Escherichia coli antitoxin MazE as transcription factor: Insights into MazE-DNA binding

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 1241-1256

  Zorzini, Valentina ^a,b   Buts, Lieven ^a,b   Schrank, Evelyne ^c   Sterckx, Yann G J ^a,b   Respondek, Michal ^c   Engelberg Kulka, Hanna ^d   Loris, Remy ^a,b   Zangger, Klaus ^c   Van Nuland, Nico A J ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY OF GRAZ   (Austria)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; MAZE PROTEIN, E COLI; MAZF PROTEIN, E COLI; PROTEIN BINDING; RIBONUCLEASE; TRANSCRIPTION FACTOR;

CHEMICAL STRUCTURE; CHEMISTRY; INVERTED REPEAT; METABOLISM; OPERATOR GENE; PROTEIN TERTIARY STRUCTURE;

DNA, BACTERIAL; DNA-BINDING PROTEINS; ENDORIBONUCLEASES; ESCHERICHIA COLI PROTEINS; INVERTED REPEAT SEQUENCES; MODELS, MOLECULAR; OPERATOR REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 84945177148     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1352     Document Type: Article

References (62)

1. Bravo, A., de Torrontegui, G., Dz, R. (1987) 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, 101-110.
2. Brown, J.M., Shaw, K.J. (2003) A novel family of Escherichia coli toxin-antitoxin gene pairs. J. Bacteriol., 185, 6600-6608.
3. Pandey, D.P., Gerdes, K. (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res., 33, 966-976.
4. Gerdes, K., Wagner, E.G.H. (2007) RNA antitoxins. Curr. Opin. Microbiol., 10, 117-124
5. Buts, L., Lah, J., Dao-Thi, M., Wyns, L., Loris, R. (2005) Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci., 30, 672-679.
6. Fineran, P.C., Blower, T.R., Foulds, I.J., Humphreys, D.P., Lilley, K.S., Salmond, G.P.C. (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. U.S.A., 106, 894-899.
7. Wang, X., Lord, D.M., Cheng, H.Y., Osbourne, D.O., Hong, S.H., Sanchez-Torres, V., Quiroga, C., Zheng, K., Herrmann, T., Peti, W. et al. (2012) A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol., 8, 855-861.
8. Wang, X., Lord, D.M., Hong, S.H., Peti, W., Benedik, M.J., Page, R., Wood, T.K. (2013) Type II toxin/antitoxin MqsR/MqsA controls type V toxin/antitoxin GhoT/GhoS. Environ. Microbiol., 15, 1734-1744.
9. Garcia-Pino, A., Balasubramanian, S., Wyns, L., Gazit, E., De Greve, H., Magnuson, R.D., Charlier, D., van Nuland, N.A., Loris, R. (2010) Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell, 142, 101-111.
10. De Jonge, N., Garcia-Pino, A., Buts, L., Haesaerts, S., Charlier, D., Zangger, K., Wyns, L., De Greve, H., Loris, R. (2009) Rejuvenation of CcdB-poisoned gyrase by an intrinsically disordered protein domain. Mol. Cell, 35, 154-163.
11. Overgaard, M., Borch, J., Jgensen, M.G., Gerdes, K. (2008) Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity. Mol. Microbiol., 69, 841-857.
12. Afif, H., Allali, N., Couturier, M., 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.
13. Gerdes, K., Rasmussen, P.B., Molin, S. (1986b) Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc. Natl. Acad. Sci. U.S.A., 83, 3116-3120.
14. Roberts, R.C., Str m, A.R., Helinski, D.R. (1994) The parDE operon of the broad-host-range plasmid RK2 specifies growth inhibition associated with plasmid loss. J. Mol. Biol., 237, 35-51.
15. Christensen, S.K., Mikkelsen, M., Pedersen, K., Gerdes, K. (2001) RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl. Acad. Sci. U.S.A., 98, 14328-14333.
16. Albrethsen, J., Agner, J., Piersma, S.R., Hrup, P., Pham, T.V., Weldingh, K., Jimenez, C.R., Andersen, P., Rosenkrands, I. (2013) Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems. Mol. Cell. Proteomics., 12, 1180-1191.
17. Aizenman, E., Engelberg-Kulka, H., Glaser, G. (1996) An Escherichia coli chromosomal 'addiction module' regulated by guanosine 3-, 5-bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl. Acad. Sci. U.S.A., 93, 6059-6063.
18. Engelberg-Kulka, H., Amitai, S., Kolodkin-Gal, I., Hazan, R. (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet., 2, 1528-1526.
