Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions

During meiosis, a single round of DNA replication is followed by two consecutive rounds of nuclear divisions called meiosis I and meiosis II. In meiosis I, homologous chromosomes segregate, while sister chromatids remain together. Determining how this unusual chromosome segregation behavior is estab...

Full description

Bibliographic Details
Main Authors: Miller, Matthew P., Unal, Elcin, Brar, Gloria A., Amon, Angelika B
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: eLife Sciences Publications, Ltd. 2014
Online Access:http://hdl.handle.net/1721.1/89177
https://orcid.org/0000-0003-2012-7546
https://orcid.org/0000-0001-9837-0314
_version_ 1826215906897821696
author Miller, Matthew P.
Unal, Elcin
Brar, Gloria A.
Amon, Angelika B
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Miller, Matthew P.
Unal, Elcin
Brar, Gloria A.
Amon, Angelika B
author_sort Miller, Matthew P.
collection MIT
description During meiosis, a single round of DNA replication is followed by two consecutive rounds of nuclear divisions called meiosis I and meiosis II. In meiosis I, homologous chromosomes segregate, while sister chromatids remain together. Determining how this unusual chromosome segregation behavior is established is central to understanding germ cell development. Here we show that preventing microtubule–kinetochore interactions during premeiotic S phase and prophase I is essential for establishing the meiosis I chromosome segregation pattern. Premature interactions of kinetochores with microtubules transform meiosis I into a mitosis-like division by disrupting two key meiosis I events: coorientation of sister kinetochores and protection of centromeric cohesin removal from chromosomes. Furthermore we find that restricting outer kinetochore assembly contributes to preventing premature engagement of microtubules with kinetochores. We propose that inhibition of microtubule–kinetochore interactions during premeiotic S phase and prophase I is central to establishing the unique meiosis I chromosome segregation pattern.
first_indexed 2024-09-23T16:38:55Z
format Article
id mit-1721.1/89177
institution Massachusetts Institute of Technology
language en_US
last_indexed 2024-09-23T16:38:55Z
publishDate 2014
publisher eLife Sciences Publications, Ltd.
record_format dspace
spelling mit-1721.1/891772022-10-03T07:22:16Z Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions Miller, Matthew P. Unal, Elcin Brar, Gloria A. Amon, Angelika B Massachusetts Institute of Technology. Department of Biology Miller, Matthew P. Unal, Elcin Amon, Angelika B. During meiosis, a single round of DNA replication is followed by two consecutive rounds of nuclear divisions called meiosis I and meiosis II. In meiosis I, homologous chromosomes segregate, while sister chromatids remain together. Determining how this unusual chromosome segregation behavior is established is central to understanding germ cell development. Here we show that preventing microtubule–kinetochore interactions during premeiotic S phase and prophase I is essential for establishing the meiosis I chromosome segregation pattern. Premature interactions of kinetochores with microtubules transform meiosis I into a mitosis-like division by disrupting two key meiosis I events: coorientation of sister kinetochores and protection of centromeric cohesin removal from chromosomes. Furthermore we find that restricting outer kinetochore assembly contributes to preventing premature engagement of microtubules with kinetochores. We propose that inhibition of microtubule–kinetochore interactions during premeiotic S phase and prophase I is central to establishing the unique meiosis I chromosome segregation pattern. Howard Hughes Medical Institute National Institutes of Health (U.S.) (grant GM62207) Jane Coffin Childs Memorial Fund for Medical Research American Cancer Society 2014-09-04T18:13:42Z 2014-09-04T18:13:42Z 2012-12 2012-07 Article http://purl.org/eprint/type/JournalArticle 2050-084X http://hdl.handle.net/1721.1/89177 Miller, Matthew P, Elçin Ünal, Gloria A Brar, and Angelika Amon. “Meiosis I Chromosome Segregation Is Established through Regulation of Microtubule–kinetochore Interactions.” eLife;1:e00117 (December 18, 2012). https://orcid.org/0000-0003-2012-7546 https://orcid.org/0000-0001-9837-0314 en_US http://dx.doi.org/10.7554/eLife.00117 eLife Creative Commons Attribution http://creativecommons.org/licenses/by/3.0/ application/pdf eLife Sciences Publications, Ltd. eLife Sciences Publications, Ltd.
spellingShingle Miller, Matthew P.
Unal, Elcin
Brar, Gloria A.
Amon, Angelika B
Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title_full Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title_fullStr Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title_full_unstemmed Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title_short Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions
title_sort meiosis i chromosome segregation is established through regulation of microtubule kinetochore interactions
url http://hdl.handle.net/1721.1/89177
https://orcid.org/0000-0003-2012-7546
https://orcid.org/0000-0001-9837-0314
work_keys_str_mv AT millermatthewp meiosisichromosomesegregationisestablishedthroughregulationofmicrotubulekinetochoreinteractions
AT unalelcin meiosisichromosomesegregationisestablishedthroughregulationofmicrotubulekinetochoreinteractions
AT brargloriaa meiosisichromosomesegregationisestablishedthroughregulationofmicrotubulekinetochoreinteractions
AT amonangelikab meiosisichromosomesegregationisestablishedthroughregulationofmicrotubulekinetochoreinteractions