NMII Forms a Contractile Transcellular Sarcomeric Network to Regulate Apical Cell Junctions and Tissue Geometry

Ebrahim, Seham; Fujita, Toshio; Millis, Bryan A.; Kozin, Elliott D.; Ma, Xuefei; Kawamoto, Sachiyo; Baird, Michelle A.; Davidson, Michael W.; Yonemura, Shigenobu; Hisa, Yasuo; Conti, Mary Anne; Adelstein, Robert S.; Sakaguchi, Hirofumi; Kachar, Bechara

doi:10.1016/j.cub.2013.03.039

Cited by 163 publications

(199 citation statements)

References 30 publications

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“…An increase in the peripheral actomyosin tension is also a possibility because vasopressin has been shown to activate myosin light chain kinase (31), which, in turn, activates myosin light chain and hence nonmuscle myosin II activity (55). In the ear's organ of Corti, the nonmuscle myosin IIB and IIC, not IIA, are organized as a sarcomeric network surrounding the apical perimeter of the cells (56). This arrangement was shown to regulate the length of the apical perimeter and the apical surface area.…”

Section: Discussionmentioning

confidence: 99%

Quantitative apical membrane proteomics reveals vasopressin-induced actin dynamics in collecting duct cells

Loo

Chen

Wang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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In kidney collecting duct cells, filamentous actin (F-actin) depolymerization is a critical step in vasopressin-induced trafficking of aquaporin-2 to the apical plasma membrane. However, the molecular components of this response are largely unknown. Using stable isotope-based quantitative protein mass spectrometry and surface biotinylation, we identified 100 proteins that showed significant abundance changes in the apical plasma membrane of mouse cortical collecting duct cells in response to vasopressin. Fourteen of these proteins are involved in actin cytoskeleton regulation, including actin itself, 10 actin-associated proteins, and 3 regulatory proteins. Identified were two integral membrane proteins (Clmn, Nckap1) and one actin-binding protein (Mpp5) that link F-actin to the plasma membrane, five F-actin end-binding proteins (Arpc2, Arpc4, Gsn, Scin, and Capzb) involved in F-actin reorganization, and two actin adaptor proteins (Dbn1, Lasp1) that regulate actin cytoskeleton organization. There were also protease (Capn1), protein kinase (Cdc42bpb), and Rho guanine nucleotide exchange factor 2 (Arhgef2) that mediate signal-induced F-actin changes. Based on these findings, we devised a live-cell imaging method to observe vasopressininduced F-actin dynamics in polarized mouse cortical collecting duct cells. In response to vasopressin, F-actin gradually disappeared near the center of the apical plasma membrane while consolidating laterally near the tight junction. This F-actin peripheralization was blocked by calcium ion chelation. Vasopressin-induced apical aquaporin-2 trafficking and forskolin-induced water permeability increase were blocked by F-actin disruption. In conclusion, we identified a vasopressin-regulated actin network potentially responsible for vasopressin-induced apical F-actin dynamics that could explain regulation of apical aquaporin-2 trafficking and water permeability increase.V asopressin regulates aquaporin-2 (AQP2) and osmotic water transport in the collecting duct by regulating total AQP2 protein abundance and AQP2 trafficking to and from the apical plasma membrane of principal cells (1). Understanding these regulatory mechanisms at the molecular level is important to the ultimate understanding of the pathophysiology of multiple water balance disorders (2). This goal is abetted by the methods of molecular systems biology (proteomics and transcriptomics), which not only reveal "parts lists" for collecting duct cells but also can identify what biological and molecular processes are regulated by vasopressin. These proteomic and transcriptomic data have been made publicly available in databases (3). Many of these studies have focused on whole cells (4-6), whereas several analyzed subcellular fractions (7-12). Analysis of subcellular fractions is technically demanding, but it has the benefit of identifying low abundance proteins with important functions. To identify proteins potentially involved in apical AQP2 trafficking, we previously used NHS-based surface biotinylation coupled to streptavidin...

