Gyrase inhibitors and thymine starvation disrupt the normal pattern of plasmid RK2 localization in Escherichia coli

Journal of Bacteriology

Volumn 187, Issue 10, 2005, Pages 3538-3547

  Johnson, Erik P ^a,b   Yao, Shiyin ^a   Helinski, Donald R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b QUEST DIAGNOSTICS NICHOLS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CEFALEXIN; DNA; GREEN FLUORESCENT PROTEIN; GYRASE INHIBITOR; HYBRID PROTEIN; NALIDIXIC ACID; NOVOBIOCIN; PROTEIN RARA; THYMINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CELL ELONGATION; DNA HELIX; DNA REPLICATION; DNA SYNTHESIS; ESCHERICHIA COLI; NONHUMAN; PLASMID; PLASMID RK2; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANTI-BACTERIAL AGENTS; CEPHALEXIN; DNA GYRASE; DNA REPLICATION; ENZYME INHIBITORS; ESCHERICHIA COLI; NALIDIXIC ACID; NOVOBIOCIN; PLASMIDS; THYMINE;

ESCHERICHIA COLI;

EID: 18244381015     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.10.3538-3547.2005     Document Type: Article

References (65)

1. Ahmad, S. I., S. H. Kirk, and A. Eisenstark. 1998. Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52:591-625.
2. Barre, F. X., B. Soballe, B. Michel, M. Aroyo, M. Robertson, and D. Sherratt. 2001. Circles: the replication-recombination-chromosome segregation connection. Proc. Natl. Acad. Sci. USA 98:8189-8195.
3. Bazill, G. W. 1967. Lethal unbalanced growth in bacteria. Nature 216:346-349.
4. Bignell, C. R., A. S. Haines, D. Khare, and C. M. Thomas. 1999. Effect of growth rate and incC mutation on symmetric plasmid distribution by the IncP-1 partitioning apparatus. Mol. Microbiol. 34:205-216.
5. Ebersbach, G., and K. Gerdes. 2004. Bacterial mitosis: partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol. Microbiol. 52:385-398.
6. Erdmann, N., T. Petroff, and B. E. Funnell. 1999. Intracellular localization of P1 ParB protein depends on ParA and parS. Proc. Natl. Acad. Sci. USA 96:14905-14910.
7. Espeli, O., P. Nurse, C. Levine, C. Lee, and K. J. Marians. 2003. SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli. Mol. Microbiol. 50:495-509.
8. Fangman, W. L. 1969. Specificity and efficiency of thymidine incorporation in Escherichia coli lacking thymidine phosphorylase. J. Bacteriol. 99:681-687.
9. Figurski, D. H., R. Meyer, and D. R. Helinski. 1979. Suppression of ColE1 replication properties by the IncP-1 plasmid RK2 in hybrid plasmids constructed in vitro. J. Mol. Biol. 133:295-318.
10. Freifelder, D. 1969. Single-strand breaks in bacterial DNA associated with thymine starvation J. Mol. Biol. 45:1-7.
11. Frenkiel-Krispin, D., I. Ben-Avraham, J. Englander, E. Shimoni, S. G. Wolf, and A. Minsky. 2004. Nucleoid restructuring in stationary-state bacteria. Mol. Microbiol. 51:395-405.
12. Gellert, M., K. Mizuuchi, M. H. O'Dea, T. Itoh, and J. I. Tomizawa. 1977. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl. Acad. Sci. USA 74:4772-4776.
13. Gellert, M., M. H. O'Dea, T. Itoh, and J. Tomizawa. 1976. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc. Natl. Acad. Sci. USA 73:4474-4478.
14. George, J. W., B. A. Stohr, D. J. Tomso, and K. N. Kreuzer. 2001. The tight linkage between DNA replication and double-strand break repair in bacteriophage T4. Proc. Natl. Acad. Sci. USA 98:8290-8297.
15. Gerdes, K., J. Moller-Jensen, G. Ebersbach, T. Kruse, and K. Nordstrom. 2004. Bacterial mitotic machineries. Cell 116:359-366.
16. Gordon, G. S., D. Sitnikov, C. D. Webb, A. Teleman, A. Straight, R. Losick, A. W. Murray, and A. Wright. 1997. Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90:1113-1121.
17. Gordon, G. S., and A. Wright. 2000. DNA segregation in bacteria. Annu. Rev. Microbiol. 54:681-708.
18. Gordon, S., J. Rech, D. Lane, and A. Wright. 2004. Kinetics of plasmid segregation in Escherichia coli. Mol. Microbiol. 51:461-469.
