Biomimicry of Cellular Motility and Communication Based on Synthetic Soft-Architectures.

Cells, sophisticated membrane-bound units that contain the fundamental molecules of life, provide a precious library for inspiration and motivation for both society and academia. Scientists from various disciplines have made great endeavors toward the understanding of the cellular evolution by engineering artificial counterparts (protocells) that mimic or initiate structural or functional cellular aspects. In this regard, several works have discussed possible building blocks, designs, functions, or dynamics that can be applied to achieve this goal. Although great progress has been made, fundamental-yet complex-behaviors such as cellular communication, responsiveness to environmental cues, and motility remain a challenge, yet to be resolved. Herein, recent efforts toward utilizing soft systems for cellular mimicry are summarized-following the main outline of cellular evolution, from basic compartmentalization, and biological reactions for energy production, to motility and communicative behaviors between artificial cell communities or between artificial and natural cell communities. Finally, the current challenges and future perspectives in the field are discussed, hoping to inspire more future research and to help the further advancement of this field.

[1]  P. Thordarson,et al.  Polymersomes as protocellular constructs , 2017 .

[2]  S. Mann,et al.  Membrane-mediated cascade reactions by enzyme-polymer proteinosomes. , 2014, Chemical communications.

[3]  Nikodem Tomczak,et al.  Multicompartmentalized polymersomes for selective encapsulation of biomacromolecules. , 2011, Chemical communications.

[4]  Dirk van Swaay,et al.  Microfluidic methods for forming liposomes. , 2013, Lab on a chip.

[5]  J. Schlenoff,et al.  Driving Forces for Oppositely Charged Polyion Association in Aqueous Solutions: Enthalpic, Entropic, but Not Electrostatic. , 2016, Journal of the American Chemical Society.

[6]  A. Najer,et al.  Mimicking Cellular Signaling Pathways within Synthetic Multicompartment Vesicles with Triggered Enzyme Activity and Induced Ion Channel Recruitment , 2019, Advanced Functional Materials.

[7]  Jie Tian,et al.  Reversibly Switching Bilayer Permeability and Release Modules of Photochromic Polymersomes Stabilized by Cooperative Noncovalent Interactions. , 2015, Journal of the American Chemical Society.

[8]  Philip C Bevilacqua,et al.  RNA catalysis through compartmentalization. , 2012, Nature chemistry.

[9]  Bastiaan C. Buddingh,et al.  Hierarchical Self-Assembly of a Copolymer-Stabilized Coacervate Protocell , 2017, Journal of the American Chemical Society.

[10]  J. Zasadzinski,et al.  Design and In Situ Characterization of Lipid Containers with Enhanced Drug Retention , 2011, Advanced materials.

[11]  Zuleykhan Tomova,et al.  Hydrodynamically driven self-assembly of giant vesicles of metal nanoparticles for remote-controlled release. , 2013, Angewandte Chemie.

[12]  T. Tang,et al.  Polynucleotides in cellular mimics: Coacervates and lipid vesicles , 2016 .

[13]  P. Zhou,et al.  In Situ Generation of Core‐Shell Protein‐Based Microcapsules with Regulated Ion Absorbance Capacity , 2017 .

[14]  Xin Huang,et al.  Construction of biological hybrid microcapsules with defined permeability towards programmed release of biomacromolecules. , 2017, Chemical communications.

[15]  Vincent Noireaux,et al.  A vesicle bioreactor as a step toward an artificial cell assembly. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Qiang He,et al.  Near-infrared light-driven Janus capsule motors: Fabrication, propulsion, and simulation , 2016, Nano Research.

[17]  Yutetsu Kuruma,et al.  Synthetic cells produce a quorum sensing chemical signal perceived by Pseudomonas aeruginosa. , 2018, Chemical communications.

[18]  Lei Wang,et al.  Interfacial self-assembly of gold nanoparticle-polymer nanoconjugates into microcapsules with near-infrared light modulated biphasic catalysis efficiency. , 2019, Chemical communications.

[19]  Shoji Takeuchi,et al.  Formation of giant lipid vesiclelike compartments from a planar lipid membrane by a pulsed jet flow. , 2007, Journal of the American Chemical Society.

[20]  S. Mansy,et al.  Toward long-lasting artificial cells that better mimic natural living cells , 2019, Emerging topics in life sciences.

