The many faces of ribosome translocation along the mRNA: reading frame maintenance, ribosome frameshifting and translational bypassing.
mRNA
recoding
ribosome
tRNA
translation fidelity
translocation
Journal
Biological chemistry
ISSN: 1437-4315
Titre abrégé: Biol Chem
Pays: Germany
ID NLM: 9700112
Informations de publication
Date de publication:
26 07 2023
26 07 2023
Historique:
received:
21
02
2023
accepted:
22
03
2023
medline:
8
9
2023
pubmed:
20
4
2023
entrez:
20
04
2023
Statut:
epublish
Résumé
In each round of translation elongation, the ribosome translocates along the mRNA by precisely one codon. Translocation is promoted by elongation factor G (EF-G) in bacteria (eEF2 in eukaryotes) and entails a number of precisely-timed large-scale structural rearrangements. As a rule, the movements of the ribosome, tRNAs, mRNA and EF-G are orchestrated to maintain the exact codon-wise step size. However, signals in the mRNA, as well as environmental cues, can change the timing and dynamics of the key rearrangements leading to recoding of the mRNA into production of trans-frame peptides from the same mRNA. In this review, we discuss recent advances on the mechanics of translocation and reading frame maintenance. Furthermore, we describe the mechanisms and biological relevance of non-canonical translocation pathways, such as hungry and programmed frameshifting and translational bypassing, and their link to disease and infection.
Identifiants
pubmed: 37077160
pii: hsz-2023-0142
doi: 10.1515/hsz-2023-0142
doi:
Substances chimiques
RNA, Messenger
0
Peptide Elongation Factor G
0
Codon
0
RNA, Transfer
9014-25-9
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
755-767Informations de copyright
© 2023 the author(s), published by De Gruyter, Berlin/Boston.
Références
Adio, S., Senyushkina, T., Peske, F., Fischer, N., Wintermeyer, W., and Rodnina, M.V. (2015). Fluctuations between multiple EF-G-induced chimeric tRNA states during translocation on the ribosome. Nat. Commun. 6: 7442. https://doi.org/10.1038/ncomms8442 .
doi: 10.1038/ncomms8442
Agirrezabala, X., Lei, J., Brunelle, J.L., Ortiz-Meoz, R.F., Green, R., and Frank, J. (2008). Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 32: 190–197, https://doi.org/10.1016/j.molcel.2008.10.001 .
doi: 10.1016/j.molcel.2008.10.001
Agirrezabala, X., Samatova, E., Klimova, M., Zamora, M., Gil-Carton, D., Rodnina, M.V., and Valle, M. (2017). Ribosome rearrangements at the onset of translational bypassing. Sci. Adv. 3: e1700147, https://doi.org/10.1126/sciadv.1700147 .
doi: 10.1126/sciadv.1700147
Altuntop, M.E., Ly, C.T., and Wang, Y. (2010). Single-molecule study of ribosome hierarchic dynamics at the peptidyl transferase center. Biophys. J. 99: 3002–3009, https://doi.org/10.1016/j.bpj.2010.08.037 .
doi: 10.1016/j.bpj.2010.08.037
Anokhina, V.S. and Miller, B.L. (2021). Targeting ribosomal frameshifting as an antiviral strategy: from HIV-1 to SARS-CoV-2. Acc. Chem. Res. 54: 3349–3361, https://doi.org/10.1021/acs.accounts.1c00316 .
doi: 10.1021/acs.accounts.1c00316
Atkins, J.F., O’Connor, K.M., Bhatt, P.R., and Loughran, G. (2021). From recoding to peptides for MHC class I immune display: enriching viral expression, virus vulnerability and virus evasion. Viruses 13: 1–29, https://doi.org/10.3390/v13071251 .
doi: 10.3390/v13071251
Ayhan, F., Perez, B.A., Shorrock, H.K., Zu, T., Banez-Coronel, M., Reid, T., Furuya, H., Clark, H.B., Troncoso, J.C., Ross, C.A., et al.. (2018). SCA8 RAN polySer protein preferentially accumulates in white matter regions and is regulated by eIF3F. EMBO J. 37: 1–15, https://doi.org/10.15252/embj.201899023 .
doi: 10.15252/embj.201899023
Bao, C., Zhu, M., Nykonchuk, I., Wakabayashi, H., Mathews, D.H., and Ermolenko, D.N. (2022). Specific length and structure rather than high thermodynamic stability enable regulatory mRNA stem-loops to pause translation. Nat. Commun. 13: 988, https://doi.org/10.1038/s41467-022-28600-5 .
doi: 10.1038/s41467-022-28600-5
Baranov, P.V., Gesteland, R.F., and Atkins, J.F. (2002). Release factor 2 frameshifting sites in different bacteria. EMBO Rep. 3: 373–377, https://doi.org/10.1093/embo-reports/kvf065 .
doi: 10.1093/embo-reports/kvf065
Bartok, O., Pataskar, A., Nagel, R., Laos, M., Goldfarb, E., Hayoun, D., Levy, R., Korner, P.R., Kreuger, I.Z.M., Champagne, J., et al.. (2021). Anti-tumour immunity induces aberrant peptide presentation in melanoma. Nature 590: 332–337, https://doi.org/10.1038/s41586-020-03054-1 .
doi: 10.1038/s41586-020-03054-1
Belardinelli, R., Sharma, H., Caliskan, N., Cunha, C.E., Peske, F., Wintermeyer, W., and Rodnina, M.V. (2016). Choreography of molecular movements during ribosome progression along mRNA. Nat. Struct. Mol. Biol. 23: 342–348, https://doi.org/10.1038/nsmb.3193 .
doi: 10.1038/nsmb.3193
Belardinelli, R., Sharma, H., Peske, F., and Rodnina, M.V. (2021). Perturbation of ribosomal subunit dynamics by inhibitors of tRNA translocation. RNA 27: 981–990, https://doi.org/10.1261/rna.078758.121 .
