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Membrane Dynamics During Cellular Wound Repair

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Journal Mol Biol Cell
Date 2016 May 27
PMID 27226483
Citations 63
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Abstract

Cells rapidly reseal after damage, but how they do so is unknown. It has been hypothesized that resealing occurs due to formation of a patch derived from rapid fusion of intracellular compartments at the wound site. However, patching has never been directly visualized. Here we study membrane dynamics in wounded Xenopus laevis oocytes at high spatiotemporal resolution. Consistent with the patch hypothesis, we find that damage triggers rampant fusion of intracellular compartments, generating a barrier that limits influx of extracellular dextrans. Patch formation is accompanied by compound exocytosis, local accumulation and aggregation of vesicles, and rupture of compartments facing the external environment. Subcellular patterning is evident as annexin A1, dysferlin, diacylglycerol, active Rho, and active Cdc42 are recruited to compartments confined to different regions around the wound. We also find that a ring of elevated intracellular calcium overlaps the region where membrane dynamics are most evident and persists for several minutes. The results provide the first direct visualization of membrane patching during membrane repair, reveal novel features of the repair process, and show that a remarkable degree of spatial patterning accompanies damage-induced membrane dynamics.

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References
1.
McNeil P, Vogel S, Miyake K, Terasaki M . Patching plasma membrane disruptions with cytoplasmic membrane. J Cell Sci. 2000; 113 ( Pt 11):1891-902. DOI: 10.1242/jcs.113.11.1891. View

2.
Ziv N, Spira M . Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J Neurophysiol. 1995; 74(6):2625-37. DOI: 10.1152/jn.1995.74.6.2625. View

3.
Bement W . Signal transduction by calcium and protein kinase C during egg activation. J Exp Zool. 1992; 263(4):382-97. DOI: 10.1002/jez.1402630406. View

4.
Ponomareva O, Eliceiri K, Halloran M . Charcot-Marie-Tooth 2b associated Rab7 mutations cause axon growth and guidance defects during vertebrate sensory neuron development. Neural Dev. 2016; 11:2. PMC: 4721196. DOI: 10.1186/s13064-016-0058-x. View

5.
Idone V, Tam C, Goss J, Toomre D, Pypaert M, Andrews N . Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J Cell Biol. 2008; 180(5):905-14. PMC: 2265401. DOI: 10.1083/jcb.200708010. View