Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages
Abstract Accumulating evidence hints heterochromatin anchoring to the inner nuclear membrane as an upstream regulatory process of gene expression. Given that the formation of neural progenitor cell lineages and the subsequent maintenance of postmitotic neuronal cell identity critically rely on trans...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Publishing Group
2024-02-01
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| Series: | Experimental and Molecular Medicine |
| Online Access: | https://doi.org/10.1038/s12276-024-01169-3 |
| _version_ | 1827328428224806912 |
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| author | Byung Su Ko Myeong Hoon Han Min Jee Kwon Dong Gon Cha Yuri Ji Eun Seo Park Min Jae Jeon Somi Kim Kyeongho Lee Yoon Ha Choi Jusung Lee Monica Torras-Llort Ki-Jun Yoon Hyosang Lee Jong Kyoung Kim Sung Bae Lee |
| author_facet | Byung Su Ko Myeong Hoon Han Min Jee Kwon Dong Gon Cha Yuri Ji Eun Seo Park Min Jae Jeon Somi Kim Kyeongho Lee Yoon Ha Choi Jusung Lee Monica Torras-Llort Ki-Jun Yoon Hyosang Lee Jong Kyoung Kim Sung Bae Lee |
| author_sort | Byung Su Ko |
| collection | DOAJ |
| description | Abstract Accumulating evidence hints heterochromatin anchoring to the inner nuclear membrane as an upstream regulatory process of gene expression. Given that the formation of neural progenitor cell lineages and the subsequent maintenance of postmitotic neuronal cell identity critically rely on transcriptional regulation, it seems possible that the development of neuronal cells is influenced by cell type-specific and/or context-dependent programmed regulation of heterochromatin anchoring. Here, we explored this possibility by genetically disrupting the evolutionarily conserved barrier-to-autointegration factor (Baf) in the Drosophila nervous system. Through single-cell RNA sequencing, we demonstrated that Baf knockdown induces prominent transcriptomic changes, particularly in type I neuroblasts. Among the differentially expressed genes, our genetic analyses identified teashirt (tsh), a transcription factor that interacts with beta-catenin, to be closely associated with Baf knockdown-induced phenotypes that were suppressed by the overexpression of tsh or beta-catenin. We also found that Baf and tsh colocalized in a region adjacent to heterochromatin in type I NBs. Notably, the subnuclear localization pattern remained unchanged when one of these two proteins was knocked down, indicating that both proteins contribute to the anchoring of heterochromatin to the inner nuclear membrane. Overall, this study reveals that the Baf-mediated transcriptional regulation of teashirt is a novel molecular mechanism that regulates the development of neural progenitor cell lineages. |
| first_indexed | 2024-03-07T15:17:45Z |
| format | Article |
| id | doaj.art-1ec26a52f76942f19aa7aa5402f7c822 |
| institution | Directory Open Access Journal |
| issn | 2092-6413 |
| language | English |
| last_indexed | 2024-03-07T15:17:45Z |
| publishDate | 2024-02-01 |
| publisher | Nature Publishing Group |
| record_format | Article |
| series | Experimental and Molecular Medicine |
| spelling | doaj.art-1ec26a52f76942f19aa7aa5402f7c8222024-03-05T17:48:11ZengNature Publishing GroupExperimental and Molecular Medicine2092-64132024-02-0156242244010.1038/s12276-024-01169-3Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineagesByung Su Ko0Myeong Hoon Han1Min Jee Kwon2Dong Gon Cha3Yuri Ji4Eun Seo Park5Min Jae Jeon6Somi Kim7Kyeongho Lee8Yoon Ha Choi9Jusung Lee10Monica Torras-Llort11Ki-Jun Yoon12Hyosang Lee13Jong Kyoung Kim14Sung Bae Lee15Department of Brain Sciences, DGISTDepartment of Brain Sciences, DGISTDepartment of Brain Sciences, DGISTDepartment of New Biology, DGISTDepartment of Brain Sciences, DGISTDepartment of New Biology, DGISTDepartment of Brain Sciences, DGISTDepartment of Life Sciences, Pohang University of Science and Technology (POSTECH)Department of Brain Sciences, DGISTDepartment of New Biology, DGISTDepartment of New Biology, DGISTInstitute of Molecular Biology of Barcelona, CSICDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Brain Sciences, DGISTDepartment of New Biology, DGISTDepartment of Brain Sciences, DGISTAbstract Accumulating evidence hints heterochromatin anchoring to the inner nuclear membrane as an upstream regulatory process of gene expression. Given that the formation of neural progenitor cell lineages and the subsequent maintenance of postmitotic neuronal cell identity critically rely on transcriptional regulation, it seems possible that the development of neuronal cells is influenced by cell type-specific and/or context-dependent programmed regulation of heterochromatin anchoring. Here, we explored this possibility by genetically disrupting the evolutionarily conserved barrier-to-autointegration factor (Baf) in the Drosophila nervous system. Through single-cell RNA sequencing, we demonstrated that Baf knockdown induces prominent transcriptomic changes, particularly in type I neuroblasts. Among the differentially expressed genes, our genetic analyses identified teashirt (tsh), a transcription factor that interacts with beta-catenin, to be closely associated with Baf knockdown-induced phenotypes that were suppressed by the overexpression of tsh or beta-catenin. We also found that Baf and tsh colocalized in a region adjacent to heterochromatin in type I NBs. Notably, the subnuclear localization pattern remained unchanged when one of these two proteins was knocked down, indicating that both proteins contribute to the anchoring of heterochromatin to the inner nuclear membrane. Overall, this study reveals that the Baf-mediated transcriptional regulation of teashirt is a novel molecular mechanism that regulates the development of neural progenitor cell lineages.https://doi.org/10.1038/s12276-024-01169-3 |
| spellingShingle | Byung Su Ko Myeong Hoon Han Min Jee Kwon Dong Gon Cha Yuri Ji Eun Seo Park Min Jae Jeon Somi Kim Kyeongho Lee Yoon Ha Choi Jusung Lee Monica Torras-Llort Ki-Jun Yoon Hyosang Lee Jong Kyoung Kim Sung Bae Lee Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages Experimental and Molecular Medicine |
| title | Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| title_full | Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| title_fullStr | Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| title_full_unstemmed | Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| title_short | Baf-mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| title_sort | baf mediated transcriptional regulation of teashirt is essential for the development of neural progenitor cell lineages |
| url | https://doi.org/10.1038/s12276-024-01169-3 |
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