An oxygen-sensitive toxin-antitoxin system

Oriol Marimon; João M.C. Teixeira; Tiago N. Cordeiro; Valerie W.C. Soo; Thammajun L. Wood; Maxim Mayzel; Irene Amata; Jesús García; Ainara Morera; Marina Gay; Marta Vilaseca; Vladislav Yu Orekhov; Thomas K. Wood; Miquel Pons

doi:10.1038/ncomms13634

An oxygen-sensitive toxin-antitoxin system

Oriol Marimon, João M.C. Teixeira, Tiago N. Cordeiro, Valerie W.C. Soo, Thammajun L. Wood, Maxim Mayzel, Irene Amata, Jesús García, Ainara Morera, Marina Gay, Marta Vilaseca, Vladislav Yu Orekhov, Thomas K. Wood, Miquel Pons

Research output: Contribution to journal › Article › peer-review

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Abstract

The Hha and TomB proteins from Escherichia coli form an oxygen-dependent toxin-antitoxin (TA) system. Here we show that YmoB, the Yersinia orthologue of TomB, and its single cysteine variant [C117S]YmoB can replace TomB as antitoxins in E. coli. In contrast to other TA systems, [C117S]YmoB transiently interacts with Hha (rather than forming a stable complex) and enhances the spontaneous oxidation of the Hha conserved cysteine residue to a -SO x H-containing species (sulfenic, sulfinic or sulfonic acid), which destabilizes the toxin. The nuclear magnetic resonance structure of [C117S]YmoB and the homology model of TomB show that the two proteins form a four-helix bundle with a conserved buried cysteine connected to the exterior by a channel with a diameter comparable to that of an oxygen molecule. The Hha interaction site is located on the opposite side of the helix bundle.

Original language	English (US)
Article number	13634
Journal	Nature communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms13634
State	Published - Dec 8 2016

All Science Journal Classification (ASJC) codes

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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@article{c4244bd33ffe4b24a99313066d50a7a5,

title = "An oxygen-sensitive toxin-antitoxin system",

abstract = "The Hha and TomB proteins from Escherichia coli form an oxygen-dependent toxin-antitoxin (TA) system. Here we show that YmoB, the Yersinia orthologue of TomB, and its single cysteine variant [C117S]YmoB can replace TomB as antitoxins in E. coli. In contrast to other TA systems, [C117S]YmoB transiently interacts with Hha (rather than forming a stable complex) and enhances the spontaneous oxidation of the Hha conserved cysteine residue to a -SO x H-containing species (sulfenic, sulfinic or sulfonic acid), which destabilizes the toxin. The nuclear magnetic resonance structure of [C117S]YmoB and the homology model of TomB show that the two proteins form a four-helix bundle with a conserved buried cysteine connected to the exterior by a channel with a diameter comparable to that of an oxygen molecule. The Hha interaction site is located on the opposite side of the helix bundle.",

author = "Oriol Marimon and Teixeira, {Jo{\~a}o M.C.} and Cordeiro, {Tiago N.} and Soo, {Valerie W.C.} and Wood, {Thammajun L.} and Maxim Mayzel and Irene Amata and Jes{\'u}s Garc{\'i}a and Ainara Morera and Marina Gay and Marta Vilaseca and Orekhov, {Vladislav Yu} and Wood, {Thomas K.} and Miquel Pons",

note = "Funding Information: This work was partially supported by funds from the Spanish MINECO (BIO2010-15683 and BIO2013-45793R cofounded with European Structural Funds, FEDER-), the EC FP7 BioNMR project (contract 261863) and the ARO (W911NF-14-1-0279). T.K.W. is the Biotechnology Endowed Professor at the Pennsylvania State University. NMR experiments were performed at the ICTS NMR LRB and CCITUB (University of Barcelona) and the Swedish NMR Centre (Goteborg University). MS experiments were performed at IRB Barcelona MS Core Facility (member of the BMBS COST Action BM 1403 and Proteored, PRB2-ISCIII (IPT13/0001ISCIII-SGEFI / ERDF). IRB Barcelona is the recipient of a Severo Ochoa Award of Excellence from MINECO (Government of Spain). Development of Chimera package by UCSF is supported by NIGMS P41-GM103311. Publisher Copyright: {\textcopyright} The Author(s) 2016.",

year = "2016",

month = dec,

day = "8",

doi = "10.1038/ncomms13634",

language = "English (US)",

volume = "7",

journal = "Nature communications",

issn = "2041-1723",

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T1 - An oxygen-sensitive toxin-antitoxin system

AU - Marimon, Oriol

AU - Teixeira, João M.C.

