Lipid vesicles in capillary electrophoretic techniques: Characterization of structural properties and associated membrane‐molecule interactions

This paper reviews the use of lipid vesicles as model membranes in capillary electrophoresis (CE). The history and utility of CE in the characterization of microparticles is summarized, focusing on the application of colloidal electromigration theories to lipid vesicles. For instance, CE experiments have been used to characterize the size, surface properties, enclosed volumes, and electrophoretic mobilities of lipid vesicles and of lipoprotein particles. Several techniques involving small molecules or macromolecules separated in the presence of lipid vesicles are discussed. Interactions between the analytes and the lipid vesicles – acting as a pseudostationary phase or coated stationary phase in electrokinetic chromatography (EKC) – can be used to obtain additional information on the characteristics of the vesicles and analytes, and to study the biophysical properties of membrane‐molecule interactions in lipid vesicles and lipoproteins. Different methods of determining binding constants by EKC are reviewed, along with the relevant binding constant calculations and a discussion of the application and limitations of these techniques as they apply to lipid vesicle systems.

[1]  A. Chrambach,et al.  Separation and characterization of sub‐μm‐ and μm‐sized particles by capillary zone electrophoresis , 2002 .

[2]  G. Siest,et al.  Characterization and quantification of serum lipoprotein subfractions by capillary isotachophoresis: relationships with lipid, apolipoprotein, and lipoprotein levels. , 1999, Journal of lipid research.

[3]  E. Villegas,et al.  Pore formation of phospholipid membranes by the action of two hemolytic arachnid peptides of different size. , 2004, Biochimica et biophysica acta.

[4]  Marja-Liisa Riekkola,et al.  Phospholipids and liposomes in liquid chromatographic and capillary electromigration techniques , 2004 .

[5]  J. Akbuǧa,et al.  Encapsulation of Enrofloxacin in Liposomes I: Preparation and In Vitro Characterization of LUV , 2004, Journal of liposome research.

[6]  Michael A. Rodriguez,et al.  Evaluation of molecule‐microbe interactions with capillary electrophoresis: Procedures, utility and restrictions , 2002, Electrophoresis.

[7]  D. Armstrong,et al.  Examination of the origin, variation, and proper use of expressions for the estimation of association constants by capillary electrophoresis , 1996 .

[8]  R. Ho,et al.  Trends and developments in liposome drug delivery systems. , 2001, Journal of pharmaceutical sciences.

[9]  Ambikanandan Misra,et al.  Topical Liposomal Gel of Idoxuridine for the Treatment of Herpes Simplex: Pharmaceutical and Clinical Implications , 2005, Pharmaceutical development and technology.

[10]  S. Boxer,et al.  Electric Field Effects in Multicomponent Fluid Lipid Membranes , 2000 .

[11]  Yukihiro Kuroda,et al.  Effect of oxidation of low‐density lipoprotein on drug binding affinity studied by high performance frontal analysis‐capillary electrophoresis , 2001, Electrophoresis.

[12]  P. Nandi,et al.  Interaction of negatively charged liposomes with nuclear membranes: adsorption, lipid mixing and lysis of the vesicles. , 1987, Biochimica et biophysica acta.

[13]  K. Awai,et al.  In vitro andin vivo stability of polymerized mixed liposomes composed of 2,4-octadecadienoyl groups of phospholipids , 2000 .

[14]  S. Boxer,et al.  Electric field-induced reorganization of two-component supported bilayer membranes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  G. Whitesides,et al.  Determination of binding constants of ligands to proteins by affinity capillary electrophoresis: compensation for electroosmotic flow. , 1994, Analytical chemistry.

[16]  J Frank,et al.  Recent advances in affinity capillary electrophoresis , 2000, Electrophoresis.

[17]  N. Heegaard,et al.  Capillary electrophoresis frontal analysis: Principles and applications for the study of drug‐plasma protein binding , 2003, Electrophoresis.

[18]  M. Riekkola,et al.  Liposomes as carriers in electrokinetic capillary chromatography , 2000, Electrophoresis.

[19]  S. Hjertén,et al.  Liposome capillary electrophoresis for analysis of interactions between lipid bilayers and solutes , 1995, Electrophoresis.

