Molecular structure and function of the novel BrnT/BrnA toxin-antitoxin system of Brucella abortus

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 12098-12110

  Heaton, Brook E ^a,b   Herrou, Julien ^a   Blackwell, Anne E ^c   Wysocki, Vicki H ^c   Crosson, Sean ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC RESOLUTION; BACTERIAL CELLS; BACTERIAL CHROMOSOMES; BRUCELLA; COEXPRESSED; CYTOPLASMIC PROTEINS; DNA GYRASES; FUNCTIONAL CHARACTERIZATION; IN-VITRO; IN-VIVO; INTRACELLULAR PATHOGENS; MAMMALIAN HOSTS; PRIMARY SEQUENCES; SITE DIRECTED MUTAGENESIS; STRUCTURAL HOMOLOGY; STRUCTURAL INVESTIGATION; TETRAMERIC COMPLEX; TETRAMERS; TOXIN ACTIVITY; TOXIN GENES; TYPE II;

ENZYME ACTIVITY; GENES; MAMMALS; METABOLITES; OLIGOMERS; RNA; TRANSCRIPTION;

TOXIC MATERIALS;

ANTITOXIN; ANTITOXIN BRNA; BACTERIAL TOXIN; RIBONUCLEASE; TOXIN BRNT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIOSTASIS; BRNA GENE; BRNT GENE; BRUCELLA ABORTUS; CONTROLLED STUDY; CRYSTAL STRUCTURE; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE SEQUENCE; GENETIC CONSERVATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; TOXIN ANALYSIS; TOXIN STRUCTURE; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BACTERIAL TOXINS; BRUCELLA ABORTUS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL VIABILITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OPERON; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RIBONUCLEASES; SEQUENCE ALIGNMENT; STRESS, PHYSIOLOGICAL; STRUCTURAL HOMOLOGY, PROTEIN; SURFACE PROPERTIES; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); BRUCELLA MELITENSIS BIOVAR ABORTUS; MAMMALIA;

EID: 84859487051     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.332163     Document Type: Article

References (67)

