{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T01:39:07Z","timestamp":1792287547792,"version":"4.4.0"},"reference-count":39,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2022,1,26]],"date-time":"2022-01-26T00:00:00Z","timestamp":1643155200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007393","name":"French Muscular Dystrophy Association","doi-asserted-by":"publisher","award":["17140"],"award-info":[{"award-number":["17140"]}],"id":[{"id":"10.13039\/100007393","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007393","name":"French Muscular Dystrophy Association","doi-asserted-by":"publisher","award":["22442"],"award-info":[{"award-number":["22442"]}],"id":[{"id":"10.13039\/100007393","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007393","name":"French Muscular Dystrophy Association","doi-asserted-by":"publisher","award":["20491"],"award-info":[{"award-number":["20491"]}],"id":[{"id":"10.13039\/100007393","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Membranes"],"abstract":"<jats:p>Defects in membrane repair contribute to the development of muscular dystrophies, such as Miyoshi muscular dystrophy 1, limb girdle muscular dystrophy (LGMD), type R2 or R12. Deciphering membrane repair dysfunctions in the development of muscular dystrophies requires precise and detailed knowledge of the membrane repair machinery in healthy human skeletal muscle cells. Using correlative light and electron microscopy (CLEM), we studied the trafficking of four members of the annexin (ANX) family, in myotubes damaged by laser ablation. Our data support a model in which ANXA4 and ANXA6 are recruited to the disruption site by propagating as a wave-like motion along the sarcolemma. They may act in membrane resealing by proceeding to sarcolemma remodeling. On the other hand, ANXA1 and A2 exhibit a progressive cytoplasmic recruitment, likely by interacting with intracellular vesicles, in order to form the lipid patch required for membrane resealing. Once the sarcolemma has been resealed, ANXA1 is released from the site of the membrane injury and returns to the cytosol, while ANXA2 remains accumulated close to the wounding site on the cytoplasmic side. On the other side of the repaired sarcolemma are ANXA4 and ANXA6 that face the extracellular milieu, where they are concentrated in a dense structure, the cap subdomain. The proposed model provides a basis for the identification of cellular dysregulations in the membrane repair of dystrophic human muscle cells.<\/jats:p>","DOI":"10.3390\/membranes12020153","type":"journal-article","created":{"date-parts":[[2022,1,26]],"date-time":"2022-01-26T11:02:53Z","timestamp":1643194973000},"page":"153","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Trafficking of Annexins during Membrane Repair in Human Skeletal Muscle Cells"],"prefix":"10.3390","volume":"12","author":[{"given":"Coralie","family":"Croissant","sequence":"first","affiliation":[{"name":"Institute of Chemistry and Biology of Membranes and Nano-Objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C\u00e9line","family":"Gounou","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biology of Membranes and Nano-Objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Flora","family":"Bouvet","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biology of Membranes and Nano-Objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sisareuth","family":"Tan","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biology of Membranes and Nano-Objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony","family":"Bouter","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biology of Membranes and Nano-Objects, UMR 5248, CNRS, University of Bordeaux, IPB, F-33600 Pessac, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,1,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1146\/annurev.cellbio.19.111301.140101","article-title":"Plasma membrane disruption: Repair, prevention, adaptation","volume":"19","author":"McNeil","year":"2003","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1152\/physiol.00019.2015","article-title":"Plasma membrane repair: A central process for maintaining cellular homeostasis","volume":"30","author":"Blazek","year":"2015","journal-title":"Physiology"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Croissant, C., Carmeille, R., Br\u00e9vart, C., and Bouter, A. (2021). Annexins and membrane repair dysfunctions in muscular dystrophies. