5S Ribosomal RNA - American Chemical Society

Miroslawa Z. Barciszewska,† Maciej Szyman´ski,† Volker A. Erdmann,‡ and ... Introduction. In all organism, a messenger-directed protein synthes...
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Fall 2000

Published by the American Chemical Society

Volume 1, Number 3

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Reviews 5S Ribosomal RNA Miroslawa Z. Barciszewska,† Maciej Szyman´ ski,† Volker A. Erdmann,‡ and Jan Barciszewski*,† Institute of Bioorganic Chemistry of the Polish Academy of Sciences, Noskowskiego 12, 61704 Poznan, Poland; and Institut fur Biochemie, Freie Universitat Berlin, Thielallee 63, 14195 Berlin, Germany Received January 24, 2000; Revised Manuscript Received May 16, 2000

1. Introduction In all organism, a messenger-directed protein synthesis is catalyzed by ribosomes. The ribosome is an extremely ancient, a large (approximately 2.5 MDa), highly complexed molecular machine composed of rRNAs and proteins which have co-evolved over 3 billion years ago in order to synthesize proteins efficiently and accurately. Although they are the universal cellular organelles and catalyze the formation of the peptide bonds, the entire protein biosynthesis process is highly complicated.1-4 The most important functional sites of the ribosomes are those associated with the conserved domains of ribosomal RNA; which are the mRNA decoding site, the peptidyl transferase, and the sites at which the two elongation factors (EF-Tu and EF-G) alternatively bind to position the tRNA molecule in the A site or to catalyze the translocation of mRNA. In the past few years a combination of X-ray crystallography, NMR spectroscopy and cryoelectron microscopy has provided a new light on structure of ribosomes.5 The bacterial ribosomes (70S) consist of the two unequal subunits, 30S (small) and 50S (large). The 50S subunit containing 34 different proteins (L1-L34), 23S rRNA of 2904 nucleotides, and 5S rRNA, has been recently crystallized and its structure was solved with high resolution.6-12 Ribosomal 5S RNA, a 120 nucleotide long RNA of molecular weight 40 000, is found in virtually all ribosomes with the exception of mitochondria * Corresponding author: Prof. dr hab. Jan Barciszewski (jbarcisz@ ibch.poznan.pl) Institute of Bioorganic Chemistry of the Polish Academy of Sciences, Noskowskiego 12, 61704 Poznan, Poland. Telephone: 004861-8528505. Fax: 0048-61-8520532. † Institute of Bioorganic Chemistry of the Polish Academy of Sciences. ‡ Freie Universitat Berlin.

of some fungi, higher animals and most protists.13,14 It binds three proteins: L5, L18, and L25. 2. Current Studies of Ribosomal 5S rRNA Recent data showed that 5S rRNA is the true organellar species in mitochondrial fractions purified from mammalian cells.15-16 This result, although interesting however, did not resolve the question whether the 5S rRNA is authentic component of mitochondria because an engineered transcript similar to 5S rRNA can also be imported into mitochondria. 5S rRNA is located in the central protuberance of the large ribosomal subunit near the peptidyl transferase and factorbinding sites.1-5 Since its discovery in 1963 as a component of Escherichia coli ribosome,17 5S rRNA has been an object of a very intensive study with different methods.18,19 During last 35 years, a large amount of sequence data has been collected for this RNA species,20 but we are still far away from the detailed knowledge of the tertiary structure and detailed functions of 5S rRNA, although the last few years resulted in new very important structural data.21,22 The crystal structures of the 62 nt domain of E. coli 5S ribosomal RNA and the duplex dodecamer encompassing an internal loop E have been determined at 3.0 and 1.5 Å, respectively.21 The three cross-strand purine stocks in loop E and helix IV significantly alter the shapes of both the major and minor grooves. The major groove of loop E is 2.1 Å narrower than A-form RNA in the dodecamer and 6 Å narrower in the fragment at the 3′ end of the molecule. The minor groove is correspondingly expanded by 2.2 Å in the dodecamer. Also the solution structure of 42 nt derivative of E. coli 5S rRNA which includes the loops D and E has been determined by nuclear magnetic resonance spectroscopy.22 It was demonstrated that loop E of the 5S rRNA is not a loop at all but it