1. Anderson, T. D., Meador, V. P., and Cheville, N. F. (1986) Pathogenesis of placentitis in the goat inoculated with Brucella abortus. I. Gross and histologic lesions. Vet. Pathol. 23, 219-226
2. Moreno, E., and Moriyon, I. (2006) in The Prokaryotes: A Handbook on the Biology of Bacteria (Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., and Stackebrandt, E., eds) 3rd Ed., pp. 315-456, Springer, New York
3. Jiang, X., Leonard, B., Benson, R., and Baldwin, C. L. (1993) Macrophage control of Brucella abortus. Role of reactive oxygen intermediates and nitric oxide. Cell. Immunol. 151, 309-319 (Pubitemid 23325454)
4. Porte, F., Liautard, J. P., and Köhler, S. (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun 67, 4041-4047 (Pubitemid 29357026)
5. Köhler, S., Michaux-Charachon, S., Porte, F., Ramuz, M., and Liautard, J. P. (2003) What is the nature of the replicative niche of a stealthy bug named Brucella? Trends Microbiol. 11, 215-219 (Pubitemid 36645004)
6. Roop, R. M., 2nd, Gaines, J. M., Anderson, E. S., Caswell, C. C., and Martin, D. W. (2009) Survival of the fittest. How Brucella strains adapt to their intracellular niche in the host. Med. Microbiol Immunol. 198, 221-238
7. Gerdes, K., Christensen, S. K., and Løbner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371-382 (Pubitemid 40590380)
8. Gerdes, K., Larsen, J. E., and Molin, S. (1985) Stable inheritance of plasmid R1 requires two different loci. J. Bacteriol 161, 292-298 (Pubitemid 15157342)
9. Jaffé, A., Ogura, T., and Hiraga, S. (1985) Effects of the ccd function of the F plasmid on bacterial growth. J. Bacteriol. 163, 841-849 (Pubitemid 15230711)
10. 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 (Pubitemid 41430517)
11. Van Melderen, L., and Saavedra De Bast, M. (2009) Bacterial toxin-antitoxin systems. More than selfish entities? PLoS Genet. 5, e1000437
12. Moyed, H. S., and Bertrand, K. P. (1983) hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155, 768-775 (Pubitemid 13048115)
13. Blower, T. R., Salmond, G. P., and Luisi, B. F. (2011) Balancing at survival's edge. The structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr. Opin. Struct. Biol. 21, 109-118
14. 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 (Pubitemid 41668860)
15. 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 (Pubitemid 39603206)
16. Maisonneuve, E., Shakespeare, L. J., Jørgensen, M. G., and Gerdes, K. (2011) Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U.S.A. 108, 13206-13211
17. Wang, X., and Wood, T. K. (2011) Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77, 5577-5583
18. Tsuchimoto, S., Nishimura, Y., and Ohtsubo, E. (1992) The stable maintenance system pem of plasmid R100. Degradation of PemI protein may allow PemK protein to inhibit cell growth. J. Bacteriol. 174, 4205-4211
19. Van Melderen, L., Bernard, P., and Couturier, M. (1994) Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol. Microbiol. 11, 1151-1157 (Pubitemid 24201630)
20. Lehnherr, H., and Yarmolinsky, M. B. (1995) Addiction protein Phd of plasmid prophage P1 is a substrate of the ClpXP serine protease of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 3274-3277
21. 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 (Pubitemid 37101369)
22. 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 (Pubitemid 36106425)
23. Schumacher, M. A., Piro, K. M., Xu, W., Hansen, S., Lewis, K., and Brennan, R. G. (2009) Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323, 396-401
24. 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 (Pubitemid 34535533)
25. Maki, S., Takiguchi, S., Miki, T., and Horiuchi, T. (1992) Modulation of DNA supercoiling activity of Escherichia coli DNA gyrase by F plasmid proteins. Antagonistic actions of LetA (CcdA) and LetD (CcdB) proteins. J. Biol. Chem. 267, 12244-12251
26. Yuan, J., Yamaichi, Y., and Waldor, M. K. (2011) The three vibrio cholerae chromosome II-encoded ParE toxins degrade chromosome I following loss of chromosome II. J. Bacteriol. 193, 611-619
27. Winther, K. S., and Gerdes, K. (2011) Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc. Natl. Acad. Sci. U.S.A. 108, 7403-7407
28. Mutschler, H., Gebhardt, M., Shoeman, R. L., and Meinhart, A. (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol. 9, e1001033
29. Lioy, V. S., Martín, M. T., Camacho, A. G., Lurz, R., Antelmann, H., Hecker, M., Hitchin, E., Ridge, Y., Wells, J. M., and Alonso, J. C. (2006) pSM19035-encoded ζ toxin induces stasis followed by death in a subpopulation of cells. Microbiology 152, 2365-2379 (Pubitemid 44219644)
30. Van Melderen, L. (2010) Toxin-antitoxin systems. Why so many, what for? Curr. Opin. Microbiol. 13, 781-785
31. Hayes, F., and Van Melderen, L. (2011) Toxins-antitoxins: Diversity, evolution, and function. Crit. Rev. Biochem. Mol. Biol. 46, 386-408
32. Khan, S. R., Gaines, J., Roop, R. M., 2nd, and Farrand, S. K. (2008) Broad-host range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl. Environ. Microbiol. 74, 5053-5062
33. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130
34. Doublié, S. (1997) Preparation of selenomethionyl proteins for phase determination. Methods Enzymol. 276, 523-530
