Abstract
A long-range glycosyl transfer reaction was observed in the collision-induced dissociation Fourier transform (CID FT) mass spectra of benzylamine-labeled and 9-aminofluorene-labeled lacto-N-fucopentaose I (LNFP I) and lacto-N-difucohexaose I (LNDFH I). The transfer reaction was observed for the protonated molecules but not for the sodiated molecules. The long-range glycosyl transfer reaction involved preferentially one of the two L-fucose units in labeled LNDFH I. CID experiments with labeled LNFP I and labeled LNFP II determined the fucose with the greatest propensity for migration. Further experiments were performed to determine the final destination of the migrating fucose. Molecular modeling supported the experiments and reaction mechanisms are proposed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Mori, T.; Guo, M. W.; Sato, E.; Baba, T.; Takasaki, S.; Mori, E. Molecular and Immunological Approaches to Mammalian Fertilization. J. Reprod. Immunol. 2000, 47, 139–158.
Sugahara, K.; Yamada, S. Structure and Function of Oversulfated Chondroitin Sulfate Variants: Unique Sulfation Patterns and Neuroregulatory Activities. Trends Glycosci. Glycotechnol. 2000, 12, 321–349.
Kunz, C.; Rudloff, S.; Baier, W.; Klein, N.; Strobel, S. Oligosaccharides in Human Milk: Structural, Functional, and Metabolic Aspects. Annu. Rev. Nutr. 2000, 20, 699–722.
Kimura, Y. Structural Features of Free N-glycans Occurring in Developing or Growing Plant Cells and Functional Feature of Plant Endo-β-N-acetylglucosaminidase. Trends Glycosci. Glycotechnol 2000, 12, 103.
Simanek, E. E.; McGarvey, G. J.; Jablonowski, J. A.; Wong, C.-H. Selectin-Carbohydrate Interactions: From Natural Ligands to Designed Mimics. Chem. Rev. 1998, 98, 833–862.
Dwek, R. A. Glycobiology: Toward Understanding the Function of Sugars. Chem. Rev. 1996, 96, 683–720.
Parodi, A. J. Protein Glucosylation and Its Role in Protein Folding. Annu. Rev. Biochem. 2000, 69, 69–93.
Prydz, K.; Dalen, K. T. Synthesis and Sorting of Proteoglycans. J. Cell Sci. 2000, 113, 193–205.
Coppin, A.; Maes, E.; Morelle, W.; Strecker, G. Structural Analysis of 13 Neutral Oligosaccharide-Alditols Released by Reductive beta-Elimination from Oviductal Mucins of Rana temporaria. Eur. J. Biochem. 1999, 266, 94–104.
Stahl, B.; Thurl, S.; Zeng, J. R.; Karas, M.; Hillenkamp, F.; Steup, M.; Sawatzi, G. Oligosacharides from Human Milk as Revealed by Matrix-Assisted Laser Desorption Ionization Mass Spectrometry. Anal. Biochem. 1994, 223, 218–226.
Martin, W. B.; Silly, L.; Murphy, C. M.; Raley, T. J. J.; Cotter, R. J.; Bean, M. F. Fragmentation of Carbohydrates in Laser Desorption, Plasma Desorption, and Fast Atom Bombardment Mass Spectrometry. Int. J. Mass Spectrom. Ion Processes 1989, 92, 243–265.
Tseng, K.; Hedrick, J. L.; Lebrilla, C. B. Catalog-Library Approach for the Rapid and Sensitive Structural Elucidation of Oligosaccharides. Anal. Chem. 1999, 71, 3747–3754.
Sato, Y.; Suzuki, M.; Nirasawa, T.; Suzuki, A.; Endo, T. Micro-Sequencing of Glycans Using 2-Aminobenzamide and MALDI-TOF Mass Spectrometry: Occurrence of Unique Linkage-Dependent Fragmentation. Anal. Chem. 2000, 72, 1207–1216.
Zaia, J.; Costello, C. E. Compositional Analysis of Glycosaminoglycans by Electrospray Mass Spectrometry. Anal. Chem. 2001, 73, 233–239.
Wheeler, S. F.; Harvey, D. J. Negative Ion Mass Spectrometry of Sialylated Carbohydrates: Discrimination of N-Acetylneuraminic Acid Linkages by MALDI-TOF and ESI-TOF Mass Spectrometry. Anal. Chem. 2000, 72, 5027–5039.
