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Cited by 260Cellular transport and secretionExtracellular vesicles in diseaseCaveolin-1 and cellular processes

The enterocyte microvillus is a vesicle-generating organelle

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McConnell, Russell E., Higginbotham, James N., Shifrin, David A., Tabb, David L., Coffey, Robert J., Tyska, Matthew J.·2009·Journal of Cell Biology
DOI 10.1083/jcb.200902147PMC PMC2712962
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Abstract

For decades, enterocyte brush border microvilli have been viewed as passive cytoskeletal scaffolds that serve to increase apical membrane surface area. However, recent studies revealed that in the in vitro context of isolated brush borders, myosin-1a (myo1a) powers the sliding of microvillar membrane along core actin bundles. This activity also leads to the shedding of small vesicles from microvillar tips, suggesting that microvilli may function as vesicle-generating organelles in vivo. In this study, we present data in support of this hypothesis, showing that enterocyte microvilli release unilamellar vesicles into the intestinal lumen; these vesicles retain the right side out orientation of microvillar membrane, contain catalytically active brush border enzymes, and are specifically enriched in intestinal alkaline phosphatase. Moreover, myo1a knockout mice demonstrate striking perturbations in vesicle production, clearly implicating this motor in the in vivo regulation of this novel activity. In combination, these data show that microvilli function as vesicle-generating organelles, which enable enterocytes to deploy catalytic activities into the intestinal lumen.

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  • Microvesicle formation involves phosphatidylserine translocation to the outer membrane leaflet and completion by actin-myosin cytoskeletal contraction.

    “Membrane budding/vesicle formation is induced by translocation of phosphatidylserine to the outer-membrane leaflet [62, 65]. The budding process is completed through contraction of cytoskeletal structures by actin-myosin interactions [66, 67].”

    From Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies (2013) · cites this paper as [67]

    The citation is attached to the sentence about actin–myosin interactions. The Introduction describes myosin-1a moving microvillar membrane over actin bundles and vesicles shedding from the tips, but the Discussion (‘Myo1a is required for proper LV production’; page unavailable) says its precise role in vesicle formation and release remains unclear. It does not establish that cytoskeletal contraction completes budding. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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References 70 · Cited by 260

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Authors
McConnell, R. E., Higginbotham, J. N., Shifrin, D. A., Tabb, D. L., Coffey, R. J., & Tyska, M. J.
Affiliations
United States Department of Veterans Affairs (US)
Corresponding author
Tyska, Matthew J.
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2009-06-29
Volume
185
Issue
7
Pages
1285-1298
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.200902147
PMC
PMC2712962
OpenAlex
W2146134298
Cited by
260
References
70
Citations by year
2026: 3 · 2025: 12 · 2024: 27 · 2023: 19 · 2022: 13 · 2021: 15 · 2020: 26 · 2019: 25 · 2018: 21 · 2017: 9 · 2016: 12 · 2015: 13 · 2014: 14 · 2013: 15 · 2012: 13
FWCI
5.34
Type
journal article
Language
en
Open access
Licence
cc-by-nc-sa
Locations
  • The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5r01ca126218-05)
  • U.S. Public Health Service (U01 084239, P50 95103)
  • National Cancer Institute (CA46413, R01-CA-126218, P50CA095103, CA-126218, R01CA163563, R01CA046413)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK075555, DK075555, P30DK058404)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007502)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
Keywords
brush border, vesicle shedding, microvillar membrane, intestinal alkaline phosphatase, brush border enzymes, membrane trafficking, intestinal lumen, actin bundles
MeSH terms
Alkaline Phosphatase, Animals, Cell Membrane, Isoenzymes, Microvilli, Organelles, Cell Polarity, Rats, Sprague-Dawley, Mice, Knockout, Myosin Heavy Chains, Enterocytes, Mice, Rats, Unilamellar Liposomes

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