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Section: Discussionmentioning

confidence: 99%

Quantitative apical membrane proteomics reveals vasopressin-induced actin dynamics in collecting duct cells

Loo

Chen

Wang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Myosin activity in these tissues reduces the distance between sarcomeric repeats, consistent with myosin motor activity pulling antiparallel F-actin arrays together, driving a pursestring-like contraction. In adjacent cells, the repeated pattern of myosin and F-actin cross-linking proteins in F-actin bundles is aligned across the junctional interface, suggesting that individual units of this sarcomeric repeat are somehow coordinated and possibly anchored across junctional interfaces (Ebrahim et al, 2013). Cell culture studies have shown that actin-myosin fibers without a clear sarcomere organization can also generate tension around the apical perimeter and can drive apical constriction (Ishiuchi and Takeichi, 2011;Ratheesh et al, 2012;Wu et al, 2014).…”

Section: Contractile Fibersmentioning

confidence: 99%

“…Classic studies of neurulation in embryos and of cultured epithelia suggested that the contraction of circumferential actin-myosin bundles or fibers underlying the adherens junctions causes the cell apex to constrict, analogous to drawing a purse-string (Baker and Schroeder, 1967;Burnside, 1973;Burgess, 1982;Owaribe and Masuda, 1982). A recent study demonstrated that circumferential actin-myosin bundles can exhibit a clear sarcomeric organization in several epithelial tissues in vivo (Ebrahim et al, 2013). Myosin activity in these tissues reduces the distance between sarcomeric repeats, consistent with myosin motor activity pulling antiparallel F-actin arrays together, driving a pursestring-like contraction.…”

Section: Contractile Fibersmentioning

confidence: 99%

Apical constriction: themes and variations on a cellular mechanism driving morphogenesis

2014

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Apical constriction is a cell shape change that promotes tissue remodeling in a variety of homeostatic and developmental contexts, including gastrulation in many organisms and neural tube formation in vertebrates. In recent years, progress has been made towards understanding how the distinct cell biological processes that together drive apical constriction are coordinated. These processes include the contraction of actin-myosin networks, which generates force, and the attachment of actin networks to cell-cell junctions, which allows forces to be transmitted between cells. Different cell types regulate contractility and adhesion in unique ways, resulting in apical constriction with varying dynamics and subcellular organizations, as well as a variety of resulting tissue shape changes. Understanding both the common themes and the variations in apical constriction mechanisms promises to provide insight into the mechanics that underlie tissue morphogenesis.

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“…Superresolution structured illumination microscopy (SIM) analysis further shows paired NMIIB alignment between epicardial cells (Fig. 1B), reminiscent of NMII localization at epithelial cell-cell junctions (Ebrahim et al, 2013) and suggesting a role for NMIIB in regulating epicardial cell-cell adhesion.…”

Section: Abnormal Epicardium and Coronary Vessels In B − /B − Heartsmentioning

confidence: 99%

Nonmuscle myosin IIB regulates epicardial integrity and epicardium-derived mesenchymal cell maturation

Sung

Yang

et al. 2017

Journal of Cell Science

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Nonmuscle myosin IIB (NMIIB; heavy chain encoded by MYH10) is essential for cardiac myocyte cytokinesis. The role of NMIIB in other cardiac cells is not known. Here, we show that NMIIB is required in epicardial formation and functions to support myocardial proliferation and coronary vessel development. Ablation of NMIIB in epicardial cells results in disruption of epicardial integrity with a loss of E-cadherin at cell-cell junctions and a focal detachment of epicardial cells from the myocardium. NMIIB-knockout and blebbistatin-treated epicardial explants demonstrate impaired mesenchymal cell maturation during epicardial epithelial-mesenchymal transition. This is manifested by an impaired invasion of collagen gels by the epicardium-derived mesenchymal cells and the reorganization of the cytoskeletal structure. Although there is a marked decrease in the expression of mesenchymal genes, there is no change in Snail (also known as Snai1) or E-cadherin expression. Studies from epicardiumspecific NMIIB-knockout mice confirm the importance of NMIIB for epicardial integrity and epicardial functions in promoting cardiac myocyte proliferation and coronary vessel formation during heart development. Our findings provide a novel mechanism linking epicardial formation and epicardial function to the activity of the cytoplasmic motor protein NMIIB.

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NMII Forms a Contractile Transcellular Sarcomeric Network to Regulate Apical Cell Junctions and Tissue Geometry

Cited by 163 publications

References 30 publications

Quantitative apical membrane proteomics reveals vasopressin-induced actin dynamics in collecting duct cells

Quantitative apical membrane proteomics reveals vasopressin-induced actin dynamics in collecting duct cells

Apical constriction: themes and variations on a cellular mechanism driving morphogenesis

Nonmuscle myosin IIB regulates epicardial integrity and epicardium-derived mesenchymal cell maturation

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