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Figure 1. General secondary structure of 5S rRNA with marked sites of occurrence of modified nucleosides.

is a double helical region with several irregularities which might be important for specific RNA-protein interactions. Those data which concern a larger part of the molecule, reveal details of a novel type of base pairings and provide a valuable structural information on the site of its interaction with protein L25. In the free and the bonded forms of the E-loop, similar chemical shifts have been observed for hydrogen bond formation in the A73-U103 and U77-A99 reverse Hoogsteen base pairs.23 Recently, a significant progress has been observed in the crystallization of short fragments of 5S rRNA. The X-ray structure of the domain E and of the helix E octamer and heptamer of Thermus flaVus 5S rRNA have been solved at atomic resolution. They adopt a helical RNA structure.24 In addition, crystals of T. flaVus were obtained under microgravity conditions and data were collected with 7.8 Å resolution.25 Eukaryotic 5S rRNAs of cytoplasmic ribosomes are usually encoded by separate genes arranged in tandem arrays of repeating units. Their number varies significantly up to several thousands in vertebrates and plants. In the prokaryotes and organelles, 5S rRNAs are synthesized as a part of single long transcript, together with 16 and 23 S rRNAs. The 5S ribosomal genes in higher eukaryotes are located independently from the 45S rDNA repeats containing 18S, 5.8S, and 26S ribosomal RNA genes. In Marchiantia polymorpha, 5S rDNA is encoded in 45S rDNA repeat unit of 16 103 bp in length and is located downstream of 18S, 5.8S, and 26S rDNA.26 This colocalization suggests that there has been structural re-organization of the rDNAs after divergence of bryophytes from the other plant species in the corse of evolution.26,27 The eukaryotic 5S rRNA genes are transcribed by polymerase III, which is strongly inhibited by p5328 and depends strongly in eukaryotic cells on the binding of a 40 kDa proteinstranscription

factor IIIA (TF IIIA)sto the internal control region of the 5S rRNA gene.29 There is also evidence for direct interactions of upstream regulatory elements and a new independent upstream promoter element centered about -17 to -20.30 In Xenopus somatic cells, histone H1 effects the transcription repression of the oocyte type 5S rRNA genes, without altering the transcription of the somatic type 5S rRNA genes. This means that the locations of positioned nucleosomes on somatic and oocyte 5S rDNAs differ significantly, resulting in a differing accessibility of the TF IIIA binding site in the two nucleosomes and the binding of TF IIIA to the oocyte nucleosomes is achieved by a nucleosome repositioning.31,32 One of the remarkable features of TF IIIA is that it is capable of specific binding to the 5S rRNA gene and the gene product with a high affinity and specificity, although the threedimensional structures of RNA and DNA are clearly different. A minimal RNA fragment that is sufficient for TF IIIA binding includes truncated/mutated helix I, helix II, and helix V, as well as structurally intact loops A and E.33 Details of the loop E structure has been deeply discussed.34 The X-ray structure of the TFIIIA-DNA complex shows how the zinc fingers have been deployed to bind to the separated promoter elements.35 The TF IIIA protein presence alters UV-induced photoproducts on DNA and reduces nucleotide excision repair.36 The two types of 5S rRNAs, somatic and oocytes, showed different protein associations and localization patterns after microinjection into the cytoplasm of oocytes. It seems that the degree to which 5S rRNA is localized to nucleoli or retained in the cytoplasm is regulated by dynamic and complex molecular interactions between the RNA molecule and other nucleoplasmic and nucleolar components with the differential binding affinities for 5S rRNA. Deletion of the bulged nucleosides in 5S rRNA molecules results in defective

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Figure 2. Activities and functions of 5S rRNA. Its participation in various complexes formation is shown.