19. BAD promoter. J. Bacteriol. 177:4121-4130.
20. Hardy, C. D., and N. R. Cozzarelli. 2003. Alteration of. Escherichia coli topoisomerase IV to novobiocin resistance. Antimicrob. Agents Chemother. 47:941-947.
21. Hashimolo-Goloh, T., and M. Sekiguchi. 1977. Mutations of temperature sensitivity in R plasmid pSC101. J. Bacteriol. 131:405-412.
22. Hiasa, H., D. O. Yousef, and K. J. Marians. 1996. DNA strand cleavage is required for replication fork arrest by a frozen topoisomerase-quinolone-DNA ternary complex. J. Biol. Chem. 271:26424-26429.
23. Hill, W. E., and W. L. Fangman. 1973. Single-strand breaks in deoxyribonucleic acid and viability loss during deoxyribonucleic acid synthesis inhibition in Escherichia coli. J. Bacteriol. 116:1329-1335.
24. Hiraga, S. 2000. Dynamic localization of bacterial and plasmid chromosomes. Annu. Rev. Genet. 34:21-59.
25. Ho, T. Q., Z. Zhong, S. Aung, and J. Pogliano. 2002. Compatible bacterial plasmids are targeted to independent cellular locations in Escherichia coli. EMBO J. 21:1864-1872.
26. Hoshino, K., A. Kitamura, I. Morrissey, K. Sato, J. Kato, and H. Ikeda. 1994. Comparison of inhibition of Escherichia coli topoisomerase IV by quinolones with DNA gyrase inhibition. Antimicrob. Agents Chemother. 38:2623-2627.
27. Howard, M. T., S. H. Neece, S. W. Matson, and K. N. Kreuzer. 1994. Disruption of a topoisomerase-DNA cleavage complex by a DNA helicase. Proc. Natl. Acad. Sci. USA 91:12031-12035.
28. - cultures of Escherichia coli K-12. J. Bacteriol. 124:1113-1121.
29. Huisman, O., and R. D'Ari. 1981. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature 290:797-799.
30. Ishino, F., and M. Matsuhashi. 1981. Peptidoglycan synthetic enzyme activities of highly purified penicillin-binding protein 3 in Escherichia coli: a septum-forming reaction sequence. Biochem. Biophys. Res. Commun. 101:905-911.
31. Jensen, R. B., and K. Gerdes. 1999. Mechanism of DNA segregation in prokaryotes: ParM partitioning protein of plasmid R1 co-localizes with its replicon during the cell cycle. EMBO J. 18:4076-4084.
32. Jensen, R. B., and K. Gerdes. 1997. Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. J. Mol. Biol. 269:505-513.
33. Jensen, R. B., S. C. Wang, and L. Shapiro. 2001. A moving DNA replication factory in Caulobacter crescentus. EMBO J. 20:4952-4963.
34. Jiang, Y., J. Pogliano, D. R. Helinski, and I. Konieczny. 2002. ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase. Mol. Microbiol. 44:971-979.
35. Khodursky, A. B., E. L. Zechiedrich, and N. R. Cozzarelli. 1995. Topoisomerase IV is a target of quinolones in Escherichia coli. Proc. Natl. Acad. Sci. USA 92:11801-11805.
36. Koppes, L. J., C. L. Woldringh, and N. Nanninga. 1999. Escherichia coli contains a DNA replication compartment in the cell center. Biochimie 81:803-810.
37. Kruse, T., J. Moller-Jensen, A. Lobner-Olesen, and K. Gerdes. 2003. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22:5283-5292.
38. Lau, I. F., S. R. Filipe, B. Soballe, O. A. Okstad, F. X. Barre, and D. J. Sherratt. 2003. Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol. Microbiol. 49:731-743.
39. Lawley, T. D, and D. E. Taylor. 2003. Characterization of the double-partitioning modules of R27: correlating plasmid stability with plasmid localization. J. Bacteriol. 185:3060-3067.
40. Lemon, K. P., and A. D. Grossman. 2001. The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev. 15:2031-2041.
41. Lemon, K. P., and A. D. Grossman. 1998. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516-1519.
42. Lemon, K. P., and A. D. Grossman. 2000. Movement of replicating DNA through a stationary replisome. Mol. Cell 6:1321-1330.