Chai, W.; Piskarev, V.; Lawson, A. M. Negative-Ion Electrospray Mass Spectrometry of Neutral Underivatized Oligosaccharides. Anal. Chem. 2001, 73, 651–657.
Harvey, D. J.; Bateman, R. H.; Green, M. R. High-Energy Collision-Induced Fragmentation of Complex Oligosaccharides Ionized by Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry. J. Mass Spectrom. 1997, 32, 167–187.
Kovácik, V.; Hirsch, J.; Heerma, W. Linkage Determination of Alditol Disaccharides Using High-Energy Collision-Induced Dissociation Spectra of Sodium Cationized Molecules. Rapid Commun. Mass Spectrom. 1997, 11, 1353–1356.
Orlando, R.; Bush, C. A.; Fenselau, C. Structural Analysis of Oligosaccharides by Tandem Mass Spectrometry: Collisional Activation of Sodium Adduct Ions. Biomed. Environ. Mass Spectrom 1990, 19, 747–754.
Küster, B.; Naven, T. J. P.; Harvey, D. J. Effect of the Reducing-Terminal Substituents on the High Energy Collision-Induced Dissociation on Matrix-Assisted Laser Desorption/Ionization Mass Spectra of Oligosaccharides. Rapid Commun. Mass Spectrom. 1996, 10, 1645–1651.
Charlwood, J.; Birrell, H.; Gribble, A.; Burdes, V.; Tolson, D.; Camilleri, P. A Probe for the Versatile Analysis and Characterization of N-Linked Oligosaccharides. Anal. Chem. 2000, 72, 1453–1461.
Mizuno, Y.; Sasagawa, T.; Dohmae, N.; Takio, K. An Automated Interpretation of MALDI/TOF Postsource Decay Spectra of Oligosaccharides. 1. Automated Peak Assignment. Anal. Chem. 1999, 71, 4764–4771.
Garozzo, D.; Nasello, V.; Spina, E.; Sturiale, L. Discrimination of Isomeric Oligosaccharides and Sequencing of Unknowns by Post Source Decay Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry. Rapid Commun. Mass Spectrom. 1997, 11, 1561–1566.
Spengler, B.; Kirsch, D.; Kaufman, R.; Lemoine, J. Structure Analysis of Branched Oligosacchiardes using Post-source Decay in Matrix-Assisted Laser Desorption Ionization Mass Spectrometry. J. Mass Spectrom. 1995, 30, 782–787.
Lemoine, J.; Chirat, F.; Domon, B. Structural Analysis of Derivatized Oligosaccharides Using Post-Source Decay Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry. J. Mass Spectrom. 1996, 31, 908–912.
Naven, T. J. P.; Harvey, D. J.; Brown, J.; Critchley, G. Fragmentation of Complex Carbohydrates Following Ionization by Matrix-Assisted Laser Desorption with an Instrument Fitted with Time-Lag Focusing. Rapid Commun. Mass Spectrom. 1997, 11, 1681–1686.
Gaucher, S. P.; Morrow, J.; Leary, J. A. STAT: A Saccharide Topology Analysis Tool Used in Combination with Tandem Mass Spectrometry. Anal. Chem. 2000, 72, 2331–2336.
Smith, G.; Leary, J. A. Differentiation of Stereochemistry of Glycosidic Bond Configuration: Tandem Mass Spectrometry of Diastereomeric Cobalt-Glucosyl-Glucose Disaccharide Complexes. J. Am. Soc. Mass Spectrom. 1996, 7, 953–957.
Li, D. T.; Her, G. R. Structural Analysis of Chromophore-Labeled Disaccharides and Oligosaccharides by Electrospray Ionization Mass Spectrometry and High-Performance Liquid Chromatography/Electrospray Ionization Mass Spectrometry. J. Mass Spectrom. 1998, 33, 644–652.
Mulroney, B.; Traeger, J. C.; Stone, B. A. Determination of Both Linkage Position and Anomeric Configuration in Underivatized Glucopyranosyl Disaccharides by Electrospray Mass Spectrometry. J. Mass Spectrom. 1995, 30, 1277–1283.
Pare, J. R. J. Stereochemical Characterization of the Glycosidic Bond by Fast-Atom-Bombardment Mass Spectrometry. Spectroscopy 1993, 11, 157–160.
