Defective membrane repair machinery impairs survival of invasive cancer cells

Bouvet, Flora; Ros, Manon; Bonedeau, E.; Croissant, Coralie; Frelin, Léo; Saltel, Frédéric; Moreau, Violaine; Bouter, Anthony

doi:10.1101/2020.04.20.050211

Cited by 8 publications

(12 citation statements)

References 67 publications

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“…Sarcolemma repair assay was performed by laser ablation in the presence of Ca 2+ and FM1-43, as previously described [ 32 , 33 ]. By analyzing changes in the FM1-43 intracellular fluorescence intensity, we first confirmed that LHCN myotubes are able to reseal a µm-size membrane damage in about 80 s ( Figure 2 A,C) as previously reported [ 26 ].…”

Section: Resultsmentioning

confidence: 99%

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Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain

Croissant

Gounou

Bouvet

et al. 2020

Cells

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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.

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Section: Resultsmentioning

confidence: 99%

“…Membrane repair was assayed as recently reported [ 32 ], according to a protocol that differed slightly from our previous studies [ 26 , 33 ]. Myotubes were cultured in complete growth medium on 18*18-mm glass coverslips (Nunc).…”

Section: Methodsmentioning

confidence: 99%

Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain

Croissant

Gounou

Bouvet

et al. 2020

Cells

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“…This allows us to test the cellular response to PM ruptures of nanoscopic dimensions in both cells and model membranes. Nanoscopic holes may be frequent during aggressive cellular migration and invasion 1,17 and therefore investigation of protein recruitment in response to nanoscopic ruptures are relevant for understanding how living cells cope with ruptures.…”

Section: Resultsmentioning

confidence: 99%

Thermoplasmonic nano-rupture of cells reveals Annexin V function in plasma membrane repair

Moreno-Pescador

Aswad

Florentsen

et al. 2021

Preprint

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Maintaining the integrity of the cell plasma membrane (PM) is critical for the survival of cells. While an efficient PM repair machinery can aid survival of healthy cells by preventing influx of extracellular calcium, it can also constitute an obstacle in drug delivery and photothermal therapy. We show how nanoscopic holes can be applied to the cell surface thus allowing identification of molecular components with a pivotal role in PM repair. Cells are punctured by locally heating gold nanostructures at the cell surface which causes nano-ruptures in cellular PMs. Recruitment of annexin V near the hole is found to locally reshape the ruptured plasma membrane. Experiments using model membranes, containing recombinant annexin V, provide further biophysical insight into the ability of annexin V to reshape edges surrounding a membrane hole. The thermoplasmonic method provides a general strategy to monitor the response to nanoscopic injuries to the cell surface.

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“…This study echoes a work which demonstrates that during the migration along type I collagen fibers, MDA-MB-231 cells undergo membrane damage during this process. These membrane lesions are repaired by the concomitant action of annexins 5 and 6 49 . One hypothesis is that these tracks could originate from membrane lesions due to a too strong adhesion to the matrix during tumor cell migration.…”

Section: Discussionmentioning

confidence: 99%

Cancer cells transfer invasive properties through tracks, a novel collagen-associated extracellular vesicle entity

Normand¹,

Rouyer

Di-Tommaso

et al. 2022

Preprint

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Metastasis is the leading cause of cancer-related deaths. During this process, tumor cells acquire invasive and migratory capacities in order to invade the surrounding tissues. To achieve this, the tumor microenvironment including the extracellular matrix (ECM) is altered to facilitate cancer cell proliferation and dissemination. Extracellular vesicles (EVs), such as exosomes or migrasomes, are already known to induce pro-tumor features such as migration, promoting tumor development and metastasis formation. Here we highlight a new type of EVs, referred as tracks, released by cancer cells during migration and specifically attached along collagen fibers. These tracks, identified by discoidin receptor 1 (DDR1) enrichment, are promoted when cell-ECM interactions are increased, such as in tumors. We characterized these tracks, their ultrastructure as well as their molecular composition in terms of proteins and nucleic acids, showing that they are different from classical EVs known so far. Moreover, these tracks are very stable structures and can be internalized by surrounding cells. After internalization, they modify the differentiation status and the phenotype of recipient cells, promoting epithelial to mesenchymal transition, matrix degradation and invasion. Thus, we identified a new class of collagen-associated EVs, tracks, that play a role in cell-cell communication by transferring invasive properties. Consequently, these cancer-related tracks could be a new player in the tumor invasion process.

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Defective membrane repair machinery impairs survival of invasive cancer cells

Cited by 8 publications

References 67 publications

Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain

Annexin-A6 in Membrane Repair of Human Skeletal Muscle Cell: A Role in the Cap Subdomain

Thermoplasmonic nano-rupture of cells reveals Annexin V function in plasma membrane repair

Cancer cells transfer invasive properties through tracks, a novel collagen-associated extracellular vesicle entity

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