Dataset Information

Actin Dynamics Drive Microvillar Motility and Clustering during Brush Border Assembly.

ABSTRACT: Transporting epithelial cells generate arrays of microvilli, known as a brush border, to enhance functional capacity. To understand brush border formation, we used live cell imaging to visualize apical remodeling early in this process. Strikingly, we found that individual microvilli exhibit persistent active motility, translocating across the cell surface at ?0.2 ?m/min. Perturbation with inhibitors and photokinetic experiments revealed that microvillar motility is driven by actin assembly at the barbed ends of core bundles, which in turn is linked to robust treadmilling of these structures. Actin regulatory factors IRTKS and EPS8 localize to the barbed ends of motile microvilli, where they control the kinetics and nature of movement. As the apical surface of differentiating epithelial cells is crowded with nascent microvilli, persistent motility promotes collisions between protrusions and ultimately clustering and consolidation into higher-order arrays. Thus, microvillar motility represents a previously unrecognized driving force for apical surface remodeling and maturation during epithelial differentiation.

SUBMITTER: Meenderink LM

PROVIDER: S-EPMC6736749 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Actin Dynamics Drive Microvillar Motility and Clustering during Brush Border Assembly.

Meenderink Leslie M LM Gaeta Isabella M IM Postema Meagan M MM Cencer Caroline S CS Chinowsky Colbie R CR Krystofiak Evan S ES Millis Bryan A BA Tyska Matthew J MJ

Developmental cell 20190801 5

Transporting epithelial cells generate arrays of microvilli, known as a brush border, to enhance functional capacity. To understand brush border formation, we used live cell imaging to visualize apical remodeling early in this process. Strikingly, we found that individual microvilli exhibit persistent active motility, translocating across the cell surface at ∼0.2 μm/min. Perturbation with inhibitors and photokinetic experiments revealed that microvillar motility is driven by actin assembly at th ...[more]

PMID: 31378589

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Project description:Microvilli generate the small intestinal brush border, the main site of nutrient digestion and absorption. Mucosal structuring of the small intestine of chicken during the perihatch period has been widely researched, yet the developmental dynamics of microvilli during this period have not been fully characterized. In this study, we examined the structural and molecular characteristics of microvilli assembly and maturation during the perihatch period. Small intestines of broiler embryos and chicks were sampled at prehatch ages 17 E and 19 E, at day of hatch (DOH) and at 1, 3, 7, and 10 d posthatch. Morphological evaluations and measurements were conducted by scanning electron microscopy (SEM) and light microscopy (LM) (n = 3/timepoint), and expression of microvilli structural genes Plastin 1, Ezrin, and Myo1a was examined by Real-Time qPCR (n = 6/timepoint). Results revealed dissimilar patterns of microvilli and villi development during the perihatch period. From 19 E to 1 d, microvilli lengths increased 4.3-fold while villi lengths increased 2.8-fold (P < 0.0001). From 3 to 7 d, villi lengths increased by 20% (P < 0.005), while microvilli lengths decreased by 41% (P = 0.001). At 10 d, microvilli lengths stabilized, while villi continued to elongate by 26% (P < 0.0001). Estimations of the microvilli amplification factor (MAF) and total enterocyte surface area (TESA) revealed similar trends, with peak values of 78.53 and 1961.67 µm2, respectively, at 3 d. Microvilli structural gene expression portrayed diverse patterns. Expression of Plastin 1, which bundles and binds actin cores to the terminal web, increased 8.7-fold between 17 E and DOH (P = 0.005), and gradually increased up to 7 d (P = 0.045). Ezrin and Myo1a, both actin core-cell membrane cross-linkers, portrayed different expression patterns throughout the perihatch period, as Ezrin expression was relatively stable, while Myo1a expression increased 15.8-fold between 17 E and 10 d (P < 0.0001). We conclude that microvilli assembly during the perihatch period is a rapid, coordinated process, which dramatically expands the digestive and absorptive surface area of the small intestine before the completion of villi maturation.

Dataset Information

Actin Dynamics Drive Microvillar Motility and Clustering during Brush Border Assembly.

Publications

Actin Dynamics Drive Microvillar Motility and Clustering during Brush Border Assembly.

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