1932

Abstract

Large biomolecular systems are at the heart of many essential cellular processes. The dynamics and energetics of an increasing number of these systems are being studied by computer simulations. Pushing the limits of length- and timescales that can be accessed by current hard- and software has expanded the ability to describe biomolecules at different levels of detail. We focus in this review on the ribosome, which exemplifies the close interplay between experiment and various simulation approaches, as a particularly challenging and prototypic nanomachine that is pivotal to cellular biology due to its central role in translation. We sketch widely used simulation methods and demonstrate how the combination of simulations and experiments advances our understanding of the function of the translation apparatus based on fundamental physics.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-111622-091147
2023-05-09
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/biophys/52/1/annurev-biophys-111622-091147.html?itemId=/content/journals/10.1146/annurev-biophys-111622-091147&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abeysirigunawardena SC, Kim H, Lai J, Ragunathan K, Rappé MC et al. 2017. Evolution of protein-coupled RNA dynamics during hierarchical assembly of ribosomal complexes. Nat. Commun. 8:492
    [Google Scholar]
  2. 2.
    Aduri R, Psciuk BT, Saro P, Taniga H, Schlegel HB, SantaLucia J. 2007. AMBER force field parameters for the naturally occurring modified nucleosides in RNA. J. Chem. Theory Comput. 3:41464–75
    [Google Scholar]
  3. 3.
    Agashe VR, Guha S, Chang HC, Genevaux P, Hayer-Hartl M et al. 2004. Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell 117:2199–209
    [Google Scholar]
  4. 4.
    Agris PF, Vendeix FA, Graham WD. 2007. tRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol. 366:11–13
    [Google Scholar]
  5. 5.
    Alderson TR, Kay LE. 2021. NMR spectroscopy captures the essential role of dynamics in regulating biomolecular function. Cell 184:3577–95
    [Google Scholar]
  6. 6.
    Åqvist J, Kamerlin SCL. 2015. The conformation of a catalytic loop is central to GTPase activity on the ribosome. Biochemistry 54:2546–56
    [Google Scholar]
  7. 7.
    Åqvist J, Kamerlin SCL. 2015. Exceptionally large entropy contributions enable the high rates of GTP hydrolysis on the ribosome. Sci. Rep. 5:15817
    [Google Scholar]
  8. 8.
    Åqvist J, Kamerlin SCL. 2016. Conserved motifs in different classes of GTPases dictate their specific modes of catalysis. ACS Catal. 6:31737–43
    [Google Scholar]
  9. 9.
    Åqvist J, Lind C, Sund J, Wallin G. 2012. Bridging the gap between ribosome structure and biochemistry by mechanistic computations. Curr. Opin. Struct. Biol. 22:6815–23
    [Google Scholar]
  10. 10.
    Arenz S, Bock LV, Graf M, Innis CA, Beckmann R et al. 2016. A combined cryo-EM and molecular dynamics approach reveals the mechanism of ErmBL-mediated translation arrest. Nat. Commun. 7:12026
    [Google Scholar]
  11. 11.
    B RP, Plotnikov NV, Lameira J, Warshel A. 2013. Quantitative exploration of the molecular origin of the activation of GTPase. PNAS 110:5120509–14
    [Google Scholar]
  12. 12.
    Bao C, Loerch S, Ling C, Korostelev AA, Grigorieff N, Ermolenko DN. 2020. mRNA stem-loops can pause the ribosome by hindering A-site tRNA binding. eLife 9:e55799
    [Google Scholar]
  13. 13.
    Beckert B, Leroy EC, Sothiselvam S, Bock LV, Svetlov MS et al. 2021. Structural and mechanistic basis for translation inhibition by macrolide and ketolide antibiotics. Nat. Commun. 12:4466
    [Google Scholar]
  14. 14.
    Belardinelli R, Sharma H, Caliskan N, Cunha CE, Peske F et al. 2016. Choreography of molecular movements during ribosome progression along mRNA. Nat. Struct. Mol. Biol. 23:4342–48
    [Google Scholar]
  15. 15.
    Belardinelli R, Sharma H, Peske F, Wintermeyer W, Rodnina MV. 2016. Translocation as continuous movement through the ribosome. RNA Biol. 13:121197–203
    [Google Scholar]
  16. 16.
    Belew AT, Meskauskas A, Musalgaonkar S, Advani VM, Sulima SO et al. 2014. Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway. Nature 512:7514265–69
    [Google Scholar]
  17. 17.
    Bernardi RC, Melo MC, Schulten K. 2015. Enhanced sampling techniques in molecular dynamics simulations of biological systems. Biochim. Biophys. Acta Gen. Subj. 1850:5872–77
    [Google Scholar]
  18. 18.
    Best RB, Zhu X, Shim J, Lopes PE, Mittal J et al. 2012. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone ϕ, ψ and side-chain χ1 and χ2 dihedral angles. J. Chem. Theory Comput. 8:93257–73
    [Google Scholar]
  19. 19.
    Bhatt PR, Scaiola A, Loughran G, Leibundgut M, Kratzel A et al. 2021. Structural basis of ribosomal frameshifting during translation of the SARS-CoV-2 RNA genome. Science 372:65481306–13
    [Google Scholar]
  20. 20.
    Bock LV, Blau C, Schröder GF, Davydov II, Fischer N et al. 2013. Energy barriers and driving forces in tRNA translocation through the ribosome. Nat. Struct. Mol. Biol. 20:121390–96
    [Google Scholar]
  21. 21.
    Bock LV, Blau C, Vaiana AC, Grubmüller H. 2015. Dynamic contact network between ribosomal subunits enables rapid large-scale rotation during spontaneous translocation. Nucleic Acids Res. 43:146747–60
    [Google Scholar]
  22. 22.
    Bock LV, Caliskan N, Korniy N, Peske F, Rodnina MV, Grubmüller H. 2019. Thermodynamic control of −1 programmed ribosomal frameshifting. Nat. Commun. 10:4598
    [Google Scholar]
  23. 23.
    Bock LV, Grubmüller H. 2022. Effects of cryo-EM cooling on structural ensembles. Nat. Commun. 13:1709
    [Google Scholar]
  24. 24.
    Bock LV, Kolář MH, Grubmüller H. 2018. Molecular simulations of the ribosome and associated translation factors. Curr. Opin. Struct. Biol. 49:27–35
    [Google Scholar]
  25. 25.
    Brierley I. 1995. Ribosomal frameshifting on viral RNAs. J. Gen. Virol. 76:81885–92
    [Google Scholar]
  26. 26.
