Solid supported lipid bilayers: From biophysical studies to sensor design

Abstract The lipid bilayer is one of the most eloquent and important self-assembled structures in nature. It not only provides a protective container for cells and sub-cellular compartments, but also hosts much of the machinery for cellular communication and transport across the cell membrane. Solid supported lipid bilayers provide an excellent model system for studying the surface chemistry of the cell. Moreover, they are accessible to a wide variety of surface-specific analytical techniques. This makes it possible to investigate processes such as cell signaling, ligand–receptor interactions, enzymatic reactions occurring at the cell surface, as well as pathogen attack. In this review, the following membrane systems are discussed: black lipid membranes, solid supported lipid bilayers, hybrid lipid bilayers, and polymer cushioned lipid bilayers. Examples of how supported lipid membrane technology is interfaced with array based systems by photolithographic patterning, spatial addressing, microcontact printing, and microfluidic patterning are explored. Also, the use of supported lipid bilayers in microfluidic devices for the development of lab-on-a-chip based platforms is examined. Finally, the utility of lipid bilayers in nanotechnology and future directions in this area are discussed.

[1]  M. L. Wagner,et al.  Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers. , 2001, Biophysical journal.

[2]  R. D. Carlson,et al.  A simple method for the preparation of homogeneous phospholipid vesicles. , 1977, Biochemistry.

[3]  M. Stelzle,et al.  Two-dimensional microelectrophoresis in supported lipid bilayers. , 1992, Biophysical journal.

[4]  L. Tamm,et al.  Measuring lipid asymmetry in planar supported bilayers by fluorescence interference contrast microscopy. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[5]  E. Sackmann,et al.  Structure of an adsorbed dimyristoylphosphatidylcholine bilayer measured with specular reflection of neutrons. , 1991, Biophysical journal.

[6]  Jay T. Groves,et al.  Synaptic pattern formation during cellular recognition , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Zasadzinski,et al.  Formation of Tethered Supported Bilayers by Vesicle Fusion onto Lipopolymer Monolayers Promoted by Osmotic Stress. , 2000, Langmuir : the ACS journal of surfaces and colloids.

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

[9]  Kristin Sott,et al.  Controlled initiation of enzymatic reactions in micrometer-sized biomimetic compartments. , 2005, The journal of physical chemistry. B.

[10]  A. Offenhäusser,et al.  The peptide-tethered lipid membrane as a biomimetic system to incorporate cytochrome c oxidase in a functionally active form , 1999 .

[11]  George M. Whitesides,et al.  Patterning Self-Assembled Monolayers: Applications in Materials Science , 1994 .

[12]  Ralph G. Nuzzo,et al.  ADSORPTION OF BIFUNCTIONAL ORGANIC DISULFIDES ON GOLD SURFACES , 1983 .

[13]  Wolfgang Knoll,et al.  Thiopeptide-supported lipid layers on solid substrates , 1997 .

[14]  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.

[15]  Y. Lvov,et al.  Molecularly Flat Films of Linear Polyions and Proteins Obtained by the Alternate Adsorption Method , 1997 .

[16]  P. Stroeve,et al.  Supported lipid bilayers lifted from the substrate by layer-by-layer polyion cushions on self-assembled monolayers , 2003 .

[17]  N. Muller,et al.  CARBON-13 SPLITTINGS IN FLUORINE NUCLEAR MAGNETIC RESONANCE SPECTRA1 , 1963 .

[18]  Vincent J. Schaefer,et al.  Activities of Urease and Pepsin Monolayers , 1938 .

[19]  H Bayley,et al.  Self‐assembling biomolecular materials in mediaine , 1994 .

[20]  M. L. Wagner,et al.  Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker. , 2000, Biophysical journal.

[21]  S. Boxer,et al.  Patterning and Composition Arrays of Supported Lipid Bilayers by Microcontact Printing , 2001 .

