Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage
Summary: The transcription factor Shavenbaby (Svb), the only member of the OvoL family in Drosophila, controls the fate of various epithelial embryonic cells and adult stem cells. Post-translational modification of Svb produces two protein isoforms, Svb-ACT and Svb-REP, which promote adult intestina...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223027013 |
| _version_ | 1797390422895493120 |
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| author | Alexandra Mancheno-Ferris Clément Immarigeon Alexia Rivero David Depierre Naomi Schickele Olivier Fosseprez Nicolas Chanard Gabriel Aughey Priscilla Lhoumaud Julien Anglade Tony Southall Serge Plaza François Payre Olivier Cuvier Cédric Polesello |
| author_facet | Alexandra Mancheno-Ferris Clément Immarigeon Alexia Rivero David Depierre Naomi Schickele Olivier Fosseprez Nicolas Chanard Gabriel Aughey Priscilla Lhoumaud Julien Anglade Tony Southall Serge Plaza François Payre Olivier Cuvier Cédric Polesello |
| author_sort | Alexandra Mancheno-Ferris |
| collection | DOAJ |
| description | Summary: The transcription factor Shavenbaby (Svb), the only member of the OvoL family in Drosophila, controls the fate of various epithelial embryonic cells and adult stem cells. Post-translational modification of Svb produces two protein isoforms, Svb-ACT and Svb-REP, which promote adult intestinal stem cell renewal or differentiation, respectively. To define Svb mode of action, we used engineered cell lines and develop an unbiased method to identify Svb target genes across different contexts. Within a given cell type, Svb-ACT and Svb-REP antagonistically regulate the expression of a set of target genes, binding specific enhancers whose accessibility is constrained by chromatin landscape. Reciprocally, Svb-REP can influence local chromatin marks of active enhancers to help repressing target genes. Along the intestinal lineage, the set of Svb target genes progressively changes, together with chromatin accessibility. We propose that Svb-ACT-to-REP transition promotes enterocyte differentiation of intestinal stem cells through direct gene regulation and chromatin remodeling. |
| first_indexed | 2024-03-08T23:11:30Z |
| format | Article |
| id | doaj.art-720d1f28390547db82acb73d52355bbc |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-08T23:11:30Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-720d1f28390547db82acb73d52355bbc2023-12-15T07:25:25ZengElsevieriScience2589-00422024-01-01271108624Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineageAlexandra Mancheno-Ferris0Clément Immarigeon1Alexia Rivero2David Depierre3Naomi Schickele4Olivier Fosseprez5Nicolas Chanard6Gabriel Aughey7Priscilla Lhoumaud8Julien Anglade9Tony Southall10Serge Plaza11François Payre12Olivier Cuvier13Cédric Polesello14Molecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Control of cell shape remodeling team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Control of cell shape remodeling team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Control of cell shape remodeling team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, FranceImperial College London, Sir Ernst Chain Building, South Kensington Campus, London SW7 2AZ, UKMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, France; Institut Jacques Monod, Université Paris Cité/CNRS, 15 rue Hélène Brion, 75205 Paris Cedex 13, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, FranceImperial College London, Sir Ernst Chain Building, South Kensington Campus, London SW7 2AZ, UKMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Laboratoire de Recherche en Sciences Végétales, CNRS/UPS/INPT, 31320 Auzeville-Tolosane, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Control of cell shape remodeling team, CBI, CNRS, UPS, 31062 Toulouse, FranceMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Chromatin Dynamics and Cell Proliferation team, CBI, CNRS, UPS, 31062 Toulouse, France; Corresponding authorMolecular, Cellular and Developmental biology department (MCD), Centre de Biologie Integrative (CBI), Université de Toulouse, CNRS, UPS, 31062 Toulouse, France; Control of cell shape remodeling team, CBI, CNRS, UPS, 31062 Toulouse, France; Corresponding authorSummary: The transcription factor Shavenbaby (Svb), the only member of the OvoL family in Drosophila, controls the fate of various epithelial embryonic cells and adult stem cells. Post-translational modification of Svb produces two protein isoforms, Svb-ACT and Svb-REP, which promote adult intestinal stem cell renewal or differentiation, respectively. To define Svb mode of action, we used engineered cell lines and develop an unbiased method to identify Svb target genes across different contexts. Within a given cell type, Svb-ACT and Svb-REP antagonistically regulate the expression of a set of target genes, binding specific enhancers whose accessibility is constrained by chromatin landscape. Reciprocally, Svb-REP can influence local chromatin marks of active enhancers to help repressing target genes. Along the intestinal lineage, the set of Svb target genes progressively changes, together with chromatin accessibility. We propose that Svb-ACT-to-REP transition promotes enterocyte differentiation of intestinal stem cells through direct gene regulation and chromatin remodeling.http://www.sciencedirect.com/science/article/pii/S2589004223027013Molecular biologyCell biology |
| spellingShingle | Alexandra Mancheno-Ferris Clément Immarigeon Alexia Rivero David Depierre Naomi Schickele Olivier Fosseprez Nicolas Chanard Gabriel Aughey Priscilla Lhoumaud Julien Anglade Tony Southall Serge Plaza François Payre Olivier Cuvier Cédric Polesello Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage iScience Molecular biology Cell biology |
| title | Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage |
| title_full | Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage |
| title_fullStr | Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage |
| title_full_unstemmed | Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage |
| title_short | Crosstalk between chromatin and Shavenbaby defines transcriptional output along the Drosophila intestinal stem cell lineage |
| title_sort | crosstalk between chromatin and shavenbaby defines transcriptional output along the drosophila intestinal stem cell lineage |
| topic | Molecular biology Cell biology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223027013 |
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