43. Lewis, R. J., O. M. Singh, C. V. Smith, T. Skarzynski, A. Maxwell, A. J. Wonacott, and D. B. Wigley. 1996. The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J. 15:1412-1420.
44. Li, Y., and S. Austin. 2002. The P1 plasmid in action: time-lapse photomicroscopy reveals some unexpected aspects of plasmid partition. Plasmid 48:174-178.
45. Li, Y., and S. Austin. 2002. The P1 plasmid is segregated to daughter cells by a "capture and ejection" mechanism coordinated with Escherichia coli cell division. Mol. Microbiol. 46:63-74.
46. Miller, C., and S. N. Cohen. 1999. Separate roles of Escherichia coli replication proteins in synthesis and partitioning of pSC101 plasmid DNA. J. Bacteriol. 181:7552-7557.
47. Moller-Jensen, J., J. Borch, M. Dam, R. B. Jensen, P. Roepstorff, and K. Gerdes. 2003. Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol. Cell 12:1477-1487.
48. Moller-Jensen, J., R. B. Jensen, J. Lowe, and K. Gerdes. 2002. Prokaryotic DNA segregation by an actin-like filament. EMBO J. 21:3119-3127.
49. Niki, H., and S. Hiraga. 1997. Subcellular distribution of actively partitioning F plasmid during the cell division cycle in E. coli. Cell 90:951-957.
50. Nordstrom, K., and K. Gerdes. 2003. Clustering versus random segregation of plasmids lacking a partitioning function: a plasmid paradox? Plasmid 50:95-101.
51. Onogi, T., T. Miki, and S. Hiraga. 2002. Behavior of sister copies of mini-F plasmid after synchronized plasmid replication in Escherichia coli cells. J. Bacteriol. 184:3142-3145.
52. Pardee, A. B., F. Jacob, and J. Monod. 1959. The genetic control and cytoplasmic expression of "inducibility" in the synthesis of β-galactosidase by E. coli. J. Mol. Biol. 1:165-178.
53. Pogliano, J., T. Q. Ho, Z. Zhong, and D. R. Helinski. 2001. Multicopy plasmids are clustered and localized in Escherichia coli. Proc. Natl. Acad. Sci. USA 98:4486-4491.
54. Reich, Z., E. J. Wachtel, and A. Minsky. 1994. Liquid-crystalline mesophases of plasmid DNA in bacteria. Science 264:1460-1463.
55. Rosche, T. M., A. Siddique, M. Larsen, and D. Figurski. 2000. Incompatibility protein IncC and global regulator KorB interact in active partition of promiscuous plasmid RK2. J. Bacteriol. 182:6014-6026.
56. Sherratt, D. J. 2003. Bacterial chromosome dynamics. Science 301:780-785.
57. Sugino, A., N. P. Higgins, P. O. Brown, C. L. Peebles, and N. R. Cozzarelli. 1978. Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc. Natl. Acad. Sci. USA 75:4838-4842.
58. Sugino, A., C. L. Peebles, K. N. Kreuzer, and N. R. Cozzarelli. 1977. Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc. Natl. Acad. Sci. USA 74:4767-4771.
59. Thomas, C. M., M. A. Cross, A. A. K. Hussain, and C. A. Smith. 1984. Analysis of copy number control elements in the region of the vegetative replication origin of the broad host range plasmid RK2. EMBO J. 3:57-63.
60. Thomas, C. M., R. Meyer, and D. R. Helinski. 1980. Regions of broad-host-range plasmid RK2 which are essential for replication and maintenance. J. Bacteriol. 141:213-222.
61. van den Ent, F., J. Moller-Jensen, L. A. Amos, K. Gerdes, and J. Lowe. 2002. F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J. 21:6935-6943.
62. Wang, J. D., M. E. Rokop, M. M. Barker, N. R. Hanson, and A. D. Grossman. 2004. Multicopy plasmids affect replisome positioning in Bacillus subtilis. J. Bacteriol. 186:7084-7090.
63. Weitao, T., S. Dasgupta, and K. Nordstrom. 2000. Plasmid R1 is present as clusters in the cells of Escherichia coli. Plasmid 43:200-204.
64. Weitao, T., S. Dasgupta, and K. Nordstrom. 2000. Role of the mukB gene in chromosome and plasmid partition in Escherichia coli. Mol. Microbiol. 38:392-400.
65. Yoshinaga, K. 1973. Double-strand scission of DNA involved in thymineless death of Escherichia coli 15 TAU. Biochim. Biophys. Acta 294:204-213.