Computational studies of molecular machines: The ribosome

Current Opinion in Structural Biology

Volumn 22, Issue 2, 2012, Pages 168-174

  Sanbonmatsu, Karissa Y ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINOPURINE; GENTAMICIN; MESSENGER RNA; PEPTIDYLTRANSFERASE; RIBOSOME RNA; TRANSFER RNA;

ACID BASE BALANCE; BINDING SITE; BIOCATALYSIS; CALCULATION; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CYTOARCHITECTURE; ENTROPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE DELETION; HYDROGEN BOND; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MONTE CARLO METHOD; MUTATIONAL ANALYSIS; PHASE TRANSITION; PHENOTYPE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROCESS MODEL; REACTION ANALYSIS; REVIEW; RIBOSOMAL FRAMESHIFTING; RIBOSOME; RIBOSOME SUBUNIT; SOLVATION; STATIC ELECTRICITY; STEREOCHEMISTRY; STOP CODON; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

COMPUTATIONAL BIOLOGY; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; RIBOSOMES;

EID: 84861765128     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2012.01.008     Document Type: Review

References (74)

1. Brimacombe R., Atmadja J., Stiege W., Schuler D. A detailed model of the three-dimensional structure of Escherichia coli 16 s ribosomal rna in situ in the 30 s subunit. J Mol Biol 1988, 199:115-136.
2. Malhotra A., Tan R.K., Harvey S.C. Prediction of the three-dimensional structure of escherichia coli 30s ribosomal subunit: a molecular mechanics approach. Proc Natl Acad Sci U S A 1990, 87:1950-1954.
3. Easterwood T.R., Major F., Malhotra A., Harvey S.C. Orientations of transfer rna in the ribosomal a and p sites. Nucleic Acids Res 1994, 22:3779-3786.
4. Malhotra A., Harvey S.C. A quantitative model of the escherichia coli 16 s rna in the 30 s ribosomal subunit. J Mol Biol 1994, 240:308-340.
5. VanLoock M.S., Agrawal R.K., Gabashvili I.S., Qi L., Frank J., Harvey S.C. Movement of the decoding region of the 16 s ribosomal rna accompanies trna translocation. J Mol Biol 2000, 304:507-515.
6. Fink D.L., Chen R.O., Noller H.F., Altman R.B. Computational methods for defining the allowed conformational space of 16s rrna based on chemical footprinting data. RNA 1996, 2:851-866.
7. Tung C.S., Joseph S., Sanbonmatsu K.Y. All-atom homology model of the escherichia coli 30s ribosomal subunit. Nat Struct Biol 2002, 9:750-755.
8. Tung C.S., Sanbonmatsu K.Y. Atomic model of the Thermus thermophilus 70s ribosome developed in silico. Biophys J 2004, 87:2714-2722.
9. Sanbonmatsu K.Y., Joseph S. Understanding discrimination by the ribosome: stability testing and groove measurement of codon-anticodon pairs. J Mol Biol 2003, 328:33-47.
10. Li W., Ma B., Shapiro B. Binding interactions between the core central domain of 16s rrna and the ribosomal protein s15 determined by molecular dynamics simulations. Nucleic Acids Res 2003, 31:629-638.
11. Chacon P., Tama F., Wriggers W. Mega-dalton biomolecular motion captured from electron microscopy reconstructions. J Mol Biol 2003, 326:485-492.
12. Baker N., Sept D., Joseph S., Holst M., McCammon J. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 2001, 98:10037-10041.
13. Sanbonmatsu K.Y., Joseph S., Tung C.S. Simulating movement of trna into the ribosome during decoding. Proc Natl Acad Sci U S A 2005, 102:15854-15859.
14. Vaiana A.C., Sanbonmatsu K.Y. Stochastic gating and drug-ribosome interactions. J Mol Biol 2009, 386:648-661.