    Bruce AG, Atkins JF, Gesteland RF. 1986. tRNA anticodon replacement experiments show that ribosomal frameshifting can be caused by doublet decoding. PNAS 83:145062–66
    [Google Scholar]
  27. 27.
    Bui PT, Hoang TX. 2016. Folding and escape of nascent proteins at ribosomal exit tunnel. J. Chem. Phys. 144:9095102
    [Google Scholar]
  28. 28.
    Bui PT, Hoang TX. 2018. Protein escape at the ribosomal exit tunnel: effects of native interactions, tunnel length, and macromolecular crowding. J. Chem. Phys. 149:4045102
    [Google Scholar]
  29. 29.
    Bui PT, Hoang TX. 2020. Protein escape at the ribosomal exit tunnel: effect of the tunnel shape. J. Chem. Phys. 153:4045105
    [Google Scholar]
  30. 30.
    Bustamante C, Alexander L, Maciuba K, Kaiser CM. 2020. Single-molecule studies of protein folding with optical tweezers. Annu. Rev. Biochem. 89:443–70
    [Google Scholar]
  31. 31.
    Cabrita LD, Cassaignau AM, Launay HM, Waudby CA, Wlodarski T et al. 2016. A structural ensemble of a ribosome–nascent chain complex during cotranslational protein folding. Nat. Struct. Mol. Biol. 23:4278–85
    [Google Scholar]
  32. 32.
    Cabrita LD, Hsu STD, Launay H, Dobson CM, Christodoulou J. 2009. Probing ribosome-nascent chain complexes produced in vivo by NMR spectroscopy. PNAS 106:5222239–44
    [Google Scholar]
  33. 33.
    Camilloni C, Cavalli A, Vendruscolo M. 2013. Replica-averaged metadynamics. J. Chem. Theory Comput. 9:125610–17
    [Google Scholar]
  34. 34.
    Carmody PJ, Zimmer MH, Kuntz CP, Harrington HR, Duckworth KE et al. 2021. Coordination of −1 programmed ribosomal frameshifting by transcript and nascent chain features revealed by deep mutational scanning. Nucleic Acids Res. 49:2212943–54
    [Google Scholar]
  35. 35.
    Cassaignau AM, Włodarski T, Chan SH, Woodburn LF, Bukvin IV et al. 2021. Interactions between nascent proteins and the ribosome surface inhibit co-translational folding. Nat. Chem. 13:121214–20
    [Google Scholar]
  36. 36.
    Caulfield T, Coban M, Tek A, Flores SC. 2019. Molecular dynamics simulations suggest a non-doublet decoding model of −1 frameshifting by tRNASer3. Biomolecules 9:11745
    [Google Scholar]
  37. 37.
    Chan SH, Waudby CA, Christodoulou J. 2022. NMR snapshots of nascent chains emerging from the ribosome during biosynthesis. ChemRxiv. https://doi.org/10.26434/chemrxiv-2022-0lmsp
  38. 38.
    Chan SH, Włodarski T, Streit JO, Cassaignau AM, Woodburn LF et al. 2022. The ribosome stabilizes partially folded intermediates of a nascent multi-domain protein. Nat. Chem. 14:101165–73
    [Google Scholar]
  39. 39.
    Chang KC, Salawu EO, Chang YY, Wen JD, Yang LW. 2019. Resolution-exchanged structural modeling and simulations jointly unravel that subunit rolling underlies the mechanism of programmed ribosomal frameshifting. Bioinformatics 35:6945–52
    [Google Scholar]
  40. 40.
    Chen CY, Chang YC, Lin BL, Huang CH, Tsai MD. 2019. Temperature-resolved cryo-EM uncovers structural bases of temperature-dependent enzyme functions. J. Am. Chem. Soc. 141:5119983–87
    [Google Scholar]
  41. 41.
    Chu X, Su X, Liu M, Li L, Li T et al. 2022. Annealing synchronizes the 70S ribosome into a minimum-energy conformation. PNAS 119:8e2111231119
    [Google Scholar]
  42. 42.
    Chung BY, Firth AE, Atkins JF. 2010. Frameshifting in alphaviruses: a diversity of 3′ stimulatory structures. J. Mol. Biol. 397:2448–56
    [Google Scholar]
  43. 43.
    Clark PL. 2004. Protein folding in the cell: reshaping the folding funnel. Trends Biochem. Sci. 29:10527–34
    [Google Scholar]
  44. 44.
    Cohen AJ, Mori-Sánchez P, Yang W 2012. Challenges for density functional theory. Chem. Rev. 112:1289–320
    [Google Scholar]
  45. 45.
    Cornish PV, Ermolenko DN, Noller HF, Ha T. 2008. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30:5578–88
    [Google Scholar]
  46. 46.
    Csaszar K, Špačková N, Štefl R, Šponer J, Leontis NB. 2001. Molecular dynamics of the frame-shifting pseudoknot from beet western yellows virus: the role of non-Watson-Crick base-pairing, ordered hydration, cation binding and base mutations on stability and unfolding. J. Mol. Biol. 313:51073–91
    [Google Scholar]
  47. 47.
    Cunha CE, Belardinelli R, Peske F, Holtkamp W, Wintermeyer W, Rodnina MV. 2013. Dual use of GTP hydrolysis by elongation factor G on the ribosome. Translation 1:1e24315
    [Google Scholar]
  48. 48.
    Daviter T, Wieden HJ, Rodnina MV. 2003. Essential role of histidine 84 in elongation factor Tu for the chemical step of GTP hydrolysis on the ribosome. J. Mol. Biol. 332:3689–99
    [Google Scholar]
  49. 49.
    de Jong DH, Baoukina S, Ingólfsson HI, Marrink SJ. 2016. Martini straight: boosting performance using a shorter cutoff and GPUs. Comput. Phys. Commun. 199:1–7
    [Google Scholar]
  50. 50.
    Deckert A, Cassaignau AME, Wang X, Włodarski T, Chan SHS et al. 2021. Common sequence motifs of nascent chains engage the ribosome surface and trigger factor. PNAS 118:52e2103015118
    [Google Scholar]
  51. 51.
    Deckert A, Waudby CA, Włodarski T, Wentink AS, Wang X et al. 2016. Structural characterization of the interaction of α-synuclein nascent chains with the ribosomal surface and trigger factor. PNAS 113:185012–17
    [Google Scholar]
  52. 52.
    Deeng J, Chan KY, van der Sluis EO, Berninghausen O, Han W et al. 2016. Dynamic behavior of trigger factor on the ribosome. J. Mol. Biol. 428:183588–602
    [Google Scholar]
  53. 53.
