Differentiating Chondroitin Sulfate Glycosaminoglycans Using Collision-Induced Dissociation;Uronic Acid Cross-Ring Diagnostic Fragments in a Single Stage of Tandem Mass Spectrometry
Restricted accessResearch articleFirst published online June, 2015
Differentiating Chondroitin Sulfate Glycosaminoglycans Using Collision-Induced Dissociation;Uronic Acid Cross-Ring Diagnostic Fragments in a Single Stage of Tandem Mass Spectrometry
The stereochemistry of the hexuronic acid residues of the structure of glycosaminoglycans (GAGs) is a key feature that affects their interactions with proteins and other biological functions. Electron-based tandem mass spectrometry methods, in particular electron detachment dissociation (EDD), have been able to distinguish glucuronic acid (GlcA) from iduronic acid (IdoA) residues in some heparan sulfate tetrasaccharides by producing epimer-specific fragments. Similarly, the relative abundance of glycosidic fragment ions produced by collision-induced dissociation (CID) or EDD has been shown to correlate with the type of hexuronic acid present in chondroitin sulfate GAGs. The present work examines the effect of charge state and degree of sodium cationization on the CID fragmentation products that can be used to distinguish GlcA and IdoA containing chondroitin sulfate A and dermatan sulfate chains. The cross-ring fragments 2,4An and 0,2Xn formed within the hexuronic acid residues are highly preferential for chains containing GlcA, distinguishing it from IdoA. The diagnostic capability of the fragments requires the selection of a molecular ion and fragment ions with specific ionization characteristics, namely charge state and number of ionizable protons. The ions with the appropriate characteristics display diagnostic properties for all the chondroitin sulfate and dermatan sulfate chains (degree of polymerization of 4–10) studied.
SisuE.FlangeaC.SerbA.ZamfirA.D., “Modern developments in mass spectrometry of chondroitin and dermatan sulfate glycosaminoglycans”, Amino Acids41, 235 (2011). doi: http://dx.doi.org/10.1007/s00726-010-0682-4
5.
AkatsuC.MizumotoS.KaneiwaT.MaccaranaM.MalmstromA.YamadaS.SugaharaK., “Dermatan sulfate epimerase 2 is the predominant isozyme in the formation of the chondroitin sulfate/dermatan sulfate hybrid structure in postnatal developing mouse brain”, Glycobiology21, 565 (2011). doi: http://dx.doi.org/10.1093/glycob/cwq208
MitsunagaC.MikamiT.MizumotoS.FukudaJ.SugaharaK., “Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum: Spatiotemporal regulation of the expression of critical disulfated disaccharides by specific sulfotransferases”, J. Biol. Chem.281, 18942 (2006). doi: http://dx.doi.org/10.1074/jbc.M510870200
8.
BaoX.F.NishimuraS.MikamiT.YamadaS.ItohN.SugaharaK., “Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of l-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities”, J. Biol. Chem.279, 9765 (2004). doi: http://dx.doi.org/10.1074/jbc.M310877200
9.
DundarM.MullerT.ZhangQ.PanJ.SteinmannB.VodopiutzJ.GruberR.SonodaT.KrabichlerB.UtermannG.BaenzigerJ.U.ZhangL.J.JaneckeA.R., “Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome”, Am. J. Hum. Genet.85, 873 (2009). doi: http://dx.doi.org/10.1016/j.ajhg.2009.11.010
10.
HouS.MaccaranaM.MinT.H.StrateI.PeraE.M., “The secreted serine protease xHtrA1 stimulates long-range FGF signaling in the early Xenopus embryo”, Dev. Cell13, 226 (2007). doi: http://dx.doi.org/10.1016/j.devcel.2007.07.001
11.
VicenteC.P.HeL.PavãoM.S.TollefsenD.M., “Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice”, Blood104, 3965 (2004). doi: http://dx.doi.org/10.1182/blood-2004-02-0598
12.
PlaasA.H.WestL.A.ThonarE.J.KarciogluZ.A.SmithC.J.KlintworthG.K.HascallV.C., “Altered fine structures of corneal and skeletal keratan sulfate and chondroitin/dermatan sulfate in macular corneal dystrophy”, J. Biol. Chem.276, 39788 (2001). doi: http://dx.doi.org/10.1074/jbc.M103227200
13.
YamadaS.SugaharaK., “Potential therapeutic application of chondroitin sulfate/dermatan sulfate”, Curr. Drug Disc. Technol.5, 289 (2008). doi: http://dx.doi.org/10.2174/157016308786733564
14.