doi: 10.1261/rna.078758.121
Belew, A.T., Hepler, N.L., Jacobs, J.L., and Dinman, J.D. (2008). PRFdb: a database of computationally predicted eukaryotic programmed -1 ribosomal frameshift signals. BMC Genom. 9: 339, https://doi.org/10.1186/1471-2164-9-339 .
doi: 10.1186/1471-2164-9-339
Bhatt, P.R., Scaiola, A., Loughran, G., Leibundgut, M., Kratzel, A., Meurs, R., Dreos, R., O’Connor, K.M., McMillan, A., Bode, J.W., et al.. (2021). Structural basis of ribosomal frameshifting during translation of the SARS-CoV-2 RNA genome. Science 372: 1306–1313, https://doi.org/10.1126/science.abf3546 .
doi: 10.1126/science.abf3546
Blanchard, S.C., Kim, H.D., Gonzalez, R.L., Puglisi, J.D., and Chu, S. (2004). tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA. 101: 12893–12898, https://doi.org/10.1073/pnas.0403884101 .
doi: 10.1073/pnas.0403884101
Blinkowa, A.L. and Walker, J.R. (1990). Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res. 18: 1725–1729, https://doi.org/10.1093/nar/18.7.1725 .
doi: 10.1093/nar/18.7.1725
Bock, L.V., Blau, C., Schroder, G.F., Davydov, I.I., Fischer, N., Stark, H., Rodnina, M.V., Vaiana, A.C., and Grubmuller, H. (2013). Energy barriers and driving forces in tRNA translocation through the ribosome. Nat. Struct. Mol. Biol. 20: 1390–1396, https://doi.org/10.1038/nsmb.2690 .
doi: 10.1038/nsmb.2690
Bock, L.V., Caliskan, N., Korniy, N., Peske, F., Rodnina, M.V., and Grubmuller, H. (2019). Thermodynamic control of -1 programmed ribosomal frameshifting. Nat. Commun. 10: 4598, https://doi.org/10.1038/s41467-019-12648-x .
doi: 10.1038/s41467-019-12648-x
Brilot, A.F., Korostelev, A.A., Ermolenko, D.N., and Grigorieff, N. (2013). Structure of the ribosome with elongation factor G trapped in the pretranslocation state. Proc. Natl. Acad. Sci. USA. 110: 20994–20999, https://doi.org/10.1073/pnas.1311423110 .
doi: 10.1073/pnas.1311423110
Caliskan, N., Katunin, V.I., Belardinelli, R., Peske, F., and Rodnina, M.V. (2014). Programmed -1 frameshifting by kinetic partitioning during impeded translocation. Cell 157: 1619–1631, https://doi.org/10.1016/j.cell.2014.04.041 .
doi: 10.1016/j.cell.2014.04.041
Caliskan, N., Wohlgemuth, I., Korniy, N., Pearson, M., Peske, F., and Rodnina, M.V. (2017). Conditional switch between frameshifting regimes upon translation of dnaX mRNA. Mol. Cell 66: 558–567.e554, https://doi.org/10.1016/j.molcel.2017.04.023 .
doi: 10.1016/j.molcel.2017.04.023
Carbone, C.E., Loveland, A.B., Gamper, H.B., Hou, Y.M., Demo, G., and Korostelev, A.A. (2021). Time-resolved cryo-EM visualizes ribosomal translocation with EF-G and GTP. Nat. Commun. 12: 7236, https://doi.org/10.1038/s41467-021-27415-0 .
doi: 10.1038/s41467-021-27415-0
Champagne, J., Pataskar, A., Blommaert, N., Nagel, R., Wernaart, D., Ramalho, S., Kenski, J., Bleijerveld, O.B., Zaal, E.A., Berkers, C.R., et al.. (2021). Oncogene-dependent sloppiness in mRNA translation. Mol. Cell 81: 4709–4721.e4709, https://doi.org/10.1016/j.molcel.2021.09.002 .
doi: 10.1016/j.molcel.2021.09.002
Chen, C., Cui, X., Beausang, J.F., Zhang, H., Farrell, I., Cooperman, B.S., and Goldman, Y.E. (2016). Elongation factor G initiates translocation through a power stroke. Proc. Natl. Acad. Sci. USA. 113: 7515–7520, https://doi.org/10.1073/pnas.1602668113 .
doi: 10.1073/pnas.1602668113
Chen, C., Stevens, B., Kaur, J., Cabral, D., Liu, H., Wang, Y., Zhang, H., Rosenblum, G., Smilansky, Z., Goldman, Y.E., et al.. (2011a). Single-molecule fluorescence measurements of ribosomal translocation dynamics. Mol. Cell 42: 367–377, https://doi.org/10.1016/j.molcel.2011.03.024 .
doi: 10.1016/j.molcel.2011.03.024
Chen, C., Stevens, B., Kaur, J., Smilansky, Z., Cooperman, B.S., and Goldman, Y.E. (2011b). Allosteric vs. spontaneous exit-site (E-site) tRNA dissociation early in protein synthesis. Proc. Natl. Acad. Sci. USA. 108: 16980–16985, https://doi.org/10.1073/pnas.1106999108 .
doi: 10.1073/pnas.1106999108
Chen, C., Zhang, H., Broitman, S.L., Reiche, M., Farrell, I., Cooperman, B.S., and Goldman, Y.E. (2013a). Dynamics of translation by single ribosomes through mRNA secondary structures. Nat. Struct. Mol. Biol. 20: 582–588, https://doi.org/10.1038/nsmb.2544 .
doi: 10.1038/nsmb.2544
Chen, J., Petrov, A., Johansson, M., Tsai, A., O’Leary, S.E., and Puglisi, J.D. (2014). Dynamic pathways of -1 translational frameshifting. Nature 512: 328–332, https://doi.org/10.1038/nature13428 .
