Overexpression of MazF Sa in Staphylococcus aureus Induces Bacteriostasis by Selectively Targeting mRNAs for Cleavage*

Journal of Bacteriology

Volumn 191, Issue 7, 2009, Pages 2051-2059

  Fu, Zhibiao ^a,b   Tamber, Sandeep ^a   Memmi, Guido ^a   Donegan, Niles P ^a   Cheung, Ambrose L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; MAZF TOXIN; MESSENGER RNA; RECA PROTEIN; RNA BINDING PROTEIN; SMAD ANCHOR FOR RECEPTOR ACTIVATION; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL RNA; RIBONUCLEASE;

ARTICLE; BACTERIAL VIABILITY; BACTERIOSTASIS; CELL DEATH; CONTROLLED STUDY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS AUREUS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL VIABILITY; RNA, BACTERIAL; RNA, MESSENGER; STAPHYLOCOCCUS AUREUS;

EID: 64049118002     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00907-08     Document Type: Article

References (32)

1. Aizenman, E., H. Engelberg-Kulka, and G. Glaser. 1996. An Escherichia colichromosomal "addiction module" regulated by guanosine [corrected] 3′,5′- bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl. Acad. Sci. USA 93:6059-6063.
2. Amitai, S., Y. Yassin, and H. Engelberg-Kulka. 2004. MazF-mediated cell death in Escherichia coli: a point of no return. J. Bacteriol. 186:8295-8300.
3. Cheung, A. L., K. J. Eberhardt, and V. A. Fischetti. 1994. A method to isolate RNA from gram-positive bacteria and mycobacteria. Anal. Biochem. 222: 511-514.
4. Cheung, A. L., Y. Chien, and A. S. Bayer. 1999. Hyperproduction of alphahemolysin in a sigB mutant is associated with elevated SarA expression in Staphylococcus aureus. Infect. Immun. 67:1331-1337.
5. Chien, Y., A. C. Manna, and A. L. Cheung. 1998. SarA level is a determinant of agr activation in Staphylococcus aureus. Mol. Microbiol. 30:991-1001.
6. Christensen, S. K., K. Pedersen, F. G. Hansen, and K. Gerdes. 2003. Toxinantitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J. Mol. Biol. 332:809- 819.
7. Condon, C. 2006. Shutdown decay of mRNA. Mol. Microbiol. 61:573-583.
8. D'Elia, M. A., M. P. Pereira, Y. S. Chung, W. Zhao, A. Chau, T. J. Kenney, M. C. Sulavik, T. A. Black, and E. D. Brown. 2006. Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J. Bacteriol. 188:4183-4189.
9. Engelberg-Kulka, H., R. Hazan, and S. Amitai. 2005. mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria. J. Cell Sci. 118:4327-4332.
10. Forsyth, R. A., R. J. Haselbeck, K. L. Ohlsen, R. T. Yamamoto, H. Xu, J. D. Trawick, D. Wall, L. Wang, V. Brown-Driver, J. M. Froelich, C. G. Kedar, P. King, M. McCarthy, C. Malone, B. Misiner, D. Robbins, Z. Tan, Z. Y. Zhu, G. Carr, D. A. Mosca, C. Zamudio, J. G. Foulkes, and J. W. Zyskind. 2002. A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol. Microbiol. 43:1387-1400.
11. Fu, Z., N. P. Donegan, G. Memmi, and A. L. Cheung. 2007. Characterization of MazFSa, an endoribonuclease from Staphylococcus aureus. J. Bacteriol. 189:8871-8879.
12. Fu, Z. B., K. L. Ng, T. L. Lam, and W. K. Wong. 2005. Cell death caused by hyper-expression of a secretory exoglucanase in Escherichia coli. Protein Expr. Purif. 42:67-77.
13. Georgellis, D., B. Sohlberg, F. U. Hartl, and A. von Gabain. 1995. Identification of GroEL as a constituent of an mRNA-protection complex in Escherichia coli. Mol. Microbiol. 16:1259-1268.
14. Gerdes, K., S. K. Christensen, and A. Lobner-Olesen. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
15. Gertz, S., S. Engelmann, R. Schmid, K. Ohlsen, J. Hacker, and M. Hecker. 1999. Regulation of sigmaB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol. Gen. Genet. 26:558-566.
16. Hazan, R., B. Sat, and H. Engelberg-Kulka. 2004. Escherichia coli mazEFmediated cell death is triggered by various stressful conditions. J. Bacteriol. 186:3663-3669.
17. Kolodkin-Gal, I., R. Hazan, A. Gaathon, S. Carmeli, and H. Engelberg- Kulka. 2007. A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli. Science 318:652-655.
18. Korch, S. B., and T. M. Hill. 2006. Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J. Bacteriol. 188:3826-3836.
19. Lioy, V. S., M. T. Martin, A. G. Camacho, R. Lurz, H. Antelmann, M. Hecker, E. Hitchin, Y. Ridge, J. M. Wells, and J. C. Alonso. 2006. pSM19035- encoded zeta toxin induces stasis followed by death in a subpopulation of cells. Microbiology 152:2365-2379.
20. Manna, A. C., and A. L. Cheung. 2006. Expression of SarX, a negative regulator of agr and exoprotein synthesis, is activated by MgrA in Staphylococcus aureus. J. Bacteriol. 188:4288-4299.
21. Pedersen, K., S. K. Christensen, and K. Gerdes. 2002. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol. 45:501-510.
22. Pedersen, K., A. V. Zavialov, M. Y. Pavlov, J. Elf, K. Gerdes, and M. Ehrenberg. 2003. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112:131-140.
23. Pellegrini, O., N. Mathy, A. Gogos, L. Shapiro, and C. Condon. 2005. The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/ PemK family and its inhibitor. Mol. Microbiol. 56:1139-1148.
24. Popovic, Z., and D. M. Templeton. 2005. A Northwestern blotting approach for studying iron regulatory element-binding proteins. Mol. Cell. Biochem. 268:67-74.
25. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Sat, B., R. Hazan, T. Fisher, H. Khaner, G. Glaser, and H. Engelberg-Kulka. 2001. Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J. Bacteriol. 183:2041-2045.
27. Schukkink, R. F., and R. H. Plasterk. 1990. TcA, the putative transposase of the C. elegans Tc1 transposon, has an N-terminal DNA binding domain. Nucleic Acids Res. 18:895-900.
28. Suzuki, M., J. Zhang, M. Liu, N. A. Woychik, and M. Inouye. 2005. Single protein production in living cells facilitated by an mRNA interferase. Mol. Cell 18:253-261.
29. Zhang, J., Y. Zhang, L. Zhu, M. Suzuki, and M. Inouye. 2004. Interference of mRNA function by sequence-specific endoribonuclease PemK. J. Biol. Chem. 279:20678-20684.
30. Zhang, Y., J. Zhang, K. P. Hoeflich, M. Ikura, G. Qing, and M. Inouye. 2003. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 12:913-923.
31. Zhang, Y., L. Zhu, J. Zhang, and M. Inouye. 2005. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J. Biol. Chem. 280: 26080-26088.
32. Zhu, L., Y. Zhang, J. S. The, J. Zhang, N. Connell, H. Rubin, and M. Inouye. 2006. Characterization of mRNA interferases from Mycobacterium tuberculosis. J. Biol. Chem. 281:18638-18643.