    Di Palma F, Decherchi S, Pardo-Avila F, Succi S, Levitt M et al. 2021. Probing interplays between human XBP1u translational arrest peptide and 80S ribosome. J. Chem. Theory Comput. 18:31905–14
    [Google Scholar]
  54. 54.
    Doster W, Cusack S, Petry W. 1989. Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337:6209754–56
    [Google Scholar]
  55. 55.
    Dror RO, Dirks RM, Grossman J, Xu H, Shaw DE. 2012. Biomolecular simulation: a computational microscope for molecular biology. Annu. Rev. Biophys. 41:429–52
    [Google Scholar]
  56. 56.
    Englander MT, Avins JL, Fleisher RC, Liu B, Effraim PR et al. 2015. The ribosome can discriminate the chirality of amino acids within its peptidyl-transferase center. PNAS 112:196038–43
    [Google Scholar]
  57. 57.
    Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H. 2010. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466:7304329–33
    [Google Scholar]
  58. 58.
    Fischer N, Neumann P, Bock LV, Maracci C, Wang Z et al. 2016. The pathway to GTPase activation of elongation factor SelB on the ribosome. Nature 540:763180–85
    [Google Scholar]
  59. 59.
    Fischer N, Neumann P, Konevega AL, Bock LV, Ficner R et al. 2015. Structure of the E. coli ribosome–EF-Tu complex at <3 Å resolution by Cs-corrected cryo-EM. Nature 520:7548567–70
    [Google Scholar]
  60. 60.
    Fogolari F, Brigo A, Molinari H. 2002. The Poisson-Boltzmann equation for biomolecular electrostatics: a tool for structural biology. J. Mol. Recognit. 15:6377–92
    [Google Scholar]
  61. 61.
    Förster T. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. 437:1–255–75
    [Google Scholar]
  62. 62.
    Frauenfelder H, Parak F, Young RD. 1988. Conformational substates in proteins. Annu. Rev. Biophys. Biophys. Chem. 17:451–79
    [Google Scholar]
  63. 63.
    Freitas FC, Fuchs G, de Oliveira RJ, Whitford PC. 2021. The dynamics of subunit rotation in a eukaryotic ribosome. Biophysica 1:2204–21
    [Google Scholar]
  64. 64.
    Frenkel D, Smit B. 2001. Understanding Molecular Simulation: From Algorithms to Applications, Vol. 1 Amsterdam: Elsevier
  65. 65.
    Fries SJ, Braun TS, Globisch C, Peter C, Drescher M, Deuerling E. 2021. Deciphering molecular details of the RAC–ribosome interaction by EPR spectroscopy. Sci. Rep. 11:8681
    [Google Scholar]
  66. 66.
    Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V. 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326:5953694–99
    [Google Scholar]
  67. 67.
    Gaus M, Cui Q, Elstner M. 2014. Density functional tight binding: application to organic and biological molecules. Wiley Interdiscip. Rev. Comput. Mol. Sci. 4:149–61
    [Google Scholar]
  68. 68.
    Ge X, Mandava CS, Lind C, Åqvist J, Sanyal S. 2018. Complementary charge-based interaction between the ribosomal-stalk protein L7/12 and IF2 is the key to rapid subunit association. PNAS 115:184649–54
    [Google Scholar]
  69. 69.
    Giraldo-Barreto J, Ortiz S, Thiede EH, Palacio-Rodriguez K, Carpenter B et al. 2021. A Bayesian approach to extracting free-energy profiles from cryo-electron microscopy experiments. Sci. Rep. 11:13657
    [Google Scholar]
  70. 70.
    Go N. 1983. Theoretical studies of protein folding. Annu. Rev. Biophys. Bioeng. 12:183–210
    [Google Scholar]
  71. 71.
    Gogonea V, Suárez D, van der Vaart A, Merz KM Jr. 2001. New developments in applying quantum mechanics to proteins. Curr. Opin. Struct. Biol. 11:2217–23
    [Google Scholar]
  72. 72.
    Goldman DH, Kaiser CM, Milin A, Righini M, Tinoco I, Bustamante C. 2015. Mechanical force releases nascent chain-mediated ribosome arrest in vitro and in vivo. Science 348:6233457–60
    [Google Scholar]
  73. 73.
    Gopich IV, Szabo A. 2012. Theory of the energy transfer efficiency and fluorescence lifetime distribution in single-molecule FRET. PNAS 109:207747–52
    [Google Scholar]
  74. 74.
    Gupta A, Bansal M. 2014. Local structural and environmental factors define the efficiency of an RNA pseudoknot involved in programmed ribosomal frameshift process. J. Phys. Chem. B 118:4111905–20
    [Google Scholar]
  75. 75.
    Gupta A, Bansal M. 2016. The role of sequence in altering the unfolding pathway of an RNA pseudoknot: a steered molecular dynamics study. Phys. Chem. Chem. Phys. 18:4128767–80
    [Google Scholar]
  76. 76.
    Halbmair K, Seikowski J, Tkach I, Höbartner C, Sezer D, Bennati M. 2016. High-resolution measurement of long-range distances in RNA: pulse EPR spectroscopy with TEMPO-labeled nucleotides. Chem. Sci. 7:53172–80
    [Google Scholar]
  77. 77.
    Harrington HR, Zimmer MH, Chamness LM, Nash V, Penn WD et al. 2020. Cotranslational folding stimulates programmed ribosomal frameshifting in the alphavirus structural polyprotein. J. Biol. Chem. 295:206798–808
    [Google Scholar]
  78. 78.
    Hartono YD, Ito M, Villa A, Nilsson L. 2018. Computational study of uracil tautomeric forms in the ribosome: the case of uracil and 5-oxyacetic acid uracil in the first anticodon position of tRNA. J. Phys. Chem. B 122:31152–60
    [Google Scholar]
  79. 79.
    Hassan A, Byju S, Whitford PC. 2021. The energetics of subunit rotation in the ribosome. Biophys. Rev. 13:61029–37
    [Google Scholar]
  80. 80.
    Heinz M, Erlenbach N, Stelzl LS, Thierolf G, Kamble NR et al. 2020. High-resolution EPR distance measurements on RNA and DNA with the non-covalent G′ spin label. Nucleic Acids Res. 48:2924–33
    [Google Scholar]
  81. 81.
    Hensen U, Meyer T, Haas J, Rex R, Vriend G, Grubmüller H 2012. Exploring protein dynamics space: the dynasome as the missing link between protein structure and function. PLOS ONE 7:5e33931
    [Google Scholar]
  82. 82.
