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

Molecular and Cellular Biology

Volumn 23, Issue 16, 2003, Pages 5638-5650

  Volkov, A ^a   Mascarenhas, J ^a   Andrei Selmer, C ^a   Ulrich, H D ^b   Graumann, P L ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA;

ANIMAL CELL; ARTICLE; BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; CHROMOSOME CONDENSATION; COMPLEX FORMATION; DNA BINDING; DNA RECOMBINATION; DNA STRUCTURE; GENETIC ORGANIZATION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATE; ADHESINS, BACTERIAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; CENTRIFUGATION, DENSITY GRADIENT; CHROMATOGRAPHY, GEL; CHROMOSOMES; DNA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; ETHIDIUM; GENOTYPE; MASS SPECTROMETRY; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SUCROSE; SURFACE PLASMON RESONANCE;

ANIMALIA; BACILLUS SUBTILIS; PROKARYOTA;

EID: 0042132009     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.16.5638-5650.2003     Document Type: Article

References (46)

1. Akhmedov, A. T., C. Frei, M. Tsai-Pflugfelder, B. Kemper, S. M. Gasser, and R. Jessberger. 1998. Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure. J. Biol. Chem. 273:24088-24094.
2. Anderson, D. E., A. Losada, H. P. Erickson, and T. Hirano. 2002. Condensin and cohesin display different arm conformations with characteristic hinge angles. J. Cell Biol. 156:419-424.
3. Bazett-Jones, D. P., K. Kimura, and T. Hirano. 2002. Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol. Cell 9:1183-1190.
4. Britton, R. A., D. C. Lin, and A. D. Grossman. 1998. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev. 12:1254-1259.
5. den Blaauwen, T., A. Lindqvist, J. Lowe, and N. Nanninga. 2001. Distribution of the Escherichia coli structural maintenance of chromosomes (SMC)-like protein MukB in the cell. Mol. Microbiol. 42:1179-1188.
6. Glaser, P., M. E. Sharpe, B. Raether, M. Perego, K. Ohlsen, and J. Errington. 1997. Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning, Genes Dev. 11:1160-1168.
7. Gordon, S., D. Sitnikov, C. D. Webb, A. Teleman, 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.
8. 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.
9. Graumann, P. L. 2001. SMC proteins in bacteria: condensation motors for chromosome segregation? Biochimie 83:53-60.
10. Graumann, P. L., R. Losick, and A. V. Strunnikov. 1998. Subcellular localization of Bacillus subtilis SMC, a protein involved in chromosome condensation and segregation. J. Bacteriol. 180:5749-5755.
11. Haering, C. H., J. Lowe, A. Hochwagen, and K. Nasmyth. 2002. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9:773-788.
12. Harvey, S. H., M. J. Krien, and M. J. O'Connell. 2002. Structural maintenance of chromosomes (SMC) proteins, a family of conserved ATPases Genome Biol. 3:REVIEWS3003.
13. Hirano, M., D. E. Anderson, H. P. Erickson, and T. Hirano. 2001. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J. 20:3238-3250.
14. Hirano, M., and T. Hirano. 1998. ATP-dependent aggregation of single-stranded DNA by a bacterial SMC homodimer. EMBO J. 17:7139-7148.
15. Hirano, T. 1999. SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates? Genes Dev. 13:11-19.
16. Hirano, T., R. Kobayashi, and M. Hirano. 1997. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89:511-521.
17. Hopfner, K. P., L. Craig, G. Moncalian, R. A. Zinkel, T. Usui, B. A. Owen, A. Karcher, B. Henderson, J. L. Bodmer, C. T. McMurray, J. P. Carney, J. H. Petrini, and J. A. Tainer. 2002. The Rad50 zinc-hook is a structure joining Mrell complexes in DNA recombination and repair. Nature 418:562-566.
18. Hopfner, K. P., A. Karcher, D. S. Shin, L. Craig, L. M. Arthur, J. P. Carney, and J. A. Tainer. 2000. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789-800.
19. Jaacks, K. J., J. Healy, R. Losick, and A. D. Grossman. 1989. Identification and characterization of genes controlled by the sporulation regulatory gene spoOH in Bacillus subtilis. J. Bacteriol. 171:4121-4129.
