Abstract
Isobaric oligosaccharides enzymatically prepared from hyaluronic acid (HA) and N-acetylheparosan (NAH), were distinguished using tandem mass spectrometry. The only difference between the two series of oligosaccharides was the linkage pattern (in HA 1→3 and in NAH 1→4) between glucuronic acid and N-acetylglucosamine residues. Tandem mass spectrometry afforded spectra in which glycosidic cleavage fragment ions were observed for both HA and NAH oligosaccharides. Cross-ring cleavage ions 0,2An and 0,2An-h (n is even number) were observed only in GlcNAc residues of NAH oligosaccharides. One exception was an 0,2A2 ion fragment observed for the disaccharide from HA. These cross-ring cleavage fragment ions are useful to definitively distinguish HA and NAH oligosaccharides.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Wu, Z. L.; Zhang, L.; Beeler, D. L.; Kuberan, B.; Rosenberg, R. D. A new strategy for defining critical functional groups on heparan sulfate. FASEB J. 2002, 16, 539–545.
Capila, I.; Linhardt, R. J. Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 2002, 41, 391–412.
Bernfield, M.; Gotte, M.; Park, P. W.; Reizes, O.; Fitzgerald, M. L.; Lincecum, J.; Zako, M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68, 729–777.
Taylor, K. R.; Gallo, R. L. Glycosaminoglycans and their proteoglycans: Host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006, 20, 9–22.
Sasisekharan, R.; Raman, R.; Prabhakar, V. Glycomics approach to structure-function relationships of glycosaminoglycans. Annu. Rev. Biomed. Eng. 2006, 8, 181–231.
Meyer, K. The mucopolysaccharides of the interfibrillar substance of the mesenchyme. Ann. N. Y. Acad. Sci. 1950, 52, 961–963.
Lindahl, U.; Kusche-Gullberg, M.; Kjellen, L. Regulated diversity of heparan sulfate. J. Biol. Chem. 1998, 273, 24979–24982.
DeAngelis, P. L.; Papaconstantinou, J.; Weigel, P. H. Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes. J. Biol. Chem. 1993, 268, 19181–19184.
Widner, B.; Behr, R.; Von Dollen, S.; Tang, M.; Heu, T.; Sloma, A.; Sternberg, D.; Deangelis, P. L.; Weigel, P. H.; Brown, S. Hyaluronic acid production in Bacillus subtilis. Appl. Environ. Microbiol. 2005, 71, 3747–3752.
Esslinger, J.; Seleim, R. S.; Blobel, H. Adhesion of Pasteurella multocida to HeLa cells and to macrophages of different animal species. Rev. Med. Veterinaire. 1994, 145(49), 53.
Vann, W. F.; Schmidt, M. A.; Jann, B.; Jann, K. The structure of the capsular polysaccharide (K5 antigen) of urinary tract infective Escherichia coli 010:K5:H4: A polymer similar to desulfo-heparin. Eur. J. Biochem. 1981, 116(359), 364.
Murphy, K. J.; Merry, C. L.; Lyon, M.; Thompson, J. E.; Roberts, I. S.; Gallagher, J. T. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J. Biol. Chem. 2004, 279, 27239–27245.
Born, J.; Jann, K.; Assmann, K. J.; Lindahl, U.; Berden, J. H. N-acetylated domains in heparan sulfates revealed by a monoclonal antibody against the Escherichia coli K5 capsular polysaccharide: Distribution of the cognate epitope in normal human kidney and transplant kidney with chronic vascular rejection. J. Biol. Chem. 1996, 271, 22802–22809.
Razi, N.; Feyzi, E.; Bjork, I.; Naggi, A.; Casu, B.; Lindahl, U. Structural and functional properties of heparin analogues obtained by chemical sulphation of Escherichia coli K5 capsular polysaccharide. Biochem. J. 1995, 309(part 2), 465–472.
