Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA

Journal of Molecular Biology

Volumn 332, Issue 4, 2003, Pages 809-819

  Christensen, Susanne K ^a   Pedersen, Kim ^a   Hansen, Flemming G ^a,b   Gerdes, Kenn ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

chpA; MazF; mRNA cleavage; Nutritional stress; RelE

Indexed keywords

ANTITOXIN; CHROMOSOMAL HOMOLOG OF PEM A KILLER PROTEIN; CHROMOSOMAL HOMOLOG OF PEM B KILLER PROTEIN; MESSENGER RNA; PROTEIN; TOXIN; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; ESCHERICHIA COLI; GENE LOCUS; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN MALNUTRITION; RNA TRANSLATION; STRESS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 0041825422     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00922-7     Document Type: Article

References (31)

1. Cashel M., Gentry D., Hernandez V.J., Vinella D. The stringent response. Neidthardt F.C. Escherichia coli and Salmonella. 1996;1458-1496 ASM Press, Washington.
2. Christensen S.K., Mikkelsen M., Pedersen K., Gerdes K. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl Acad. Sci. USA. 98:2001;14328-14333.
3. Masuda Y., Miyakawa K., Nishimura Y., Ohtsubo E. chpA and chpB. Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100. J. Bacteriol. 175:1993;6850-6856.
4. Bravo A., de Torrontegui G., Diaz R. Identification of components of a new stability system of plasmid R1. ParD, that is close to the origin of replication of this plasmid. Mol. Gen. Genet. 210:1987;101-110.
5. Hiraga S., Jaffe A., Ogura T., Mori H., Takahashi H. F plasmid ccd mechanism in Escherichia coli. J. Bacteriol. 166:1986;100-104.
6. Jensen R.B., Gerdes K. Programmed cell death in bacteria: proteic plasmid stabilization systems. Mol. Microbiol. 17:1995;205-210.
7. Gotfredsen M., Gerdes K. The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol. Microbiol. 29:1998;1065-1076.
8. Gronlund H., Gerdes K. Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. J. Mol. Biol. 285:1999;1401-1415.
9. Gerdes K. Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J. Bacteriol. 182:2000;561-572.
10. Grady R., Hayes F. Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium. Mol. Microbiol. 47:2003;1419-1432.
11. Mittenhuber G. Occurrence of mazEF-like antitoxin/toxin systems in bacteria. J. Mol. Microbiol. Biotechnol. 1:1999;295-302.
12. Aizenman E., Engelberg-Kulka H., Glaser G. An Escherichia coli chromosomal "addiction module" regulated by guanosine 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl Acad. Sci. USA. 93:1996;6059-6063.
13. Marianovsky I., Aizenman E., Engelberg-Kulka H., Glaser G. The regulation of the Escherichia coli mazEF promoter involves an unusual alternating palindrome. J. Biol. Chem. 276:2001;5975-5984.
14. Pedersen K., Christensen S.K., Gerdes K. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol. 45:2002;501-510.
15. Ruiz-Echevarria M.J., Gimenez-Gallego G., Sabariegos-Jareno R., Diaz-Orejas R. Kid, a small protein of the parD stability system of plasmid R1, is an inhibitor of DNA replication acting at the initiation of DNA synthesis. J. Mol. Biol. 247:1995;568-577.
16. Galvani C., Terry J., Ishiguro E.E. Purification of the RelB and RelE proteins of Escherichia coli: RelE binds to RelB and to ribosomes. J. Bacteriol. 183:2001;2700-2703.
17. Pedersen K., Zavialov A.V., Pavlov M.Y., Elf J., Gerdes K., Ehrenberg M. The Bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell. 112:2003;131-140.
18. Christensen, S.K., Gerdes, K. (2003). RelE toxins from bacteria and archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol. Microbiol.
19. Lanzer M., Bujard H. Promoters largely determine the efficiency of repressor action. Proc. Natl Acad. Sci. USA. 85:1988;8973-8977.
20. Karzai A.W., Susskind M.M., Sauer R.T. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 18:1999;3793-3799.
21. Nakamura K., Pirtle R.M., Pirtle I.L., Takeishi K., Inouye M. Messenger ribonucleic acid of the lipoprotein of the Escherichia coli outer membrane. II. The complete nucleotide sequence. J. Biol. Chem. 255:1980;210-216.
22. Tosa T., Pizer L.I. Effect of serine hydroxamate on the growth of Escherichia coli. J. Bacteriol. 106:1971;966-971.
23. Hargreaves D., Santos-Sierra S., Giraldo R., Sabariegos-Jareno R., Cueva-Mendez G., Boelens R., et al. Structural and functional analysis of the kid toxin protein from E. coli plasmid R1. Structure (Camb.). 10:2002;1425-1433.
24. Kuroda A., Murphy H., Cashel M., Kornberg A. Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J. Biol. Chem. 272:1997;21240-21243.
25. Kuroda A., Nomura K., Ohtomo R., Kato J., Ikeda T., Takiguchi N., et al. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science. 293:2001;705-708.
26. Kuroda A., Tanaka S., Ikeda T., Kato J., Takiguchi N., Ohtake H. Inorganic polyphosphate kinase is required to stimulate protein degradation and for adaptation to amino acid starvation in Escherichia coli. Proc. Natl Acad. Sci. USA. 96:1999;14264-14269.
27. Chang D.E., Smalley D.J., Conway T. Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model. Mol. Microbiol. 45:2002;289-306.
28. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA. 97:2000;6640-6645.
29. Bertani G. Studies of lysogenesis I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:1951;293-300.
30. Xiao H., Kalman M., Ikehara K., Zemel S., Glaser G., Cashel M. Residual guanosine 3′,5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266:1991;5980-5990.
31. Metzger S., Sarubbi E., Glaser G., Cashel M. Protein sequences encoded by the relA and the spoT genes of Escherichia coli are interrelated. J. Biol. Chem. 264:1989;9122-9125.