Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: Involvement of the yefM-yoeB toxin-antitoxin system

Molecular Microbiology

Volumn 51, Issue 6, 2004, Pages 1705-1717

  Christensen, Susanne K ^a   Maenhaut Michel, Geneviève ^b   Mine, Natacha ^b   Gottesman, Susan ^c   Gerdes, Kenn ^a   Van Melderen, Laurence ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTITOXIN; BACTERIAL TOXIN; ENDOPEPTIDASE LA; MESSENGER RNA; PROTEINASE; UNCLASSIFIED DRUG; YEFM ANTITOXIN; YOEB TOXIN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA TRANSLATION; TOXIN ANALYSIS;

ADENOSINE TRIPHOSPHATASES; ATP-DEPENDENT PROTEASES; BACTERIAL TOXINS; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; DNA PRIMERS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENES, BACTERIAL; GENES, LETHAL; HEAT-SHOCK PROTEINS; HYDROLYSIS; METHIONINE; PROTEASE LA; PROTEIN BIOSYNTHESIS; RNA, BACTERIAL; RNA, MESSENGER; SERINE ENDOPEPTIDASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 1642483754     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03941.x     Document Type: Article

References (42)

1. 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 USA 93: 6059-6063.
2. Bech, F.W., Jorgensen, S.T., Diderichsen, B., and Karlstrom, O.H. (1985) Sequence of the relB transcription unit from Escherichia coli and identification of the relB gene. EMBO J 4: 1059-1066.
3. Biran, D., Gur, E., Gollan, L., and Ron, E.Z. (2000) Control of methionine biosynthesis in Escherichia coli by proteolysis. Mol Microbiol 37: 1436-1443.
4. Bukhari, A.I., and Zipser, D. (1973) Mutants of Escherichia coli with a defect in the degradation of nonsense fragments. Nat New Biol 243: 238-241.
5. 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.
6. 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 USA 98: 14328-14333.
7. Christensen, S.K., Pedersen, K., Hansen, G.H., 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.
8. Claret, L., and Hughes, C. (2000) Rapid turnover of FlhD and FlhC, the flagellar regulon transcriptional activator proteins, during Proteus swarming. J Bacteriol 182: 833-836.
9. Clark, D., and Maaloe, O. (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 23: 99-112.
10. Couturier, M., Bahassi el, M., and Van Melderen, L. (1998) Bacterial death by DNA gyrase poisoning. Trends Microbiol 6: 269-275.
11. Dam Mikkelsen, N., and Gerdes, K. (1997) Sok antisense RNA from plasmid R1 is functionally inactivated by RNase E and polyadenylated by poly (A) polymerase I. Mol Microbiol 26: 311-320.
12. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
13. Engelberg-Kulka, H., and Glaser, G. (1999) Addiction modules and programmed cell death and antideath in bacterial cultures. Annu Rev Microbiol 53: 43-70.
14. Gerdes, K. (2000) Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J Bacteriol 182: 561-572.
15. Gillet, R., and Felden, B. (2001) Emerging views on tmRNA-mediated protein tagging and ribosome rescue. Mol Microbiol 42: 879-885.
16. Glansdorff, N. (1965) Topography of cotransducible arginine mutations in E. coli K-12. Genetics 51: 167-179.
17. Goff, S.A., and Goldberg, A.L. (1987) An increased content of protease La, the lon gene product, increases protein degradation and blocks growth in Escherichia coli. J Biol Chem 262: 4508-4515.
18. Gotfredsen, M., and Gerdes, K. (1998) The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol Microbiol 29: 1065-1076.
19. Gottesman, S. (1999) Regulation by proteolysis: developmental switches. Curr Opin Microbiol 2: 142-147.
20. Gottesman, S., and Zipser, D. (1978) Deg phenotype of Escherichia coli lon mutants. J Bacteriol 133: 844-851.
21. Grady, R., and Hayes, F. (2003) Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium. Mol Microbiol 47: 1419-1432.
22. 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.
23. Jenal, U., and Hengge-Aronis, R. (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6: 163-172.
24. Komine, Y., Kitabatake, M., Yokogawa, T., Nishikawa, K., and Inokuchi, H. (1994) A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc Natl Acad Sci USA 91: 9223-9227.
25. Kuroda, A., Nomura, K., Ohtomo, R., Kato, J., Ikeda, T., Takiguchi, N., Ohtake, H., and Kornberg, A. (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293: 705-708.
26. 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 USA 92: 3274-3277.
27. Liu, J., Cosby, W.M., and Zuber, P. (1999) Role of lon and ClpX in the post-translational regulation of a sigma subunit of RNA polymerase required for cellular differentiation in Bacillus subtilis. Mol Microbiol 33: 415-428.
28. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory Press.
29. Masuda, Y., Miyakawa, K., Nishimura, Y., and 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.
30. Maurizi, M.R., Trisler, P., and Gottesman, S. (1985) Insertional mutagenesis of the lon gene in Escherichia coli: Ion is dispensabl. J Bacteriol 164: 1124-1135.
31. Miller, J.H. (1972) Experiments in Molecular Genetics. Plainview, NY: Cold Spring Harbor Laboratory Press.
32. 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.
33. 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.
34. Sat, B., Hazan, R., Fisher, T., Khaner, H., Glaser, G., and Engelberg-Kulka, H. (2001) Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J Bacteriol 183: 2041-2045.
35. Sat, B., Reches, M., and Engelberg-Kulka, H. (2003) The Escherichia coli mazEF suicide module mediates thymineless death. J Bacteriol 185: 1803-1807.
36. 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.
37. 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.
38. Van Melderen, L., and Gottesman, S. (1999) Substrate sequestration by a proteolytically inactive Lon mutant. Proc Natl Acad Sci USA 96: 6064-6071.
39. Wang, L., Elliott, M., and Elliott, T. (1999a) Conditional stability of the HemA protein (glutamyl-tRNA reductase) regulates heme biosynthesis in Salmonella typhimurium. J Bacteriol 181: 1211-1219.
40. Wang, L., Wilson, S., and Elliott, T. (1999b) A mutant HemA protein with positive charge close to the N terminus is stabilized against heme-regulated proteolysis in Salmonella typhimurium. J Bacteriol 181: 6033-6041.
41. Wright, R., Stephens, C., Zweiger, G., Shapiro, L., and Alley, M.R. (1996) Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev 10: 1532-1542.
42. Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G., and Cashel, M. (1991) Residual guanosine 3′,5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266: 5980-5990.