Khoo, K. H.; Dell, A. Assignment of Anomeric Configurations of Pyranose Sugars in Oligosaccharides Using a Sensitive FAB-MS Strategy. Glycobiol 1990, 1, 83–91.
Domon, B.; Mueller, D. R.; Richter, W. J. Determination of Interglycosidic Linkages in Disaccharides by High Performance Tandem Mass Spectrometry. Int. J. Mass Spectrom. Ion Processes 1990, 100, 301–311.
Domon, B.; Mueller, D. R.; Richter, W. J. Identification of Interglycosidic Linkages and Sugar Constituents in Disaccharide Subunits of Larger Glycosides by Tandem Mass Spectrometry. Org. Mass Spectrom. 1989, 24, 357–359.
Cancilla, M. T.; Gaucher, S. P.; Desaire, H.; Leary, J. A. Combined Partial Acid Hydrolysis and Electrospray Ionization-Mass Spectrometry for the Structural Determination of Oligosaccharides. Anal. Chem. 2000, 72, 2901–2907.
Zhou, Z.; Ogden, S.; Leary, J. A. Linkage Position Determination in Oligosaccharides: MS/MS Study of Lithium-Cationized Carbohydrates. J. Org. Chem. 1990, 55, 5444–5446.
Hofmeister, G. E.; Zhou, Z.; Leary, J. A. Linkage Position Determination in Lithium-Cationized Disaccharides: Tandem Mass Spectrometry and Semiempirical Calculations. J. Am. Chem. Soc. 1991, 113, 5964–5970.
Yoon, E.; Laine, R. A. Linkage Position Determination in a Novel Set of Permethylated Neutral Trisaccharides by Collisional-Induced Dissocation and Tandem Mass Spectrometry. Org. Mass Spectrom. 1992, 479–485.
Xie, Y.; Tseng, K.; Hedrick, J. L.; Lebrilla, C. B. Targeted Use of Exoglycosidase Digestion for the Structural Elucidation of Neutral O-linked Oligosaccharides. J. Am. Soc. Mass Spectrom. 2001, 12, 877–884.
Harvey, D. J.; Rudd, P. M.; Bateman, R. H.; Bordoli, R. S.; Howes, K.; Hoyes, J. B.; Vickers, R. G. Examination of Complex Oligosaccharides by Matrix-Assisted Laser Desorption/ Ionization Mass Spectrometry on Time-of-Flight and Magnetic Sector Instruments. Org. Mass Spectrom. 1994, 29, 753–765.
Reinhold, V. N.; Reinhold, B. B.; Costello, C. E. Carbohydrate Molecular Weight Profiling, Sequence, Linkage, and Branching Data: ES-MS and CID. Anal. Chem. 1995, 67, 1772–1784.
Phillips, N. J.; Apicella, M. A.; Griffiss, J. M.; Gibson, B. W. Structural Studies of the Lipooligosaccharides from Haemophilus influenzae Type b Strain A2. Biochemistry 1993, 32, 2003–2012.
Burlingame, A. L.; Boyd, R. K.; Gaskell, S. J. Mass Spectrometry. Anal. Chem. 1994, 66, 634R-683R.
Yang, Y.; Orlando, R. Simplifying the Exoglycosidase Digestion/MALDI-MS Procedures for Sequencing N-Linked Carbohydrate Side Chains. Anal. Chem. 1996, 68, 570–572.
Mechref, Y.; Novotny, M. V. Mass Spectrometric Mapping and Sequencing of N-Linked Oligosaccharides Derived from Sub-microgram Amounts of Glycoproteins. Anal. Chem. 1998, 70, 455–463.
Colangelo, J.; Orlando, R. On-Target Exoglycosidase Digestions/MALDI-MS for Determining the Primary Structures of Carbohydrate Chains. Anal. Chem. 1999, 71, 1479–1482.
Geyer, H.; Schmitt, S.; Wuhrer, M.; Geyer, R. Structural Analysis of Glycoconjugates by On-Target Enzymic Digestion and MALDI-TOF-MS. Anal. Chem. 1999, 71, 476–482.
Franz, A. H.; Molinski, T. F.; Lebrilla, C. B. MALDI-FTMS Characterization of Oligosaccharides Labeled with 9-Aminofluorene. J. Am. Soc. Mass Spectrom. 2001, 12, 1254–1261.
