A conserved mode of protein recognition and binding in a ParD-ParE toxin - antitoxin complex

Biochemistry

Volumn 49, Issue 10, 2010, Pages 2205-2215

  Dalton, Kevin M ^a   Crosson, Sean ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CHROMOSOMES; BINDING INTERFACE; CELL DEVELOPMENT; COMPLEX STRUCTURE; CROSS-SPECIES; ENVIRONMENTAL STRESS; GENETIC ELEMENTS; HETEROTETRAMERS; HYDROPHOBIC CONTACT; LOW LEVEL; PRIMARY SEQUENCES; PROTEIN RECOGNITION; SUBDOMAIN; TOXIN BINDING; TOXIN STRUCTURE;

CHROMOSOMES; CRYSTAL STRUCTURE; MICROBIOLOGY; PROTEINS;

TOXIC MATERIALS;

ANTITOXIN; PARD ANTITOXIN; PARE TOXIN; PROTEIN SUBUNIT; TOXIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL CHROMOSOME; BINDING SITE; CAULOBACTER CRESCENTUS; CRYSTAL STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SPECIES COMPARISON; TOXIN ANTITOXIN COMPLEX; TOXIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CAULOBACTER CRESCENTUS; CHROMOSOMES, BACTERIAL; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA TOPOISOMERASE IV; DNA-BINDING PROTEINS; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES; PROKARYOTA;

EID: 77949367813     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902133s     Document Type: Article

References (55)