    Hoefling M, Lima N, Haenni D, Seidel CA, Schuler B, Grubmüller H. 2011. Structural heterogeneity and quantitative FRET efficiency distributions of polyprolines through a hybrid atomistic simulation and Monte Carlo approach. PLOS ONE 6:5e19791
    [Google Scholar]
  83. 83.
    Holtkamp W, Cunha CE, Peske F, Konevega AL, Wintermeyer W, Rodnina MV. 2014. GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits. EMBO J. 33:91073–85
    [Google Scholar]
  84. 84.
    Holtkamp W, Kokic G, Jager M, Mittelstaet J, Komar AA, Rodnina MV. 2015. Cotranslational protein folding on the ribosome monitored in real time. Science 350:62641104–7
    [Google Scholar]
  85. 85.
    Hori N, Denesyuk NA, Thirumalai D. 2016. Salt effects on the thermodynamics of a frameshifting RNA pseudoknot under tension. J. Mol. Biol. 428:142847–59
    [Google Scholar]
  86. 86.
    Hsu CF, Chang KC, Chen YL, Hsieh PS, Lee AI et al. 2021. Formation of frameshift-stimulating RNA pseudoknots is facilitated by remodeling of their folding intermediates. Nucleic Acids Res. 49:126941–57
    [Google Scholar]
  87. 87.
    Huter P, Arenz S, Bock LV, Graf M, Frister JO et al. 2017. Structural basis for polyproline-mediated ribosome stalling and rescue by the translation elongation factor EF-P. Mol. Cell 68:3515–27
    [Google Scholar]
  88. 88.
    Igaev M, Kutzner C, Bock LV, Vaiana AC, Grubmüller H 2019. Automated cryo-EM structure refinement using correlation-driven molecular dynamics. eLife 8:e43542
    [Google Scholar]
  89. 89.
    Imai H, Uchiumi T, Kodera N. 2020. Direct visualization of translational GTPase factor pool formed around the archaeal ribosomal P-stalk by high-speed AFM. PNAS 117:5132386–94
    [Google Scholar]
  90. 90.
    Invernizzi M, Piaggi PM, Parrinello M. 2020. Unified approach to enhanced sampling. Phys. Rev. X 10:4041034
    [Google Scholar]
  91. 91.
    Jiang Y, O'Brien EP. 2021. Mechanical forces have a range of effects on the rate of ribosome catalyzed peptidyl transfer depending on direction. J. Phys. Chem. B 125:267128–36
    [Google Scholar]
  92. 92.
    Jo S, Kim T, Iyer VG, Im W. 2008. CHARMM-GUI: a web-based graphical user interface for CHARMM. J. Comput. Chem. 29:111859–65
    [Google Scholar]
  93. 93.
    Jones CP, Ferré-D'amaré AR. 2022. Crystal structure of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) frameshifting pseudoknot. RNA 28:2239–49
    [Google Scholar]
  94. 94.
    Jones RO. 2015. Density functional theory: its origins, rise to prominence, and future. Rev. Mod. Phys. 87:3897
    [Google Scholar]
  95. 95.
    Juette MF, Terry DS, Wasserman MR, Zhou Z, Altman RB et al. 2014. The bright future of single-molecule fluorescence imaging. Curr. Opin. Chem. Biol. 20:1103–11
    [Google Scholar]
  96. 96.
    Kalinin S, Peulen T, Sindbert S, Rothwell PJ, Berger S et al. 2012. A toolkit and benchmark study for FRET-restrained high-precision structural modeling. Nat. Methods 9:121218–25
    [Google Scholar]
  97. 97.
    Karplus M, McCammon JA. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:9646–52
    [Google Scholar]
  98. 98.
    Karplus M, Petsko GA. 1990. Molecular dynamics simulations in biology. Nature 347:6294631–39
    [Google Scholar]
  99. 99.
    Kästner J, Sherwood P. 2010. The ribosome catalyzes peptide bond formation by providing high ionic strength. Mol. Phys. 108:3–4293–306
    [Google Scholar]
  100. 100.
    Kazantsev A, Ignatova Z. 2021. Constraints on error rate revealed by computational study of G·U tautomerization in translation. Nucleic Acids Res. 1:125687913–14
    [Google Scholar]
  101. 101.
    Kazemi M, Himo F, Åqvist J. 2016. Peptide release on the ribosome involves substrate-assisted base catalysis. ACS Catal. 6:128432–39
    [Google Scholar]
  102. 102.
    Kim DN, Moriarty NW, Kirmizialtin S, Afonine PV, Poon B et al. 2019. Cryo_fit: democratization of flexible fitting for cryo-EM. J. Struct. Biol. 208:11–6
    [Google Scholar]
  103. 103.
    Kim H, Abeysirigunawarden SC, Chen K, Mayerle M, Ragunathan K et al. 2014. Protein-guided RNA dynamics during early ribosome assembly. Nature 506:7488334–38
    [Google Scholar]
  104. 104.
    Kim YG, Su L, Maas S, O'Neill A, Rich A. 1999. Specific mutations in a viral RNA pseudoknot drastically change ribosomal frameshifting efficiency. PNAS 96:2514234–39
    [Google Scholar]
  105. 105.
    Koehl P. 2006. Electrostatics calculations: latest methodological advances. Curr. Opin. Struct. Biol. 16:2142–51
    [Google Scholar]
  106. 106.
    Kolář MH, Nagy G, Kunkel J, Vaiana SM, Bock LV, Grubmüller H. 2022. Folding of VemP into translation-arresting secondary structure is driven by the ribosome exit tunnel. Nucleic Acids Res. 50:42258–69
    [Google Scholar]
  107. 107.
    Korostelev AA. 2022. The structural dynamics of translation. Annu. Rev. Biochem. 91:245–67
    [Google Scholar]
  108. 108.
    Kuhlenkoetter S, Wintermeyer W, Rodnina MV. 2011. Different substrate-dependent transition states in the active site of the ribosome. Nature 476:7360351–54
    [Google Scholar]
  109. 109.
    Kurland C. 1992. Translational accuracy and the fitness of bacteria. Annu. Rev. Genet. 26:29–50
    [Google Scholar]
  110. 110.
    Kutzner C, Páll S, Fechner M, Esztermann A, de Groot BL, Grubmüller H 2019. More bang for your buck: improved use of GPU nodes for GROMACS 2018. J. Comput. Chem. 40:272418–31
    [Google Scholar]
  111. 111.
