Free‐flow electrophoresis in the proteomic era: A technique in flux

Since its introduction five decades ago, free‐flow electrophoresis (FFE) has been mainly employed for the isolation and fractionation of cells, cell organelles and protein mixtures. In the meantime, the growing interest in the proteome of these bio‐particles and biopolymers has shed light on two further facets in the potential of FFE, namely its applicability as an analytical tool and sensor. This review is intended to outline recent innovations, FFE has gained in the proteomic era, and to point out the valuable contributions it has made to the analysis of the proteome of cells, sub‐cellular organelles and functional protein networks.

[1]  T. Brüning,et al.  Characterization of apolipoprotein B-containing lipoproteins separated by preparative free flow isotachophoresis. , 1990, Journal of lipid research.

[2]  J. Carlis,et al.  Proteomics Analysis of Cells in Whole Saliva from Oral Cancer Patients via Value-added Three-dimensional Peptide Fractionation and Tandem Mass Spectrometry*S , 2008, Molecular & Cellular Proteomics.

[3]  E. Hansen,et al.  Antigen-specific electrophoretic cell separation (ASECS): isolation by human T and B lymphocyte subpopulations by free-flow electrophoresis after reaction with antibodies. , 1982, Journal of immunological methods.

[4]  J. Klose From 2‐D electrophoresis to proteomics , 2009, Electrophoresis.

[5]  M. Clifton,et al.  Conditions for purification of proteins by free‐flow zone electrophoresis , 1990, Electrophoresis.

[6]  C. Obermaier,et al.  Free‐flow isoelectric focusing of proteins remaining in cell fragments following sonication of thyroid carcinoma cells , 2005, Electrophoresis.

[7]  B. Hering,et al.  Fractions from commercial collagenase preparations: use in enzymic isolation of the islets of Langerhans from porcine pancreas. , 1996, Cell transplantation.

[8]  D. Müller-Wieland,et al.  Enhancing mass spectrometry based serum profiling by a combination of free flow electrophoresis and ClinProt™ , 2009, Archives of physiology and biochemistry.

[9]  Alexey I Nesvizhskii,et al.  Optimized peptide separation and identification for mass spectrometry based proteomics via free-flow electrophoresis. , 2006, Journal of proteome research.

[10]  M. Bier,et al.  Purification of lentil lectins using preparative electrophoresis. , 1988, Journal of chromatography.

[11]  R. Kuhn,et al.  Application of free flow electrophoresis to the preparative purification of basic proteins from an E. coli cell extract. , 1989, Journal of chromatography.

[12]  W. Hymer,et al.  Mammalian pituitary growth hormone: Applications of free flow electrophoresis , 2000, Electrophoresis.

[13]  C. Eckerskorn,et al.  Peroxisomes from the heavy mitochondrial fraction: isolation by zonal free flow electrophoresis and quantitative mass spectrometrical characterization. , 2010, Journal of proteome research.

[14]  D. Kohlheyer,et al.  Miniaturizing free‐flow electrophoresis – a critical review , 2008, Electrophoresis.

[15]  P. Boček,et al.  Optimized continuous flow electrophoresis , 1996, Electrophoresis.

[16]  P. Brown,et al.  Free-flow electrophoresis as a preparative separation technique , 1994 .

[17]  H. Fahimi,et al.  Isolation of rat hepatic peroxisomes by means of immune free flow electrophoresis , 1997, Electrophoresis.

[18]  H. Hustedt,et al.  Correlation of migration behavior in free‐flow zone electrophoresis and electrophoretic titration curve , 1990, Electrophoresis.

[19]  D. Burggraf,et al.  Free flow‐isoelectric focusing of human cellular lysates as sample preparation for protein analysis , 1995, Electrophoresis.

[20]  Free-flow electrophoresis of the human urinary proteome. , 2008, Methods in molecular biology.

[21]  P. Ping,et al.  Exploring proteasome complexes by proteomic approaches , 2007, Proteomics.