[22]  A. Offenhäusser,et al.  Fusion of small unilamellar vesicles onto laterally mixed self-assembled monolayers of thiolipopeptides. , 2003, Journal of colloid and interface science.

[23]  M Montal,et al.  Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[24]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[25]  S. Boxer,et al.  Early steps of supported bilayer formation probed by single vesicle fluorescence assays. , 2002, Biophysical journal.

[26]  S. Boxer,et al.  Micropatterning Fluid Lipid Bilayers on Solid Supports , 1997, Science.

[27]  Barbara Baird,et al.  Visualization of plasma membrane compartmentalization with patterned lipid bilayers. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[28]  E. Sackmann,et al.  On the application of supported bilayers as receptive layers for biosensors with electrical detection , 1993 .

[29]  A. Peña,et al.  Incorporation of ionic channels from yeast plasma membranes into black lipid membranes. , 1989, Biophysical journal.

[30]  Carolyn R. Bertozzi,et al.  Control of cell adhesion and growth with micropatterned supported lipid membranes , 2001 .

[31]  I. Langmuir The mechanism of the surface phenomena of flotation , 1920 .

[32]  Y. Lvov,et al.  Nanoparticle/polyion assembly on microtemplates (lipid tubules and latex spheres) , 2002 .

[33]  R. Weis,et al.  Supported planar membranes in studies of cell-cell recognition in the immune system. , 1986, Biochimica et biophysica acta.

[34]  S. Boxer,et al.  Polymer-supported lipid bilayers on benzophenone-modified substrates. , 2001, Biomacromolecules.

[35]  P. Cremer,et al.  Effect of average phospholipid curvature on supported bilayer formation on glass by vesicle fusion. , 2006, Biophysical journal.

[36]  B. Frisken,et al.  Studies of Vesicle Extrusion , 2000 .

[37]  J. Groves,et al.  Electrostatically Targeted Intermembrane Lipid Exchange with Micropatterned Supported Membranes , 2003 .

[38]  J. Israelachvili,et al.  Polymer-cushioned bilayers. II. An investigation of interaction forces and fusion using the surface forces apparatus. , 1999, Biophysical journal.

[39]  George M. Whitesides,et al.  The interaction of proteins and cells with self-assembled monolayers of alkanethiolates on gold and silver , 1999 .

[40]  S. Boxer,et al.  Cell adhesion to protein-micropatterned-supported lipid bilayer membranes. , 2001, Journal of biomedical materials research.

[41]  L. Tamm,et al.  Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers. , 1992, Biochimica et biophysica acta.

[42]  Cremer,et al.  Creating addressable aqueous microcompartments above solid supported phospholipid bilayers using lithographically patterned poly(dimethylsiloxane) molds , 2000, Analytical chemistry.

[43]  N. Thompson,et al.  Formation and Characterization of Planar Phospholipid Bilayers Supported on TiO2 and SrTiO3 Single Crystals , 2000 .

[44]  Lance Kam and,et al.  Formation of Supported Lipid Bilayer Composition Arrays by Controlled Mixing and Surface Capture , 2000 .

[45]  A. Charrier,et al.  Main phase transitions in supported lipid single-bilayer. , 2005, Biophysical journal.

[46]  S. Bezrukov,et al.  Probing alamethicin channels with water-soluble polymers. Effect on conductance of channel states. , 1993, Biophysical journal.

[47]  J Y Wong,et al.  Structural studies of polymer-cushioned lipid bilayers. , 1998, Biophysical journal.

[48]  R. H. Firth,et al.  Colloids , 1914, Physics Subject Headings (PhySH).

[49]  Anne L Plant,et al.  Cell membrane hybrid bilayers containing the G-protein-coupled receptor CCR5. , 2002, Analytical biochemistry.

[50]  Dietmar Pum,et al.  Patterning of monolayers of crystalline S-layer proteins on a silicon surface by deep ultraviolet radiation , 1997 .

[51]  H. Bayley,et al.  Stochastic sensors inspired by biology , 2001, Nature.

