Glycosylation analysis of glycoproteins and proteoglycans using capillary electrophoresis‐mass spectrometry strategies

This review highlights recent developments in glycosylation analysis by modern MS in combination with CE based preseparation. Focused on CE‐MS strategies aimed for glycotyping, the review addresses the detailed glycoform analysis of glycoproteins, glycopeptides, and proteoglycans. Glycoform analysis in the context of modern glycoproteomics is briefly addressed, as well. CZE, CIEF, and frontal analysis CE approaches hyphenated to high‐resolution multistage MS for the detailed analysis of protein‐linked glycan structures are overviewed in a comprehensive way. Advantages and limitations of various methodological approaches and techniques as well as mass spectrometric instrumentation are discussed in the particular context of glycoanalysis.

[1]  S. Olson,et al.  The oligosaccharide side chain on Asn-135 of alpha-antithrombin, absent in beta-antithrombin, decreases the heparin affinity of the inhibitor by affecting the heparin-induced conformational change. , 1997, Biochemistry.

[2]  D. Josić,et al.  Determination of the site‐specific and isoform‐specific glycosylation in human plasma‐derived antithrombin by IEF and capillary HPLC‐ESI‐MS/MS , 2005, Proteomics.

[3]  J. Peter-Katalinic,et al.  Isolation and structural characterization of sialic-acid-containing glycopeptides of the O-glycosidic type from the urine of two patients with an hereditary deficiency in alpha-N-acetylgalactosaminidase activity. , 1989, Biological chemistry Hoppe-Seyler.

[4]  N. Volpi.  Advances in chondroitin sulfate analysis: application in physiological and pathological States of connective tissue and during pharmacological treatment of osteoarthritis. , 2006, Current pharmaceutical design.

[5]  Mary Ann Comunale,et al.  Proteomic analysis of serum associated fucosylated glycoproteins in the development of primary hepatocellular carcinoma. , 2006, Journal of proteome research.

[6]  M. Galceran,et al.  Pressure-assisted capillary electrophoresis-electrospray ion trap mass spectrometry for the analysis of heparin depolymerised disaccharides. , 2001, Journal of chromatography. A.

[7]  A. Deelder,et al.  Electron transfer dissociation of N-glycopeptides: loss of the entire N-glycosylated asparagine side chain. , 2007, Rapid communications in mass spectrometry : RCM.

[8]  G. Allmaier,et al.  Characterization of glyco isoforms in plasmaderived human antithrombin by on‐line capillary zone electrophoresis‐electrospray ionization‐quadrupole ion trap‐mass spectrometry of the intact glycoproteins , 2004, Electrophoresis.

[9]  T. Toyo’oka,et al.  Resolution of N-linked oligosaccharides in glycoproteins based upon transglycosylation reaction by CE-TOF-MS. , 2005, Chemical communications.

[10]  D A Cumming,et al.  Glycosylation of recombinant protein therapeutics: control and functional implications. , 1991, Glycobiology.

[11]  B. Devreese,et al.  On-column sample enrichment for the high-sensitivity sheath-flow CE-MS analysis of peptides , 2006, Analytical and bioanalytical chemistry.

[12]  T. Masuko,et al.  Collection of alpha1-acid glycoprotein molecular species by capillary electrophoresis and the analysis of their molecular masses and carbohydrate chains. Basic studies on the analysis of glycoprotein glycoforms. , 2002, Journal of chromatography. A.

[13]  A. Mort,et al.  Chapter 1 Preparation of carbohydrates for analysis by modern chromatography and electrophoresis , 2002 .

[14]  J. Michalski,et al.  The use of mass spectrometry for the proteomic analysis of glycosylation , 2006, Proteomics.

[15]  J. Zaia,et al.  A tandem mass spectrometric approach to determination of chondroitin/dermatan sulfate oligosaccharide glycoforms. , 2006, Glycobiology.

[16]  Haojie Lu,et al.  Comparative glycoproteomics based on lectins affinity capture of N‐linked glycoproteins from human Chang liver cells and MHCC97‐H cells , 2007, Proteomics.

[17]  William S Hancock,et al.  A study of glycoproteins in human serum and plasma reference standards (HUPO) using multilectin affinity chromatography coupled with RPLC‐MS/MS , 2005, Proteomics.

