Crosstalk between chromatin structure, cohesin activity and transcription
Abstract Background A complex interplay between chromatin and topological machineries is critical for genome architecture and function. However, little is known about these reciprocal interactions, even for cohesin, despite its multiple roles in DNA metabolism. Results We have used genome-wide analy...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2019-07-01
|
| Series: | Epigenetics & Chromatin |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13072-019-0293-6 |
| _version_ | 1819076961144668160 |
|---|---|
| author | Douglas Maya-Miles Eloísa Andújar Mónica Pérez-Alegre Marina Murillo-Pineda Marta Barrientos-Moreno María J. Cabello-Lobato Elena Gómez-Marín Macarena Morillo-Huesca Félix Prado |
| author_facet | Douglas Maya-Miles Eloísa Andújar Mónica Pérez-Alegre Marina Murillo-Pineda Marta Barrientos-Moreno María J. Cabello-Lobato Elena Gómez-Marín Macarena Morillo-Huesca Félix Prado |
| author_sort | Douglas Maya-Miles |
| collection | DOAJ |
| description | Abstract Background A complex interplay between chromatin and topological machineries is critical for genome architecture and function. However, little is known about these reciprocal interactions, even for cohesin, despite its multiple roles in DNA metabolism. Results We have used genome-wide analyses to address how cohesins and chromatin structure impact each other in yeast. Cohesin inactivation in scc1-73 mutants during the S and G2 phases causes specific changes in chromatin structure that preferentially take place at promoters; these changes include a significant increase in the occupancy of the − 1 and + 1 nucleosomes. In addition, cohesins play a major role in transcription regulation that is associated with specific promoter chromatin architecture. In scc1-73 cells, downregulated genes are enriched in promoters with short or no nucleosome-free region (NFR) and a fragile “nucleosome − 1/RSC complex” particle. These results, together with a preferential increase in the occupancy of nucleosome − 1 of these genes, suggest that cohesins promote transcription activation by helping RSC to form the NFR. In sharp contrast, the scc1-73 upregulated genes are enriched in promoters with an “open” chromatin structure and are mostly at cohesin-enriched regions, suggesting that a local accumulation of cohesins might help to inhibit transcription. On the other hand, a dramatic loss of chromatin integrity by histone depletion during DNA replication has a moderate effect on the accumulation and distribution of cohesin peaks along the genome. Conclusions Our analyses of the interplay between chromatin integrity and cohesin activity suggest that cohesins play a major role in transcription regulation, which is associated with specific chromatin architecture and cohesin-mediated nucleosome alterations of the regulated promoters. In contrast, chromatin integrity plays only a minor role in the binding and distribution of cohesins. |
| first_indexed | 2024-12-21T18:49:37Z |
| format | Article |
| id | doaj.art-d93a05ce1df040268d90fc7c0957d1ae |
| institution | Directory Open Access Journal |
| issn | 1756-8935 |
| language | English |
| last_indexed | 2024-12-21T18:49:37Z |
| publishDate | 2019-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Epigenetics & Chromatin |
| spelling | doaj.art-d93a05ce1df040268d90fc7c0957d1ae2022-12-21T18:53:48ZengBMCEpigenetics & Chromatin1756-89352019-07-0112111810.1186/s13072-019-0293-6Crosstalk between chromatin structure, cohesin activity and transcriptionDouglas Maya-Miles0Eloísa Andújar1Mónica Pérez-Alegre2Marina Murillo-Pineda3Marta Barrientos-Moreno4María J. Cabello-Lobato5Elena Gómez-Marín6Macarena Morillo-Huesca7Félix Prado8Department of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideGenomic Unit, Andalusian Molecular Biology and Regenerative Medicine Center (CABIMER), CSIC-University of Seville-University Pablo de OlavideGenomic Unit, Andalusian Molecular Biology and Regenerative Medicine Center (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideDepartment of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine (CABIMER), CSIC-University of Seville-University Pablo de OlavideAbstract Background A complex interplay between chromatin and topological machineries is critical for genome architecture and function. However, little is known about these reciprocal interactions, even for cohesin, despite its multiple roles in DNA metabolism. Results We have used genome-wide analyses to address how cohesins and chromatin structure impact each other in yeast. Cohesin inactivation in scc1-73 mutants during the S and G2 phases causes specific changes in chromatin structure that preferentially take place at promoters; these changes include a significant increase in the occupancy of the − 1 and + 1 nucleosomes. In addition, cohesins play a major role in transcription regulation that is associated with specific promoter chromatin architecture. In scc1-73 cells, downregulated genes are enriched in promoters with short or no nucleosome-free region (NFR) and a fragile “nucleosome − 1/RSC complex” particle. These results, together with a preferential increase in the occupancy of nucleosome − 1 of these genes, suggest that cohesins promote transcription activation by helping RSC to form the NFR. In sharp contrast, the scc1-73 upregulated genes are enriched in promoters with an “open” chromatin structure and are mostly at cohesin-enriched regions, suggesting that a local accumulation of cohesins might help to inhibit transcription. On the other hand, a dramatic loss of chromatin integrity by histone depletion during DNA replication has a moderate effect on the accumulation and distribution of cohesin peaks along the genome. Conclusions Our analyses of the interplay between chromatin integrity and cohesin activity suggest that cohesins play a major role in transcription regulation, which is associated with specific chromatin architecture and cohesin-mediated nucleosome alterations of the regulated promoters. In contrast, chromatin integrity plays only a minor role in the binding and distribution of cohesins.http://link.springer.com/article/10.1186/s13072-019-0293-6ChromatinCohesinTranscriptionScc1 |
| spellingShingle | Douglas Maya-Miles Eloísa Andújar Mónica Pérez-Alegre Marina Murillo-Pineda Marta Barrientos-Moreno María J. Cabello-Lobato Elena Gómez-Marín Macarena Morillo-Huesca Félix Prado Crosstalk between chromatin structure, cohesin activity and transcription Epigenetics & Chromatin Chromatin Cohesin Transcription Scc1 |
| title | Crosstalk between chromatin structure, cohesin activity and transcription |
| title_full | Crosstalk between chromatin structure, cohesin activity and transcription |
| title_fullStr | Crosstalk between chromatin structure, cohesin activity and transcription |
| title_full_unstemmed | Crosstalk between chromatin structure, cohesin activity and transcription |
| title_short | Crosstalk between chromatin structure, cohesin activity and transcription |
| title_sort | crosstalk between chromatin structure cohesin activity and transcription |
| topic | Chromatin Cohesin Transcription Scc1 |
| url | http://link.springer.com/article/10.1186/s13072-019-0293-6 |
| work_keys_str_mv | AT douglasmayamiles crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT eloisaandujar crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT monicaperezalegre crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT marinamurillopineda crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT martabarrientosmoreno crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT mariajcabellolobato crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT elenagomezmarin crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT macarenamorillohuesca crosstalkbetweenchromatinstructurecohesinactivityandtranscription AT felixprado crosstalkbetweenchromatinstructurecohesinactivityandtranscription |