AU - Cordeiro, Tiago N.

AU - Soo, Valerie W.C.

AU - Wood, Thammajun L.

AU - Mayzel, Maxim

AU - Amata, Irene

AU - García, Jesús

AU - Morera, Ainara

AU - Gay, Marina

AU - Vilaseca, Marta

AU - Orekhov, Vladislav Yu

AU - Wood, Thomas K.

AU - Pons, Miquel

N1 - Funding Information: This work was partially supported by funds from the Spanish MINECO (BIO2010-15683 and BIO2013-45793R cofounded with European Structural Funds, FEDER-), the EC FP7 BioNMR project (contract 261863) and the ARO (W911NF-14-1-0279). T.K.W. is the Biotechnology Endowed Professor at the Pennsylvania State University. NMR experiments were performed at the ICTS NMR LRB and CCITUB (University of Barcelona) and the Swedish NMR Centre (Goteborg University). MS experiments were performed at IRB Barcelona MS Core Facility (member of the BMBS COST Action BM 1403 and Proteored, PRB2-ISCIII (IPT13/0001ISCIII-SGEFI / ERDF). IRB Barcelona is the recipient of a Severo Ochoa Award of Excellence from MINECO (Government of Spain). Development of Chimera package by UCSF is supported by NIGMS P41-GM103311. Publisher Copyright: © The Author(s) 2016.

PY - 2016/12/8

Y1 - 2016/12/8

N2 - The Hha and TomB proteins from Escherichia coli form an oxygen-dependent toxin-antitoxin (TA) system. Here we show that YmoB, the Yersinia orthologue of TomB, and its single cysteine variant [C117S]YmoB can replace TomB as antitoxins in E. coli. In contrast to other TA systems, [C117S]YmoB transiently interacts with Hha (rather than forming a stable complex) and enhances the spontaneous oxidation of the Hha conserved cysteine residue to a -SO x H-containing species (sulfenic, sulfinic or sulfonic acid), which destabilizes the toxin. The nuclear magnetic resonance structure of [C117S]YmoB and the homology model of TomB show that the two proteins form a four-helix bundle with a conserved buried cysteine connected to the exterior by a channel with a diameter comparable to that of an oxygen molecule. The Hha interaction site is located on the opposite side of the helix bundle.

AB - The Hha and TomB proteins from Escherichia coli form an oxygen-dependent toxin-antitoxin (TA) system. Here we show that YmoB, the Yersinia orthologue of TomB, and its single cysteine variant [C117S]YmoB can replace TomB as antitoxins in E. coli. In contrast to other TA systems, [C117S]YmoB transiently interacts with Hha (rather than forming a stable complex) and enhances the spontaneous oxidation of the Hha conserved cysteine residue to a -SO x H-containing species (sulfenic, sulfinic or sulfonic acid), which destabilizes the toxin. The nuclear magnetic resonance structure of [C117S]YmoB and the homology model of TomB show that the two proteins form a four-helix bundle with a conserved buried cysteine connected to the exterior by a channel with a diameter comparable to that of an oxygen molecule. The Hha interaction site is located on the opposite side of the helix bundle.

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U2 - 10.1038/ncomms13634

DO - 10.1038/ncomms13634

M3 - Article

C2 - 27929062

AN - SCOPUS:85005943302

SN - 2041-1723

VL - 7

JO - Nature communications

JF - Nature communications

M1 - 13634

ER -

An oxygen-sensitive toxin-antitoxin system

Abstract

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