[18]  B. Domon,et al.  A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates , 1988, Glycoconjugate Journal.

[19]  J. Zaia.  Mass spectrometry of oligosaccharides. , 2004, Mass spectrometry reviews.

[20]  J. Peter-Katalinic,et al.  Methods in enzymology: O-glycosylation of proteins. , 2005, Methods in enzymology.

[21]  C. Neusüss,et al.  Characterization of transferrin glycoforms in human serum by CE‐UV and CE‐ESI‐MS , 2007, Electrophoresis.

[22]  J. Hirabayashi,et al.  Separation technologies for glycomics. , 2002, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[23]  G. Her,et al.  Analysis of phospholipase A2 glycosylation patterns from venom of individual bees by capillary electrophoresis/electrospray ionization mass spectrometry using an ion trap mass spectrometer. , 2000, Rapid communications in mass spectrometry : RCM.

[24]  M. Pelzing,et al.  Glycoform characterization of erythropoietin combining glycan and intact protein analysis by capillary electrophoresis – electrospray – time‐of‐flight mass spectrometry , 2006, Electrophoresis.

[25]  J. Peter-Katalinic,et al.  Electrospray ionization quadrupole time-of-flight tandem mass spectrometric analysis of hexamethylenediamine-modified maltodextrin and dextran. , 2006, Rapid communications in mass spectrometry : RCM.

[26]  M. Fukuda.  Possible roles of tumor-associated carbohydrate antigens. , 1996, Cancer research.

[27]  R. Iozzo.  Matrix proteoglycans: from molecular design to cellular function. , 1998, Annual review of biochemistry.

[28]  F. Regnier,et al.  Targeted glycoproteomics: serial lectin affinity chromatography in the selection of O-glycosylation sites on proteins from the human blood proteome. , 2006, Journal of chromatography. A.

[29]  Anne Varenne,et al.  Frontal analysis capillary electrophoresis hyphenated to electrospray ionization mass spectrometry for the characterization of the antithrombin/heparin pentasaccharide complex. , 2007, Analytical chemistry.

[30]  Y. Mechref,et al.  Differentiating structural isomers of sialylated glycans by matrix-assisted laser desorption/ionization time-of-flight/time-of-flight tandem mass spectrometry. , 2006, Rapid communications in mass spectrometry : RCM.

[31]  N. Karamanos,et al.  Derivatization of carbohydrates for chromatographic, electrophoretic and mass spectrometric structure analysis. , 2003, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[32]  J. V. Van Beeumen,et al.  Characterization of cellobiohydrolase I N-glycans and differentiation of their phosphorylated isomers by capillary electrophoresis-Q-Trap mass spectrometry. , 2004, Analytical chemistry.

[33]  Anna Flamigni,et al.  Overview on advances in capillary electrophoresis‐mass spectrometry of carbohydrates: A tabulated review , 2006, Electrophoresis.

[34]  Huwei Liu,et al.  Ionene-dynamically coated capillary for analysis of urinary and recombinant human erythropoietin by capillary electrophoresis and online electrospray ionization mass spectrometry. , 2005, Journal of separation science.

[35]  F. Regnier,et al.  Comparative glycoproteomics of N-linked complex-type glycoforms containing sialic acid in human serum. , 2005, Analytical chemistry.

[36]  Ionel Ciucanu,et al.  A simple and rapid method for the permethylation of carbohydrates , 1984 .

[37]  D. Harvey,et al.  Matrix-assisted laser desorption/ionization mass spectrometry of carbohydrates. , 1999, Mass spectrometry reviews.

[38]  J. Peter-Katalinic,et al.  Copper-coated microsprayer interface for on-line sheathless capillary electrophoresis electrospray mass spectrometry of carbohydrates. , 2006, Journal of separation science.

[39]  J. V. Van Beeumen,et al.  New insights in Rapana venosa hemocyanin N-glycosylation resulting from on-line mass spectrometric analyses. , 2007, Glycobiology.

[40]  M. Zehl,et al.  Determination of glycopeptide structures by multistage mass spectrometry with low-energy collision-induced dissociation: comparison of electrospray ionization quadrupole ion trap and matrix-assisted laser desorption/ionization quadrupole ion trap reflectron time-of-flight approaches. , 2004, Rapid communications in mass spectrometry : RCM.

