Toxin-antitoxin regulation: Bimodal interaction of YefM-YoeB with paired DNA palindromes exerts transcriptional autorepression

Nucleic Acids Research

Volumn 35, Issue 1, 2007, Pages 325-339

  Kȩdzierska, Barbara ^b   Lian, Lu Yun ^a   Hayes, Finbarr ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; BETA GALACTOSIDASE; ESCHERICHIA COLI ENDOTOXIN; HISTIDINE; OLIGONUCLEOTIDE; PALINDROMIC DNA; PROTEIN YEFM; PROTEIN YOEB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CIRCULAR DICHROISM; DNA BINDING; DNA PROTEIN COMPLEX; ENHANCER REGION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACID STRUCTURE; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN SYNTHESIS;

BACTERIAL TOXINS; BASE SEQUENCE; BINDING SITES; DIMERIZATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; MOLECULAR SEQUENCE DATA; OPERATOR REGIONS (GENETICS); PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, SECONDARY; REPETITIVE SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33846680128     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl1028     Document Type: Article

References (54)

1. Potts,M. (2001) Desiccation tolerance: A simple process? Trends Microbiol., 9, 553-559.
2. Chang,D.E., Smalley,D.J., Tucker,D.L., Leatham,M.P., Norris,W.E., Stevenson,S.J., Anderson,A.B., Grissom,J.E., Laux,D.C., Cohen,P.S. et al. (2004) Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl Acad. Sci. USA, 101, 7427-7432.
3. Nystrom,T. (2004) Stationary-phase physiology. Annu. Rev. Microbiol., 58, 161-181.
4. Shapiro,J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol., 52, 81-104.
5. Hall-Stoodley,L., Costerton,J.W. and Stoodley,P. (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nature Rev. Microbiol., 2, 95-108.
6. Camilli,A. and Bassler,B.L. (2006) Bacterial small-molecule signaling pathways. Science, 311, 1113-1116.
7. Hayes,F. (2003) Toxins-antitoxins: Plasmid maintenance, programmed cell death, and cell cycle arrest. Science, 301, 1496-1499.
8. Anantharaman,V. and Aravind,L. (2003) New connections in the prokaryotic toxin-antitoxin network: Relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol., 4, R81.
9. Pandey,D.P. and Gerdes,K. (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res., 33, 966-976.
10. Engelberg-Kulka,H. and Glaser,G. (1999) Addiction modules and programmed cell death and antideath in bacterial cultures. Annu. Rev. Microbiol., 53, 43-70.
11. Hazan,R., Sat,B. and Engelberg-Kulka,H. (2004) Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol., 186, 3663-3669.
12. Pedersen,K., Zavialov,A.V., Pavlov,M.Y., Elf,J., Gerdes,K. and Ehrenberg,M. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell, 112, 131-140.
13. Christensen,S.K., Mikkelsen,M., Pedersen,K. and Gerdes,K. (2001) RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl Acad. Sci. USA, 98, 14328-14333.
14. Engelberg-Kulka,H., Sat,B., Reches,M., Amitai,S. and Hazan,R. (2004) Bacterial programmed cell death systems as targets for antibiotics. Trends Microbiol., 12, 66-71.
15. Zhang,Y., Zhang,J., Hara,H., Kato,I. and Inouye,M. (2005) Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J. Biol. Chem., 280, 3143-3150.
16. Munoz-Gomez,A.J., Santos-Sierra,S., Berzal-Herranz,A., Lemonnier,M. and Diaz-Orejas,R. (2004) Insights into the specificity of RNA cleavage by the Escherichia coli MazF toxin. FEBS Lett., 567, 316-320.
17. Christensen,S.K., Pedersen,K., Hansen,F.G. and Gerdes,K. (2003) Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J. Mol. Biol., 332, 809-819.
18. Pomerantsev,A.P., Golovliov,I.R., Ohara,Y., Mokrievich,A.N., Obuchi,M., Norqvist,A., Kuoppa,K. and Pavlov,V.M. (2001) Genetic organization of the Francisella plasmid pFNL10. Plasmid, 46, 210-222.
19. Grady,R. and Hayes,F. (2003) Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of, Enterococcus faecium. Mol. Microbiol., 47, 1419-1432.
20. Cherny,I., Rockah,L. and Gazit,E. (2005) The YoeB toxin is a folded protein that forms a physical complex with the unfolded YefM antitoxin. Implications for a structural-based differential stability of toxin-antitoxin systems. J. Biol. Chem., 280, 30063-30072.
21. Kamada,K. and Hanaoka,F. (2005) Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol. Cell, 19, 497-509.
22. Christensen,S.K., Maenhaut-Michel,G., Mine,N., Gottesman,S., Gerdes,K. and Van Melderen,L. (2004) Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: Involvement of the yefM-yoeB toxin-antitoxin system. Mol. Microbiol., 51, 1705-1717.
23. Ren,D., Bedzyk,L.A., Thomas,S.M., Ye,R.W. and Wood,T.K. (2004) Gene expression in Escherichia coli biofilms. Appl. Microbiol. Biotechnol., 64, 515-524.
24. Cherny,I. and Gazit,E. (2004) The YefM antitoxin defines a family of natively unfolded proteins: Implications as a novel antibacterial target. J. Biol. Chem., 279, 8252-8261.
