The conformation of ribosomes and rRNA

Current Opinion in Structural Biology

Volumn 7, Issue 3, 1997, Pages 343-347

  Moore, Peter B ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; BACTERIAL RNA; PAROMOMYCIN; RIBOSOME RNA; RNA 16S;

ARTICLE; COMPLEX FORMATION; DRUG BINDING; ELECTRON MICROSCOPY; ESCHERICHIA COLI; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; RIBOSOME; RNA BINDING; RNA CONFORMATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0030978401     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(97)80049-8     Document Type: Article

References (36)

1. Wittmann-Liebold B, Kopke AKE, Arndt E, Kromer W, Hatakeyama T, Wittmann HG. Sequence comparison and evolution of ribosomal proteins and their genes. Hill WE, Dahlberg A, Garrett RA, Moore PB, Schlessigner D, Warner JR. The Ribosome. Structure, Function, & Genetics. 1990;598-616 American Society for Microbiology, Washington, DC.
2. Matheson AT, Davies JE, Dennis PP, Hill WE. Frontiers in translation. Biochem Cell Biol. 73:1995;739-1227 This is the sixth comprehensive review volume published by the ribosome fraternity since 1974. Not only is it definitive with respect to the position of the ribosome field as of mid 1995, it will remain the best single source of information about ribosomes until a successor is produced. of outstanding interest.
3. Zimmermann RA, Dahlberg AE. Ribosomal RNA. Structure, Evolution, Processing, and Function in Protein Biosynthesis. 1996;CRC Press, Boca Raton, FL, This long anticipated volume contains reviews written by experts on every aspect of ribosomal RNA biochemistry and molecular biology. of special interest.
4. Stark H, Mueller F, Orlova EV, Schatz M, Dube P, Erdemir T, Zemlin F, Brimacombe R, van Heel M. The 70S Escherichia coli ribosome at 23Å resolution: fitting the ribosomal RNA. Structure. 3:1995;815-821 This paper describes the first high-resolution reconstruction of the ribosome based on unstained images produced by van Heel and coworkers. The tentative fitting of some rRNA sequences into this electron density map is also presented. The huge advances in resolution reported in this paper and in [5] make them landmarks in both ribosome biochemistry and electron microscopy. of outstanding interest.
5. Frank J, Zhu J, Penczek P, Li Y, Srivastava S, Verschoor A, Rademacher M, Grassucci R, Lata RK, Agrawal RK. A model for protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature. 376:1995;441-444 This paper describes the first high-resolution reconstruction of the ribosome obtained by Frank and coworkers independent of van Heel. All the superlatives appropriate for the van Heel reconstruction [4] are appropriate here also. The differences between the two reconstructions will have to be adjudicated at some point. of outstanding interest.
6. Agrawal RK, Penczek P, Grassucci RA, Li Y, Leith A, Nierhaus KH, Frank J. Direct visualization of A-, P-, and E-site transfer RNAs in the Escherichia coli ribosome. Science. 271:1996;1000-1002 This paper reports the first structure - function experiment carried out using the reconstruction technology described in [5]. What emerges are the positions of the three tRNA binding sites on the ribosome - information that is of the utmost importance to those interested in the mechanism of protein synthesis. of outstanding interest.
7. 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. 133:1996;495-505.
8. 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. 245:1996;43-52 These 37 Å reconstructions of the small subunit document small conformational changes between activated, inactivated, and 50S-bound subunits. Although the resolution obtained is not as high as that reported for 70S particles, the 30S images shown are significantly better than anything published previously. of special interest.
