In Vitro characterization of the type i toxin-antitoxin system bsrE/SR5 from Bacillus subtilis

Journal of Biological Chemistry

Volumn 291, Issue 2, 2016, Pages 560-571

  Meißner, Christin ^a,b   Jahn, Natalie ^a   Brantl, Sabine ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b FRAUNHOFER GESELLSCHAFT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BINS; CHROMOSOMES; GENE ENCODING; GENES; RATE CONSTANTS; RNA; TOXIC MATERIALS;

BACILLUS SUBTILIS; BINDING RATE CONSTANTS; IN-VITRO ANALYSIS; OVER-EXPRESSION; RNA INTERACTION; RNA-BINDING PROTEIN; SECONDARY STRUCTURES; TIME-COURSE EXPERIMENTS;

NUCLEIC ACIDS;

AMINO ACID; ANTITOXIN; BACTERIAL RNA; BACTERIAL TOXIN; MESSENGER RNA; RNA BINDING PROTEIN; BACTERIAL PROTEIN; PROTEIN BINDING;

3' UNTRANSLATED REGION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL MUTATION; BINDING AFFINITY; BSRE GENE; CONTROLLED STUDY; CYTOLYSIS; GENE OVEREXPRESSION; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; SR5 GENE; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TIME FACTOR;

ANTITOXINS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; GENE EXPRESSION REGULATION, BACTERIAL; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RNA, MESSENGER; TIME FACTORS;

EID: 84954169051     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.697524     Document Type: Article

References (53)

