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WIREs Nanomed Nanobiotechnol
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Engineering spatiotemporal organization and dynamics in synthetic cells

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Abstract Constructing synthetic cells has recently become an appealing area of research. Decades of research in biochemistry and cell biology have amassed detailed part lists of components involved in various cellular processes. Nevertheless, recreating any cellular process in vitro in cell‐sized compartments remains ambitious and challenging. Two broad features or principles are key to the development of synthetic cells—compartmentalization and self‐organization/spatiotemporal dynamics. In this review article, we discuss the current state of the art and research trends in the engineering of synthetic cell membranes, development of internal compartmentalization, reconstitution of self‐organizing dynamics, and integration of activities across scales of space and time. We also identify some research areas that could play a major role in advancing the impact and utility of engineered synthetic cells. This article is categorized under: Biology‐Inspired Nanomaterials > Lipid‐Based Structures Biology‐Inspired Nanomaterials > Protein and Virus‐Based Structures
Recent advances in constructing synthetic cells involve engineering synthetic cell membranes, development of compartmentalization strategies, and reconstituting dynamic processes in space and time. Black arrows depict the flow of molecules and the exchange of information happening across lipid/protein membranes or between the phase‐separated liquid condensates of a membrane‐less compartment
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A range of spatial scales in natural cellular life (left) and in synthetic cells (right). In the synthetic cell context, nanometric functional compartments have been generated as well as millimeter‐sized protein expression patterns. Energy modules were constructed with nanometer‐sized proteoliposomes and inverted membranes. Synthetic cells or Synells have also been developed which can interact with each other. Additionally, a plausible mechanism for de novo liposome production was developed yielding compartments of compatible size with biological cells. Subcellular structures and their dependence on cell volume were studied by reconstructing mitotic spindles in droplets. Finally, protein expression patterns, compartments capable of mitosis, and multicellular structures have been produced in relevant spatial scales where eukaryotic cells and tissues operate. Some illustration images in were created with BioRender.com
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Several temporal scales involved in biological cells (left) and synthetic cells (right). The in vitro reconstituted phenomena range from oscillations with multi‐second periods up to multicellular structures whose aggregation unfolds in the order of days. In between, temporal scales range from metabolic processes that can be sustained for several hours, the oscillations of coupled micro‐compartments, the formation of self‐organized structures in Xenopus laevis egg extracts, and the fast timescale response of the engineered phosphorylation regulatory networks. Some illustration images in were created with BioRender.com
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Examples of Min/FtsZ system reconstitutions. (a) MinD and MinE have been shown to form a variety of patterns when reconstituted in cell‐free setups. In this example, GFP‐MinD (cyan) and MinE‐Alexa647 (magenta) were preincubated with ATP and infused into a flowcell coated with a SLB. Still images show the different types of patterns supported by the decreasing protein density in the flowcell from inlet to outlet. Adapted with permission from (Mizuuchi & Vecchiarelli, 2018). (b) Reconstitution of Min oscillations in a rod‐shaped trough has been shown to confine FtsZ‐YFP‐MTS polymerization to the middle of the compartment. Adapted from (Zieske & Schwille, 2014) under the CC BY 4.0 license
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Protein organelles and LLPS for designing compartmentalization in synthetic cells. (a) The two known classes of protein organelles, encapsulin nanocompartments (Encs), and bacterial microcompartments (BMCs). (b) Potential problems for enzymes and pathways arising without compartmentalization. (c) The advantages of compartmentalizing metabolic pathways. (d) Integration of different types of designed and modular protein‐based compartmentalization systems for optimizing synthetic cell metabolism
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Possible molecular composition for the boundaries of synthetic cells. Left. (a) A membrane composed by phospholipids and cholesterol is shown. Enlargements show the molecular structures of 1‐palmitoyl‐2‐oleoyl‐sn‐glycero‐3‐phosphocholine (POPC) and cholesterol. (b) Membrane structure of a proteinosome, showing the spatial organization of oleosin molecules. The enlargement shows a random peptide sequence. (c) Polymerosomal membrane composed by block copolymers. The enlargement shows the molecular structure of polystyrene‐b‐polyacrilic acid (PS‐b‐PAA). (d) A phospholipid/block copolymer hybrid membrane is shown. The illustrations are not drawn to scale. Right. Relative comparison of different characteristics between phospholipids, polypeptides, and block copolymers as a chassis material for synthetic cells
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Biology-Inspired Nanomaterials > Protein and Virus-Based Structures
Biology-Inspired Nanomaterials > Lipid-Based Structures

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