A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy

Research on giant vesicles is becoming increasingly popular. Giant vesicles provide model biomembrane systems for systematic measurements of mechanical and rheological properties of bilayers as a function of membrane composition and temperature, as well as hydrodynamic interactions. Membrane response to external factors (for example electric fields, ions and amphiphilic molecules) can be directly visualized under the microscope. In this paper we review our current understanding of lipid bilayers as obtained from studies on giant unilamellar vesicles. Because research on giant vesicles increasingly attracts the interest of scientists from various backgrounds, we also try to provide a concise introduction for newcomers in the field. Finally, we summarize some recent developments on curvature effects induced by polymers, domain formation in membranes and shape transitions induced by electric fields.

[1]  D. Zhelev,et al.  Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension. , 1993, Biochimica et biophysica acta.

[2]  G. Gompper,et al.  Giant hexagonal superstructures in diblock-copolymer membranes. , 2002, Physical Review Letters.

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

[4]  S. Svetina,et al.  The frequency dependence of phospholipid vesicle shapes in an external electric field , 2000, Pflügers Archiv.

[5]  J. Korlach,et al.  Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  R. Lipowsky,et al.  Elastic Properties of Polymer-Decorated Membranes , 1996 .

[8]  W. Helfrich,et al.  Deformation of giant lipid vesicles by electric fields. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[9]  J. Killian,et al.  Transbilayer movement of phospholipids in biogenic membranes. , 2004, Biochemistry.

[10]  Evans,et al.  Entropy-driven tension and bending elasticity in condensed-fluid membranes. , 1990, Physical review letters.

[11]  Gerhard Gompper,et al.  Advanced flicker spectroscopy of fluid membranes. , 2003, Physical review letters.

[12]  C. Keating,et al.  Dynamic microcompartmentation in synthetic cells , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Masahito Yamazaki,et al.  A new method for the preparation of giant liposomes in high salt concentrations and growth of protein microcrystals in them. , 2002, Biochimica et biophysica acta.

[14]  Olivier Sandre,et al.  Dynamics of transient pores in stretched vesicles. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E. Sackmann,et al.  Viscoelastic properties of erythrocyte membranes in high-frequency electric fields , 1984, Nature.

[16]  P. Saffman,et al.  Brownian motion in biological membranes. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Reinhard Lipowsky,et al.  Behavior of giant vesicles with anchored DNA molecules. , 2007, Biophysical journal.

[18]  H. Döbereiner,et al.  Properties of giant vesicles , 2000 .

[19]  M. R. Tarasevich,et al.  246 - Electric breakdown of bilayer lipid membranes I. The main experimental facts and their qualitative discussion , 1979 .

[20]  R. Lipowsky,et al.  Novel method for measuring the adhesion energy of vesicles. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[21]  Shape fluctuations and elastic properties of two-component bilayer membranes , 2004, cond-mat/0412407.

[22]  D. Boal,et al.  Mechanics of the cell , 2001 .

[23]  Rumiana Dimova,et al.  Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. , 2006, Biophysical journal.

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

[25]  Daniel J. Estes,et al.  Giant liposomes in physiological buffer using electroformation in a flow chamber. , 2005, Biochimica et biophysica acta.

[26]  M. Fukugita,et al.  Atomic effects on the estimation ofve mass from the β-spectrum in tritium decay , 1981 .

[27]  E Gratton,et al.  Lipid rafts reconstituted in model membranes. , 2001, Biophysical journal.

[28]  H. Itoh,et al.  Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. , 1996, Biophysical journal.

[29]  Winterhalter,et al.  Electric-field-dependent thermal fluctuations of giant vesicles. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[30]  K. Mecke,et al.  A fluid floating bilayer , 2001 .

[31]  Reinhard Lipowsky,et al.  Domains in membranes and vesicles , 2003 .

[32]  E. Evans,et al.  Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20 degrees C below to 10 degrees C above the liquid crystal-crystalline phase transition at 24 degrees C. , 1988, Biochemistry.

[33]  U. Seifert,et al.  Mapping vesicle shapes into the phase diagram: A comparison of experiment and theory , 1996, cond-mat/9612151.

[34]  Ivan B. Ivanov,et al.  Drag of a Solid Particle Trapped in a Thin Film or at an Interface: Influence of Surface Viscosity and Elasticity. , 2000, Journal of colloid and interface science.

