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Inhibition by Siomycin and Thiostrepton of Both Aminoacyl

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Inhibition by Siomycin and Thiostrepton of Both Aminoacyl Proc. Nat. Acad. Sci. USA Vol. 68, No. 8, pp. 1796-1800, August 1971 Inhibition by Siomycin and Thiostrepton of Both Aminoacyl-tRNA and Factor G Binding to Ribosomes (Millipore filter/Tu/tetracycline/streptogramin/puromycin) JUAN MODOLE LL*, BARTOLOM]R CABRER*, ANDREA PARMEGGIANIt, AND DAVID VAZQUEZ* * Instituto de Biologia Celular, Velazquez 144, Madrid 6, Spain; and t Gesellschaft far Molekularbiologische Forschung, 3301 Stbckheim tiber Braunschweig, Germany Communicated by Bernard D. Davis, June 8, 1971 ABSTRACT Siomycin, a peptide antibiotic that inter- described (6, 7). Homogeneous initiation factor F1 and par- acts with the 50S ribosomal subunit and inhibits binding were of factor G, is shown also to inhibit binding of aminoacyl- tially purified factor F2 a gift of Dr. S. Ochoa. Elonga- tRNA; however, it does not impair binding of fMet-tRNA tion factors G and T (T. plus Tu) and ['y-82P]GTP were and completion of the initiation complex. Moreover, unlike prepared as described (2, 8). Commercial deacylated tRNA other inhibitors of aminoacyl-tRNA binding (tetracycline, was charged with labeled methionine (under formylating con- sparsomycin, and streptogramin A), siomycin completely ditions), phenylalanine, or alanine in the absence of other abolishes the GTPase activity associated with the binding of aminoacyl-tRNA catalyzed by factor Tu. A single-site unlabeled amino acids. Specific activities were 3900 cpm/ interaction of siomycin appears to be responsible for its pmol f-[3H]Met-tRNA, 740 cpm/pmol [14C]Phe-tRNA and effect on both the binding of the aminoacyl-tRNA-Tu- 180 cpm/pmol [14C]Ala-tRNA. GTP complex and that of factor G. Binding of aminoacyl-tRNA to ribosomes was assayed by Factor one of the supernatant proteins necessary for filtration (9). Reaction mixtures for the binding of fMet- G, tRNA contained: 80 mM NH4Cl, 50 mM Tris HOl (pH 7.7), ribosomal activity in Escherichia coli, is involved in the 5 mM Mg(acetate)2, 6 mM mercaptoethanol, 0.4 mM GTP, coupling of GTP hydrolysis to polypeptide elongation. This hydrolysis is thought to provide the energy necessary for the 0.3 mg/ml of crude initiation factors, 4.7 pmol f-[3H]Met- rearrangements of tRNA, tRNA per A260 unit ribosomes, 1.2 mg/ml of R17-RNA, mRNA, and ribosomal subunits, 35 A260 units/ml of and other additions as in each round of peptide bond that result in ribosomes, specified. formation, Unless otherwise indicated, incubation was at 34°C for 10 translocation of mRNA and peptidyl-tRNA (reviewed in min and was followed and ref. 1). GTP hydrolysis can also by filtration analysis. occur in the absence of mRNA Ala-tRNA was bound to preformed fMet-tRNA-70S and peptidyl-tRNA, the reaction requiring only factor G and ribosome-R17 RNA complex. An incubated reaction mixture ribosomes (2, 3). In recent work this reaction has been used to for the binding of fMet-tRNA was cooled to 0°C, and supple- show that there is a binding site for factor G (the G-site) on mented with 7.8 pmol of [14C]Ala-tRNA per A2w unit of the 50S subunit (4, 5). Our studies have further shown that a ribosomes and 0.08 mg/ml of T-factor. Binding was measured peptide antibiotic, siomycin, inactivates this site, preventing after incubation at 18°C for 15 min. In all experiments, the interaction of this site with factor G. Moreover, the G-site binding was corrected for the values obtained in parallel is evidently distinct from the peptidyl transferase center on mixtures without messenger. the 50S subunit (5). T-factor-dependent binding of Phe-tRNA to ribosomes and We have now shown that siomycin-treated ribosomes can its associated GTPase activity were measured as follows: carry out the initiation step in protein synthesis, with either ribosomes (68 A260 units/ml) were first incubated at 30°C for viral messenger or triplet AUG, and the bound fMet-tRNA 12 min in a mixture containing 150 mM NH4Cl, 16 mM can reach the puromycin-reactive position. However, no Mg(acetate)2, 85 mM Tris- HOl (pH 7.7), 1.6 mM dithio- peptide bond can be formed because the ribosomes do not threitol and 90 ,ug/ml of poly(U). This treatment was found bind aminoacyl-tRNA in the recognition site (the A-site). to decrease nonenzymic binding of Phe-tRNA without Moreover, the siomycin-treated ribosomes can complement the After at T affecting T-factor-dependent binding. cooling neither the GTPase activity associated with factor nor that 00C, 40-,ul portions were supplemented with antibiotics and associated with factor G. These effects appear to be the con- other components for the binding reaction (final volume, 70 sequence of a single action of siomycin on the 50S subunit, ;l). Final concentrations were: 90 mM NH4Cl, 24 mM thus suggesting a relationship between the binding site of (NH4)2S04 (carried over with the T-factor preparation), 50 factor G and that of the aminoacyl-tRNA-T.