Dynamic contact network between ribosomal subunits enables rapid large-scale rotation during spontaneous translocation

Nucleic Acids Research

Volumn 43, Issue 14, 2015, Pages 6747-6760

  Bock, Lars V ^a   Blau, Christian ^a   Vaiana, Andrea C ^a   Grubmüller, Helmut ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 23S; TRANSFER RNA;

CHEMISTRY; LARGE RIBOSOMAL SUBUNIT; MOLECULAR DYNAMICS; PROTEIN SYNTHESIS; ROTATION; SMALL RIBOSOMAL SUBUNIT; THERMODYNAMICS;

MOLECULAR DYNAMICS SIMULATION; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, LARGE; RIBOSOME SUBUNITS, SMALL; RNA, RIBOSOMAL, 23S; RNA, TRANSFER; ROTATION; THERMODYNAMICS;

EID: 84955290538     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv649     Document Type: Article

References (81)

1. 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.
2. 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.
3. Shoji, S., Walker, S. E. and Fredrick, K. (2006) Reverse translocation of tRNA in the ribosome. Mol. Cell, 24, 931-942.
4. Frank, J. and Agrawal, R. K. (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature, 406, 318-322.
5. Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M. and Frank, J. (2003) Locking and unlocking of ribosomal motions. Cell, 114, 123-134.
6. 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.
7. Julián, P., Konevega, A. L., Scheres, S. H. W., Lázaro, 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. U. S. A., 105, 16924-16927.
8. 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.
9. Zhang, W., Dunkle, J. A. and Cate, J. H. D. (2009) Structures of the ribosome in intermediate states of ratcheting. Science, 325, 1014-1017.
10. Ratje, A. H., Loerke, J., Mikolajka, A., Brünner, M., Hildebrand, P. W., Starosta, A. L., Dönhöfer, 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.
11. 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. D. (2011) Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science, 332, 981-984.
12. Agirrezabala, X., Liao, H. Y., Schreiner, E., Fu, J., Ortiz-Meoz, R. F., Schulten, K., Green, R. and Frank, J. (2012) Structural characterization of mRNA-tRNA translocation intermediates. Proc. Natl. Acad. Sci. U. S. A., 109, 6094-6099.
13. Zhou, J., Lancaster, L., Donohue, J. P. and Noller, H. F. (2013) Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science, 340, 1236086.
14. Tourigny, D. S., Fernández, I. S., Kelley, A. C. and Ramakrishnan, V. (2013) Elongation factor G bound to the ribosome in an intermediate state of translocation. Science, 340, 1235490.
15. Pulk, A. and Cate, J. H. D. (2013) Control of ribosomal subunit rotation by elongation factor G. Science, 340, 1235970.
16. 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. U. S. A., 110, 20994-20999.
17. Ramrath, D. J. F., Lancaster, L., Sprink, T., Mielke, T., Loerke, J., Noller, H. F. and Spahn, C. M. T. (2013) Visualization of two transfer RNAs trapped in transit during elongation factor G-mediated translocation. Proc. Natl. Acad. Sci. U. S. A., 110, 20964-20969.
18. Chen, J., Petrov, A., Tsai, A., O'Leary, S. E. and Puglisi, J. D. (2013) Coordinated conformational and compositional dynamics drive ribosome translocation. Nat. Struct. Mol. Biol., 20, 718-727.
19. Budkevich, T. V., Giesebrecht, J., Behrmann, E., Loerke, J., Ramrath, D. J. F., Mielke, T., Ismer, J., Hildebrand, P. W., Tung, C.-S., Nierhaus, K. H. et al. (2014) Regulation of the mammalian elongation cycle by subunit rolling: a eukaryotic-specific ribosome rearrangement. Cell, 158, 121-131.
20. 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.
