Aminoacylation of short hairpin RNAs through kissing-loop interactions indicates evolutionary trend of RNA molecules

Mutsuro‐Aoki, Hiromi; Hamachi, Kokoro; Kurihara, Ryodai; Tamura, Koji

doi:10.1016/j.biosystems.2020.104206

Cited by 5 publications

(8 citation statements)

References 49 publications

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“…Hairpin RNAs are composed of a stem and loop; the loop region is the most plausible place for interactions between different molecules. In fact, a kissing-loop interaction between two nonfunctional independent molecules can induce a conformational change and produce one function (e.g., the formation of a G:U wobble base pair corresponding to G3:U70 in tRNA Ala [ 14 ], which is the major identity determinant by AlaRS [ 15 , 16 ]). The present study clearly emphasizes that a kissing-loop interaction between two nonfunctional independent molecules produces dual functions simultaneously.…”

Section: Discussionmentioning

confidence: 99%

“…An amount of 15 µL of 30 µM of the combination of RNA(s) shown in Figure 3 in R3C buffer (50 mM Tris-HCl (pH 8.5) and 15 mM MgCl 2 ) was heated at 37 °C for 5 min and then incubated at 23 °C for 18.5 h. After the addition of loading buffer containing glycerol, the solution was analyzed by electrophoresis through nondenaturing 8% polyacrylamide gels in R3C buffer. The gel was stained with 0.04% toluidine blue [ 12 , 14 , 18 ].…”

Section: Methodsmentioning

confidence: 99%

“…The acquisition of a function through a kissing-loop interaction-induced rearrangement is not limited to the case of R3C ribozymes. We also demonstrated that a kissing-loop interaction between trans -molecules produced a unique G:U wobble base pair in an appropriate position, corresponding to the acceptor stem of tRNA [ 14 ], which can be a critical recognition site for alanyl-tRNA synthetase (AlaRS) [ 15 , 16 ]. Therefore, two small nonfunctional RNAs can gain a function through a kissing-loop interaction.…”

Section: Introductionmentioning

confidence: 99%

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Acquisition of Dual Ribozyme-Functions in Nonfunctional Short Hairpin RNAs through Kissing-Loop Interactions

Mutsuro‐Aoki

Tamura

2022

Life

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The acquisition of functions via the elongation of nucleotides is an important factor in the development of the RNA world. In our previous study, we found that the introduction of complementary seven-membered kissing loops into inactive R3C ligase ribozymes revived their ligation activity. In this study, we applied the kissing complex formation-induced rearrangement of RNAs to two nonfunctional RNAs by introducing complementary seven-membered loops into each of them. By combining these two forms of RNAs, the ligase activity (derived from the R3C ligase ribozyme) as well as cleavage activity (derived from the hammerhead ribozyme) was obtained. Thus, effective RNA evolution toward the formation of a life system may require the achievement of “multiple” functions via kissing-loop interactions, as indicated in this study. Our results point toward the versatility of kissing-loop interactions in the evolution of RNA, i.e., two small nonfunctional RNAs can gain dual functions via a kissing-loop interaction.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Acquisition of Dual Ribozyme-Functions in Nonfunctional Short Hairpin RNAs through Kissing-Loop Interactions

Mutsuro‐Aoki

Tamura

2022

Life

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“…After being incubated on ice for 2 h and the addition of 1 µL of 10 × loading buffer (150 mM Mg(OAc) 2 , 50% glycerol), the solution (final 150 µM) was analyzed by electrophoresis at 4 • C through nondenaturing 8% polyacrylamide gels in THM running buffer (50 mM Tris-HCl (pH 7.5), 100 mM KCl, 10 mM Mg(OAc) 2 ). The gel was stained with 0.04% toluidine blue [21,22].…”

Section: Electrophoretic Mobility Shift Assaymentioning

confidence: 99%

Peptide Bond Formation between Aminoacyl-Minihelices by a Scaffold Derived from the Peptidyl Transferase Center