[20]  Michael A. Rodriguez,et al.  Separation and analysis of colloidal/nano-particles including microorganisms by capillary electrophoresis: a fundamental review. , 2004, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[21]  K. Tsukagoshi,et al.  Characterization of Dyestuff-containing Liposome by Capillary Zone Electrophoresis Using On-Line Chemiluminescence Detection , 1996 .

[22]  R. Nossal,et al.  Light scattering characterization of extruded lipid vesicles , 1999, European Biophysics Journal.

[23]  L. Zhang,et al.  Study on the multiple sites binding of human serum albumin and porphyrin by affinity capillary electrophoresis. , 2002, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[24]  M. Stastna,et al.  Capillary zone electrophoresis of sub‐μm‐sized particles in electrolyte solutions of various ionic strengths: Size‐dependent electrophoretic migration and separation efficiency , 2000, Electrophoresis.

[25]  N. Heegaard,et al.  Recent applications of affinity interactions in capillary electrophoresis , 2003, Electrophoresis.

[26]  D. Armstrong,et al.  Methods for the determination of binding constants by capillary electrophoresis , 2001, Electrophoresis.

[27]  Amarnath Sharma,et al.  Liposomes in drug delivery: Progress and limitations , 1997 .

[28]  J J Bao,et al.  Capillary electrophoretic immunoassays. , 1997, Journal of chromatography. B, Biomedical sciences and applications.

[29]  A. Estepa,et al.  Membrane-related effects underlying the biological activity of the anthraquinones emodin and barbaloin. , 2004, Biochemical pharmacology.

[30]  Tomoko Kimura,et al.  Plasma protein binding study of oxybutynin by high-performance frontal analysis. , 2002, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[31]  P. Kinnunen,et al.  Binding of daidzein to liposomes. , 1996, Biochimica et biophysica acta.

[32]  C. Prestidge,et al.  Attenuated total reflectance infrared studies of liposome adsorption at the solid-liquid interface. , 2004, Colloids and surfaces. B, Biointerfaces.

[33]  R. W. O'Brien,et al.  The electrophoresis of a spheroid with a thin double layer , 1988 .

[34]  M. Khaledi,et al.  Rapid determination of liposome-water partition coefficients (Klw) using liposome electrokinetic chromatography (LEKC). , 2002, Journal of pharmaceutical sciences.

[35]  S. De Carlo,et al.  Electron Cryo‐Microscopy Reveals Mechanism of Action of Propranolol on Artificial Membranes , 2004, Journal of liposome research.

[36]  Shuliang Li,et al.  Structure of small actin-containing liposomes probed by atomic force microscopy: effect of actin concentration & liposome size. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[37]  Z. Deyl,et al.  Affinity electrochromatography of acidic drugs using a liposome-modified capillary. , 2003, Journal of chromatography. A.

[38]  M. Riekkola,et al.  Study on liposomes by capillary electrophoresis , 2001, Electrophoresis.

[39]  R. New,et al.  Liposomes : a practical approach , 1990 .

[40]  J. Foley,et al.  Electrokinetic chromatography using thermodynamically stable vesicles and mixed micelles formed from oppositely charged surfactants. , 1998, Analytical chemistry.

[41]  L. Holland,et al.  Bilayered phospholipid micelles and capillary electrophoresis: A new additive for electrokinetic chromatography , 2003, Electrophoresis.

[42]  A. L. Loeb,et al.  Calculation of the electrophoretic mobility of a spherical colloid particle , 1966 .

[43]  Q. Yang,et al.  Liposome chromatography: liposomes immobilized in gel beads as a stationary phase for aqueous column chromatography. , 1991, Journal of chromatography.

[44]  M. Orchard,et al.  The use of capillary electrophoresis with entangled polymer matrix to analyse plasmid DNA and a cationic lipid/cholesterol liposome: DNA complex , 1999 .

[45]  Beate I. Escher,et al.  Evaluation of Liposome−Water Partitioning of Organic Acids and Bases. 2. Comparison of Experimental Determination Methods , 2000 .

[46]  B. Ruozi,et al.  Cationic Liposomes for Gene Transfection , 2003, Journal of drug targeting.

[47]  Shen Hu,et al.  Characterization of the interaction between phospholipid and protein by capillary electrophoresis with laser-induced fluorescence detection. , 2001, Journal of chromatography. A.

