The role of noncanonical stacking interactions of heterocyclic RNA bases in ribosome functioning

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Abstract

Identification and analysis of recurrent elements (motifs) in DNA, RNA and protein macromolecules is an important step in studying the structure and functions of these biopolymers. In this paper, we investigated the functional role of NA-BSE (Non-Adjacent Base-Stacking Element), a widespread motif in the tertiary structure of various RNAs, in RNA-RNA interactions at various stages of ribosome function during translation of genetic information. Motifs of this type, reversibly formed during mRNA decoding, movement of ribosome subunits relative to each other, and movement of mRNA and tRNA along the ribosome during translocation, are described. EF-G-dependent formation of NA-BSE involving nucleotide residues of 5S rRNA and 23S rRNA is considered in particular.

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About the authors

V. G. Metelev

Lomonosov Moscow State University

Email: bogdanov@belozersky.msu.ru

Faculty of Chemistry

Russian Federation, 119991 Moscow

E. F. Baulin

Moscow Institute of Physics and Technology

Email: bogdanov@belozersky.msu.ru
Russian Federation, 141701 Dolgoprudny, Moscow Region

A. A. Bogdanov

Lomonosov Moscow State University; Lomonosov Moscow State University; Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Author for correspondence.
Email: bogdanov@belozersky.msu.ru

Faculty of Chemistry, Lomonosov Moscow State University; A. N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Russian Federation, 119991 Moscow; 119992 Moscow; 117997 Moscow

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Supplementary files

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2. Fig. 1. Formation of NA-BSE in the decoding center of the E. coli ribosome. a – Both the A- and P-sites of the ribosome are involved in codon-anticodon interactions (PDB ID: 5UYM); b – the A-site of the ribosome is free (PDB ID: 5UYK) (details in the text). Construction of spatial structures of RNA, their analysis and creation of all illustrations were carried out using the Discovery Studio Visualizer v.21.1.0.20298 program.

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3. Fig. 2. Formation of stacked NA-BSE involving G530 of 16S rRNA and A3 stop codon of mRNA located in the A-site of the ribosome (PDB ID: 4V67, a). Universal method of fixation of tRNA in the P-site of the ribosome by formation of NA-BSE from C34 tRNA and C1400 of 16S rRNA exposed from its polynucleotide chain due to formation of NA-BSE C1399–G1401 (PDB ID: 7K00, b)

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4. Fig. 3. Formation (PDB ID: 7SS9, a) and destruction (PDB ID: 7SSL, b) of the B7 “bridge” between the subunits of the E. coli ribosome

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5. Fig. 4. NA-BSE formed during the translocation of tRNA along the ribosome in its A- and E-sites

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6. Fig. 5. NA-BSE formed upon binding of the 3′ end of deacylated tRNA to the E-site of the E. coli ribosome. a – “Pocket” for binding of the acceptor end of tRNA in a vacant ribosome (PDB ID: 6PJ6); b – NA-BSE G2421–A76–C2422, deacylated tRNA is in the ribosome in an intermediate P/E state (PDB ID: 8SYL); c – formation of a flat conformation C75–A76 and a stacked NA-BSE involving the C75 residue of tRNA before dissociation of tRNA from the ribosome (PDB ID: 7K00)

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7. Fig. 6. Relative arrangement of residues G19 and C56 of the tRNA “elbow” and G2112 and G2168 of the “L1-protrusion” of 23S rRNA, a – at the initial stage of tRNA movement from the P-site to the E-site of the ribosome (PDB ID: 7ST6); b – upon complete movement of tRNA to the E-site (PDB ID: 7SSN); c – at the initial stage of tRNA dissociation from the E-site (PDB ID: 7ST2)

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8. Fig. 7. NA-BSE formed by nucleotide residues of the D-loop of 5S rRNA and the so-called “loop 960” closing the helix H39 of 23S rRNA in the E. coli ribosome (PDB ID: 5MDV)

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9. Fig. 8. Mutual arrangement of nucleotide residues of U89 tRNA and U958 23S rRNA, a – in the presence (PDB ID: 7SSL) and b – in the absence (PDB ID: 7SSW) of the elongation factor EF-G in the E. coli ribosome

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10. Fig. 9. Contact in the form of NA-BSE adjacent to the D-loop of the double helix IV of 5S rRNA and n.a. A1124 of the double loop of the 23S rRNA of Haloarcula marismortui ribosomes

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11. Appendix. Table P1
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12. Appendix. Table P2
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