Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 15, 2008, Pages 5885-5890

  Liu, Mohan ^a   Zhang, Yonglong ^a   Inouye, Masayori ^a   Woychik, Nancy A ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

16S rRNA; Antitoxin; Bacteriophage P1; Hygromycin B; Postsegregational killing

Indexed keywords

DOC TOXIN; HYGROMYCIN B; MESSENGER RNA; RIBOSOME RNA; TOXIN;

ARTICLE; BINDING SITE; CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RIBOSOME SUBUNIT;

BACTERIOPHAGE P1; BINDING SITES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA STABILITY; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 44449119912     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0711949105     Document Type: Article

References (53)

1. Gerdes K, Christensen SK, Lobner-Olesen A (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3:371-382.
2. Pandey DP, Gerdes K (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33:966-976.
3. Suzuki M, Zhang J, Liu M, Woychik NA, Inouye M (2005) Single protein production in living cells facilitated by an mRNA interferase. Mol Cell 18:253-261.
4. Amitai S, Yassin Y, Engelberg-Kulka H (2004) MazF-mediated cell death in Escherichia coli: A point of no return. J Bacteriol 186:8295-8300.
5. Engelberg-Kulka H, Hazan R, Amitai S (2005) mazEF: A chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria. J Cell Sci 118:4327-4332.
6. Pedersen K, Christensen SK, Gerdes K (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol Microbiol 45:501-510.
7. Engelberg-Kulka H, Sat B, Reches M, Amitai S, Hazan R (2004) Bacterial programmed cell death systems as targets for antibiotics. Trends Microbiol 12:66-71.
8. Nariya H, Inouye M (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132:55-66.
9. Brooun A, Liu S, Lewis K (2000) A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 44:640-646.
10. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172-8180.
11. Lewis K (2005) Persister cells and the riddle of biofilm survival. Biochemistry (Moscow) 70:267-274.
12. Moyed HS, Bertrand KP (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.
13. Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746-6751.
14. Jensen RB, Gerdes K (1995) Programmed cell death in bacteria: Proteic plasmid stabilization systems. Mol Microbiol 17:205-210.
15. Lehnherr H, Maguin E, Jafri S, Yarmolinsky MB (1993) Plasmid addiction genes of bacteriophage P1: Doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J Mol Biol 233:414-428.
16. Magnuson R, Lehnherr H, Mukhopadhyay G, Yarmolinsky MB (1996) Autoregulation of the plasmid addiction operon of bacteriophage P1. J Biol Chem 271:18705-18710.
17. Gazit E, Sauer RT (1999) The Doc toxin and Phd antidote proteins of the bacteriophage P1 plasmid addiction system form a heterotrimeric complex. J Biol Chem 274:16813-16818.
18. Gazit E, Sauer RT (1999) Stability and DNA binding of the phd protein of the phage P1 plasmid addiction system. J Biol Chem 274:2652-2657.
19. Magnuson R, Yarmolinsky MB (1998) Corepression of the P1 addiction operon by Phd and Doc. J Bacteriol 180:6342-6351.
20. Lehnherr H, Yarmolinsky MB (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.
21. McKinley JE, Magnuson RD (2005) Characterization of the Phd repressor-antitoxin boundary. J Bacteriol 187:765-770.
22. Smith JA, Magnuson RD (2004) Modular organization of the Phd repressor/antitoxin protein. J Bacteriol 186:2692-2698.
23. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
24. Hazan R, Sat B, Reches M, Engelberg-Kulka H (2001) Postsegregational killing mediated by the P1 phage "addiction module" phd-doc requires the Escherichia coli programmed cell death system mazEF. J Bacteriol 183:2046-2050.
25. Halegoua S, Hirashima A, Sekizawa J, Inouye M (1976) Protein synthesis in toluene-treated Escherichia coli. Exclusive synthesis of membrane proteins. Eur J Biochem 69:163-167.
26. Mukherjee S, Shukla A, Guptasarma P (2003) Single-step purification of a protein-folding catalyst, the SlyD peptidyl prolyl isomerase (PPI), from cytoplasmic extracts of Escherichia coli. Biotechnol Appl Biochem 37:183-186.
27. Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G, Inouye M (2003) MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 12:913-923.
28. Zhang Y, Zhu L, Zhang J, Inouye M (2005) Characterization of ChpBK, an mRNA interferase from Escherichia coli. J Biol Chem 280:26080-26088.
29. Pimentel B, Madine MA, de la Cueva-Mendez G (2005) Kid cleaves specific mRNAs at UUACU sites to rescue the copy number of plasmid R1. EMBO J 24:3459-3469.
30. Zhang J, Zhang Y, Zhu L, Suzuki M, Inouye M (2004) Interference of mRNA function by sequence-specific endoribonuclease PemK. J Biol Chem 279:20678-20684.
31. Christensen-Dalsgaard M, Gerdes K (2006) Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 62:397-411.
32. Pedersen S, Reeh S (1978) Functional mRNA half lives in E. coli. Mol Gen Genet 166:329-336.
33. Deana A, Ehrlich R, Reiss C (1998) Silent mutations in the Escherichia coli ompA leader peptide region strongly affect transcription and translation in vivo. Nucleic Acids Res 26:4778-4782.
34. Christensen SK, Gerdes K (2003) RelE toxins from Bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol Microbiol 48:1389-1400.
35. Hayes CS, Sauer RT (2003) Cleavage of the Asitem RNA codon during ribosome pausing provides a mechanism for translational quality control. Mol Cell 12:903-911.
36. Pedersen K, et al. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112:131-140.
37. Christensen SK, et al. (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.
38. Cabanas MJ, Vazquez D, Modolell J (1978) Dual interference of hygromycin B with ribosomal translocation and with aminoacyl-tRNA recognition. Eur J Biochem 87:21-27.
39. Cabanas MJ, Vazquez D, Modolell J (1978) Inhibition of ribosomal translocation by aminoglycoside antibiotics. Biochem Biophys Res Commun 83:991-997.
40. Eustice DC, Wilhelm JM (1984) Fidelity of the eukaryotic codon-anticodon interaction: Interference by aminoglycoside antibiotics. Biochemistry 23:1462-1467.
41. Brodersen DE, et al. (2000) The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103:1143-1154.
42. DeStasio EA, Dahlberg AE (1990) Effects of mutagenesis of a conserved base-paired site near the decoding region of Escherichia coli 16 S ribosomal RNA J Mol Biol 212:127-133.
43. DeStasio EA, Moazed D, Noller HF, Dahlberg AE(1989) Mutations in 16S ribosomal RNA disrupt antibiotic-RNA interactions. EMBO J 8:1213-1216.
44. Pfister P, Risch M, Brodersen DE, Bottger EC (2003) Role of 16S rRNA helix 44 in ribosomal resistance to hygromycin B. Antimicrob Agents Chemother 47:1496-1502.
45. Eustice DC, Wilhelm JM (1984) Mechanisms of action of aminoglycoside antibiotics in eukaryotic protein synthesis. Antimicrob Agents Chemother 26:53-60.
46. Ganoza MC, Kiel MC (2001) A ribosomal ATPase is a target for hygromycin B inhibition on Escherichia coli ribosomes. Antimicrob Agents Chemother 45:2813-2819.
47. Gonzalez A, Jimenez A, Vazquez D, Davies JE, Schindler D (1978) Studies on the mode of action of hygromycin B, an inhibitor of translocation in eukaryotes. Biochim Biophys Acta 521:459-469.
48. Franceschi F, Duffy EM (2006) Structure-based drug design meets the ribosome. Biochem Pharmacol 71:1016-1025.
49. Halegoua S, Hirashima A, Inouye M (1976) Puromycin-resistant biosynthesis of a specific outer-membrane lipoprotein of Escherichia coli. J Bacteriol 126:183-191.
50. Moses RE, Richardson CC (1970) Replication and repair of DNA in cells of Escherichia coli treated with toluene. Proc Natl Acad Sci USA 67:674-681.
51. Peterson RL, Radcliffe CW, Pace NR (1971) Ribonucleic acid synthesis in bacteria treated with toluene. J Bacteriol 107:585-588.
52. Hirashima A, Inouye M (1973) Specific biosynthesis of an envelope protein of Escherichia coli. Nature 242:405-407.
53. Sarmientos P, Sylvester JE, Contente S, Cashel M (1983) Differential stringent control of the tandem E. coli ribosomal RNA promoters from the rrnA operon expressed in vivo in multicopy plasmids. Cell 32:1337-1346.