[21]  Stephen Mann,et al.  Chloroplast-containing coacervate micro-droplets as a step towards photosynthetically active membrane-free protocells† †Electronic supplementary information (ESI) available: Details of experiments, microscopy data, supplementary videos, photosynthetic assay data, zeta measurements and schematic of s , 2018, Chemical communications.

[22]  Stephen Mann,et al.  Enzyme-powered motility in buoyant organoclay/DNA protocells , 2018, Nature Chemistry.

[23]  M. Klein,et al.  Self-assembly of amphiphilic Janus dendrimers into uniform onion-like dendrimersomes with predictable size and number of bilayers , 2014, Proceedings of the National Academy of Sciences.

[24]  Benjamin G Davis,et al.  Sugar synthesis in a protocellular model leads to a cell signalling response in bacteria. , 2009, Nature chemistry.

[25]  Jiwei Cui,et al.  Innovation in Layer-by-Layer Assembly. , 2016, Chemical reviews.

[26]  Soodabeh Davaran,et al.  Liposome: classification, preparation, and applications , 2013, Nanoscale Research Letters.

[27]  A. Golestani,et al.  Interaction of hexokinase with the outer mitochondrial membrane and a hydrophobic matrix , 2001, Molecular and Cellular Biochemistry.

[28]  Christine D. Keating,et al.  Aqueous Phase Separation as a Possible Route to Compartmentalization of Biological Molecules , 2012, Accounts of chemical research.

[29]  P. Beales,et al.  Nature's lessons in design: nanomachines to scaffold, remodel and shape membrane compartments. , 2015, Physical chemistry chemical physics : PCCP.

[30]  Yiyong Mai,et al.  Self-assembly of block copolymers. , 2012, Chemical Society reviews.

[31]  Giuseppe Battaglia,et al.  Synthetic bio-nanoreactor: mechanical and chemical control of polymersome membrane permeability. , 2012, Angewandte Chemie.

[32]  Edward S Boyden,et al.  Engineering genetic circuit interactions within and between synthetic minimal cells , 2016, Nature chemistry.

[33]  Stephen Mann,et al.  Gene-Mediated Chemical Communication in Synthetic Protocell Communities. , 2017, ACS synthetic biology.

[34]  Stephen Mann,et al.  Electrostatically gated membrane permeability in inorganic protocells. , 2015 .

[35]  P. Walde,et al.  Permeability Enhancement of Lipid Vesicles to Nucleotides by Use of Sodium Cholate: Basic Studies and Application to an Enzyme-Catalyzed Reaction Occurring inside the Vesicles , 2002 .

[36]  P. Zhou,et al.  Multifunctional and Programmable Modulated Interface Reactions on Proteinosomes. , 2018, ACS applied materials & interfaces.

[37]  Stephen Mann,et al.  Predatory behaviour in synthetic protocell communities. , 2017, Nature chemistry.

[38]  Daniel A Fletcher,et al.  Unilamellar vesicle formation and encapsulation by microfluidic jetting , 2008, Proceedings of the National Academy of Sciences.

[39]  Petra Schwille,et al.  Liposomes and polymersomes: a comparative review towards cell mimicking. , 2018, Chemical Society reviews.

[40]  D. Appelhans,et al.  A facile and universal method to efficiently fabricate diverse protein capsules for multiple potential applications. , 2019, ACS applied materials & interfaces.

[41]  G. Battaglia,et al.  Chemotactic synthetic vesicles: Design and applications in blood-brain barrier crossing , 2016, Science Advances.

[42]  A. Patil,et al.  Modulation of Higher‐order Behaviour in Model Protocell Communities by Artificial Phagocytosis , 2019, Angewandte Chemie.

[43]  Madhavan Nallani,et al.  A three-enzyme cascade reaction through positional assembly of enzymes in a polymersome nanoreactor. , 2009, Chemistry.

[44]  Lei Wang,et al.  Dynamic Behaviours in Microcompartments. , 2019, Chemistry.

[45]  S. Turgeon,et al.  Protein–polysaccharide complexes and coacervates , 2007 .

[46]  Joseph J. Richardson,et al.  Technology-driven layer-by-layer assembly of nanofilms , 2015, Science.

[47]  M. Antognozzi,et al.  Small-molecule uptake in membrane-free peptide/nucleotide protocells , 2013 .