doi: 10.1038/nature13428
Chen, J., Petrov, A., Tsai, A., O’Leary, S.E., and Puglisi, J.D. (2013b). Coordinated conformational and compositional dynamics drive ribosome translocation. Nat. Struct. Mol. Biol. 20: 718–727, https://doi.org/10.1038/nsmb.2567 .
doi: 10.1038/nsmb.2567
Choi, J., O’Loughlin, S., Atkins, J.F., and Puglisi, J.D. (2020). The energy landscape of -1 ribosomal frameshifting. Sci. Adv. 6: eaax6969, https://doi.org/10.1126/sciadv.aax6969 .
doi: 10.1126/sciadv.aax6969
Choi, J. and Puglisi, J.D. (2017). Three tRNAs on the ribosome slow translation elongation. Proc. Natl. Acad. Sci. USA. 114: 13691–13696, https://doi.org/10.1073/pnas.1719592115 .
doi: 10.1073/pnas.1719592115
Chung, B.Y., Firth, A.E., and Atkins, J.F. (2010). Frameshifting in alphaviruses: a diversity of 3′ stimulatory structures. J. Mol. Biol. 397: 448–456, https://doi.org/10.1016/j.jmb.2010.01.044 .
doi: 10.1016/j.jmb.2010.01.044
Cornish, P.V., Ermolenko, D.N., Noller, H.F., and Ha, T. (2008). Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30: 578–588, https://doi.org/10.1016/j.molcel.2008.05.004 .
doi: 10.1016/j.molcel.2008.05.004
Cornish, P.V., Ermolenko, D.N., Staple, D.W., Hoang, L., Hickerson, R.P., Noller, H.F., and Ha, T. (2009). Following movement of the L1 stalk between three functional states in single ribosomes. Proc. Natl. Acad. Sci. USA. 106: 2571–2576, https://doi.org/10.1073/pnas.0813180106 .
doi: 10.1073/pnas.0813180106
Craigen, W.J. and Caskey, C.T. (1986). Expression of peptide chain release factor 2 requires high-efficiency frameshift. Nature 322: 273–275, https://doi.org/10.1038/322273a0 .
doi: 10.1038/322273a0
Cunha, C.E., Belardinelli, R., Peske, F., Holtkamp, W., Wintermeyer, W., and Rodnina, M.V. (2013). Dual use of GTP hydrolysis by elongation factor G on the ribosome. Translation (Austin) 1: e24315, https://doi.org/10.4161/trla.24315 .
doi: 10.4161/trla.24315
Czworkowski, J., Wang, J., Steitz, T.A., and Moore, P.B. (1994). The crystal structure of elongation factor G complexed with GDP, at 2.7 A resolution. EMBO J. 13: 3661–3668, https://doi.org/10.1002/j.1460-2075.1994.tb06675.x .
doi: 10.1002/j.1460-2075.1994.tb06675.x
Davies, J.E. and Rubinsztein, D.C. (2006). Polyalanine and polyserine frameshift products in Huntington’s disease. J. Med. Genet. 43: 893–896, https://doi.org/10.1136/jmg.2006.044222 .
doi: 10.1136/jmg.2006.044222
Davydov, I.I., Wohlgemuth, I., Artamonova, I.I., Urlaub, H., Tonevitsky, A.G., and Rodnina, M.V. (2013). Evolution of the protein stoichiometry in the L12 stalk of bacterial and organellar ribosomes. Nat. Commun. 4: 1387, https://doi.org/10.1038/ncomms2373 .
doi: 10.1038/ncomms2373
Desai, V.P., Frank, F., Lee, A., Righini, M., Lancaster, L., Noller, H.F., Tinoco, I., and Bustamante, C. (2019). Co-Temporal force and fluorescence measurements reveal a ribosomal gear shift mechanism of translation regulation by structured mRNAs. Mol. Cell 75: 1007–1019.e1005, https://doi.org/10.1016/j.molcel.2019.07.024 .
doi: 10.1016/j.molcel.2019.07.024
Diaconu, M., Kothe, U., Schlunzen, F., Fischer, N., Harms, J.M., Tonevitsky, A.G., Stark, H., Rodnina, M.V., and Wahl, M.C. (2005). Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 121: 991–1004, https://doi.org/10.1016/j.cell.2005.04.015 .
doi: 10.1016/j.cell.2005.04.015
Donly, B.C. and Tate, W.P. (1991). Frameshifting by eukaryotic ribosomes during expression of Escherichia coli release factor 2. Proc. Biol. Sci. 244: 207–210, https://doi.org/10.1098/rspb.1991.0072 .
doi: 10.1098/rspb.1991.0072
Dunkle, J.A., Wang, L., Feldman, M.B., Pulk, A., Chen, V.B., Kapral, G.J., Noeske, J., Richardson, J.S., Blanchard, S.C., and Cate, J.H. (2011). Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332: 981–984, https://doi.org/10.1126/science.1202692 .
doi: 10.1126/science.1202692
Ermolenko, D.N., Majumdar, Z.K., Hickerson, R.P., Spiegel, P.C., Clegg, R.M., and Noller, H.F. (2007). Observation of intersubunit movement of the ribosome in solution using FRET. J. Mol. Biol. 370: 530–540, https://doi.org/10.1016/j.jmb.2007.04.042 .
doi: 10.1016/j.jmb.2007.04.042
Ermolenko, D.N. and Noller, H.F. (2011). mRNA translocation occurs during the second step of ribosomal intersubunit rotation. Nat. Struct. Mol. Biol. 18: 457–462, https://doi.org/10.1038/nsmb.2011 .
doi: 10.1038/nsmb.2011
Evarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., al-Karadaghi, S., Svensson, L.A., and Liljas, A. (1994). Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J. 13: 3669–3677, https://doi.org/10.1002/j.1460-2075.1994.tb06676.x .