ribosome assembly and increase a binding affinity to an unknown nucleoplasmic component.37 Mapping elements in ribosomal protein L5 that mediate nuclear protein import defines three separate such activities NLS 1-3, which are functional in bith oocytes and somatic cells. RNA binding activity involves N-terminal as well as C-terminal elements of L5.38 Some modified nucleosides have been found in 5S rRNAs (Figure 1). In the future there will be many more rare bases discovered in 5S rRNA, especially when the new method based on matrix assisted laser desorption/ionization mass spectrometry (MALDI-MS) is applied.39 In Sulfololus acidocaldanies, 2′-o-methylatedcytidine in stem C has been found.39 5S rRNA is the only known RNA species that binds ribosomal proteins before it is incorporated into the ribosomes both in prokaryotes and eukaryotes (Figure 2). In eukaryotes, 5S rRNA molecule binds only ribosomal protein L5, whereas in bacteria it interacts with three ribosomal proteins L5, L18, and L25. The 5S rRNA assembly to 23 S rRNA requires proteins L18 and L5, but not L25, which already binds to 5S rRNA.40 The N-terminal fragment (residues 1-91) of the ribosomal protein Thermus thermophilus TL5 binds specifically to 5S rRNA and the region of that fragment containing residues 80-91 is a necessity for its RNA-binding activity. The fragment of E. coli 5S rRNA protected by TL5 against RNase A hydrolysis contains the loop E and helices IV and V.41 Although complex formation of yeast ribosomal protein L5 (L1, L1a, or YL3) with 5S rRNA in vitro is difficult, there are data on the successful assembly of a RNA complex using a fusion protein consisting of the yeast L5 fused to the carboxy terminus of an E. coli maltose-binding protein.42 The NMR solution tertiary structure of L25 showed also a high similarity to tRNA anticodonbinding domain of glutaminyl-tRNA synthetase.43 L25

shows a new topology for binding of RNA. Many of the residues of L25 are distributed through the amino acid sequence and are located on a contignos surface of the protein structure. The crystal structure of E. coli ribosomal protein L25 bound to an 18-base pair portion of 5S rRNA which contains loop E has been determined at 1.8 Å resolution. The structure of loop E is almost the same as that of uncomplexed RNA. Those residues interacting with the RNA backbone are the most conserved among known L25 sequences, whereas those interacting with bases are not.44 A limited trypsinisation of eukaryotic ribosomes releases two peptides of 32 and 14 kDa suggesting that the amino and carboxyl terminal ends of L5 protein were first to be hydrolyzed and exposed on the surface of the ribosome.45 The protein L5 being a central component of the 5S rRNA export system, interacts also with eukaryotic initiation factor 5A which on the other hand bind HIV-1 Rev.46 5S rRNA binds the viral protein47 and enhances the methionyl- and isoleucyl-tRNA synthetase activities by direct interactions with MetRS and tRNAMet in the macromolecular aminoacyl-tRNA synthetases complex.48 Recently 5S rRNA has been identified in the degradosome complex.49 It has been also demonstrated that it is complementary with 12 and 15 nt strings to the intron 1 sequences of cobrotoxin b and cobrotoxin genes.50 It seems that in addition to 5S rRNA-protein interactions an important role is played by the contacts of 5S rRNA with 23S rRNA. Multiple hydrogen bonds from 5S rRNA to the two distinct regions of the 23S rRNA have been observed. The first and second regions were located at sites between nucleotides 885 and 992 and 2272 and 2345 of 23 rRNA, respectively.51 The base paired interaction between 5S rRNA (residues: 91-110) in the large subunit and 18 S rRNA in

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Reviews Table 1. Nucleotide Sequence Entries in the 5S RRNA Database for Major Taxonomic Groups taxonomic group

no. of entries

eubacteria archaea organelles mitochondria chloroplasts eukaryota protista fungi animals plants tot.

470 60 72 9 63 1383 57 217 367 742 1985

models of eukaryotic and prokaryotic 5S rRNAs are shown in Figure 3. Most of the 5S rRNA sequences can be folded according to one of these models, although Eubacteria and Archaea show much higher variability than the Eukaryotes. The ability of the sequence to adopt correct one, consensus secondary structure can be used to discriminate between genes and pseudogenes, that are often found in eukaryotic genomes. Improved programming algorithms for 5S rRNA secondary structure prediction were published.52-54 The predicted structures for E. coli and X. laeVis 5S rRNAs are inconsistent with the model shown in Figure 3.

