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Downloaded 10/4/2021 4:59:49 AM Lab on a Chip View Article Online TUTORIAL REVIEW View Journal | View Issue Droplet microfluidics for the construction of Cite this: Lab Chip,2018,18,2488 compartmentalised model membranes T. Trantidou, †a M. S. Friddin, †a A. Salehi-Reyhani, †abc O. Ces *abc and Y. Elani *abc The design of membrane-based constructs with multiple compartments is of increasing importance given their potential applications as microreactors, as artificial cells in synthetic-biology, as simplified cell models, and as drug delivery vehicles. The emergence of droplet microfluidics as a tool for their construction has allowed rapid scale-up in generation throughput, scale-down of size, and control over gross membrane ar- chitecture. This is true on several levels: size, level of compartmentalisation and connectivity of compart- ments can all be programmed to various degrees. This tutorial review explains and explores the reasons behind this. We discuss microfluidic strategies for the generation of a family of compartmentalised systems Received 10th January 2018, that have lipid membranes as the basic structural motifs, where droplets are either the fundamental build- Accepted 20th June 2018 Creative Commons Attribution 3.0 Unported Licence. ing blocks, or are precursors to the membrane-bound compartments. We examine the key properties as- sociated with these systems (including stability, yield, encapsulation efficiency), discuss relevant device fab- DOI: 10.1039/c8lc00028j rication technologies, and outline the technical challenges. In doing so, we critically review the state-of- rsc.li/loc play in this rapidly advancing field. 1. Introduction Membranes comprised of phospholipid bilayers are essential a Department of Chemistry, Imperial College London, London, SW7 2AZ, UK. to the function of all living cells. They serve as a critical bar- This article is licensed under a E-mail: [email protected], [email protected] rier between the cell and its environment, and are necessary b Institute of Chemical Biology, Imperial College London, London, SW7 2AZ, UK c fabriCELL, Imperial College London, SW7 2AZ, UK for intracellular structure and communication. Bilayer mem- † Authors contributed equally to this work. branes provide mechanical supports for anchoring the Open Access Article. Published on 01 August 2018. Downloaded 10/4/2021 4:59:49 AM. Tatiana Trantidou received her Mark Friddin received his PhD PhD (2014) in biomedical in Electrical Engineering from electronics from Imperial College the University of Southampton London, UK. From 2014–2015 (2014), was awarded a Master she worked as a post-doctoral re- of Engineering in micro- and searchscientistattheSouth- nano-technology from the Uni- ampton Nanofabrication Centre versity of Liverpool (2009) and (UK) on the development of has a Bachelors degree in Bio- novel digital manufacturing tech- chemistry from the University of nologies for biomedical applica- Nottingham (2008). His exper- tions. Since 2015, she is a Re- tise is in the assembly, search Fellow at the Department functionalisation and electrical Tatiana Trantidou of Chemistry developing techno- Mark Friddin characterisation of model mem- logical platforms to scale up the branes formed between aqueous production of smart therapeutics. Her research interests are on microdroplets in oil. Since joining the Chemistry Department at conventional and unconventional micro/nanofabrication technolo- Imperial College in 2015 his research has mainly focused on the gies for tissue engineering and for micro/nanofluidics for synthetic development of new micro- and opto-fluidic platform technologies biology. She is author of 15 journal papers, 1 patent and 12 con- for constructing model membranes, particularly using rapid ference papers. prototyping. 2488 | Lab Chip,2018,18, 2488–2509 This journal is © The Royal Society of Chemistry 2018 View Article Online Lab on a Chip Tutorial review molecular machinery required to regulate the exchange of cades, lipid bilayer constructs have been formed as bilayer metabolic components and chemical signals between the cell encapsulated fluid spheres (lipid vesicles/liposomes), black interior and exterior, and can act as 2D surfaces which bio- lipid membranes (BLMs) and supported lipid bilayers – chemical reactions take place on.1 Membranes are known to (SLBs),2 4 although new classes of multi-compartment struc- be highly dynamic fluid surfaces, serving a multitude of pur- tures are increasingly being developed. poses and have been the focus of intensive research for many The broad adoption of these biomimetic model architec- decades.2 tures has led to success in studying reconstituted membrane Such features have long motivated interest in studying the proteins,2 bilayer phase behaviour,5,6 