15. Whitford P.C., Geggier P., Altman R.B., Blanchard S.C., Onuchic J.N., Sanbonmatsu K.Y. Accommodation of aminoacyl-trna into the ribosome involves reversible excursions along multiple pathways. RNA 2010, 16:1196-1204.
16. 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 U S A 2003, 100:9319-9323.
17. Wang Y., Rader A.J., Bahar I., Jernigan R.L. Global ribosome motions revealed with elastic network model. J Struct Biol 2004, 147:302-314.
18. Gorba C., Miyashita O., Tama F. Normal-mode flexible fitting of high-resolution structure of biological molecules toward one-dimensional low-resolution data. Biophys J 2008, 94:1589-1599.
19. Mitra K., Schaffitzel C., Shaikh T., Tama F., Jenni S., Brooks C.L., Ban N., Frank J. Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 2005, 438:318-324.
20. Kurkcuoglu O., Doruker P., Sen T.Z., Kloczkowski A., Jernigan R.L. The ribosome structure controls and directs mrna entry, translocation and exit dynamics. Phys Biol 2008, 5:046005.
21. Baxter-Roshek J.L., Petrov A.N., Dinman J.D. Optimization of ribosome structure and function by rrna base modification. PLoS One 2007, 2:e174.
22. Meskauskas A., Dinman J.D. Ribosomal protein l3: gatekeeper to the a site. Mol Cell 2007, 25:877-888.
23. Rakauskaite R., Dinman J.D. Mutations of highly conserved bases in the peptidyltransferase center induce compensatory rearrangements in yeast ribosomes. RNA 2011, 17:855-864.
24. Burakovsky D.E., Sergiev P.V., Steblyanko M.A., Konevega A.L., Bogdanov A.A., Dontsova O.A. The structure of helix 89 of 23s rrna is important for peptidyl transferase function of escherichia coli ribosome. FEBS Lett 2011, 585:3073-3078.
25. Burakovsky D.E., Sergiev P.V., Steblyanko M.A., Kubarenko A.V., Konevega A.L., Bogdanov A.A., Rodnina M.V., Dontsova O.A. Mutations at the accommodation gate of the ribosome impair rf2-dependent translation termination. RNA 2010, 16:1848-1853.
26. Trabuco L.G., Schreiner E., Eargle J., Cornish P., Ha T., Luthey-Schulten Z., Schulten K. The role of l1 stalk-trna interaction in the ribosome elongation cycle. J Mol Biol 2010, 402:741-760.
27. Trabuco L.G., Harrison C.B., Schreiner E., Schulten K. Recognition of the regulatory nascent chain tnac by the ribosome. Structure 2010, 18:627-637.
28. Gumbart J., Trabuco L.G., Schreiner E., Villa E., Schulten K. Regulation of the protein-conducting channel by a bound ribosome. Structure 2009, 17:1453-1464.
29. Whitford P.C., Onuchic J.N., Sanbonmatsu K.Y. Connecting energy landscapes with experimental rates for aminoacyl-trna accommodation in the ribosome. J Am Chem Soc 2010, 132:13170-13171.
30. Trylska J., Tozzini V., McCammon J.A. Exploring global motions and correlations in the ribosome. Biophys J 2005, 89:1455-1463.
31. Trylska J., Konecny R., Tama F., Brooks C.L., McCammon J.A. Ribosome motions modulate electrostatic properties. Biopolymers 2004, 74:423-431.
32. Trylska J., McCammon J.A., Brooks C.L. Exploring assembly energetics of the 30s ribosomal subunit using an implicit solvent approach. J Am Chem Soc 2005, 127:11125-11133.
33. Zhang Z., Sanbonmatsu K.Y., Voth G.A. Key intermolecular interactions in the E. coli 70s ribosome revealed by coarse-grained analysis. J Am Chem Soc 2011, 133:16828-16838.
34. Trobro S., Aqvist J. Mechanism of peptide bond synthesis on the ribosome. Proc Natl Acad Sci U S A 2005, 102:12395-12400.