35. Otwinowski, Z., and Minor, W. (1997)Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
36. Dauter, Z. (2002) One-and-a-half wavelength approach. Acta Crystallogr. D 58, 1958-1967
37. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX, a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221
38. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D 66, 486-501
39. Eisenberg D., Schwarz, E., Komaromy, M., and Wall, R. (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179, 125-142 (Pubitemid 16223392)
40. Ashkenazy, H., Erez, E., Martz, E., Pupko, T., and Ben-Tal, N. (2010) Con-Surf 2010, calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529-533
41. Terribilini, M., Sander, J. D., Lee, J. H., Zaback, P., Jernigan, R. L., Honavar, V., and Dobbs, D. (2007) RNABindR, a server for analyzing and predicting RNA-binding sites in proteins. Nucleic Acids Res. 35, W578-584
42. Wang, L., and Brown, S. J. (2006) BindN, a web-based tool for efficient prediction of DNA and RNA binding sites in amino acid sequences. Nucleic Acids Res. 34, W243-248 (Pubitemid 44529772)
43. Murakami, Y., Spriggs, R. V., Nakamura, H., and Jones, S. (2010) PiRaNhA, a server for the computational prediction of RNA-binding residues in protein sequences. Nucleic Acids Res. 38, W412-416
44. Miller, J. H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
45. Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2009) Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4, 19
46. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database. Nucleic Acids Res. 38, D211-222
47. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
48. Tanford, C., Kawahara, K., Lapanje, S., Hooker, T. M., Jr., Zarlengo, M. H., Salahuddin, A., Aune, K. C., and Takagi, T. (1967) Proteins as random coils. 3. Optical rotatory dispersion in 6 M guanidine hydrochloride. J. Am. Chem. Soc. 89, 5023-5029
49. 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 (Pubitemid 41140007)
50. Bauerová-Hlinková, V., Dvorský, R., Perecko, D., Povazanec, F., and Sevcík, J. (2009) Structure of RNase Sa2 complexes with mononucleotides. New aspects of catalytic reaction and substrate recognition. FEBS J. 276, 4156-4168
51. Heinemann, U., and Saenger, W. (1983) Crystallographic study of mechanism of ribonuclease T1-catalyzed specific RNA hydrolysis. J. Biomol. Struct. Dyn. 1, 523-538 (Pubitemid 14082481)
52. Yakovlev, G. I., Mitkevich, V. A., Shaw, K. L., Trevino, S., Newsom, S., Pace, C. N., and Makarov, A. A. (2003) Contribution of active site residues to the activity and thermal stability of ribonuclease Sa. Protein Sci. 12, 2367-2373 (Pubitemid 37163371)
53. Sevcik, J., Zegers, I., Wyns, L., Dauter, Z., and Wilson, K. S. (1993) Complex of ribonuclease Sa with a cyclic nucleotide and a proposed model for the reaction intermediate. Eur. J. Biochem. 216, 301-305 (Pubitemid 23255200)
54. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. (2011) CDD, a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-229
55. Fiebig, A., Castro Rojas, C. M., Siegal-Gaskins, D., and Crosson, S. (2010) Interaction specificity, toxicity, and regulation of a paralogous set of ParE/RelE-family toxin-antitoxin systems. Mol. Microbiol. 77, 236-251
56. 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 (Pubitemid 38661567)
57. 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. U.S.A. 98, 14328-14333 (Pubitemid 33121391)
58. Aizenman, E., Engelberg-Kulka, H., and 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
59. Donegan, N. P., Thompson, E. T., Fu, Z., and Cheung, A. L. (2010) Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J. Bacteriol 192, 1416-1422
60. Pedersen, K., Christensen, S. K., and Gerdes, K. (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol 45, 501-510 (Pubitemid 34779839)
61. Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Drèze, P., and Van Melderen, L. (2011) Diversity of bacterial type II toxin-antitoxin systems. A comprehensive search and functional analysis of novel families. Nucleic Acids Res. 39, 5513-5525
62. Yamaguchi, Y., and Inouye, M. (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 9, 779-790
63. Brown, B. L., Grigoriu, S., Kim, Y., Arruda, J. M., Davenport, A., Wood, T. K., Peti, W., and Page, R. (2009) Three-dimensional structure of the MqsR·MqsA complex. A novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties. PLoS Pathog. 5, e1000706
64. Jørgensen, M. G., Pandey, D. P., Jaskolska, M., and Gerdes, K. (2009) HicA of Escherichia coli defines a novel family of translation- independent mRNA interferases in bacteria and archaea. J. Bacteriol. 191, 1191-1199
65. Tian, Q. B., Hayashi, T., Murata, T., and Terawaki, Y. (1996) Gene product identification and promoter analysis of high locus of plasmid Rts1. Biochem. Biophys. Res. Commun. 225, 679-684 (Pubitemid 26355657)
66. Kedzierska, B., Lian, L. Y., and Hayes, F. (2007) Toxin-antitoxin regulation. Bimodal interaction of YefM-YoeB with paired DNA palindromes exerts transcriptional autorepression. Nucleic Acids Res. 35, 325-339 (Pubitemid 46189857)
67. Bailey, S. E., and Hayes, F. (2009) Influence of operator site geometry on transcriptional control by the YefM-YoeB toxin-antitoxin complex. J. Bacteriol. 191, 762-772