XB-ART-54823
Science
2018 Feb 09;3596376:. doi: 10.1126/science.aao6135.
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A pathway for mitotic chromosome formation.
Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N, Nuebler J, Kanemaki MT, Xie L, Paulson JR, Earnshaw WC, Mirny LA, Dekker J.
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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, ~80-kb inner loops are nested within ~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 ~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.
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R01 GM114190 NIGMS NIH HHS , R01 HG003143 NHGRI NIH HHS , Howard Hughes Medical Institute , U54 DK107980 NIDDK NIH HHS , Wellcome Trust , U54 CA193419 NCI NIH HHS , 107022 Wellcome Trust
Species referenced: Xenopus laevis
Genes referenced: cdk1
References [+] :
Abe,
The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II.
2011, Pubmed
Abe, The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. 2011, Pubmed
Adolph, Isolation of a protein scaffold from mitotic HeLa cell chromosomes. 1977, Pubmed
Alipour, Self-organization of domain structures by DNA-loop-extruding enzymes. 2012, Pubmed
Belmont, Large-scale chromatin structure and function. 1999, Pubmed
Belmont, A three-dimensional approach to mitotic chromosome structure: evidence for a complex hierarchical organization. 1987, Pubmed
Belton, Hi-C: a comprehensive technique to capture the conformation of genomes. 2012, Pubmed
Bishop, Design of allele-specific inhibitors to probe protein kinase signaling. 1998, Pubmed
Booth, 3D-CLEM Reveals that a Major Portion of Mitotic Chromosomes Is Not Chromatin. 2016, Pubmed
Boy de la Tour, The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness. 1988, Pubmed
Cockerill, Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. 1986, Pubmed
Cox, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. 2008, Pubmed
Craig, Chromosome bands--flavours to savour. 1993, Pubmed
Crane, Condensin-driven remodelling of X chromosome topology during dosage compensation. 2015, Pubmed
Dixon, Topological domains in mammalian genomes identified by analysis of chromatin interactions. 2012, Pubmed
Earnshaw, Architecture of metaphase chromosomes and chromosome scaffolds. 1983, Pubmed
Earnshaw, Localization of topoisomerase II in mitotic chromosomes. 1985, Pubmed
Eastman, Efficient nonbonded interactions for molecular dynamics on a graphics processing unit. 2010, Pubmed
Eastman, OpenMM 7: Rapid development of high performance algorithms for molecular dynamics. 2017, Pubmed
Eltsov, Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. 2008, Pubmed
Flyamer, Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. 2017, Pubmed
Fudenberg, Formation of Chromosomal Domains by Loop Extrusion. 2016, Pubmed
Gasser, The organisation of chromatin loops: characterization of a scaffold attachment site. 1986, Pubmed
Georgatos, Nuclear envelope breakdown in mammalian cells involves stepwise lamina disassembly and microtubule-drive deformation of the nuclear membrane. 1997, Pubmed
Gerlich, Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. 2006, Pubmed
Goloborodko, Chromosome Compaction by Active Loop Extrusion. 2016, Pubmed
Goloborodko, Compaction and segregation of sister chromatids via active loop extrusion. 2016, Pubmed
Green, Contrasting roles of condensin I and condensin II in mitotic chromosome formation. 2012, Pubmed
Hirota, Distinct functions of condensin I and II in mitotic chromosome assembly. 2004, Pubmed
Hochegger, An essential role for Cdk1 in S phase control is revealed via chemical genetics in vertebrate cells. 2007, Pubmed
Holland, Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. 2012, Pubmed
Hudson, Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. 2003, Pubmed
Imakaev, Iterative correction of Hi-C data reveals hallmarks of chromosome organization. 2012, Pubmed
Kim, Condensin I associates with structural and gene regulatory regions in vertebrate chromosomes. 2013, Pubmed
Kobe, Turn up the HEAT. 1999, Pubmed
Kustatscher, Chromatin enrichment for proteomics. 2014, Pubmed
Lajoie, The Hitchhiker's guide to Hi-C analysis: practical guidelines. 2015, Pubmed
Landt, ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. 2012, Pubmed
Liang, Chromosomes Progress to Metaphase in Multiple Discrete Steps via Global Compaction/Expansion Cycles. 2015, Pubmed
Lieberman-Aiden, Comprehensive mapping of long-range interactions reveals folding principles of the human genome. 2009, Pubmed
Losada, Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. 2002, Pubmed , Xenbase
Maeshima, A two-step scaffolding model for mitotic chromosome assembly. 2003, Pubmed
Maritan, Optimal shapes of compact strings. 2000, Pubmed
Marko, Polymer models of meiotic and mitotic chromosomes. 1997, Pubmed
Marsden, Metaphase chromosome structure: evidence for a radial loop model. 1979, Pubmed
Mazumdar, Human chromokinesin KIF4A functions in chromosome condensation and segregation. 2004, Pubmed
