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The bacterial antitoxin HipB establishes a ternary complex with operator DNA and phosphorylated toxin HipA to regulate bacterial persistence.

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Wen Y, Behiels E, Felix J, Elegheert J, Vergauwen B, Devreese B, Savvides SN
OpenAccess logo Nucleic Acids Res 42 10134-47 (2014)
Related entries: 4pu3, 4pu4, 4pu5, 4pu8

Cited: 33 times
EuropePMC logo PMID: 25056321

Abstract

Nearly all bacteria exhibit a type of phenotypic growth described as persistence that is thought to underlie antibiotic tolerance and recalcitrant chronic infections. The chromosomally encoded high-persistence (Hip) toxin-antitoxin proteins HipASO and HipBSO from Shewanella oneidensis, a proteobacterium with unusual respiratory capacities, constitute a type II toxin-antitoxin protein module. Here we show that phosphorylated HipASO can engage in an unexpected ternary complex with HipBSO and double-stranded operator DNA that is distinct from the prototypical counterpart complex from Escherichia coli. The structure of HipBSO in complex with operator DNA reveals a flexible C-terminus that is sequestered by HipASO in the ternary complex, indicative of its role in binding HipASO to abolish its function in persistence. The structure of HipASO in complex with a non-hydrolyzable ATP analogue shows that HipASO autophosphorylation is coupled to an unusual conformational change of its phosphorylation loop. However, HipASO is unable to phosphorylate the translation factor Elongation factor Tu, contrary to previous reports, but in agreement with more recent findings. Our studies suggest that the phosphorylation state of HipA is an important factor in persistence and that the structural and mechanistic diversity of HipAB modules as regulatory factors in bacterial persistence is broader than previously thought.

Reviews - 4pu7 mentioned but not cited (1)

  1. Wake me when it's over - Bacterial toxin-antitoxin proteins and induced dormancy. Coussens NP, Daines DA. Exp Biol Med (Maywood) 241 1332-1342 (2016)

Articles - 4pu7 mentioned but not cited (3)

  1. The bacterial antitoxin HipB establishes a ternary complex with operator DNA and phosphorylated toxin HipA to regulate bacterial persistence. Wen Y, Behiels E, Felix J, Elegheert J, Vergauwen B, Devreese B, Savvides SN. Nucleic Acids Res 42 10134-10147 (2014)
  2. Structure and DNA damage-dependent derepression mechanism for the XRE family member DG-DdrO. Lu H, Wang L, Li S, Pan C, Cheng K, Luo Y, Xu H, Tian B, Zhao Y, Hua Y. Nucleic Acids Res 47 9925-9933 (2019)
  3. Structural basis of DNA binding by YdaT, a functional equivalent of the CII repressor in the cryptic prophage CP-933P from Escherichia coli O157:H7. Prolič-Kalinšek M, Volkov AN, Hadži S, Van Dyck J, Bervoets I, Charlier D, Loris R. Acta Crystallogr D Struct Biol 79 245-258 (2023)


Reviews citing this publication (5)

  1. Keeping the Wolves at Bay: Antitoxins of Prokaryotic Type II Toxin-Antitoxin Systems. Chan WT, Espinosa M, Yeo CC. Front Mol Biosci 3 9 (2016)
  2. Toxin-antitoxin systems and their role in disseminating and maintaining antimicrobial resistance. Yang QE, Walsh TR. FEMS Microbiol Rev 41 343-353 (2017)
  3. Phenotypic Heterogeneity, a Phenomenon That May Explain Why Quorum Sensing Does Not Always Result in Truly Homogenous Cell Behavior. Grote J, Krysciak D, Streit WR. Appl Environ Microbiol 81 5280-5289 (2015)
  4. The Variety in the Common Theme of Translation Inhibition by Type II Toxin-Antitoxin Systems. Jurėnas D, Van Melderen L. Front Genet 11 262 (2020)
  5. Clostridium difficile recurrent infection: possible implication of TA systems. Gil F, Pizarro-Guajardo M, Álvarez R, Garavaglia M, Paredes-Sabja D. Future Microbiol 10 1649-1657 (2015)

Articles citing this publication (24)