SudoM.SatoK.ChaidedgumjornA.ToyodaH.ToidaT.ImanariT., “1H nuclear magnetic resonance spectroscopic analysis for determination of glucuronic and iduronic acids in dermatan sulfate, heparin, and heparan sulfate”, Anal. Biochem.297, 42 (2001). doi: http://dx.doi.org/10.1006/abio.2001.5296
ScottJ.E.HeatleyF., “Detection of secondary structure in glycosaminoglycans via the H NMR signal of the acetamido NH droup”, Biochem. J.207, 139 (1982).
17.
KailemiaM.J.LiL.LyM.LinhardtR.J.AmsterI.J., “Complete mass spectral characterization of a synthetic ultralow-molecular-weight heparin using collision-induced dissociation”, Anal. Chem.84, 5475 (2012). doi: http://dx.doi.org/10.1021/ac3015824
18.
KailemiaM.J.LiL.XuY.LiuJ.LinhardtR.J.AmsterI.J., “Structurally informative tandem mass spectrometry of highly sulfated natural and chemoenzymatically synthesized heparin and heparan sulfate glycosaminoglycans”, Mol. Cell. Proteomics12, 979 (2013). doi: http://dx.doi.org/10.1074/mcp.M112.026880
19.
LeachF.E.IIILyM.LaremoreT.N.WolffJ.J.PerlowJ.LinhardtR.J.AmsterI.J., “Hexuronic acid stereochemistry determination in chondroitin sulfate glycosaminoglycan oligosaccharides by electron detachment dissociation”, J. Am. Soc. Mass. Spectrom.23, 1488 (2012). doi: http://dx.doi.org/10.1007/s13361-012-0428-5
20.
WolffJ.J.AmsterI.J.ChiL.LinhardtR.J., “Electron detachment dissociation of glycosaminoglycan tetrasaccharides”, J. Am. Soc. Mass. Spectrom.18, 234 (2007). doi: http://dx.doi.org/10.1016/j.jasms.2006.09.020
21.
WolffJ.J.ChiL.LinhardtR.J.AmsterI.J., “Distinguishing glucuronic from iduronic acid in glycosaminoglycan tetrasaccharides by using electron detachment dissociation”, Anal. Chem.79, 2015 (2007). doi: http://dx.doi.org/10.1021/ac061636x
22.
WolffJ.J.LaremoreT.N.BuschA.M.LinhardtR.J.AmsterI.J., “Influence of charge state and sodium cationization on the electron detachment dissociation and infrared multiphoton dissociation of glycosaminoglycan oligosaccharides”, J. Am. Soc. Mass. Spectrom.19, 790 (2008). doi: http://dx.doi.org/10.1016/j.jasms.2008.03.010
23.
WolffJ.J.LaremoreT.N.BuschA.M.LinhardtR.J.AmsterI.J., “Electron detachment dissociation of dermatan sulfate oligosaccharides”, J. Am. Soc. Mass. Spectrom.19, 294 (2008). doi: http://dx.doi.org/10.1016/j.jasms.2007.10.007
24.
BielikA.M.ZaiaJ., “Multistage tandem mass spectrometry of chondroitin sulfate and dermatan sulfate”, Int. J. Mass Spectrom.305, 131 (2011). doi: http://dx.doi.org/10.1016/j.ijms.2010.10.017
25.
MillerM.J.C.CostelloC.E.MalmströmA.ZaiaJ., “A tandem mass spectrometric approach to determination of chondroitin/dermatan sulfate oligosaccharide glycoforms”, Glycobiology16, 502 (2006). doi: http://dx.doi.org/10.1093/glycob/cwj093
26.
SaadO.LearyJ., “Delineating mechanisms of dissociation for isomeric heparin disaccharides using isotope labeling and ion trap tandem mass spectrometry”, J. Am. Soc. Mass. Spectrom.15, 1274 (2004). doi: http://dx.doi.org/10.1016/j.jasms.2004.05.008
27.
ZaiaJ.LiX.Q.ChanS.Y.CostelloC.E., “Tandem mass spectrometric strategies for determination of sulfation positions and uronic acid epimerization in chondroitin sulfate oligosaccharides”, J. Am. Soc. Mass. Spectrom.14, 1270 (2003). doi: http://dx.doi.org/10.1016/s1044-0305(03)00541-5
28.
ZaiaJ.McClellanJ.E.CostelloC.E., “Tandem mass spectrometric determination of the 4S/6S sulfation sequence in chondroitin sulfate oligosaccharides”, Anal. Chem.73, 6030 (2001). doi: http://dx.doi.org/10.1021/ac015577t
29.