Kawabata

Kawashima

Mutsuro‐Aoki

et al. 2022

Life

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The peptidyl transferase center (PTC) in the ribosome is composed of two symmetrically arranged tRNA-like units that contribute to peptide bond formation. We prepared units of the PTC components with putative tRNA-like structure and attempted to obtain peptide bond formation between aminoacyl-minihelices (primordial tRNAs, the structures composed of a coaxial stack of the acceptor stem on the T-stem of tRNA). One of the components of the PTC, P1c2UGGU (74-mer), formed a dimer and a peptide bond was formed between two aminoacyl-minihelices tethered by the dimeric P1c2UGGU. Peptide synthesis depended on both the existence of the dimeric P1c2UGGU and the sequence complementarity between the ACCA-3′ sequence of the minihelix. Thus, the tRNA-like structures derived from the PTC could have originated as a scaffold of aminoacyl-minihelices for peptide bond formation through an interaction of the CCA sequence of minihelices. Moreover, with the same origin, some would have evolved to constitute the present PTC of the ribosome, and others to function as present tRNAs.

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“…An RNA minihelix recapitulates the domain within tRNA that harbors the amino acid attachment site and may have been the progenitor of modern tRNA [ 11 , 12 ]. Multiple kissing-loop interaction-mediated conformational changes starting from short-hairpin RNAs possibly produced minihelix-like and then tRNA-like structures [ 13 ]. On the contrary, the duplication of minihelix-like RNA molecules could have evolved to the peptidyl transferase center on the ribosome [ 14 , 15 ].…”

Section: Introductionmentioning

confidence: 99%

Mechanism of Chiral-Selective Aminoacylation of an RNA Minihelix Explored by QM/MM Free-Energy Simulations

Ando

Tamura

2023

Life

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Aminoacylation of a primordial RNA minihelix composed of D-ribose shows L-amino acid preference over D-amino acid without any ribozymes or enzymes. This preference in the amino acylation reaction likely plays an important role in the establishment of homochirality in L-amino acid in modern proteins. However, molecular mechanisms of the chiral selective reaction remain unsolved mainly because of difficulty in direct observation of the reaction at the molecular scale by experiments. For seeking a possible mechanism of the chiral selectivity, quantum mechanics/molecular mechanics (QM/MM) umbrella sampling molecular dynamics (MD) simulations of the aminoacylation reactions in a modeled RNA were performed to investigate differences in their free-energy profiles along the reactions for L- and D-alanine and its physicochemical origin. The reaction is initiated by approaching a 3′-oxygen of the RNA minihelix to the carbonyl carbon of an aminoacyl phosphate oligonucleotide. The QM/MM umbrella sampling MD calculations showed that the height of the free-energy barrier for L-alanine aminoacylation reaction was 17 kcal/mol, which was 9 kcal/mol lower than that for the D-alanine system. At the transition state, the distance between the negatively charged 3′-oxygen and the positively charged amino group of L-alanine was shorter than that of D-alanine, which was caused by the chirality difference of the amino acid. These results indicate that the transition state for L-alanine is more electrostatically stabilized than that for D-alanine, which would be a plausible mechanism previously unexplained for chiral selectivity in the RNA minihelix aminoacylation.

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Aminoacylation of short hairpin RNAs through kissing-loop interactions indicates evolutionary trend of RNA molecules

Cited by 5 publications

References 49 publications

Acquisition of Dual Ribozyme-Functions in Nonfunctional Short Hairpin RNAs through Kissing-Loop Interactions

Acquisition of Dual Ribozyme-Functions in Nonfunctional Short Hairpin RNAs through Kissing-Loop Interactions

Peptide Bond Formation between Aminoacyl-Minihelices by a Scaffold Derived from the Peptidyl Transferase Center

Mechanism of Chiral-Selective Aminoacylation of an RNA Minihelix Explored by QM/MM Free-Energy Simulations

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