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RNA Biology, volume 18, issue 8, pages 1193-1205

Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment

Ogawa Tetsuhiro ^{1, 2}

Takahashi Kazutoshi ¹

Ishida Wataru ¹

AONO Toshihiro ^{2, 3}

Hidaka Makoto ^{1, 2}

Terada Tohru ^{1, 2}

Masaki Haruhiko ¹

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Department of Biotechnology, Graduate School of Agricultural and Life Sciences, the University of Tokyo, Tokyo, Japan |

Collaborative Research Institute for Innovative Microbiology, the University of Tokyo, Tokyo, Japan |

Biotechnology Research Center, The University of Tokyo, Tokyo, Japan |

Publication type: Journal Article

Publication date: 2020-11-19

Taylor & Francis

Journal: RNA Biology

Quartile SCImago

Quartile WOS

Impact factor: 4.1

ISSN: 15476286, 15558584

DOI: 10.1080/15476286.2020.1838782

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PubMed ID: 33211605

Molecular Biology

Cell Biology

Abstract

ABSTRACT Colicin D is a plasmid-encoded bacteriocin that specifically cleaves tRNAArg of sensitive Escherichia coli cells. E. coli has four isoaccepting tRNAArgs; the cleavage occurs at the 3′ end of anticodon-loop, leading to translation impairment in the sensitive cells. tRNAs form a common L-shaped structure and have many conserved nucleotides that limit tRNA identity elements. How colicin D selects tRNAArgs from the tRNA pool of sensitive E. coli cells is therefore intriguing. Here, we reveal the recognition mechanism of colicin D via biochemical analyses as well as structural modelling. Colicin D recognizes tRNAArg ICG, the most abundant species of E. coli tRNAArgs, at its anticodon-loop and D-arm, and selects it as the most preferred substrate by distinguishing its anticodon-loop sequence from that of others. It has been assumed that translation impairment is caused by a decrease in intact tRNA molecules due to cleavage. However, we found that intracellular levels of intact tRNAArg ICG do not determine the viability of sensitive cells after such cleavage; rather, an accumulation of cleaved ones does. Cleaved tRNAArg ICG dominant-negatively impairs translation in vitro. Moreover, we revealed that EF-Tu, which is required for the delivery of tRNAs, does not compete with colicin D for binding tRNAArg ICG, which is consistent with our structural model. Finally, elevation of cleaved tRNAArg ICG level decreases the viability of sensitive cells. These results suggest that cleaved tRNAArg ICG transiently occupies ribosomal A-site in an EF-Tu-dependent manner, leading to translation impairment. The strategy should also be applicable to other tRNA-targeting RNases, as they, too, recognize anticodon-loops. Abbreviations: mnm5U: 5-methylaminomethyluridine; mcm5s2U: 5-methoxycarbonylmethyl-2-thiouridine

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Citations by journals

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International Journal of Molecular Sciences	International Journal of Molecular Sciences, 2, 28.57% International Journal of Molecular Sciences 2 publications, 28.57%
Non-coding RNA	Non-coding RNA, 1, 14.29% Non-coding RNA 1 publication, 14.29%
Frontiers in Microbiology	Frontiers in Microbiology, 1, 14.29% Frontiers in Microbiology 1 publication, 14.29%
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Molecular Cell	Molecular Cell, 1, 14.29% Molecular Cell 1 publication, 14.29%
	1 2

Citations by publishers

	1 2 3
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 3, 42.86% Multidisciplinary Digital Publishing Institute (MDPI) 3 publications, 42.86%
Elsevier	Elsevier, 2, 28.57% Elsevier 2 publications, 28.57%
Frontiers Media S.A.	Frontiers Media S.A., 1, 14.29% Frontiers Media S.A. 1 publication, 14.29%
	1 2 3

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Ogawa T. et al. Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment // RNA Biology. 2020. Vol. 18. No. 8. pp. 1193-1205.

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Ogawa T., Takahashi K., Ishida W., AONO T., Hidaka M., Terada T., Masaki H. Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment // RNA Biology. 2020. Vol. 18. No. 8. pp. 1193-1205.

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RIS Copy

TY - JOUR

DO - 10.1080/15476286.2020.1838782

UR - https://doi.org/10.1080%2F15476286.2020.1838782

TI - Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment

T2 - RNA Biology

AU - Ogawa, Tetsuhiro

AU - Takahashi, Kazutoshi

AU - Ishida, Wataru

AU - AONO, Toshihiro

AU - Hidaka, Makoto

AU - Terada, Tohru

AU - Masaki, Haruhiko

PY - 2020

DA - 2020/11/19 00:00:00

PB - Taylor & Francis

SP - 1193-1205

IS - 8

VL - 18

PMID - 33211605

SN - 1547-6286

SN - 1555-8584

ER -

BibTex |

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BibTex Copy

@article{2020_Ogawa,

author = {Tetsuhiro Ogawa and Kazutoshi Takahashi and Wataru Ishida and Toshihiro AONO and Makoto Hidaka and Tohru Terada and Haruhiko Masaki},

title = {Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment},

journal = {RNA Biology},

year = {2020},

volume = {18},

publisher = {Taylor & Francis},

month = {nov},

url = {https://doi.org/10.1080%2F15476286.2020.1838782},

number = {8},

pages = {1193--1205},

doi = {10.1080/15476286.2020.1838782}

}

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Ogawa, Tetsuhiro, et al. “Substrate recognition mechanism of tRNA-targeting ribonuclease, colicin D, and an insight into tRNA cleavage-mediated translation impairment.” RNA Biology, vol. 18, no. 8, Nov. 2020, pp. 1193-1205. https://doi.org/10.1080%2F15476286.2020.1838782.

Found error?

Publisher

Taylor & Francis

Journal

RNA Biology

Quartile SCImago

Quartile WOS

Impact factor

4.1

ISSN

15476286 (Print)
15558584 (Electronic)