Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis
Abstract Background The endocytosis of Gap junction plaques (GJP) requires cytoskeletal forces to internalize such large membranous structures. Actin, which partners the connexin proteins constituting Gap junctions and is located close to Annular Gap Junctions (AGJ), could be actively involved in th...
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| Format: | Article |
| Language: | English |
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BMC
2023-08-01
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| Series: | Basic and Clinical Andrology |
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| Online Access: | https://doi.org/10.1186/s12610-023-00194-y |
| _version_ | 1797752811936546816 |
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| author | Dominique Segretain Mathilde Di Marco Chloé Dufeu Diane Carette Alain Trubuil Georges Pointis |
| author_facet | Dominique Segretain Mathilde Di Marco Chloé Dufeu Diane Carette Alain Trubuil Georges Pointis |
| author_sort | Dominique Segretain |
| collection | DOAJ |
| description | Abstract Background The endocytosis of Gap junction plaques (GJP) requires cytoskeletal forces to internalize such large membranous structures. Actin, which partners the connexin proteins constituting Gap junctions and is located close to Annular Gap Junctions (AGJ), could be actively involved in this physiological process. Results Electron Microscopy and Light Microscopy images, associated with time-lapse analysis and 3D reconstruction, used at high resolution and enhanced using ImageJ based software analysis, revealed that: i) actin cables, originating from Donor cells, insert on the edge of GJP and contribute to their invagination, giving rise to AGJ, whereas actin cables on the Acceptor cell side of the plaque are not modified; ii) actin cables from the Donor cell are continuous with the actin network present over the entire GJP surface. These actin cables fuse at a single point distant from the plaque, which then detaches itself from the membrane, condensing to form an actin mass during the final internalization process; iii) the Acceptor cell participates in the last step of the endocytic invagination process by forming an annular actin structure known as an actin ring. Conclusions Together, these data suggest that the endocytosis of GJP is an example of a unique cooperative mechanism between the Donor (the traction of its actin cables) and the Acceptor cells (forming the actin ring). |
| first_indexed | 2024-03-12T17:08:52Z |
| format | Article |
| id | doaj.art-04defef642ed49a393a291ddd916ad35 |
| institution | Directory Open Access Journal |
| issn | 2051-4190 |
| language | English |
| last_indexed | 2024-03-12T17:08:52Z |
| publishDate | 2023-08-01 |
| publisher | BMC |
| record_format | Article |
| series | Basic and Clinical Andrology |
| spelling | doaj.art-04defef642ed49a393a291ddd916ad352023-08-06T11:09:26ZengBMCBasic and Clinical Andrology2051-41902023-08-0133111110.1186/s12610-023-00194-yCooperative cell–cell actin network remodeling to perform Gap junction endocytosisDominique Segretain0Mathilde Di Marco1Chloé Dufeu2Diane Carette3Alain Trubuil4Georges Pointis5UMR S1147, Université Paris DescartesUMR S1147, Université Paris DescartesFaculté de Pharmacie, Université Paris-SaclayINSERMMaIAGE, INRAE, Université Paris-SaclayINSERM U 1065, Team 5 Physiopathological Control of Germ Cell Proliferation: Genomic and Non-Genomic Mechanisms, University of Nice Sophia-AntipolisAbstract Background The endocytosis of Gap junction plaques (GJP) requires cytoskeletal forces to internalize such large membranous structures. Actin, which partners the connexin proteins constituting Gap junctions and is located close to Annular Gap Junctions (AGJ), could be actively involved in this physiological process. Results Electron Microscopy and Light Microscopy images, associated with time-lapse analysis and 3D reconstruction, used at high resolution and enhanced using ImageJ based software analysis, revealed that: i) actin cables, originating from Donor cells, insert on the edge of GJP and contribute to their invagination, giving rise to AGJ, whereas actin cables on the Acceptor cell side of the plaque are not modified; ii) actin cables from the Donor cell are continuous with the actin network present over the entire GJP surface. These actin cables fuse at a single point distant from the plaque, which then detaches itself from the membrane, condensing to form an actin mass during the final internalization process; iii) the Acceptor cell participates in the last step of the endocytic invagination process by forming an annular actin structure known as an actin ring. Conclusions Together, these data suggest that the endocytosis of GJP is an example of a unique cooperative mechanism between the Donor (the traction of its actin cables) and the Acceptor cells (forming the actin ring).https://doi.org/10.1186/s12610-023-00194-yAnnular Gap Junction (AGJ)Gap Junction (GJ)Gap Junction Plaque (GJP)Jonction gap (GJ)Plaque de jonctions gap (GJP)Jonction gap annulaire (GJA) |
| spellingShingle | Dominique Segretain Mathilde Di Marco Chloé Dufeu Diane Carette Alain Trubuil Georges Pointis Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis Basic and Clinical Andrology Annular Gap Junction (AGJ) Gap Junction (GJ) Gap Junction Plaque (GJP) Jonction gap (GJ) Plaque de jonctions gap (GJP) Jonction gap annulaire (GJA) |
| title | Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis |
| title_full | Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis |
| title_fullStr | Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis |
| title_full_unstemmed | Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis |
| title_short | Cooperative cell–cell actin network remodeling to perform Gap junction endocytosis |
| title_sort | cooperative cell cell actin network remodeling to perform gap junction endocytosis |
| topic | Annular Gap Junction (AGJ) Gap Junction (GJ) Gap Junction Plaque (GJP) Jonction gap (GJ) Plaque de jonctions gap (GJP) Jonction gap annulaire (GJA) |
| url | https://doi.org/10.1186/s12610-023-00194-y |
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