Microvilli are actin-rich membrane protrusions common to a variety of epithelial cell types. Within microvilli of the enterocyte brush border (BB), myosin-1a (Myo1a) forms an ordered ensemble of bridges that link the plasma membrane to the underlying polarized actin bundle. Despite decades of investigation, the function of this unique actomyosin array has remained unclear. Here, we show that addition of ATP to isolated BBs induces a plus end–directed translation of apical membrane along microvillar actin bundles. Upon reaching microvillar tips, membrane is “shed” into solution in the form of small vesicles. Because this movement demonstrates the polarity, velocity, and nucleotide dependence expected for a Myo1a-driven process, and BBs lacking Myo1a fail to undergo membrane translation, we conclude that Myo1a powers this novel form of motility. Thus, in addition to providing a means for amplifying apical surface area, we propose that microvilli function as actomyosin contractile arrays that power the release of BB membrane vesicles into the intestinal lumen.
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21 May 2007
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May 14 2007
Myosin-1a powers the sliding of apical membrane along microvillar actin bundles
Russell E. McConnell,
Russell E. McConnell
Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232
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Matthew J. Tyska
Matthew J. Tyska
Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232
Search for other works by this author on:
Russell E. McConnell
Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232
Matthew J. Tyska
Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232
Correspondence to Matthew J. Tyska: [email protected]
Abbreviations used in this paper: AP, alkaline phosphatase; BB, brush border; KO, knock-out; MSA, membrane shedding assay; Myo1a, myosin-1a; Myo2, myosin-II; SDCM, spinning disk confocal microscopy; SI, sucrase isomaltase; TEM, transmission electron microscopy; WT, wild type.
Received:
March 07 2007
Accepted:
April 18 2007
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2007
J Cell Biol (2007) 177 (4): 671–681.
Article history
Received:
March 07 2007
Accepted:
April 18 2007
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Russell E. McConnell, Matthew J. Tyska; Myosin-1a powers the sliding of apical membrane along microvillar actin bundles . J Cell Biol 21 May 2007; 177 (4): 671–681. doi: https://doi.org/10.1083/jcb.200701144
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