Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development
Abstract Background During meiosis of mammalian cells, chromatin undergoes drastic reorganization. However, the dynamics of the three‐dimensional (3D) chromatin structure during the development of female germline stem cells (FGSCs) are poorly understood. Methods The high‐throughput chromosome confor...
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| Format: | Article |
| Language: | English |
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Wiley
2022-06-01
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| Series: | Clinical and Translational Medicine |
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| Online Access: | https://doi.org/10.1002/ctm2.927 |
| _version_ | 1828314091420123136 |
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| author | Geng G. Tian Changliang Hou Jing Li Ji Wu |
| author_facet | Geng G. Tian Changliang Hou Jing Li Ji Wu |
| author_sort | Geng G. Tian |
| collection | DOAJ |
| description | Abstract Background During meiosis of mammalian cells, chromatin undergoes drastic reorganization. However, the dynamics of the three‐dimensional (3D) chromatin structure during the development of female germline stem cells (FGSCs) are poorly understood. Methods The high‐throughput chromosome conformation capture technique was used to probe the 3D structure of chromatin in mouse germ cells at each stage of FGSC development. Results The global 3D genome was dramatically reorganized during FGSC development. In topologically associating domains, the chromatin structure was weakened in germinal vesicle stage oocytes and still present in meiosis I stage oocytes but had vanished in meiosis II oocytes. This switch between topologically associating domains was related to the biological process of FGSC development. Moreover, we constructed a landscape of chromosome X organization, which showed that the X chromosome occupied a smaller proportion of the active (A) compartment than the autosome during FGSC development. By comparing the high‐order chromatin structure between female and male germline development, we found that 3D genome organization was remodelled by two different potential mechanisms during gamete development, in which interchromosomal interactions, compartments, and topologically associating domain were decreased during FGSC development but reorganized and recovered during spermatogenesis. Finally, we identified conserved chromatin structures between FGSC development and early embryonic development. Conclusions These results provide a valuable resource to characterize chromatin organization and for further studies of FGSC development. |
| first_indexed | 2024-04-13T16:39:46Z |
| format | Article |
| id | doaj.art-2bfe55226587417ba018d5e29122d217 |
| institution | Directory Open Access Journal |
| issn | 2001-1326 |
| language | English |
| last_indexed | 2024-04-13T16:39:46Z |
| publishDate | 2022-06-01 |
| publisher | Wiley |
| record_format | Article |
| series | Clinical and Translational Medicine |
| spelling | doaj.art-2bfe55226587417ba018d5e29122d2172022-12-22T02:39:17ZengWileyClinical and Translational Medicine2001-13262022-06-01126n/an/a10.1002/ctm2.927Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell developmentGeng G. Tian0Changliang Hou1Jing Li2Ji Wu3Renji Hospital Key Laboratory for the Genetics of Developmental & Neuropsychiatric Disorders (Ministry of Education) Bio‐X Institutes School of Medicine Shanghai Jiao Tong University Shanghai ChinaRenji Hospital Key Laboratory for the Genetics of Developmental & Neuropsychiatric Disorders (Ministry of Education) Bio‐X Institutes School of Medicine Shanghai Jiao Tong University Shanghai ChinaDepartment of Bioinformatics and Biostatistics School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaRenji Hospital Key Laboratory for the Genetics of Developmental & Neuropsychiatric Disorders (Ministry of Education) Bio‐X Institutes School of Medicine Shanghai Jiao Tong University Shanghai ChinaAbstract Background During meiosis of mammalian cells, chromatin undergoes drastic reorganization. However, the dynamics of the three‐dimensional (3D) chromatin structure during the development of female germline stem cells (FGSCs) are poorly understood. Methods The high‐throughput chromosome conformation capture technique was used to probe the 3D structure of chromatin in mouse germ cells at each stage of FGSC development. Results The global 3D genome was dramatically reorganized during FGSC development. In topologically associating domains, the chromatin structure was weakened in germinal vesicle stage oocytes and still present in meiosis I stage oocytes but had vanished in meiosis II oocytes. This switch between topologically associating domains was related to the biological process of FGSC development. Moreover, we constructed a landscape of chromosome X organization, which showed that the X chromosome occupied a smaller proportion of the active (A) compartment than the autosome during FGSC development. By comparing the high‐order chromatin structure between female and male germline development, we found that 3D genome organization was remodelled by two different potential mechanisms during gamete development, in which interchromosomal interactions, compartments, and topologically associating domain were decreased during FGSC development but reorganized and recovered during spermatogenesis. Finally, we identified conserved chromatin structures between FGSC development and early embryonic development. Conclusions These results provide a valuable resource to characterize chromatin organization and for further studies of FGSC development.https://doi.org/10.1002/ctm2.927chromatin structureFGSC developmentHi‐C |
| spellingShingle | Geng G. Tian Changliang Hou Jing Li Ji Wu Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development Clinical and Translational Medicine chromatin structure FGSC development Hi‐C |
| title | Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| title_full | Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| title_fullStr | Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| title_full_unstemmed | Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| title_short | Three‐dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| title_sort | three dimensional genome structure shapes the recombination landscape of chromatin features during female germline stem cell development |
| topic | chromatin structure FGSC development Hi‐C |
| url | https://doi.org/10.1002/ctm2.927 |
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