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      Collagen, stiffness, and adhesion: the evolutionary basis of vertebrate mechanobiology

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      Molecular Biology of the Cell
      The American Society for Cell Biology

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          Abstract

          The emergence of collagen I in vertebrates resulted in a dramatic increase in the stiffness of the extracellular environment, supporting long-range force propagation and the development of low-compliant tissues necessary for the development of vertebrate traits including pressurized circulation and renal filtration. Vertebrates have also evolved integrins that can bind to collagens, resulting in the generation of higher tension and more efficient force transmission in the extracellular matrix. The stiffer environment provides an opportunity for the vertebrates to create new structures such as the stress fibers, new cell types such as endothelial cells, new developmental processes such as neural crest delamination, and new tissue organizations such as the blood–brain barrier. Molecular players found only in vertebrates allow the modification of conserved mechanisms as well as the design of novel strategies that can better serve the physiological needs of the vertebrates. These innovations collectively contribute to novel morphogenetic behaviors and unprecedented increases in the complexities of tissue mechanics and functions.

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          Most cited references246

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          The collagen family.

          Collagens are the most abundant proteins in mammals. The collagen family comprises 28 members that contain at least one triple-helical domain. Collagens are deposited in the extracellular matrix where most of them form supramolecular assemblies. Four collagens are type II membrane proteins that also exist in a soluble form released from the cell surface by shedding. Collagens play structural roles and contribute to mechanical properties, organization, and shape of tissues. They interact with cells via several receptor families and regulate their proliferation, migration, and differentiation. Some collagens have a restricted tissue distribution and hence specific biological functions.
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            Angiocrine functions of organ-specific endothelial cells.

            Endothelial cells that line capillaries are not just passive conduits for delivering blood. Tissue-specific endothelium establishes specialized vascular niches that deploy sets of growth factors, known as angiocrine factors. These cues participate actively in the induction, specification, patterning and guidance of organ regeneration, as well as in the maintainance of homeostasis and metabolism. When upregulated following injury, they orchestrate self-renewal and differentiation of tissue-specific resident stem and progenitor cells into functional organs. Uncovering the mechanisms by which organotypic endothelium distributes physiological levels of angiocrine factors both spatially and temporally will lay the foundation for clinical trials that promote organ repair without scarring.
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              The extracellular matrix in development and morphogenesis: a dynamic view.

              The extracellular matrix (ECM) is synthesized and secreted by embryonic cells beginning at the earliest stages of development. Our understanding of ECM composition, structure and function has grown considerably in the last several decades and this knowledge has revealed that the extracellular microenvironment is critically important for cell growth, survival, differentiation and morphogenesis. ECM and the cellular receptors that interact with it mediate both physical linkages with the cytoskeleton and the bidirectional flow of information between the extracellular and intracellular compartments. This review considers the range of cell and tissue functions attributed to ECM molecules and summarizes recent findings specific to key developmental processes. The importance of ECM as a dynamic repository for growth factors is highlighted along with more recent studies implicating the 3-dimensional organization and physical properties of the ECM as it relates to cell signaling and the regulation of morphogenetic cell behaviors. Embryonic cell and tissue generated forces and mechanical signals arising from ECM adhesion represent emerging areas of interest in this field. Copyright 2009 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: Monitoring Editor
                Journal
                Mol Biol Cell
                Mol. Biol. Cell
                molbiolcell
                mbc
                mboc
                Molecular Biology of the Cell
                The American Society for Cell Biology
                1059-1524
                1939-4586
                01 August 2020
                : 31
                : 17
                : 1823-1834
                Affiliations
                [a ]Department of Cell and Developmental Biology, University of Illinois, Urbana–Champaign, Urbana, IL 61801
                University of Wisconsin, Madison
                Author notes

                Competing interests: No competing interests declared.

                *Address correspondence to: Vivian W. Tang ( vtang@ 123456illinois.edu ).
                Article
                E19-12-0709
                10.1091/mbc.E19-12-0709
                7525820
                32730166
                b089805c-bfb9-48cd-bf91-1f1de16f29e2
                © 2020 Tang. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.

                This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.

                History
                : 06 April 2020
                : 11 May 2020
                : 28 May 2020
                Categories
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                Molecular biology
                Molecular biology

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