The ribosome at higher resolution - The donut takes shape

Current Opinion in Structural Biology

Volumn 7, Issue 2, 1997, Pages 266-272

  Frank, Joachim ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RNA; TRANSFER RNA;

CELL ULTRASTRUCTURE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; RIBOSOME; STRUCTURE ACTIVITY RELATION;

EID: 0030990359     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(97)80035-8     Document Type: Article

References (61)

1. Frank J, Zhu J, Penczek P, Li Y, Srivastava S, Verschoor A, Radermacher M, Grassucci R, Lata RK, Agrawal RK: A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature 1995, 376:441-444. The 70S ribosome from E. coli is reconstructed from 4300 projections of randomly oriented particles embedded in ice, with a resolution of 25 Å as determined by the differential phase residual criterion. An energy-filtering microscope is used in the data collection. The orientations of projections are found by reference to an earlier lower resolution reconstruction, and the 3D map is corrected for the effects of the contrast transfer function. The model is presented with a hypothetical interpretation of the channels and tunnels observed in terms of pathways of mRNA and nascent polypeptide chain, as well as with placement of A- and P-site tRNAs.
2. Stark H, Müller F, Orlova EV, Schatz M, Dube P, Erdemir T, Zemlin F, Brimacombe R, Van Heel M: The 70S Escherichia coli ribosome at 23 Å resolution: fitting the ribosomal RNA. Structure 1995, 3:815-821. The 70S ribosome from E. coli is reconstructed from 2447 projections of single particles embedded in ice, which are classified into groups and averaged. Orientations are found by applying a common-lines method to these class averages. The resolution of the reconstruction is given as 23 Å, as determined by the Fourier shell correlation criterion. No attempt is made to correct the contrast transfer function. The model is presented with a plausible placement of A- and P-site tRNAs.
3. Lata KR, Agrawal RK, Penczek P, Grassucci R, Zhu J, Frank J: Three-dimensional reconstruction of the Escherichia coli 30S ribosomal subunit in ice. J Mol Biol 1996, 262:43-52. This study reveals a large conformational change in the 30S subunit as it associates during initiation with the 50S subunit. During the process, the channel through the subunit neck appears to form. If this channel is indeed the conduit for incoming mRNA, then the channel formation would be tantamount to the capturing of mRNA.
4. Verschoor A, Srivastava S, Grassucci R, Frank J: Native 3D structure of eukaryotic 80S ribosome: morphological homology with the E. coli 70S ribosome. J Cell Biol 1996, 113:495-505.
5. Liljas A, Garber M: Ribosomal proteins and elongation factors. Curr Opin Struct Biol 1995, 5:721-727.
6. Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Reshetnikova L, Clark BFC, Nyborg J: Crystal structure of the ternary complex of Phe-tRNA(phe), EF-Tu, and a GTP analog. Science 1995, 270:1464-1472. This work uncovers the remarkable resemblance between the ternary complex and elongation factor G, suggesting that both moieties compete for the same binding site on the ribosome. The large size (120 Å) should make it easy to localize these complexes when bound on the ribosome.
7. Kawashima T, Bertet-Colominas C, Wulff M, Cusack S, Leberman R: The structure of the Escherichia coli EF-T-EF-Ts complex at 2.5 Å resolution. Nature 1996, 379:511-518.
8. Nierhaus KH: An elongation factor turn-on. Nature 1996, 379:491-492.
9. Moore P: Molecular mimicry in protein synthesis? Science 1995, 270:1453-1454.
10. Abel K, Jurnak F: A complex profile of protein elongation: translating chemical energy into molecular movement Structure 1996, 15:229-238.
11. Stuhrmann HB, Burkhardt N, Diedrich G, Jünemann R, Meerwinck W, Schmitt M, Wadzack J, Willumeit R, Zhao J, Nierhaus KH: Proton and deuteron spin targets in biological structure research. Nucl Instrum Meth Phys Res A 1995, 356:124-132.
12. 2·mRNA complex was found to move within the subunit-subunit interface space by a distance of 12 Å, closely matching the linear size of one codon (10 Å).
13. Malhotra A, Harvey SC: A quantitative model of the Escherichia coli 16S RNA in the 30S ribosomal subunit. J Mol Biol 1994, 240:308-340.
14. Yonath A, Leonard KR, Wittmann HG: A tunnel in the large ribosomal subunit revealed by three-dimensional image reconstruction. Science 1987, 236:813-817.
