Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability
Abstract
Chromosomally-encoded toxin-antitoxin complexes are ubiquitous in bacteria and regulate growth through the release of the toxin component typically in a stress-dependent manner. Type II ribosome-dependent toxins adopt a RelE-family RNase fold and inhibit translation by degrading mRNAs while bound to the ribosome. Here, we present biochemical and structural studies of the Escherichia coli YoeB toxin interacting with both a UAA stop and an AAU sense codon in pre- and post-mRNA cleavage states to provide insights into possible mRNA substrate selection. Both mRNAs undergo minimal changes during the cleavage event in contrast to type II ribosome-dependent RelE toxin. Further, the 16S rRNA decoding site nucleotides that monitor the mRNA in the aminoacyl(A) site adopt different orientations depending upon which toxin is present. Although YoeB is a RelE family member, it is the sole ribosome-dependent toxin that is dimeric. We show that engineered monomeric YoeB is active against mRNAs bound to both the small and large subunit. However, the stability of monomeric YoeB is reduced ~20°C, consistent with potential YoeB activation during heat shock in E. coli as previously demonstrated. These data provide a molecular basis for the ability of YoeB to function in response to thermal stress.
- Authors:
-
- Emory Univ. School of Medicine, Atlanta, GA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Institutes of Health (NIH)
- OSTI Identifier:
- 1573380
- Grant/Contract Number:
- AC02-06CH11357; R01GM093278; GM103403; S10 RR029205
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 47; Journal Issue: 19; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Pavelich, Ian J., Maehigashi, Tatsuya, Hoffer, Eric D., Ruangprasert, Ajchareeya, Miles, Stacey J., and Dunham, Christine M. Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability. United States: N. p., 2019.
Web. doi:10.1093/nar/gkz760.
Pavelich, Ian J., Maehigashi, Tatsuya, Hoffer, Eric D., Ruangprasert, Ajchareeya, Miles, Stacey J., & Dunham, Christine M. Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability. United States. https://doi.org/10.1093/nar/gkz760
Pavelich, Ian J., Maehigashi, Tatsuya, Hoffer, Eric D., Ruangprasert, Ajchareeya, Miles, Stacey J., and Dunham, Christine M. Tue .
"Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability". United States. https://doi.org/10.1093/nar/gkz760. https://www.osti.gov/servlets/purl/1573380.
@article{osti_1573380,
title = {Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability},
author = {Pavelich, Ian J. and Maehigashi, Tatsuya and Hoffer, Eric D. and Ruangprasert, Ajchareeya and Miles, Stacey J. and Dunham, Christine M.},
abstractNote = {Chromosomally-encoded toxin-antitoxin complexes are ubiquitous in bacteria and regulate growth through the release of the toxin component typically in a stress-dependent manner. Type II ribosome-dependent toxins adopt a RelE-family RNase fold and inhibit translation by degrading mRNAs while bound to the ribosome. Here, we present biochemical and structural studies of the Escherichia coli YoeB toxin interacting with both a UAA stop and an AAU sense codon in pre- and post-mRNA cleavage states to provide insights into possible mRNA substrate selection. Both mRNAs undergo minimal changes during the cleavage event in contrast to type II ribosome-dependent RelE toxin. Further, the 16S rRNA decoding site nucleotides that monitor the mRNA in the aminoacyl(A) site adopt different orientations depending upon which toxin is present. Although YoeB is a RelE family member, it is the sole ribosome-dependent toxin that is dimeric. We show that engineered monomeric YoeB is active against mRNAs bound to both the small and large subunit. However, the stability of monomeric YoeB is reduced ~20°C, consistent with potential YoeB activation during heat shock in E. coli as previously demonstrated. These data provide a molecular basis for the ability of YoeB to function in response to thermal stress.},
doi = {10.1093/nar/gkz760},
journal = {Nucleic Acids Research},
number = 19,
volume = 47,
place = {United States},
year = {Tue Sep 10 00:00:00 EDT 2019},
month = {Tue Sep 10 00:00:00 EDT 2019}
}
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Translation affects YoeB and MazF messenger RNA interferase activities by different mechanisms
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YoeB–ribosome structure: a canonical RNase that requires the ribosome for its specific activity
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Molecular basis of ribosome recognition and mRNA hydrolysis by the E. coli YafQ toxin
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Mechanism of endonuclease cleavage by the HigB toxin
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Escherichia coli ItaT is a type II toxin that inhibits translation by acetylating isoleucyl-tRNAIle
journal, June 2018
- Wilcox, Brendan; Osterman, Ilya; Serebryakova, Marina
- Nucleic Acids Research, Vol. 46, Issue 15
The bacterial translation stress response
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- FEMS Microbiology Reviews, Vol. 38, Issue 6
Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity
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- Overgaard, Martin; Borch, Jonas; Jørgensen, Mikkel G.
- Molecular Microbiology, Vol. 69, Issue 4
Bacterial toxin YafQ is an endoribonuclease that associates with the ribosome and blocks translation elongation through sequence-specific and frame-dependent mRNA cleavage
journal, March 2009
- Prysak, Meredith H.; Mozdzierz, Christopher J.; Cook, Angela M.
- Molecular Microbiology, Vol. 71, Issue 5
Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses
journal, January 2010
- Christensen-Dalsgaard, Mikkel; Jørgensen, Mikkel Girke; Gerdes, Kenn
- Molecular Microbiology, Vol. 75, Issue 2
Structure of the 70S Ribosome Complexed with mRNA and tRNA
journal, September 2006
- Selmer, M.
- Science, Vol. 313, Issue 5795
HicA of Escherichia coli Defines a Novel Family of Translation-Independent mRNA Interferases in Bacteria and Archaea
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- Jorgensen, M. G.; Pandey, D. P.; Jaskolska, M.
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F plasmid ccd mechanism in Escherichia coli.
journal, April 1986
- Hiraga, S.; Jaffé, A.; Ogura, T.
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Epistasis analysis of 16S rRNA ram mutations helps define the conformational dynamics of the ribosome that influence decoding
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mRNA bound to the 30S subunit is a HigB toxin substrate
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