Figure 3. General secondary structure model of eubacterial (A) and eukaryotic (B) 5S rRNAs. An alternative base-pairing scheme for the region of helix IV-loop D-helix V-loop E for plant 5S rRNA (C) is presented in the inset. The conserved positions are identified with letters (R, purine; Y, pyrimidine), variable positions are marked with gray and open circles. The differences in nucleotide sequences of eukaryotic and eubacterial 5S rRNA are denoted with black circles.

small subunit could contribute to the reversible association of the ribosomal subunits.52 Taking together, 5S rRNA is attractive model system for an exploring fundamental issues of RNA conformation and RNA protein interaction due to its relatively small size, ease of preparation and rich array of noncanonical base pairs.22 3. Secondary Structure of 5S rRNA. The nucleotide sequence of 5S rRNA is highly conserved throughout nature, and phylogenetic analysis alone provided an initial model for its secondary structure. This model was refined later on to include five helical regions, three internal loops, and two hairpin loops forming an unknown threedimensional structure by chemical modification, site directed mutagenesis, physical characterization, and computer modeling.18,19 The secondary structure of all analyzed 5S rRNAs consists of five helices (I-V), two hairpin loops (C and E), two internal loops (B and D), and a hinge region (A), organized into the three-helix junction. The general secondary structure

4. 5S rRNA Database To get a consistent picture of the structure-function relationships of 5S rRNA, detailed knowledge concerning the primary structure of this RNA species from different sources is required. Therefore, we have prepared the data bank.20 The database entries use the format of the EMBL Nucleotides Sequence Data Bank. The 5S rDNA nucleotide entries contain the 5S rRNA coding sequence as well as the information on the length of the original clone and location of the structural gene. The database contains 1985 nucleotide sequences of 5S rRNAs and 5S rDNAs published through 1999. In Table 1 we show distribution of the sequence entries for the main taxonomic groups. Files with the primary structure data and the nucleotide sequence alignments are available via the WWW at http://rose.man.poznan.pl/5Sdata/ index.html or [email protected]. Any nucleotide sequence can be retrieved using the taxonomy browser or alphabetical list of organisms. 5. Summary Ribosomes have been visualized in electron micrographs in 1943 but 5S rRNA was discovered 20 years later. The next four decades witnessed big advances in our understanding of the ribosome using biochemical, genetic and low resolution structural approaches. During those times many experimental data accumulates also on 5S rRNA, but its precise function remains unknown. To understand the role of this RNA in ribosome a high-resolution structure is urgently needed. Because the ribosome is a dynamic machine, details on the interaction of 5S rRNA with proteins within entire ribosome are required. Big progress in the