[41]  F. Regnier,et al.  Use of a lectin affinity selector in the search for unusual glycosylation in proteomics. , 2002, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[42]  Z. Rassi.  Chapter 18 Capillary electrophoresis and electrochromatography of carbohydrates , 2002 .

[43]  T. Veenstra,et al.  On-column sample enrichment for capillary electrophoresis sheathless electrospray ionization mass spectrometry: evaluation for peptide analysis and protein identification. , 2003, Analytical chemistry.

[44]  C. Larive,et al.  Ultraperformance ion-pair liquid chromatography coupled to electrospray time-of-flight mass spectrometry for compositional profiling and quantification of heparin and heparan sulfate. , 2008, Analytical chemistry.

[45]  A. Zamfir,et al.  Capillary electrophoresis and off-line capillary electrophoresis-electrospray ionization quadrupole time-of-flight tandem mass spectrometry of carbohydrates. , 2000, Journal of chromatography. A.

[46]  Carolyn R. Bertozzi,et al.  Essentials of Glycobiology , 1999 .

[47]  R. Kannagi,et al.  Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. , 1993, Cancer research.

[48]  E. Balaguer,et al.  Intact Glycoform Characterization of Erythropoietin-α and Erythropoietin-β by CZE-ESI-TOF-MS , 2006 .

[49]  Yehia Mechref,et al.  Solid-phase permethylation of glycans for mass spectrometric analysis. , 2005, Rapid communications in mass spectrometry : RCM.

[50]  Jennifer J. Kohler,et al.  Chemical methods for glycoprotein discovery. , 2007, Current opinion in chemical biology.

[51]  J. Peter-Katalinic,et al.  Galactosaminoglycan Function and Oligosaccharide Structure Determination , 2007, TheScientificWorldJournal.

[52]  W. Michalski.  The Mass Spectrometric Analysis of Glycoproteins and their Glycan Structures , 2005 .

[53]  J. Huntington,et al.  Antithrombin-heparin affinity reduced by fucosylation of carbohydrate at asparagine 155. , 1996, Biochemistry.

[54]  R. Parekh,et al.  Use of hydrazine to release in intact and unreduced form both N- and O-linked oligosaccharides from glycoproteins. , 1993, Biochemistry.

[55]  Catherine E Costello,et al.  Glycoform quantification of chondroitin/dermatan sulfate using a liquid chromatography-tandem mass spectrometry platform. , 2006, Biochemistry.

[56]  D. J. Harrison,et al.  Separation and identification of peptides from gel-isolated membrane proteins using a microfabricated device for combined capillary electrophoresis/nanoelectrospray mass spectrometry. , 2000, Analytical chemistry.

[57]  J. Peter-Katalinic,et al.  Off‐line capillary electrophoresis/fully automated nanoelectrospray chip quadrupole time‐of‐flight mass spectrometry and tandem mass spectrometry for glycoconjugate analysis , 2004 .

[58]  A. Rizzi,et al.  Capillary isoelectric focusing hyphenated to single‐ and multistage matrix‐assisted laser desorption/ionization‐mass spectrometry using automated sheath‐flow‐assisted sample deposition , 2008, Electrophoresis.

[59]  J. Esko,et al.  The sweet and sour of cancer: glycans as novel therapeutic targets , 2005, Nature Reviews Cancer.

[60]  T. Endo.  Chapter 7 Lectin-affinity chromatography of carbohydrates , 2002 .

[61]  W. Lindberg,et al.  Single run measurements of drug-protein binding by high-performance frontal analysis capillary electrophoresis and mass spectrometry. , 2005, Rapid communications in mass spectrometry : RCM.

[62]  J. Peter-Katalinic,et al.  Glycoscreening by on‐line sheathless capillary electrophoresis/electrospray ionization‐quadrupole time of flight‐tandem mass spectrometry , 2001, Electrophoresis.

[63]  M. Pelzing,et al.  Glycoform characterization of intact erythropoietin by capillary electrophoresis‐electrospray‐time of flight‐mass spectrometry , 2005, Electrophoresis.