19. Lewis, K. (2010) Persister cells. Annu. Rev. Microbiol., 64, 357-372.
20. Gerdes, K., Maisonneuve, E. (2012) Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol., 66, 103-123.
21. Tripathi, A., Dewan, P.C., Siddique, S.A., Varadarajan, R. (2014) MazF-induced growth inhibition and persister generation in Escherichia coli. J. Biol. Chem., 289, 4191-205.
22. Loris, R., Garcia-Pino, A. (2014) Disorder-and dynamics-based regulatory mechanisms in toxin-antitoxin modules. Chem. Rev., 114, 6933-6947.
23. Tsuchimoto, S., Ohtsubo, H., Ohtsubo, E. (1988) Two genes, pemK and pemI, responsible for stable maintenance of resistance plasmid R100. J. Bacteriol., 170, 1461-1466.
24. Masuda, Y., Miyakawa, K., Nishimura, Y., Ohtsubo, E. (1993). chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100. J. Bacteriol., 175, 6850-6856.
25. Zhang, J., Zhang, Y., Hoeflich, K.P., Ikura, M., Qing, G., Inouye, M. (2003) MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell, 12, 913-923.
26. Vesper, O., Amitai, S., Belitsky, M., Byrgazov, K., Kaberdina, A.C., Engelberg-Kulka, H., Moll, I. (2011) Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell, 147, 147-157.
27. Loris, R., Marianovsky, I., Lah, J., Laeremans, T., Engelberg-Kulka, H., Glaser, G., Muyldermans, S., Wyns, L. (2003) Crystal structure of the intrinsically flexible addiction antidote MazE. J. Biol. Chem., 278, 28252-28257.
28. Coles, M., Djuranovic, S., Sding, J., Frickey, T., Koretke, K., Truffault, V., Martin, J., Lupas, A.N. (2005) AbrB-like transcription factors assume a swapped hairpin fold that is evolutionarily related to double-psi beta barrels. Structure, 13, 919-928.
29. Chumsakul, O., Takahashi, H., Oshima, T., Hishimoto, T., Kanaya, S., Ogasawara, N., Ishikawa, S. (2011) Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation. Nucleic Acids Res., 39, 414-428.
30. Bagyan, I., Hobot, J., Cutting, S. (1996) A compartmentalized regulator of developmental gene expression in Bacillus subtilis. J. Bacteriol., 178, 4500-4507.
31. Asen, I., Djuranovic, S., Lupas, A.N., Zeth, K. (2009) Crystal structure of SpoVT, the final modulator of gene expression during spore development in Bacillus subtilis. J. Mol. Biol., 386, 962-975.
32. Kamada, K., Hanaoka, F., Burley, S.K. (2003) Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. Mol. Cell, 11, 875-884.
33. Marianovsky, I., Aizenman, E., Engelberg-Kulka, H., Glaser, G. (2001) The regulation of the Escherichia coli mazEF promoter involves an unusual alternating palindrome. J. Biol. Chem., 276, 5975-5984.
34. Lah, J., Marianovsky, I., Glaser, G., Engelberg-Kulka, H., Kinne, J., Wyns, L., Loris, R. (2003) Recognition of the intrinsically flexible addiction antidote MazE by a dromedary single domain antibody fragment. Structure, thermodynamics of binding, stability, and influence on interactions with DNA. J. Biol. Chem., 278, 14101-14111.
35. Bailey, S.E.S., Hayes, F. (2009) Influence of operator site geometry on transcriptional control by the YefM-YoeB toxin-antitoxin complex. J. Bacteriol., 191, 762-772.
36. Monti, M.C., Hernandez-Arriaga, A.M., Kamphuis, M.B., Lopez-Villarejo, J., Heck, A.J.R., Boelens, R., Diaz-Orejas, R., van den Heuvel, R.H.H (2007) Interactions of Kid-Kis toxin-antitoxin complexes with the parD operator-promoter region of plasmid R1 are piloted by the Kis antitoxin and tuned by the stoichiometry of Kid-Kis oligomers. Nucleic Acids Res., 35, 1737-1749.
37. Oberer, M., Zangger, K., Gruber, K., Keller, W. (2007) The solution structure of ParD, the antidote of the ParDE toxin antitoxin module, provides the structural basis for DNA and toxin binding. Protein Sci., 16, 1676-1688.
38. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
39. Johnson, B.A., Blevins, R.A. (1994) NMR View: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4, 603-614.