Lindahl, U.; Li, J. P.; Kusche-Gullberg, M.; Salmivirta, M.; Alaranta, S.; Veromaa, T.; Emeis, J.; Roberts, I.; Taylor, C.; Oreste, P.; Zoppetti, G.; Naggi, A.; Torri, G.; Casu, B. Generation of “neoheparin” from E. coli K5 capsular polysaccharide. J. Med. Chem. 2005, 48, 349–352.
Leali, D.; Belleri, M.; Urbinati, C.; Coltrini, D.; Oreste, P.; Zoppetti, G.; Ribatti, D.; Rusnati, M.; Presta, M. Fibroblast growth factor-2 antagonist activity and angiostatic capacity of sulfated Escherichia coli K5 polysaccharide derivatives. J. Biol. Chem. 2001, 276, 37900–37908.
Kuberan, B.; Beeler, D. L.; Lawrence, R.; Lech, M.; Rosenberg, R. D. Rapid two-step synthesis of mitrin from heparosan: A replacement for heparin. J. Am. Chem. Soc. 2003, 125, 12424–12425.
Banerji, S.; Wright, A. J.; Noble, M.; Mahoney, D. J.; Campbell, I. D.; Day, A. J.; Jackson, D. G. Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction. Nat. Struct. Mol. Biol. 2007, 14, 234–239.
Seyfried, N. T.; McVey, G. F.; Almond, A.; Mahoney, D. J.; Dudhia, J.; Day, A. J. Expression and purification of functionally active hyaluronan-binding domains from human cartilage link protein, aggrecan and versican: Formation of ternary complexes with defined hyaluronan oligosaccharides. J. Biol. Chem. 2005, 280, 5435–5448.
Blundell, C. D.; Mahoney, D. J.; Almond, A.; DeAngelis, P. L.; Kahmann, J. D.; Teriete, P.; Pickford, A. R.; Campbell, I. D.; Day, A. J. The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. J. Biol. Chem. 2003, 278, 49261–49270.
Zaia, J. Mass spectrometry of oligosaccharides. Mass Spectrom. Rev. 2004, 23, 161–227.
Chi, L.; Amster, J.; Linhardt, R. J. Mass spectrometry for the analysis of highly charged sulfated carbohydrate. Current. Anal. Chem. 2005, 1, 223–240.
Storm, T.; Reemtsma, T.; Jekel, M. Use of volatile amines as ion-pairing agents for the high-performance liquid chromatographic-tandem mass spectrometric determination of aromatic sulfonates in industrial waste water. J. Chromatogr. A. 1999, 854, 175–185.
Guan, F.; Ishii, A.; Seno, H.; Watanabe-Suzuki, K.; Kumazawa, T.; Suzuki, O. Use of an ion-pairing reagent for high-performance liquid chromatography-atmospheric pressure chemical ionization mass spectrometry determination of anionic anticoagulant rodenticides in body fluids. J. Chromatogr. B Biomed. Sci. Appl. 1999, 731, 155–165.
Kuberan, B.; Lech, M.; Zhang, L.; Wu, Z. L.; Beeler, D. L.; Rosenberg, R. D. Analysis of heparan sulfate oligosaccharides with ion pair-reverse phase capillary high performance liquid chromatography-microelectrospray ionization time-of-flight mass spectrometry. J. Am. Chem. Soc. 2002, 124, 8707–8718.
Minamisawa, T.; Suzuki, K.; Kajimoto, N.; Iida, M.; Maeda, H.; Hirabayashi, J. Microscale preparation of even- and odd-numbered N-acetylheparosan oligosaccharides. Carbohydr. Res. 2006, 341, 230–237.
Blundell, C. D.; Reed, M. A.; Almond, A. Complete assignment of hyaluronan oligosaccharides up to hexasaccharides. Carbohydr. Res. 2006, 341, 2803–2815.
Kuhn, A. V.; Ruttinger, H. H.; Neubert, R. H.; Raith, K. Identification of hyaluronic acid oligosaccharides by direct coupling of capillary electrophoresis with electrospray ion trap mass spectrometry. Rapid Commun. Mass Spectrom. 2003, 17, 576–582.