[48]  W. C. Purdy,et al.  Chromatographic techniques for the isolation and purification of lipoproteins. , 1995, Journal of chromatography. B, Biomedical applications.

[49]  V. Richter,et al.  Analytical capillary isotachophoresis of human serum lipoproteins , 1997, Electrophoresis.

[50]  K. Kairemo,et al.  Targeted liposomal drug delivery in cancer. , 2004, Current pharmaceutical design.

[51]  I. Khozin-Goldberg,et al.  Differences in Membrane Fluidity and Fatty Acid Composition between Phenotypic Variants of Streptococcus pneumoniae , 2004, Journal of bacteriology.

[52]  Lee R. White,et al.  Electrophoretic mobility of a spherical colloidal particle , 1978 .

[53]  M. Riekkola,et al.  Simple coating of capillaries with anionic liposomes in capillary electrophoresis. , 2003, Journal of chromatography. A.

[54]  A. Kusumi,et al.  Cholesterol effects on the phosphatidylcholine bilayer polar region: a molecular simulation study. , 2000, Biophysical journal.

[55]  Dieter Blaas,et al.  Capillary electrophoresis of biological particles: Viruses, bacteria, and eukaryotic cells , 2004, Electrophoresis.

[56]  T. E. Thompson,et al.  Cholesterol-induced fluid-phase immiscibility in membranes. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Q. Dai,et al.  Capillary electrophoresis of cardiolipin with on‐line dye interaction and spectrophotometric detection , 2003, Electrophoresis.

[58]  David D Y Chen,et al.  Applications of on‐line weak affinity interactions in free solution capillary electrophoresis , 2002, Electrophoresis.

[59]  E. Levy,et al.  New lipids in enteral feeding , 2004, Current opinion in clinical nutrition and metabolic care.

[60]  G. Schmitz,et al.  Analysis of lipoproteins with analytical capillary isotachophoresis , 1994, Electrophoresis.

[61]  M. Stastna,et al.  Polydispersity of liposome preparations as a likely source of peak width in capillary zone electrophoresis. , 2001, Journal of chromatography. B, Biomedical sciences and applications.

[62]  A. Banerjee,et al.  Investigations on the binding and antioxidant properties of the plant flavonoid fisetin in model biomembranes , 2004, FEBS letters.

[63]  Qing Yang,et al.  Self-assembly and immobilization of liposomes in fused-silica capillary by avidin–biotin binding , 1998 .

[64]  Z. Deyl,et al.  Application of capillaries with minimized electroosmotic flow to the electrokinetic study of acidic drug–β-oleoyl-γ-palmitoyl-l-α-phosphatidyl choline liposome interactions , 2003 .

[65]  D. S. Hage,et al.  Guidelines in selecting ligand concentrations for the determination of binding constants by affinity capillary electrophoresis. , 1997, Journal of chromatography. B, Biomedical sciences and applications.

[66]  Yukihiro Kuroda,et al.  Binding analysis of nilvadipine to plasma lipoproteins by capillary electrophoresis-frontal analysis. , 1999, Journal of pharmaceutical and biomedical analysis.

[67]  Yukihiro Kuroda,et al.  Enantioselective binding analysis of verapamil to plasma lipoproteins by capillary electrophoresis-frontal analysis. , 2000, Journal of chromatography. A.

[68]  J. Hernández-Méndez,et al.  Micellar electrokinetic chromatography with bis(2-ethylhexyl)sodium sulfosuccinate vesicles determination of synthetic food antioxidants. , 2000, Journal of chromatography. A.

[69]  B. Nordén,et al.  Vesicle membrane interactions of penetratin analogues. , 2004, Biochemistry.

[70]  S. Boxer,et al.  Electric field-induced critical demixing in lipid bilayer membranes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[71]  P. Pennefather,et al.  Properties of a self-assembled phospholipid membrane supported on lipobeads. , 2004, Biophysical journal.

[72]  Yukihiro Kuroda,et al.  Role of phospholipids in drug-LDL bindings as studied by high-performance frontal analysis/capillary electrophoresis. , 2003, Journal of pharmaceutical and biomedical analysis.

[73]  H. Boelens,et al.  Comparison of five methods for the study of drug-protein binding in affinity capillary electrophoresis. , 1997, Journal of chromatography. A.

