Compartmentalized reactions as a case of soft-matter biotechnology: synthesis of proteins and nucleic acids inside lipid vesicles

In this mini-review we would like to summarize the recent advances in the field of protein and nucleic acid synthesis inside lipid vesicles (liposomes). This research, which originated within the origin of life community, is now recognized as an example of synthetic biology. Current approaches are based on the convergence of liposome technology and cell-free in vitro technology. In particular, in addition to the classical liposome preparation methods, the new water-in-oil droplet transfer method appears very interesting for progressing in the assembly of these cell-like systems, possibly in combination with microfluidic devices. As an alternative to cell extract, the use of a transcription/translation kit composed of purified components is also presented as a new tool for carrying out protein synthesis inside liposomes. Data presented in the literature are collected and shortly discussed, and the potential relevance of this new soft-matter biotechnology in various research fields is also commented on.

[1]  Irene A. Chen,et al.  The Emergence of Competition Between Model Protocells , 2004, Science.

[2]  Pasquale Stano,et al.  Approaches to semi-synthetic minimal cells: a review , 2005, Naturwissenschaften.

[3]  Geoffrey Chang,et al.  The past, present and future of cell-free protein synthesis. , 2005, Trends in biotechnology.

[4]  Natalio Krasnogor,et al.  The imitation game—a computational chemical approach to recognizing life , 2006, Nature Biotechnology.

[5]  Florian Hollfelder,et al.  The potential of microfluidic water-in-oil droplets in experimental biology. , 2009, Molecular bioSystems.

[6]  Fabio Mavelli,et al.  On the way towards 'basic autonomous agents': Stochastic simulations of minimal lipid-peptide cells , 2008, Biosyst..

[7]  Sophie Pautot,et al.  Engineering asymmetric vesicles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  J. Hillebrecht,et al.  A comparative study of protein synthesis in in vitro systems: from the prokaryotic reconstituted to the eukaryotic extract-based , 2008, BMC biotechnology.

[9]  R. Mart,et al.  Creating Functional Vesicle Assemblies from Vesicles and Nanoparticles , 2009, Pharmaceutical Research.

[10]  Pier Luigi Luisi,et al.  Giant Vesicles as Biochemical Compartments: The Use of Microinjection Techniques , 1998 .

[11]  P. Luisi Autopoiesis: a review and a reappraisal , 2003, Naturwissenschaften.

[12]  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 .

[13]  M. Abkarian,et al.  Dynamics of vesicles in a wall-bounded shear flow. , 2005, Biophysical journal.

[14]  Lingling Chen,et al.  SecA protein is required for secretory protein translocation into E. coli membrane vesicles , 1988, Cell.

[15]  Shigemichi Nishikawa,et al.  Establishment and characterization of cell-free translation/glycosylation in insect cell (Spodoptera frugiperda 21) extract prepared with high pressure treatment , 2001, Applied Microbiology and Biotechnology.

[16]  D. Deamer,et al.  Lipid-assisted Synthesis of RNA-like Polymers from Mononucleotides , 2008, Origins of Life and Evolution of Biospheres.

[17]  F. Caruso,et al.  Enzyme encapsulation in layer-by-layer engineered polymer multilayer capsules. , 2000 .

[18]  N. Chaniotakis,et al.  Fluorescence detection of enzymatic activity within a liposome based nano-biosensor. , 2005, Biosensors & bioelectronics.

[19]  M. Homma,et al.  Dynamic behavior of giant liposomes at desired osmotic pressures. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[20]  George M Church,et al.  Towards synthesis of a minimal cell , 2006, Molecular systems biology.

[21]  P. Monnard,et al.  Liposome-entrapped Polymerases as Models for Microscale/Nanoscale Bioreactors , 2003, The Journal of Membrane Biology.

[22]  M. Yoshimoto,et al.  Novel immobilized liposomal glucose oxidase system using the channel protein OmpF and catalase. , 2005, Biotechnology and bioengineering.

[23]  A. Suyama,et al.  Compartment size dependence of performance of polymerase chain reaction inside giant vesicles , 2011 .

[24]  Alberto Diaspro,et al.  Protein synthesis in liposomes with a minimal set of enzymes. , 2007, Biochemical and biophysical research communications.

