Dysfunctional MreB inhibits chromosome segregation in Escherichia coli

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5283-5292

  Kruse, Thomas ^a   Møeller Jensen, Jakob ^a   Løbner Olesen, Anders ^b   Gerdes, Kenn ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ROSKILDE UNIVERSITY   (Denmark)

Author keywords

Actin; Chromosome segregation; MreB; OriC; TerC

Indexed keywords

ACTIN; BACTERIAL PROTEIN; CELL PROTEIN; MREB PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL DIVISION; CELLULAR DISTRIBUTION; CHROMOSOME SEGREGATION; ESCHERICHIA COLI; FLOW CYTOMETRY; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; ORIGIN RECOGNITION COMPLEX; RNA; TELOMERASE; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 0141864658     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg504     Document Type: Article

References (55)

1. Aussel, L., Barre, F.X., Aroyo, M., Stasiak, A., Stasiak, A.Z. and Sherratt, D. (2002) FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell, 108, 195-205.
2. Bemander, R. and Nordstrom, K. (1990) Chromosome replication does not trigger cell division in E. coli. Cell, 60, 365-374.
3. Bork, P., Sander, C. and Valencia, A. (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA, 89, 7290-7294.
4. Carballido-Lopez, R. and Errington, J. (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell, 4, 19-28.
5. Casadaban, M.J. and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol., 138, 179-207.
6. Daniel, R.A. and Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell, 113, 767-776.
7. 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.
8. de Boer, P.A., Crossley, R.E. and Rothfield, L.I. (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell, 56, 641-649.
9. De Pedro, M.A., Donachie, W.D., Holtje, J.V. and Schwarz,H. (2001) Constitutive septal murein synthesis in Escherichia coli with impaired activity of the morphogenetic proteins RodA and penicillin-binding protein 2. J. Bacteriol., 183, 4115-4126.
10. Doi, M., Wachi, M., Ishino, F., Tomioka, S., Ito, M., Sakagami, Y., Suzuki, A. and Matsuhashi, M. (1988) Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells. J. Bacteriol., 170, 4619-4624.
11. Draper, G.C. and Gober, J.W. (2002) Bacterial chromosome segregation. Annu. Rev. Microbiol., 56, 567-597.
12. Dworkin, J. and Losick, R. (2002) Does RNA polymerase help drive chromosome segregation in bacteria? Proc. Natl Acad. Sci. USA, 99, 14089-14094.
13. Gerdes, K., Moller-Jensen, J. and Jensen R.B (2000) Plasmid and chromosome partitioning: surprises from phylogeny. Mol. Microbiol., 37, 455-466.
14. Glaser, P., Sharpe, M.E., Raether, B., Perego, M., Ohlsen, K. and Errington, J. (1997) Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev., 11, 1160-1168.
15. Gordon, G.S. and Wright, A. (1998) DNA segregation: putting chromosomes in their place. Curr. Biol., 8, R925-R927.
16. Gordon, G.S. and Wright, A. (2000) DNA segregation in bacteria. Annu. Rev. Microbiol., 54, 681-708.
17. Gordon, G.S., Sitnikov, D., Webb, C.D., Teleman, A., Straight, A., Losick, R., Murray, A.W. and Wright, A. (1997) Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell, 90, 1113-1121.
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. 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.
20. Harry, E.J., Pogliano, K. and Losick, R. (1995) Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis. J. Bacteriol., 177, 3386-3393.
21. Hayes, F. (2000) The partition system of multidrug resistance plasmid TP228 includes a novel protein that epitomizes an evolutionarily distinct subgroup of the ParA superfamily. Mol. Microbiol., 37, 528-541.
22. Jacob, F., Brenner, S. and Cuzin, F. (1963) On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp. Quant. Biol., 23, 329-348.
23. Jensen, R.B. and Gerdes, K. (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.
24. Jensen, R.B. and Gerdes, K. (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.
25. Jensen, R.B. and Shapiro, L. (1999) Chromosome segregation during the prokaryotic cell division cycle. Curr. Opin. Cell Biol., 11, 726-731.
26. Jones, L.J., Carballido-Lopez, R. and Errington, J. (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell, 104, 913-922.
27. Lemon, K.P. and Grossman, A.D. (2000) Movement of replicating DNA through a stationary replisome. Mol. Cell, 6, 1321-1330.