    Leininger SE, Rodriguez J, Vu QV, Jiang Y, Li MS et al. 2021. Ribosome elongation kinetics of consecutively charged residues are coupled to electrostatic force. Biochemistry 60:433223–35
    [Google Scholar]
  112. 112.
    Levi M, Nguyen K, Dukaye L, Whitford PC. 2017. Quantifying the relationship between single-molecule probes and subunit rotation in the ribosome. Biophys. J. 113:122777–86
    [Google Scholar]
  113. 113.
    Levi M, Noel JK, Whitford PC. 2019. Studying ribosome dynamics with simplified models. Methods 162:128–40
    [Google Scholar]
  114. 114.
    Levi M, Walak K, Wang A, Mohanty U, Whitford PC. 2020. A steric gate controls P/E hybrid-state formation of tRNA on the ribosome. Nat. Commun. 11:5706
    [Google Scholar]
  115. 115.
    Levi M, Whitford PC. 2019. Dissecting the energetics of subunit rotation in the ribosome. J. Phys. Chem. B 123:132812–23
    [Google Scholar]
  116. 116.
    Levine IN, Busch DH, Shull H. 2009. Quantum Chemistry, Vol. 6 Hoboken, NJ: Prentice Hall
  117. 117.
    Lin J, Zhou D, Steitz TA, Polikanov YS, Gagnon MG. 2018. Ribosome-targeting antibiotics: modes of action, mechanisms of resistance, and implications for drug design. Annu. Rev. Biochem. 87:451–78
    [Google Scholar]
  118. 118.
    Lind C, Åqvist J. 2016. Principles of start codon recognition in eukaryotic translation initiation. Nucleic Acids Res. 44:178425–32
    [Google Scholar]
  119. 119.
    Lind C, Oliveira A, Åqvist J. 2017. Origin of the omnipotence of eukaryotic release factor 1. Nat. Commun. 8:1425
    [Google Scholar]
  120. 120.
    Lindorff-Larsen K, Best RB, DePristo MA, Dobson CM, Vendruscolo M. 2005. Simultaneous determination of protein structure and dynamics. Nature 433:7022128–32
    [Google Scholar]
  121. 121.
    Liu K, Chen X, Kaiser CM 2019. Energetic dependencies dictate folding mechanism in a complex protein. PNAS 116:5125641–48
    [Google Scholar]
  122. 122.
    Liu T, Kaplan A, Alexander L, Yan S, Wen JD et al. 2014. Direct measurement of the mechanical work during translocation by the ribosome. eLife 3:e03406
    [Google Scholar]
  123. 123.
    Liutkute M, Samatova E, Rodnina MV. 2020. Cotranslational folding of proteins on the ribosome. Biomolecules 10:197
    [Google Scholar]
  124. 124.
    Lu J, Deutsch C. 2008. Electrostatics in the ribosomal tunnel modulate chain elongation rates. J. Mol. Biol. 384:173–86
    [Google Scholar]
  125. 125.
    Maier JA, Martinez C, Kasavajhala K, Wickstrom L, Hauser KE, Simmerling C. 2015. ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput. 11:83696–713
    [Google Scholar]
  126. 126.
    Makarov GI, Makarova TM, Sumbatyan NV, Bogdanov AA. 2016. Investigation of ribosomes using molecular dynamics simulation methods. Biochemistry 81:131579–88
    [Google Scholar]
  127. 127.
    Malygin AA, Graifer DM, Meschaninova MI, Venyaminova AG, Krumkacheva OA et al. 2015. Doubly spin-labeled RNA as an EPR reporter for studying multicomponent supramolecular assemblies. Biophys. J. 109:122637–43
    [Google Scholar]
  128. 128.
    Malygin AA, Graifer DM, Meschaninova MI, Venyaminova AG, Timofeev IO et al. 2018. Structural rearrangements in mRNA upon its binding to human 80S ribosomes revealed by EPR spectroscopy. Nucleic Acids Res. 46:2897–904
    [Google Scholar]
  129. 129.
    Malygin AA, Krumkacheva OA, Graifer DM, Timofeev IO, Ochkasova AS et al. 2019. Exploring the interactions of short RNAs with the human 40S ribosomal subunit near the mRNA entry site by EPR spectroscopy. Nucleic Acids Res. 47:2211850–60
    [Google Scholar]
  130. 130.
    Maracci C, Peske F, Dannies E, Pohl C, Rodnina MV. 2014. Ribosome-induced tuning of GTP hydrolysis by a translational GTPase. PNAS 111:4014418–23
    [Google Scholar]
  131. 131.
    Marrink SJ, De Vries AH, Mark AE. 2004. Coarse grained model for semiquantitative lipid simulations. J. Phys. Chem. B 108:2750–60
    [Google Scholar]
  132. 132.
    Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, De Vries AH. 2007. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111:277812–24
    [Google Scholar]
  133. 133.
    Marrink SJ, Tieleman DP. 2013. Perspective on the Martini model. Chem. Soc. Rev. 42:166801–22
    [Google Scholar]
  134. 134.
    Marshall RA, Dorywalska M, Puglisi JD. 2008. Irreversible chemical steps control intersubunit dynamics during translation. PNAS 105:4015364–69
    [Google Scholar]
  135. 135.
    McGrath H, Černeková M, Kolář MH. 2022. Binding of the peptide deformylase on the ribosome surface modulates the exit tunnel interior. Biophys. J. 121:234443–51
    [Google Scholar]
  136. 136.
    Mondal D, Warshel A. 2018. EF-Tu and EF-G are activated by allosteric effects. PNAS 115:133386–91
    [Google Scholar]
  137. 137.
    Munro JB, Altman RB, O'Connor N, Blanchard SC 2007. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25:4505–17
    [Google Scholar]
  138. 138.
    Munro JB, Vaiana A, Sanbonmatsu KY, Blanchard SC. 2008. A new view of protein synthesis: mapping the free energy landscape of the ribosome using single-molecule FRET. Biopolymers 89:7565–77
    [Google Scholar]
  139. 139.
    Nadezhdin KD, Neuberger A, Trofimov YA, Krylov NA, Sinica V et al. 2021. Structural mechanism of heat-induced opening of a temperature-sensitive TRP channel. Nat. Struct. Mol. Biol. 28:7564–72
    [Google Scholar]
  140. 140.
    Nguyen K, Whitford PC. 2016. Steric interactions lead to collective tilting motion in the ribosome during mRNA–tRNA translocation. Nat. Commun. 7:10586
    [Google Scholar]
  141. 141.