[35]  C. Lee,et al.  All-optical measurements of the bending rigidity of lipid-vesicle membranes across structural phase transitions. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[36]  R. Lipowsky,et al.  The shape of polymer-decorated membranes , 2000 .

[37]  F. Bates,et al.  Electromechanical limits of polymersomes. , 2001, Physical review letters.

[38]  K. Kinosita,et al.  Steady-state deformation of a vesicle in alternating electric fields , 1993 .

[39]  R. Hochmuth Electro-mechanical permeabilization of lipid vesicles , 2005 .

[40]  Reinhard Lipowsky,et al.  Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution , 2006, Proceedings of the National Academy of Sciences.

[41]  C. Keating,et al.  Aqueous phase separation in giant vesicles. , 2002, Journal of the American Chemical Society.

[42]  Bensimon,et al.  Observation of toroidal vesicles. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[43]  S. Leibler,et al.  Unbinding transitions of interacting membranes. , 1986, Physical review letters.

[44]  Krassimir D. Danov,et al.  Falling ball viscosimetry of giant vesicle membranes: Finite-size effects , 1999 .

[45]  K. Mecke,et al.  Fluctuating Lipid Bilayer in an Arbitrary Potential: Theory and Experimental Determination of Bending Rigidity , 2003 .

[46]  Frédéric Pincet,et al.  Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy. , 2005, Colloids and surfaces. B, Biointerfaces.

[47]  K. Marsh,et al.  Viscosities of nonelectrolyte liquid mixtures. I. n-hexadecane + n-octane , 1987 .

[48]  The budding transition of phospholipid vesicles : a quantitative study via phase contrast microscopy , 1995 .

[49]  R. Dimova,et al.  Pretransitional effects in dimyristoylphosphatidylcholine vesicle membranes: optical dynamometry study. , 2000, Biophysical journal.

[50]  Reinhard Lipowsky,et al.  The conformation of membranes , 1991, Nature.

[51]  K. Moriyasu,et al.  A study of double-scattering effects in πd andpd interactions between 15 and 400 GeV , 1981 .

[52]  E. Neumann,et al.  Electroporation and Electrofusion in Cell Biology , 1989, Springer US.

[53]  F. J. Iglesias,et al.  Orientation of Schizosaccharomyces POMBE Nonliving Cells under Alternating Uniform and Nonuniform Electric Fields. , 1985, Biophysical journal.

[54]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[55]  M. Angelova,et al.  Preparation of giant vesicles by external AC electric fields. Kinetics and applications , 1992 .

[56]  K. Danov,et al.  Viscous drag of a solid sphere straddling a spherical or flat surface , 2000 .

[57]  W. Helfrich,et al.  Undulations, steric interaction and cohesion of fluid membranes , 1984 .

[58]  J. Henriksen,et al.  Thermal undulations of quasi-spherical vesicles stabilized by gravity , 2002, The European physical journal. E, Soft matter.

[59]  Sarah L Veatch,et al.  Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. , 2003, Biophysical journal.

[60]  D. Hammer,et al.  Polymersomes: tough vesicles made from diblock copolymers. , 1999, Science.

[61]  R. Kornberg,et al.  Inside-outside transitions of phospholipids in vesicle membranes. , 1971, Biochemistry.

[62]  P. Gennes,et al.  Transient pores in stretched vesicles: role of leak-out , 2000, Physica A: Statistical Mechanics and its Applications.

[63]  S. Schreiber,et al.  Transbilayer movement of phospholipids at the main phase transition of lipid membranes: implications for rapid flip-flop in biological membranes. , 2002, Biophysical Journal.

[64]  Gerhard Gompper,et al.  Mobility and elasticity of self-assembled membranes. , 1999 .

[65]  Watt W. Webb,et al.  Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension , 2003, Nature.

[66]  O. G. Mouritsen,et al.  Density fluctuations in saturated phospholipid bilayers increase as the acyl-chain length decreases. , 1990, Biophysical journal.

[67]  E. Evans,et al.  Elasticity of ``Fuzzy'' Biomembranes , 1997 .

[68]  K. Marsh,et al.  Viscosities of nonelectrolyte liquid mixtures. II. Binary and quaternary systems of some n-alkanes , 1988 .

