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      Shaping mitotic chromosomes: From classical concepts to molecular mechanisms

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          Abstract

          How eukaryotic genomes are packaged into compact cylindrical chromosomes in preparation for cell divisions has remained one of the major unsolved questions of cell biology. Novel approaches to study the topology of DNA helices inside the nuclei of intact cells, paired with computational modeling and precise biomechanical measurements of isolated chromosomes, have advanced our understanding of mitotic chromosome architecture. In this Review Essay, we discuss – in light of these recent insights – the role of chromatin architecture and the functions and possible mechanisms of SMC protein complexes and other molecular machines in the formation of mitotic chromosomes. Based on the information available, we propose a stepwise model of mitotic chromosome condensation that envisions the sequential generation of intra-chromosomal linkages by condensin complexes in the context of cohesin-mediated inter-chromosomal linkages, assisted by topoisomerase II. The described scenario results in rod-shaped metaphase chromosomes ready for their segregation to the cell poles.

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          Organization of the mitotic chromosome.

          Natalia Naumova, Maxim Imakaev, Geoffrey Fudenberg … (2013)
          Mitotic chromosomes are among the most recognizable structures in the cell, yet for over a century their internal organization remains largely unsolved. We applied chromosome conformation capture methods, 5C and Hi-C, across the cell cycle and revealed two distinct three-dimensional folding states of the human genome. We show that the highly compartmentalized and cell type-specific organization described previously for nonsynchronous cells is restricted to interphase. In metaphase, we identified a homogenous folding state that is locus-independent, common to all chromosomes, and consistent among cell types, suggesting a general principle of metaphase chromosome organization. Using polymer simulations, we found that metaphase Hi-C data are inconsistent with classic hierarchical models and are instead best described by a linearly organized longitudinally compressed array of consecutive chromatin loops.
          Article 0 comments Cited 391 times – based on 0 reviews     Review now
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            Self-organization of domain structures by DNA-loop-extruding enzymes

            Elnaz Alipour, John Marko (2012)
            The long chromosomal DNAs of cells are organized into loop domains much larger in size than individual DNA-binding enzymes, presenting the question of how formation of such structures is controlled. We present a model for generation of defined chromosomal loops, based on molecular machines consisting of two coupled and oppositely directed motile elements which extrude loops from the double helix along which they translocate, while excluding one another sterically. If these machines do not dissociate from DNA (infinite processivity), a disordered, exponential steady-state distribution of small loops is obtained. However, if dissociation and rebinding of the machines occurs at a finite rate (finite processivity), the steady state qualitatively changes to a highly ordered ‘stacked’ configuration with suppressed fluctuations, organizing a single large, stable loop domain anchored by several machines. The size of the resulting domain can be simply regulated by boundary elements, which halt the progress of the extrusion machines. Possible realizations of these types of molecular machines are discussed, with a major focus on structural maintenance of chromosome complexes and also with discussion of type I restriction enzymes. This mechanism could explain the geometrically uniform folding of eukaryote mitotic chromosomes, through extrusion of pre-programmed loops and concomitant chromosome compaction.
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              Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells.

              Takao Ono, Ana Paula Losada, Michiko Hirano … (2003)
              The canonical condensin complex (henceforth condensin I) plays an essential role in mitotic chromosome assembly and segregation from yeast to humans. We report here the identification of a second condensin complex (condensin II) from vertebrate cells. Condensins I and II share the same pair of structural maintenance of chromosomes (SMC) subunits but contain different sets of non-SMC subunits. siRNA-mediated depletion of condensin I- or condensin II-specific subunits in HeLa cells produces a distinct, highly characteristic defect in chromosome morphology. Simultaneous depletion of both complexes causes the severest defect. In Xenopus egg extracts, condensin I function is predominant, but lack of condensin II results in the formation of irregularly shaped chromosomes. Condensins I and II show different distributions along the axis of chromosomes assembled in vivo and in vitro. We propose that the two condensin complexes make distinct mechanistic contributions to mitotic chromosome architecture in vertebrate cells.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Bioessays
                Journal ID (iso-abbrev): Bioessays
                Journal ID (publisher-id): bies
                Title: Bioessays
                Publisher: Blackwell Publishing Ltd (Oxford, UK )
                ISSN (Print): 0265-9247
                ISSN (Electronic): 1521-1878
                Publication date (Print): July 2015
                Publication date (Electronic): 18 May 2015
                Volume: 37
                Issue: 7
                Pages: 755-766
                Affiliations
                European Molecular Biology Laboratory (EMBL), Heidelberg Germany
                Author notes
                * Corresponding author: Christian Haering E-mail: christian.haering@ 123456embl.de
                Article
                DOI: 10.1002/bies.201500020
                PMC ID: 4683672
                PubMed ID: 25988527
                SO-VID: a0356221-2940-404c-8ed2-d8830ff2c8f1
                Copyright © © 2015 The Authors. Bioessays published by WILEY Periodicals, Inc.
                License:

                This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                Categories
                Subject: Prospects & Overviews

                ScienceOpen disciplines: Cell biology
                Keywords: chromosome condensation,chromosome segregation,cohesin,condensin,mitosis,smc complex,topoisomerase ii
                Data availability:
                ScienceOpen disciplines: Cell biology
                Keywords: chromosome condensation, chromosome segregation, cohesin, condensin, mitosis, smc complex, topoisomerase ii

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