    Nguyen KKQ, Gomez YK, Bakhom M, Radcliffe A, La P et al. 2017. Ensemble simulations: folding, unfolding and misfolding of a high-efficiency frameshifting RNA pseudoknot. Nucleic Acids Res. 45:84893–904
    [Google Scholar]
  142. 142.
    Niesen MJM, Müller-Lucks A, Hedman R, von Heijne G, Miller TF. 2018. Forces on nascent polypeptides during membrane insertion and translocation via the Sec translocon. Biophys. J. 115:101885–94
    [Google Scholar]
  143. 143.
    Niesen MJM, Wang CY, Van Lehn RC, Miller TF. 2017. Structurally detailed coarse-grained model for Sec-facilitated co-translational protein translocation and membrane integration. PLOS Comput. Biol. 13:3e1005427
    [Google Scholar]
  144. 144.
    Nissley DA, Jiang Y, Trovato F, Sitarik I, Narayan KB et al. 2022. Universal protein misfolding intermediates can bypass the proteostasis network and remain soluble and less functional. Nat. Commun. 13:3081
    [Google Scholar]
  145. 145.
    Nissley DA, O'Brien EP. 2018. Structural origins of FRET-observed nascent chain compaction on the ribosome. J. Phys. Chem. B 122:439927–37
    [Google Scholar]
  146. 146.
    Nissley DA, Vu QV, Trovato F, Ahmed N, Jiang Y et al. 2020. Electrostatic interactions govern extreme nascent protein ejection times from ribosomes and can delay ribosome recycling. J. Am. Chem. Soc. 142:136103–10
    [Google Scholar]
  147. 147.
    Noel JK, Levi M, Raghunathan M, Lammert H, Hayes RL et al. 2016. SMOG 2: a versatile software package for generating structure-based models. PLOS Comput. Biol. 12:3e1004794
    [Google Scholar]
  148. 148.
    O'Brien EP, Christodoulou J, Vendruscolo M, Dobson CM. 2012. Trigger factor slows co-translational folding through kinetic trapping while sterically protecting the nascent chain from aberrant cytosolic interactions. J. Am. Chem. Soc. 134:2610920–32
    [Google Scholar]
  149. 149.
    O'Brien EP, Hsu STD, Christodoulou J, Vendruscolo M, Dobson CM. 2010. Transient tertiary structure formation within the ribosome exit port. J. Am. Chem. Soc. 132:4716928–37
    [Google Scholar]
  150. 150.
    Omar SI, Zhao M, Sekar RV, Moghadam SA, Tuszynski JA, Woodside MT. 2021. Modeling the structure of the frameshift-stimulatory pseudoknot in SARS-CoV-2 reveals multiple possible conformers. PLOS Comput. Biol. 17:1e1008603
    [Google Scholar]
  151. 151.
    Pape T, Wintermeyer W, Rodnina MV. 1998. Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. EMBO J. 17:247490–97
    [Google Scholar]
  152. 152.
    Park SJ, Kim YG, Park HJ. 2011. Identification of RNA pseudoknot-binding ligand that inhibits the −1 ribosomal frameshifting of SARS-coronavirus by structure-based virtual screening. J. Am. Chem. Soc. 133:2610094–100
    [Google Scholar]
  153. 153.
    Petrone PM, Snow CD, Lucent D, Pande VS. 2008. Side-chain recognition and gating in the ribosome exit tunnel. PNAS 105:4316549–54
    [Google Scholar]
  154. 154.
    Polikanov YS, Steitz TA, Innis CA. 2014. A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol. 21:9787–93
    [Google Scholar]
  155. 155.
    Qi Y, Ingólfsson HI, Cheng X, Lee J, Marrink SJ, Im W. 2015. CHARMM-GUI Martini Maker for coarse-grained simulations with the Martini force field. J. Chem. Theory Comput. 11:94486–94
    [Google Scholar]
  156. 156.
    Ribeiro JV, Bernardi RC, Rudack T, Stone JE, Phillips JC et al. 2016. QwikMD—integrative molecular dynamics toolkit for novices and experts. Sci. Rep. 6:26536
    [Google Scholar]
  157. 157.
    Rico F, Russek A, González L, Grubmüller H, Scheuring S. 2019. Heterogeneous and rate-dependent streptavidin–biotin unbinding revealed by high-speed force spectroscopy and atomistic simulations. PNAS 116:146594–601
    [Google Scholar]
  158. 158.
    Riegger RJ, Caliskan N. 2022. Thinking outside the frame: impacting genomes capacity by programmed ribosomal frameshifting. Front. Mol. Biosci. 9:129
    [Google Scholar]
  159. 159.
    Robustelli P, Kohlhoff K, Cavalli A, Vendruscolo M. 2010. Using NMR chemical shifts as structural restraints in molecular dynamics simulations of proteins. Structure 18:8923–33
    [Google Scholar]
  160. 160.
    Rodnina MV. 2018. Translation in prokaryotes. Cold Spring Harb. Perspect. Biol. 10:9a032664
    [Google Scholar]
  161. 161.
    Rodnina MV. 2023. Decoding and recoding of mRNA sequences by the ribosome. Annu. Rev. Biophys. 52: In press
    [Google Scholar]
  162. 162.
    Rodnina MV, Fischer N, Maracci C, Stark H. 2017. Ribosome dynamics during decoding. Philos. Trans. R. Soc. B 372:171620160182
    [Google Scholar]
  163. 163.
    Rodnina MV, Fricke R, Kuhn L, Wintermeyer W. 1995. Codon-dependent conformational change of elongation factor Tu preceding GTP hydrolysis on the ribosome. EMBO J. 14:112613–19
    [Google Scholar]
  164. 164.
    Rundlet EJ, Holm M, Schacherl M, Natchiar SK, Altman RB et al. 2021. Structural basis of early translocation events on the ribosome. Nature 595:7869741–45
    [Google Scholar]
  165. 165.
    Saio T, Guan X, Rossi P, Economou A, Kalodimos CG. 2014. Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science 344:61841250494
    [Google Scholar]
  166. 166.
    Saio T, Kawagoe S, Ishimori K, Kalodimos CG 2018. Oligomerization of a molecular chaperone modulates its activity. eLife 7:e35731
    [Google Scholar]
  167. 167.
    Sanbonmatsu KY. 2012. Computational studies of molecular machines: the ribosome. Curr. Opin. Struct. Biol. 22:2168–74
    [Google Scholar]
  168. 168.
    Sanbonmatsu KY. 2019. Large-scale simulations of nucleoprotein complexes: ribosomes, nucleosomes, chromatin, chromosomes and CRISPR. Curr. Opin. Struct. Biol. 55:104–13
    [Google Scholar]
  169. 169.
