A pathway for mitotic chromosome formation

被引:481
作者
Gibcus, Johan H. [1 ]
Samejima, Kumiko [2 ]
Goloborodko, Anton [3 ,4 ]
Samejima, Itaru [2 ]
Naumova, Natalia [1 ]
Nuebler, Johannes [3 ,4 ]
Kanemaki, Masato T. [5 ,6 ]
Xie, Linfeng [7 ]
Paulson, James R. [7 ]
Earnshaw, William C. [2 ]
Mirny, Leonid A. [3 ,4 ]
Dekker, Job [1 ,8 ]
机构
[1] Univ Massachusetts, Dept Biochem & Mol Pharmacol, Program Syst Biol, Med Sch, 368 Plantation St, Worcester, MA 01605 USA
[2] Univ Edinburgh, Wellcome Ctr Cell Biol, Kings Bldg, Edinburgh EH9 3BF, Midlothian, Scotland
[3] MIT, Inst Med Engn & Sci, 77 Massachusetts Ave, Cambridge, MA 02139 USA
[4] MIT, Dept Phys, Cambridge, MA 02139 USA
[5] Res Org Informat & Syst, Div Mol Cell Engn, Natl Inst Genet, Yata 1111, Mishima, Shizuoka 4118540, Japan
[6] SOKENDAI, Dept Genet, Mishima, Shizuoka 4118540, Japan
[7] Univ Wisconsin, Dept Chem, 800 Algoma Blvd, Oshkosh, WI 54901 USA
[8] Univ Massachusetts, Howard Hughes Med Inst, Med Sch, 368 Plantation St, Worcester, MA 01605 USA
基金
日本学术振兴会; 英国惠康基金; 美国国家科学基金会;
关键词
SISTER-CHROMATID RESOLUTION; CONDENSIN-I; METAPHASE CHROMOSOMES; VERTEBRATE CELLS; TOPOISOMERASE-II; SCAFFOLD ATTACHMENT; CHROMOKINESIN KIF4A; MAMMALIAN-CELLS; LOOP EXTRUSION; HUMAN GENOME;
D O I
10.1126/science.aao6135
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Mitotic chromosomes fold as compact arrays of chromatin loops. To identify the pathway of mitotic chromosome formation, we combined imaging and Hi-C analysis of synchronous DT40 cell cultures with polymer simulations. Here we show that in prophase, the interphase organization is rapidly lost in a condensin-dependent manner, and arrays of consecutive 60-kilobase (kb) loops are formed. During prometaphase, similar to 80-kb inner loops are nested within similar to 400-kb outer loops. The loop array acquires a helical arrangement with consecutive loops emanating from a central "spiral staircase" condensin scaffold. The size of helical turns progressively increases to similar to 12 megabases during prometaphase. Acute depletion of condensin I or II shows that nested loops form by differential action of the two condensins, whereas condensin II is required for helical winding.
引用
收藏
页码:652 / +
页数:13
相关论文
共 84 条
[71]   Two independent modes of chromatin organization revealed by cohesin removal [J].
Schwarzer, Wibke ;
Abdennur, Nezar ;
Goloborodko, Anton ;
Pekowska, Aleksandra ;
Fudenberg, Geoffrey ;
Loe-Mie, Yann ;
Fonseca, Nuno A. ;
Huber, Wolfgang ;
Haering, Christian H. ;
Mirny, Leonid ;
Spitz, Francois .
NATURE, 2017, 551 (7678) :51-+
[72]   Mitotic chromosome assembly despite nucleosome depletion in Xenopus egg extracts [J].
Shintomi, Keishi ;
Inoue, Fukashi ;
Watanabe, Hiroshi ;
Ohsumi, Keita ;
Ohsugi, Miho ;
Hirano, Tatsuya .
SCIENCE, 2017, 356 (6344) :1284-1287
[73]   The relative ratio of condensin I to II determines chromosome shapes [J].
Shintomi, Keishi ;
Hirano, Tatsuya .
GENES & DEVELOPMENT, 2011, 25 (14) :1464-1469
[74]   Homologous DNA recombination in vertebrate cells [J].
Sonoda, E ;
Takata, M ;
Yamashita, YM ;
Morrison, C ;
Takeda, S .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2001, 98 (15) :8388-8394
[75]   Engineered chromosome regions with altered sequence composition demonstrate hierarchical large-scale folding within metaphase chromosomes [J].
Strukov, YG ;
Wang, Y ;
Belmont, AS .
JOURNAL OF CELL BIOLOGY, 2003, 162 (01) :23-35
[76]   Condensin I-mediated mitotic chromosome assembly requires association with chromokinesin KIF4A [J].
Takahashi, Motoko ;
Wakai, Toshifumi ;
Hirota, Toru .
GENES & DEVELOPMENT, 2016, 30 (17) :1931-1936
[77]   The condensin complex is a mechanochemical motor that translocates along DNA [J].
Terakawa, Tsuyoshi ;
Bisht, Shveta ;
Eeftens, Jorine M. ;
Dekker, Cees ;
Haering, Christian H. ;
Greene, Eric C. .
SCIENCE, 2017, 358 (6363) :672-676
[78]   Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase [J].
Waizenegger, IC ;
Hauf, S ;
Meinke, A ;
Peters, JM .
CELL, 2000, 103 (03) :399-410
[79]   A Cascade of Histone Modifications Induces Chromatin Condensation in Mitosis [J].
Wilkins, Bryan J. ;
Rall, Nils A. ;
Ostwal, Yogesh ;
Kruitwagen, Tom ;
Hiragami-Hamada, Kyoko ;
Winkler, Marco ;
Barral, Yves ;
Fischle, Wolfgang ;
Neumann, Heinz .
SCIENCE, 2014, 343 (6166) :77-80
[80]   THE HIGHER-ORDER STRUCTURE OF CHROMATIN - EVIDENCE FOR A HELICAL RIBBON ARRANGEMENT [J].
WOODCOCK, CLF ;
FRADO, LLY ;
RATTNER, JB .
JOURNAL OF CELL BIOLOGY, 1984, 99 (01) :42-52