1. Brantl, S. (2009) Bacterial chromosome-encoded regulatory RNAs. Future Microbiol. 4, 85-103
2. Brantl, S. (2012) Acting antisense: plasmid-and chromosome-encoded sRNAs from Gram-positive bacteria. Future Microbiol. 7, 853-871
3. Brantl, S., and Brückner, R. (2014) Small regulatory RNAs from low-GC Gram-positive bacteria. RNA Biol. 11, 443-456
4. Brantl, S. (2012) Bacterial type I toxin-antitoxin systems. RNA Biol. 9, 1488-1490
5. Brantl, S., and Jahn, N. (2015) sRNAs in bacterial type I and type III toxin/antitoxin systems. FEMS Microbiol. Rev. 39, 413-427
6. Gerdes, K., Rasmussen, P. B., and Molin, S. (1986) Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc. Natl. Acad. Sci. U.S.A. 83, 3116-3120
7. Gerdes, K., and Wagner, E. G. (2007) RNA antitoxins. Curr. Opin. Microbiol. 10, 117-124
8. Weaver, K. E. (2012) The par toxin-antitoxin system from Enterococcus faecalis plasmid pAD1 and its chromosomal homologs. RNA Biol. 9, 1498-1503
9. Weaver, K. E. (2015) The type I toxin-antitoxin par locus from Enterococcus faecalis plasmid pAD1: RNA regulation by both cis-and trans-acting elements. Plasmid 78, 65-70
10. Wagner, E. G., and Unoson, C. (2012) The toxin-antitoxin system tisBistR1: expression, regulation and biological role in persister phenotypes. RNA Biol. 9, 1513-1519
11. Kawano, M. (2012) Divergently overlapping cis-encoded antisense RNA regulating toxin-antitoxin systems from E. coli: hok/sok, ldr/rdl, symE/symR. RNA Biol. 9, 1520-1527
12. Fozo, E. M. (2012) New type I toxin-antitoxin families from "wild" and laboratory strains of E. coli: Ibs-Sib, ShoB-OhsC and Zor-Orz. RNA Biol. 9, 1504-1512
13. Silvaggi, J. M., Perkins, J. B., and Losick, R. (2005) Small untranslated RNA antitoxin in Bacillus subtilis. J. Bacteriol. 187, 6641-6650
14. Jahn, N., Preis, H., Wiedemann, C., and Brantl, S. (2012) BsrG/SR4 from Bacillus subtilis: the first temperature-dependent type I toxin-antitoxin system. Mol. Microbiol. 83, 579-598
15. Jahn, N., and Brantl, S. (2013) One antitoxin-two functions: SR4 controls toxin mRNA decay and translation. Nucleic Acids Res. 41, 9870-9880
16. Weaver, K. E., Ehli, E. A., Nelson, J. S., and Patel, S. (2004) Antisense RNA regulation by stable complex formation in the Enterococcus faecalis plasmid pAD1 par addiction system. J. Bacteriol. 186, 6400-6408
17. Dörr, T., Vulić, M., and Lewis, K. (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLos Biol. 8, e1000317
18. Gurnev, P. A., Ortenberg, R., Dörr, T., Lewis, K., and Bezrukov, S. M. (2012) Persister-promoting bacterial toxin TisB produces anion-selective pores in planar lipid bilayers. FEBS Lett. 586, 2529-2534
19. Verstraeten, N., Knapen, W. J., Kint, C. I., Liebens, V., Van den Bergh, B., Dewachter, L., Michiels, J. E., Fu, Q., David, C. C., Fierro, A. C., Marchal, K., Beirlant, J., Versées, W., Hofkens, J., Jansen, M., Fauvart, M., and Michiels, J. (2015) Obg and membrane polarization are part of a microbial bet-hedging strategy that leads to antibiotic tolerance. Mol. Cell 59, 9-21
20. Koyanagi, S., and Lévesque, C. M. (2013) Characterization of a Streptococcus mutans intergenic region containing a small toxin peptide and its cis-encoded antisense small RNA antitoxin. PLoS One 8, e54291
21. Kawano, M., Aravind, L., and Storz, G. (2007) An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol. Microbiol. 64, 738-754
22. Weel-Sneve, R., Kristiansen, K. I., Odsbu, I., Dalhus, B., Booth, J., Rognes, T., Skarstad, K., and Bjørås, M. (2013) Single transmembrane peptide DinQ modulates membrane-dependent activities. PLoS Genet. 9, e1003260
23. Guo, Y., Quiroga, C., Chen, Q., McAnulty, M. J., Benedik, M. J., Wood, T. K., and Wang, X. (2014) RalR (a DNase) and RalA (a small RNA) form a type I toxin-antitoxin system in Escherichia coli. Nucleic Acids Res. 42, 6448-6462
24. Durand, S., Jahn, N., Condon, C., and Brantl, S. (2012a) Type I toxinantitoxin systems in Bacillus subtilis. RNA Biol. 9, 1491-1497
25. Jahn, N., Brantl, S., and Strahl, H. (2015) Against the mainstream: the membrane associated type I toxin BsrG from Bacillus subtilis interferes with cell envelope biosynthesis without increasing membrane permeability. Mol. Microbiol. 98, 651-666
26. Thisted, T., and Gerdes, K. (1992) Mechanism of post-segregational killing by the hok/sok system of plasmid R1. Sok antisense RNA regulates hok gene expression indirectly through the overlapping mok gene. J. Mol. Biol. 223, 41-54
27. Han, K., Kim, K.-S., Bak, G., Park, H., and Lee, Y. (2010) Recognition and discrimination of target mRNAs by Sib RNAs, a cis-encoded sRNA family. Nucleic Acids Res. 38, 5851-5866