doi: 10.1002/j.1460-2075.1994.tb06676.x
Fei, J., Bronson, J.E., Hofman, J.M., Srinivas, R.L., Wiggins, C.H., and Gonzalez, R.L. (2009). Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc. Natl. Acad. Sci. USA. 106: 15702–15707, https://doi.org/10.1073/pnas.0908077106 .
doi: 10.1073/pnas.0908077106
Fei, J., Kosuri, P., MacDougall, D.D., and Gonzalez, R.L. (2008). Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell 30: 348–359, https://doi.org/10.1016/j.molcel.2008.03.012 .
doi: 10.1016/j.molcel.2008.03.012
Fischer, N., Konevega, A.L., Wintermeyer, W., Rodnina, M.V., and Stark, H. (2010). Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466: 329–333, https://doi.org/10.1038/nature09206 .
doi: 10.1038/nature09206
Frank, J. and Agrawal, R.K. (2000). A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 318–322, https://doi.org/10.1038/35018597 .
doi: 10.1038/35018597
Gallant, J. and Lindsley, D. (1993). Ribosome frameshifting at hungry codons: sequence rules, directional specificity and possible relationship to mobile element behaviour. Biochem. Soc. Trans. 21: 817–821, https://doi.org/10.1042/bst0210817 .
doi: 10.1042/bst0210817
Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., and Ramakrishnan, V. (2009). The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326: 694–699, https://doi.org/10.1126/science.1179709 .
doi: 10.1126/science.1179709
Gaspar, C., Jannatipour, M., Dion, P., Laganiere, J., Sequeiros, J., Brais, B., and Rouleau, G.A. (2000). CAG tract of MJD-1 may be prone to frameshifts causing polyalanine accumulation. Hum. Mol. Genet. 9: 1957–1966, https://doi.org/10.1093/hmg/9.13.1957 .
doi: 10.1093/hmg/9.13.1957
Gavrilova, L.P. and Spirin, A.S. (1971). Stimulation of “non-enzymic” translocation in ribosomes by p-chloromercuribenzoate. FEBS Lett. 17: 324–326, https://doi.org/10.1016/0014-5793(71)80177-1 .
doi: 10.1016/0014-5793(71)80177-1
Giedroc, D.P. and Cornish, P.V. (2009). Frameshifting RNA pseudoknots: structure and mechanism. Virus Res. 139: 193–208, https://doi.org/10.1016/j.virusres.2008.06.008 .
doi: 10.1016/j.virusres.2008.06.008
Girstmair, H., Saffert, P., Rode, S., Czech, A., Holland, G., Bannert, N., and Ignatova, Z. (2013). Depletion of cognate charged transfer RNA causes translational frameshifting within the expanded CAG stretch in huntingtin. Cell Rep. 3: 148–159, https://doi.org/10.1016/j.celrep.2012.12.019 .
doi: 10.1016/j.celrep.2012.12.019
Guo, Z. and Noller, H.F. (2012). Rotation of the head of the 30S ribosomal subunit during mRNA translocation. Proc. Natl. Acad. Sci. USA. 109: 20391–20394, https://doi.org/10.1073/pnas.1218999109 .
doi: 10.1073/pnas.1218999109
Gurvich, O.L., Baranov, P.V., Zhou, J., Hammer, A.W., Gesteland, R.F., and Atkins, J.F. (2003). Sequences that direct significant levels of frameshifting are frequent in coding regions of Escherichia coli. EMBO J. 22: 5941–5950, https://doi.org/10.1093/emboj/cdg561 .
doi: 10.1093/emboj/cdg561
Guydosh, N.R. and Green, R. (2014). Dom34 rescues ribosomes in 3′ untranslated regions. Cell 156: 950–962, https://doi.org/10.1016/j.cell.2014.02.006 .
doi: 10.1016/j.cell.2014.02.006
Halma, M.T.J., Ritchie, D.B., Cappellano, T.R., Neupane, K., and Woodside, M.T. (2019). Complex dynamics under tension in a high-efficiency frameshift stimulatory structure. Proc. Natl. Acad. Sci. USA. 116: 19500–19505, https://doi.org/10.1073/pnas.1905258116 .
doi: 10.1073/pnas.1905258116
Halma, M.T.J., Ritchie, D.B., and Woodside, M.T. (2021). Conformational Shannon entropy of mRNA structures from force Spectroscopy measurements predicts the efficiency of -1 programmed ribosomal frameshift stimulation. Phys. Rev. Lett. 126: 038102, https://doi.org/10.1103/physrevlett.126.038102 .
doi: 10.1103/physrevlett.126.038102
Han, W., Peng, B.Z., Wang, C., Townsend, G.E., Barry, N.A., Peske, F., Goodman, A.L., Liu, J., Rodnina, M.V., and Groisman, E.A. (2023). Gut colonization by Bacteroides requires translation by an EF-G paralog lacking GTPase activity. EMBO J. 42: e112372, https://doi.org/10.15252/embj.2022112372 .
doi: 10.15252/embj.2022112372
Hill, C.H., Pekarek, L., Napthine, S., Kibe, A., Firth, A.E., Graham, S.C., Caliskan, N., and Brierley, I. (2021). Structural and molecular basis for Cardiovirus 2A protein as a viral gene expression switch. Nat. Commun. 12: 7166, https://doi.org/10.1038/s41467-021-27400-7 .
doi: 10.1038/s41467-021-27400-7
Hoffer, E.D., Hong, S., Sunita, S., Maehigashi, T., Gonzalez, R.L.J., Whitford, P.C., and Dunham, C.M. (2020). Structural insights into mRNA reading frame regulation by tRNA modification and slippery codon-anticodon pairing. eLife 9: 1–20, https://doi.org/10.7554/elife.51898 .
doi: 10.7554/elife.51898
Holtkamp, W., Cunha, C.E., Peske, F., Konevega, A.L., Wintermeyer, W., and Rodnina, M.V. (2014). GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits. EMBO J. 33: 1073–1085, https://doi.org/10.1002/embj.201387465 .
