Actin Homolog MreB Affects Chromosome Segregation by Regulating Topoisomerase IV in Escherichia coli

Molecular Cell

Volumn 33, Issue 2, 2009, Pages 171-180

  Madabhushi, Ram ^a   Marians, Kenneth J ^a,b  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

CELLCYCLE; DNA; PROTEINS

Indexed keywords

ACTIN; DNA TOPOISOMERASE IV; MREB PROTEIN; PROTEIN PARC;

ARTICLE; BACTERIAL STRAIN; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY;

ACTINS; BINDING SITES; CELL CYCLE; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; CYTOSKELETON; DNA TOPOISOMERASE IV; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, BIOLOGICAL; MUTATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 58649111971     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.01.001     Document Type: Article

References (40)

1. Adams D.E., Shekhtman E.M., Zechiedrich E.L., Schmid M.B., and Cozzarelli N.R. The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell 71 (1992) 277-288
2. Bean G.J., and Amann K.J. Polymerization properties of the Thermotoga maritima actin MreB: roles of temperature, nucleotides, and ions. Biochemistry 47 (2008) 826-835
3. Carballido-Lopez R. The bacterial actin-like cytoskeleton. Microbiol. Mol. Biol. Rev. 70 (2006) 888-909
4. Carballido-Lopez R., and Errington J. A dynamic bacterial cytoskeleton. Trends Cell Biol. 13 (2003) 577-583
5. Chen J., Rauch C.A., White J.H., Englund P.T., and Cozzarelli N.R. The topology of the kinetoplast DNA network. Cell 80 (1995) 61-69
6. Cooper J.A., and Pollard T.D. Methods to measure actin polymerization. Methods Enzymol. 85 (1982) 182-210
7. Espeli O., and Marians K.J. Untangling intracellular DNA topology. Mol. Microbiol. 52 (2004) 925-931
8. Espeli O., Levine C., Hassing H., and Marians K.J. Temporal regulation of topoisomerase IV activity in E. coli. Mol. Cell 11 (2003) 189-201
9. Espeli O., Nurse P., Levine C., Lee C., and Marians K.J. SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli. Mol. Microbiol. 50 (2003) 495-509
10. Esue O., Cordero M., Wirtz D., and Tseng Y. The assembly of MreB, a prokaryotic homolog of actin. J. Biol. Chem. 280 (2005) 2628-2635
11. Figge R.M., Divakaruni A.V., and Gober J.W. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51 (2004) 1321-1332
12. Gitai Z., Dye N., and Shapiro L. An actin-like gene can determine cell polarity in bacteria. Proc. Natl. Acad. Sci. USA 101 (2004) 8643-8648
13. Gitai Z., Dye N.A., Reisenauer A., Wachi M., and Shapiro L. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120 (2005) 329-341
14. Hojgaard A., Szerlong H., Tabor C., and Kuempel P. Norfloxacin-induced DNA cleavage occurs at the dif resolvase locus in Escherichia coli and is the result of interaction with topoisomerase IV. Mol. Microbiol. 33 (1999) 1027-1036
15. Karczmarek A., Martinez-Arteaga R., Alexeeva S., Hansen F.G., Vicente M., Nanninga N., and den Blaauwen T. DNA and origin region segregation are not affected by the transition from rod to sphere after inhibition of Escherichia coli MreB by A22. Mol. Microbiol. 65 (2007) 51-63
16. Kato J., Nishimura Y., Yamada M., Suzuki H., and Hirota Y. Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli. J. Bacteriol. 170 (1988) 3967-3977
17. Kato J., Nishimura Y., Imamura R., Niki H., Hiraga S., and Suzuki H. New topoisomerase essential for chromosome segregation in E. coli. Cell 63 (1990) 393-404
18. Kruse T., and Gerdes K. Bacterial DNA segregation by the actin-like MreB protein. Trends Cell Biol. 15 (2005) 343-345
19. Kruse T., Moller-Jensen J., Lobner-Olesen A., and Gerdes K. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22 (2003) 5283-5292