[22]  R. Lewensohn,et al.  Use of narrow‐range peptide IEF to improve detection of lung adenocarcinoma markers in plasma and pleural effusion , 2009, Proteomics.

[23]  M. Mayr,et al.  Proteomic analysis of the secretome of human umbilical vein endothelial cells using a combination of free‐flow electrophoresis and nanoflow LC‐MS/MS , 2009, Proteomics.

[24]  K. Hannig Eine Neuentwicklung der trägerfreien kontinuierlichen Elektrophorese. Zur Trennung hochmolekularer und grobdisperser Teilchen , 1964 .

[25]  Free flow electrophoresis for the purification of proteins: I. Zone electrophoresis and isotachophoresis , 1990, Electrophoresis.

[26]  A. Millar,et al.  Free-flow electrophoresis for purification of plant mitochondria by surface charge. , 2007, The Plant journal : for cell and molecular biology.

[27]  T. Griffin,et al.  Preparative peptide isoelectric focusing as a tool for improving the identification of lysine-acetylated peptides from complex mixtures. , 2007, Journal of proteome research.

[28]  F. McLafferty,et al.  Top down versus bottom up protein characterization by tandem high- resolution mass spectrometry , 1999 .

[29]  M. Mackova,et al.  Mapping the peptide and protein immune response in the larvae of the fleshfly Sarcophaga bullata , 2008, Journal of peptide science : an official publication of the European Peptide Society.

[30]  R. Moritz,et al.  Continuous free‐flow electrophoresis separation of cytosolic proteins from the human colon carcinoma cell line LIM 1215: A non two‐dimensional gel electrophoresis‐based proteome analysis strategy , 2001, Proteomics.

[31]  Eugene A. Kapp,et al.  A proteome strategy for fractionating proteins and peptides using continuous free-flow electrophoresis coupled off-line to reversed-phase high-performance liquid chromatography. , 2004, Analytical chemistry.

[32]  J. Duman Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. , 1994, Biochimica et biophysica acta.

[33]  Min-Seok Kwon,et al.  Efficient prefractionation of low‐abundance proteins in human plasma and construction of a two‐dimensional map , 2005, Proteomics.

[34]  H. Balmann,et al.  STUDY OF ELECTROHYDRODYNAMIC PHENOMENA DURING PURIFICATION OF PROTEINS BY CONTINUOUS FLOW ELECTROPHORESIS , 1991 .

[35]  T. Griffin,et al.  Evaluating preparative isoelectric focusing of complex peptide mixtures for tandem mass spectrometry-based proteomics: a case study in profiling chromatin-enriched subcellular fractions in Saccharomyces cerevisiae. , 2005, Analytical Chemistry.

[36]  T. Meitinger,et al.  Improved proteome analysis of Saccharomyces cerevisiae mitochondria by free‐flow electrophoresis , 2003, Proteomics.

[37]  C. Obermaier,et al.  Two‐dimensional separation of human plasma proteins using iterative free‐flow electrophoresis , 2007, Proteomics.

[38]  C. Eckerskorn,et al.  Efficient separation and analysis of peroxisomal membrane proteins using free‐flow isoelectric focusing , 2004, Electrophoresis.

[39]  Ruedi Aebersold,et al.  Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry , 2003, Nature Biotechnology.

[40]  Gerhard Weber,et al.  Chapter 6 Electrophoresis in Space , 1999 .

[41]  Eugene A. Kapp,et al.  Application of 2‐D free‐flow electrophoresis/RP‐HPLC for proteomic analysis of human plasma depleted of multi high‐abundance proteins , 2005, Proteomics.

[42]  P. Boček,et al.  Continuous free‐flow electrophoresis , 1998, Electrophoresis.

[43]  P. Boček,et al.  Interval isotachophoresis for purification and isolation of ionogenic species , 1998, Electrophoresis.

[44]  R. T. Turgeon,et al.  Micro free-flow electrophoresis: theory and applications , 2009, Analytical and bioanalytical chemistry.

