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A Switch in Microtubule Orientation during C. elegans Meiosis

2018; Elsevier BV; Volume: 28; Issue: 18 Linguagem: Inglês

10.1016/j.cub.2018.07.012

1879-0445

Stefanie Redemann, Ina Lantzsch, Norbert Lindow, Steffen Prohaska, Martin Srayko, Thomas Müller‐Reichert,

Microtubule and mitosis dynamics

In oocytes of many organisms, meiotic spindles form in the absence of centrosomes [1Albertson D.G. Thomson J.N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans.Chromosome Res. 1993; 1: 15-26Crossref PubMed Scopus (214) Google Scholar, 2Schuh M. Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes.Cell. 2007; 130: 484-498Abstract Full Text Full Text PDF PubMed Scopus (399) Google Scholar, 3Dumont J. Desai A. Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis.Trends Cell Biol. 2012; 22: 241-249Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar, 4Holubcová Z. Blayney M. Elder K. Schuh M. Human oocytes. Error-prone chromosome-mediated spindle assembly favors chromosome segregation defects in human oocytes.Science. 2015; 348: 1143-1147Crossref PubMed Scopus (178) Google Scholar, 5Bennabi I. Terret M.E. Verlhac M.H. Meiotic spindle assembly and chromosome segregation in oocytes.J. Cell Biol. 2016; 215: 611-619Crossref PubMed Scopus (117) Google Scholar]. Such female meiotic spindles have a pointed appearance in metaphase with microtubules focused at acentrosomal spindle poles. At anaphase, the microtubules of acentrosomal spindles then transition to an inter-chromosomal array, while the spindle poles disappear. This transition is currently not understood. Previous studies have focused on this inter-chromosomal microtubule array and proposed a pushing model to drive chromosome segregation [6Dumont J. Oegema K. Desai A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis.Nat. Cell Biol. 2010; 12: 894-901Crossref PubMed Scopus (136) Google Scholar, 7Laband K. Le Borgne R. Edwards F. Stefanutti M. Canman J.C. Verbavatz J.M. Dumont J. Chromosome segregation occurs by microtubule pushing in oocytes.Nat. Commun. 2017; 8: 1499Crossref PubMed Scopus (44) Google Scholar]. This model includes an end-on orientation of microtubules with chromosomes. Alternatively, chromosomes were thought to associate along bundles of microtubules [8Muscat C.C. Torre-Santiago K.M. Tran M.V. Powers J.A. Wignall S.M. Kinetochore-independent chromosome segregation driven by lateral microtubule bundles.eLife. 2015; 4 (e06462)Crossref PubMed Scopus (49) Google Scholar, 9Mullen T.J. Wignall S.M. Interplay between microtubule bundling and sorting factors ensures acentriolar spindle stability during C. elegans oocyte meiosis.PLoS Genet. 2017; 13 (e1006986)Crossref PubMed Scopus (26) Google Scholar]. Starting with metaphase, this second model proposed a pure lateral chromosome-to-microtubule association up to the final meiotic stages of anaphase. Here, we applied large-scale electron tomography [10Redemann S. Baumgart J. Lindow N. Shelley M. Nazockdast E. Kratz A. Prohaska S. Brugués J. Fürthauer S. Müller-Reichert T. C. elegans chromosomes connect to centrosomes by anchoring into the spindle network.Nat. Commun. 2017; 8: 15288Crossref PubMed Scopus (72) Google Scholar] of staged C. elegans oocytes in meiosis to analyze the orientation of microtubules in respect to chromosomes. We show that microtubules at metaphase I are primarily oriented laterally to the chromosomes and that microtubules switch to an end-on orientation during progression through anaphase. We further show that this switch in microtubule orientation involves a kinesin-13 microtubule depolymerase, KLP-7, which removes laterally associated microtubules around chromosomes. From this, we conclude that both lateral and end-on modes of microtubule-to-chromosome orientations are successively used in C. elegans oocytes to segregate meiotic chromosomes.