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      Controlled packing and single-droplet resolution of 3D-printed functional synthetic tissues

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          Abstract

          3D-printing networks of droplets connected by interface bilayers are a powerful platform to build synthetic tissues in which functionality relies on precisely ordered structures. However, the structural precision and consistency in assembling these structures is currently limited, which restricts intricate designs and the complexity of functions performed by synthetic tissues. Here, we report that the equilibrium contact angle ( θ DIB) between a pair of droplets is a key parameter that dictates the tessellation and precise positioning of hundreds of picolitre-sized droplets within 3D-printed, multi-layer networks. When θ DIB approximates the geometrically-derived critical angle ( θ c) of 35.3°, the resulting networks of droplets arrange in regular hexagonal close-packed (hcp) lattices with the least fraction of defects. With this improved control over droplet packing, we can 3D-print functional synthetic tissues with single-droplet-wide conductive pathways. Our new insights into 3D droplet packing permit the fabrication of complex synthetic tissues, where precisely positioned compartments perform coordinated tasks.

          Abstract

          Precise patterning of lipid-stabilised aqueous droplets is a key challenge in building synthetic tissue designs. Here, the authors show how the interactions between pairs of droplets direct the packing of droplets within 3D-printed networks, enabling the formation of synthetic tissues with high-resolution features.

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          Most cited references 36

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          A tissue-like printed material.

          Living cells communicate and cooperate to produce the emergent properties of tissues. Synthetic mimics of cells, such as liposomes, are typically incapable of cooperation and therefore cannot readily display sophisticated collective behavior. We printed tens of thousands of picoliter aqueous droplets that become joined by single lipid bilayers to form a cohesive material with cooperating compartments. Three-dimensional structures can be built with heterologous droplets in software-defined arrangements. The droplet networks can be functionalized with membrane proteins; for example, to allow rapid electrical communication along a specific path. The networks can also be programmed by osmolarity gradients to fold into otherwise unattainable designed structures. Printed droplet networks might be interfaced with tissues, used as tissue engineering substrates, or developed as mimics of living tissue.
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            Droplet interface bilayers.

            Droplet interface bilayers (DIBs) provide a superior platform for the biophysical analysis of membrane proteins. The versatile DIBs can also form networks, with features that include built-in batteries and sensors.
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              Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis.

              Artificial planar lipid bilayers are a powerful tool for the functional study of membrane proteins, yet they have not been widely used due to their low stability and reproducibility. This paper describes an accessible method to form a planar lipid bilayer, simply by contacting two monolayers assembled at the interface between water and organic solvent in a microfluidic chip. The membrane of an organic solvent containing phospholipids at the interface was confirmed to be a bilayer by the capacitance measurement and by measuring the ion channel signal from reconstituted antibiotic peptides. We present two different designs for bilayer formation. One equips two circular wells connected, in which the water/solvent/water interface was formed by simply injecting a water droplet into each well. Another equips the cross-shaped microfluidic channel. In the latter design, formation of the interface at the sectional area was controlled by external syringe pumps. Both methods are extremely simple and reproducible, especially in microdevices, and will lead to automation and multiple bilayer formation for the high-throughput screening of membrane transport in physiological and pharmaceutical studies.
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                Author and article information

                Contributors
                ravinash.krishnakumar@chem.ox.ac.uk
                hagan.bayley@chem.ox.ac.uk
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                30 April 2020
                30 April 2020
                2020
                : 11
                Affiliations
                [1 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Department of Chemistry, , University of Oxford, Chemistry Research Laboratory, ; 12 Mansfield Road, Oxford, OX1 3TA UK
                [2 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Department of Zoology, , University of Oxford, Zoology Research & Administration Building, ; 11a Mansfield Road, Oxford, OX1 3SZ UK
                [3 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Micron Advanced Bioimaging Unit, Department of Biochemistry, University of Oxford, ; South Parks Road, Oxford, OX1 3QU UK
                [4 ]ISNI 0000 0004 1936 9262, GRID grid.11835.3e, Present Address: Department of Physics and Astronomy, , University of Sheffield, ; Sheffield, S3 7RH UK
                [5 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Present Address: Chemical and Physical Sciences, University of Toronto Mississauga, ; 3359 Mississauga Rd, Mississauga, ON L5L 1C6 Canada
                Article
                15953
                10.1038/s41467-020-15953-y
                7192927
                32355158
                © The Author(s) 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/.

                Funding
                Funded by: EPSRC & BBSRC Centre for Doctoral Training in Synthetic Biology (grant EP/L016494/1) Clarendon Fund Scholarship
                Funded by: EPSRC Life Sciences Interface Centre for Doctoral Training (grant EP/F500394/1)
                Funded by: EPSRC & BBSRC Centre for Doctoral Training in Synthetic Biology (grant EP/L016494/1) Clarendon Fund Scholarship Oxford-Broomhead Graduate Scholarship
                Funded by: European Research Council Advanced Grant OxSyBio Ltd.
                Categories
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                Custom metadata
                © The Author(s) 2020

                Uncategorized

                tissues, nanopores, biomimetics, bioinspired materials, membrane biophysics

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