Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
In somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosi...
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| Format: | Article |
| Language: | English |
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The Royal Society
2023-11-01
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| Series: | Open Biology |
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| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.230133 |
| _version_ | 1797361046080454656 |
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| author | Claudia Baumann Xiangyu Zhang Maria M. Viveiros Rabindranath De La Fuente |
| author_facet | Claudia Baumann Xiangyu Zhang Maria M. Viveiros Rabindranath De La Fuente |
| author_sort | Claudia Baumann |
| collection | DOAJ |
| description | In somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosis. Pericentric satellite RNAs are also expressed in human oocytes. However, the specific biological function(s) during oocyte meiosis remain to be established. Here, we use validated locked nucleic acid gapmers for major satellite RNA depletion followed by live cell imaging, and superresolution analysis to determine the role of pericentric non-coding RNAs during female meiosis. Depletion of satellite RNA induces mesoscale changes in pericentric heterochromatin structure leading to chromosome instability, kinetochore attachment errors and abnormal chromosome alignment. Chromosome misalignment is associated with spindle defects, microtubule instability and, unexpectedly, loss of acentriolar microtubule organizing centre (aMTOC) tethering to spindle poles. Pericentrin fragmentation and failure to assemble ring-like aMTOCs with loss of associated polo-like kinase 1 provide critical insight into the mechanisms leading to impaired spindle pole integrity. Inhibition of transcription or RNA splicing phenocopies the chromosome alignment errors and spindle defects, suggesting that pericentric transcription during oocyte meiosis is required to regulate heterochromatin structure, chromosome segregation and maintenance of spindle organization. |
| first_indexed | 2024-03-08T15:48:18Z |
| format | Article |
| id | doaj.art-f62fcdfb040a4527b28498ce1d1537ec |
| institution | Directory Open Access Journal |
| issn | 2046-2441 |
| language | English |
| last_indexed | 2024-03-08T15:48:18Z |
| publishDate | 2023-11-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj.art-f62fcdfb040a4527b28498ce1d1537ec2024-01-09T09:30:51ZengThe Royal SocietyOpen Biology2046-24412023-11-01131110.1098/rsob.230133Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organizationClaudia Baumann0Xiangyu Zhang1Maria M. Viveiros2Rabindranath De La Fuente3Department of Physiology and Pharmacology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602-0002, USADepartment of Physiology and Pharmacology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602-0002, USADepartment of Physiology and Pharmacology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602-0002, USADepartment of Physiology and Pharmacology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602-0002, USAIn somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosis. Pericentric satellite RNAs are also expressed in human oocytes. However, the specific biological function(s) during oocyte meiosis remain to be established. Here, we use validated locked nucleic acid gapmers for major satellite RNA depletion followed by live cell imaging, and superresolution analysis to determine the role of pericentric non-coding RNAs during female meiosis. Depletion of satellite RNA induces mesoscale changes in pericentric heterochromatin structure leading to chromosome instability, kinetochore attachment errors and abnormal chromosome alignment. Chromosome misalignment is associated with spindle defects, microtubule instability and, unexpectedly, loss of acentriolar microtubule organizing centre (aMTOC) tethering to spindle poles. Pericentrin fragmentation and failure to assemble ring-like aMTOCs with loss of associated polo-like kinase 1 provide critical insight into the mechanisms leading to impaired spindle pole integrity. Inhibition of transcription or RNA splicing phenocopies the chromosome alignment errors and spindle defects, suggesting that pericentric transcription during oocyte meiosis is required to regulate heterochromatin structure, chromosome segregation and maintenance of spindle organization.https://royalsocietypublishing.org/doi/10.1098/rsob.230133meiosispericentric heterochromatinmajor satellite transcriptsnon-coding RNAspindleaMTOC |
| spellingShingle | Claudia Baumann Xiangyu Zhang Maria M. Viveiros Rabindranath De La Fuente Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization Open Biology meiosis pericentric heterochromatin major satellite transcripts non-coding RNA spindle aMTOC |
| title | Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| title_full | Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| title_fullStr | Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| title_full_unstemmed | Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| title_short | Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| title_sort | pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization |
| topic | meiosis pericentric heterochromatin major satellite transcripts non-coding RNA spindle aMTOC |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.230133 |
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