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structural analysis of ribosome will stimulate further understanding of 5S rRNA. Acknowledgment. This work has been supported by the Polish State Committee for Scientific Research and the Deutsche Forschungsgemeinschaft (Gottfried Wilhelm Leibnitz Prize to V.A.E., the Deutsche Agentur fur Raumfahrtangelegenheiten GmbH, the Fonds der Chemischen Industrie e.V.) References and Notes (1) Porse, B. T.; Garrett, R. A. Ribosomal mechanics, antibiotics, and GTP hydrolysis. Cell 1999, 97, 423-426. (2) Garrett, R. Mechanics of the ribosome. Nature 1999, 400, 811812. (3) Pennisi, E. Ribosome finally begins to yield its complete structure. Science 1999, 285, 1343. (4) Green, R.; Puglisi, J. D. The ribosome revealed. Nat. Struct. Biol. 1999, 6, 999-1003. (5) Agrawal, R. K.; Frank, J. Structural studies of the translational apparatus. Current Opin. Struct. Biol. 1999, 9, 215-221. (6) Moore, P. B. The three-dimensional structure of ribosome and its components. Annu. ReV. Biomol. Struct. 1998, 27, 35-58. (7) Ban, N.; Nissen, P.; Penczek, P.; Hansen, J.; Capel, M.; Moore, P. B.; Steitz, T. A. Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit. Nature 1999, 400, 841-847. (8) Clemons, W. M.; May, J. L. C.; Wimberly, B. T.; McCutcheon, J. P.; Capel, M. S.; Ramakrishan, V. Structure of a bacterial 30S ribosomal subunit at 5.5 Å-resolution. Nature 1999, 400, 833-840. (9) Cate, J. H.; Yusupov, M. M.; Yusupova, G. Zh.; Earnest, T. N.; Noller, H. F. X-ray crystal structures of 70S ribosome functional complexes. Science 1999, 285, 2095-2104. (10) Spahn, Ch. M. T.; Grassucci, R. A.; Penczek, P.; Frank, J. Direct three-dimensional localization and positive identification of RNA helices within the ribosome by means of genetic tagging and cryoelectron microscopy. Structure 1999, 7, 1567-1573. (11) Stark, H.; Rodnina, M. V.; Wieden, H.-J.; van Heel, M.; Wintermeyer, W. Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 2000, 100, 301-309. (12) Gabashvili, I. S.; Agrawal, R. K.; Spahn, Ch. M. T.; Grassucci, R. A.; Svergun, D. I.; Frank, J.; Penczek, P. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 2000, 100, 537549. (13) Gray, M. W.; Burger, G.; Lang, B. F. Mitochondrial evolution. Science 1999, 283, 1476-1481. (14) Spruyt, N.; Delarbe, C.; Gachelin, G.; Laudet, V. Complete sequence of the amphioxus (Branchiostoma lanceolatum) mitochondrial genome: relations to vertebrates. Nucleic Acids Res. 1998, 26, 32793285. (15) Magalhaes, P. J.; Andreu, A. L.; Schon, E. A. Evidence for the presence of 5S rRNA in mammalian mitochondria. Mol. Biol. Cell 1998, 9, 2375-2382. (16) Taanman, J.-W. The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1999, 1410, 103123. (17) Rosset, R.; Monier, R. Ribonucleic acid composition of bacteria as a function of growth rate. Biochim. Biophys. Acta 1963, 68, 653656. (18) Barciszewska, M.; Erdmann, V. A.; Barciszewski, J. Ribosomal 5S RNA: tertiary structure and interactions with proteins. Biol. ReV. 1996, 71, 1-25. (19) Zheng, P.; Burrows, C. J.; Rokita, S. E. Nickel- and cobalt- dependent reagents identify structural features of RNA that are not detected by dimethyl sulfate or RNase T1. Biochemistry 1998, 37, 2207-2214. (20) Szymanski, M.; Barciszewska, M.; Barciszewski, J.; Erdmann, V. A. 5S ribosomal RNA database Y2K. Nucleic Acids Res. 2000, 28, 166-167. (21) Correll, C. C.; Freeborn, B.; Moore, P. B.; Steitz, T. A. Metals, motifs, and recognition in the crystal structure of 5S rRNA domain. Cell 1997, 91, 705-712. (22) Dallas, A.; Moore, P. B. The loop E-loop D region of Escherichia coli 5S rRNA: the solution structure reveals an unusual loop that may be important for binding ribosomal proteins. Structure 1997, 5, 1639-1653.

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(43) Stoldt, M.; Wohnert, J.; Gorlach, M.; Brown, L. R. The NMR structure of Escherichia coli ribosomal protein L25 shows homology to general stress proteins and glutaminyl-tRNA synthetases. EMBO J. 1998, 17, 6377-6384. (44) Lu, M.; Steitz, T. A. Structure of Escherichia coli ribosomal protein L25 complexed with a 5S rRNA fragment at 1.8 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 2023-2028. (45) Lin, E.; Liu, S.-R.; Lin, A. Biochemical analysis of a 5S rRNAassociated sub-particles from trypsinized eukaryotic ribosomes. J. Biochem. 1999, 125, 1029-1033. (46) Schatz, O.; Oft, M.; Dascher, C.; Schebesta, M.; Rosorius, O.; Jaksche, H.; Dobrovnik, D.; Bevec, D.; Hauber, J. Interaction of the HIV-1 rev cofactor eukaryotic initiation factor 5A with ribosomal protein L5. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 1607-1612. (47) Lam, W.-H.; Seifert, J. M.; Amberger, F.; Graf, C.; Auer, M.; Millar, D. Structural dynamics of HIV-1 Rev and its complexes with RRE and 5S RNA. Biochemistry 1998, 37, 1800-1809. (48) Ogata, K.; Ohno, R.; Morioka, S.; Terao, K. Further study on association of 5S rRNA-L5 protein complex and methionyl-tRNA synthetase in macromolecular aminoacyl-tRNA synthetase complex. J. Biochem. 1996, 120, 869-880.

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