35. Sharma P.K., Xiang Y., Kato M., Warshel A. What are the roles of substrate-assisted catalysis and proximity effects in peptide bond formation by the ribosome?. Biochemistry 2005, 44:11307-11314.
36. Adamczyk A.J., Warshel A. Converting structural information into an allosteric-energy-based picture for elongation factor tu activation by the ribosome. Proc Natl Acad Sci U S A 2011, 108:9827-9832.
37. Wieden H.J., Mercier E., Gray J., Steed B., Yawney D. A combined molecular dynamics and rapid kinetics approach to identify conserved three-dimensional communication networks in elongation factor tu. Biophys J 2010, 99:3735-3743.
38. Wallin G., Aqvist J. The transition state for peptide bond formation reveals the ribosome as a water trap. Proc Natl Acad Sci U S A 2010, 107:1888-1893.
39. Trobro S., Aqvist J. Mechanism of the translation termination reaction on the ribosome. Biochemistry 2009, 48:11296-11303.
40. Almlof M., Ander M., Aqvist J. Energetics of codon-anticodon recognition on the small ribosomal subunit. Biochemistry 2007, 46:200-209.
41. Sanbonmatsu K.Y. Energy landscape of the ribosomal decoding center. Biochimie 2006, 88:1053-1059.
42. Romanowska J., Setny P., Trylska J. Molecular dynamics study of the ribosomal a-site. J Phys Chem B 2008, 112:15227-15243.
43. Vaiana A.C., Westhof E., Auffinger P. A molecular dynamics simulation study of an aminoglycoside/a-site rna complex: conformational and hydration patterns. Biochimie 2006, 88:1061-1073.
44. Kaul M., Barbieri C.M., Pilch D.S. Aminoglycoside-induced reduction in nucleotide mobility at the ribosomal rna a-site as a potentially key determinant of antibacterial activity. J Am Chem Soc 2006, 128:1261-1271.
45. Dlugosz M., Trylska J. Aminoglycoside association pathways with the 30s ribosomal subunit. J Phys Chem B 2009, 113:7322-7330.
46. Besseova I., Reblova K., Leontis N.B., Sponer J. Molecular dynamics simulations suggest that rna three-way junctions can act as flexible rna structural elements in the ribosome. Nucleic Acids Res 2010, 38:6247-6264.
47. Reblova K., Razga F., Li W., Gao H., Frank J., Sponer J. Dynamics of the base of ribosomal a-site finger revealed by molecular dynamics simulations and cryo-em. Nucleic Acids Res 2010, 38:1325-1340.
48. Kirmizialtin S., Ganesan V., Makarov D.E. Translocation of a beta-hairpin-forming peptide through a cylindrical tunnel. J Chem Phys 2004, 121:10268-10277.
49. Ziv G., Haran G., Thirumalai D. Ribosome exit tunnel can entropically stabilize alpha-helices. Proc Natl Acad Sci U S A 2005, 102:18956-18961.
50. Contreras Martinez L.M., Martinez-Veracoechea F.J., Pohkarel P., Stroock A.D., Escobedo F.A., DeLisa M.P. Protein translocation through a tunnel induces changes in folding kinetics: a lattice model study. Biotechnol Bioeng 2006, 94:105-117.
51. Ishida H., Hayward S. Path of nascent polypeptide in exit tunnel revealed by molecular dynamics simulation of ribosome. Biophys J 2008, 95:5962-5973.
52. Petrone P.M., Snow C.D., Lucent D., Pande V.S. Side-chain recognition and gating in the ribosome exit tunnel. Proc Natl Acad Sci U S A 2008, 105:16549-16554.
53. Lucent D., Snow C.D., Aitken C.E., Pande V.S. Non-bulk-like solvent behavior in the ribosome exit tunnel. PLoS Comput Biol 2010, 6:e1000963.
54. Ge X., Roux B. Absolute binding free energy calculations of sparsomycin analogs to the bacterial ribosome. J Phys Chem B 2010, 114:9525-9539.