40. Cavanagh, J., Fairbrother, W.J., Palmer, A.G., Rance, M., Skelton, N.J. (2007) Protein NMR Spectroscopy, 2nd edn, Academic Press, San Diego, CA.
41. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J., Laue, E.D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
42. Guntert, P., Mumenthaler, C., Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298.
43. Herrmann, T., Guntert, P., Wuthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR, 24, 171-189.
44. Shen, Y., Delaglio, F., Cornilescu, G., Bax, A. (2009) TALOS plus: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 44, 213-223.
45. Nederveen, A.J., Doreleijers, J.F., Vranken, W., Miller, Z., Spronk, C.A., Nabuurs, S.B., Guntert, P., Livny, M., Markley, J.L., Nilges, M. et al. (2005) RECOORD: a recalculated coordinate database of 500 +proteins from the PDB using restraints from the BioMagResBank. Proteins, 59, 662-672.
46. Brnger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
47. Dominguez, C., Boelens, R., Bonvin, A.M. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc., 125, 1731-1737.
48. Hubbard, S., Thornton, J. (1993) Naccess-Computer Program. Department of Biochemistry and Molecular Biology, University College London.
49. Mat, M.J., Vincentelli, R., Foos, N., Raoult, D., Cambillau, C., Ortiz-Lombard, M. (2011) Crystal structure of the DNA-bound VapBC2 antitoxin/toxin pair from Rickettsia felis. Nucleic Acids Res., 40, 3245-3258.
50. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
51. Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J., Svergun, D.I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst, 36, 1277-1282.
52. Konarev, P.V., Petoukhov, M.V., Volkov, V.V., Svergun, D.I. (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Cryst., 39, 277-286.
53. Rambo, R.P., Tainer, J.A. (2013) Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496, 477-481.
54. Pelikan, M., Hura, G.L., Hammel, M. (2009) Structure and flexibility within proteins as identified through small angle X-ray scattering. Gen. Physiol. Biophys., 28, 174-189.
55. Schneidman-Duhovny, D., Hammel, M., Sali, A. (2010) FoXs: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res., 38, W540-W544.
56. Weinkam, P., Pons, J., Sali, A. (2012) Structure-based model of allostery predicts coupling between distant sites. Proc. Natl. Acad. Sci. U.S.A., 109, 4875-4880.
57. Sterckx, Y.G., Volkov, A.N., Vranken, W.F., Kragelj, J., Jensen, M.R., Buts, L., Garcia-Pino, A., Jov, T., Van Melderen, L., Blackledge, M. et al. (2014) Small-angle X-Ray scattering-and nuclear magnetic resonance-derived conformational ensemble of the highly flexible antitoxin PaaA2. Structure, 22, 854-865.
58. Zorzini, V., Buts, L., Sleutel, M., Garcia-Pino, A., Talavera, A., Haesaerts, S., Greve, H.D., Cheung, A., van Nuland, N.A., Loris, R. (2014) Structural and biophysical characterization of Staphylococcus aureus SaMazF shows conservation of functional dynamics. Nucleic Acids Res., 42, 6709-6725.
59. Fischer, H., de Oliveira Neto, M., Napolitano, H.B., Craievich, A.F., Polikarpov, I. (2010) The molecular weight of proteins in solution can be determined from a single SAXS measurement on a relative scale. J. Appl. Cryst., 43, 101-109.
60. Dao-Thi, M.H., Charlier, D., Loris, R., Maes, D., Messens, J., Wyns, L., Backmann, J. (2002) Intricate interactions within the ccd plasmid addiction system. J. Biol. Chem., 277, 3733-3742.
61. Kamphuis, M.B., Monti, M.C., van den Heuvel, R.H., Santos-Sierra, S., Folkers, G.E., Lemonnier, M., Dz-Orejas, R., Heck, A.J., Boelens, R. (2007) Interactions between the toxin Kid of the bacterial parD system and the antitoxins Kis and MazE. Proteins, 67, 219-231.
62. Coles, M., Hulko, M., Djuranovic, S., Truffault, V., Koretke, K., Martin, J., Lupas, A.N. (2006) Common evolutionary origin of swapped-hairpin and double-psi beta barrels. Structure, 14, 1489-1498.