Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2
Abstract Glioblastoma (GBM) is a malignant brain tumor with diffuse infiltration. Here, we demonstrate how GBM cells usurp guidance receptor Plexin-B2 for confined migration through restricted space. Using live-cell imaging to track GBM cells negotiating microchannels, we reveal endocytic vesicle ac...
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55056-6 |
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| author | Chrystian Junqueira Alves Theodore Hannah Sita Sadia Christy Kolsteeg Angela Dixon Robert J. Wiener Ha Nguyen Murray J. Tipping Júlia Silva Ladeira Paula Fernandes da Costa Franklin Nathália de Paula Dutra de Nigro Rodrigo Alves Dias Priscila V. Zabala Capriles José P. Rodrigues Furtado de Mendonça Paul A. Slesinger Kevin D. Costa Hongyan Zou Roland H. Friedel |
| author_facet | Chrystian Junqueira Alves Theodore Hannah Sita Sadia Christy Kolsteeg Angela Dixon Robert J. Wiener Ha Nguyen Murray J. Tipping Júlia Silva Ladeira Paula Fernandes da Costa Franklin Nathália de Paula Dutra de Nigro Rodrigo Alves Dias Priscila V. Zabala Capriles José P. Rodrigues Furtado de Mendonça Paul A. Slesinger Kevin D. Costa Hongyan Zou Roland H. Friedel |
| author_sort | Chrystian Junqueira Alves |
| collection | DOAJ |
| description | Abstract Glioblastoma (GBM) is a malignant brain tumor with diffuse infiltration. Here, we demonstrate how GBM cells usurp guidance receptor Plexin-B2 for confined migration through restricted space. Using live-cell imaging to track GBM cells negotiating microchannels, we reveal endocytic vesicle accumulation at cell front and filamentous actin assembly at cell rear in a polarized manner. These processes are interconnected and require Plexin-B2 signaling. We further show that Plexin-B2 governs membrane tension and other membrane features such as endocytosis, phospholipid composition, and inner leaflet surface charge, thus providing biophysical mechanisms by which Plexin-B2 promotes GBM invasion. Together, our studies unveil how GBM cells regulate membrane tension and mechano-electrical coupling to adapt to physical constraints and achieve polarized confined migration. |
| format | Article |
| id | doaj-art-a45b6ec52cff474eaeb56ad3ec9d0037 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-a45b6ec52cff474eaeb56ad3ec9d00372025-01-05T12:41:06ZengNature PortfolioNature Communications2041-17232025-01-0116112010.1038/s41467-024-55056-6Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2Chrystian Junqueira Alves0Theodore Hannah1Sita Sadia2Christy Kolsteeg3Angela Dixon4Robert J. Wiener5Ha Nguyen6Murray J. Tipping7Júlia Silva Ladeira8Paula Fernandes da Costa Franklin9Nathália de Paula Dutra de Nigro10Rodrigo Alves Dias11Priscila V. Zabala Capriles12José P. Rodrigues Furtado de Mendonça13Paul A. Slesinger14Kevin D. Costa15Hongyan Zou16Roland H. Friedel17Nash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiDepartment of Biology, College of Arts and Sciences, Case Western Reserve UniversityCardiovascular Research Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiMolecular Cytology Core Facility, Memorial Sloan Kettering Cancer CenterDepartment of Computer Sciences, Federal University of Juiz de ForaDepartment of Computer Sciences, Federal University of Juiz de ForaDepartment of Computer Sciences, Federal University of Juiz de ForaDepartment of Physics, Federal University of Juiz de ForaDepartment of Computer Sciences, Federal University of Juiz de ForaDepartment of Physics, Federal University of Juiz de ForaNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiCardiovascular Research Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiNash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount SinaiAbstract Glioblastoma (GBM) is a malignant brain tumor with diffuse infiltration. Here, we demonstrate how GBM cells usurp guidance receptor Plexin-B2 for confined migration through restricted space. Using live-cell imaging to track GBM cells negotiating microchannels, we reveal endocytic vesicle accumulation at cell front and filamentous actin assembly at cell rear in a polarized manner. These processes are interconnected and require Plexin-B2 signaling. We further show that Plexin-B2 governs membrane tension and other membrane features such as endocytosis, phospholipid composition, and inner leaflet surface charge, thus providing biophysical mechanisms by which Plexin-B2 promotes GBM invasion. Together, our studies unveil how GBM cells regulate membrane tension and mechano-electrical coupling to adapt to physical constraints and achieve polarized confined migration.https://doi.org/10.1038/s41467-024-55056-6 |
| spellingShingle | Chrystian Junqueira Alves Theodore Hannah Sita Sadia Christy Kolsteeg Angela Dixon Robert J. Wiener Ha Nguyen Murray J. Tipping Júlia Silva Ladeira Paula Fernandes da Costa Franklin Nathália de Paula Dutra de Nigro Rodrigo Alves Dias Priscila V. Zabala Capriles José P. Rodrigues Furtado de Mendonça Paul A. Slesinger Kevin D. Costa Hongyan Zou Roland H. Friedel Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 Nature Communications |
| title | Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 |
| title_full | Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 |
| title_fullStr | Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 |
| title_full_unstemmed | Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 |
| title_short | Invasion of glioma cells through confined space requires membrane tension regulation and mechano-electrical coupling via Plexin-B2 |
| title_sort | invasion of glioma cells through confined space requires membrane tension regulation and mechano electrical coupling via plexin b2 |
| url | https://doi.org/10.1038/s41467-024-55056-6 |
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