[25]  Rick L. Stevens,et al.  Building the blueprint of life , 2010, Biotechnology journal.

[26]  David A. Weitz,et al.  Production of Unilamellar Vesicles Using an Inverted Emulsion , 2003 .

[27]  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.

[28]  Kensuke Kurihara,et al.  Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. , 2011, Nature chemistry.

[29]  A. Griffiths,et al.  Droplets as Microreactors for High‐Throughput Biology , 2007, Chembiochem : a European journal of chemical biology.

[30]  P. Luisi,et al.  Autopoietic Self-Reproduction of Fatty Acid Vesicles , 1994 .

[31]  Maik Hadorn,et al.  DNA-Mediated Self-Assembly of Artificial Vesicles , 2010, PloS one.

[32]  Y. Baba,et al.  Effect of cationic liposomes in an in vitro transcription and translation system. , 2002, Biological & pharmaceutical bulletin.

[33]  Brent D. Foy,et al.  Stochastic simulation and analysis of biomolecular reaction networks , 2009, BMC Systems Biology.

[34]  M. Hicks,et al.  Preparation and properties of vesicles enclosed by fatty acid membranes. , 1976, Chemistry and physics of lipids.

[35]  S. Yokoyama,et al.  A human cell-derived in vitro coupled transcription/translation system optimized for production of recombinant proteins. , 2008, Protein expression and purification.

[36]  Pier Luigi Luisi,et al.  Self‐Reproduction of Micelles and Vesicles: Models for the Mechanisms of Life from the Perspective of Compartmented Chemistry , 2007 .

[37]  David W. Deamer,et al.  Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions , 2005, Journal of Molecular Evolution.

[38]  D. Oesterhelt,et al.  Incorporation of in vitro synthesized GPCR into a tethered artificial lipid membrane system. , 2007, Angewandte Chemie.

[39]  Shigemichi Nishikawa,et al.  Direct preparation of giant proteo-liposomes by in vitro membrane protein synthesis. , 2008, Journal of biotechnology.

[40]  P. Bassereau,et al.  A minimal system allowing tubulation with molecular motors pulling on giant liposomes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Harold P. Erickson,et al.  Reconstitution of Contractile FtsZ Rings in Liposomes , 2008, Science.

[42]  Tetsuya Yomo,et al.  Quantifying epistatic interactions among the components constituting the protein translation system , 2009, Molecular systems biology.

[43]  E. Bamberg,et al.  Functional cell-free synthesis of a seven helix membrane protein: in situ insertion of bacteriorhodopsin into liposomes. , 2007, Journal of molecular biology.

[44]  A. Bangham,et al.  Membrane models with phospholipids. , 1968, Progress in biophysics and molecular biology.

[45]  P. Luisi,et al.  Cell‐free Protein Synthesis through Solubilisate Exchange in Water/Oil Emulsion Compartments , 2004, Chembiochem : a European journal of chemical biology.

[46]  Petra Schwille,et al.  Reconstitution and Anchoring of Cytoskeleton inside Giant Unilamellar Vesicles , 2008, Chembiochem : a European journal of chemical biology.

[47]  B. Paegel,et al.  Stepwise Synthesis of Giant Unilamellar Vesicles on a Microfluidic Assembly Line , 2011, Journal of the American Chemical Society.

[48]  T. Peterson,et al.  Membrane protein expression: no cells required. , 2009, Trends in biotechnology.

[49]  H. Bui,et al.  Cationic liposome can interfere mRNA translation in an E. coli cell-free translation system , 2010 .

[50]  Pasquale Stano,et al.  Minimal cells: Relevance and interplay of physical and biochemical factors , 2011, Biotechnology journal.

[51]  Wim E Hennink,et al.  Optimization and quantification of protein synthesis inside liposomes , 2010, Journal of liposome research.

[52]  Ikuo Morita,et al.  Direct formation of proteo-liposomes by in vitro synthesis and cellular cytosolic delivery with connexin-expressing liposomes. , 2009, Biomaterials.

[53]  D. Bartel,et al.  Synthesizing life : Paths to unforeseeable science & technology , 2001 .

[54]  Jennifer Lippincott-Schwartz,et al.  Membrane scission by the ESCRT-III complex , 2009, Nature.

