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Journal of Cell Science 114, 3487-3494 (2001)
© 2001 The Company of Biologists Limited

RESEARCH ARTICLE

An actin barrier to resealing

Katsuya Miyake1,*,{ddagger}, Paul L. McNeil2,{ddagger}, Kazunori Suzuki1, Rikiya Tsunoda1 and Naonori Sugai1

1 Second Department of Anatomy, School of Medicine, Fukushima Medical University, Fukushima 960-1295, Japan
2 Institute of Molecular Medicine and Genetics, Department of Cellular Biology and Anatomy, The Medical College of Georgia, Augusta, GA 30912-2000, USA
* Present address: Institute of Molecular Medicine and Genetics, Department of Cellular Biology and Anatomy, The Medical College of Georgia, Augusta, GA 30912-2000, USA

{ddagger}Author for correspondence (e-mail: kmiyake{at}mail.mcg.edu; pmcneil{at}mail.mcg.edu)

Accepted June 20, 2001

Plasma membrane disruption is a common form of cell injury in many normal biological environments, including many mammalian tissues. Survival depends on the initiation of a rapid resealing response that is mounted only in the presence of physiological levels of extracellular Ca2+. Vesicle-vesicle and vesicle-plasma membrane fusion events occurring in cortical cytoplasm surrounding the defect are thought to be a crucial element of the resealing mechanism. However, in mammalian cells, the vesicles used in this fusion reaction (endosomes/lysosomes) are not present in a ‘pre-docked’ configuration and so must be brought into physical contact with one another and with the plasma membrane. We propose that a requisite prelude to fusion is the disassembly in local cell cortex of the physical barrier constituted by filamentous actin. Consistent with this hypothesis, we found that rat gastric epithelial (RGM1) cell cortical staining with phalloidin was apparently reduced at presumptive disruption sites. Moreover, flow cytofluorometric analysis of wounded RGM1 populations revealed a small, but significant, Ca2+-dependent reduction in whole cell phalloidin staining. The functional significance of this disruption-induced depolymerization response was confirmed in several independent tests. Introduction into RGM1 cells of the filamentous actin-depolymerizing agent, DNase1, enhanced resealing, although cytochalasin treatment, by itself, had no effect. By contrast, when the filamentous actin cytoskeleton was stabilized experimentally, using phalloidin or jasplakinolide, resealing was strongly inhibited. Cells in wounded cultures displayed an enhanced cortical array of filamentous actin, and resealing by such cells was enhanced strongly by both cytochalasin and DNase 1, demonstrating the specific reversibility of a biologically mediated, polymerization-induced inhibition of resealing. We conclude that localized filamentous actin disassembly removes a cortical barrier standing in the way of membrane-membrane contacts leading to resealing-requisite homotypic and exocytotic fusion events.

Key words: Plasma membrane, Disruption, Resealing, Exocytosis, Actin


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