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22105276"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2631","DOI":"10.1242\/jcs.01245","article-title":"Annexins--unique membrane binding proteins with diverse functions","volume":"117","author":"Rescher","year":"2004","journal-title":"J. Cell Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1146\/annurev.bb.23.060194.001205","article-title":"Annexin structure and membrane interactions: A molecular perspective","volume":"23","author":"Swairjo","year":"1994","journal-title":"Annu. Rev. Biophys. Biomol. Struct."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"35202","DOI":"10.1074\/jbc.M606406200","article-title":"Requirement for annexin A1 in plasma membrane repair","volume":"281","author":"McNeil","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3795","DOI":"10.1038\/ncomms4795","article-title":"S100A11 is required for efficient plasma membrane repair and survival of invasive cancer cells","volume":"5","author":"Jaiswal","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1038\/s41467-017-01743-6","article-title":"Annexin A4 and A6 induce membrane curvature and constriction during cell membrane repair","volume":"8","author":"Boye","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6726","DOI":"10.1038\/s41598-019-43143-4","article-title":"Annexin A7 is required for ESCRT III-mediated plasma membrane repair","volume":"9","author":"Boye","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1046","DOI":"10.1016\/j.bbamcr.2016.12.007","article-title":"Annexin A2 is involved in Ca2+-dependent plasma membrane repair in primary human endothelial cells","volume":"1864","author":"Koerdt","year":"2017","journal-title":"Biochim. Biophys. Acta-Mol. Cell Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1016\/j.bbamcr.2014.12.038","article-title":"Annexin-A5 promotes membrane resealing in human trophoblasts","volume":"1853","author":"Carmeille","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/ncomms1270","article-title":"Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair","volume":"2","author":"Bouter","year":"2011","journal-title":"Nat. Commun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"50466","DOI":"10.1074\/jbc.M307247200","article-title":"Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing","volume":"278","author":"Lennon","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/j.devcel.2011.12.008","article-title":"In vivo imaging of molecular interactions at damaged sarcolemma","volume":"22","author":"Roostalu","year":"2012","journal-title":"Dev. Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2267","DOI":"10.1016\/j.bbamcr.2016.06.003","article-title":"Membrane repair of human skeletal muscle cells requires Annexin-A5","volume":"1863","author":"Carmeille","year":"2016","journal-title":"Biochim. Biophys. Acta-Mol. Cell Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1083\/jcb.201512022","article-title":"An actin-dependent annexin complex mediates plasma membrane repair in muscle","volume":"213","author":"Demonbreun","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Croissant, C., Gounou, C., Bouvet, F., Tan, S., and Bouter, A. (2020). Annexin-A6 in membrane repair of human skeletal muscle cell: A role in the cap subdomain. Cells, 9.","DOI":"10.3390\/cells9071742"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Bittel, D.C., Chandra, G., Tirunagri, L.M.S., Deora, A.B., Medikayala, S., Scheffer, L., Defour, A., and Jaiswal, J.K. (2020). Annexin A2 mediates dysferlin accumulation and muscle cell membrane repair. Cells, 9.","DOI":"10.3390\/cells9091919"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1038\/nature01573","article-title":"Defective membrane repair in dysferlin-deficient muscular dystrophy","volume":"423","author":"Bansal","year":"2003","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1900","DOI":"10.1093\/hmg\/ddw063","article-title":"Defective membrane fusion and repair in Anoctamin5 -deficient muscular dystrophy","volume":"25","author":"Griffin","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1002\/humu.9364","article-title":"Mutation finding in patients with dysferlin deficiency and role of the dysferlin interacting proteins annexin A1 and A2 in muscular dystrophies","volume":"26","author":"Cagliani","year":"2005","journal-title":"Hum. Mutat."