[55]  Shoji Takeuchi,et al.  Microfluidic formation of monodisperse, cell-sized, and unilamellar vesicles. , 2009, Angewandte Chemie.

[56]  M. Yoshimoto,et al.  Enhancement of apparent substrate selectivity of proteinase K encapsulated in liposomes through a cholate‐induced alteration of the bilayer permeability , 2004, Biotechnology and bioengineering.

[57]  T. Rapoport Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes , 2007, Nature.

[58]  Pasquale Stano,et al.  Lecithin‐Based Water‐In‐Oil Compartments as Dividing Bioreactors , 2007, Chembiochem : a European journal of chemical biology.

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

[60]  Noah Malmstadt,et al.  Microfluidic fabrication of asymmetric giant lipid vesicles. , 2011, ACS applied materials & interfaces.

[61]  P. Luisi,et al.  Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. , 1995, Biochemical and biophysical research communications.

[62]  Pier Luigi Luisi,et al.  Autocatalytic self-replicating micelles as models for prebiotic structures , 1992, Nature.

[63]  D. Deamer,et al.  Oligomerization of Thioglutamic Acid: Encapsulated Reactions and Lipid Catalysis , 2007, Origins of Life and Evolution of Biospheres.

[64]  Thomas H Segall-Shapiro,et al.  Creation of a Bacterial Cell Controlled by a Chemically Synthesized Genome , 2010, Science.

[65]  G. F. Joyce,et al.  Self-Sustained Replication of an RNA Enzyme , 2009, Science.

[66]  Pasquale Stano,et al.  The Minimal Size of Liposome‐Based Model Cells Brings about a Remarkably Enhanced Entrapment and Protein Synthesis , 2009, Chembiochem : a European journal of chemical biology.

[67]  P. Holliger,et al.  Ribozyme-Catalyzed Transcription of an Active Ribozyme , 2011, Science.

[68]  Heinz Rüterjans,et al.  High level cell-free expression and specific labeling of integral membrane proteins. , 2004, European journal of biochemistry.

[69]  P. Luisi,et al.  Stereoselectivity Aspects in the Condensation of Racemic NCA−Amino Acids in the Presence and Absence of Liposomes , 2001 .

[70]  Pasquale Stano,et al.  Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. , 2010, Chemical communications.

[71]  M. Dogterom,et al.  Membrane tube formation from giant vesicles by dynamic association of motor proteins , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[72]  P. Walde,et al.  Fatty acid vesicles , 2007 .

[73]  Tetsuya Yomo,et al.  Detection of association and fusion of giant vesicles using a fluorescence-activated cell sorter. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[74]  M. Tomita,et al.  Efficient formation of giant liposomes through the gentle hydration of phosphatidylcholine films doped with sugar. , 2009, Colloids and surfaces. B, Biointerfaces.

[75]  P. Luisi,et al.  The Use of Liposomes for Constructing Cell Models , 2002, Journal of biological physics.

[76]  Pier Luigi Luisi,et al.  The Notion of a DNA Minimal Cell: A General Discourse and Some Guidelines for an Experimental Approach , 2002 .

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

[78]  Pasquale Stano,et al.  Chemical approaches to synthetic biology. , 2009, Current opinion in biotechnology.

[79]  Anthony G Lee,et al.  How lipids affect the activities of integral membrane proteins. , 2004, Biochimica et biophysica acta.

[80]  Yutetsu Kuruma,et al.  A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. , 2009, Biochimica et biophysica acta.

[81]  D. Deamer,et al.  Liposomes from ionic, single-chain amphiphiles. , 1978, Biochemistry.

[82]  Tadashi Sugawara,et al.  DNA polymerization on the inner surface of a giant liposome for synthesizing an artificial cell model. , 2006, Soft matter.

[83]  Pierre-Alain Monnard,et al.  Models of primitive cellular life: polymerases and templates in liposomes , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[84]  Kazufumi Hosoda,et al.  Quantitative study of the structure of multilamellar giant liposomes as a container of protein synthesis reaction. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[85]  Aldo Jesorka,et al.  Generation of phospholipid vesicle-nanotube networks and transport of molecules therein , 2011, Nature Protocols.

[86]  P. Luisi About Various Definitions of Life , 1998, Origins of life and evolution of the biosphere.

