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      C. elegans chromosomes connect to centrosomes by anchoring into the spindle network

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          Abstract

          The mitotic spindle ensures the faithful segregation of chromosomes. Here we combine the first large-scale serial electron tomography of whole mitotic spindles in early C. elegans embryos with live-cell imaging to reconstruct all microtubules in 3D and identify their plus- and minus-ends. We classify them as kinetochore (KMTs), spindle (SMTs) or astral microtubules (AMTs) according to their positions, and quantify distinct properties of each class. While our light microscopy and mutant studies show that microtubules are nucleated from the centrosomes, we find only a few KMTs directly connected to the centrosomes. Indeed, by quantitatively analysing several models of microtubule growth, we conclude that minus-ends of KMTs have selectively detached and depolymerized from the centrosome. In toto, our results show that the connection between centrosomes and chromosomes is mediated by an anchoring into the entire spindle network and that any direct connections through KMTs are few and likely very transient.

          Abstract

          A connection between centrosomes and chromosomes is a key feature of mitotic spindles. Here the authors generate 3D reconstructions of whole mitotic spindles in early C. elegans embryos and show that chromosomes are anchored by the entire spindle network and that connections through kinetochore microtubules are few and likely very transient.

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          Most cited references56

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          Specific interference by ingested dsRNA.

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            Dynamic instability of microtubule growth.

            We report here that microtubules in vitro coexist in growing and shrinking populations which interconvert rather infrequently. This dynamic instability is a general property of microtubules and may be fundamental in explaining cellular microtubule organization.
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              Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts.

              Functional nuclei and mitotic spindles are shown to assemble around DNA-coated beads incubated in Xenopus egg extracts. Bipolar spindles assemble in the absence of centrosomes and kinetochores, indicating that bipolarity is an intrinsic property of microtubules assembling around chromatin in a mitotic cytoplasm. Microtubules nucleated at dispersed sites with random polarity rearrange into two arrays of uniform polarity. Spindle-pole formation requires cytoplasmic dynein-dependent translocation of microtubules across one another. It is proposed that spindles form in the absence of centrosomes by motor-dependent sorting of microtubules according to their polarity.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                11 May 2017
                2017
                : 8
                : 15288
                Affiliations
                [1 ]Technische Universität Dresden, Experimental Center, Medical Faculty Carl Gustav Carus , Fiedlerstraße 42, 01307 Dresden, Germany
                [2 ]Max Planck Institute for the Physics of Complex Systems , Nöthnitzer Straße 38, 01187 Dresden, Germany
                [3 ]Zuse Institute Berlin , Takustraße 7, 14195 Berlin, Germany
                [4 ]The Courant Institute of Mathematical Sciences, New York University , 251 Mercer Street, New York, New York 10012, USA
                [5 ]Flatiron Institute, Center for Computational Biology, 162 Fifth Avenue, New York, New York 10011, USA
                [6 ]Max Planck Institute of Molecular Cell Biology and Genetics , Pfotenhauerstraße 108, 01307 Dresden, Germany
                [7 ]Centre for Systems Biology Dresden , Pfotenhauerstr. 108, 01307 Dresden, Germany
                Author notes
                Author information
                http://orcid.org/0000-0001-7384-5715
                Article
                ncomms15288
                10.1038/ncomms15288
                5437269
                28492281
                a647cbd2-4937-412a-952d-a5c45ba4ae89
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 04 February 2017
                : 10 March 2017
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