[48]  C. Keating,et al.  Phosphorylation-mediated RNA/peptide complex coacervation as a model for intracellular liquid organelles. , 2016, Nature chemistry.

[49]  Nikodem Tomczak,et al.  Self-assembled architectures with multiple aqueous compartments , 2012 .

[50]  Frank Caruso,et al.  Layer-by-layer-assembled capsules and films for therapeutic delivery. , 2010, Small.

[51]  S. Sánchez,et al.  Lipase-Powered Mesoporous Silica Nanomotors for Triglyceride Degradation. , 2019, Angewandte Chemie.

[52]  Daeyeon Lee,et al.  Double emulsion templated monodisperse phospholipid vesicles. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[53]  Pasquale Stano,et al.  Giant Vesicles: Preparations and Applications , 2010, Chembiochem : a European journal of chemical biology.

[54]  Giuseppe Battaglia,et al.  Novel aspects of encapsulation and delivery using polymersomes. , 2014, Current opinion in pharmacology.

[55]  Rona Chandrawati,et al.  A microreactor with thousands of subcompartments: enzyme-loaded liposomes within polymer capsules. , 2009, Angewandte Chemie.

[56]  H. Umakoshi,et al.  Kinetic study on giant vesicle formation with electroformation method. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[57]  S. Mann,et al.  Response-retaliation behaviour in synthetic protocell communities. , 2019, Angewandte Chemie.

[58]  K. Jarrell,et al.  The surprisingly diverse ways that prokaryotes move , 2008, Nature Reviews Microbiology.

[59]  Changyou Gao,et al.  Layer-by-layer assembly of microcapsules and their biomedical applications. , 2012, Chemical Society reviews.

[60]  B. Voit,et al.  Engineering Functional Polymer Capsules toward Smart Nanoreactors. , 2016, Chemical reviews.

[61]  V. Kolb Handbook of Astrobiology , 2018 .

[62]  David S. Williams,et al.  Polymer/nucleotide droplets as bio-inspired functional micro-compartments , 2012 .

[63]  Luis E Contreras-Llano,et al.  Minimizing Context Dependency of Gene Networks Using Artificial Cells. , 2018, ACS applied materials & interfaces.

[64]  Stephen Mann,et al.  Interfacial assembly of protein–polymer nano-conjugates into stimulus-responsive biomimetic protocells , 2013, Nature Communications.

[65]  Fernando Albericio,et al.  Engineering advanced capsosomes: maximizing the number of subcompartments, cargo retention, and temperature-triggered reaction. , 2010, ACS nano.

[66]  W. Cao,et al.  Electroformation of giant unilamellar vesicles using interdigitated ITO electrodes , 2013 .

[67]  Yudong Huang,et al.  A facile approach for the reduction of 4‑nitrophenol and degradation of congo red using gold nanoparticles or laccase decorated hybrid inorganic nanoparticles/polymer-biomacromolecules vesicles. , 2019, Materials science & engineering. C, Materials for biological applications.

[68]  Philip C Bevilacqua,et al.  Bioreactor droplets from liposome-stabilized all-aqueous emulsions , 2014, Nature Communications.

[69]  Jessica L. Terrell,et al.  Integrating artificial with natural cells to translate chemical messages that direct E. coli behaviour , 2014, Nature Communications.

[70]  Jan C. M. van Hest,et al.  Mimicking Cellular Compartmentalization in a Hierarchical Protocell through Spontaneous Spatial Organization , 2019, ACS central science.

[71]  P. Formánek,et al.  Functional Cellular Mimics for the Spatiotemporal Control of Multiple Enzymatic Cascade Reactions. , 2017, Angewandte Chemie.

[72]  Jan C M van Hest,et al.  Positional assembly of enzymes in polymersome nanoreactors for cascade reactions. , 2007, Angewandte Chemie.

[73]  Hagan Bayley Building blocks for cells and tissues: Beyond a game , 2019 .

[74]  Björn Stuhrmann,et al.  Encapsulation of active cytoskeletal protein networks in cell-sized liposomes. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[75]  Hao Sun,et al.  Architecture-transformable polymers: Reshaping the future of stimuli-responsive polymers , 2019, Progress in Polymer Science.

[76]  Stephen Mann,et al.  Peptide-nucleotide microdroplets as a step towards a membrane-free protocell model. , 2011, Nature chemistry.