[52]  H. Mao,et al.  Design and characterization of immobilized enzymes in microfluidic systems. , 2002, Analytical chemistry.

[53]  H. Bayley,et al.  Stochastic Sensing with Protein Pores , 2000 .

[54]  N. Thompson,et al.  Rebinding of IgE Fabs at haptenated planar membranes: measurement by total internal reflection with fluorescence photobleaching recovery. , 2000, Biochemistry.

[55]  J. Hubbard,et al.  Self assembly driven by hydrophobic interactions at alkanethiol monolayers: mechanisms of formation of hybrid bilayer membranes. , 1998, Biophysical chemistry.

[56]  J. Israelachvili,et al.  Polymer-cushioned bilayers. I. A structural study of various preparation methods using neutron reflectometry. , 1999, Biophysical journal.

[57]  H. Craighead,et al.  Mast Cell Activation on Patterned Lipid Bilayers of Subcellular Dimensions , 2003 .

[58]  A. Plant,et al.  Hybrid bilayer membranes in air and water: infrared spectroscopy and neutron reflectivity studies. , 1998, Biophysical journal.

[59]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[60]  H. Bayley,et al.  Stochastic sensing of nanomolar inositol 1,4,5-trisphosphate with an engineered pore. , 2002, Chemistry & biology.

[61]  D. O. Rudin,et al.  Reconstitution of Cell Membrane Structure in vitro and its Transformation into an Excitable System , 1962, Nature.

[62]  A. Singh,et al.  Micrometer-sized supported lipid bilayer arrays for bacterial toxin binding studies through total internal reflection fluorescence microscopy. , 2005, Biophysical journal.

[63]  L. Mayer,et al.  Vesicles of variable sizes produced by a rapid extrusion procedure. , 1986, Biochimica et biophysica acta.

[64]  M. Mayer,et al.  Hydrogel stamping of arrays of supported lipid bilayers with various lipid compositions for the screening of drug-membrane and protein-membrane interactions. , 2005, Angewandte Chemie.

[65]  Dietmar Pum,et al.  S-layer Ultrafiltration Membranes: A New Support for Stabilizing Functionalized Lipid Membranes , 2001 .

[66]  E. Sackmann,et al.  Supported Membranes: Scientific and Practical Applications , 1996, Science.

[67]  E. Gouaux α-Hemolysin fromStaphylococcus aureus:An Archetype of β-Barrel, Channel-Forming Toxins , 1998 .

[68]  E. Chang,et al.  Self-assembly of a virus-mimicking nanostructure system for efficient tumor-targeted gene delivery. , 2002, Human gene therapy.

[69]  H. Mcconnell,et al.  Allogeneic stimulation of cytotoxic T cells by supported planar membranes. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[70]  A. Plant,et al.  Investigation of Hybrid Bilayer Membranes with Neutron Reflectometry: Probing the Interactions of Melittin , 2001 .

[71]  Fernando Albertorio,et al.  Fluid and air-stable lipopolymer membranes for biosensor applications. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[72]  W. Dressick,et al.  Fabrication of nanoscale metallic spirals using phospholipid microtubule organizational templates. , 2003, Journal of the American Chemical Society.

[73]  A. Plant Supported Hybrid Bilayer Membranes as Rugged Cell Membrane Mimics , 1999 .

[74]  S. Boxer,et al.  Substrate−Membrane Interactions: Mechanisms for Imposing Patterns on a Fluid Bilayer Membrane , 1998 .

[75]  G. Whitesides,et al.  Rapid Prototyping of Microfluidic Systems in Poly(dimethylsiloxane). , 1998, Analytical chemistry.

[76]  E. Sackmann,et al.  Functionalisation of Si/SiO2 and glass surfaces with ultrathin dextran films and deposition of lipid bilayers. , 1996, Biosensors & bioelectronics.