doi: 10.1002/embj.201387465
Jacks, T., Power, M.D., Masiarz, F.R., Luciw, P.A., Barr, P.J., and Varmus, H.E. (1988). Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331: 280–283, https://doi.org/10.1038/331280a0 .
doi: 10.1038/331280a0
Jager, N., Ayyub, S.A., Korniy, N., Peske, F., Hoffmann, M., Rodnina, M.V., and Pohlmann, S. (2022). Mutagenic analysis of the HIV restriction factor Shiftless. Viruses 14: 1–19, https://doi.org/10.3390/v14071454 .
doi: 10.3390/v14071454
Julian, P., Konevega, A.L., Scheres, S.H., Lazaro, M., Gil, D., Wintermeyer, W., Rodnina, M.V., and Valle, M. (2008). Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc. Natl. Acad. Sci. USA 105: 16924–16927, https://doi.org/10.1073/pnas.0809587105 .
doi: 10.1073/pnas.0809587105
Katunin, V.I., Savelsbergh, A., Rodnina, M.V., and Wintermeyer, W. (2002). Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome. Biochemistry 41: 12806–12812, https://doi.org/10.1021/bi0264871 .
doi: 10.1021/bi0264871
Kelly, J.A., Olson, A.N., Neupane, K., Munshi, S., San Emeterio, J., Pollack, L., Woodside, M.T., and Dinman, J.D. (2020). Structural and functional conservation of the programmed -1 ribosomal frameshift signal of SARS coronavirus 2 (SARS-CoV-2). J. Biol. Chem. 295: 10741–10748, https://doi.org/10.1074/jbc.ac120.013449 .
doi: 10.1074/jbc.ac120.013449
Kelly, J.A., Woodside, M.T., and Dinman, J.D. (2021). Programmed -1 ribosomal frameshifting in coronaviruses: a therapeutic target. Virology 554: 75–82, https://doi.org/10.1016/j.virol.2020.12.010 .
doi: 10.1016/j.virol.2020.12.010
Kendra, J.A., Advani, V.M., Chen, B., Briggs, J.W., Zhu, J., Bress, H.J., Pathy, S.M., and Dinman, J.D. (2018). Functional and structural characterization of the Chikungunya virus translational recoding signals. J. Biol. Chem. 293: 17536–17545, https://doi.org/10.1074/jbc.ra118.005606 .
doi: 10.1074/jbc.ra118.005606
Kendra, J.A., de la Fuente, C., Brahms, A., Woodson, C., Bell, T.M., Chen, B., Khan, Y.A., Jacobs, J.L., Kehn-Hall, K., and Dinman, J.D. (2017). Ablation of programmed -1 ribosomal frameshifting in Venezuelan equine encephalitis virus results in attenuated neuropathogenicity. J. Virol. 91: 1–13, https://doi.org/10.1128/jvi.01766-16 .
doi: 10.1128/jvi.01766-16
Kim, H.D., Puglisi, J.D., and Chu, S. (2007). Fluctuations of transfer RNAs between classical and hybrid states. Biophys. J. 93: 3575–3582, https://doi.org/10.1529/biophysj.107.109884 .
doi: 10.1529/biophysj.107.109884
Klimova, M., Senyushkina, T., Samatova, E., Peng, B.Z., Pearson, M., Peske, F., and Rodnina, M.V. (2019). EF-G-induced ribosome sliding along the noncoding mRNA. Sci. Adv. 5: eaaw9049, https://doi.org/10.1126/sciadv.aaw9049 .
doi: 10.1126/sciadv.aaw9049
Konevega, A.L., Fischer, N., Semenkov, Y.P., Stark, H., Wintermeyer, W., and Rodnina, M.V. (2007). Spontaneous reverse movement of mRNA-bound tRNA through the ribosome. Nat. Struct. Mol. Biol. 14: 318–324, https://doi.org/10.1038/nsmb1221 .
doi: 10.1038/nsmb1221
Korniy, N., Goyal, A., Hoffmann, M., Samatova, E., Peske, F., Pohlmann, S., and Rodnina, M.V. (2019a). Modulation of HIV-1 Gag/Gag-Pol frameshifting by tRNA abundance. Nucleic Acids Res. 47: 5210–5222, https://doi.org/10.1093/nar/gkz202 .
doi: 10.1093/nar/gkz202
Korniy, N., Samatova, E., Anokhina, M.M., Peske, F., and Rodnina, M.V. (2019b). Mechanisms and biomedical implications of -1 programmed ribosome frameshifting on viral and bacterial mRNAs. FEBS Lett. 593: 1468–1482, https://doi.org/10.1002/1873-3468.13478 .
doi: 10.1002/1873-3468.13478
Lang, B.F., Jakubkova, M., Hegedusova, E., Daoud, R., Forget, L., Brejova, B., Vinar, T., Kosa, P., Fricova, D., Nebohacova, M., et al.. (2014). Massive programmed translational jumping in mitochondria. Proc. Natl. Acad. Sci. USA. 111: 5926–5931, https://doi.org/10.1073/pnas.1322190111 .
doi: 10.1073/pnas.1322190111
Lill, R., Robertson, J.M., and Wintermeyer, W. (1986). Affinities of tRNA binding sites of ribosomes from Escherichia coli. Biochemistry 25: 3245–3255, https://doi.org/10.1021/bi00359a025 .
doi: 10.1021/bi00359a025
Lin, J., Gagnon, M.G., Bulkley, D., and Steitz, T.A. (2015). Conformational changes of elongation factor G on the ribosome during tRNA translocation. Cell 160: 219–227, https://doi.org/10.1016/j.cell.2014.11.049 .
doi: 10.1016/j.cell.2014.11.049
Maracci, C. and Rodnina, M.V. (2016). Review: translational GTPases. Biopolymers 105: 463–475, https://doi.org/10.1002/bip.22832 .
