Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential
Centromeres provide a robust model for epigenetic inheritance as they are specified by sequence-independent mechanisms involving the histone H3-variant centromere protein A (CENP-A). Prevailing models indicate that the high intrinsic stability of CENP-A nucleosomes maintains centromere identity inde...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier BV
2020
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| Online Access: | https://hdl.handle.net/1721.1/128138 |
| _version_ | 1811093266308792320 |
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| author | Swartz, S. Zachary McKay, Liliana S. Su, Kuan-Chung Bury, Leah Padeganeh, Abbas Maddox, Paul S. Knouse, Kristin A. Cheeseman, Iain M |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Swartz, S. Zachary McKay, Liliana S. Su, Kuan-Chung Bury, Leah Padeganeh, Abbas Maddox, Paul S. Knouse, Kristin A. Cheeseman, Iain M |
| author_sort | Swartz, S. Zachary |
| collection | MIT |
| description | Centromeres provide a robust model for epigenetic inheritance as they are specified by sequence-independent mechanisms involving the histone H3-variant centromere protein A (CENP-A). Prevailing models indicate that the high intrinsic stability of CENP-A nucleosomes maintains centromere identity indefinitely. Here, we demonstrate that CENP-A is not stable at centromeres but is instead gradually and continuously incorporated in quiescent cells including G0-arrested tissue culture cells and prophase I-arrested oocytes. Quiescent CENP-A incorporation involves the canonical CENP-A deposition machinery but displays distinct requirements from cell cycle-dependent deposition. We demonstrate that Plk1 is required specifically for G1 CENP-A deposition, whereas transcription promotes CENP-A incorporation in quiescent oocytes. Preventing CENP-A deposition during quiescence results in significantly reduced CENP-A levels and perturbs chromosome segregation following the resumption of cell division. In contrast to quiescent cells, terminally differentiated cells fail to maintain CENP-A levels. Our work reveals that quiescent cells actively maintain centromere identity providing an indicator of proliferative potential. |
| first_indexed | 2024-09-23T15:42:31Z |
| format | Article |
| id | mit-1721.1/128138 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T15:42:31Z |
| publishDate | 2020 |
| publisher | Elsevier BV |
| record_format | dspace |
| spelling | mit-1721.1/1281382022-10-02T03:34:11Z Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential Swartz, S. Zachary McKay, Liliana S. Su, Kuan-Chung Bury, Leah Padeganeh, Abbas Maddox, Paul S. Knouse, Kristin A. Cheeseman, Iain M Massachusetts Institute of Technology. Department of Biology Centromeres provide a robust model for epigenetic inheritance as they are specified by sequence-independent mechanisms involving the histone H3-variant centromere protein A (CENP-A). Prevailing models indicate that the high intrinsic stability of CENP-A nucleosomes maintains centromere identity indefinitely. Here, we demonstrate that CENP-A is not stable at centromeres but is instead gradually and continuously incorporated in quiescent cells including G0-arrested tissue culture cells and prophase I-arrested oocytes. Quiescent CENP-A incorporation involves the canonical CENP-A deposition machinery but displays distinct requirements from cell cycle-dependent deposition. We demonstrate that Plk1 is required specifically for G1 CENP-A deposition, whereas transcription promotes CENP-A incorporation in quiescent oocytes. Preventing CENP-A deposition during quiescence results in significantly reduced CENP-A levels and perturbs chromosome segregation following the resumption of cell division. In contrast to quiescent cells, terminally differentiated cells fail to maintain CENP-A levels. Our work reveals that quiescent cells actively maintain centromere identity providing an indicator of proliferative potential. 2020-10-21T21:22:32Z 2020-10-21T21:22:32Z 2019-10 2019-05 2020-10-19T15:01:19Z Article http://purl.org/eprint/type/JournalArticle 1534-5807 https://hdl.handle.net/1721.1/128138 Swartz, S. Zachary et al. "Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential." Developmental Cell 51, 1 (October 2019): P35-48.e7 © 2019 Elsevier Inc en http://dx.doi.org/10.1016/j.devcel.2019.07.016 Developmental Cell Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier BV PMC |
| spellingShingle | Swartz, S. Zachary McKay, Liliana S. Su, Kuan-Chung Bury, Leah Padeganeh, Abbas Maddox, Paul S. Knouse, Kristin A. Cheeseman, Iain M Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title | Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title_full | Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title_fullStr | Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title_full_unstemmed | Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title_short | Quiescent Cells Actively Replenish CENP-A Nucleosomes to Maintain Centromere Identity and Proliferative Potential |
| title_sort | quiescent cells actively replenish cenp a nucleosomes to maintain centromere identity and proliferative potential |
| url | https://hdl.handle.net/1721.1/128138 |
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