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Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage

To prevent chromosome mis-segregation, a surveillance mechanism known as the spindle checkpoint delays the cell cycle if kinetochores are not attached to spindle microtubules, allowing the cell additional time to correct improper attachments. During spindle checkpoint activation, checkpoint proteins...

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Detalles Bibliográficos
Autores principales: MacKenzie, Anne, Vicory, Victoria, Lacefield, Soni
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10109492/
https://www.ncbi.nlm.nih.gov/pubmed/37018287
http://dx.doi.org/10.1371/journal.pgen.1010707
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author MacKenzie, Anne
Vicory, Victoria
Lacefield, Soni
author_facet MacKenzie, Anne
Vicory, Victoria
Lacefield, Soni
author_sort MacKenzie, Anne
collection PubMed
description To prevent chromosome mis-segregation, a surveillance mechanism known as the spindle checkpoint delays the cell cycle if kinetochores are not attached to spindle microtubules, allowing the cell additional time to correct improper attachments. During spindle checkpoint activation, checkpoint proteins bind the unattached kinetochore and send a diffusible signal to inhibit the anaphase promoting complex/cyclosome (APC/C). Previous work has shown that mitotic cells with depolymerized microtubules can escape prolonged spindle checkpoint activation in a process called mitotic slippage. During slippage, spindle checkpoint proteins bind unattached kinetochores, but the cells cannot maintain the checkpoint arrest. We asked if meiotic cells had as robust of a spindle checkpoint response as mitotic cells and whether they also undergo slippage after prolonged spindle checkpoint activity. We performed a direct comparison between mitotic and meiotic budding yeast cells that signal the spindle checkpoint through two different assays. We find that the spindle checkpoint delay is shorter in meiosis I or meiosis II compared to mitosis, overcoming a checkpoint arrest approximately 150 minutes earlier in meiosis than in mitosis. In addition, cells in meiosis I escape spindle checkpoint signaling using two mechanisms, silencing the checkpoint at the kinetochore and through slippage. We propose that meiotic cells undertake developmentally-regulated mechanisms to prevent persistent spindle checkpoint activity to ensure the production of gametes.
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spelling pubmed-101094922023-04-18 Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage MacKenzie, Anne Vicory, Victoria Lacefield, Soni PLoS Genet Research Article To prevent chromosome mis-segregation, a surveillance mechanism known as the spindle checkpoint delays the cell cycle if kinetochores are not attached to spindle microtubules, allowing the cell additional time to correct improper attachments. During spindle checkpoint activation, checkpoint proteins bind the unattached kinetochore and send a diffusible signal to inhibit the anaphase promoting complex/cyclosome (APC/C). Previous work has shown that mitotic cells with depolymerized microtubules can escape prolonged spindle checkpoint activation in a process called mitotic slippage. During slippage, spindle checkpoint proteins bind unattached kinetochores, but the cells cannot maintain the checkpoint arrest. We asked if meiotic cells had as robust of a spindle checkpoint response as mitotic cells and whether they also undergo slippage after prolonged spindle checkpoint activity. We performed a direct comparison between mitotic and meiotic budding yeast cells that signal the spindle checkpoint through two different assays. We find that the spindle checkpoint delay is shorter in meiosis I or meiosis II compared to mitosis, overcoming a checkpoint arrest approximately 150 minutes earlier in meiosis than in mitosis. In addition, cells in meiosis I escape spindle checkpoint signaling using two mechanisms, silencing the checkpoint at the kinetochore and through slippage. We propose that meiotic cells undertake developmentally-regulated mechanisms to prevent persistent spindle checkpoint activity to ensure the production of gametes. Public Library of Science 2023-04-05 /pmc/articles/PMC10109492/ /pubmed/37018287 http://dx.doi.org/10.1371/journal.pgen.1010707 Text en © 2023 MacKenzie et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
MacKenzie, Anne
Vicory, Victoria
Lacefield, Soni
Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title_full Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title_fullStr Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title_full_unstemmed Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title_short Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
title_sort meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10109492/
https://www.ncbi.nlm.nih.gov/pubmed/37018287
http://dx.doi.org/10.1371/journal.pgen.1010707
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