[77]  A. Plant,et al.  Assessing the Molecular Structure of Alkanethiol Monolayers in Hybrid Bilayer Membranes with Vibrational Spectroscopies , 1998 .

[78]  Fredrik Höök,et al.  Intact Vesicle Adsorption and Supported Biomembrane Formation from Vesicles in Solution: Influence of Surface Chemistry, Vesicle Size, Temperature, and Osmotic Pressure† , 2003 .

[79]  P. Mazeran,et al.  Two-Step Formation of Streptavidin-Supported Lipid Bilayers by PEG-Triggered Vesicle Fusion. Fluorescence and Atomic Force Microscopy Characterization† , 2003 .

[80]  A. Guo,et al.  Formation of supported phospholipid bilayers on molecular surfaces: role of surface charge density and electrostatic interaction. , 2006, Biophysical journal.

[81]  K. Furusawa,et al.  Liposome Adhesion on Mica Surface Studied by Atomic Force Microscopy , 1999 .

[82]  W. Knoll,et al.  The polymer-supported phospholipid bilayer: tethering as a new approach to substrate-membrane stabilization. , 2002, Biomacromolecules.

[83]  H. Ringsdorf,et al.  Influence of Anchor Lipids on the Homogeneity and Mobility of Lipid Bilayers on Thin Polymer Films , 1996 .

[84]  V. Gerke,et al.  Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study. , 2002, Biochemistry.

[85]  W. Knoll,et al.  Synthesis and Characterization of Hydrophilic Lipopolymers for the Support of Lipid Bilayers , 1999 .

[86]  Owe Orwar,et al.  Molecular engineering: Networks of nanotubes and containers , 2001, Nature.

[87]  I. Gustafson,et al.  Planar lipid bilayers on solid supports from liposomes--factors of importance for kinetics and stability. , 1997, Biochimica et biophysica acta.

[88]  R N Zare,et al.  Chemical transformations in individual ultrasmall biomimetic containers. , 1999, Science.

[89]  J. Kleijn,et al.  Order in phospholipid Langmuir-Blodgett layers and the effect of the electrical potential of the substrate. , 1999, Biophysical journal.

[90]  H. Ti Tien,et al.  METHODS FOR THE FORMATION OF SINGLE BIMOLECULAR LIPID MEMBRANES IN AQUEOUS SOLUTION , 1963 .

[91]  A. Plant,et al.  Reconstitution of the Pore-Forming Toxin α-Hemolysin in Phospholipid/18-Octadecyl-1-thiahexa(ethylene oxide) and Phospholipid/n-Octadecanethiol Supported Bilayer Membranes , 2000 .

[92]  Miss A.O. Penney (b) , 1974, The New Yale Book of Quotations.

[93]  Kristin Sott,et al.  Micropipet Writing Technique for Production of Two-Dimensional Lipid Bilayer Nanotube−Vesicle Networks on Functionalized and Patterned Surfaces , 2003 .

[94]  S. Boxer,et al.  Printing via Photolithography on Micropartitioned Fluid Lipid Membranes , 2000 .

[95]  C. Bourdillon,et al.  Formation of streptavidin-supported lipid bilayers on porous anodic alumina: electrochemical monitoring of triggered vesicle fusion. , 2001, Journal of the American Chemical Society.

[96]  E. Freed,et al.  Plasma membrane rafts play a critical role in HIV-1 assembly and release , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[97]  Fernanda F. Rossetti,et al.  Interactions between titanium dioxide and phosphatidyl serine-containing liposomes: formation and patterning of supported phospholipid bilayers on the surface of a medically relevant material. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[98]  H. Mcconnell,et al.  Supported phospholipid bilayers. , 1985, Biophysical journal.

[99]  Lance C. Kam,et al.  Patterning Hybrid Surfaces of Proteins and Supported Lipid Bilayers , 2000 .

[100]  J. Israelachvili,et al.  Formation of tethered supported bilayers via membrane-inserting reactive lipids , 1998 .