9. Schlunzen F, Hansen HAS, Thygesen J, Bennett WS, Volkmann N, Levin I, Harms J, Bartles H, Zaytzev-Bashan A, Berkovitch-Yellin Z, et al. A milestone in ribosomal crystallography: the construction of preliminary electron density maps at intermediate resolution. Biochem Cell Biol. 73:1995;739-749 Yonath and coworkers may have obtained some heavy atom derivatives of their ribosome crystals, but the quality of the electron density maps shown in this paper suggests that problems remain. Thus, this paper is notable more as a description of the direction being taken by those responsible for a pioneering crystallographic effort rather than for the results it contains. of special interest.
10. Thygesen J, Weinstein S, Franceschi F, Yonath A. The suitability of multi-metal clusters for phasing in crystallography of large macromolecular assemblies. Structure. 4:1996;513-518.
11. Thygesen J, Krumbholz S, Levin I, Zaytzev-Bashan A, Harms J, Bartels H, Schlunzen F, Hansen HAS, Bennett WS, Volkmann N, Agmon I, et al. Ribosomal crystallography: from crystal growth to initial phasing. J Cryst Growth. 168:1996;308-323.
12. Woese CR, Winker S, Gutell RR. Architecture of ribosomal RNA. Constraints on the sequence of tetra loops. Proc Natl Acad Sci USA. 87:1990;8467-8471.
13. Cheong C, Varani G, Tinoco I. Solution structure of an unusually stable RNA hairpin, 5'GGAC(UUCG)GUCC. Nature. 346:1990;680-682.
14. Heus HA, Pardi A. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA lloops. Science. 253:1991;191-194.
15. Cate J, Gooding AR, Podell E, Zhou K, Golden BL, Kundrot CE, Cech TR, Doudna JA. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science. 273:1996;1678-1685.
16. Jucker FM, Pardi A. Solution structure of the CUUG hairpin loop: a novel RNA tetraloop motif. Biochemistry. 34:1995;14416-14427 This spectroscopic paper describes the organizational scheme characteristic of CUUG tetraloops - the last of the unusually abundant tetraloops found in rRNAs to be studied by NMR. of special interest.
17. Jucker FM, Heus HA, Yip PF, Moors HM, Pardi A. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J Mol Biol. 264:1996;968-980 Solution structures are derived for three GNRA tetraloops: GAGA; GCAA; and GAAA. As the oligonucleotides used in this study are quite small and heteronuclear labeling is used, the assignments are unusually complete, and the structures shown are unusually well determined. of special interest.
18. Fountain MA, Serra MJ, Krugh TR, Turner D. Structural features of a six-nucleotide RNA hairpin loop found in ribosomal RNA. Biochemistry. 35:1996;6539-6548 These two papers [18,19] describe the results of NMR studies of the hairpin loop between C1092 and G1099 in the 23S rRNA of E. coli, which is part of the factor-binding center. The two results differ in detail for reasons that have yet to be explained. of special interest.
19. Huang SG, Wang YX, Draper DE. Structure of a hexanucleotide RNA hairpin loop conserved in ribosomal RNAs. J Mol Biol. 258:1996;308-321 See annotation [18]. of special interest.
20. Dallas A, Rycyna R, Moore PB. A proposal for the conformation of loop E in Escherichia coli 5S rRNA. Biochem Cell Biol. 73:1995;887-897.
21. Nolte A, Klussman S, Lorenz S, Bald R, Betzel C, Dauter Z, Wilson K, Furste JP, Erdmann Va. Crystallization and preliminary diffraction studies of the structural domain E of Thermus flavus 5S rRNA. FEBS Lett. 374:1995;292-294.
22. Grune M, Furste JP, Erdmann VA, Brown LR. Detection of multiple conformations of the E-domain of 5S rRNA from Escherichia coli in solution and in crystals by NMR spectroscopy. Nucleic Acids Res. 24:1996;2592-2596.
23. Grune M, Gorlach M, Soskic V, Klussman S, Bald P, Furste JP, Erdmann VA, Brown LR. Initial analysis of 750 MHz spectra of selectively 15 N G-labelled E. coli 5S rRNA. FEBS Lett. 385:1996;114-118.
24. Davis DR, Yamaizumi Z, Nishimura S, Poulter CD. Nitrogen-15-labeled 5S RNA. Identification of uridine base pairs in Escherichia coli 5S RNA by proton - nitrogen-15 multiple quantum NMR. Biochemistry. 28:1989;4105-4108.
25. Gewirth DT, Abo SR, Leontis NB, Moore PB. Secondary structure of 5S RNA: NMR experiments on RNA molecules partially labeled with nitrogen-15. Biochemistry. 26:1987;5213-5220.