doi: 10.1002/bip.22832
Matsumoto, S., Caliskan, N., Rodnina, M.V., Murata, A., and Nakatani, K. (2018). Small synthetic molecule-stabilized RNA pseudoknot as an activator for -1 ribosomal frameshifting. Nucleic Acids Res. 46: 8079–8089, https://doi.org/10.1093/nar/gky689 .
doi: 10.1093/nar/gky689
McLoughlin, H.S., Moore, L.R., and Paulson, H.L. (2020). Pathogenesis of SCA3 and implications for other polyglutamine diseases. Neurobiol. Dis. 134: 104635, https://doi.org/10.1016/j.nbd.2019.104635 .
doi: 10.1016/j.nbd.2019.104635
Meydan, S., Klepacki, D., Karthikeyan, S., Margus, T., Thomas, P., Jones, J.E., Khan, Y., Briggs, J., Dinman, J.D., Vazquez-Laslop, N., et al.. (2017). Programmed ribosomal frameshifting generates a copper transporter and a copper chaperone from the same gene. Mol. Cell 65: 207–219, https://doi.org/10.1016/j.molcel.2016.12.008 .
doi: 10.1016/j.molcel.2016.12.008
Miettinen, T.P. and Bjorklund, M. (2015). Modified ribosome profiling reveals high abundance of ribosome protected mRNA fragments derived from 3′ untranslated regions. Nucleic Acids Res. 43: 1019–1034, https://doi.org/10.1093/nar/gku1310 .
doi: 10.1093/nar/gku1310
Moazed, D. and Noller, H.F. (1989). Intermediate states in the movement of transfer RNA in the ribosome. Nature 342: 142–148, https://doi.org/10.1038/342142a0 .
doi: 10.1038/342142a0
Mohan, S., Donohue, J.P., and Noller, H.F. (2014). Molecular mechanics of 30S subunit head rotation. Proc. Natl. Acad. Sci. USA. 111: 13325–13330, https://doi.org/10.1073/pnas.1413731111 .
doi: 10.1073/pnas.1413731111
Mohan, S. and Noller, H.F. (2017). Recurring RNA structural motifs underlie the mechanics of L1 stalk movement. Nat. Commun. 8: 14285, https://doi.org/10.1038/ncomms14285 .
doi: 10.1038/ncomms14285
Moomau, C., Musalgaonkar, S., Khan, Y.A., Jones, J.E., and Dinman, J.D. (2016). Structural and functional characterization of programmed ribosomal frameshift signals in west nile virus Strains reveals high structural plasticity among cis-acting RNA elements. J. Biol. Chem. 291: 15788–15795, https://doi.org/10.1074/jbc.m116.735613 .
doi: 10.1074/jbc.m116.735613
Munro, J.B., Altman, R.B., O’Connor, N., and Blanchard, S.C. (2007). Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25: 505–517, https://doi.org/10.1016/j.molcel.2007.01.022 .
doi: 10.1016/j.molcel.2007.01.022
Munro, J.B., Sanbonmatsu, K.Y., Spahn, C.M., and Blanchard, S.C. (2009). Navigating the ribosome’s metastable energy landscape. Trends Biochem. Sci. 34: 390–400, https://doi.org/10.1016/j.tibs.2009.04.004 .
doi: 10.1016/j.tibs.2009.04.004
Munro, J.B., Wasserman, M.R., Altman, R.B., Wang, L., and Blanchard, S.C. (2010). Correlated conformational events in EF-G and the ribosome regulate translocation. Nat. Struct. Mol. Biol. 17: 1470–1477, https://doi.org/10.1038/nsmb.1925 .
doi: 10.1038/nsmb.1925
Namy, O., Moran, S.J., Stuart, D.I., Gilbert, R.J., and Brierley, I. (2006). A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 441: 244–247, https://doi.org/10.1038/nature04735 .
doi: 10.1038/nature04735
Napthine, S., Bell, S., Hill, C.H., Brierley, I., and Firth, A.E. (2019). Characterization of the stimulators of protein-directed ribosomal frameshifting in Theiler’s murine encephalomyelitis virus. Nucleic Acids Res. 47: 8207–8223, https://doi.org/10.1093/nar/gkz503 .
doi: 10.1093/nar/gkz503
Napthine, S., Hill, C.H., Nugent, H.C.M., and Brierley, I. (2021). Modulation of viral programmed ribosomal frameshifting and stop codon readthrough by the host restriction factor Shiftless. Viruses 13: 1–14, https://doi.org/10.3390/v13071230 .
doi: 10.3390/v13071230
Napthine, S., Ling, R., Finch, L.K., Jones, J.D., Bell, S., Brierley, I., and Firth, A.E. (2017). Protein-directed ribosomal frameshifting temporally regulates gene expression. Nat. Commun. 8: 15582, https://doi.org/10.1038/ncomms15582 .
doi: 10.1038/ncomms15582
Neupane, K., Zhao, M., Lyons, A., Munshi, S., Ileperuma, S.M., Ritchie, D.B., Hoffer, N.Q., Narayan, A., and Woodside, M.T. (2021). Structural dynamics of single SARS-CoV-2 pseudoknot molecules reveal topologically distinct conformers. Nat. Commun. 12: 4749, https://doi.org/10.1038/s41467-021-25085-6 .
doi: 10.1038/s41467-021-25085-6
Pan, D., Kirillov, S.V., and Cooperman, B.S. (2007). Kinetically competent intermediates in the translocation step of protein synthesis. Mol. Cell 25: 519–529, https://doi.org/10.1016/j.molcel.2007.01.014 .
doi: 10.1016/j.molcel.2007.01.014
Peng, B.Z., Bock, L.V., Belardinelli, R., Peske, F., Grubmuller, H., and Rodnina, M.V. (2019). Active role of elongation factor G in maintaining the mRNA reading frame during translation. Sci. Adv. 5: eaax8030, https://doi.org/10.1126/sciadv.aax8030 .