WolffJ.J.AmsterI.J.ChiL.LinhardtR.J., “Electron detachment dissociation of glycosaminoglycan tetrasaccharides”, J. Am. Soc. Mass. Spectrom.18, 234 (2007). doi: http://dx.doi.org/10.1016/j.jasms.2006.09.020
30.
ZaiaJ.LiX.-Q.ChanS.-Y.CostelloC.E., “Tandem mass spectrometric strategies for determination of sulfation positions and uronic acid epimerization in chondroitin sulfate oligosaccharides”, J. Am. Soc. Mass. Spectrom.14, 1270 (2003). doi: http://dx.doi.org/10.1016/s1044-0305(03)00541-5
31.
ZaiaJ.MillerM.J.C.SeymourJ.L.CostelloC.E., “The role of mobile protons in negative ion CID of oligosaccharides”, J. Am. Soc. Mass. Spectrom.18, 952 (2007). doi: http://dx.doi.org/10.1016/j.jasms.2007.01.016
32.
ZamfirA.SeidlerD.G.KresseH.Peter-KatalinićJ., “Structural characterization of chondroitin/dermatan sulfate oligosaccharides from bovine aorta by capillary electrophoresis and electrospray ionization quadrupole time-of-flight tandem mass spectrometry”, Rapid Commun. Mass Spectrom.16, 2015 (2002). doi: http://dx.doi.org/10.1002/rcm.820
33.
ZamfirA.SeidlerD.G.KresseH.Peter-KatalinićJ., “Structural investigation of chondroitin/dermatan sulfate oligosaccharides from human skin fibroblast decorin”, Glycobiology13, 733 (2003). doi: http://dx.doi.org/10.1093/glycob/cwg086
34.
ZhouZ.OgdenS.LearyJ.A., “Linkage position determination in oligosaccharides: Mass spectrometry (MS/MS) study of lithium-cationized carbohydrates”, J. Org. Chem.55, 5444 (1990). doi: http://dx.doi.org/10.1021/jo00307a011
35.
WolffJ.J.LaremoreT.N.BuschA.M.LinhardtR.J.AmsterI.J., “Influence of Charge State and Sodium Cationization on the Electron Detachment Dissociation and Infrared Multiphoton Dissociation of Glycosaminoglycan Oligosaccharides”, J. Am. Soc. Mass. Spectrom.19, 790 (2008). doi: http://dx.doi.org/10.1016/j.jasms.2008.03.010
36.
ZamfirA.SeidlerD.G.KresseH.Peter-KatalinićJ., “Structural investigation of chondroitin/dermatan sulfate oligosaccharides from human skin fibroblast decorin”, Glycobiology13, 733 (2003). doi: http://dx.doi.org/10.1093/glycob/cwg086
37.
LyM.LeachF.E.IIILaremoreT.N.ToidaT.AmsterI.J.LinhardtR.J., “The proteoglycan bikunin has a defined sequence”, Nat. Chem. Biol.7, 827 (2011). doi: http://dx.doi.org/10.1038/nchembio.673
38.
HitchcockA.M.CostelloC.E.ZaiaJ., “Glycoform quantification of chondroitin/dermatan sulfate using a liquid chromatography-tandem mass spectrometry platform”, Biochemistry45, 2350 (2006). doi: http://dx.doi.org/10.1021/bi052100t
39.
PervinA.GalloC.JandikK.A.HanX.-J.LinhardtR.J., “Preparation and structural characterization of large heparin-derived oligosaccharides”, Glycobiology5, 83 (1995). doi: http://dx.doi.org/10.1093/glycob/5.1.83
40.
MuñozE.XuD.AvciF.KempM.LiuJ.LinhardtR.J., “Enzymatic synthesis of heparin related polysaccharides on sensor chips: Rapid screening of heparin–protein interactions”, Biochem. Biophys. Res. Commun.339, 597 (2006). doi: http://dx.doi.org/10.1016/j.bbrc.2005.11.051
41.
CeroniA.MaassK.GeyerH.GeyerR.DellA.HaslamS.M., “Glycoworkbench: A tool for the computer-assisted annotation of mass spectra of glycans”, J. Proteome Res.7, 1650 (2008). doi: http://dx.doi.org/10.1021/pr7008252
42.
DomonB.CostelloC.E., “a systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates”, Glycoconj. J.5, 397 (1988). doi: http://dx.doi.org/10.1007/Bf01049915
43.
KailemiaM.J.LiL.XuY.LiuJ.LinhardtR.J.AmsterI.J., “Structurally informative tandem mass spectrometry of highly sulfated natural and chemoenzymatically synthesized heparin and heparan sulfate glycosaminoglycans”, Mol. Cell. Proteomics12, 979 (2013). doi: http://dx.doi.org/10.1074/mcp.M112.026880