Broberg, S.; Broberg, A.; Duus, J. O. Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry of Oligosaccharides Derivatized by Reductive Amination and N,N-Dimethylation. Rapid Commun. Mass Spectrom. 2000, 14, 1801–1805.
Ernst, B.; Mueller, D. R.; Richter, W. J. False Sugar Sequence Ions in Electrospray Tandem Mass Spectrometry of Underivatized Sialyl-Lewis-type Oligosaccharides. Int. J. Mass Spectrom. Ion Processes, 1997;160: 283–290.
Olsthoorn, M. M. A.; Lopez-Lara, I. M.; Petersen, B. O.; Bock, K.; Haverkamp, J.; Spaink, H. P.; Thomas-Oates, J. E. Novel Branched Nod Factor Structure Results from α-(l→3) Fucosyl Transferase Activity: The Major Lipo-Chitin Oligosaccharides from Mesorhizobium loti Strain NZP2213 Bear an α-(1→3) Fucosyl Substituent on a Nonterminal Backbone Residue. Biochemistry 1998, 37, 9024–9032.
Brull, L. P.; Heerma, W.; Thomas-Oates, J.; Haverkamp, J.; Kovacik, V.; Kovac, P. Loss of Internal 1→6 Substituted Monosaccharide Residues from Underivatized and Per-O-Methylated Trisaccharides. J. Am. Soc. Mass Spectrom. 1997, 8, 43–49.
Kovacik, V.; Hirsch, J.; Kovac, P.; Heerma, W.; Thomas-Oates, J.; Haverkamp, J. Oligosaccharide Characterization Using Collision-Induced Dissociation Fast Atom Bombardment Mass Spectrometry: Evidence for Internal Monosaccharide Residue Loss. J. Mass Spectrom. 1995, 30, 949–958.
McNeil, M. Elimination of Internal Glycosyl Residues During Chemical Ionization-Mass Spectrometry of Per-O-Alkylated Oligosaccharide-Alditols. Carbohydr. Res. 1983, 123, 31–40.
Thorne, G. C.; Ballard, K. D.; Gaskell, S. J. Metastable Decomposition of Peptide [M + H] + Ions Via Rearrangement Involving Loss of C-Terminal Amino Acid Residue. J. Am. Soc. Mass Spectrom. 1990, 1, 249–257.
Cancilla, M. T.; Wong, A. W.; Voss, L. R.; Lebrilla, C. B. Fragmentation Reactions in the Mass Spectrometry Analysis of Neutral Oligosaccharides. Anal. Chem. 1999, 71, 3206–3218.
Cancilla, M. T.; Penn, S. G.; Lebrilla, C. B. Alkaline Degradation of Oligosaccharides Coupled with Matrix-Assisted Laser Desorption/Ionization Fourier Transform Mass Spectrometry: A Method for Sequencing Oligosaccharides. Anal. Chem. 1998, 70, 663–672.
Tseng, K.; Lindsay, L. L.; Penn, S.; Hedrick, J. L.; Lebrilla, C. B. Characterization of Neutral Oligosaccharide-Alditols from Xenopus laevis Egg Jelly Coats by Matrix-Assisted Laser Desorption Fourier Transform Mass Spectrometry. Anal. Biochem. 1997, 250, 18–28.
Packer, N. H.; Lawson, M. A.; Jardine, D. R.; Redmond, J. W. A General Approach to Desalting Oligosaccharides Released from Glycoproteins. Glycoconj. J. 1998, 15, 737–747.
Ramirez, J.; Ahn, S.; Grigorean, G.; Lebrilla, C. B. Evidence for the Formation of Gas-Phase Inclusion Complexes with Cyclodextrins and Amino Acids. J. Am. Chem. Soc. 2000, 122, 6884–6890.
Domon, B.; Costello, C. E. A Systematic Nomenclature for Carbohydrate Fragmentations in FAB-MS/MS Spectra of Glycoconjugates. Glycoconj. J. 1988, 5, 397–409.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Franz, A.H., Lebrilla, C.B. Evidence for long-range glycosyl transfer reactions in the gas phase. J Am Soc Mass Spectrom 13, 325–337 (2002). https://doi.org/10.1016/S1044-0305(02)00343-4
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1016/S1044-0305(02)00343-4