21. 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.
22. 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. U. S. A., 106, 2571-2576.
23. Trabuco, L. G., Schreiner, E., Eargle, J., Cornish, P., Ha, T., Luthey-Schulten, Z. and Schulten, K. (2010) The role of L1 stalk-tRNA interaction in the ribosome elongation cycle. J. Mol. Biol., 402, 741-760.
24. Fischer, N., Konevega, A., Wintermeyer, W., Rodnina, M. and Stark, H. (2010) Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature, 466, 329-333.
25. Bock, L. V., Blau, C., Schröder, G. F., Davydov, I. I., Fischer, N., Stark, H., Rodnina, M. V., Vaiana, A. C. and Grubmüller, H. (2013) Energy barriers and driving forces in tRNA translocation through the ribosome. Nat. Struct. Mol. Biol., 20, 1390-1396.
26. Ning, W., Fei, J. and Gonzalez, R. L. (2014) The ribosome uses cooperative conformational changes to maximize and regulate the efficiency of translation. Proc. Natl. Acad. Sci. U. S. A., 111, 12073-12078.
27. Horan, L. H. and Noller, H. F. (2007) Intersubunit movement is required for ribosomal translocation. Proc. Natl. Acad. Sci. U. S. A., 104, 4881-4885.
28. Qin, P., Yu, D., Zuo, X. and Cornish, P. V. (2014) Structured mRNA induces the ribosome into a hyper-rotated state. EMBO Rep., 15, 185-190.
29. Schuwirth, B. S., Borovinskaya, M. A., Hau, C. W., Zhang, W., Vila-Sanjurjo, A., Holton, J. M. and Cate, J. H. D. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science, 310, 827-834.
30. Spahn, C. M. T., Gomez-Lorenzo, M. G., Grassucci, R. A., Jørgensen, R., Andersen, G. R., Beckmann, R., Penczek, P. A., Ballesta, J. P. G. and Frank, J. (2004) Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J., 23, 1008-1019.
31. Mohan, S., Donohue, J. P. and Noller, H. F. (2014) Molecular mechanics of 30S subunit head rotation. Proc. Natl. Acad. Sci. U. S. A., 111, 13325-13330.
32. Spirin, A. S. (1974) Structural transformations of ribosomes (dissociation, unfolding and disassembly). FEBS Lett., 40, S38-S47.
33. Gao, N., Zavialov, A. V., Li, W., Sengupta, J., Valle, M., Gursky, R. P., Ehrenberg, M. and Frank, J. (2005) Mechanism for the disassembly of the posttermination complex inferred from cryo-EM studies. Mol. Cell, 18, 663-674.
34. Cornish, P. V., Ermolenko, D. N., Noller, H. F. and Ha, T. (2008) Spontaneous intersubunit rotation in single ribosomes. Mol. Cell, 30, 578-588.
35. Frank, J., Verschoor, A., Li, Y., Zhu, J., Lata, R. K., Radermacher, M., Penczek, P., Grassucci, R., Agrawal, R. K. and Srivastava, S. (1995) A model of the translational apparatus based on a three-dimensional reconstruction of the Escherichia coli ribosome. Biochem. Cell Biol., 73, 757-765.
36. Gabashvili, I. S., Agrawal, R. K., Spahn, C. M., Grassucci, R. A., Svergun, D. I., Frank, J. and Penczek, P. (2000) Solution structure of the E. Coli 70S ribosome at 11.5 A resolution. Cell, 100, 537-549.
37. Gao, H., Sengupta, J., Valle, M., Korostelev, A., Eswar, N., Stagg, S. M., Roey, P. V., Agrawal, R. K., Harvey, S. C., Sali, A. et al. (2003) Study of the structural dynamics of the E. Coli 70S ribosome using real-space refinement. Cell, 113, 789-801.
38. Tama, F., Valle, M., Frank, J. and Brooks, C. L. (2003) Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy. Proc. Natl. Acad. Sci. U. S. A., 100, 9319-9323.
39. Cate, J. H., Yusupov, M. M., Yusupova, G. Z., Earnest, T. N. and Noller, H. F. (1999) X-ray crystal structures of 70S ribosome functional complexes. Science, 285, 2095-2104.
40. Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H. D. and Noller, H. F. (2001) Crystal structure of the ribosome at 5.5 angstrom resolution. Science, 292, 883-896.