    Sanbonmatsu KY, Joseph S, Tung CS 2005. Simulating movement of tRNA into the ribosome during decoding. PNAS 102:4415854–59
    [Google Scholar]
  170. 170.
    Satpati P, Åqvist J. 2014. Why base tautomerization does not cause errors in mRNA decoding on the ribosome. Nucleic Acids Res. 42:2012876–84
    [Google Scholar]
  171. 171.
    Schlick T, Zhu Q, Dey A, Jain S, Yan S, Laederach A 2021. To knot or not to knot: multiple conformations of the SARS-CoV-2 frameshifting RNA element. J. Am. Chem. Soc. 143:3011404–22
    [Google Scholar]
  172. 172.
    Schlick T, Zhu Q, Jain S, Yan S 2021. Structure-altering mutations of the SARS-CoV-2 frameshifting RNA element. Biophys. J. 120:61040–53
    [Google Scholar]
  173. 173.
    Schmeing TM, Huang KS, Kitchen DE, Strobel SA, Steitz TA. 2005. Structural insights into the roles of water and the 2′ hydroxyl of the P site tRNA in the peptidyl transferase reaction. Mol. Cell 20:3437–48
    [Google Scholar]
  174. 174.
    Schmeing TM, Voorhees RM, Kelley AC, Gao YG, Murphy FV et al. 2009. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326:5953688–94
    [Google Scholar]
  175. 175.
    Schröder GF, Grubmüller H. 2003. Maximum likelihood trajectories from single molecule fluorescence resonance energy transfer experiments. J. Chem. Phys. 119:189920–24
    [Google Scholar]
  176. 176.
    Schütz S, Sprangers R. 2020. Methyl TROSY spectroscopy: a versatile NMR approach to study challenging biological systems. Prog. Nuclear Magn. Reson. Spectrosc. 116:56–84
    [Google Scholar]
  177. 177.
    Senn HM, Thiel W. 2009. QM/MM methods for biomolecular systems. Angew. Chem. Int. Ed. 48:71198–229
    [Google Scholar]
  178. 178.
    Sharma PK, Xiang Y, Kato M, Warshel A. 2005. What are the roles of substrate-assisted catalysis and proximity effects in peptide bond formation by the ribosome?. Biochemistry 44:3411307–14
    [Google Scholar]
  179. 179.
    Shaw DE, Adams PJ, Azaria A, Bank JA, Batson B et al. 2021. Anton 3: twenty microseconds of molecular dynamics simulation before lunch. SC`21: Proceedings of the International Conference for High Performance Computing, Networking, Storage and Analysis1–11. New York: ACM
    [Google Scholar]
  180. 180.
    Singh AK, McGoldrick LL, Demirkhanyan L, Leslie M, Zakharian E, Sobolevsky AI. 2019. Structural basis of temperature sensation by the TRP channel TRPV3. Nat. Struct. Mol. Biol. 26:11994–98
    [Google Scholar]
  181. 181.
    Small MC, Lopes P, Andrade RB, MacKerell AD. 2013. Impact of ribosomal modification on the binding of the antibiotic telithromycin using a combined grand canonical Monte Carlo/molecular dynamics simulation approach. PLOS Comput. Biol. 9:6e1003113
    [Google Scholar]
  182. 182.
    Sothiselvam S, Liu B, Han W, Ramu H, Klepacki D et al. 2014. Macrolide antibiotics allosterically predispose the ribosome for translation arrest. PNAS 111:279804–9
    [Google Scholar]
  183. 183.
    Stark H, Rodnina MV, Rinke-Appel J, Brimacombe R, Wintermeyer W, Van Heel M. 1997. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389:6649403–6
    [Google Scholar]
  184. 184.
    Stryer L, Haugland RP. 1967. Energy transfer: a spectroscopic ruler. PNAS 58:2719–26
    [Google Scholar]
  185. 185.
    Su T, Cheng J, Sohmen D, Hedman R, Berninghausen O et al. 2017. The force-sensing peptide VemP employs extreme compaction and secondary structure formation to induce ribosomal stalling. eLife 6:e25642
    [Google Scholar]
  186. 186.
    Sudhakar S, Kazem M, Tobias A, Jachowski J, Bugiel M et al. 2021. Germanium nanospheres for ultraresolution picotensiometry of kinesin motors. Science 371:6530eabd9944
    [Google Scholar]
  187. 187.
    Tavakoli M, Jazani S, Sgouralis I, Heo W, Ishii K et al. 2020. Direct photon-by-photon analysis of time-resolved pulsed excitation data using Bayesian nonparametrics. Cell Rep. Phys. Sci. 1:11100234
    [Google Scholar]
  188. 188.
    Thiel W. 2014. Semiempirical quantum–chemical methods. Wiley Interdiscip. Rev. Comput. Mol. Sci. 4:2145–57
    [Google Scholar]
  189. 189.
    Tian P, Steward A, Kudva R, Su T, Shilling PJ et al. 2018. Folding pathway of an Ig domain is conserved on and off the ribosome. PNAS 115:48E11284–93
    [Google Scholar]
  190. 190.
    Trabuco LG, Schreiner E, Eargle J, Cornish P, Ha T et al. 2010. The role of L1 stalk–tRNA interaction in the ribosome elongation cycle. J. Mol. Biol. 402:4741–60
    [Google Scholar]
  191. 191.
    Trabuco LG, Villa E, Mitra K, Frank J, Schulten K 2008. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16:5673–83
    [Google Scholar]
  192. 192.
    Trovato F, O'Brien EP. 2016. Insights into cotranslational nascent protein behavior from computer simulations. Annu. Rev. Biophys. 45:345–69
    [Google Scholar]
  193. 193.
    Tuckerman M. 2010. Statistical Mechanics: Theory and Molecular Simulation Oxford, UK: Oxford Univ. Press
  194. 194.
    Uusitalo JJ, Ingólfsson HI, Marrink SJ, Faustino I 2017. Martini coarse-grained force field: extension to RNA. Biophys. J. 113:2246–56
    [Google Scholar]
  195. 195.
    Vaiana AC, Sanbonmatsu KY. 2009. Stochastic gating and drug–ribosome interactions. J. Mol. Biol. 386:3648–61
    [Google Scholar]
  196. 196.
    van Gunsteren WF, Berendsen HJ. 1990. Computer simulation of molecular dynamics: methodology, applications, and perspectives in chemistry. Angew. Chem. Int. Ed. 29:9992–1023
    [Google Scholar]
  197. 197.
