Intercellular adhesion boots collective cell migration through elevated membrane tension
Abstract In multicellular systems, the migration pattern of individual cells critically relies on the interactions with neighboring cells. Depending on the strength of these interactions, cells either move as a collective, as observed during morphogenesis and wound healing, or migrate individually,...
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| Format: | Article |
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Nature Portfolio
2025-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56941-4 |
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| author | Brent M. Bijonowski Jongkwon Park Martin Bergert Christina Teubert Alba Diz-Muñoz Milos Galic Seraphine V. Wegner |
| author_facet | Brent M. Bijonowski Jongkwon Park Martin Bergert Christina Teubert Alba Diz-Muñoz Milos Galic Seraphine V. Wegner |
| author_sort | Brent M. Bijonowski |
| collection | DOAJ |
| description | Abstract In multicellular systems, the migration pattern of individual cells critically relies on the interactions with neighboring cells. Depending on the strength of these interactions, cells either move as a collective, as observed during morphogenesis and wound healing, or migrate individually, as it is the case for immune cells and fibroblasts. Mediators of cell-cell adhesions, such as cadherins coordinate collective dynamics by linking the cytoskeleton of neighboring cells. However, whether intercellular binding alone triggers signals that originate from within the plasma membrane itself, remains unclear. Here, we address this question through artificial photoswitchable cell-cell adhesions that selectively connect adjacent plasma membranes without linking directly to cytoskeletal elements. We find that these intercellular adhesions are sufficient to achieve collective cell migration. Linking adjacent cells increases membrane tension, which activates the enzyme phospholipase D2. The resulting increase in phosphatidic acid, in turn, stimulates the mammalian target of rapamycin, a known actuator of collective cell migration. Collectively, these findings introduce a membrane-based signaling axis as promotor of collective cell dynamics, which is independent of the direct coupling of cell-cell adhesions to the cytoskeleton. |
| format | Article |
| id | doaj-art-ed2faa25d62f484193409ad56d7dbb42 |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-ed2faa25d62f484193409ad56d7dbb422025-08-20T02:48:27ZengNature PortfolioNature Communications2041-17232025-02-0116111410.1038/s41467-025-56941-4Intercellular adhesion boots collective cell migration through elevated membrane tensionBrent M. Bijonowski0Jongkwon Park1Martin Bergert2Christina Teubert3Alba Diz-Muñoz4Milos Galic5Seraphine V. Wegner6Institute of Physiological Chemistry and Pathobiochemistry, University of MünsterInstitute of Physiological Chemistry and Pathobiochemistry, University of MünsterCell Biology and Biophysics Unit, European Molecular Biology LaboratoryInstitute of Medical Physics and Biophysics, University of MünsterCell Biology and Biophysics Unit, European Molecular Biology LaboratoryInstitute of Medical Physics and Biophysics, University of MünsterInstitute of Physiological Chemistry and Pathobiochemistry, University of MünsterAbstract In multicellular systems, the migration pattern of individual cells critically relies on the interactions with neighboring cells. Depending on the strength of these interactions, cells either move as a collective, as observed during morphogenesis and wound healing, or migrate individually, as it is the case for immune cells and fibroblasts. Mediators of cell-cell adhesions, such as cadherins coordinate collective dynamics by linking the cytoskeleton of neighboring cells. However, whether intercellular binding alone triggers signals that originate from within the plasma membrane itself, remains unclear. Here, we address this question through artificial photoswitchable cell-cell adhesions that selectively connect adjacent plasma membranes without linking directly to cytoskeletal elements. We find that these intercellular adhesions are sufficient to achieve collective cell migration. Linking adjacent cells increases membrane tension, which activates the enzyme phospholipase D2. The resulting increase in phosphatidic acid, in turn, stimulates the mammalian target of rapamycin, a known actuator of collective cell migration. Collectively, these findings introduce a membrane-based signaling axis as promotor of collective cell dynamics, which is independent of the direct coupling of cell-cell adhesions to the cytoskeleton.https://doi.org/10.1038/s41467-025-56941-4 |
| spellingShingle | Brent M. Bijonowski Jongkwon Park Martin Bergert Christina Teubert Alba Diz-Muñoz Milos Galic Seraphine V. Wegner Intercellular adhesion boots collective cell migration through elevated membrane tension Nature Communications |
| title | Intercellular adhesion boots collective cell migration through elevated membrane tension |
| title_full | Intercellular adhesion boots collective cell migration through elevated membrane tension |
| title_fullStr | Intercellular adhesion boots collective cell migration through elevated membrane tension |
| title_full_unstemmed | Intercellular adhesion boots collective cell migration through elevated membrane tension |
| title_short | Intercellular adhesion boots collective cell migration through elevated membrane tension |
| title_sort | intercellular adhesion boots collective cell migration through elevated membrane tension |
| url | https://doi.org/10.1038/s41467-025-56941-4 |
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