[74]  E. Arriaga,et al.  Determination of electrophoretic mobility distributions through the analysis of individual mitochondrial events by capillary electrophoresis with laser-induced fluorescence detection. , 2002, Analytical chemistry.

[75]  H. Poppe,et al.  Principles and limitations of methods available for the determination of binding constants with affinity capillary electrophoresis , 1997 .

[76]  K. Tsukagoshi,et al.  Migration behavior of dyestuff-containing liposomes in capillary electrophoresis with chemiluminescence detection , 1998 .

[77]  Lateral Reorganization of Fluid Lipid Membranes in Response to the Electric Field Produced by a Buried Charge , 2000 .

[78]  R. W. O'Brien The solution of the electrokinetic equations for colloidal particles with thin double layers , 1983 .

[79]  A. Manosroi,et al.  Characterization of Amphotericin B Liposome Formulations , 2004, Drug development and industrial pharmacy.

[80]  A. Mohammed,et al.  Liposome formulation of poorly water soluble drugs: optimisation of drug loading and ESEM analysis of stability. , 2004, International journal of pharmaceutics.

[81]  R. Rubin,et al.  Steroid hormones partition to distinct sites in a model membrane bilayer: direct demonstration by small-angle X-ray diffraction. , 1998, Biochimica et biophysica acta.

[82]  Vincent Chan,et al.  Shape recovery of an optically trapped vesicle: effect of flow velocity and temperature , 2004, IEEE Transactions on NanoBioscience.

[83]  O Orwar,et al.  Electroinjection of colloid particles and biopolymers into single unilamellar liposomes and cells for bioanalytical applications. , 2000, Analytical chemistry.

[84]  S. Panyim,et al.  Structural design and characterization of a channel-forming peptide. , 2004, Journal of biochemistry and molecular biology.

[85]  N. Chiaramoni,et al.  Stability of Liposomal Formulations in Physiological Conditions for Oral Drug Delivery , 2004, Drug delivery.

[86]  J. Petersen,et al.  Capillary electrophoresis and its application in the clinical laboratory. , 2003, Clinica chimica acta; international journal of clinical chemistry.

[87]  M. Hayes,et al.  Examination of the electrophoretic behavior of liposomes. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[88]  C. Lunte,et al.  Correlation of the Capacity Factor in Vesicular Electrokinetic Chromatography with the Octanol: Water Partition Coefficient for Charged and Neutral Analytes , 2004, Pharmaceutical Research.

[89]  B. Lin,et al.  Recent advances in the study of biomolecular interactions by capillary electrophoresis , 2004, Electrophoresis.

[90]  G. McIntire,et al.  Determination of the electrophoretic mobility of polystyrene particles by capillary electrophoresis , 1994 .

[91]  C. Lucy,et al.  Phospholipid bilayer coatings for the separation of proteins in capillary electrophoresis. , 2002, Analytical chemistry.

[92]  E. Arriaga,et al.  Determination of the cardiolipin content of individual mitochondria by capillary electrophoresis with laser‐induced fluorescence detection , 2002, Electrophoresis.

[93]  R. Apkarian,et al.  Study of lipid and apolipoprotein binding interactions using vesicle affinity capillary electrophoresis. , 2003, Analytical Chemistry.

[94]  Mahendra Kumar Jain Introduction to biological membranes , 1980 .

[95]  N. Heegaard,et al.  Identification, quantitation, and characterization of biomolecules by capillary electrophoretic analysis of binding interactions , 1999, Electrophoresis.

[96]  Z. Değim,et al.  The effect of various liposome formulations on insulin penetration across Caco-2 cell monolayer. , 2004, Life sciences.

[97]  R A Durst,et al.  Liposome behavior in capillary electrophoresis. , 1996, Analytical chemistry.

[98]  D. Richards,et al.  Determination of properties of individual liposomes by capillary electrophoresis with postocolumn laser-induced fluorescence detection. , 2001, Analytical chemistry.

[99]  G. McIntire,et al.  Analytical separation of polystyrene nanospheres by capillary electrophoresis , 1989 .

[100]  R. Schwarzenbach,et al.  Evaluation of Liposome−Water Partitioning of Organic Acids and Bases. 1. Development of a Sorption Model , 2000 .

[101]  T. Miida,et al.  Capillary isotachophoretic analysis of serum lipoproteins using a carrier ampholyte as spacer ion , 2000, Annals of clinical biochemistry.