    Volkhardt A, Grubmüller H. 2022. Estimating ruggedness of free-energy landscapes of small globular proteins from principal component analysis of molecular dynamics trajectories. Phys. Rev. E 105:4044404
    [Google Scholar]
  198. 198.
    Voorhees RM, Weixlbaumer A, Loakes D, Kelley AC, Ramakrishnan V. 2009. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16:5528–33
    [Google Scholar]
  199. 199.
    Vu QV, Jiang Y, Li MS, O'Brien EP. 2021. The driving force for co-translational protein folding is weaker in the ribosome vestibule due to greater water ordering. Chem. Sci. 12:3511851–57
    [Google Scholar]
  200. 200.
    Wallin G, Åqvist J. 2010. The transition state for peptide bond formation reveals the ribosome as a water trap. PNAS 107:51888–93
    [Google Scholar]
  201. 201.
    Wallin G, Kamerlin SCL, Åqvist J. 2013. Energetics of activation of GTP hydrolysis on the ribosome. Nat. Commun. 4:1733
    [Google Scholar]
  202. 202.
    Wang A, Levi M, Mohanty U, Whitford PC. 2022. Diffuse ions coordinate dynamics in a ribonucleoprotein assembly. J. Am. Chem. Soc. 144:219510–22
    [Google Scholar]
  203. 203.
    Wang X, Kirkpatrick JP, Launay HM, de Simone A, Häussinger D et al. 2019. Probing the dynamic stalk region of the ribosome using solution NMR. Sci. Rep. 9:13528
    [Google Scholar]
  204. 204.
    Warias M, Grubmüller H, Bock LV. 2020. tRNA dissociation from EF-Tu after GTP hydrolysis: primary steps and antibiotic inhibition. Biophys. J. 118:1151–61
    [Google Scholar]
  205. 205.
    Warshel A. 2003. Computer simulations of enzyme catalysis: methods, progress, and insights. Annu. Rev. Biophys. Biomol. Struct. 32:425–43
    [Google Scholar]
  206. 206.
    Waudby CA, Dobson CM, Christodoulou J. 2019. Nature and regulation of protein folding on the ribosome. Trends Biochem. Sci. 44:11914–26
    [Google Scholar]
  207. 207.
    Waudby CA, Włodarski T, Karyadi ME, Cassaignau AM, Chan SH et al. 2018. Systematic mapping of free energy landscapes of a growing filamin domain during biosynthesis. PNAS 115:399744–49
    [Google Scholar]
  208. 208.
    White KH, Orzechowski M, Fourmy D, Visscher K. 2011. Mechanical unfolding of the Beet Western Yellow Virus −1 frameshift signal. J. Am. Chem. Soc. 133:259775–82
    [Google Scholar]
  209. 209.
    Whitford PC, Blanchard SC, Cate JHD, Sanbonmatsu KY. 2013. Connecting the kinetics and energy landscape of tRNA translocation on the ribosome. PLOS Comput. Biol. 9:3e1003003
    [Google Scholar]
  210. 210.
    Whitford PC, Geggier P, Altman RB, Blanchard SC, Onuchic JN, Sanbonmatsu KY. 2010. Accommodation of aminoacyl-tRNA into the ribosome involves reversible excursions along multiple pathways. RNA 16:61196–204
    [Google Scholar]
  211. 211.
    Wilson DN, Arenz S, Beckmann R. 2016. Translation regulation via nascent polypeptide-mediated ribosome stalling. Curr. Opin. Struct. Biol. 37:123–33
    [Google Scholar]
  212. 212.
    Wruck F, Katranidis A, Nierhaus KH, Büldt G, Hegner M. 2017. Translation and folding of single proteins in real time. PNAS 114:22E4399–407
    [Google Scholar]
  213. 213.
    Wruck F, Tian P, Kudva R, Best RB, von Heijne G et al. 2021. The ribosome modulates folding inside the ribosomal exit tunnel. Commun. Biol. 4:523
    [Google Scholar]
  214. 214.
    Xu Y, Vanommeslaeghe K, Aleksandrov A, MacKerell AD Jr., Nilsson L. 2016. Additive CHARMM force field for naturally occurring modified ribonucleotides. J. Comput. Chem. 37:10896–912
    [Google Scholar]
  215. 215.
    Yang H, Bandarkar P, Horne R, Leite VB, Chahine J, Whitford PC. 2019. Diffusion of tRNA inside the ribosome is position-dependent. J. Chem. Phys. 151:8085102
    [Google Scholar]
  216. 216.
    Yang YI, Shao Q, Zhang J, Yang L, Gao YQ 2019. Enhanced sampling in molecular dynamics. J. Chem. Phys. 151:7070902
    [Google Scholar]
  217. 217.
    Ye W, Götz M, Celiksoy S, Tüting L, Ratzke C et al. 2018. Conformational dynamics of a single protein monitored for 24 h at video rate. Nano Lett. 18:106633–37
    [Google Scholar]
  218. 218.
    Zhang J, Pan X, Yan K, Sun S, Gao N, Sui SF 2015. Mechanisms of ribosome stalling by SecM at multiple elongation steps. eLife 4:e09684
    [Google Scholar]
  219. 219.
    Zhang K, Zheludev IN, Hagey RJ, Haslecker R, Hou YJ et al. 2021. Cryo-EM and antisense targeting of the 28-kDa frameshift stimulation element from the SARS-CoV-2 RNA genome. Nat. Struct. Mol. Biol. 28:9747–54
    [Google Scholar]
  220. 220.
    Zhang Y, Hong S, Ruangprasert A, Skiniotis G, Dunham CM. 2018. Alternative mode of E-site tRNA binding in the presence of a downstream mRNA stem loop at the entrance channel. Structure 26:3437–45.e3
    [Google Scholar]
  221. 221.
    Zhong Z, Yang L, Zhang H, Shi J, Vandana JJ et al. 2016. Mechanical unfolding kinetics of the SRV-1 gag-pro mRNA pseudoknot: possible implications for −1 ribosomal frameshifting stimulation. Sci. Rep. 6:39549
    [Google Scholar]
  222. 222.
    Zhu X, Lopes PE, MacKerell AD Jr. 2012. Recent developments and applications of the CHARMM force fields. Wiley Interdiscip. Rev. Comput. Mol. Sci. 2:1167–85
    [Google Scholar]
  223. 223.
    Zimmer MH, Niesen MJ, Miller TF III 2021. Force transduction creates long-ranged coupling in ribosomes stalled by arrest peptides. Biophys. J. 120:122425–35
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-111622-091147
Loading
/content/journals/10.1146/annurev-biophys-111622-091147
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error