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      The apical ECM preserves embryonic integrity and distributes mechanical stress during morphogenesis

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          Abstract

          Epithelia are bound by both basal and apical extracellular matrices (ECM). Although the composition and function of the former have been intensively investigated, less is known about the latter. The embryonic sheath, the ECM apical to the Caenorhabditis elegans embryonic epidermis, has been suggested to promote elongation of the embryo. In an RNAi screen for the components of the sheath, we identified the zona pellucida domain proteins NOAH-1 and NOAH-2. We found that these proteins act in the same pathway, and in parallel to three other putative sheath proteins, the leucine-rich repeat proteins SYM-1, LET-4 and FBN-1/Fibrillin, to ensure embryonic integrity and promote elongation. Laser nano-ablation experiments to map the stress field show that NOAH-1 and NOAH-2, together with PAK-1/p21-activated kinase, maintain and relay the actomyosin-dependent stress generated within the lateral epidermis before muscles become active. Subsequently, loss-of-function experiments show that apical ECM proteins are essential for muscle anchoring and for relaying the mechanical input from muscle contractions, which are essential for elongation. Hence, the apical ECM contributes to morphogenesis by maintaining embryonic integrity and relaying mechanical stress.

          Abstract

          Summary: In C. elegans, embryonic apical extracellular matrix acts as a protective layer, a rigid anchor for muscle function and transmit actomyosin forces to promote embryonic elongation.

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          Most cited references37

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          Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters

          The extracellular matrix (ECM) is a major component of tumors and a significant contributor to cancer progression. In this study, we use proteomics to investigate the ECM of human mammary carcinoma xenografts and show that primary tumors of differing metastatic potential differ in ECM composition. Both tumor cells and stromal cells contribute to the tumor matrix and tumors of differing metastatic ability differ in both tumor- and stroma-derived ECM components. We define ECM signatures of poorly and highly metastatic mammary carcinomas and these signatures reveal up-regulation of signaling pathways including TGFβ and VEGF. We further demonstrate that several proteins characteristic of highly metastatic tumors (LTBP3, SNED1, EGLN1, and S100A2) play causal roles in metastasis, albeit at different steps. Finally we show that high expression of LTBP3 and SNED1 correlates with poor outcome for ER−/PR−breast cancer patients. This study thus identifies novel biomarkers that may serve as prognostic and diagnostic tools. DOI: http://dx.doi.org/10.7554/eLife.01308.001
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            Global tissue revolutions in a morphogenetic movement controlling elongation.

            Polarized cell behaviors drive axis elongation in animal embryos, but the mechanisms underlying elongation of many tissues remain unknown. Eggs of Drosophila undergo elongation from a sphere to an ellipsoid during oogenesis. We used live imaging of follicles (developing eggs) to elucidate the cellular basis of egg elongation. We find that elongating follicles undergo repeated rounds of circumferential rotation around their long axes. Follicle epithelia mutant for integrin or collagen IV fail to rotate and elongate, which results in round eggs. We present evidence that polarized rotation is required to build a polarized, fibrillar extracellular matrix (ECM) that constrains tissue shape. Thus, global tissue rotation is a morphogenetic behavior that uses planar polarity information in the ECM to control tissue elongation.
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              Subdiffusion and Anomalous Local Viscoelasticity in Actin Networks.

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                Author and article information

                Journal
                Development
                Development
                DEV
                develop
                Development (Cambridge, England)
                The Company of Biologists Ltd
                0950-1991
                1477-9129
                1 December 2017
                1 December 2017
                : 144
                : 23
                : 4336-4349
                Affiliations
                [1 ]Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire de Biologie du Développement - Institut de Biologie Paris Seine (LBD - IBPS) , Paris 75005, France
                [2 ]Development and Stem Cells Program, IGBMC, CNRS (UMR7104), INSERM (U964), Université de Strasbourg, 1 rue Laurent Fries, BP10142 , Illkirch 67400, France
                Author notes
                Author information
                http://orcid.org/0000-0001-6594-2881
                Article
                DEV150383
                10.1242/dev.150383
                5769628
                28526752
                5b66c273-8cea-4ace-aead-9c769df7ff55
                © 2017. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 20 February 2017
                : 11 May 2017
                Funding
                Funded by: European Research Council, http://dx.doi.org/10.13039/501100000781;
                Award ID: 294744
                Funded by: Centre National de la Recherche Scientifique, http://dx.doi.org/10.13039/501100004794;
                Funded by: Agence Nationale de la Recherche, http://dx.doi.org/10.13039/501100001665;
                Award ID: ANR-10-LABX-0030-INRT
                Award ID: ANR-10-IDEX-0002-02
                Categories
                Research Article

                Developmental biology
                apical extracellular matrix,c. elegans,embryonic elongation,laser nano-ablation,muscle anchoring,zona pellucida protein

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