28. Irnov, I., Sharma, C. M., Vogel, J., and Winkler, W. C. (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res. 38, 6637-6651
29. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
30. Heidrich, N., Chinali, A., Gerth, U., and Brantl, S. (2006) The small untranslated RNA SR1 from the B. subtilis genome is involved in the regulation of arginine catabolism. Mol. Microbiol. 62, 520-536
31. Heidrich, N., and Brantl, S. (2007) Antisense RNA-mediated transcriptional attenuation in plasmid pIP501: the simultaneous interaction between two complementary loop pairs is required for efficient inhibition by the antisense RNA. Microbiology 153, 420-427
32. Preis, H., Eckart R. A., Gudipati, R. K., Heidrich, N., and Brantl, S. (2009) CodY activates transcription of a small RNA in Bacillus subtilis. J. Bacteriol. 191, 5446-5457
33. Brantl, S., and Wagner, E. G. (2000) Antisense RNA-mediated transcriptional attenuation: an in vitro study of plasmid pT181. Mol. Microbiol. 35, 1469-1482
34. Heidrich, N., Moll, I., and Brantl, S. (2007) In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res. 35, 4331-4346
35. Franch, T., and Gerdes, K. (2000) U-turns and regulatory RNAs. Curr. Opin. Microbiol. 3, 159-164
36. Heidrich, N., and Brantl, S. (2003) Antisense-RNA mediated transcriptional attenuation: importance of a U-turn loop structure in the target RNA of plasmid pIP501 for efficient inhibition by the antisense RNA. J. Mol. Biol. 333, 917-929
37. Dambach, M., Irnov, I., and Winkler, W. C. (2013) Association of RNAs with Bacillus subtilis Hfq. PLoS One 8, e455156
38. Durand, S., Gilet, L., and Condon, C. (2012b) The essential function of B. subtilis RNase III is to silence foreign toxic genes. PLoS Genet. 8, e1003181
39. Kolb, F. A., Engdahl, H. M., Slagter-Jäger, J. G., Ehresmann, B., Ehresmann, C., Westhof, E., Wagner, E. G., and Romby, P. (2000) Progression of a loop-loop complex to a four-way junction is crucial for the activity of a regulatory antisense RNA. EMBO J. 19, 5905-5915
40. Thisted, T., Sørensen, N. S., Wagner, E. G., and Gerdes, K. (1994) Mechanism of post-segregational killing: Sok antisense RNA interacts with Hok mRNA via its 5′-end single stranded leader and competes with the 3′-end of Hok mRNA for binding to the mok translational initiation region. EMBO J. 13, 1960-1968
41. Greenfield, T. J., Franch, T., Gerdes, K., and Weaver, K. E. (2001) Antisense RNA regulation of the par post-segregational killing system: structural analysis and mechanism of binding of the antisense RNA, RNAII and its target, RNAI. Mol. Microbiol. 42, 527-537
42. Wen, J., Won, D., and Fozo, E. M. (2014) The ZorO-OrzO type I toxinantitoxin locus: repression by the OrzO antitoxin. Nucleic Acids Res. 42, 1930-1946
43. Brantl, S. (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr. Opin. Microbiol. 10, 102-109
44. Franch, T., Petersen, M., Wagner, E. G., Jacobsen, J. P., and Gerdes, K. (1999) Antisense RNA regulation in prokaryotes: rapid RNA/RNA interaction facilitated by a general U-turn loop structure. J. Mol. Biol. 294, 1115-1125
45. Shokeen, S., Johnson, C. M., Greenfield, T. J., Manias, D. A., Dunny, G. M., and Weaver, K. E. (2010) Structural analysis of AntiQ-Qs interaction: RNA-mediated regulation of E. faecalis plasmid pCF10 conjugation. Plasmid 64, 26-35
46. Kwong S. M., and Firth, N. (2015) Structural and sequence requirements for the antisense RNA regulating replication of staphylococcal multiresistance plasmid pSK41. Plasmid 78, 17-25
47. Li, G. W., Oh, E., and Weissman, J. S. (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484, 538-541
48. Gottesman, S., and Storz, G. (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 3, a003798
49. Papenfort, K., and Vanderpool, C. K. (2015) Target activation by regulatory RNAs in bacteria. FEMS Microbiol. Rev. 39, 362-378
50. Nielsen, J. S., Lei, L. K., Ebersbach, T., Olsen A. S., Klitgaard, J. K., Valentin-Hansen P., and Kallipolitis, B. H. (2010) Defining a role for Hfq in Grampositive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes. Nucleic Acids Res. 38, 907-919
51. Romeo, T., Vakulskas, C. A., and Babitzke, P. (2013) Posttranscriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ. Microbiol. 15, 313-324
52. Jørgensen, M. G., Thomason, M. K., Havelund, J., Valentin-Hansen, P., and Storz, G. (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev. 27, 1132-1145
53. Mukherjee, S., Yakhnin, H., Kysela, D., Sokoloski, J., Babitzke, P., and Kearns, D. B. (2011) CsrA-FliW interaction governs flagellin homeostasis and a checkpoint on flagellar morphogenesis in Bacillus subtilis. Mol. Microbiol. 82, 447-461