Interfacing Living and Synthetic Cells as an Emerging Frontier in Synthetic Biology

Elani, Yuval

doi:10.1002/ange.202006941

Cited by 19 publications

(12 citation statements)

References 110 publications

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“…Within this framework, we outline recent findings and achievements in addition to outstanding goals and unrealized needs in the synthetic tissue field. We limit ourselves to synthetic tissue considerations as comprehensive reviews on single synthetic cells have been published elsewhere. − We also attempt, where appropriate, to mention quantitative aspects of the systems since tissue properties are sensitive to molecular binding strengths and forces. We hope that this review acts to galvanize the field to fill in the gaps on the road to engineering synthetic cells with tissue-scale behavior.…”

Section: Introductionmentioning

confidence: 99%

Engineering Tissue-Scale Properties with Synthetic Cells: Forging One from Many

2023

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In metazoans, living cells achieve capabilities beyond individual cell functionality by assembling into multicellular tissue structures. These higher-order structures represent dynamic, heterogeneous, and responsive systems that have evolved to regenerate and coordinate their actions over large distances. Recent advances in constructing micrometer-sized vesicles, or synthetic cells, now point to a future where construction of synthetic tissue can be pursued, a boon to pressing material needs in biomedical implants, drug delivery systems, adhesives, filters, and storage devices, among others. To fully realize the potential of synthetic tissue, inspiration has been and will continue to be drawn from new molecular findings on its natural counterpart. In this review, we describe advances in introducing tissue-scale features into synthetic cell assemblies. Beyond mere complexation, synthetic cells have been fashioned with a variety of natural and engineered molecular components that serve as initial steps toward morphological control and patterning, intercellular communication, replication, and responsiveness in synthetic tissue. Particular attention has been paid to the dynamics, spatial constraints, and mechanical strengths of interactions that drive the synthesis of this next-generation material, describing how multiple synthetic cells can act as one.

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Section: Introductionmentioning

confidence: 99%

Engineering Tissue-Scale Properties with Synthetic Cells: Forging One from Many

2023

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“…Synthetic protobiology is concerned with the construction, reconstitution, and functionalization of individual cell-like entities, − development of living cell/synthetic cell constructs (cellular bionics) and signaling networks, − and implementation of protocell dynamics and chemical communication in populations of artificial cells. − Studies of dispersed protocell communities explore contact-dependent and through-space chemical interactions as steps toward the development of higher-order cytomimetic behaviors such as division and growth, prototissue assembly, − signal processing, ,− self-sorting, and DNA-based computation. , Nested communities of synthetic cells can be prepared by sequential processing or microfluidic techniques to produce vesicle-in-vesicle, proteinosome-in-proteinosome, polymersome-in-polymersome, polymersome-in-polymer capsule, coacervate-in-coacervate droplet, and living cell-in-vesicle , arrangements. Alternatively, properties such as wetting and interfacial tension can be utilized for the development of physically interactive artificial cell communities that exhibit behaviors such as artificial phagocytosis, parasitism, and predation − to produce nested protocells via mechanisms of engulfment, processing, and functional integration (artificial endosymbiosis).…”

Section: Introductionmentioning

confidence: 99%

Autonomic Integration in Nested Protocell Communities

Yin

Gao

et al. 2023

J. Am. Chem. Soc.

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The self-driven organization of model protocells into higher-order nested cytomimetic systems with coordinated structural and functional relationships offers a step toward the autonomic implementation of artificial multicellularity. Here, we describe an endosymbiotic-like pathway in which proteinosomes are captured within membranized alginate/silk fibroin coacervate vesicles by guest-mediated reconfiguration of the host protocells. We demonstrate that interchange of coacervate vesicle and droplet morphologies through proteinosome-mediated urease/glucose oxidase activity produces discrete nested communities capable of integrated catalytic activity and selective disintegration. The self-driving capacity is modulated by an internalized fuel-driven process using starch hydrolases sequestered within the host coacervate phase, and structural stabilization of the integrated protocell populations can be achieved by on-site enzyme-mediated matrix reinforcement involving dipeptide supramolecular assembly or tyramine−alginate covalent cross-linking. Our work highlights a semi-autonomous mechanism for constructing symbiotic cell-like nested communities and provides opportunities for the development of reconfigurable cytomimetic materials with structural, functional, and organizational complexity.

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“…[ 30–32 ] When aiming to develop a digestive protocell, these smart multicompartments need to have the following features: i) switchable and controlled membrane permeability and controlled degradation which is spatially and time‐resolved, ii) high stability of the digestive enzyme such as a peptidase which can be achieved by anchoring the enzyme in the nanocompartment, allowing long‐term function and preserving the integrity of the other biological compartments, and iii) controlled size‐dependent capture and degradation of pathogens, as a step further toward personalized therapies. [ 31,33,34 ] Although enormous challenges remain, this work contributes to the simplification and standardization of an artificial cell with digestive properties besides first successfully reported work of phagocytosis‐like uptake of larger (sub‐)microobjects (e.g., bacteria or solid particles) by synthetic cells. [ 35–37 ]…”

Section: Introductionmentioning

confidence: 99%

Biomimetic Protocells Featuring Macrophage‐Like Capture and Digestion of Protein Pathogens

Xu,

Moreno,

Gentzel

et al. 2023

Small Methods

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Modern medical research develops interest in sophisticated artificial nano‐ and microdevices for future treatment of human diseases related to biological dysfunctions. This covers the design of protocells capable of mimicking the structure and functionality of eukaryotic cells. The authors use artificial organelles based on trypsin‐loaded pH‐sensitive polymeric vesicles to provide macrophage‐like digestive functions under physiological conditions. Herein, an artificial cell is established where digestive artificial organelles (nanosize) are integrated into a protocell (microsize). With this method, mimicking crossing of different biological barriers, capture of model protein pathogens, and compartmentalized digestive function are possible. This allows the integration of different components (e.g., dextran as stabilizing block) and the diffusion of pathogens in simulated cytosolic environment under physiological conditions. An integrated characterization approach is carried out, with identifying electrospray ionization mass spectrometry as an excellent detection method for the degradation of a small peptide such as β‐amyloid. The degradation of model enzymes is measured by enzyme activity assays. This work is an important contribution to effective biomimicry with the design of cell‐like functions having potential for therapeutic action.

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Interfacing Living and Synthetic Cells as an Emerging Frontier in Synthetic Biology

Cited by 19 publications

References 110 publications

Engineering Tissue-Scale Properties with Synthetic Cells: Forging One from Many

Engineering Tissue-Scale Properties with Synthetic Cells: Forging One from Many

Autonomic Integration in Nested Protocell Communities

Biomimetic Protocells Featuring Macrophage‐Like Capture and Digestion of Protein Pathogens

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