28. Lemon. K.P. and Grossman, A.D. (2001) The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev., 15, 2031-2041.
29. Lewis, P.J. and Errington, J. (1997) Direct evidence for active segregation of oriC regions of the Bacillus subtilis chromosome and colocalization with the SpoOJ partitioning protein. Mol. Microbiol., 25, 945-954.
30. Li, Y., Sergueev, K. and Austin, S. (2002) The segregation of the Escherichia coli origin and terminus of replication. Mol. Microbiol., 46, 985-996.
31. Lin, D.C. and Grossman, A.D. (1998) Identification and characterization of a bacterial chromosome partitioning site. Cell, 92, 675-685.
32. Lobner-Olesen, A., Skarstad, K., Hansen, F.G., von Meyenburg, K. and Boye, E. (1989) The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell, 57, 881-889.
33. Moller-Jensen, J., Jensen, R.B., Lowe, J. and Gerdes, K. (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J., 21, 3119-3127.
34. Niki, H. and Hiraga, S. (1998) Polar localization of the replication origin and terminus in Escherichia coli nucleoids during chromosome partitioning. Genes Dev., 12, 1036-1045.
35. Niki, H., Jaffe, A., Imamura, R., Ogura, T. and Hiraga, S. (1991) The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J., 10, 183-193.
36. Niki, H., Yamaichi, Y. and Hiraga, S. (2000) Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev., 14, 212-223.
37. Norris, V. (1995) Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol. Microbiol., 16, 1051-1057.
38. Rodionov, O., Lobocka, M. and Yarmolinsky, M. (1999) Silencing of genes flanking the P1 plasmid centromere. Science, 283, 546-549.
39. Sawitzke, J.A. and Austin, S. (2000) Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc. Natl Acad. Sci. USA, 97, 1671-1676.
40. Sharpe, M.E. and Errington, J. (1999) Upheaval in the bacterial nucleoid. An active chromosome segregation mechanism. Trends Genet., 15, 70-74.
41. Shih, Y.L., Le, T. and Rothfield, L. (2003) Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc. Natl Acad. Sci. USA, 100, 7865-7870.
42. Skarstad, K., Boye, E. and Steen, H.B. (1986) Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J., 5, 1711-1717.
43. Teleman, A.A., Graumann, P.L., Lin, D.C.H., Grossman, A.D. and Losick, R. (1998) Chromosome arrangement within a bacterium. Curr. Biol., 8, 1102-1109.
44. van den Ent, F., Amos, L.A. and Lowe, J. (2001) Prokaryotic origin of the actin cytoskeleton. Nature, 413, 39-44.
45. van den Ent, F., Moller-Jensen, J., Amos, L.A., Gerdes, K. and Lowe, J. (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J., 21, 6935-6943.
46. Van Helvoort, J.M. and Woldringh, C.L. (1994) Nucleoid partitioning in Escherichia coli during steady-state growth and upon recovery from chloramphenicol treatment. Mol. Microbiol., 13, 577-583.
47. Wachi, M. and Matsuhashi, M. (1989) Negative control of cell division by mreB, a gene that functions in determining the rod shape of Escherichia coli cells. J. Bacteriol., 171, 3123-3127.
48. Wachi, M., Doi, M., Tamaki, S., Park, W., Nakajima-Iijima, S. and Matsuhashi, M. (1987) Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J. Bacteriol., 169, 4935-4940.
49. Webb, C.D., Teleman, A., Gordon, S., Straight, A., Belmont, A., Lin, D.C., Grossman, A.D., Wright, A. and Losick, R. (1997) Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell. 88, 667-674.
50. Webb, C.D., Graumann, P.L., Kahana, J.A., Teleman, A.A., Silver, P.A. and Losick, R. (1998) Use of time-lapse microscopy to visualize rapid movement of the replication origin region of the chromosome during the cell cycle in Bacillus subtilis. Mol. Microbiol., 28, 883-892.
51. Weitao, T., Nordstrom, K. and Dasgupta, S. (1999) Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. Mol. Microbiol., 34, 157-168.
52. Woldringh, C.L. (2002) The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol. Microbiol., 45, 17-29.
53. Woldringh, C.L., Zaritsky, A. and Grover, N.B. (1994) Nucleoid partitioning and the division plane in Escherichia coli. J. Bacteriol., 176, 6030-6038.
54. Wu, L.J. and Errington, J. (2002) A large dispersed chromosomal region required for chromosome segregation in sporulating cells of Bacillus subtilis. EMBO J., 21, 4001-4011.
55. Yamaichi, Y. and Niki, H. (2000) Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc. Natl Acad. Sci. USA, 97, 14656-14661.