and the lateral organi- biophysical properties of lipid bilayers and membrane pro- sation of membranes.7 Such achievements have motivated re- teins using model architectures engineered from user- cent interest in developing approaches beyond simply assem- defined mixtures of phospholipids and cell extracts. For de- bling single membranes, and towards engineering spatially organised multi-compartment architectures that more closely resemble biological cells. In this sense, spatially distinct, Dr. Ali Salehi-Reyhani is an inter-communicating compartments are likely to be vital for EPSRC-UKRI Innovation Fellow providing the complexity necessary to serve higher-order at Imperial College London functions. This is best evident in cells where various biologi- where he leads the Systems and cal functions are performed using membranes – trafficking Synthetic Biology group, of material within and between organelles as well as extracel- conducting multidisciplinary re- lular signalling and exchange of cargo are all enabled by search and leveraging transla- membranes and compartmentalisation across a broad range tional activity to drive impacts of length-scales. These processes emphasise the degree of or- on healthcare. He pioneered ganisation required on the microscale and how this, in turn, Creative Commons Attribution 3.0 Unported Licence. single molecule microfluidic supports the emergence of the collective ordering of cells on platforms for single cell analy- the macroscale. sis supporting over £10m in re- The advantages of compartmentalisation arise from the Ali Salehi-Reyhani search funding. His microfluidic spatial organisation of chemical species in space. This en- expertise is also helping to ables the establishment of concentration gradients, mainte- miniaturise high-performance liquid chromatography for point- nance of non-equilibrium states, isolation of otherwise inter- of-care, has founded several spinouts and sits on scientific advi- fering processes, and the existence of spatially distinct sory boards for MedTech start-ups. His interest in bottom-up microenvironments chemically optimised for defined pur- synthetic biology lies in the opportunity to create simplified cell poses. These features are utilised by cells, but can also be This article is licensed under a mimetics to understand the underlying mechanisms of cell taken advantage of in the construction of artificial function. membrane-bound microsystems. Multi-compartment Open Access Article. Published on 01 August 2018. Downloaded 10/4/2021 4:59:49 AM. OscarCesisaProfessorof Yuval is an EPSRC Research Fel- Chemical Biology at the Depart- low at Imperial College. His ment of Chemistry at Imperial group works in the areas of Soft College London and a Fellow of Microsystems Engineering and the Royal Society of Chemistry. Chemical Synthetic Biology. He He is currently Director of the received multidisciplinary train- Institute of Chemical Biology ing at Cambridge and Imperial, (ICB), the EPSRC ICB Centre for and has expertise in soft-matter, Doctoral Training, the microfluidics, optofluidics, chem- Leverhulme Doctoral Training ical biology, and biophysics. He Centre for Cellular Bionics and is particularly interested in ex- Co-Director of both fabriCELL ploring biointerfaces between liv- Oscar Ces and the Imperial College Ad- Yuval Elani ing and synthetic cells and in op- vanced Hackspace. His research tical manipulation techniques is focussed on biomembrane engineering, drug-membrane interac- for synthetic biology. Yuval's work has been recognised through tions, biomimicry, soft condensed matter, chemical biology, micro- awards from the Royal Society of Chemistry, World Economic Fo- fluidics, artificial cells, single cell analysis and lipid membrane rum, and the Parliamentary and Scientific Committee. He co- mechanics. founded the fabriCELL centre for artificial cell research and the Cellular Bionics Doctoral Training Centre. This journal is © The Royal Society of Chemistry 2018 Lab Chip,2018,18,2488–2509 | 2489 View Article Online Tutorial review Lab on a Chip architectures have potential as microreactor chassis,8,9 where large-scale networked assemblies existing in a bulk oil envi- individual steps of multi-step reactions occur in isolated ronment. These structures are illustrated in Fig. 1A. compartments with different chemical conditions (different These bilayer constructs offer exciting possibilities for pH, redox states, solvents, buffers etc.). bottom-up synthetic biologists. However precise control over Compartmentalisation aids the development of responsive architecture, compartment number, size and connectivity, systems, where membranes can be broken down selectively and the content of the membrane and encapsulated cargo in response to defined stimuli,
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