Kuhn, A. V.; Raith, K.; Sauerland, V.; Neubert, R. H. Quantification of hyaluronic acid fragments in pharmaceutical formulations using LC-ESI-MS. J. Pharm. Biomed. Anal. 2003, 30, 1531–1537.
Zhang, Z.; Yu, G.; Zhao, X.; Liu, H.; Guan, H.; Lawson, A. M.; Chai, W. Sequence analysis of alginate-derived oligosaccharides by negative-ion electrospray tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 2006, 17, 621–630.
Domon, B.; Costello, C. E. A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj. J. 1988, 5, 397–409.
Spengler, B.; Dolce, J. W.; Cotter, R. J. Infrared-Laser Desorption Mass-Spectrometry of Oligosaccharides—Fragmentation Mechanisms and Isomer Analysis. Anal. Chem. 1990, 62, 1731–1737.
Dallinga, J. W.; Heerma, W. Reaction mechanism and fragment ion structure determination of deprotonated small oligosaccharides, studied by negative ion fast atom bombardment (tandem) mass spectrometry. Biol. Mass Spectrom. 1991, 20, 215–231.
Zaia, J.; Miller, M. J.; Seymour, J. L.; Costello, C. E. The role of mobile protons in negative ion CID of oligosaccharides. J. Am. Soc. Mass Spectrom. 2007, 18, 952–960.
Von Seggern, C. E.; Zarek, P. E.; Cotter, R. J. Fragmentation of sialylated carbohydrates using infrared atmospheric pressure MALDI ion trap mass spectrometry from cation-doped liquid matrixes. Anal. Chem. 2003, 75, 6523–6530.
Chai, W.; Piskarev, V.; Lawson, A. M. Negative-ion electrospray mass spectrometry of neutral underivatized oligosaccharides. Anal. Chem. 2001, 73, 651–657.
Pfenninger, A.; Karas, M.; Finke, B.; Stahl, B. Structural analysis of underivatized neutral human milk oligosaccharides in the negative ion mode by nano-electrospray MS(n): Part 1: Methodology. J. Am. Soc. Mass Spectrom. 2002, 13, 1331–1340.
Pfenninger, A.; Karas, M.; Finke, B.; Stahl, B. Structural analysis of underivatized neutral human milk oligosaccharides in the negative ion mode by nano-electrospray MS(n): Part 2: Application to isomeric mixtures. J. Am. Soc. Mass Spectrom. 2002, 13, 1341–1348.
Chai, W.; Piskarev, V.; Lawson, A. M. Branching pattern and sequence analysis of underivatized oligosaccharides by combined MS/MS of singly and doubly charged molecular ions in negative-ion electrospray mass spectrometry. J. Am. Soc. Mass Spectrom. 2002, 13, 670–679.
Harvey, D. J. Fragmentation of negative ions from carbohydrates: Part 3: Fragmentation of hybrid and complex N-linked glycans. J. Am. Soc. Mass Spectrom. 2005, 16, 647–659.
Harvey, D. J. Fragmentation of negative ions from carbohydrates: Part 2: Fragmentation of high-mannose N-linked glycans. J. Am. Soc. Mass Spectrom. 2005, 16, 631–646.
Saad, O. M.; Myers, R. A.; Castleton, D. L.; Leary, J. A. Analysis of hyaluronan content in chondroitin sulfate preparations by using selective enzymatic digestion and electrospray ionization mass spectrometry. Anal. Biochem. 2005, 344, 232–239.
Zhang, Y.; Kariya, Y.; Conrad, A. H.; Tasheva, E. S.; Conrad, G. W. Analysis of keratan sulfate oligosaccharides by electrospray ionization tandem mass spectrometry. Anal. Chem. 2005, 77, 902–910.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published online October 30, 2007
Rights and permissions
About this article
Cite this article
Zhang, Z., Xie, J., Liu, J. et al. Tandem MS can distinguish hyaluronic acid from N-acetylheparosan. J. Am. Soc. Spectrom. 19, 82–90 (2008). https://doi.org/10.1016/j.jasms.2007.10.012
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.jasms.2007.10.012