[87]  C. Keating,et al.  Polymer encapsulation within giant lipid vesicles. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[88]  P. Luisi,et al.  Spontaneous Protein Crowding in Liposomes: A New Vista for the Origin of Cellular Metabolism , 2010, Chembiochem : a European journal of chemical biology.

[89]  K. Yoshikawa,et al.  Protein Synthesis in Giant Liposomes Using the In Vitro Translation System of Thermococcus kodakaraensis , 2009, IEEE Transactions on NanoBioscience.

[90]  Mun'delanji C. Vestergaard,et al.  Construction of asymmetric cell-sized lipid vesicles from lipid-coated water-in-oil microdroplets. , 2008, The journal of physical chemistry. B.

[91]  Dennis E. Discher,et al.  Polymer vesicles : Materials science: Soft surfaces , 2002 .

[92]  E. Koonin,et al.  A minimal gene set for cellular life derived by comparison of complete bacterial genomes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Hirohide Saito,et al.  Time‐Resolved Tracking of a Minimum Gene Expression System Reconstituted in Giant Liposomes , 2009, Chembiochem : a European journal of chemical biology.

[94]  Takuya Ueda,et al.  Cell-free translation reconstituted with purified components , 2001, Nature Biotechnology.

[95]  R. Dowben,et al.  Formation and properties of thin‐walled phospholipid vesicles , 1969, Journal of cellular physiology.

[96]  D. Branton,et al.  Characterization of individual polynucleotide molecules using a membrane channel. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[97]  A. Theberge,et al.  Microdroplets in microfluidics: an evolving platform for discoveries in chemistry and biology. , 2010, Angewandte Chemie.

[98]  S. Kusumoto,et al.  A novel complete reconstitution system for membrane integration of the simplest membrane protein. , 2010, Biochemical and biophysical research communications.

[99]  A. Moya,et al.  Determination of the Core of a Minimal Bacterial Gene Set , 2004, Microbiology and Molecular Biology Reviews.

[100]  F. Mavelli,et al.  Stochastic simulations of minimal self-reproducing cellular systems , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[101]  E. Korn,et al.  Single bilayer liposomes prepared without sonication. , 1973, Biochimica et biophysica acta.

[102]  Pasquale Stano,et al.  Reactivity and fusion between cationic vesicles and fatty acid anionic vesicles. , 2010, Journal of colloid and interface science.

[103]  J. Lenormand,et al.  Production of membrane proteins using cell–free expression systems , 2007, Expert review of proteomics.

[104]  A. deMello,et al.  Droplet microfluidics: recent developments and future applications. , 2011, Chemical communications.

[105]  David Avnir,et al.  Enzymes and Other Proteins Entrapped in Sol-Gel Materials , 1994 .

[106]  Antoine Danchin,et al.  Synthetic biology: discovering new worlds and new words , 2008, EMBO reports.

[107]  T. Oberholzer,et al.  Giant Vesicles as Microreactors for Enzymatic mRNA Synthesis , 2002, Chembiochem : a European journal of chemical biology.

[108]  Takuya Ueda,et al.  Protein synthesis by pure translation systems. , 2005, Methods.

[109]  Kazufumi Hosoda,et al.  Replication of Genetic Information with Self‐Encoded Replicase in Liposomes , 2008, ChemBioChem.

[110]  Pier Luigi Luisi,et al.  Chemical Aspects of Synthetic Biology , 2007, Chemistry & biodiversity.

[111]  W. Meier,et al.  Nanoreactors from Polymer-Stabilized Liposomes , 2001 .

[112]  Fabio Mavelli,et al.  ENVIRONMENT: a computational platform to stochastically simulate reacting and self-reproducing lipid compartments , 2010, Physical biology.

[113]  M. Bally,et al.  Production of large unilamellar vesicles by a rapid extrusion procedure: characterization of size distribution, trapped volume and ability to maintain a membrane potential. , 1985, Biochimica et biophysica acta.

[114]  H. Bui,et al.  Liposome membrane itself can affect gene expression in the Escherichia coli cell-free translation system. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[115]  J W Szostak,et al.  Reconstructing the emergence of cellular life through the synthesis of model protocells. , 2009, Cold Spring Harbor symposia on quantitative biology.

[116]  D. Deamer,et al.  Membrane self‐assembly processes: Steps toward the first cellular life , 2002, The Anatomical record.