-GTP complex. mM Tris HCl (pH 7.7), 9 mM Mg (acetate)2, 1 mM dithio- MATERIALS AND METHODS threitol, 0.43,MM [7y_82P] GTP, 800-1200 cpm/pmol, 50 Mg/ml and of poly(U), 8 pmol of [14C] Phe-tRNA per A260 unit ribosomes, Ribosomes washed with ammonium chloride (1 M) crude 38 of ribosomes. initiation factors from E. coli MRE600 were prepared as 27 Mug/ml of T-factor, and A260 units/ml After incubation at 300C for 10 min, the reaction mixtures were chilled and divided into two portions: one was analyzed Abbreviations: (Me)2SO, dimethylsulphoxide; Complex II, for [14C]Phe-tRNA bound to ribosomes (9) and the other for GTP-factor Tu-aminoacyl-tRNA complex; Sio, siomycin. 82P-labeled inorganic phosphate (8). Binding of Phe-tRNA 1796 Downloaded by guest on September 30, 2021 Proc. Nat. Acad. Sci. USA 68 (1971) Siomycin Blocks the Ribosomal A-site 1797 TABLE 1. Binding offMet-tRNA to 70S ribosomes and TABLE 2. Requirements for Ala-tRNA reaction with puromycin, insensitivity to siomycin binding to 70S ribosomes fMet-tRNA bon pmol bound/A unit Incuba- bound tion f-[3HjMet-tRNA [14C]Ala-tRNA time (pmol/A unit) Expt. Messenger Addition (min) - Sio + Sio -T +T -T +T Complete 2.02 2.02 0.24 1.78 1 R17-RNA - 10 0.26 0.17 -fMet-tRNA -0.11 0.21 GTP 10 1.00 1.11 -R17-RNA 0.52 0.53 0.19 0.33 2 AUG F2 15 2.6 3.9 F2 + F, 15 4.6 5.5 [4C]Ala-tRNA was bound to ribosomes carrying prebound 3 R17-RNA GTP 10 - 0.97 f-[3H]Met-tRNA. GTP 12 0.97 GTP; at 10 min puromycin 12 - 0.22 elongation. Although we used crude initiation factors to form the initiation complex (which could result in substantial con- Reaction mixtures for Expts. 1 and 3 were as described in tamination with elongation factors, acylated-tRNA, and Methods, except that GTP was present only when indicated. other undefined components), subsequent binding of [14C]- In Expt. 3, 0.1 mM puromycin was added to one portion of the Ala-tRNA showed a good requirement for T factor, fMet- reaction mixture and the incubation was continued for two more tRNA, and R17-RNA (Table 2). Moreover, binding of minutes before the analysis. In Expt. 2, the reaction mixture Ala-tRNA to ribosomes was not the result of extensive contained 0.06 mM AUG, 0.2 mM GTP, 1 mM dithiothreitol, polypeptide formation: when the 1C-labeled product re- 0.069 units/ml of factor F2 (see ref. 10) with or without 60 jg/ml tained by the Millipore filter was released by 1 M NH40H of factor F1, 19 A26. units/ml of 70S ribosomes and 13.6 pmol of and with 0.5 M KOH at for 30 min f-[3H]Met-tRNA per A26. unit of ribosomes. Incubation was at hydrolyzed 37°C (7), 250C. All mixtures contained 2.5% Me2SO. Siomycin was 11 75% of the radioactivity was found to have the same electro- ,uM. Subtracted values from control reactions without mes- phoretic mobility as chemically synthesized formylmethionyl- senger were between 0.13 and 0.48 pmol. alanine (data not shown). Thus, under the conditions em- ployed, most of the Ala-tRNA retained by ribosomes did bind to the recognition site (the A site) of initiation com- and hydrolysis of GTP were corrected for the values obtained plexes and accepted the transfer of formylmethionine. in parallel mixtures without T-factor or without [14C]Phe- With this system it could be shown (Table 3) that sio- tRNA, respectively. mycin, and the closely related antibiotic thiostrepton (13), Siomycin and thiostrepton were dissolved in dimethyl- strongly inhibited the binding of Ala-tRNA. Moreover, in sulfoxide (Me)2SO. Consequently, between 2 and 4% Me2SO agreement with studies in other systems (14-17) tetracycline, was present in reaction mixtures with the antibiotics. Unless otherwise indicated, an equal amount of Me2SO was added to other reaction mixtures in the experiment. TABLE 3. Effect of antibiotics on the binding of Ala-tRNA to AUG was obtained from Miles Laboratories. Phage R17 preformed fMet-tRNA-70S ribosome-R17-RNA complex RNA was prepared as described (6). Poly(U) was from Schwartz. [3H]Methylmethionine (11.1 Ci/mmol), [14C]- pmol bound/A unit phenylalanine (0.477 Ci/mmol) and [14C]alanine (0.152 f-['H] Met- ["4C] Ala- Ci/mmol) were from The Radiochemical Center, Amersham. Expt. Additions tRNA tRNA RESULTS 1 None 1.32 1.36 Lack of effect of siomycin on initiation Fusidic acid (1.2 mM) 1.30 1.35 Tetracycline (0.1 mM) 1.46 0.21 Siomycin did not inhibit, but slightly stimulated, the binding Me2SO (2.5%) 1.61 1.86 of f-[3H]Met-tRNA to NH4Cl-washed ribosomes, either with Siomycin (0.011 mM) + 1.69 0.16 crude initiation factors and R17-RNA (Table 1, Expt.
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