20. Kaltwasser, M., T. Wiegert, and W. Schumann. 2002. Construction and application of epitope- and green fluorescent protein-tagging integration vectors for Bacillus subtilis. Appl. Environ. Microbiol. 68:2624-2628.
21. Kimura, K., and T. Hirano. 2000. Dual roles of the 11S regulatory subcomplex in condensin functions. Proc. Natl. Acad. Sci. USA 97:11972-11977.
22. Klein, W., and M. A. Marahiel. 2002. Structure-function relationship and regulation of two Bacillus subtilis DNA-binding proteins, HBsu and AbrB. J. Mol. Microbiol. Biotechnol. 4:323-329.
23. Lemon, K. P., and A. D. Grossman. 2001. The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev. 15:2031-2041.
24. Lemon, K. P., and A. D. Grossman. 1998. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516-1519.
25. Lewis, P. J., and A. L. Marston. 1999. GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227:101-110.
26. Lindow, J. C., M. Kuwano, S. Moriya, and A. D. Grossman. 2002. Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol. Microbiol. 46:997-1009.
27. Lowe, J., S. C. Cordell, and F. van den Ent. 2001. Crystal structure of the SMC head domain: an AbC ATPase with 900 residues antiparallel coiled-coil inserted. J. Mol. Biol. 306:25-35.
28. Mascarenhas, J., J. Soppa, A. Strunnikov, and P. L. Grauman. 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.
29. Melby, T. E., C. N. Ciampaglio, G. Briscoe, and H. P. Erickson. 1998. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell Biol. 142:1595-1604.
30. Moriya, S., E. Tsujikawa, A. K. Hassan, K. Asai, T. Kodama, and N. Ogasawara. 1998. A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol. Microbiol. 29:179-187.
31. Muskhelishvili, G., and A. Travers. 2003. Transcription factor as a topological homeostat. Front. Biosci. 8:D279-D285.
32. Niki, H., A. Jaffe, R. Imamura, T. Ogura, and S. Hiraga. 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.
33. Niki, H., Y. Yamaichi, and S. Hiraga. 2000. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14:212-223.
34. Ohsumi, K., M. Yamazoe, and S. Hiraga. 2001. Different localization of SeqA-bound nascent DNA clusters and MukF-MukE-MukB complex in Escherichia coli cells. Mol. Microbiol. 40:835-845.
35. Quisel, J. D., W. F. Burkholder, and A. D. Grossman. 2001. In vivo effects of sporulation kinases on mutant Spo0A proteins in Bacillus subtilis. J. Bacteriol. 183:6573-6578.
36. Schleiffer, A., S. Kaitna, S. Maurer-Stroh, M. Glotzer, K. Nasmyth, and F. Eisenhaber. 2003. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol. Cell 11:571-575.
37. Soppa, J. 2001. Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins. Gene 278:253-264.
38. Soppa, J., K. Kobayashi, M. F. Noirot-Gros, D. Oesterhelt, S. D. Ehrlich, E. Dervyn, N. Ogasawara, and S. Moriya. 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.
39. Strunnikov, A. V., and R. Jessberger. 1999. Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions. Eur. J. Biochem. 263:6-13.
40. Sunako, Y., T. Onogi, and S. Hiraga. 2001. Sister chromosome cohesion of Escherichia coli. Mol. Microbiol. 42:1233-1242.
41. Teleman, A. A., P. L. Graumann, D. C. H. Lin, A. D. Grossman, and R. Losick. 1998. Chromosome arrangement within a bacterium. Curr. Biol. 8:1102-1109.
42. Webb, C. D., P. L. Graumann, J. Kahana, A. A. Teleman, P. Silver, and R. Losick. 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.
43. Webb, C. D., A. Teleman, S. Gordon, A. Straight, A. Belmont, D. C.-H. Lin, A. D. Grossman, A. Wright, and R. Losick. 1997. Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell 88:667-674.
44. 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.
45. Yamazoe, M., T. Onogi, Y. Sunako, H. Niki, K. Yamanaka, T. Ichimura, and S. Hiraga. 1999. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J. 18:5873-5884.
46. Yoshimura, S. H., K. Hizume, A. Murakami, T. Sutani, K. Takeyasu, and M. Yanagida. 2002. Condensin architecture and interaction with DNA: regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr. Biol. 12:508-513.