[117]  Daniel A. Fletcher,et al.  Biology under construction: in vitro reconstitution of cellular function , 2009, Nature Reviews Molecular Cell Biology.

[118]  Pier Luigi Luisi,et al.  OPARIN'S REACTIONS REVISITED : ENZYMATIC SYNTHESIS OF POLY(ADENYLIC ACID) IN MICELLES AND SELF-REPRODUCING VESICLES , 1994 .

[119]  M Wakabayashi,et al.  Synthesis of functional protein in liposome. , 2001, Journal of bioscience and bioengineering.

[120]  A. Bangham,et al.  Diffusion of univalent ions across the lamellae of swollen phospholipids. , 1965, Journal of molecular biology.

[121]  Kenichi Yoshikawa,et al.  Giant Liposome as a Biochemical Reactor: Transcription of DNA and Transportation by Laser Tweezers , 2001 .

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

[123]  F. Varela,et al.  Self-replicating micelles — A chemical version of a minimal autopoietic system , 1989, Origins of life and evolution of the biosphere.

[124]  Kenichi Yoshikawa,et al.  Gene Expression within Cell‐Sized Lipid Vesicles , 2003, Chembiochem : a European journal of chemical biology.

[125]  Kazufumi Hosoda,et al.  Cellular compartment model for exploring the effect of the lipidic membrane on the kinetics of encapsulated biochemical reactions. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[126]  Cristina Del Bianco,et al.  Intravesicle Isothermal DNA Replication , 2011, BMC Research Notes.

[127]  Ying Zhang,et al.  Artificial cells: building bioinspired systems using small-scale biology. , 2008, Trends in biotechnology.

[128]  D. Deamer,et al.  Non-enzymatic transfer of sequence information under plausible prebiotic conditions. , 2011, Biochimie.

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

[130]  S. Ichikawa,et al.  Enzymes inside lipid vesicles: preparation, reactivity and applications. , 2001, Biomolecular engineering.

[131]  P. Luisi,et al.  Toward the engineering of minimal living cells , 2002, The Anatomical record.

[132]  Sosaku Ichikawa,et al.  Novel method for obtaining homogeneous giant vesicles from a monodisperse water-in-oil emulsion prepared with a microfluidic device. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[133]  Guillaume Salbreux,et al.  Reconstitution of an actin cortex inside a liposome. , 2009, Biophysical journal.

[134]  Pier Luigi Luisi,et al.  Coexistence and Mutual Competition of Vesicles with Different Size Distributions , 2003 .

[135]  Pier Luigi Luisi,et al.  Liposome-Assisted Selective Polycondensation of α-Amino Acids and Peptides , 2000 .

[136]  P. Luisi,et al.  Protein expression in liposomes. , 1999, Biochemical and biophysical research communications.

[137]  D. Fletcher,et al.  Actin polymerization serves as a membrane domain switch in model lipid bilayers. , 2006, Biophysical journal.

[138]  H. Kikuchi,et al.  Gene delivery using liposome technology. , 1999, Journal of controlled release : official journal of the Controlled Release Society.

[139]  Ronald R. Breaker,et al.  Production of RNA by a polymerase protein encapsulated within phospholipid vesicles , 1994, Journal of Molecular Evolution.

[140]  Pasquale Stano,et al.  Question 7: New Aspects of Interactions Among Vesicles , 2007, Origins of Life and Evolution of Biospheres.

[141]  Tetsuya Yomo,et al.  Femtoliter compartment in liposomes for in vitro selection of proteins. , 2006, Analytical biochemistry.

[142]  Tetsuya Yomo,et al.  Expression of a cascading genetic network within liposomes , 2004, FEBS letters.

[143]  H. Bui,et al.  Charged liposome affects the translation and folding steps of in vitro expression of green fluorescent protein. , 2009, Journal of bioscience and bioengineering.

[144]  Dan S. Tawfik,et al.  Man-made cell-like compartments for molecular evolution , 1998, Nature Biotechnology.

[145]  P. Luisi,et al.  Polymerase chain reaction in liposomes. , 1995, Chemistry & biology.

[146]  Phillip L Geissler,et al.  Membrane-induced bundling of actin filaments. , 2008, Nature physics.