Condensin confers the longitudinal rigidity of chromosomes

Nature Cell Biology

Volumn 17, Issue 6, 2015, Pages 771-781

  Houlard, Martin ^a   Godwin, Jonathan ^a   Metson, Jean ^a   Lee, Jibak ^b   Hirano, Tatsuya ^c   Nasmyth, Kim ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KOBE UNIVERSITY   (Japan)

^c RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; CONDENSIN; CONDENSIN I; CONDENSIN II; MESSENGER RNA; PROTEINASE; TEV PROTEASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; NCAPH2 PROTEIN, MOUSE; NONHISTONE PROTEIN; NUCLEAR PROTEIN;

ALLELE; ANIMAL CELL; ARTICLE; CELL DIVISION; CHROMATIN; CHROMOSOME BIVALENT; CHROMOSOME LONGITUDINAL RIGIDITY; CHROMOSOME STRUCTURE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONTROLLED STUDY; FEMALE; GERMINAL VESICLE BREAKDOWN; IN VITRO STUDY; MEIOSIS; METAPHASE; MOUSE; MUTANT; NONHUMAN; OOCYTE; POLAR BODY EXTRUSION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SISTER CHROMATID DISENTANGLEMENT; THREAD FORMATION; WILD TYPE; ANIMAL; CHROMATID; CHROMOSOME; CHROMOSOME SEGREGATION; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

TOBACCO ETCH VIRUS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CHROMOSOMES; DNA-BINDING PROTEINS; MEIOSIS; MICE; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; OOCYTES;

EID: 84930168665     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3167     Document Type: Article

References (44)