[102]  M. Hayes,et al.  Effects of pH gradients on liposomal charge states examined by capillary electrophoresis , 2002 .

[103]  Pradeep Tyagi,et al.  Anisamide‐targeted stealth liposomes: A potent carrier for targeting doxorubicin to human prostate cancer cells , 2004, International journal of cancer.

[104]  K. Markides,et al.  Method for immobilization of liposomes in capillary electrophoresis by electrostatic interaction with derivatized agarose , 2002, Electrophoresis.

[105]  R. W. O'Brien The electrical conductivity of a dilute suspension of charged particles , 1981 .

[106]  F. Gomez,et al.  Use of mobility ratios to estimate binding constants of ligands to proteins in affinity capillary electrophoresis. , 1998, Journal of chromatography. B, Biomedical sciences and applications.

[107]  M. Riekkola,et al.  Influence of cetyltrimethylammonium bromide on phosphatidylcholine-coated capillaries , 2004, Analytical and bioanalytical chemistry.

[108]  S. Terabe,et al.  Estimation of binding constants by capillary electrophoresis. , 2002, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[109]  D. L. Cole,et al.  Determination of free and encapsulated oligonucleotides in liposome formulated drug product. , 2000, Journal of pharmaceutical and biomedical analysis.

[110]  S. Petersen,et al.  Effects of capillary temperature control and electrophoretic heterogeneity on parameters characterizing separations of particles by capillary zone electrophoresis , 1992 .

[111]  Harlan K. Jones,et al.  Separations of chemically different particles by capillary electrophoresis , 1990 .

[112]  Jan Lichtenberg,et al.  Analysis of lipoproteins by capillary zone electrophoresis in microfluidic devices: assay development and surface roughness measurements. , 2002, Analytical chemistry.

[113]  J. Stocks,et al.  Analysis of apolipoproteins and lipoproteins by capillary electrophoresis , 1999, Electrophoresis.

[114]  N. Melik-Nubarov,et al.  Doxorubicin-poly(acrylic acid) complexes: interaction with liposomes. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[115]  T. E. Thompson,et al.  Modulation of phospholipid acyl chain order by cholesterol. A solid-state 2H nuclear magnetic resonance study. , 1990, Biochemistry.

[116]  A. Ballangrud,et al.  Binding and interstitial penetration of liposomes within avascular tumor spheroids , 2004, International journal of cancer.

[117]  M. Riekkola,et al.  Phospholipid‐lysozyme coating for chiral separation in capillary electrophoresis , 2004, Electrophoresis.

[118]  M. Riekkola,et al.  Cholesterol‐containing phosphatidylcholine liposomes: Characterization and use as dispersed phase in electrokinetic capillary chromatography , 2002 .

[119]  M. Khaledi,et al.  Characterization of solvation properties of lipid bilayer membranes in liposome electrokinetic chromatography. , 2002, Journal of chromatography. A.

[120]  W. Meier,et al.  Liposome-based nanocapsules , 2004, IEEE Transactions on NanoBioscience.

[121]  F. Booth Theory of Electrokinetic Effects , 1948, Nature.

[122]  Huabei Zhang,et al.  pH‐Dependent Partitioning of Acidic and Basic Drugs into Liposomes—A Quantitative Structure‐Activity Relationship Analysis , 2001 .

[123]  M. Khaledi,et al.  Evaluation of liposomal delivery of antisense oligonucleotide by capillary electrophoresis with laser-induced fluorescence detection. , 2003, Journal of chromatography. A.

[124]  E. Arriaga,et al.  Analysis of individual acidic organelles by capillary electrophoresis with laser-induced fluorescence detection facilitated by the endocytosis of fluorescently labeled microspheres. , 2003, Analytical chemistry.

[125]  M. Riekkola,et al.  Anionic liposomes in capillary electrophoresis: Effect of calcium on 1-palmitoyl-2-oleyl-sn-glycero-3-phosphatidylcholine / phosphatidylserine-coating in silica capillaries , 2004, Analytical and bioanalytical chemistry.

[126]  W. Jiskoot,et al.  OVCAR-3 cells internalize TAT-peptide modified liposomes by endocytosis. , 2004, Biochimica et biophysica acta.