[77]  Maïté Marguet,et al.  Cascade reactions in multicompartmentalized polymersomes. , 2014, Angewandte Chemie.

[78]  Mathias Winterhalter,et al.  Reconstitution of Channel Proteins in (Polymerized) ABA Triblock Copolymer Membranes , 2000 .

[79]  Qiang He,et al.  Near infrared-modulated propulsion of catalytic Janus polymer multilayer capsule motors. , 2015, Chemical communications.

[80]  F. Simmel,et al.  Chemical communication between bacteria and cell-free gene expression systems within linear chains of emulsion droplets. , 2016, Integrative biology : quantitative biosciences from nano to macro.

[81]  Loai K. E. A. Abdelmohsen,et al.  Spatial Organization in Proteinaceous Membrane-Stabilized Coacervate Protocells. , 2019, Small.

[82]  Jan C M van Hest,et al.  Stimuli-responsive polymersomes and nanoreactors. , 2016, Journal of materials chemistry. B.

[83]  Lei Wang,et al.  Continuous Microfluidic Self-Assembly of Hybrid Janus-Like Vesicular Motors: Autonomous Propulsion and Controlled Release. , 2015, Small.

[84]  T. Pott,et al.  Giant unilamellar vesicle formation under physiologically relevant conditions. , 2008, Chemistry and physics of lipids.

[85]  Ferran Feixas,et al.  Intrinsic enzymatic properties modulate the self-propulsion of micromotors , 2019, Nature Communications.

[86]  D. Wilson,et al.  Entrapment of metal nanoparticles in polymer stomatocytes. , 2012, Journal of the American Chemical Society.

[87]  Xin Huang,et al.  Synthetic cellularity based on non-lipid micro-compartments and protocell models. , 2014, Current opinion in chemical biology.

[88]  S. Mann,et al.  Single-step fabrication of multi-compartmentalized biphasic proteinosomes. , 2017, Chemical communications.

[89]  Marlies Nijemeisland,et al.  Dynamic Loading and Unloading of Proteins in Polymeric Stomatocytes: Formation of an Enzyme-Loaded Supramolecular Nanomotor. , 2016, ACS nano.

[90]  Maaruthy Yelleswarapu,et al.  Microfluidic Assembly of Monodisperse Vesosomes as Artificial Cell Models. , 2017, Journal of the American Chemical Society.

[91]  F. Gervasio,et al.  Molecular engineering of polymersome surface topology , 2016, Science Advances.

[92]  D. Velegol,et al.  Motility of Enzyme-Powered Vesicles , 2019, bioRxiv.

[93]  Zhiguang Wu,et al.  Autonomous movement of controllable assembled Janus capsule motors. , 2012, ACS nano.

[94]  S. Diez,et al.  Assembled capsules transportation driven by motor proteins. , 2009, Biochemical and biophysical research communications.

[95]  J. Fei,et al.  Coassembly of Photosystem II and ATPase as Artificial Chloroplast for Light-Driven ATP Synthesis. , 2016, ACS nano.

[96]  Yudong Huang,et al.  Design and Construction of Hybrid Microcapsules with Higher‐Order Structure and Multiple Functions , 2017, Advanced science.

[97]  Kanaka Hettiarachchi,et al.  Controlled microfluidic encapsulation of cells, proteins, and microbeads in lipid vesicles. , 2006, Journal of the American Chemical Society.

[98]  David S. Williams,et al.  Stabilization and enhanced reactivity of actinorhodin polyketide synthase minimal complex in polymer-nucleotide coacervate droplets. , 2012, Chemical communications.

[99]  J. Gohy,et al.  Photo-responsive polymers: synthesis and applications , 2017 .

[100]  Yudong Huang,et al.  Programmable Modulation of Membrane Permeability of Proteinosome upon Multiple Stimuli Responses. , 2016, ACS macro letters.

[101]  Y. Maitani,et al.  Liposomes with temperature-responsive reversible surface properties. , 2019, Colloids and surfaces. B, Biointerfaces.

[102]  J. Szostak,et al.  Template-directed synthesis of a genetic polymer in a model protocell , 2008, Nature.

[103]  Wolfgang Meier,et al.  Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z , 2007, Proceedings of the National Academy of Sciences.