Mirkovitch, Scaffold attachment of DNA loops in metaphase chromosomes. 1988, Pubmed
Molnár, The genome of the chicken DT40 bursal lymphoma cell line. 2014, Pubmed
Moore, HCP-4, a CENP-C-like protein in Caenorhabditis elegans, is required for resolution of sister centromeres. 2001, Pubmed
Nagano, Cell-cycle dynamics of chromosomal organization at single-cell resolution. 2017, Pubmed
Nagasaka, Sister chromatid resolution is an intrinsic part of chromosome organization in prophase. 2016, Pubmed
Nasmyth, Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. 2001, Pubmed
Naumova, Organization of the mitotic chromosome. 2013, Pubmed
Nishimura, An auxin-based degron system for the rapid depletion of proteins in nonplant cells. 2009, Pubmed
Nishino, Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. 2012, Pubmed
Nora, Spatial partitioning of the regulatory landscape of the X-inactivation centre. 2012, Pubmed
Nora, Targeted Degradation of CTCF Decouples Local Insulation of Chromosome Domains from Genomic Compartmentalization. 2017, Pubmed
Nuebler, Chromatin organization by an interplay of loop extrusion and compartmental segregation. 2018, Pubmed
Ohnuki, Structure of chromosomes. I. Morphological studies of the spiral structure of human somatic chromosomes. 1968, Pubmed
Ohta, Proteomics Analysis with a Nano Random Forest Approach Reveals Novel Functional Interactions Regulated by SMC Complexes on Mitotic Chromosomes. 2016, Pubmed
Ohta, The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. 2010, Pubmed
Okada, The DT40 system as a tool for analyzing kinetochore assembly. 2006, Pubmed , Xenbase
Ono, Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. 2003, Pubmed , Xenbase
Ono, Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. 2004, Pubmed
Ou, ChromEMT: Visualizing 3D chromatin structure and compaction in interphase and mitotic cells. 2017, Pubmed
Paturej, Molecular structure of bottlebrush polymers in melts. 2016, Pubmed
Paulson, The structure of histone-depleted metaphase chromosomes. 1977, Pubmed
Pienta, A structural analysis of the role of the nuclear matrix and DNA loops in the organization of the nucleus and chromosome. 1984, Pubmed
Rao, A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. 2014, Pubmed
Rattner, Radial loops and helical coils coexist in metaphase chromosomes. 1985, Pubmed
Riggs, DNA methylation and late replication probably aid cell memory, and type I DNA reeling could aid chromosome folding and enhancer function. 1990, Pubmed
ROBBINS, THE ULTRASTRUCTURE OF A MAMMALIAN CELL DURING THE MITOTIC CYCLE. 1964, Pubmed
Saitoh, Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. 1994, Pubmed
Samejima, Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase IIα. 2012, Pubmed
Samejima, A promoter-hijack strategy for conditional shutdown of multiply spliced essential cell cycle genes. 2008, Pubmed
Samejima, Functional analysis after rapid degradation of condensins and 3D-EM reveals chromatin volume is uncoupled from chromosome architecture in mitosis. 2018, Pubmed
Sanyal, The long-range interaction landscape of gene promoters. 2012, Pubmed
Schwanhäusser, Global quantification of mammalian gene expression control. 2011, Pubmed
Schwarzer, Two independent modes of chromatin organization revealed by cohesin removal. 2017, Pubmed
Shintomi, The relative ratio of condensin I to II determines chromosome shapes. 2011, Pubmed , Xenbase
Shintomi, Mitotic chromosome assembly despite nucleosome depletion in Xenopus egg extracts. 2017, Pubmed , Xenbase
Sonoda, Homologous DNA recombination in vertebrate cells. 2001, Pubmed
Strukov, Engineered chromosome regions with altered sequence composition demonstrate hierarchical large-scale folding within metaphase chromosomes. 2003, Pubmed
Takahashi, Condensin I-mediated mitotic chromosome assembly requires association with chromokinesin KIF4A. 2016, Pubmed
Terakawa, The condensin complex is a mechanochemical motor that translocates along DNA. 2017, Pubmed
Waizenegger, Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. 2000, Pubmed , Xenbase
Warren, A New Chicken Genome Assembly Provides Insight into Avian Genome Structure. 2017, Pubmed
Wilkins, A cascade of histone modifications induces chromatin condensation in mitosis. 2014, Pubmed
Wiśniewski, A "proteomic ruler" for protein copy number and concentration estimation without spike-in standards. 2014, Pubmed
Woodcock, The higher-order structure of chromatin: evidence for a helical ribbon arrangement. 1984, Pubmed
Yanagida, Clearing the way for mitosis: is cohesin a target? 2009, Pubmed
Yoshimura, HEAT repeats - versatile arrays of amphiphilic helices working in crowded environments? 2016, Pubmed
Zhang, Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. 2012, Pubmed
Zhang, Condensin I and II behaviour in interphase nuclei and cells undergoing premature chromosome condensation. 2016, Pubmed
Zhiteneva, Mitotic post-translational modifications of histones promote chromatin compaction in vitro. 2017, Pubmed