Abstract
The structures of eukaryotic ribosomal 5S RNA from rat liver and of prokaryotic 5S RNA from E. coli (A-conformer) have been investigated by scattering methods. For both molecules, a molar mass of 44,500±4,000 was determined from small angle X-ray scattering as well as from dynamic light scattering. The shape parameters of the two rRNAs, volume V c, surface O c, radius of gyration R s, maximum dimension of the molecule L, thickness D, and cross section radius of gyration R sq, agree within the experimental error limits. The mean values are V c=57±3 nm3, O c=165±10 nm2, R s=3.37±0.05 nm, L=10.8±0.7 nm, D=1.57±0.07 nm, R sa=0.92±0.01 nm.
Identical structures for the E. coli 5S rRNA and the rat liver 5S rRNA at a resolution of 1 nm can be deduced from this agreement and from the comparison of experimental X-ray scattering curves and of experimental electron distance distribution function. The flat shape model derived for prokaryotic and eukaryotic 5S rRNA shows a compact region and two protruding arms. Double helical stems are eleven-fold helices with a mean base pair distance of 0.28 nm. Combining the shape information obtained from X-ray scattering with the information about the frictional behaviour of the molecules, deduced from the diffusion coefficients D 020,w =(5.9±0.2)·10-7 cm2s-1 and (6.2±0.2)·10-7 cm2s-1 for rat liver 5S rRNA and E. coli 5S rRNA, respectively, a solvation shell of about 0.3 nm thickness around both molecules is determined. This structural similarity and the consensus secondary structure pattern derived from comparative sequence analyses suggest that all 5S rRNAs may indeed have conserved essentially the same type of folding of their polynucleotide strands during evolution, despite having very different sequences.
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Arnott S, Hukins DWL, Dover SD (1972) Optimized parameters for RNA double-helices. Biochem Biophys Res Commun 48:1392–1399
Behlke J, Welfle H, Wendel I, Bielka H (1980) Physicochemical studies of the 7S complex of rat liver ribosomes and its components. Acta Biol Med Germ 39:33–40
Böhm S, Fabian H, Welfle H (1982) Universal structural features of prokaryotic and eukaryotic ribosomal 5S RNA derived from comparative analysis of their sequences. Acta Biol Med Germ 41:1–16
Connors PG, Beeman WW (1972) Size and shape of 5S ribosomal RNA. J Mol Biol 71:31–37
Damaschun G, Pürschel HV (1971) Röntgen-Keinwinkelstreuung von isotropen Proben ohne Fernordnung. I. Allgemeine Theorie. Acta Cryst A 27:193–197
Damaschun S, Müller JJ, Bielka H (1978) Scattering studies of ribosomes and ribosomal components. Methods Enzymol 59:706–750
Delihas N, Andersen J (1982) Generalized structures of the 5S ribosomal RNAs. Nucleic Acids Res 10:7323–7344
Erdmann VA, Doberer HG, Sprinzl M (1971) Structure and function of 5S RNA: The role of the 3′ terminus in 5S RNA function. Mol Gen Genet 114:89–94
Erdmann VA, Wolters J, Huysmans E, Vandenberghe A, De Wachter R (1984) Collection of published 5S and 5.8 S ribosomal RNA sequences. Nucleic Acids Res 12:r133–166
Fedorov BA, Kröber R, Damaschun G, Ruckpaul K (1976) Experimental and theoretical large-angle X-ray diffuse scattering by globins in solution. Sensitivity of the method. FEBS Lett 65:92–95
Fedorov BA, Timchenko AA, Denesyuk AI, Ptitsyn OB, Damaschun G (1979) Comparative analysis of globular protein structures in crystal and in solution with X-ray diffuse scattering. In: Hofmann E (ed) Proteins: structure, function and industrial applications. Pergamon Press, Oxford, pp 153–158
Fox JW, Wong KP (1979) The hydrodynamic shape, conformation and molecular model of E. coli ribosomal 5S RNA. J Biol Chem 254:10139–10144
Fox JW, Wong KP (1982) Aquisition of native conformation of ribosomal 5S ribonucleic acid from E. coli. Hydrodynamic and spectroscopic studies on the unfolding and refolding of ribonucleic acid. Biochemistry 21:2096–2102
Gast K, Zirwer D, Fahrenbruch B, Pittelkow R (1979) Eine einfache Meßanordnung für die quasi-elastische Lichtstreuung. Exp Tech Phys 27:319–329
Gast K, Zirwer D, Ladhoff AM, Schreiber J, Koelsch R, Kretschmar K, Lasch J (1982) Auto-oxidation-induced fusion of lipid vesicles. Biochim Biophys Acta 686:99–109