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2430","DOI":"10.1038\/s41467-019-10438-z","article-title":"Fibroadipogenic progenitors are responsible for muscle loss in limb girdle muscular dystrophy 2B","volume":"10","author":"Hogarth","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1002\/path.4301","article-title":"Macrophage activation and skeletal muscle healing following traumatic injury","volume":"232","author":"Novak","year":"2014","journal-title":"J. Pathol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1111\/j.1474-9726.2007.00306.x","article-title":"Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: Consequences in aging muscle and therapeutic strategies for muscular dystrophies","volume":"6","author":"Zhu","year":"2007","journal-title":"Aging Cell"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"9862","DOI":"10.1364\/OE.21.009862","article-title":"How to display data by color schemes compatible with red-green color perception deficiencies","volume":"21","author":"Geissbuehler","year":"2013","journal-title":"Opt. Express"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"21821","DOI":"10.1038\/s41598-020-77902-5","article-title":"Defective membrane repair machinery impairs survival of invasive cancer cells","volume":"10","author":"Bouvet","year":"2020","journal-title":"Sci Rep"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1096\/fj.02-0070com","article-title":"Modulating signaling events in smooth muscle: Cleavage of annexin 2 abolishes its binding to lipid rafts","volume":"16","author":"Babiychuk","year":"2002","journal-title":"FASEB J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"308976","DOI":"10.1155\/2014\/308976","article-title":"Annexin A2: Its molecular regulation and cellular expression in cancer development","volume":"2014","author":"Wang","year":"2014","journal-title":"Dis. Markers"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2515","DOI":"10.1016\/j.bbagen.2017.08.024","article-title":"Protein phosphorylation and its role in the regulation of Annexin A2 function","volume":"1861","author":"Grindheim","year":"2017","journal-title":"Biochim. Biophys. Acta-Gen. Subj."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1016\/j.bbamcr.2018.12.013","article-title":"Phosphorylation cycling of Annexin A2 Tyr23 is critical for calcium-regulated exocytosis in neuroendocrine cells","volume":"1866","author":"Gabel","year":"2019","journal-title":"Biochim. Biophys. Acta-Mol. Cell Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1002\/jcp.22178","article-title":"Role of Annexin A1 in mouse myoblast cell differentiation","volume":"224","author":"Bizzarro","year":"2010","journal-title":"J. Cell. Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1016\/j.yexcr.2007.11.015","article-title":"Heterogeneity and timing of translocation and membrane-mediated assembly of different annexins","volume":"314","author":"Skrahina","year":"2008","journal-title":"Exp. Cell Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3318","DOI":"10.1091\/mbc.e06-01-0041","article-title":"Annexin A4 self-association modulates general membrane protein mobility in living cells","volume":"17","author":"Schultz","year":"2006","journal-title":"Mol. Biol. Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1038\/ncb1812","article-title":"MG53 nucleates assembly of cell membrane repair machinery","volume":"11","author":"Cai","year":"2009","journal-title":"Nat. Cell Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4192","DOI":"10.1021\/bi002507s","article-title":"Phosphorylation mutants elucidate the mechanism of annexin IV-mediated membrane aggregation","volume":"40","author":"Kaetzel","year":"2001","journal-title":"Biochemistry"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e55","DOI":"10.1002\/cpcb.55","article-title":"Imaging Membrane Repair in Single Cells Using Correlative Light and Electron Microscopy","volume":"81","author":"Croissant","year":"2018","journal-title":"Curr. Protoc. Cell Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4339","DOI":"10.1091\/mbc.11.12.4339","article-title":"A Decrease in Membrane Tension Precedes Successful Cell-Membrane Repair","volume":"11","author":"Togo","year":"2000","journal-title":"Mol. Biol. Cell"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"10309","DOI":"10.1038\/s41598-018-28481-z","article-title":"Annexins induce curvature on free-edge membranes displaying distinct morphologies","volume":"8","author":"Boye","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"12875","DOI":"10.1038\/ncomms12875","article-title":"Dysferlin-mediated phosphatidylserine sorting engages macrophages in sarcolemma repair","volume":"7","author":"Middel","year":"2016","journal-title":"Nat. Commun."}],"container-title":["Membranes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/2\/153\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:08:26Z","timestamp":1760134106000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/2\/153"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,26]]},"references-count":39,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["membranes12020153"],"URL":"https:\/\/doi.org\/10.3390\/membranes12020153","relation":{},"ISSN":["2077-0375"],"issn-type":[{"value":"2077-0375","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,26]]}}}