[64]  J. Peter-Katalinic,et al.  Structural investigation of chondroitin/dermatan sulfate oligosaccharides from human skin fibroblast decorin. , 2003, Glycobiology.

[65]  T. Janáky,et al.  Design and performance of a sheathless capillary electrophoresis/mass spectrometry interface by combining fused-silica capillaries with gold-coated nanoelectrospray tips. , 2005, Rapid communications in mass spectrometry : RCM.

[66]  André M Deelder,et al.  Glycoproteomics based on tandem mass spectrometry of glycopeptides. , 2007, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[67]  P. Gareil,et al.  Identification of heparin oligosaccharides by direct coupling of capillary electrophoresis/ionspray-mass spectrometry. , 1999, Rapid communications in mass spectrometry : RCM.

[68]  André M Deelder,et al.  Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum , 2007, Proteomics.

[69]  P. Schmitt‐Kopplin,et al.  Capillary electrophoresis – mass spectrometry: Survey on developments and applications 2003–2004 , 2005, Electrophoresis.

[70]  J. Peter-Katalinic,et al.  Sheathless reverse‐polarity capillary electrophoresis‐electrospray‐mass spectrometry for analysis of underivatized glycoconjugates , 2005, Electrophoresis.

[71]  J. Michalski,et al.  Sequencing of oligosaccharides derivatized with benzylamine using electrospray ionization‐quadrupole time of flight‐tandem mass spectrometry , 2004, Electrophoresis.

[72]  F. Regnier,et al.  Proteomics of glycoproteins based on affinity selection of glycopeptides from tryptic digests. , 2001, Journal of chromatography. B, Biomedical sciences and applications.

[73]  S. Tsuboi,et al.  Dual roles of sialyl Lewis X oligosaccharides in tumor metastasis and rejection by natural killer cells , 1999, The EMBO journal.

[74]  H. Perreault,et al.  Isolation and identification of sialylated glycopeptides from bovine α1-acid glycoprotein by off-line capillary electrophoresis MALDI-TOF mass spectrometry , 2006 .

[75]  Shuhei Yamada,et al.  Oversulfated Chondroitin/Dermatan Sulfates Containing GlcAβ1/IdoAα1–3GalNAc(4,6-O-disulfate) Interact with L- and P-selectin and Chemokines* , 2002, The Journal of Biological Chemistry.

[76]  Yehia Mechref,et al.  Structural investigations of glycoconjugates at high sensitivity. , 2002, Chemical reviews.

[77]  P. Crocker,et al.  Carbohydrate recognition systems: functional triads in cell-cell interactions. , 1996, Current opinion in structural biology.

[78]  M. Taverna,et al.  Chapter 20 Analysis of glycoproteins and their glycopeptide and glycan fragments by electrophoresis and capillary electrophoresis , 2002 .

[79]  M. Novotny,et al.  High‐performance capillary electrophoresis of glycoconjugates , 1993, Electrophoresis.

[80]  B. Ueberheide,et al.  The utility of ETD mass spectrometry in proteomic analysis. , 2006, Biochimica et biophysica acta.

[81]  Raymond A. Dwek,et al.  Glycobiology: Toward Understanding the Function of Sugars. , 1996, Chemical reviews.

[82]  S. Amon,et al.  Capillary zone electrophoresis of glycopeptides under controlled electroosmotic flow conditions coupled to electrospray and matrix‐assisted laser desorption/ionization mass spectrometry , 2006, Electrophoresis.

[83]  J. Trowbridge,et al.  Dermatan Sulfate Proteoglycan and Glycosaminoglycan Synthesis Is Induced in Fibroblasts by Transfer to a Three-dimensional Extracellular Environment* , 2004, Journal of Biological Chemistry.

[84]  E. Bayer,et al.  Chapter 27 Mass spectrometry of oligosaccharides , 2002 .

[85]  Her,et al.  Sheathless capillary electrophoresis/electrospray mass spectrometry using a carbon-coated fused-silica capillary , 2000, Analytical chemistry.

[86]  P. Thibault,et al.  Probing genetic variation and glycoform distribution in lectins of the Erythrina genus by mass spectrometry. , 2004, Archives of Biochemistry and Biophysics.