1. Cremer, T., Tesin, D., Hopman, A. H. & Manuelidis, L. Rapid interphase and metaphase assessment of specific chromosomal changes in neuroectodermal tumor cells by in situ hybridization with chemically modified DNA probes. Exp. Cell Res. 176, 199-220 (1988)
2. Flemming, W. Beitrage zur Kenntnisseder Zelle undIhreer Lebenserscheinungen. Archiv f. mikrosk. Anatomie. 18, 151-259 (1880)
3. Nasmyth, K. Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565 (2002)
4. Nasmyth, K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745 (2001)
5. Schleiffer, A. et al. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol. Cell 11, 571-575 (2003)
6. Hirano, T. & Mitchison, T. J. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79, 449-458 (1994)
7. Hirano, T., Kobayashi, R. & Hirano, M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89, 511-521 (1997)
8. Ono, T. et al. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115, 109-121 (2003)
9. Saka, Y. et al. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J. 13, 4938-4952 (1994)
10. Sutani, T. et al. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev. 13, 2271-2283 (1999)
11. Strunnikov, A. V., Hogan, E. & Koshland, D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev. 9, 587-599 (1995)
12. Lavoie, B. D., Tuffo, K. M., Oh, S., Koshland, D. & Holm, C. Mitotic chromosome condensation requires Brn1p, the yeast homologue of Barren. Mol. Biol. Cell 11, 1293-1304 (2000)
13. Bhalla, N., Biggins, S. & Murray, A. W. Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior. Mol. Biol. Cell 13, 632-645 (2002)
14. Lieb, J. D., Albrecht, M. R., Chuang, P. T. & Meyer, B. J. MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 92, 265-277 (1998)
15. Hagstrom, K. A., Holmes, V. F., Cozzarelli, N. R. & Meyer, B. J. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 16, 729-742 (2002)
16. Bhat, M. A., Philp, A. V., Glover, D. M. & Bellen, H. J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 87, 1103-1114 (1996)
17. Steffensen, S. et al. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr. Biol. 11, 295-307 (2001)
18. Hudson, D. F., Vagnarelli, P., Gassmann, R. & Earnshaw, W. C. Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev. Cell 5, 323-336 (2003)
19. Vagnarelli, P. et al. Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 8, 1133-1142 (2006)
20. Gerlich, D., Hirota, T., Koch, B., Peters, J. M. & Ellenberg, J. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr. Biol. 16, 333-344 (2006)
21. Ribeiro, S. A. et al. Condensin regulates the stiffness of vertebrate centromeres. Mol. Biol. Cell 20, 2371-2380 (2009)
22. Oliveira, R. A., Coelho, P. A. & Sunkel, C. E. The condensin I subunit Barren/CAP-H is essential for the structural integrity of centromeric heterochromatin during mitosis. Mol. Cell Biol. 25, 8971-8984 (2005)
23. Poirier, M. G. & Marko, J. F. Micromechanical studies of mitotic chromosomes. Curr. Top Dev. Biol. 55, 75-141 (2003)
24. Almagro, S., Riveline, D., Hirano, T., Houchmandzadeh, B. & Dimitrov, S. The mitotic chromosome is an assembly of rigid elastic axes organized by structural maintenance of chromosomes (SMC) proteins and surrounded by a soft chromatin envelope. J. Biol. Chem. 279, 5118-5126 (2004)
25. Nicklas, R. B. How cells get the right chromosomes. Science 275, 632-637 (1997)
26. Lan, Z. J., Xu, X. & Cooney, A. J. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol. Reprod. 71, 1469-1474 (2004)
27. Sironi, L. et al. Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J. 20, 6371-6382 (2001)
28. Miyanari, Y., Ziegler-Birling, C. & Torres-Padilla, M. E. Live visualization of chromatin dynamics with fluorescent TALEs. Nat. Struct. Mol. Biol. 20, 1321-1324 (2013)
29. Lee, J., Ogushi, S., Saitou, M. & Hirano, T. Condensins I and II are essential for construction of bivalent chromosomes in mouse oocytes. Mol. Biol. Cell 22, 3465-3477 (2011)
30. Tachibana-Konwalski, K. et al. Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev. 24, 2505-2516 (2010)
31. Wassmann, K., Niault, T. & Maro, B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 13, 1596-1608 (2003)
32. Hirota, T., Gerlich, D., Koch, B., Ellenberg, J. & Peters, J. M. Distinct functions of condensin I and II in mitotic chromosome assembly. J. Cell Sci. 117, 6435-6445 (2004)
33. Renshaw, M. J. et al. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev. Cell 19, 232-244 (2010)
34. Charbin, A., Bouchoux, C. & Uhlmann, F. Condensin aids sister chromatid decatenation by topoisomerase II. Nucleic Acids Res. 42, 340-348 (2014)
35. Poirier, M., Eroglu, S., Chatenay, D. & Marko, J. F. Reversible and irreversible unfolding of mitotic newt chromosomes by applied force. Mol. Biol. Cell 11, 269-276 (2000)
36. Cuylen, S., Metz, J. & Haering, C. H. Condensin structures chromosomal DNA through topological links. Nat. Struct. Mol. Biol. 18, 894-901 (2011)
37. Shintomi, K. & Hirano, T. The relative ratio of condensin I to II determines chromosome shapes. Genes Dev. 25, 1464-1469 (2011)
38. Fujiwara, T., Tanaka, K., Kuroiwa, T. & Hirano, T. Spatiotemporal dynamics of condensins I and II: evolutionary insights from the primitive red alga Cyanidioschyzon merolae. Mol. Biol. Cell 24, 2515-2527 (2013)
39. Burmann, F. et al. An asymmetric SMC-kleisin bridge in prokaryotic condensin. Nat. Struct. Mol. Biol. 20, 371-379 (2013)
40. Cuylen, S., Metz, J., Hruby, A. & Haering, C. H. Entrapment of chromosomes by condensin rings prevents their breakage during cytokinesis. Dev. Cell 27, 469-478 (2013)
41. Oliveira, R. A., Hamilton, R. S., Pauli, A., Davis, I. & Nasmyth, K. Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat. Cell Biol. 12, 185-192 (2010)
42. Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R. Manipulating the Mouse Embryo A Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory Press, 2003)
43. Kitajima, T. S., Ohsugi, M. & Ellenberg, J. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146, 568-581 (2011)
44. Rattani, A. et al. Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. eLife 2, e01133 (2013).