Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli

Journal of Bacteriology

Volumn 188, Issue 24, 2006, Pages 8360-8367

  Correia, Frederick F ^a   D'Onofrio, Anthony ^a   Rejtar, Tomas ^a   Li, Lingyun ^a   Karger, Barry L ^a   Makarova, Kira ^b   Koonin, Eugene V ^b   Lewis, Kim ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; BACTERIAL TOXIN; CEFOTAXIME; CHLORAMPHENICOL; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); HIPA PROTEIN; HIPBA TOXIN; MITOMYCIN C; OFLOXACIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL KINASE; PROTEIN KINASE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; TOBRAMYCIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIUM MUTANT; DRUG TOLERANCE; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GENE OVEREXPRESSION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MULTIDRUG TOLERANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; CULTURE MEDIA; DRUG TOLERANCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN-SERINE-THREONINE KINASES;

ESCHERICHIA COLI;

EID: 33845428404     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01237-06     Document Type: Article

References (36)

1. Adachi, J., P. J. Waddell, W. Martin, and M. Hasegawa. 2000. Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J. Mol. Evol. 50:348-358.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Balaban, N. Q., J. Merrin, R. Chait, L. Kowalik, and S. Leibler. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1625.
4. Barylko, B., S. H. Gerber, D. D. Binns, N. Grichine, M. Khvotchev, T. C. Sudhof, and J. P. Albanesi. 2001. A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J. Biol. Chem. 276:7705-7708.
5. Barylko, B., P. Wlodarski, D. D. Binns, S. H. Gerber, S. Earnest, T. C. Sudhof, N. Grichine, and J. P. Albanesi. 2002. Analysis of the catalytic domain of phosphatidylinositol 4-kinase type II. J. Biol. Chem. 277:44366-44375.
6. Bigger, J. W. 1944. Treatment of staphylococcal infections with penicillin. Lancet ii:497-500.
7. Black, D. S., B. Irwin, and H. S. Moyed. 1994. Autoregulation of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 176:4081-4091.
8. Black, D. S., A. J. Kelly, M. J. Mardis, and H. S. Moyed. 1991. Structure and organization of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 173:5732-5739.
9. Brooun, A., S. Liu, and K. Lewis. 2000. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44:640-646.
10. Brown, J. M., and K. J. Shaw. 2003. A novel family of Escherichia coli toxin-antitoxin gene pairs. J. Bacteriol. 185:6600-6608.
11. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
12. Falla, T. J., and I. Chopra. 1998. Joint tolerance to beta-lactam and fluoroquinolone antibiotics in Escherichia coli results from overexpression of hipA. Antimicrob. Agents Chemother. 42:3282-3284.
13. Gerdes, K., S. K. Christensen, and A. Lobner-Olesen. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
14. BAD promoter. J. Bacteriol. 177:4121-4130.
15. Harrison, J. J., H. Ceri, N. J. Roper, E. A. Badry, K. M. Sproule, and R. J. Turner. 2005. Persister cells mediate tolerance to metal oxyanions in Escherichia coli. Microbiology 151:3181-3195.
16. Harrison, J. J., R. J. Turner, and H. Ceri. 2005. Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environ. Microbiol. 7:981-994.
17. Keren, I., N. Kaldalu, A. Spoering, Y. Wang, and K. Lewis. 2004. Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230:13-18.
18. Keren, I., D. Shah, A. Spoering, N. Kaldalu, and K. Lewis. 2004. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186:8172-8180.
19. Korch, S. B., T. A. Henderson, and T. M. Hill. 2003. Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50:1199-1213.
20. 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.
21. Lewis, K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64:503-514.
22. Lewis, K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45:999-1007.
23. Lewis, K., A. Salyers, H. Taber, and R. Wax. 2002. Bacterial resistance to antimicrobials: mechanisms, genetics, medical practice and public health. Marcel Dekker, New York, N.Y.
24. Lewis, K., A. Spoering, N. Kaldalu, I. Keren, and D. Shah. 2005. Persisters: specialized cells responsible for biofilm tolerance to antimicrobial agents, p. 241-256. In J. Pace, M. E. Rupp, and R. G. Finch (ed.), Biofilms, infection, and antimicrobial therapy. Taylor & Francis, Boca Raton, Fla.
25. McCormack, A. L., D. M. Schieltz, B. Goode, S. Yang, G. Barnes, D. Drubin, and J. R. Yates III. 1997. Direct analysis and identification of proteins in mixtures by LC/MS/MS and database searching at the low-femtomole level. Anal. Chem. 69:767-776.
26. Meinhart, A., J. C. Alonso, N. Strater, and W. Saenger. 2003. Crystal structure of the plasmid maintenance system epsilon/zeta: functional mechanism of toxin zeta and inactivation by epsilon 2 zeta 2 complex formation. Proc. Natl. Acad. Sci. USA 100:1661-1666.
27. Moyed, H. S., and K. P. Bertrand. 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.
28. Moyed, H. S., and S. H. Broderick. 1986. Molecular cloning and expression of hipA, a gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 166:399-403.
29. Pandey, D. P., and K. Gerdes. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 33:966-976.
30. 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.
31. Shah, D. V., Z. Zhang, K. Kurg, N. Kaldalu, A. Khodursky, and K. Lewis. 2006. Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6:53.
32. Spoering, A. L., and K. Lewis. 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183:6746-6751.
33. Spoering, A. L., M. Vulić, and K. Lewis. 2006. GlpD and PlsB participate in persister cell formation in Escherichia coli. J. Bacteriol. 188:5136-5144.
34. Steen, H., J. A. Jebanathirajah, M. Springer, and M. W. Kirschner. 2005. Stable isotope-free relative and absolute quantitation of protein phosphorylation stoichiometry by MS. Proc. Natl. Acad. Sci. USA 102:3948-3953.
35. Vázquez-Laslop, N., H. Lee, and A. A. Neyfakh. 2006. Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J. Bacteriol. 188:3494-3497.
36. Wiuff, C., R. M. Zappala, R. R. Regoes, K. N. Garner, F. Baquero, and B. R. Levin. 2005. Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob. Agents Chemother. 49:1483-1494.