25. Ruiz-Echevarria,M.J., Berzal-Herranz,A., Gerdes,K. and Diaz-Orejas,R. (1991) The kis and kid genes of the parD maintenance system of plasmid R1 form an operon that is autoregulated at the level of transcription by the co-ordinated action of the Kis and Kid proteins. Mol. Microbiol., 5, 2685-2693.
26. Magnuson,R. and Yarmolinsky,M.B. (1998) Corepression of the P1 addiction operon by Phd and Doc. J. Bacteriol., 180, 6342-6351.
27. Gotfredsen,M. and Gerdes,K. (1998) The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol. Microbiol., 29, 1065-1076.
28. Gazit,E. and Sauer,R.T. (1999) Stability and DNA binding of the Phd protein of the phage P1 plasmid addiction system. J. Biol. Chem., 274, 2652-2657.
29. Afif,H., Allali,N., Couturier,M. and Van Melderen,L. (2001) The ratio between CcdA and CcdB modulates the transcriptional repression of the ccd poison-antidote system. Mol. Microbiol., 41, 73-82.
30. Marianovsky,I., Aizenman,E., Engelberg-Kulka,H. and Glaser,G. (2001) The regulation of the Escherichia coli mazEF promoter involves an unusual alternating palindrome. J. Biol. Chem., 276, 5975-5984.
31. Dao-Thi,M.H., Charlier,D., Loris,R., Maes,D., Messens,J., Wyns,L. and Backmann,J. (2002) Intricate interactions within the ccd plasmid addiction system. J. Biol. Chem., 277, 3733-3742.
32. Lemonnier,M., Santos-Sierra,S., Pardo-Abarrio,C. and Diaz-Orejas,R. (2004) Identification of residues of the Kid toxin involved in autoregulation of the parD system. J. Bacteriol., 186, 240-243.
33. Zhao,X. and Magnuson,R.D. (2005) Percolation of the Phd repressor-operator interface. J. Bacteriol., 187, 1901-1912.
34. Simons,R.W., Houman,F. and Kleckner,N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene, 53, 85-96.
35. BAD promoter. J. Bacteriol., 177, 4121-4130.
36. Hayes,F., Radnedge,L., Davis,M.A. and Austin,S.J. (1994) The homologous operons for P1 and P7 plasmid partition are autoregulated from dissimilar operator sites. Mol. Microbiol., 11, 249-260.
37. Miller,J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual for Escherichia coli and Related Bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 72-74.
38. Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
39. Thompson,J.D., Higgins,D.G. and Gibson,T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
40. Linding,R., Russell,R.B., Neduva,V. and Gibson,T.J. (2003) GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res., 31, 3701-3708.
41. Frunzio,R., Bruni,C.B. and Blasi,F. (1981) In vivo and in vitro detection of the leader RNA of the histidine operon of Escherichia coli K-12. Proc. Natl Acad. Sci. USA, 78, 2767-2771.
42. Verde,P., Frunzio,R., di Nocera,P.P., Blasi,F. and Bruni,C.B. (1981) Identification, nucleotide sequence and expression of the regulatory region of the histidine operon of Escherichia coli K-12. Nucleic Acids Res., 9, 2075-2086.
43. Patzer,S.I. and Hantke,K. (2000) The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J. Biol. Chem., 275, 24321-24332.
44. Rojo,F. (2001) Mechanisms of transcriptional repression. Curr. Opin. Microbiol., 4, 145-151.
45. Zhou,N.E., Kay,C.M. and Hodges,R.S. (1992) Synthetic model proteins. Positional effects of interchain hydrophobic interactions on stability of two-stranded α-helical coiled-coils. J. Biol. Chem., 267, 2664-2670.
46. Sreerama,N. and Woody,R.W. (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set. Anal. Biochem., 287, 252-260.
47. Sprecher,C.A., Baase,W.A. and Johnson,W.C.,Jr (1979) Conformation and circular dichroism of DNA. Biopolymers, 18, 1009-1019.
48. Santos-Sierra,S., Giraldo,R. and Diaz-Orejas,R. (1998) Functional interactions between chpB and parD, two homologous conditional killer systems found in the Escherichia coli chromosome and in plasmid R1. FEMS Microbiol. Lett., 168, 51-58.
49. Erie,D.A., Yang,G., Schultz,H.C. and Bustamante,C. (1994) DNA bending by Cro protein in specific and nonspecific complexes: Implications for protein site recognition and specificity. Science, 266, 1562-1566.
50. Spronk,C.A., Folkers,G.E., Noordman,A.M., Wechselberger,R., van den Brink,N., Boelens,R. and Kaptein,R. (1999) Hinge-helix formation and DNA bending in various lac repressor-operator complexes. EMBO J., 18, 6472-6480.
51. Akakura,R. and Winans,S.C. (2002) Mutations in the occQ operator that decrease OccR-induced DNA bending do not cause constitutive promoter activity. J. Biol. Chem., 277, 15773-15780.
52. Schumacher,M.A., Miller,M.C., Grkovic,S., Brown,M.H., Skurray,R.A. and Brennan,R.G. (2002) Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J., 21, 1210-1218.
53. Magnuson,R., Lehnherr,H., Mukhopadhyay,G. and Yarmolinsky,M.B. (1996) Autoregulation of the plasmid addiction operon of bacteriophage P1. J. Biol. Chem., 271, 18705-18710.
54. Smith,J.A. and Magnuson,R.D. (2004) Modular organization of the Phd repressor/antitoxin protein. J. Bacteriol., 186, 2692-2698.