doi: 10.1126/sciadv.aax8030
Petropoulos, A.D. and Green, R. (2012). Further in vitro exploration fails to support the allosteric three-site model. J. Biol. Chem. 287: 11642–11648, https://doi.org/10.1074/jbc.c111.330068 .
doi: 10.1074/jbc.c111.330068
Petrychenko, V., Peng, B.Z., de, AP, Schwarzer, A.C., Peske, F., Rodnina, M.V., and Fischer, N. (2021). Structural mechanism of GTPase-powered ribosome-tRNA movement. Nat. Commun. 12: 5933, https://doi.org/10.1038/s41467-021-26133-x .
doi: 10.1038/s41467-021-26133-x
Poulis, P., Patel, A., Rodnina, M.V., and Adio, S. (2022). Altered tRNA dynamics during translocation on slippery mRNA as determinant of spontaneous ribosome frameshifting. Nat. Commun. 13: 4231, https://doi.org/10.1038/s41467-022-31852-w .
doi: 10.1038/s41467-022-31852-w
Ramrath, D.J., Lancaster, L., Sprink, T., Mielke, T., Loerke, J., Noller, H.F., and Spahn, C.M. (2013). Visualization of two transfer RNAs trapped in transit during elongation factor G-mediated translocation. Proc. Natl. Acad. Sci. USA. 110: 20964–20969, https://doi.org/10.1073/pnas.1320387110 .
doi: 10.1073/pnas.1320387110
Ratje, A.H., Loerke, J., Mikolajka, A., Brunner, M., Hildebrand, P.W., Starosta, A.L., Donhofer, A., Connell, S.R., Fucini, P., Mielke, T., et al.. (2010). Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468: 713–716, https://doi.org/10.1038/nature09547 .
doi: 10.1038/nature09547
Rexroad, G., Donohue, J.P., Lancaster, L., and Noller, H.F. (2022). The role of GTP hydrolysis by EF-G in ribosomal translocation. Proc. Natl. Acad. Sci. USA. 119: e2212502119, https://doi.org/10.1073/pnas.2212502119 .
doi: 10.1073/pnas.2212502119
Riegger, R.J. and Caliskan, N. (2022). Thinking outside the frame: impacting genomes capacity by programmed ribosomal frameshifting. Front. Mol. Biosci. 9: 842261, https://doi.org/10.3389/fmolb.2022.842261 .
doi: 10.3389/fmolb.2022.842261
Ritchie, D.B., Cappellano, T.R., Tittle, C., Rezajooei, N., Rouleau, L., Sikkema, W.K.A., and Woodside, M.T. (2017). Conformational dynamics of the frameshift stimulatory structure in HIV-1. RNA 23: 1376–1384, https://doi.org/10.1261/rna.061655.117 .
doi: 10.1261/rna.061655.117
Ritchie, D.B., Foster, D.A., and Woodside, M.T. (2012). Programmed -1 frameshifting efficiency correlates with RNA pseudoknot conformational plasticity, not resistance to mechanical unfolding. Proc. Natl. Acad. Sci. USA. 109: 16167–16172, https://doi.org/10.1073/pnas.1204114109 .
doi: 10.1073/pnas.1204114109
Ritchie, D.B., Soong, J., Sikkema, W.K., and Woodside, M.T. (2014). Anti-frameshifting ligand reduces the conformational plasticity of the SARS virus pseudoknot. J. Am. Chem. Soc. 136: 2196–2199, https://doi.org/10.1021/ja410344b .
doi: 10.1021/ja410344b
Rodnina, M.V., Korniy, N., Klimova, M., Karki, P., Peng, B.Z., Senyushkina, T., Belardinelli, R., Maracci, C., Wohlgemuth, I., Samatova, E., et al.. (2020). Translational recoding: canonical translation mechanisms reinterpreted. Nucleic Acids Res. 48: 1056–1067, https://doi.org/10.1093/nar/gkz783 .
doi: 10.1093/nar/gkz783
Rodnina, M.V., Peske, F., Peng, B.Z., Belardinelli, R., and Wintermeyer, W. (2019). Converting GTP hydrolysis into motion: versatile translational elongation factor G. Biol. Chem. 401: 131–142, https://doi.org/10.1515/hsz-2019-0313 .
doi: 10.1515/hsz-2019-0313
Rodnina, M.V., Savelsbergh, A., Katunin, V.I., and Wintermeyer, W. (1997). Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385: 37–41, https://doi.org/10.1038/385037a0 .
doi: 10.1038/385037a0
Rundlet, E.J., Holm, M., Schacherl, M., Natchiar, S.K., Altman, R.B., Spahn, C.M.T., Myasnikov, A.G., and Blanchard, S.C. (2021). Structural basis of early translocation events on the ribosome. Nature 595: 741–745, https://doi.org/10.1038/s41586-021-03713-x .
doi: 10.1038/s41586-021-03713-x
Salsi, E., Farah, E., Dann, J., and Ermolenko, D.N. (2014). Following movement of domain IV of elongation factor G during ribosomal translocation. Proc. Natl. Acad. Sci. USA. 111: 15060–15065, https://doi.org/10.1073/pnas.1410873111 .
doi: 10.1073/pnas.1410873111
Salsi, E., Farah, E., Netter, Z., Dann, J., and Ermolenko, D.N. (2015). Movement of elongation factor G between compact and extended conformations. J. Mol. Biol. 427: 454–467, https://doi.org/10.1016/j.jmb.2014.11.010 .
doi: 10.1016/j.jmb.2014.11.010
Savelsbergh, A., Matassova, N.B., Rodnina, M.V., and Wintermeyer, W. (2000). Role of domains 4 and 5 in elongation factor G functions on the ribosome. J. Mol. Biol. 300: 951–961, https://doi.org/10.1006/jmbi.2000.3886 .
doi: 10.1006/jmbi.2000.3886
Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M., and Cate, J.H. (2005). Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827–834, https://doi.org/10.1126/science.1117230 .