20. Kruse T., Bork-Jensen J., and Gerdes K. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol. Microbiol. 55 (2005) 78-89
21. Kruse T., Blagoev B., Lobner-Olesen A., Wachi M., Sasaki K., Iwai N., Mann M., and Gerdes K. Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev. 20 (2006) 113-124
22. Lew D.J., Weinert T., and Pringle J.R. Cell cycle control in Saccharomyces cerevisiae. In: Pringle J.R., Broach J.R., and Jones E.W. (Eds). The Molecular and Cellular Biology of the Yeast Saccharomyces (1997), Cold Spring Harbor Laboratory Press, Plainview, N.Y. 607-695
23. Maiato H., Sampaio P., and Sunkel C.E. Microtubule-associated proteins and their essential roles during mitosis. Int. Rev. Cytol. 241 (2004) 53-153
24. Miller K.G., Liu L.F., and Englund P.T. A homogeneous type II DNA topoisomerase from HeLa cell nuclei. J. Biol. Chem. 256 (1981) 9334-9339
25. Mohammadi T., Karczmarek A., Crouvoisier M., Bouhss A., Mengin-Lecreulx D., and den Blaauwen T. The essential peptidoglycan glycosyltransferase MurG forms a complex with proteins involved in lateral envelope growth as well as with proteins involved in cell division in Escherichia coli. Mol. Microbiol. 65 (2007) 1106-1121
26. Mossessova E., Levine C., Peng H., Nurse P., Bahng S., and Marians K.J. Mutational analysis of Escherichia coli topoisomerase IV. I. Selection of dominant-negative parE alleles. J. Biol. Chem. 275 (2000) 4099-4103
27. Nurse P., Bahng S., Mossessova E., and Marians K.J. Mutational analysis of Escherichia coli topoisomerase IV. II. ATPase negative mutants of parE induce hyper-DNA cleavage. J. Biol. Chem. 275 (2000) 4104-4111
28. Nurse P., Levine C., Hassing H., and Marians K.J. Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J. Biol. Chem. 278 (2003) 8653-8660
29. Peng H., and Marians K.J. Decatenation activity of topoisomerase IV during oriC and pBR322 DNA replication in vitro. Proc. Natl. Acad. Sci. USA 90 (1993) 8571-8575
30. Sawitzke J.A., and Austin S. Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc. Natl. Acad. Sci. USA 97 (2000) 1671-1676
31. Sherratt D.J., Lau I.F., and Barre F.X. Chromosome segregation. Curr. Opin. Microbiol. 4 (2001) 653-659
32. Slovak P.M., Wadhams G.H., and Armitage J.P. Localization of MreB in Rhodobacter sphaeroides under conditions causing changes in cell shape and membrane structure. J. Bacteriol. 187 (2005) 54-64
33. Soufo H.J., and Graumann P.L. Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr. Biol. 13 (2003) 1916-1920
34. Steck T.R., and Drlica K. Bacterial chromosome segregation: evidence for DNA gyrase involvement in decatenation. Cell 36 (1984) 1081-1088
35. Stone M.D., Bryant Z., Crisona N.J., Smith S.B., Vologodskii A., Bustamante C., and Cozzarelli N.R. Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl. Acad. Sci. USA 100 (2003) 8654-8659
36. van den Ent F., Amos L.A., and Lowe J. Prokaryotic origin of the actin cytoskeleton. Nature 413 (2001) 39-44
37. Vats P., and Rothfield L. Duplication and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. Proc. Natl. Acad. Sci. USA 104 (2007) 17795-17800
38. Wang S.C., and Shapiro L. The topoisomerase IV ParC subunit colocalizes with the Caulobacter replisome and is required for polar localization of replication origins. Proc. Natl. Acad. Sci. USA 101 (2004) 9251-9256
39. Zechiedrich E.L., Khodursky A.B., Bachellier S., Schneider R., Chen D., Lilley D.M., and Cozzarelli N.R. Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J. Biol. Chem. 275 (2000) 8103-8113
40. Zimmerman S.B., and Murphy L.D. Release of compact nucleoids with characteristic shapes from Escherichia coli. J. Bacteriol. 183 (2001) 5041-5049