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      Spatiotemporal control of signal-driven enzymatic reaction in artificial cell-like polymersomes

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      Nature Communications
      Nature Publishing Group UK
      Chemical engineering, Enzymes, Polymers, Synthetic biology

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          Abstract

          Living cells can spatiotemporally control biochemical reactions to dynamically assemble membraneless organelles and remodel cytoskeleton. Herein, we present a microfluidic approach to prepare semi-permeable polymersomes comprising of amphiphilic triblock copolymer to achieve external signal-driven complex coacervation as well as biophysical reconstitution of cytoskeleton within the polymersomes. We also show that the microfluidic synthesis of polymersomes enables precise control over size, efficient encapsulation of enzymes as well as regulation of substrates without the use of biopores. Moreover, we demonstrate that the resulting triblock copolymer-based membrane in polymersomes is size-selective, allowing phosphoenol pyruvate to readily diffuse through the membrane and induce enzymatic reaction and successive coacervation or actin polymerization in the presence of pyruvate kinase and adenosine diphosphate inside the polymersomes. We envision that the Pluronic-based polymersomes presented in this work will shed light in the design of in vitro enzymatic reactions in artificial cell-like vesicles.

          Abstract

          Researchers have been trying to mimick the cellular spatiotemporal control in normal cells with different approaches. Here, the authors present semi-permeable polymersomes comprising of amphiphilic triblock copolymers to achieve external signal-driven complex coacervation and biophysical reconstitution of cytoskeleton.

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          Most cited references56

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          Liposomes and polymersomes: a comparative review towards cell mimicking

          Minimal cells: we compare and contrast liposomes and polymersomes for a better a priori choice and design of vesicles and try to understand the advantages and shortcomings associated with using one or the other in many different aspects (properties, synthesis, self-assembly, applications). Cells are integral to all forms of life due to their compartmentalization by the plasma membrane. However, living organisms are immensely complex. Thus there is a need for simplified and controllable models of life for a deeper understanding of fundamental biological processes and man-made applications. This is where the bottom-up approach of synthetic biology comes from: a stepwise assembly of biomimetic functionalities ultimately into a protocell. A fundamental feature of such an endeavor is the generation and control of model membranes such as liposomes and polymersomes. We compare and contrast liposomes and polymersomes for a better a priori choice and design of vesicles and try to understand the advantages and shortcomings associated with using one or the other in many different aspects (properties, synthesis, self-assembly, applications) and which aspects have been studied and developed with each type and update the current development in the field.
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            Artificial Cells: Synthetic Compartments with Life-like Functionality and Adaptivity

            Conspectus Cells are highly advanced microreactors that form the basis of all life. Their fascinating complexity has inspired scientists to create analogs from synthetic and natural components using a bottom-up approach. The ultimate goal here is to assemble a fully man-made cell that displays functionality and adaptivity as advanced as that found in nature, which will not only provide insight into the fundamental processes in natural cells but also pave the way for new applications of such artificial cells. In this Account, we highlight our recent work and that of others on the construction of artificial cells. First, we will introduce the key features that characterize a living system; next, we will discuss how these have been imitated in artificial cells. First, compartmentalization is crucial to separate the inner chemical milieu from the external environment. Current state-of-the-art artificial cells comprise subcompartments to mimic the hierarchical architecture of eukaryotic cells and tissue. Furthermore, synthetic gene circuits have been used to encode genetic information that creates complex behavior like pulses or feedback. Additionally, artificial cells have to reproduce to maintain a population. Controlled growth and fission of synthetic compartments have been demonstrated, but the extensive regulation of cell division in nature is still unmatched. Here, we also point out important challenges the field needs to overcome to realize its full potential. As artificial cells integrate increasing orders of functionality, maintaining a supporting metabolism that can regenerate key metabolites becomes crucial. Furthermore, life does not operate in isolation. Natural cells constantly sense their environment, exchange (chemical) signals, and can move toward a chemoattractant. Here, we specifically explore recent efforts to reproduce such adaptivity in artificial cells. For instance, synthetic compartments have been produced that can recruit proteins to the membrane upon an external stimulus or modulate their membrane composition and permeability to control their interaction with the environment. A next step would be the communication of artificial cells with either bacteria or another artificial cell. Indeed, examples of such primitive chemical signaling are presented. Finally, motility is important for many organisms and has, therefore, also been pursued in synthetic systems. Synthetic compartments that were designed to move in a directed, controlled manner have been assembled, and directed movement toward a chemical attractant is among one of the most life-like directions currently under research. Although the bottom-up construction of an artificial cell that can be truly considered “alive” is still an ambitious goal, the recent work discussed in this Account shows that this is an active field with contributions from diverse disciplines like materials chemistry and biochemistry. Notably, research during the past decade has already provided valuable insights into complex synthetic systems with life-like properties. In the future, artificial cells are thought to contribute to an increased understanding of processes in natural cells and provide opportunities to create smart, autonomous, cell-like materials.
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              Sequential bottom-up assembly of mechanically stabilized synthetic cells by microfluidics.

              Compartments for the spatially and temporally controlled assembly of biological processes are essential towards cellular life. Synthetic mimics of cellular compartments based on lipid-based protocells lack the mechanical and chemical stability to allow their manipulation into a complex and fully functional synthetic cell. Here, we present a high-throughput microfluidic method to generate stable, defined sized liposomes termed 'droplet-stabilized giant unilamellar vesicles (dsGUVs)'. The enhanced stability of dsGUVs enables the sequential loading of these compartments with biomolecules, namely purified transmembrane and cytoskeleton proteins by microfluidic pico-injection technology. This constitutes an experimental demonstration of a successful bottom-up assembly of a compartment with contents that would not self-assemble to full functionality when simply mixed together. Following assembly, the stabilizing oil phase and droplet shells are removed to release functional self-supporting protocells to an aqueous phase, enabling them to interact with physiologically relevant matrices.
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                Author and article information

                Contributors
                hyomin@postech.ac.kr
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                2 September 2022
                2 September 2022
                2022
                : 13
                : 5179
                Affiliations
                GRID grid.49100.3c, ISNI 0000 0001 0742 4007, Department of Chemical Engineering, , Pohang University of Science and Technology (POSTECH), ; Pohang, 37673 Republic of Korea
                Author information
                http://orcid.org/0000-0002-0968-431X
                Article
                32889
                10.1038/s41467-022-32889-7
                9440086
                36056018
                bcaaa80a-f28f-4ae1-bb17-4c4205b8cb1b
                © The Author(s) 2022

                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/.

                History
                : 13 January 2022
                : 23 August 2022
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100003725, National Research Foundation of Korea (NRF);
                Award ID: 2020R1C1C1004642
                Award ID: 2019K1A4A7A02113715
                Award ID: 2021R1A4A1021972
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100003710, Korea Health Industry Development Institute (KHIDI);
                Award ID: HP20C0006
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2022

                Uncategorized
                chemical engineering,enzymes,polymers,synthetic biology
                Uncategorized
                chemical engineering, enzymes, polymers, synthetic biology

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