55. Orzechowski M., Tama F. Flexible fitting of high-resolution x-ray structures into cryoelectron microscopy maps using biased molecular dynamics simulations. Biophys J 2008, 95:5692-5705.
56. Trabuco L.G., Villa E., Mitra K., Frank J., Schulten K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 2008, 16:673-683.
57. Villa E., Sengupta J., Trabuco L.G., LeBarron J., Baxter W.T., Shaikh T.R., Grassucci R.A., Nissen P., Ehrenberg M., Schulten K., Frank J. Ribosome-induced changes in elongation factor tu conformation control gtp hydrolysis. Proc Natl Acad Sci U S A 2009, 106:1063-1068.
58. 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. Head swivel on the ribosome facilitates translocation by means of intra-subunit trna hybrid sites. Nature 2010, 468:713-716.
59. Whitford P.C., Ahmed A., Yu Y., Hennelly S.P., Tama F., Spahn C.M.T., Onuchic J.N., Sanbonmatsu K.Y. Excited states of ribosome translocation revealed through integrative molecular modeling. Proc Natl Acad Sci U S A 2011, 108:18943-18948.
60. Li W., Frank J. Transfer rna in the hybrid p/e state: correlating molecular dynamics simulations with cryo-em data. Proc Natl Acad Sci U S A 2007, 104:16540-16545.
61. 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.
62. Ahmed A, Whitford PC, Sanbonmatsu KY, Tama F: Consensus among flexible fitting approaches improves the interpretation of cryo-em data. J Struct Biol 2011. [Epub ahead of print].
63. Korostelev A., Noller H.F. Analysis of structural dynamics in the ribosome by tls crystallographic refinement. J Mol Biol 2007, 373:1058-1070.
64. Demeshkina N., Jenner L., Yusupova G., Yusupov M. Interactions of the ribosome with mrna and trna. Curr Opin Struct Biol 2010, 20:325-332.
65. Ben-Shem A., Garreau de Loubresse N., Melnikov S., Jenner L., Yusupova G., Yusupov M. The structure of the eukaryotic ribosome at 3.0 a resolution. Science 2011, 334:1524-1529.
66. Dunkle J.A., Wang L., Feldman M.B., Pulk A., Chen V.B., Kapral G.J., Noeske J., Richardson J.S., Blanchard S.C., Cate J.H. Structures of the bacterial ribosome in classical and hybrid states of trna binding. Science 2011, 332:981-984.
67. Dunkle J.A., Cate J.H. Ribosome structure and dynamics during translocation and termination. Annu Rev Biophys 2010, 39:227-244.
68. Blanchard S.C. Single-molecule observations of ribosome function. Curr Opin Struct Biol 2009, 19:103-109.
69. Geggier P., Dave R., Feldman M.B., Terry D.S., Altman R.B., Munro J.B., Blanchard S.C. Conformational sampling of aminoacyl-trna during selection on the bacterial ribosome. J Mol Biol 2010, 399:576-595.
70. Munro J.B., Altman R.B., Tung C.S., Sanbonmatsu K.Y., Blanchard S.C. A fast dynamic mode of the ef-g-bound ribosome. EMBO J 2010, 29:770-781.
71. Munro J.B., Altman R.B., Tung C.S., Cate J.H., Sanbonmatsu K.Y., Blanchard S.C. Spontaneous formation of the unlocked state of the ribosome is a multistep process. Proc Natl Acad Sci U S A 2010, 107:709-714.
72. Munro J.B., Vaiana A., Sanbonmatsu K.Y., Blanchard S.C. A new view of protein synthesis: mapping the free energy landscape of the ribosome using single-molecule fret. Biopolymers 2008, 89:565-577.
73. Sharma A.K., Chowdhury D. Stochastic theory of protein synthesis and polysome: ribosome profile on a single mrna transcript. J Theor Biol 2011, 289:36-46.
74. Sharma A.K., Chowdhury D. Distribution of dwell times of a ribosome: effects of infidelity, kinetic proofreading and ribosome crowding. Phys Biol 2011, 8:026005.