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Volume 151, Issue 11

Genetic interaction of the SMC complex with topoisomerase IV in Free

Abstract

The role of topoisomerase IV (Topo IV) and of the structural maintenance of chromosomes (SMC) complex in chromosome compaction and in global protein synthesis was investigated. Lowering of the levels of Topo IV led to chromosome decondensation, while overproduction induced chromosome hyper-compaction, showing that Topo IV has an influence on the compaction of the whole chromosome, in a manner similar to that of the SMC protein, though different in mechanism. Increased synthesis of Topo IV in -deleted cells partially rescued the growth and condensation defect of the deletion, but not the segregation defect, revealing that the two systems interact at a genetic level. Two-dimensional gel investigations showed that global protein synthesis is highly aberrant in -deleted cells, and, to a different extent, also in cells lacking ScpA or ScpB, which form the SMC complex together with SMC protein. Overproduction of Topo IV partially rescued the defect in protein synthesis in mutant cells, indicating that Topo IV can restore the loss of negative supercoiling caused by the absence of SMC protein, but does not fully rescue the segregation defect. The data also show that the SMC protein has a dual function, in chromosome supercoiling and in active segregation.

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Keyword(s): 2D, two-dimensional , SMC, structural maintenance of chromosomes , Topo I, topoisomerase I , Topo III, topoisomerase III and Topo IV, topoisomerase IV
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2005-11-01
2024-04-20
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References

  1. Chuang P. T., Albertson D. G., Meyer B. J. 1994; DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79:459–474 [CrossRef]
     [Google Scholar]
  2. Dervyn E., Noirot-Gros M. F., Mervelet P., McGovern S., Ehrlich S. D., Polard P., Noirot P. 2004; The bacterial condensin/cohesin-like protein complex acts in DNA repair and regulation of gene expression. Mol Microbiol 51:1629–1640 [CrossRef]
     [Google Scholar]
  3. Espeli O., Marians K. J. 2004; Untangling intracellular DNA topology. Mol Microbiol 52:925–931 [CrossRef]
     [Google Scholar]
  4. Espeli O., Levine C., Hassing H., Marians K. J. 2003; Temporal regulation of topoisomerase IV activity in E. coli . Mol Cell 11:189–201 [CrossRef]
     [Google Scholar]
  5. Eymann C., Dreisbach A., Albrecht D. 10 other authors 2004; A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4:2849–2876 [CrossRef]
     [Google Scholar]
  6. Graumann P. L. 2000; Bacillus subtilis SMC is required for proper arrangement of the chromosome and for efficient segregation of replication termini but not for bipolar movement of newly duplicated origin regions. J Bacteriol 182:6463–6471 [CrossRef]
     [Google Scholar]
  7. Graumann P., Schroder K., Schmid R., Marahiel M. A. 1996; Cold shock stress-induced proteins in Bacillus subtilis . J Bacteriol 178:4611–4619
     [Google Scholar]
  8. Gruber S., Haering C. H., Nasmyth K. 2003; Chromosomal cohesin forms a ring. Cell 112:765–777 [CrossRef]
     [Google Scholar]
  9. Hirano T. 2002; The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev 16:399–414 [CrossRef]
     [Google Scholar]
  10. Jaacks K. J., Healy J., Losick R., Grossman A. D. 1989; Identification and characterization of genes controlled by the sporulation regulatory gene spo0H in Bacillus subtilis . J Bacteriol 171:4121–4129
     [Google Scholar]
  11. Kato J., Nishimura Y., Imamura R., Niki H., Hiraga S., Suzuki H. 1990; New topoisomerase essential for chromosome segregation in E. coli . Cell 63:393–404 [CrossRef]
     [Google Scholar]
  12. Kimura K., Rybenkov V. V., Crisona N. J., Hirano T., Cozzarelli N. R. 1999; 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98:239–248 [CrossRef]
     [Google Scholar]
  13. Klein J., Harding G., Klein E. 2002; A new isoelectric focusing gel for two-dimensional electrophoresis constructed in microporous hollow fiber membranes. J Proteome Res 1:41–45 [CrossRef]
     [Google Scholar]
  14. Lemon K. P., Grossman A. D. 2000; Movement of replicating DNA through a stationary replisome. Mol Cell 6:1321–1330 [CrossRef]
     [Google Scholar]
  15. Lindow J. C., Britton R. A., Grossman A. D. 2002a; Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo . J Bacteriol 184:5317–5322 [CrossRef]
     [Google Scholar]
  16. Lindow J. C., Kuwano M., Moriya S., Grossman A. D. 2002b; Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol Microbiol 46:997–1009 [CrossRef]
     [Google Scholar]
  17. Mascarenhas J., Soppa J., Strunnikov A., Grauman P. L. 2002; Cell cycle dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21:3108–3118 [CrossRef]
     [Google Scholar]
  18. Mascarenhas J., Volkov A. V., Rinn C., Schiener J., Guckenberger R., Graumann P. L. 2005; Dynamic assembly, localization and proteolysis of the Bacillus subtilis SMC complex. BMC Cell Biology 6:28 http://www.biomedcentral.com/1471-2121/6/28 [CrossRef]
     [Google Scholar]
  19. Quisel J. D., Burkholder W. F., Grossman A. D. 2001; In vivo effects of sporulation kinases on mutant Spo0A proteins in Bacillus subtilis . J Bacteriol 183:6573–6578 [CrossRef]
     [Google Scholar]
  20. Sawitzke J. A., Austin S. 2000; Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc Natl Acad Sci U S A 97:1671–1676 [CrossRef]
     [Google Scholar]
  21. Soppa J., Kobayashi K., Noirot-Gros M. F., Oesterhelt D., Ehrlich S. D., Dervyn E., Ogasawara N., Moriya S. 2002; Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB. Mol Microbiol 45:59–71 [CrossRef]
     [Google Scholar]
  22. Volkov A., Mascarenhas J., Andrei-Selmer C., Ulrich H. D., Graumann P. L. 2003; A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid and binds to DNA as a ring-like structure. Mol Cell Biol 23:5638–5650 [CrossRef]
     [Google Scholar]
  23. Zechiedrich E. L., Khodursky A. B., Bachellier S., Schneider R., Chen D., Lilley D. M., Cozzarelli N. R. 2000; Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli . J Biol Chem 275:8103–8113 [CrossRef]
     [Google Scholar]
  24. Zhu Q., Pongpech P., DiGate R. J. 2001; Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli . Proc Natl Acad Sci U S A 98:9766–9771 [CrossRef]
     [Google Scholar]
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Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis
Microbiology 151, 3729 (2005); https://doi.org/10.1099/mic.0.28234-0
/content/journal/micro/10.1099/mic.0.28234-0
/content/journal/micro/10.1099/mic.0.28234-0
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