Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain
Defects in membrane repair contribute to the development of some muscular dystrophies, highlighting the importance to decipher the membrane repair mechanisms in human skeletal muscle. In murine myofibers, the formation of a cap subdomain composed notably by annexins (Anx) is critical for membrane re...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2020-07-01
|
| Series: | Cells |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2073-4409/9/7/1742 |
| _version_ | 1797561795609624576 |
|---|---|
| author | Coralie Croissant Céline Gounou Flora Bouvet Sisareuth Tan Anthony Bouter |
| author_facet | Coralie Croissant Céline Gounou Flora Bouvet Sisareuth Tan Anthony Bouter |
| author_sort | Coralie Croissant |
| collection | DOAJ |
| description | Defects in membrane repair contribute to the development of some muscular dystrophies, highlighting the importance to decipher the membrane repair mechanisms in human skeletal muscle. In murine myofibers, the formation of a cap subdomain composed notably by annexins (Anx) is critical for membrane repair. We applied membrane damage by laser ablation to human skeletal muscle cells and assessed the behavior of annexin-A6 (AnxA6) tagged with GFP by correlative light and electron microscopy (CLEM). We show that AnxA6 was recruited to the site of membrane injury within a few seconds after membrane injury. In addition, we show that the deficiency in AnxA6 compromises human sarcolemma repair, demonstrating the crucial role played by AnxA6 in this process. An AnxA6-containing cap-subdomain was formed in damaged human myotubes in about one minute. Through transmission electron microscopy (TEM), we observed that extension of the sarcolemma occurred during membrane resealing, which participated in forming a dense lipid structure in order to plug the hole. By properties of membrane folding and curvature, AnxA6 helped in the formation of this tight structure. The compaction of intracellular membranes—which are used for membrane resealing and engulfed in extensions of the sarcolemma—may also facilitate elimination of the excess of lipid and protein material once cell membrane has been repaired. These data reinforce the role played by AnxA6 and the cap subdomain in membrane repair of skeletal muscle cells. |
| first_indexed | 2024-03-10T18:19:42Z |
| format | Article |
| id | doaj.art-449c5b4091cd44d59ec1f9f2087920e1 |
| institution | Directory Open Access Journal |
| issn | 2073-4409 |
| language | English |
| last_indexed | 2024-03-10T18:19:42Z |
| publishDate | 2020-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cells |
| spelling | doaj.art-449c5b4091cd44d59ec1f9f2087920e12023-11-20T07:25:56ZengMDPI AGCells2073-44092020-07-0197174210.3390/cells9071742Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap SubdomainCoralie Croissant0Céline Gounou1Flora Bouvet2Sisareuth Tan3Anthony Bouter4Institute of Chemistry and Biology of Membranes and Nano-objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, FranceInstitute of Chemistry and Biology of Membranes and Nano-objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, FranceInstitute of Chemistry and Biology of Membranes and Nano-objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, FranceInstitute of Chemistry and Biology of Membranes and Nano-objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, FranceInstitute of Chemistry and Biology of Membranes and Nano-objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, FranceDefects in membrane repair contribute to the development of some muscular dystrophies, highlighting the importance to decipher the membrane repair mechanisms in human skeletal muscle. In murine myofibers, the formation of a cap subdomain composed notably by annexins (Anx) is critical for membrane repair. We applied membrane damage by laser ablation to human skeletal muscle cells and assessed the behavior of annexin-A6 (AnxA6) tagged with GFP by correlative light and electron microscopy (CLEM). We show that AnxA6 was recruited to the site of membrane injury within a few seconds after membrane injury. In addition, we show that the deficiency in AnxA6 compromises human sarcolemma repair, demonstrating the crucial role played by AnxA6 in this process. An AnxA6-containing cap-subdomain was formed in damaged human myotubes in about one minute. Through transmission electron microscopy (TEM), we observed that extension of the sarcolemma occurred during membrane resealing, which participated in forming a dense lipid structure in order to plug the hole. By properties of membrane folding and curvature, AnxA6 helped in the formation of this tight structure. The compaction of intracellular membranes—which are used for membrane resealing and engulfed in extensions of the sarcolemma—may also facilitate elimination of the excess of lipid and protein material once cell membrane has been repaired. These data reinforce the role played by AnxA6 and the cap subdomain in membrane repair of skeletal muscle cells.https://www.mdpi.com/2073-4409/9/7/1742annexin-A6membrane repairhuman skeletal musclecap subdomainfluorescenceelectron microscopy |
| spellingShingle | Coralie Croissant Céline Gounou Flora Bouvet Sisareuth Tan Anthony Bouter Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain Cells annexin-A6 membrane repair human skeletal muscle cap subdomain fluorescence electron microscopy |
| title | Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain |
| title_full | Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain |
| title_fullStr | Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain |
| title_full_unstemmed | Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain |
| title_short | Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain |
| title_sort | annexin a6 in membrane repair of human skeletal muscle cell a role in the cap subdomain |
| topic | annexin-A6 membrane repair human skeletal muscle cap subdomain fluorescence electron microscopy |
| url | https://www.mdpi.com/2073-4409/9/7/1742 |
| work_keys_str_mv | AT coraliecroissant annexina6inmembranerepairofhumanskeletalmusclecellaroleinthecapsubdomain AT celinegounou annexina6inmembranerepairofhumanskeletalmusclecellaroleinthecapsubdomain AT florabouvet annexina6inmembranerepairofhumanskeletalmusclecellaroleinthecapsubdomain AT sisareuthtan annexina6inmembranerepairofhumanskeletalmusclecellaroleinthecapsubdomain AT anthonybouter annexina6inmembranerepairofhumanskeletalmusclecellaroleinthecapsubdomain |