1. 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.
2. Gronlund, H., and Gerdes, K. (1999) Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in. prokaryotes. J. Mol. Biol. 285, 1401-1415.
3. 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.
4. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371-382.
5. Buts, L., Lah, J., Dao-Thi, M. H., Wyns, L., and Loris, R. (2005) Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci. 30, 672-679.
6. Hayes, F. (2003) Toxins-antitoxins: Plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301, 1496-1499.
7. Van Melderen, L., and De Bast, M.S. (2009) Bacterial toxin-antitoxin systems: More than selfish entities? PLoS Genet. 5, e1000437.
8. Lehnherr, H., and Yarmolinsky, M. B. (1995) Addiction protein Phd of plasmid prophage Pl is a substrate of the ClpXP serine protease of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 3274-3277.
9. Tsuchimoto, S., Nishimura, Y., and Ohtsubo, E. (1992) The stable maintenance system pern of plasmid R100: Degradation of Peml protein may allow PemK protein to inhibit cell growth. J. Bacteriol. 174, 4205-4211.
10. Van Melderen, L., Bernard, P., and Couturier, M. (1994) Londependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol. Microbiol. 11, 1151-1157.
11. Gerdes, K., Rasmussen, P. B., and Molin, S. (1986) Unique type of plasmid maintenance function: Postsegregational killing of plasmidfree cells. Proc. Natl. Acad. Sci. U.S.A. 83, 3116-3120.
12. Jaffe, A., Ogura, T., and Hiraga, S. (1985) Effects of the ccd function of the F plasmid on bacterial growth. J. Bacteriol. 163, 841-849.
13. Roberts, R. C., and Helinski, D. R. (1992) Definition of a minimal plasmid stabilization system from the broad-host-range plasmid RK2. J. Bacteriol. 174, 8119-8132.
14. Lehnherr, H., Maguin, E., Jafri, S., and Yarmolinsky, M. B. (1993) Plasmid addiction genes of bacteriophage Pl : doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. MoI, Biol, 233, 414-428.
15. Roberts, R. C., Strom, A. R., and Helinski, D. R. (1994) The parDE operon of the broad-host-range plasmid R.K2 specifies growth, inhibition associated with, plasmid loss. J. Mol. Biol. 237, 35-51.
16. Engelberg-Kulka, H., Amitai, S., Kolodkin-Gal, I., and Hazan, R. (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet. 2, e135.
17. Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180.
18. Szekeres, S., Dauti, M., Wilde, C., Mazel, D., and Rowe-Magnus, D. A. (2007) Chromosomal toxin-antitoxin loci can diminish largescale genome reductions in the absence of selection. Mol. Microbiol. 63, 1588-1605.
19. Nariya, H., and Inouye, M. (2008) MazF, an mRNA interferase, mediates programmed cell death, during multicellular Myxococcus development. Cell 132, 55-66.
20. Tsilibaris, V., Maenhaut-Michel, G., Mine, N., and Van Melderen, L. (2007) What is the benefit to Escherichia coli of having multiple toxinantitoxin systems in its genome? J. Bacteriol 189, 6101-6108.
21. Jiang, Y., Pogliano, J., Helinski, D. R., and Konieczny, I. (2002) ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase. Mol. Microbiol. 44, 971-979.
22. Pedersen, K., Zavialov, A. V., Pavlov, M. Y., Elf, J., Gerdes, K., and Ehrenberg, M. (2003) The bacterial toxin. RelE displays codonspecific cleavage of mRNAs in the ribosomal A site. Cell 112, 131-140.
23. Christensen, S. K., and Gerdes, K. (2003) RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol. Microbiol, 48, 1389-1400.
24. 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.
25. 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.
26. Li, G. Y., Zhang, Y., Inouye, M., and Ikura, M. (2008) Structural mechanism of transcriptional autorepression of the Escherichia coli RelB/RelE antitoxin/toxin module. J. Mol. Biol. 380, 107-119.
27. Madl, T., Van Melderen, L., Mine, N., Respondek, M., Oberer, M., Keller, W., Khatai, L., and Zangger, K. (2006) Structural basis for nucleic acid and toxin recognition of the bacterial antitoxin CcdA. J. Mol. Biol. 364, 170-185.
28. Oberer, M., Zangger, K., Gruber, K., and 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.
29. Garcia-Pino, A., Christensen-Dalsgaard, M., Wyns, L., Yarmolinsky, M., Magnuson, R. D., Gerdes, K., and Loris, R. (2008) Doc of prophage P1 is inhibited by its antitoxin partner Phd through fold complementation. J. Biol. Chem. 283, 30821-30827.
30. Li, G. Y., Zhang, Y., Inouye, M., and Ikura, M. (2009) Inhibitory mechanism of Escherichia coli RelE-RelB toxin-antitoxin module involves a helix displacement near an mRNA interferase active site. J. Biol. Chem. 284, 14628-14636.
31. Kumar, P., Issac, B., Dodson, E. J., Turkenburg, J. P., and Mande, S. C. (2008) Crystal structure of Mycobacterium tuberculosis YefM antitoxin reveals that it is not an intrinsically unstructured protein. J. Mol. Biol. 383, 482-493.
32. Oberer, M., Zangger, K., Prytulla, S., and Keller, W. (2002) The antitoxin ParD of plasmid RK2 consists of two structurally distinct moieties and belongs to the ribbon-helix-helix family of DNA-binding proteins. Biochem. J. 361, 41-47.
33. Johnson, E. P., Strom, A. R., and Helinski, D. R. (1996) Plasmid RK2 toxin protein ParE: Purification and interaction with the ParD antitoxin protein. J. Bacteriol. 178, 1420-1429.
34. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
35. Doublie, S. (2007) Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 363, 91-108.
36. Luft, J. R., Collins, R. J., Fehrman, N. A., Lauricella, A. M., Veatch, C. K., and DeTitta, G. T. (2003) A deliberate approach to screening for initial crystallization conditions of biological macromolecules. J. Struct. Biol. 142, 170-179.
37. Schneider, T. R., and Sheldrick, G. M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D58, 1772-1779.
38. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D50, 760-763.
39. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.
40. Cowtan, K. (2006) The Buccaneer software for automated model building. Acta Crystallogr. D62, 1002-1011.
41. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
42. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read,R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr. D58, 1948-1954.
43. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
44. Strong, M., Sawaya, M. R., Wang, S., Phillips, M., Cascio, D., and Eisenberg, D. (2006) Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 103, 8060-8065.
45. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein Identification and Analysis Tools on the ExPASy Server. In The Proteomics Protocols Handbook (Walker, J. M., Ed.) pp 571-607, Humana Press, Totowa, NJ.
46. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606-1619.
47. Svergun, D. I. (1992) Determination of the Regularisation Parameter in Indirect-Transform Methods Using Perceptual Criteria. J. Appl. Crystallogr. 25, 495-503.
48. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: A. program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773.
49. Dauter, Z. (2002) One-and-a-half wavelength approach. Acta Crvstalloer. D58. 1958-1967.
50. Holm, L., Kaariainen, S., Rosenstrom, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24, 2780-2781.
51. Zhang, Y., and Inouye, M. (2009) The inhibitory mechanism of protein, synthesis by YoeB, an Escherichia coli toxin. J. Biol. Chem. 284, 6627-6638.
52. Neubauer, C., Gao, Y. G., Andersen, K. R., Dunham, C. M., Kelley, A. C., Hentschel, J., Gerdes, K., Ramakrishnan, V., and Brodersen, D. E. (2009) The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 139, 1084-1095.
53. Schreiter, E. R., and Drennan, C. L. (2007) Ribbon-helix-helix transcription factors: Variations on a theme. Nat. Rey. Microbiol. 5, 710-720.
54. 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.
55. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting Coiled Coils from Protein Sequences. Science 252, 1162-1164.