  1. Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases. Germain E, Roghanian M, Gerdes K, Maisonneuve E. Proc Natl Acad Sci U S A 112 5171-5176 (2015)
  2. Identification and characterization of a HEPN-MNT family type II toxin-antitoxin in Shewanella oneidensis. Yao J, Guo Y, Zeng Z, Liu X, Shi F, Wang X. Microb Biotechnol 8 961-973 (2015)
  3. The chromosomal SezAT toxin-antitoxin system promotes the maintenance of the SsPI-1 pathogenicity island in epidemic Streptococcus suis. Yao X, Chen T, Shen X, Zhao Y, Wang M, Rao X, Yin S, Wang J, Gong Y, Lu S, Le S, Tan Y, Tang J, Fuquan H, Li M. Mol Microbiol 98 243-257 (2015)
  4. Type II toxin/antitoxin system ParESO /CopASO stabilizes prophage CP4So in Shewanella oneidensis. Yao J, Guo Y, Wang P, Zeng Z, Li B, Tang K, Liu X, Wang X. Environ Microbiol 20 1224-1239 (2018)
  5. A dual role in regulation and toxicity for the disordered N-terminus of the toxin GraT. Talavera A, Tamman H, Ainelo A, Konijnenberg A, Hadži S, Sobott F, Garcia-Pino A, Hõrak R, Loris R. Nat Commun 10 972 (2019)
  6. Why Close a Bacterial Genome? The Plasmid of Alteromonas Macleodii HOT1A3 is a Vector for Inter-Specific Transfer of a Flexible Genomic Island. Fadeev E, De Pascale F, Vezzi A, Hübner S, Aharonovich D, Sher D. Front Microbiol 7 248 (2016)
  7. Structural Insights Into the Transcriptional Regulation of HigBA Toxin-Antitoxin System by Antitoxin HigA in Pseudomonas aeruginosa. Liu Y, Gao Z, Liu G, Geng Z, Dong Y, Zhang H. Front Microbiol 10 3158 (2019)
  8. Mechanistic insight into how multidrug resistant Acinetobacter baumannii response regulator AdeR recognizes an intercistronic region. Wen Y, Ouyang Z, Yu Y, Zhou X, Pei Y, Devreese B, Higgins PG, Zheng F. Nucleic Acids Res 45 9773-9787 (2017)
  9. Characterization of YjjJ toxin of Escherichia coli. Maeda Y, Lin CY, Ishida Y, Inouye M, Yamaguchi Y, Phadtare S. FEMS Microbiol Lett 364 (2017)
  10. Functional investigation of the chromosomal ccdAB and hipAB operon in Escherichia coli Nissle 1917. Xu J, Xia K, Li P, Qian C, Li Y, Liang X. Appl Microbiol Biotechnol 104 6731-6747 (2020)
  11. Complete Genome Sequence of Highly Virulent Aeromonas hydrophila Strain D4, Isolated from a Diseased Blunt-Snout Bream in China. Zhu L, Zheng JS, Wang WM, Luo Y. Microbiol Resour Announc 8 e01035-18 (2019)
  12. Phylogeny Reveals Novel HipA-Homologous Kinase Families and Toxin-Antitoxin Gene Organizations. Gerdes K, Bærentsen R, Brodersen DE. mBio 12 e0105821 (2021)
  13. ATP and autophosphorylation driven conformational changes of HipA kinase revealed by ion mobility and crosslinking mass spectrometry. Wen Y, Sobott F, Devreese B. Anal Bioanal Chem 408 5925-5933 (2016)
  14. Characterization of Two Toxin-Antitoxin Systems in Deep-Sea Streptomyces sp. SCSIO 02999. Zhan W, Yao J, Tang K, Li Y, Guo Y, Wang X. Mar Drugs 17 E211 (2019)
  15. Molecular mechanism of toxin neutralization in the HipBST toxin-antitoxin system of Legionella pneumophila. Zhen X, Wu Y, Ge J, Fu J, Ye L, Lin N, Huang Z, Liu Z, Luo ZQ, Qiu J, Ouyang S. Nat Commun 13 4333 (2022)
  16. Functional diversification despite structural congruence in the HipBST toxin-antitoxin system of Legionella pneumophila. Lin JD, Stogios PJ, Abe KT, Wang A, MacPherson J, Skarina T, Gingras A-C, Savchenko A, Ensminger AW. mBio 14 e0151023 (2023)
  17. Structural basis for kinase inhibition in the tripartite E. coli HipBST toxin-antitoxin system. Bærentsen RL, Nielsen SV, Skjerning RB, Lyngsø J, Bisiak F, Pedersen JS, Gerdes K, Sørensen MA, Brodersen DE. Elife 12 RP90400 (2023)
  18. A Bibliometric Analysis of Research on Bacterial Persisters. Ju Y, Zhang F, Yu P, Zhang Y, Zhao P, Xu P, Sun L, Bao Y, Long H. Biomed Res Int 2023 4302914 (2023)
  19. Characterization of the Key Determinants of Phd Antitoxin Mediated Doc Toxin Inactivation in Salmonella. de Castro GV, Worm DJ, Grabe GJ, Rowan FC, Haggerty L, de la Lastra AL, Popescu O, Helaine S, Barnard A. ACS Chem Biol 17 1598-1606 (2022)
  20. Immune Response Modulation by Pseudomonas aeruginosa Persister Cells. Hastings CJ, Himmler GE, Patel A, Marques CNH. mBio 14 e0005623 (2023)
  21. Insights into virulence: structure classification of the Vibrio parahaemolyticus RIMD mobilome. Kinch LN, Schaeffer RD, Zhang J, Cong Q, Orth K, Grishin N. mSystems 8 e0079623 (2023)
  22. Search for Origins of Anti-CRISPR Proteins by Structure Comparison. Sahakyan H, Makarova KS, Koonin EV. CRISPR J 6 222-231 (2023)
  23. The Haemophilus influenzae HipBA toxin-antitoxin system adopts an unusual three-com-ponent regulatory mechanism. Koo JS, Kang SM, Jung WM, Kim DH, Lee BJ. IUCrJ 9 625-631 (2022)
  24. Type II bacterial toxin-antitoxins: hypotheses, facts, and the newfound plethora of the PezAT system. Chan WT, Garcillán-Barcia MP, Yeo CC, Espinosa M. FEMS Microbiol Rev 47 fuad052 (2023)


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