

    Google Scholar 

  • 31.

    Spirin, A. S., Belitsina, N. V. & Yusupova, G. Z. Ribosomal synthesis of polypeptides from aminoacyl-tRNA without polynucleotide template. Methods Enzymol. 164, 631–649 (1988).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Mesters, J. R., Vorstenbosch, E. L. H., de Boer, A. J. & Kraal, B. Complete purification of tRNA, charged or modified with hydrophobic groups, by reversed-phase high-performance liquid chromatography on a C4/C18 column system. J. Chromatogr. A 679, 93–98 (1994).

    CAS 
    Article 

    Google Scholar 

  • 33.

    Mechulam, Y., Guillon, L., Yatime, L., Blanquet, S. & Schmitt, E. Protection-based assays to measure aminoacyl-tRNA binding to translation initiation factors. Methods Enzymol. 430, 265–281 (2007).

    CAS 
    Article 

    Google Scholar 

  • 34.

    Wojdyla, J. A. et al. DA+ data acquisition and analysis software at the Swiss Light Source macromolecular crystallography beamlines. J. Synchrotron Radiat. 25, 293–303 (2018).

    CAS 
    Article 

    Google Scholar 

  • 35.

    Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795–800 (1993).

    CAS 
    Article 

    Google Scholar 

  • 36.

    Afonine, P. V. et al. FEM: feature-enhanced map. Acta Crystallogr. D Biol. Crystallogr. 71, 646–666 (2015).

    CAS 
    Article 

    Google Scholar 

  • 37.

    Zhou, J., Lancaster, L., Donohue, J. P. & Noller, H. F. Spontaneous ribosomal translocation of mRNA and tRNAs into a chimeric hybrid state. Proc. Natl Acad. Sci. USA 116, 7813–7818 (2019).

    CAS 
    Article 

    Google Scholar 

  • Leave a Reply

    Your email address will not be published. Required fields are marked *