15. Berkovitch-Yellin Z, Bennett WS, Yonath A: Aspects in structural studies on ribosomes. CRC Crit Rev Biochem Mol Biol 1992, 27:403-444. A detailed review that summarizes more than a decade of crystallography and 3D reconstructions of ribosomes.
16. Frank J, Verschoor A, Li Y, Zhu J, Penczek P, Lata RK, Radermacher M, Penczek P, Grassucci R, Agrawal RK, Srivastava S: A model of the translational apparatus based on three-dimensional reconstruction of the E. coli ribosome. Biochem Cell Biol 1995, 73:757-765.
17. Yonath A, Berkovitch-Yellin Z: Hollows, voids, gaps and tunnels in the ribosome. Curr Opin Struct Biol 1992, 3:175-181.
18. Avila-Sakar AJ, Guan T-L, Arad T, Schmid MF, Loke TW, Yonath A, Piefke J, Franceschi F, Chiu W: Electron cryomicroscopy of Bacillus stearothermophilus 50S ribosomal subunits crystallized on phospholipid monolayers. J Mol Biol 1994, 239:689-697.
19. Frank J: Three-dimensional Electron Microscopy of Macromolecular Assemblies, edn 1. San Diego: Academic Press; 1996.
20. Radermacher M, Wagenknecht T, Verschoor A, Frank J: Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit J Microsc 1987, 146:113-136.
21. Van Heel M: Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 1987, 21:111-124.
22. Penczek P, Zhu J, Frank J: A common-lines based method for determining orientations for N > 3 particle projections simultaneously. Ultramicroscopy 1996, 63:365-385.
23. Radermacher M, Rao V, Grassucci R, Frank J, Timerman AP, Fleischer S, Wagenknecht T: Cryo-electron microscopy and three- dimensional reconstruction of the calcium release channel/ryanodine receptor from skeletal muscle. J Cell Biol 1994, 127:411-423.
24. Serysheva II, Orlova EV, Chiu W, Sherman MB, Hamilton S, Van Heel M: Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nat Struct Biol 1995, 2:18-24.
25. Moore P: Ribosomes seen through a glass less darkly. Structure 1995, 3:851-852.
26. Zimmermann RA: Ins and outs of the ribosome. Nature 1995, 376:391-392.
27. Noller HF, Hoffarth V, Zimniak L: Unusual resistance of peptidyl transferase to protein extraction procedures. Science 1992, 256:1416-1419.
28. Hardesty B, Odom O, Kudlicki W, Kramer G: Extension and folding of nascent peptides on ribosomes. In The Translational Apparatus. Edited by Nierhaus KH, Subramanian AR, Erdmann VA, Franceschi F, Wittmann-Liebold B. Belgium: Plenum Press; 1993:347-358.
29. Zhu J, Penczek PA, Schröder R, Frank J: Three-dimensional reconstruction with contrast transfer function correction from energy-filtered cryo-electron micrographs: procedure and application to the 70S Escherichia coli ribosome. J Struct Biol 1997, in press.
30. Bernabeu C, Lake JA: Nascent polypeptide chains emerge from the exit domain of the large ribosomal subunit: immune mapping of the nascent chain. Proc Natl Acad Sci USA 1982, 79:3111-3115.
31. Stewart PL, Fuller SD, Burnett RM: Difference imaging of adenovirus: bridging the resolution gap between X-ray crystallography and electron microscopy. EMBO J 1993, 12:2589-2599.
32. Rayment I, Holden H, Whittaker M, Yohn C, Lorenz M, Holmes K, Milligan R: Structure of the actin-myosin complex and its implications for muscle contraction. Science 1993, 261:58-65.
33. Baker TS, Johnson JE: Low resolution meets high: towards a resolution continuum. Curr Opin Struct Biol 1996, 6:585-594.
34. Brimacombe R: The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur J Biochem 1995, 230:365-385. This is an excellent expose on the current state of knowledge about the ribosomal RNA structure and its functional centers. An argument is presented in favor of the S-model for the A-site and P-site tRNA configuration.
35. Thygesen J, Krumbholz S, Levin I, Zaytzev-Bashan A, Harms J, Bartels H, Schlünzen F, Hansen HAS, Bennett WS, Volkmann N, Agmon I et al.: Ribosomal crystallography: from crystal growth to initial phasing. J Cryst Growth 1996, 168:308-323. The article summarizes the efforts that have gone into ribosome crystallography and the present state of the experiments. Phasing still faces numerous hurdles because of the weakness of heavy atom scattering relative to the scattering of the whole ribosome, and because of the lack of crystal isomorphism.
36. Berriman JA, Unwin PNT: Analysis of transient structures by cryo-electron microscopy combined with rapid mixing of spray droplets. Ultramicroscopy 1994, 56:241-252.
37. Phe. Under these conditions, all three (A-, P-, and E-) sites are known to be occupied. The difference mass (after subtraction of the control reconstruction) is interpreted in terms of an arrangement of three tRNAs.