[104]  Xiaoman Liu,et al.  Engineering proteinosomes with renewable predatory behaviour towards living organisms , 2020, Materials Horizons.

[105]  S. Armes,et al.  Controlling polymersome surface topology at the nanoscale by membrane confined polymer/polymer phase separation. , 2011, ACS nano.

[106]  Darrell Velegol,et al.  Positive and negative chemotaxis of enzyme-coated liposome motors , 2019, Nature Nanotechnology.

[107]  Daniela A Wilson,et al.  Autonomous movement of platinum-loaded stomatocytes. , 2012, Nature chemistry.

[108]  S. Mann,et al.  Coordinated Membrane Fusion of Proteinosomes by Contact-Induced Hydrogel Self-Healing. , 2017, Small.

[109]  Michele Forlin,et al.  Two-Way Chemical Communication between Artificial and Natural Cells , 2017, ACS central science.

[110]  Reinhard Lipowsky,et al.  A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy , 2006, Journal of physics. Condensed matter : an Institute of Physics journal.

[111]  M. Klein,et al.  Bioactive cell-like hybrids from dendrimersomes with a human cell membrane and its components , 2018, Proceedings of the National Academy of Sciences.

[112]  Jianmin Song,et al.  Autonomic Behaviors in Lipase-Active Oil Droplets. , 2019, Angewandte Chemie.

[113]  Assaf Zinger,et al.  Synthetic Cells Synthesize Therapeutic Proteins inside Tumors , 2018, Advanced healthcare materials.

[114]  Maïté Marguet,et al.  Multicompartmentalized polymeric systems: towards biomimetic cellular structure and function. , 2013, Chemical Society reviews.

[115]  Brigitte Städler,et al.  A Critical Look at Multilayered Polymer Capsules in Biomedicine: Drug Carriers, Artificial Organelles, and Cell Mimics , 2011 .

[116]  J. V. van Hest,et al.  The hallmarks of living systems: towards creating artificial cells , 2018, Interface Focus.

[117]  A. Kishimura,et al.  Semipermeable polymer vesicle (PICsome) self-assembled in aqueous medium from a pair of oppositely charged block copolymers: physiologically stable micro-/nanocontainers of water-soluble macromolecules. , 2006, Journal of the American Chemical Society.

[118]  Ludwig Klermund,et al.  Biocatalysis in Polymersomes: Improving Multienzyme Cascades with Incompatible Reaction Steps by Compartmentalization , 2017 .

[119]  D. Appelhans,et al.  Fine-tuning the pH response of polymersomes for mimicking and controlling the cell membrane functionality , 2017 .

[120]  Sameer Jadhav,et al.  Chemistry and Physics of Lipids , 2013 .

[121]  Jan C. M. van Hest,et al.  A Compartmentalized Out-of-Equilibrium Enzymatic Reaction Network for Sustained Autonomous Movement , 2016, ACS central science.

[122]  Daniela A Wilson,et al.  Fuel concentration dependent movement of supramolecular catalytic nanomotors. , 2013, Nanoscale.

[123]  D. B. Kearns,et al.  A field guide to bacterial swarming motility , 2010, Nature Reviews Microbiology.

[124]  Jan C. M. van Hest,et al.  Multifaceted cell mimicry in coacervate-based synthetic cells. , 2019, Emerging topics in life sciences.

[125]  Daniela A Wilson,et al.  Self-propelled supramolecular nanomotors with temperature-responsive speed regulation. , 2017, Nature chemistry.

[126]  C. Palivan,et al.  How do the properties of amphiphilic polymer membranes influence the functional insertion of peptide pores? , 2019, Biomacromolecules.

[127]  M. Tirrell,et al.  Thermodynamic characterization of polypeptide complex coacervation. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[128]  Jan Steyaert,et al.  Therapeutic nanoreactors: combining chemistry and biology in a novel triblock copolymer drug delivery system. , 2005, Nano letters.

[129]  K. Goldie,et al.  Confined multiple enzymatic (cascade) reactions within poly(dopamine)-based capsosomes. , 2014, ACS applied materials & interfaces.

[130]  H. Möhwald,et al.  Movement of polymer microcarriers using a biomolecular motor. , 2010, Biomaterials.

[131]  G. Bolognesi,et al.  Sculpting and fusing biomimetic vesicle networks using optical tweezers , 2018, Nature Communications.