Entrapment of Chromosomes by Condensin Rings Prevents Their Breakage during Cytokinesis

被引:34
作者
Cuyien, Sara [1 ,2 ]
Metz, Jutta [1 ,2 ]
Hruby, Andrea [1 ,2 ]
Haering, Christian H. [1 ,2 ]
机构
[1] European Mol Biol Lab, Cell Biol & Biophys Unit, D-69117 Heidelberg, Germany
[2] European Mol Biol Lab, Struct & Computat Biol Unit, D-69117 Heidelberg, Germany
关键词
SISTER-CHROMATID SEPARATION; SACCHAROMYCES-CEREVISIAE; BUDDING YEAST; DNA-DAMAGE; NUCLEAR DIVISION; TOPOISOMERASE-II; CHECKPOINT; SEGREGATION; COHESIN; ANAPHASE;
D O I
10.1016/j.devcel.2013.10.018
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Successful segregation of chromosomes during mitosis and meiosis depends on the action of the ring-shaped condensin complex, but how condensin ensures the complete disjunction of sister chromatids is unknown. We show that the failure to segregate chromosome arms, which results from condensin release from chromosomes by proteolytic cleavage of its ring structure, leads to a DNA damage checkpoint-dependent cell-cycle arrest. Checkpoint activation is triggered by the formation of chromosome breaks during cytokinesis, which proceeds with normal timing despite the presence of lagging chromosome arms. Remarkably, enforcing condensin ring reclosure by chemically induced dimerization just before entry into anaphase is sufficient to restore chromosome arm segregation. We suggest that topological entrapment of chromosome arms by condensin rings ensures their clearance from the cleavage plane and thereby avoids their breakage during cytokinesis.
引用
收藏
页码:469 / 478
页数:10
相关论文
共 38 条
[1]   RELATIONSHIP OF ACTIN AND TUBULIN DISTRIBUTION TO BUD GROWTH IN WILD-TYPE AND MORPHOGENETIC-MUTANT SACCHAROMYCES-CEREVISIAE [J].
ADAMS, AEM ;
PRINGLE, JR .
JOURNAL OF CELL BIOLOGY, 1984, 98 (03) :934-945
[2]   Differential regulation of the cellular response to DNA double-strand breaks in G1 [J].
Barlow, Jacqueline H. ;
Lisby, Michael ;
Rothstein, Rodney .
MOLECULAR CELL, 2008, 30 (01) :73-85
[3]   Positive Supercoiling of Mitotic DNA Drives Decatenation by Topoisomerase II in Eukaryotes [J].
Baxter, J. ;
Sen, N. ;
Lopez Martinez, V. ;
Monturus De Carandini, M. E. ;
Schvartzman, J. B. ;
Diffley, J. F. X. ;
Aragon, L. .
SCIENCE, 2011, 331 (6022) :1328-1332
[4]   Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast [J].
Baxter, Jonathan ;
Diffley, John F. X. .
MOLECULAR CELL, 2008, 30 (06) :790-802
[5]   Condensin and the Spindle Midzone Prevent Cytokinesis Failure Induced by Chromatin Bridges in C. elegans Embryos [J].
Bembenek, Joshua N. ;
Verbrugghe, Koen J. C. ;
Khanikar, Jayshree ;
Csankovszki, Gyoergyi ;
Chan, Raymond C. .
CURRENT BIOLOGY, 2013, 23 (11) :937-946
[6]   Condensins Promote Coorientation of Sister Chromatids During Meiosis I in Budding Yeast [J].
Brito, Ilana L. ;
Yu, Hong-Guo ;
Amon, Angelika .
GENETICS, 2010, 185 (01) :55-U104
[7]   Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p [J].
Chuang, JS ;
Schekman, RW .
JOURNAL OF CELL BIOLOGY, 1996, 135 (03) :597-610
[8]   Deciphering condensin action during chromosome segregation [J].
Cuylen, Sara ;
Haering, Christian H. .
TRENDS IN CELL BIOLOGY, 2011, 21 (09) :552-559
[9]   Condensin structures chromosomal DNA through topological links [J].
Cuylen, Sara ;
Metz, Jutta ;
Haering, Christian H. .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2011, 18 (08) :894-U52
[10]   Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation [J].
D'Ambrosio, Claudio ;
Kelly, Gavin ;
Shirahige, Katsuhiko ;
Uhlmann, Frank .
CURRENT BIOLOGY, 2008, 18 (14) :1084-1089