[69]  Reinhard Lipowsky,et al.  Spontaneous curvature of fluid vesicles induced by trans-bilayer sugar asymmetry , 1999, European Biophysics Journal.

[70]  H. Döbereiner,et al.  Mesoscopic structure in the chain-melting regime of anionic phospholipid vesicles: DMPG. , 2004, Biophysical journal.

[71]  E. Evans,et al.  Effect of chain length and unsaturation on elasticity of lipid bilayers. , 2000, Biophysical journal.

[72]  K. Wakabayashi,et al.  Transient and Steady-State Deformations of a Vesicle with an Insulating Membrane in Response to Step-Function or Alternating Electric Fields , 1991 .

[73]  Kazuhiko Kinosita,et al.  Deformation of vesicles under the influence of strong electric fields II , 1991 .

[74]  D. Mitov,et al.  Bending elasticities of model membranes: influences of temperature and sterol content. , 1997, Biophysical journal.

[75]  Reinhard Lipowsky,et al.  Gravity-induced shape transformations of vesicles , 1995 .

[76]  E. Tekle,et al.  Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. , 2001, Biophysical journal.

[77]  I. Marrucho,et al.  Viscosity and Liquid Density of Asymmetric n-Alkane Mixtures: Measurement and Modeling , 2005 .

[78]  G. Niggemann,et al.  The Bending Rigidity of Phosphatidylcholine Bilayers: Dependences on Experimental Method, Sample Cell Sealing and Temperature , 1995 .

[79]  D. Marsh,et al.  Phospholipid Bilayers: Physical Principles and Models , 1987 .

[80]  P. Saffman Brownian motion in thin sheets of viscous fluid , 1976, Journal of Fluid Mechanics.

[81]  H. Itoh,et al.  Electroporation of cell membrane visualized under a pulsed-laser fluorescence microscope. , 1988, Biophysical journal.

[82]  T. Heimburg Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. , 1998, Biochimica et biophysica acta.

[83]  W. Helfrich,et al.  Alignment and Opening of Giant Lecithin Vesicles by Electric Fields , 1979 .

[84]  E. Evans,et al.  Molecular friction and epitactic coupling between monolayers in supported bilayers , 1989 .

[85]  U. Seifert,et al.  Hyperviscous diblock copolymer vesicles , 2002 .

[86]  R. Lipowsky Bending of Membranes by Anchored Polymers , 1995 .

[87]  U. Zimmermann,et al.  Electrical breakdown, electropermeabilization and electrofusion. , 1986, Reviews of physiology, biochemistry and pharmacology.

[88]  D Needham,et al.  Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. , 1989, Biophysical journal.

[89]  T. McIntosh,et al.  [38] Depth of water penetration into lipid bilayers , 1986 .

[90]  R. Dimova,et al.  Composition dependence of vesicle morphology and mixing properties in a bacterial model membrane system. , 2005, Biochimica et biophysica acta.

[91]  Evan Evans,et al.  Dynamic tension spectroscopy and strength of biomembranes. , 2003, Biophysical journal.

[92]  Seifert,et al.  Shape transformations of vesicles: Phase diagram for spontaneous- curvature and bilayer-coupling models. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[93]  Mathias Winterhalter,et al.  Giant liposome microreactors for controlled production of calcium phosphate crystals. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[94]  John M. Walker,et al.  Lipid Rafts , 2007, Methods in Molecular Biology.

[95]  Udo Seifert,et al.  Configurations of fluid membranes and vesicles , 1997 .

[96]  T. McIntosh,et al.  Depth of water penetration into lipid bilayers. , 1986, Methods in enzymology.

[97]  F. Pincet,et al.  Hemifusion and fusion of giant vesicles induced by reduction of inter-membrane distance , 2004, The European physical journal. E, Soft matter.

[98]  V. F. Pastushenko,et al.  Electric breakdown of bilayer lipid membranes , 1979 .

[99]  Rumiana Dimova,et al.  Electro-deformation and poration of giant vesicles viewed with high temporal resolution. , 2005, Biophysical journal.

[100]  M. Antonietti,et al.  Binding of calcium to phosphatidylcholine-phosphatidylserine membranes , 2006 .