41. Selmer, M., Dunham, C. M., Murphy, F. V., Weixlbaumer, A., Petry, S., Kelley, A. C., Weir, J. R. and Ramakrishnan, V. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935-1942.
42. Tung, C.-S. and Sanbonmatsu, K. Y. (2004) Atomic model of the Thermus thermophilus 70S ribosome developed in silico. Biophys. J., 87, 2714-2722.
43. Maiväli, U. and Remme, J. (2004) Definition of bases in 23S rRNA essential for ribosomal subunit association. RNA, 10, 600-604.
44. Liiv, A. and O'Connor, M. (2006) Mutations in the intersubunit bridge regions of 23 S rRNA. J. Biol. Chem., 281, 29850-29862.
45. Ali, I. K., Lancaster, L., Feinberg, J., Joseph, S. and Noller, H. F. (2006) Deletion of a conserved, central ribosomal intersubunit RNA bridge. Mol. Cell, 23, 865-874.
46. Kipper, K., Hetényi, C., Sild, S., Remme, J. and Liiv, A. (2009) Ribosomal intersubunit bridge B2a is involved in factor-dependent translation initiation and translational processivity. J. Mol. Biol., 385, 405-422.
47. Pulk, A., Maiväli, U. and Remme, J. (2006) Identification of nucleotides in E. Coli 16S rRNA essential for ribosome subunit association. RNA, 12, 790-796.
48. Zhou, J., Lancaster, L., Trakhanov, S. and Noller, H. F. (2012) Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA, 18, 230-240.
49. Cukras, A. R., Southworth, D. R., Brunelle, J. L., Culver, G. M. and Green, R. (2003) Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA: tRNA complex. Mol. Cell, 12, 321-328.
50. Komoda, T., Sato, N. S., Phelps, S. S., Namba, N., Joseph, S. and Suzuki, T. (2006) The A-site finger in 23 S rRNA acts as a functional attenuator for translocation. J. Biol. Chem., 281, 32303-32309.
51. Sergiev, P. V., Kiparisov, S. V., Burakovsky, D. E., Lesnyak, D. V., Leonov, A. A., Bogdanov, A. A. and Dontsova, O. A. (2005) The conserved A-site finger of the 23S rRNA: just one of the intersubunit bridges or a part of the allosteric communication pathway? J. Mol. Biol., 353, 116-123.
52. Liu, Q. and Fredrick, K. (2013) Contribution of intersubunit bridges to the energy barrier of ribosomal translocation. Nucleic. Acids Res., 41, 565-574.
53. Savelsbergh, A., Katunin, V. I., Mohr, D., Peske, F., Rodnina, M. V. and Wintermeyer, W. (2003) An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell, 11, 1517-1523.
54. Julián, P., Milon, P., Agirrezabala, X., Lasso, G., Gil, D., Rodnina, M. V. and Valle, M. (2011) The Cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLoS Biol., 9, e1001095.
55. Fagan, C. E., Dunkle, J. A., Maehigashi, T., Dang, M. N., Devaraj, A., Miles, S. J., Qin, D., Fredrick, K. and Dunham, C. M. (2013) Reorganization of an intersubunit bridge induced by disparate 16S ribosomal ambiguity mutations mimics an EF-Tu-bound state. Proc. Natl. Acad. Sci. U. S. A., 110, 9716-9721.
56. Wilson, D. N., Schluenzen, F., Harms, J. M., Yoshida, T., Ohkubo, T., Albrecht, R., Buerger, J., Kobayashi, Y. and Fucini, P. (2005) X-ray crystallography study on ribosome recycling: the mechanism of binding and action of RRF on the 50S ribosomal subunit. EMBO J., 24, 251-260.
57. Stanley, R. E., Blaha, G., Grodzicki, R. L., Strickler, M. D. and Steitz, T. A. (2010) The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70S ribosome. Nat. Struct. Mol. Biol., 17, 289-293.
58. Wang, L., Pulk, A., Wasserman, M. R., Feldman, M. B., Altman, R. B., Cate, J. H. D. and Blanchard, S. C. (2012) Allosteric control of the ribosome by small-molecule antibiotics. Nat. Struct. Mol. Biol., 19, 957-963.