26. Fourmy D, Recht MI, Blanchard SC, Puglisi JD. Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science. 274:1996;1367-1371 This paper reports the most spectacular contribution of NMR spectroscopy to the ribosome story to date: a high-resolution model for paromomycin bound to the aminoglycoside-binding site in 16S rRNA. of outstanding interest.
27. Nikonov S, Nevskaya N, Eliseikina I, Fomenkova N, Nikulin A, Ossina N, Garber M, Jonsson BH, Briand C, Al-karadaghi S, et al. Crystal structure of the RNA binding ribosomal protein L1 from Thermus thermophilus. EMBO J. 15:1996;1350-1359 The protein structures reported in these five papers [27-31] are new entries in a slowly growing, but important list of proteins of known structure that bind RNA. As the number of structures grows, comparisons become more and more interesting, and the use of these structures in ribosome models is bound to increase. In the end, they may play an important role in the interpretation of the electron density maps of intact ribosomes, and, when it becomes possible, a comparison of the structures of these proteins within the ribosome and free of the ribosome is bound to be instructive. of special interest.
28. Davies C, Ramakrishnan V, White SW. Structural evidence for specific S8-RNA and S8-protein interactions within the 30S ribosomal subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9Å resolution. Structure. 4:1996;1093-1104 See annotation [27]. of special interest.
29. Davies C, White SW, Ramakrishnan V. The crystal structure of ribosomal protein L14 reveals an important organizational component of the translational apparatus. Structure. 4:1996;55-66 See annotation [27]. of special interest.
30. Jaishree TN, Ramakrishnan V, White SW. Solution structure of prokaryotic ribosomal protein S17 by high-resolution NMR spectroscopy. Biochemistry. 35:1996;2845-2853 See annotation [27]. of special interest.
31. Hoffman DW, Cameron Cs, Davies C, White SW, Ramakrishnan V. Ribosomal protein L9: a structure determination by combined use of X-ray crystallography and NMR spectroscopy. J Mol Biol. 264:1995;1058-1071 See annotation [27]. of special interest.
32. Capel MS, Kjeldgaard M, Engelman DM, Moore PB. The positions of S2, S13, S16, S17, S19, and S21 in the 30S ribosomal subunit of Escherichia coli. J Mol Biol. 200:1987;65-87.
33. Brimacombe R. The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur J Biochem. 230:1995;365-383 This paper reviews not only the author's efforts to model the ribosome, but also the arguments that justify his approach. In so doing, a critical evaluation of what others have done is provided. Reviews of this kind are of unusual value and are all too seldom encountered. of special interest.
34. Easterwood TR, Harvey SC. Modeling the structure of the ribosome. Biochem Cell Biol. 73:1995;751-756 These three papers [34-36] are the latest statements from the three groups that have dominated the modeling field recently. The differences between the models are instructive about the adequacy of the information available today. A strong feature of the effort described in [34] is the emphasis on quantitative evaluation of uncertainties. of special interest.
35. Noller HF, Green R, Heilek G, Hoffarth V, Huttenhofer A, Joseph S, Lee I, Lieberman K, Mankin A, Merryman C, et al. Structure and function of ribosomal RNA. Biochem Cell Biol. 73:1995;997-1009 See also annotation [34]. The modeling done by this group has always been driven by the fitting of rRNA into the neutron map of the small ribosomal subunit (see [32]). The authors' most recent models make direct use of the 3D structures of ribosome proteins and are the first to do so. of special interest.
36. Mueller F, Doring T, Erdemir T, Greuner B, Junke N, Osswald M, Rinke-Appel J, Stade K, Thamm S, Brimacombe R. Getting closer to an understanding of the three-dimensional structure of ribosomal RNA. Biochem Cell Biol. 73:1995;767-773 See also annotation [34]. Brimacombe and coworkers' models are strongly driven by RNA cross-linking data, and, unlike those of their competitors, they start by ignoring what is known about the 3D positions of ribosomal proteins. Protein positions are used later to check the models obtained. of special interest.