Holbrook SR, Sussman JL, Warrant RW, Kim SH (1978) Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. J Mol Biol 123:631–660
Kao TH, Crothers DM (1980) A proton-coupled conformational switch of E. coli 5S rRNA. Proc Natl Acad Sci USA 77:3360–3364
Kumosinski TF, Pessen H (1982) Estimation of sedimentation coefficients of globular proteins: An application of smallangle X-ray scattering. Arch Biochem Biophys 219:89–100
Leontis NB, Moore PB (1984) A small angle X-ray scattering study of a fragment derived from E. coli 5S RNA. Nucleic Acids Res 12:2193–2203
Morikawa K, Fujiyoshi Y, Ishizuka K, Kawakami M, Takemura S (1984) Various types of 5S rRNA crystals as studied by X-ray diffraction and electron microscopy. Nucleic Acids Res 15:143–146
Müller JJ (1983) Calculation of scattering curves for macromolecules in solution and comparison with results of methods using effective atomic scattering factors. J Appl Cryst 16:74–82
Müller JJ, Damaschun G, Walter G (1977) Über ein Computer-Programmsystem für die Strukturuntersuchung von Biopolymeren mit Hilfe der Röntgen-Kleinwinkelstreuung. In: Exp Methoden der Molekülphysik, Physikalische Gesellschaft der DDR, Reinhardsbrunn, pp 11–30
Müller JJ, Welfle H, Damaschun G, Bielka H (1981) Shape and secondary structure of native 5S RNA from rat liver ribosomes. A small angle and wide angle X-ray scattering study. Biochim Biophys Acta 654:156–165
Müller JJ, Damaschun G, Wilhelm P, Welfle H, Pilz I (1982) Comparison of the structures of the native form of rat liver 5S rRNA and yeast tRNAPhe. Small angle and wide angle X-ray scattering study. Int J Biol Macromol 4:289–296
Müller JJ, Glatter O, Zirwer D, Damaschun G (1983a) Calculation of small angle X-ray and neutron scattering curves and of translational coefficients on the common basis of finite elements. Studia Biophys 93:39–46
Müller JJ, Zirwer D, Damaschun G, Welfle H, Gast K, Plietz P (1983b) The translational frictional coefficients of rape seed 11S globulin, tRNAPhe and ribosomal 5S RNA. Calculation on the basis of finite elements. Studia Biophys 96: 103–108
Müller JJ, Damaschun H, Damaschun G, Gast K, Plietz P, Zirwer D (1984) Determination of hydrodynamic properties of biopolymers from small angle X-ray scattering data. Studia Biophys 102:171–175
Müller JJ, Misselwitz R, Zirwer D, Damaschun G, Welfle H (1985a) A-form to A′-form conformational switch of double helices in rat liver 5S and 5.8S rRNA. Eur J Biochem 148:89–95
Müller JJ, Damaschun G, Schmidt PW (1985b) The model resolution function — a technique for estimating the quality of approximation of particles by models in small angle X-ray or neutron scattering. J Appl Cryst 18:241–247
Nazar RN, Wildeman AG (1983) Three helical domains from a protein binding site in the 5S RNA-protein complex from eukaryotic ribosomes. Nucleic Acids Res 11: 3155–3168
Österberg R, Sjöberg B, Garrett RA (1976) Molecular model for 5S RNA. A small angle X-ray scattering study of native, denatured and aggregated 5S RNA from E. coli ribosomes. Eur J Biochem 68:481–487
Pieler T, Digweed M, Erdmann VA (1984) The structure and function of ribosomal 5S rRNAs. In: Clark BFC, Petersen HU (eds) Gene expression. Alfred Bencon Symposium 19. Munksgaard, Copenhagen
Pilz I (1969) Absolute intensity measurements of small angle X-ray scattering by means of a standard sample. J Colloid Interface Sci 30:140–144
Provencher SW (1982a) A constrained regularization method for inverting data represented by linear algebraic or intergral equations. Comput Phys Commun 27:213–227
Provencher SW (1982b) CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations. Comput Phys Commun 27:229–242
Wrede P, Erdmann VA (1973) Activities of B. Stearothermophilus 50S ribosomes reconstituted with prokaryotic and eukaryotic 5S RNA. FEBS Lett 33:315–319
Teller DC, Swanson E, De Haen CH (1979) The translational friction coefficient of proteins. Methods Enzymol 61: 103–124
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Müller, J.J., Zalkova, T.N., Ziwer, D. et al. Comparison of the structure of ribosomal 5S RNA from E. coli and from rat liver using X-ray scattering and dynamic light scattering. Eur Biophys J 13, 301–307 (1986). https://doi.org/10.1007/BF00254212
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DOI: https://doi.org/10.1007/BF00254212