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...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-04-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010707 |
| _version_ | 1827952936602304512 |
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| author | Anne MacKenzie Victoria Vicory Soni Lacefield |
| author_facet | Anne MacKenzie Victoria Vicory Soni Lacefield |
| author_sort | Anne MacKenzie |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-09T14:05:11Z |
| format | Article |
| id | doaj.art-268e0c7544b34840979cf9d2f4319e75 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-09T14:05:11Z |
| publishDate | 2023-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-268e0c7544b34840979cf9d2f4319e752023-05-07T05:31:50ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-04-01194e101070710.1371/journal.pgen.1010707Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage.Anne MacKenzieVictoria VicorySoni LacefieldTo 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.https://doi.org/10.1371/journal.pgen.1010707 |
| spellingShingle | Anne MacKenzie Victoria Vicory Soni Lacefield Meiotic cells escape prolonged spindle checkpoint activity through kinetochore silencing and slippage. PLoS Genetics |
| 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 |
| url | https://doi.org/10.1371/journal.pgen.1010707 |
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