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Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy

The glycocalyx is a highly hydrated, glycoprotein-rich coat shrouding many eukaryotic and prokaryotic cells. The intestinal epithelial glycocalyx, comprising glycosylated transmembrane mucins, is part of the primary host-microbe interface and is essential for nutrient absorption. Its disruption has...

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Autores principales: Sun, Willy W., Krystofiak, Evan S., Leo-Macias, Alejandra, Cui, Runjia, Sesso, Antonio, Weigert, Roberto, Ebrahim, Seham, Kachar, Bechara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946683/
https://www.ncbi.nlm.nih.gov/pubmed/31925335
http://dx.doi.org/10.1038/s42003-019-0735-5
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author Sun, Willy W.
Krystofiak, Evan S.
Leo-Macias, Alejandra
Cui, Runjia
Sesso, Antonio
Weigert, Roberto
Ebrahim, Seham
Kachar, Bechara
author_facet Sun, Willy W.
Krystofiak, Evan S.
Leo-Macias, Alejandra
Cui, Runjia
Sesso, Antonio
Weigert, Roberto
Ebrahim, Seham
Kachar, Bechara
author_sort Sun, Willy W.
collection PubMed
description The glycocalyx is a highly hydrated, glycoprotein-rich coat shrouding many eukaryotic and prokaryotic cells. The intestinal epithelial glycocalyx, comprising glycosylated transmembrane mucins, is part of the primary host-microbe interface and is essential for nutrient absorption. Its disruption has been implicated in numerous gastrointestinal diseases. Yet, due to challenges in preserving and visualizing its native organization, glycocalyx structure-function relationships remain unclear. Here, we characterize the nanoarchitecture of the murine enteric glycocalyx using freeze-etching and electron tomography. Micrometer-long mucin filaments emerge from microvillar-tips and, through zigzagged lateral interactions form a three-dimensional columnar network with a 30 nm mesh. Filament-termini converge into globular structures ~30 nm apart that are liquid-crystalline packed within a single plane. Finally, we assess glycocalyx deformability and porosity using intravital microscopy. We argue that the columnar network architecture and the liquid-crystalline packing of the filament termini allow the glycocalyx to function as a deformable size-exclusion filter of luminal contents.
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spelling pubmed-69466832020-01-13 Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy Sun, Willy W. Krystofiak, Evan S. Leo-Macias, Alejandra Cui, Runjia Sesso, Antonio Weigert, Roberto Ebrahim, Seham Kachar, Bechara Commun Biol Article The glycocalyx is a highly hydrated, glycoprotein-rich coat shrouding many eukaryotic and prokaryotic cells. The intestinal epithelial glycocalyx, comprising glycosylated transmembrane mucins, is part of the primary host-microbe interface and is essential for nutrient absorption. Its disruption has been implicated in numerous gastrointestinal diseases. Yet, due to challenges in preserving and visualizing its native organization, glycocalyx structure-function relationships remain unclear. Here, we characterize the nanoarchitecture of the murine enteric glycocalyx using freeze-etching and electron tomography. Micrometer-long mucin filaments emerge from microvillar-tips and, through zigzagged lateral interactions form a three-dimensional columnar network with a 30 nm mesh. Filament-termini converge into globular structures ~30 nm apart that are liquid-crystalline packed within a single plane. Finally, we assess glycocalyx deformability and porosity using intravital microscopy. We argue that the columnar network architecture and the liquid-crystalline packing of the filament termini allow the glycocalyx to function as a deformable size-exclusion filter of luminal contents. Nature Publishing Group UK 2020-01-07 /pmc/articles/PMC6946683/ /pubmed/31925335 http://dx.doi.org/10.1038/s42003-019-0735-5 Text en © This is a U.S. government work and not under copyright protection in the US; foreign copyright protection may apply 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Sun, Willy W.
Krystofiak, Evan S.
Leo-Macias, Alejandra
Cui, Runjia
Sesso, Antonio
Weigert, Roberto
Ebrahim, Seham
Kachar, Bechara
Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title_full Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title_fullStr Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title_full_unstemmed Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title_short Nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
title_sort nanoarchitecture and dynamics of the mouse enteric glycocalyx examined by freeze-etching electron tomography and intravital microscopy
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946683/
https://www.ncbi.nlm.nih.gov/pubmed/31925335
http://dx.doi.org/10.1038/s42003-019-0735-5
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