[87]  J. Peter-Katalinic,et al.  Structural characterization of chondroitin/dermatan sulfate oligosaccharides from bovine aorta by capillary electrophoresis and electrospray ionization quadrupole time-of-flight tandem mass spectrometry. , 2002, Rapid communications in mass spectrometry : RCM.

[88]  S. Selleck,et al.  Order out of chaos: assembly of ligand binding sites in heparan sulfate. , 2002, Annual review of biochemistry.

[89]  Catherine E Costello,et al.  Tandem mass spectrometry of sulfated heparin-like glycosaminoglycan oligosaccharides. , 2003, Analytical chemistry.

[90]  H. Stutz.  Advances in the analysis of proteins and peptides by capillary electrophoresis with matrix‐assisted laser desorption/ionization and electrospray‐mass spectrometry detection , 2005, Electrophoresis.

[91]  S. Müller,et al.  A serial lectin approach to the mucin‐type O‐glycoproteome of Drosophila melanogaster S2 cells , 2007, Proteomics.

[92]  Joseph Zaia,et al.  Size-exclusion chromatography of heparin oligosaccharides at high and low pressure. , 2006, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[93]  B. Domon,et al.  Capillary electrophoresis/electrospray ion trap mass spectrometry for the analysis of negatively charged derivatized and underivatized glycans. , 2002, Rapid communications in mass spectrometry : RCM.

[94]  Alejandro Cifuentes,et al.  On‐line capillary electrophoresis‐mass spectrometry for the analysis of biomolecules , 2004, Electrophoresis.

[95]  C. Neusüss,et al.  Glycoprotein characterization combining intact protein and glycan analysis by capillary electrophoresis-electrospray ionization-mass spectrometry. , 2006, Analytical chemistry.

[96]  T. Takao,et al.  A method for determination of N-glycosylation sites in glycoproteins by collision-induced dissociation analysis in fast atom bombardment mass spectrometry: identification of the positions of carbohydrate-linked asparagine in recombinant alpha-amylase by treatment with peptide-N-glycosidase F in 18O- , 1992, Analytical biochemistry.

[97]  Zhihong Guo,et al.  Chip‐based CE coupled to a quadrupole TOF mass spectrometer for the analysis of a glycopeptide , 2007, Electrophoresis.

[98]  R. Neubert,et al.  Identification of hyaluronic acid oligosaccharides by direct coupling of capillary electrophoresis with electrospray ion trap mass spectrometry. , 2003, Rapid communications in mass spectrometry : RCM.

[99]  E. Schönherr,et al.  On‐line sheathless capillary electrophoresis/nanoelectrospray ionization‐tandem mass spectrometry for the analysis of glycosaminoglycan oligosaccharides , 2004, Electrophoresis.

[100]  P. Manavalan,et al.  Transgenically produced human antithrombin: structural and functional comparison to human plasma-derived antithrombin. , 1998, Blood.

[101]  Stacey Ma,et al.  Capillary electrophoresis-mass spectrometry as a characterization tool for therapeutic proteins. , 2006, Analytical biochemistry.

[102]  Hyun Joo An,et al.  Improved capillary electrophoretic separation and mass spectrometric detection of oligosaccharides. , 2003, Journal of chromatography. A.

[103]  J. Briggs,et al.  Oligosaccharide release and MALDI-TOF MS analysis of N-linked carbohydrate structures from glycoproteins. , 2005, Methods in molecular biology.

[104]  J. Peter-Katalinic,et al.  Capillary electrophoresis‐mass spectrometry for glycoscreening in biomedical research , 2004, Electrophoresis.

[105]  J. Abrahams,et al.  Structure of beta-antithrombin and the effect of glycosylation on antithrombin's heparin affinity and activity. , 2003, Journal of molecular biology.

[106]  E. Bayer,et al.  Recent advances in capillary electrophoresis/electrospray‐mass spectrometry , 2001, Electrophoresis.

[107]  R. Zeng,et al.  Capillary electrophoresis-electrospray mass spectrometry for the characterization of high-mannose-type N-glycosylation and differential oxidation in glycoproteins by charge reversal and protease/glycosidase digestion. , 2001, Analytical chemistry.

[108]  Shigeo Suzuki,et al.  A tabulated review of capillary electrophoresis of carbohydrates , 1998, Electrophoresis.