[101]  E. Wang,et al.  Formation of a supported hybrid bilayer membrane on gold: A sterically enhanced hydrophobic effect , 2002 .

[102]  H. Macleod,et al.  Assembly and molecular organization of self-assembled lipid bilayers on solid substrates monitored by surface plasmon resonance spectroscopy. , 1994, Biochimica et biophysica acta.

[103]  Kristin Sott,et al.  Micropipet-Assisted Formation of Microscopic Networks of Unilamellar Lipid Bilayer Nanotubes and Containers , 2001 .

[104]  Mathias Winterhalter,et al.  Nanoreactors based on (polymerized) ABA-triblock copolymer vesicles , 2000 .

[105]  C. Yee,et al.  Membrane Photolithography: Direct Micropatterning and Manipulation of Fluid Phospholipid Membranes in the Aqueous Phase Using Deep‐UV Light , 2004 .

[106]  Formation of Self-Assembled, Air-Stable Lipid Bilayer Membranes on Solid Supports , 2001 .

[107]  S. Boxer,et al.  Micropattern formation in supported lipid membranes. , 2002, Accounts of chemical research.

[108]  G. Zampighi,et al.  Phospholipid vesicle formation and transmembrane protein incorporation using octyl glucoside. , 1981, Biochemistry.

[109]  Owe Orwar,et al.  Artificial cells: Unique insights into exocytosis using liposomes and lipid nanotubes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[110]  A. Plant,et al.  Supported phospholipid/alkanethiol biomimetic membranes: insulating properties. , 1994, Biophysical journal.

[111]  A. Plant,et al.  Characterization of biomimetic surfaces formed from cell membranes. , 1997, Biophysical journal.

[112]  Michael C. Petty,et al.  Langmuir-Blodgett films: Interaction of electromagnetic radiation with organic thin films , 1996 .

[113]  G. Csucs,et al.  Interaction of phospholipid vesicles with smooth metal-oxide surfaces. , 1998, Biochimica et biophysica acta.

[114]  F. Brodsky,et al.  Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. , 2002, Immunity.

[115]  George M. Whitesides,et al.  Electron Transport through Thin Organic Films in Metal−Insulator−Metal Junctions Based on Self-Assembled Monolayers , 2001 .

[116]  D. Struck,et al.  Injection of DNA into liposomes by bacteriophage lambda. , 1983, The Journal of biological chemistry.

[117]  A. Plant Self-assembled phospholipid/alkanethiol biomimetic bilayers on gold , 1993 .

[118]  T G Clark,et al.  Creating biological membranes on the micron scale: forming patterned lipid bilayers using a polymer lift-off technique. , 2003, Biophysical journal.

[119]  P K Hansma,et al.  Atomic force microscopy of hydrated phosphatidylethanolamine bilayers. , 1991, Biophysical journal.

[120]  A. Offenhäusser,et al.  Polysaccharide-Supported Planar Bilayer Lipid Model Membranes† , 2003 .

[121]  Oksana Sirenko,et al.  Cell membrane array fabrication and assay technology , 2005, BMC biotechnology.

[122]  High refractive index substrates for fluorescence microscopy of biological interfaces with high z contrast , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[123]  Lance C. Kam,et al.  Spatially Selective Manipulation of Supported Lipid Bilayers by Laminar Flow: Steps Toward Biomembrane Microfluidics† , 2003 .

[124]  P. Couturier Japan , 1988, The Lancet.

[125]  Xiaofeng Lu,et al.  Simultaneous stochastic sensing of divalent metal ions , 2000, Nature Biotechnology.

[126]  E. Bamberg,et al.  Formation of ionic channels in black lipid membranes by succinic derivatives of Gramicidin A , 1979, The Journal of Membrane Biology.

[127]  W. Knoll,et al.  Oriented attachment and membrane reconstitution of His-tagged cytochrome c oxidase to a gold electrode: in situ monitoring by surface-enhanced infrared absorption spectroscopy. , 2004, Journal of the American Chemical Society.