59. Ermolenko, D. N., Spiegel, P. C., Majumdar, Z. K., Hickerson, R. P., Clegg, R. M. and Noller, H. F. (2007) The antibiotic viomycin traps the ribosome in an intermediate state of translocation. Nat. Struct. Mol. Biol., 14, 493-497.
60. Schlessinger, D., Mangiarotti, G. and Apirion, D. (1967) The formation and stabilization of 30S and 50S ribosome couples in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A., 58, 1782-1789.
61. 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.
62. Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D. et al. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845-854.
63. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A. and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
64. Berendsen, H. J. C., Grigera, J. R. and Straatsma, T. P. (1987) The missing term in effective pair potentials. J. Phys. Chem., 91, 6269-6271.
65. Joung, I. S. and Cheatham, T. E. (2008) Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B, 112, 9020-9041.
66. Blau, C. and Grubmuller, H. (2013) g contacts: fast contact search in bio-molecular ensemble data. Comput. Phys. Commun., 184, 2856-2859.
67. Espinosa, E., Molins, E. and Lecomte, C. (1998) Hydrogen bond strengths revealed by topological analyses of experimentally observed electron densities. Chem. Phys. Lett., 285, 170-173.
68. Amadei, A., Linssen, A. B. and Berendsen, H. J. (1993) Essential dynamics of proteins. Proteins, 17, 412-425.
69. Subramanian, A. R. and Dabbs, E. R. (1980) Functional studies on ribosomes lacking protein L1 from mutant Escherichia coli. Eur. J. Biochem., 112, 425-430.
70. Moazed, D. and Noller, H. F. (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature, 342, 142-148.
71. Jin, H., Kelley, A. C. and Ramakrishnan, V. (2011) Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc. Natl. Acad. Sci. U. S. A., 108, 15798-15803.
72. Cukras, A. R. and Green, R. (2005) Multiple effects of S13 in modulating the strength of intersubunit interactions in the ribosome during translation. J. Mol. Biol., 349, 47-59.
73. Schlitter, J. (1993) Estimation of absolute and relative entropies of macromolecules using the covariance matrix. Chem. Phys. Lett., 215, 617-621.
74. Borovinskaya, M. A., Pai, R. D., Zhang, W., Schuwirth, B. S., Holton, J. M., Hirokawa, G., Kaji, H., Kaji, A. and Cate, J. H. D. (2007) Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Mol. Biol., 14, 727-732.
75. Frank, J., Gao, H., Sengupta, J., Gao, N. and Taylor, D. J. (2007) The process of mRNA-tRNA translocation. Proc. Natl. Acad. Sci. U. S. A., 104, 19671-19678.
76. Shasmal, M., Chakraborty, B. and Sengupta, J. (2010) Intrinsic molecular properties of the protein-protein bridge facilitate ratchet-like motion of the ribosome. Biochem. Biophys. Res. Commun., 399, 192-197.
77. Rhodin, M. H. J. and Dinman, J. D. (2011) An extensive network of information flow through the B1b/c intersubunit bridge of the yeast ribosome. PLoS One, 6, e20048.
78. Allen, G. S., Zavialov, A., Gursky, R., Ehrenberg, M. and Frank, J. (2005) The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell, 121, 703-712.
79. Klaholz, B. P., Myasnikov, A. G. and Heel, M. V. (2004) Visualization of release factor 3 on the ribosome during termination of protein synthesis. Nature, 427, 862-865.
80. Noeske, J., Wasserman, M. R., Terry, D. S., Altman, R. B., Blanchard, S. C. and Cate, J. H. D. (2015) High-resolution structure of the Escherichia coli ribosome. Nat. Struct. Mol. Biol., 22, 336-341.
81. Aitken, C. E. and Puglisi, J. D. (2010) Following the intersubunit conformation of the ribosome during translation in real time. Nat. Struct. Mol. Biol., 17, 793-800.