38. Lim VI, Vanclovas C: Codon-anticodon pairing. A model for interacting codon-anticodon duplexes located at the ribosomal A- and P-sites. FEBS Lett 1992, 313:133-137.
39. Lim VI: Analysis of interactions between the codon-anticodon duplexes within the ribosome: their role in translation. J Mol Biol 1997, in press. A viable atomic model of the complex tRNA·mRNA·tRNA is presented that includes a dihedral angle of 100° between the A- and P-site tRNAs. The model is discussed in terms of interactions between the tRNA molecules during translation.
40. Smith TS, Chase ES, Schmidt TJ, Olson NH, Baker TS: Neutralization antibody to human rhinovirus 14 penetrates the receptor-binding canyon. Nature 1996, 383:350-354.
41. Boisset N, Taveau JC, Penczek P, Frank J: Three-dimensional reconstruction in vitreous ice of Androctonus australis hemocyanin labelled with a monoclonal Fab fragment. J Struct Biol 1995, 115:16-29.
42. Davies C, Ramakrishnan V, White SW: Structural evidence for specific S8-RNA and S8-protein interactions within the 30S ribosomal subunit: the structure of ribosomal protein S8 from Bacillus stearothermophilus at 1.9 Å. Structure 1996, 4:1093-1104.
43. Jaishree TN, Ramakrishnan V, White SW: Solution structure of prokaryotic ribosomal protein S17 by high resolution NMR spectroscopy. Biochemistry 1995, 35:2845-2853.
44. Hoffman DW, Cameron CS, Davies C, White SW, Ramakrishnan V: Ribosomal protein L9: Structure refinement using a combination of X-ray diffraction and NMR data. J Mol Biol 1997, in press.
45. Markus MA, Hinck AP, Huang D, Draper DE, Torchia DA: High resolution solution structure of ribosomal protein L11-C76, a helical protein with a flexible loop that becomes structured upon binding to RNA. Nat Struct Biol 1997, 4:70-77.
46. Davies C, White SW, Ramakrishnan V: The crystal structure of ribosomal protein L14 reveals an important organizational component of the translational apparatus. Structure 1996, 4:55-66.
47. Nevskaya N, Eliseikina I, Fomenkova N, Nikulin A, Ossina N, Garber M, Jonsson B-H, Brian C, Al-Karadaghi S, Svensson A et al.: Crystal structure of the RNA-binding ribosomal protein L1 from Thermus thermophilus. EMBO J 1995, 15:1350-1359.
48. Leijonmarck M, Liljas A: Structure of the C-terminal domain of the ribosomal protein L7/L12 from Escherichia coli at 1.7 Å. J Mol Biol 1987, 195:555-580.
49. Strycharz WA, Nomura M, Lake JA: Ribosomal proteins L7/L12 localized at a single region of the large subunit by immune electron microscopy. J Mol Biol 1978, 126:123-140.
50. Lake JA, Strycharz WA: Ribosomal proteins L1, L17 and L27 from Escherichia coli localized at single sites on the large subunit by immune electron microscopy. J Mol Biol 1981, 153:979-992.
51. Capel MS, Kjeldgaard M, Engelman DM, Moore PB: Positions of S2, S13, S16, S17, S17, and S21 in the 30S ribosomal subunit of Escherichia coli. J Mol Biol 1988, 200:65-87.
52. May RP, Nowotny V, Nowotny P, Voss H, Nierhaus KH: Interprotein distances within the large subunit from Escherichia coli ribosomes. EMBO J 1992, 11:373-378.
53. Scheinman A, Atha T, Aguinaldo AM, Kahan L, Sharkvwiler G, Lake JA: Mapping the three-dimensional locations of ribosomal RNA and proteins. Biochimie 1992, 74:307-317.
54. Stöffler-Meilicke M, Stöffler G: Topography of the ribosomal proteins from Escherichia coli within the intact subunits as determined by immunoelectron microscopy and protein-protein cross-linking. In The Ribosome. Edited by Hill WE et al.. Washington, DC: American Society of Microbiology Press; 1990:123-133.
55. Frank J, Penczek P, Grassucci R, Srivastava S: Three-dimensional reconstruction of the 70S E. coli ribosome in ice: the distribution of ribosomal RNA. J Cell Biol 1991, 115:597-605.
56. Frank J, Penczek P: On the correction of the contrast transfer function in biological electron microscopy. Optik 1995, 98:125-129.
57. Beniac DR, Czarnota GJ, Bartlett TA, Rutherford BL, Ottensmeyer FP, Harauz G: Challenges of three-dimensional reconstruction of ribonucleoprotein complexes from electron spectroscopic images - reconstructing ribosomal RNA. Scann Microsc 1997, in press.
58. Oakes MI, Lake JA: DNA-hybridization electron microscopy. J Mol Biol 1990, 211:897-906.
59. Montesano-Roditis L, Ryazantsev S, Traut RR, Glitz DG: From antibodies to 14A gold clusters as probes of ribosome structure. Abstract of the International Conference on the Structure and Function of the Ribosome, 1995 May 20-25, Victoria, Canada.
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