[128]  Jay T. Groves,et al.  Direct Patterning of Membrane‐Derivatized Colloids Using In‐Situ UV‐Ozone Photolithography , 2005 .

[129]  O. Orwar,et al.  Nanofluidic networks based on surfactant membrane technology. , 2003, Analytical chemistry.

[130]  Anthony G. Frutos,et al.  Method for Fabricating Supported Bilayer Lipid Membranes on Gold , 2000 .

[131]  J. Moiroux,et al.  Formation of Tethered and Streptavidin-Supported Lipid Bilayers on a Microporous Electrode for the Reconstitution of Membranes of Large Surface Area , 2002 .

[132]  D. Pum,et al.  S-layer stabilized solid support lipid bilayers. , 1997, Journal of structural biology.

[133]  P. Cullis,et al.  Generation of large unilamellar vesicles from long-chain saturated phosphatidylcholines by extrusion technique , 1989 .

[134]  P. Stroeve,et al.  Mobile Phospholipid Bilayers Supported on a Polyion/Alkylthiol Layer Pair , 2000 .

[135]  Steve Granick,et al.  Electrostatic stitching in gel-phase supported phospholipid bilayers. , 2006, The journal of physical chemistry. B.

[136]  Sean Conlan,et al.  Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter , 1999, Nature.

[137]  Harold G. Craighead,et al.  Nanofabrication and Biosystems: Integrating Materials Science, Engineering and Biology , 1997 .

[138]  J. Drews Drug discovery: a historical perspective. , 2000, Science.

[139]  P. Nollert,et al.  Impedance spectroscopy of porin and gramicidin pores reconstituted into supported lipid bilayers on indium-tin-oxide electrodes , 1998 .

[140]  H. Mao,et al.  Fabrication of phospholipid bilayer-coated microchannels for on-chip immunoassays. , 2001, Analytical chemistry.

[141]  H. Mao,et al.  Investigations of bivalent antibody binding on fluid-supported phospholipid membranes: the effect of hapten density. , 2003, Journal of the American Chemical Society.

[142]  Seung-Yong Jung,et al.  Creating fluid and air-stable solid supported lipid bilayers. , 2004, Journal of the American Chemical Society.

[143]  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 .

[144]  Dumas,et al.  Understanding the function of bacterial outer membrane channels by reconstitution into black lipid membranes , 2000, Biophysical chemistry.

[145]  Paul S. Cremer,et al.  Formation and Spreading of Lipid Bilayers on Planar Glass Supports , 1999 .

[146]  A. Plant,et al.  Phospholipid/alkanethiol bilayers for cell-surface receptor studies by surface plasmon resonance. , 1995, Analytical biochemistry.

[147]  Erich Sackmann,et al.  High Electric Resistance Polymer/Lipid Composite Films on Indium−Tin−Oxide Electrodes , 1999 .

[148]  Erich Sackmann,et al.  Polymer-supported membranes as models of the cell surface , 2005, Nature.

[149]  Janos H. Fendler,et al.  Chemical Self-assembly for Electronic Applications , 2001 .

[150]  H. Mao,et al.  A microfluidic device with a linear temperature gradient for parallel and combinatorial measurements. , 2002, Journal of the American Chemical Society.

[151]  D. Chiu,et al.  Formation of geometrically complex lipid nanotube-vesicle networks of higher-order topologies , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[152]  H. Ringsdorf,et al.  Polymer-supported bilayer on a solid substrate. , 1992, Biophysical journal.

[153]  S. Boxer,et al.  Arrays of mobile tethered vesicles on supported lipid bilayers. , 2003, Journal of the American Chemical Society.

[154]  Y. Sanai,et al.  Involvement of Lipid Raft Signaling in Ganglioside-Mediated Neural Function , 2001 .

[155]  W. Knoll,et al.  Polyelectrolyte-supported lipid membranes. , 2002, Bioelectrochemistry.