[45]  A. Burlingame,et al.  Proteomic analysis of plasma membrane vesicles isolated from the rat renal cortex , 2005, Proteomics.

[46]  H. Balmann,et al.  Continuous-flow electrophoresis: a separation criterion applied to the separation of model proteins , 1992 .

[47]  Free flow electrophoresis coupled with liquid chromatography-mass spectrometry for a proteomic study of the human cell line (K562/CR3). , 2004, Journal of chromatography. A.

[48]  H. Hustedt,et al.  Separation of enzymes from microorganism crude extracts by free‐flow zone electrophoresis , 2000, Biotechnology and Bioengineering.

[49]  Patrick G. A. Pedrioli,et al.  A high-quality catalog of the Drosophila melanogaster proteome , 2007, Nature Biotechnology.

[50]  M. Nissum,et al.  Analysis of human plasma proteins: a focus on sample collection and separation using free-flow electrophoresis , 2008, Expert review of proteomics.

[51]  A. Millar,et al.  Novel Proteins, Putative Membrane Transporters, and an Integrated Metabolic Network Are Revealed by Quantitative Proteomic Analysis of Arabidopsis Cell Culture Peroxisomes1[W][OA] , 2008, Plant Physiology.

[52]  C. Ivory,et al.  On‐Line Optical Fiber Detection in a Preparative Free‐Flow Electrofocusing Apparatus , 2006, Biotechnology progress.

[53]  P. Boček,et al.  Recent developments in preparative free flow isoelectric focusing , 1998, Electrophoresis.

[54]  G. Fischer,et al.  Differentation by preparative continuous free flowisoelectric focusing of cyclosporin A inhibitable peptidyl‐prolyl cis/trans isomerase of human erythrocytes , 1994, Electrophoresis.

[55]  A. Heck,et al.  Accurate molecular weight analysis of histones using FFE and RP-HPLC on monolithic capillary columns. , 2009, Journal of separation science.

[56]  A. Lustig,et al.  Rapid isolation of OmpF porin-LPS complexes suitable for structure-function studies. , 1989, Biochemistry.

[57]  V. Kašička,et al.  Correlation of capillary zone electrophoresis with continuous free‐flow zone electrophoresis: Application to the analysis and purification of synthetic growth hormone releasing peptide , 1990, Electrophoresis.

[58]  E. Harms,et al.  Human lysosomes can be purified from diploid skin fibroblasts by free-flow electrophoresis. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Brüning,et al.  Macrophage interaction of HDL subclasses separated by free flow isotachophoresis. , 1990, Journal of lipid research.

[60]  R. Aebersold,et al.  Mass Spectrometric Detection of Tissue Proteins in Plasma*S , 2007, Molecular & Cellular Proteomics.

[61]  H. Wagner,et al.  Scale‐up of free flow electrophoresis: I. Purification of alcohol dehydrogenase from a crude yeast extract by zone electrophoresis , 1990, Electrophoresis.

[62]  H. Wagner,et al.  Free-flow electrophoresis , 1989, Nature.

[63]  J. Klose Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues , 1975, Humangenetik.

[64]  H. Wrba,et al.  Notizen: Isolierung von vitalen Tumorzellen durch trägerfreie Elektrophorese , 1964 .

[65]  A. Reichert,et al.  Differential Analysis of Saccharomyces cerevisiae Mitochondria by Free Flow Electrophoresis*S , 2006, Molecular & Cellular Proteomics.

[66]  Kurt Hannig,et al.  Die trägerfreie kontinuierliche Elektrophorese und ihre Anwendung , 1961 .

[67]  S. Schmid,et al.  Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis , 1987, The Journal of cell biology.

[68]  I. Mellman,et al.  Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes , 1994, Nature.

[69]  Howard M. Goodman,et al.  Resolution of simian virus 40 proteins in whole cell extracts by two-dimensional electrophoresis: Heterogeneity of the major capsid protein , 1976, Cell.

