Literature DB >> 24449860

Toxin Kid uncouples DNA replication and cell division to enforce retention of plasmid R1 in Escherichia coli cells.

Belén Pimentel1, Radhika Nair, Camino Bermejo-Rodríguez, Mark A Preston, Chukwuma A Agu, Xindan Wang, Juan A Bernal, David J Sherratt, Guillermo de la Cueva-Méndez.   

Abstract

Worldwide dissemination of antibiotic resistance in bacteria is facilitated by plasmids that encode postsegregational killing (PSK) systems. These produce a stable toxin (T) and a labile antitoxin (A) conditioning cell survival to plasmid maintenance, because only this ensures neutralization of toxicity. Shortage of antibiotic alternatives and the link of TA pairs to PSK have stimulated the opinion that premature toxin activation could be used to kill these recalcitrant organisms in the clinic. However, validation of TA pairs as therapeutic targets requires unambiguous understanding of their mode of action, consequences for cell viability, and function in plasmids. Conflicting with widespread notions concerning these issues, we had proposed that the TA pair kis-kid (killing suppressor-killing determinant) might function as a plasmid rescue system and not as a PSK system, but this remained to be validated. Here, we aimed to clarify unsettled mechanistic aspects of Kid activation, and of the effects of this for kis-kid-bearing plasmids and their host cells. We confirm that activation of Kid occurs in cells that are about to lose the toxin-encoding plasmid, and we show that this provokes highly selective restriction of protein outputs that inhibits cell division temporarily, avoiding plasmid loss, and stimulates DNA replication, promoting plasmid rescue. Kis and Kid are conserved in plasmids encoding multiple antibiotic resistance genes, including extended spectrum β-lactamases, for which therapeutic options are scarce, and our findings advise against the activation of this TA pair to fight pathogens carrying these extrachromosomal DNAs.

Entities:  

Keywords:  PemK; RNase; mRNA interferase; parD; plasmid stability

Mesh:

Substances:

Year:  2014        PMID: 24449860      PMCID: PMC3932891          DOI: 10.1073/pnas.1308241111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  45 in total

Review 1.  Prevalence and significance of plasmid maintenance functions in the virulence plasmids of pathogenic bacteria.

Authors:  Manjistha Sengupta; Stuart Austin
Journal:  Infect Immun       Date:  2011-05-09       Impact factor: 3.441

2.  Xylella fastidiosa plasmid-encoded PemK toxin is an endoribonuclease.

Authors:  Min Woo Lee; Elizabeth E Rogers; Drake C Stenger
Journal:  Phytopathology       Date:  2012-01       Impact factor: 4.025

3.  RNase/anti-RNase activities of the bacterial parD toxin-antitoxin system.

Authors:  Ana J Muñoz-Gómez; Marc Lemonnier; Sandra Santos-Sierra; Alfredo Berzal-Herranz; Ramón Díaz-Orejas
Journal:  J Bacteriol       Date:  2005-05       Impact factor: 3.490

4.  Kid cleaves specific mRNAs at UUACU sites to rescue the copy number of plasmid R1.

Authors:  Belén Pimentel; Mark A Madine; Guillermo de la Cueva-Méndez
Journal:  EMBO J       Date:  2005-09-15       Impact factor: 11.598

5.  Programmed cell death by hok/sok of plasmid R1: processing at the hok mRNA 3'-end triggers structural rearrangements that allow translation and antisense RNA binding.

Authors:  T Franch; A P Gultyaev; K Gerdes
Journal:  J Mol Biol       Date:  1997-10-17       Impact factor: 5.469

6.  Two genes, pemK and pemI, responsible for stable maintenance of resistance plasmid R100.

Authors:  S Tsuchimoto; H Ohtsubo; E Ohtsubo
Journal:  J Bacteriol       Date:  1988-04       Impact factor: 3.490

7.  Comparison of ccd of F, parDE of RP4, and parD of R1 using a novel conditional replication control system of plasmid R1.

Authors:  R B Jensen; E Grohmann; H Schwab; R Díaz-Orejas; K Gerdes
Journal:  Mol Microbiol       Date:  1995-07       Impact factor: 3.501

8.  Recent advancements in toxin and antitoxin systems involved in bacterial programmed cell death.

Authors:  Ming-Xi Hu; Xiao Zhang; Er-Li Li; Yong-Jun Feng
Journal:  Int J Microbiol       Date:  2010-12-27

Review 9.  Gene and cell survival: lessons from prokaryotic plasmid R1.

Authors:  Guillermo de la Cueva-Méndez; Belén Pimentel
Journal:  EMBO Rep       Date:  2007-05       Impact factor: 8.807

10.  Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15.

Authors:  Teresa M Coque; Angela Novais; Alessandra Carattoli; Laurent Poirel; Johann Pitout; Luísa Peixe; Fernando Baquero; Rafael Cantón; Patrice Nordmann
Journal:  Emerg Infect Dis       Date:  2008-02       Impact factor: 6.883

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  6 in total

Review 1.  Plasmids in the driving seat: The regulatory RNA Rcd gives plasmid ColE1 control over division and growth of its E. coli host.

Authors:  Hannah Gaimster; David Summers
Journal:  Plasmid       Date:  2014-11-11       Impact factor: 3.466

2.  Coupling between the basic replicon and the Kis-Kid maintenance system of plasmid R1: modulation by Kis antitoxin levels and involvement in control of plasmid replication.

Authors:  Juan López-Villarejo; Damián Lobato-Márquez; Ramón Díaz-Orejas
Journal:  Toxins (Basel)       Date:  2015-02-05       Impact factor: 4.546

Review 3.  Toxin-Antitoxin Modules Are Pliable Switches Activated by Multiple Protease Pathways.

Authors:  Meenakumari Muthuramalingam; John C White; Christina R Bourne
Journal:  Toxins (Basel)       Date:  2016-07-09       Impact factor: 4.546

4.  Plasmid interference for curing antibiotic resistance plasmids in vivo.

Authors:  Muhammad Kamruzzaman; Shereen Shoma; Christopher M Thomas; Sally R Partridge; Jonathan R Iredell
Journal:  PLoS One       Date:  2017-02-28       Impact factor: 3.240

Review 5.  The Importance of the Expendable: Toxin-Antitoxin Genes in Plasmids and Chromosomes.

Authors:  Ramón Díaz-Orejas; Manuel Espinosa; Chew Chieng Yeo
Journal:  Front Microbiol       Date:  2017-08-04       Impact factor: 5.640

6.  Identification of novel mazEF/pemIK family toxin-antitoxin loci and their distribution in the Staphylococcus genus.

Authors:  Michal Bukowski; Karolina Hyz; Monika Janczak; Marcin Hydzik; Grzegorz Dubin; Benedykt Wladyka
Journal:  Sci Rep       Date:  2017-10-18       Impact factor: 4.379

  6 in total

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