Energy barriers and driving forces in tRNA translocation through the ribosome

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

Frank, J. & Agrawal, R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318–322 (2000).

Tama, F., Valle, M., Frank, J. & Brooks, C.L. Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy. Proc. Natl. Acad. Sci. USA 100, 9319–9323 (2003).

Valle, M. et al. Locking and unlocking of ribosomal motions. Cell 114, 123–134 (2003).

Konevega, A.L. et al. Spontaneous reverse movement of mRNA-bound tRNA through the ribosome. Nat. Struct. Mol. Biol. 14, 318–324 (2007).

Shoji, S., Walker, S.E. & Fredrick, K. Reverse translocation of tRNA in the ribosome. Mol. Cell 24, 931–942 (2006).

Spirin, A.S. Energetics of the ribosome. Prog. Nucleic Acid Res. Mol. Biol. 21, 39–62 (1978).

Noller, H.F., Yusupov, M.M., Yusupova, G.Z., Baucom, A. & Cate, J.H. Translocation of tRNA during protein synthesis. FEBS Lett. 514, 11–16 (2002).

Liu, Q. & Fredrick, K. Contribution of intersubunit bridges to the energy barrier of ribosomal translocation. Nucleic Acids Res. 41, 565–574 (2013).

Fischer, N., Konevega, A.L., Wintermeyer, W., Rodnina, M.V. & Stark, H. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466, 329–333 (2010).

Agirrezabala, X. et al. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 32, 190–197 (2008).

Fei, J., Kosuri, P., MacDougall, D. & Gonzalez, R. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell 30, 348–359 (2008).

Julián, P. et al. Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc. Natl. Acad. Sci. USA 105, 16924–16927 (2008).

Munro, J.B., Altman, R.B., O'Connor, N. & Blanchard, S.C. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25, 505–517 (2007).

Cornish, P.V. et al. Following movement of the L1 stalk between three functional states in single ribosomes. Proc. Natl. Acad. Sci. USA 106, 2571–2576 (2009).

Trabuco, L.G. et al. The role of L1 stalk-tRNA interaction in the ribosome elongation cycle. J. Mol. Biol. 402, 741–760 (2010).

Sanbonmatsu, K.Y., Joseph, S. & Tung, C.-S. Simulating movement of tRNA into the ribosome during decoding. Proc. Natl. Acad. Sci. USA 102, 15854–15859 (2005).

Zhang, W., Dunkle, J.A. & Cate, J.H.D. Structures of the ribosome in intermediate states of ratcheting. Science 325, 1014–1017 (2009).

Caulfield, T.R., Devkota, B. & Rollins, G.C. Examinations of tRNA range of motion using simulations of cryo-EM microscopy and X-ray data. J. Biophys. 2011, 219515 (2011).

Tama, F., Miyashita, O. & Brooks, C.L. Flexible multi-scale fitting of atomic structures into low-resolution electron density maps with elastic network normal mode analysis. J. Mol. Biol. 337, 985–999 (2004).

Whitford, P.C. et al. An all-atom structure-based potential for proteins: bridging minimal models with all-atom empirical forcefields. Proteins 75, 430–441 (2009).

Tan, R.K.Z., Devkota, B. & Harvey, S.C. YUP.SCX: coaxing atomic models into medium resolution electron density maps. J. Struct. Biol. 163, 163–174 (2008).

Schröder, G.F., Brunger, A. & Levitt, M. Combining efficient conformational sampling with a deformable elastic network model facilitates structure refinement at low resolution. Structure 15, 1630–1641 (2007).

Ahmed, A. & Tama, F. Consensus among multiple approaches as a reliability measure for flexible fitting into cryo-EM data. J. Struct. Biol. 182, 67–77 (2013).

Orzechowski, M. & Tama, F. Flexible fitting of high-resolution X-ray structures into cryoelectron microscopy maps using biased molecular dynamics simulations. Biophys. J. 95, 5692–5705 (2008).

Dunkle, J.A. et al. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981–984 (2011).

de Groot, B.L., Engel, A. & Grubmuller, H. The structure of the aquaporin-1 water channel: a comparison between cryo-electron microscopy and X-ray crystallography. J. Mol. Biol. 325, 485–493 (2003).

Schuwirth, B.S. et al. Structures of the bacterial ribosome at 3.5 A resolution. Science 310, 827–834 (2005).

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

Rodnina, M.V., Savelsbergh, A., Katunin, V.I. & Wintermeyer, W. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37–41 (1997).

Pan, D., Kirillov, S.V. & Cooperman, B.S. Kinetically competent intermediates in the translocation step of protein synthesis. Mol. Cell 25, 519–529 (2007).

Fei, J., Richard, A.C., Bronson, J.E. & Gonzalez, R.L. Transfer RNA–mediated regulation of ribosome dynamics during protein synthesis. Nat. Struct. Mol. Biol. 18, 1043–1051 (2011).

Munro, J.B., Sanbonmatsu, K.Y., Spahn, C.M. & Blanchard, S.C. Navigating the ribosome's metastable energy landscape. Trends Biochem. Sci. 34, 390–400 (2009).

Chen, C. et al. Single-molecule fluorescence measurements of ribosomal translocation dynamics. Mol. Cell 42, 367–377 (2011).

Blanchard, S.C., Kim, H.D., Gonzalez, R.L. Jr., Puglisi, J.D. & Chu, S. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA 101, 12893–12898 (2004).

Rhodin, M.H.J. & Dinman, J.D. An extensive network of information flow through the B1b/c intersubunit bridge of the yeast ribosome. PLoS ONE 6, e20048 (2011).

Subramanian, A.R. & Dabbs, E.R. Functional studies on ribosomes lacking protein L1 from mutant Escherichia coli. Eur. J. Biochem. 112, 425–430 (1980).

Pan, D., Kirillov, S., Zhang, C.M., Hou, Y.M. & Cooperman, B.S. Rapid ribosomal translocation depends on the conserved 18–55 base pair in P-site transfer RNA. Nat. Struct. Mol. Biol. 13, 354–359 (2006).

Rhodin, M.H.J. & Dinman, J.D. A flexible loop in yeast ribosomal protein L11 coordinates P-site tRNA binding. Nucleic Acids Res. 38, 8377–8389 (2010).

Frauenfelder, H., Sligar, S.G. & Wolynes, P.G. The energy landscapes and motions of proteins. Science 254, 1598–1603 (1991).

Yusupov, M.M. et al. Crystal structure of the ribosome at 5.5 Å resolution. Science 292, 883–896 (2001).

Gao, Y.G. et al. The structure of the ribosome with elongation factor F trapped in the posttranslocational state. Science 326, 694–699 (2009).

Budkevich, T. et al. Structure and dynamics of the mammalian ribosomal pretranslocation complex. Mol. Cell 44, 214–224 (2011).

Grishaev, A., Ying, J., Canny, M., Pardi, A. & Bax, A. Solution structure of tRNA Val from refinement of homology model against residual dipolar coupling and SAXS data. J. Biomol. NMR 42, 99–109 (2008).

Hess, B., Kutzner, C., van der Spoel, D. & Lindahl, E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435–447 (2008).

Hornak, V. et al. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712–725 (2006).