[70]  V. Klyushnichenko,et al.  Methods of preparation of recombinant cytokine proteins. , 1998, Protein expression and purification.

[71]  G. Fischer,et al.  Influence of additives on resolution and focusing efficiency in free-flow isoelectric focusing , 1994 .

[72]  Improving sensitivity in micro‐free flow electrophoresis using signal averaging , 2009, Electrophoresis.

[73]  H. Hustedt,et al.  Application of continuous zone electrophoresis to preparative separation of proteins , 1993, Biotechnology and bioengineering.

[74]  R. Wildgruber,et al.  Free-flow electrophoresis system for plasma proteomic applications. , 2008, Methods in molecular biology.

[75]  G. Ziegelberger,et al.  Three pheromone-binding proteins in olfactory sensilla of the two silkmoth species Antheraea polyphemus and Antheraea pernyi. , 2000, European journal of biochemistry.

[76]  Timothy J Griffin,et al.  A Catalogue of Human Saliva Proteins Identified by Free Flow Electrophoresis-based Peptide Separation and Tandem Mass Spectrometry*S , 2005, Molecular & Cellular Proteomics.

[77]  Monilola A. Olayioye,et al.  Breast cancer protein StarD10 identified by three‐dimensional separation using free‐flow electrophoresis, reversed‐phase high‐performance liquid chromatography, and sodium dodecyl sulfate‐polyacrylamide gel electrophoresis , 2005, Electrophoresis.

[78]  T. Barth,et al.  Application of capillary and free-flow zone electrophoresis and isotachophoresis to the analysis and preparation of the synthetic tetrapeptide fragment of growth hormone-releasing peptide. , 1994, Journal of chromatography. B, Biomedical applications.

[79]  T. Hirokawa,et al.  Preparative procedures in isotachophoresis , 1994 .

[80]  H. Miyatake,et al.  Development of a novel ampholyte buffer for isoelectric focusing: electric charge-separation of protein samples for X-ray crystallography using free-flow isoelectric focusing. , 2005, Acta crystallographica. Section D, Biological crystallography.

[81]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[82]  R. Wildgruber,et al.  Functional and Complementary Phosphorylation State Attributes of Human Insulin-like Growth Factor-Binding Protein-1 (IGFBP-1) Isoforms Resolved by Free Flow Electrophoresis , 2009, Molecular & Cellular Proteomics.

[83]  R. Kuhn,et al.  Free flow electrophoresis as a method for the purification of enzymes from E. coli cell extract , 1989, Electrophoresis.

[84]  Dietrich Kohlheyer,et al.  Bubble-free operation of a microfluidic free-flow electrophoresis chip with integrated Pt electrodes. , 2008, Analytical chemistry.

[85]  J. Bauer,et al.  Counterbalancing hydrodynamic sample distortion effects increases resolution of free‐flow zone electrophoresis , 1998, Electrophoresis.

[86]  Monica H. Elliott,et al.  Free‐flow electrophoresis for top‐down proteomics by Fourier transform ion cyclotron resonance mass spectrometry , 2008, Proteomics.

[87]  R. Vera-Estrella,et al.  Enhanced separation of membranes during free flow zonal electrophoresis in plants. , 2007, Analytical chemistry.

[88]  R. Wildgruber,et al.  Resolution of adiponectin oligomers in human plasma using free flow electrophoresis , 2009, Archives of physiology and biochemistry.

[89]  Comparative studies of recycling isoelectric focusing and continuous flow electrophoresis: Separation of proteins with minor charge differences , 1990, Electrophoresis.

[90]  Richard D. Smith,et al.  Proteomics by FTICR mass spectrometry: top down and bottom up. , 2005, Mass spectrometry reviews.

[91]  D. M. Morré,et al.  Antitumor sulfonylurea-inhibited NADH oxidase of cultured HeLa cells shed into media. , 1996, Biochimica et biophysica acta.

[92]  V. V. Osipov,et al.  Application of free‐flow electrophoresis for isolation and purification of proteins and peptides , 1998, Electrophoresis.