doi: 10.1126/science.1117230
Semenkov, Y.P., Rodnina, M.V., and Wintermeyer, W. (1996). The “allosteric three-site model” of elongation cannot be confirmed in a well-defined ribosome system from Escherichia coli. Proc. Natl. Acad. Sci. USA. 93: 12183–12188, https://doi.org/10.1073/pnas.93.22.12183 .
doi: 10.1073/pnas.93.22.12183
Sharma, H., Adio, S., Senyushkina, T., Belardinelli, R., Peske, F., and Rodnina, M.V. (2016). Kinetics of spontaneous and EF-G-accelerated rotation of ribosomal subunits. Cell Rep. 16: 2187–2196, https://doi.org/10.1016/j.celrep.2016.07.051 .
doi: 10.1016/j.celrep.2016.07.051
Shoji, S., Walker, S.E., and Fredrick, K. (2006). Reverse translocation of tRNA in the ribosome. Mol. Cell 24: 931–942, https://doi.org/10.1016/j.molcel.2006.11.025 .
doi: 10.1016/j.molcel.2006.11.025
Stark, H., Rodnina, M.V., Wieden, H.J., van Heel, M., and Wintermeyer, W. (2000). Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100: 301–309, https://doi.org/10.1016/s0092-8674(00)80666-2 .
doi: 10.1016/s0092-8674(00)80666-2
Stochmanski, S.J., Therrien, M., Laganiere, J., Rochefort, D., Laurent, S., Karemera, L., Gaudet, R., Vyboh, K., Van Meyel, D.J., Di Cristo, G., et al.. (2012). Expanded ATXN3 frameshifting events are toxic in Drosophila and mammalian neuron models. Hum. Mol. Genet. 21: 2211–2218, https://doi.org/10.1093/hmg/dds036 .
doi: 10.1093/hmg/dds036
Tabrizi, S.J., Flower, M.D., Ross, C.A., and Wild, E.J. (2020). Huntington disease: new insights into molecular pathogenesis and therapeutic opportunities. Nat. Rev. Neurol. 16: 529–546, https://doi.org/10.1038/s41582-020-0389-4 .
doi: 10.1038/s41582-020-0389-4
Takyar, S., Hickerson, R.P., and Noller, H.F. (2005). mRNA helicase activity of the ribosome. Cell 120: 49–58, https://doi.org/10.1016/j.cell.2004.11.042 .
doi: 10.1016/j.cell.2004.11.042
Temperley, R., Richter, R., Dennerlein, S., Lightowlers, R.N., and Chrzanowska-Lightowlers, Z.M. (2010). Hungry codons promote frameshifting in human mitochondrial ribosomes. Science 327: 301, https://doi.org/10.1126/science.1180674 .
doi: 10.1126/science.1180674
Toulouse, A., Au-Yeung, F., Gaspar, C., Roussel, J., Dion, P., and Rouleau, G.A. (2005). Ribosomal frameshifting on MJD-1 transcripts with long CAG tracts. Hum. Mol. Genet. 14: 2649–2660, https://doi.org/10.1093/hmg/ddi299 .
doi: 10.1093/hmg/ddi299
Uemura, S., Aitken, C.E., Korlach, J., Flusberg, B.A., Turner, S.W., and Puglisi, J.D. (2010). Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464: 1012–1017, https://doi.org/10.1038/nature08925 .
doi: 10.1038/nature08925
Wang, X., Xuan, Y., Han, Y., Ding, X., Ye, K., Yang, F., Gao, P., Goff, S.P., and Gao, G. (2019). Regulation of HIV-1 gag-pol expression by Shiftless, an inhibitor of programmed -1 ribosomal frameshifting. Cell 176: 625–635.e614, https://doi.org/10.1016/j.cell.2018.12.030 .
doi: 10.1016/j.cell.2018.12.030
Wasserman, M.R., Alejo, J.L., Altman, R.B., and Blanchard, S.C. (2016). Multiperspective smFRET reveals rate-determining late intermediates of ribosomal translocation. Nat. Struct. Mol. Biol. 23: 333–341, https://doi.org/10.1038/nsmb.3177 .
doi: 10.1038/nsmb.3177
Wojciechowska, M., Olejniczak, M., Galka-Marciniak, P., Jazurek, M., and Krzyzosiak, W.J. (2014). RAN translation and frameshifting as translational challenges at simple repeats of human neurodegenerative disorders. Nucleic Acids Res. 42: 11849–11864, https://doi.org/10.1093/nar/gku794 .
doi: 10.1093/nar/gku794
Zhang, W., Dunkle, J.A., and Cate, J.H. (2009). Structures of the ribosome in intermediate states of ratcheting. Science 325: 1014–1017, https://doi.org/10.1126/science.1175275 .
doi: 10.1126/science.1175275
Zhou, J., Lancaster, L., Donohue, J.P., and Noller, H.F. (2014). How the ribosome hands the A-site tRNA to the P site during EF-G-catalyzed translocation. Science 345: 1188–1191, https://doi.org/10.1126/science.1255030 .
doi: 10.1126/science.1255030
Zhou, J., Lancaster, L., Donohue, J.P., and Noller, H.F. (2019). Spontaneous ribosomal translocation of mRNA and tRNAs into a chimeric hybrid state. Proc. Natl. Acad. Sci. USA. 116: 7813–7818, https://doi.org/10.1073/pnas.1901310116 .
doi: 10.1073/pnas.1901310116
Zimmer, M.M., Kibe, A., Rand, U., Pekarek, L., Ye, L., Buck, S., Smyth, R.P., Cicin-Sain, L., and Caliskan, N. (2021). The short isoform of the host antiviral protein ZAP acts as an inhibitor of SARS-CoV-2 programmed ribosomal frameshifting. Nat. Commun. 12: 7193, https://doi.org/10.1038/s41467-021-27431-0 .
doi: 10.1038/s41467-021-27431-0