Importance of a tRNA anticodon loop modification and a conserved, noncanonical anticodon stem pairing in tRNACGGPro for decoding

Nguyen, Ha An; Hoffer, Eric D.; Dunham, Christine M.

doi:10.1074/jbc.RA119.007410

Title: Importance of a tRNA anticodon loop modification and a conserved, noncanonical anticodon stem pairing in tRNACGGPro for decoding

Journal Article · Mon Apr 01 00:00:00 EDT 2019 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA119.007410· OSTI ID:1769206

Nguyen, Ha An; Hoffer, Eric D.;

Modification of anticodon nucleotides allows tRNAs to decode multiple codons, expanding the genetic code. Additionally, modifications located in the anticodon loop, but outside the anticodon itself, stabilize tRNA–codon interactions, increasing decoding fidelity. Anticodon loop nucleotide 37 is 3' to the anticodon and, in tRNA$$_{CGG}^{Pro}$$, is methylated at the N1 position in its nucleobase (m¹G37). The m¹G37 modification in tRNA$$_{CGG}^{Pro}$$ stabilizes its interaction with the codon and maintains the mRNA frame. However, it is unclear how m¹G37 affects binding at the decoding center to both cognate and +1 slippery codons. Here, we show that the tRNA$$_{CGG}^{Pro}$$ m¹G37 modification is important for the association step during binding to a cognate CCG codon. In contrast, m¹G37 prevented association with a slippery CCC-U or +1 codon. Similar analyses of frameshift suppressor tRNA^SufA6, a tRNA$$_{CGG}^{Pro}$$ derivative containing an extra nucleotide in its anticodon loop that undergoes +1 frameshifting, reveal that m¹G37 destabilizes interactions with both the cognate CCG and slippery codons. One reason for this destabilization is the disruption of a conserved U32·A38 nucleotide pairing in the anticodon stem through insertion of G37.5. Restoring the tRNA^SufA6 U32·A37.5 pairing results in a high-affinity association on the slippery CCC-U codon. Further, an X-ray crystal structure of the 70S ribosome bound to tRNA^SufA6 U32·A37.5 at 3.6 Å resolution shows a reordering of the anticodon loop consistent with the findings from the high-affinity measurements. In conclusion, our results reveal how the tRNA modification at nucleotide 37 stabilizes interactions with the mRNA codon to preserve the mRNA frame.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); USDOE Office of Science (SC); National Science Foundation (NSF)

Grant/Contract Number:: P30 GM124165; RR25528; RR028976; AC02-06CH11357; W-31-109-Eng-38; R01 GM093278; CHE 1808711

OSTI ID:: 1769206

Alternate ID(s):: OSTI ID: 1513024

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 294 Journal Issue: 14; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 17 works

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Title: Importance of a tRNA anticodon loop modification and a conserved, noncanonical anticodon stem pairing in tRNACGGPro for decoding

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