Structurally informative tandem mass spectrometry of highly sulfated natural and chemoenzymatically synthesized heparin and heparan sulfate glycosaminoglycans

Molecular and Cellular Proteomics

Volumn 12, Issue 4, 2013, Pages 979-990

  Kailemia, Muchena J ^a   Li, Lingyun ^b   Xu, Yongmei ^c   Liu, Jian ^c   Linhardt, Robert J ^b   Amster, I Jonathan ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c University of North Carolina   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYL GROUP; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; TETRASACCHARIDE;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DRUG SYNTHESIS; ELECTROSPRAY; ISOMER; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; STEREOCHEMISTRY; TANDEM MASS SPECTROMETRY; WATER LOSS;

ANIMALS; BIOCATALYSIS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; HEPARIN; HEPARITIN SULFATE; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PHOSPHOADENOSINE PHOSPHOSULFATE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SULFOTRANSFERASES; SULFURIC ACID ESTERS; SUS SCROFA; TANDEM MASS SPECTROMETRY;

EID: 84875997500     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.026880     Document Type: Article

References (53)

1. Capila, I., and Linhardt, R. J. (2002) Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 41, 391-412
2. Casu, B. (1985) Structure and biological activity of heparin. Adv. Carbohydr. Chem. Biochem. 43, 51-134
3. Ampofo, S. A., Wang, H. M., and Linhardt, R. J. (1991) Disaccharide compositional analysis of heparin and heparan sulfate using capillary zone electrophoresis. Anal. Biochem. 199, 249-255
4. Velve-Casquillas, G., Le Berre, M., Piel, M., and Tran, P. T. (2010) Micro- fluidic tools for cell biological research. Nano Today 5, 28-47
5. Chi, L., Amster, J., and Linhardt, R. J. (2005) Mass spectrometry for the analysis of highly charged sulfated carbohydrates. Curr. Anal. Chem. 1, 223-240
6. Conrad, H. E. (1998) Heparin Binding Proteins, 183-411, Academic Press, San Diego, CA
7. Vanboeckel, C. A., and Petitou, M. (1993) The unique antithrombin-III binding domain of heparin - a lead to new synthetic antithrombotics. Angew. Chem. Int. Ed. Engl. 32, 1671-1690
8. Petitou, M., Mourey, L., Samama, J. P., and Pascal, M. (1993) Molecular interaction of synthetic oligosaccharides with antithrombin-III. J. Cell. Biochem. 17A, 369-369
9. Hess, G. (2008) Congress investigates tainted heparin. Chem. Eng. News 86, 8
10. Kemsley, J. (2008) Heparin undone. Chem. Eng. News 86, 38-40
11. Liu, H., Zhang, Z., and Linhardt, R. J. (2009) Lessons learned from the contamination of heparin. Nat. Prod. Rep. 26, 313-321
12. Yang, B., Solakyildirim, K., Chang, Y., and Linhardt, R. (2010) Hyphenated techniques for the analysis of heparin and heparan sulfate. Anal. Bioanal. Chem. 399, 541-557
13. Wolff, J. J., Amster, I. J., Chi, L., and Linhardt, R. J. (2007) Electron detachment dissociation of glycosaminoglycan tetrasaccharides. J. Am. Soc. Mass. Spectrom. 18, 234-244
14. Wolff, J. J., Chi, L., Linhardt, R. J., and Amster, I. J. (2007) Distinguishing glucuronic from iduronic acid in glycosaminoglycan tetrasaccharides by using electron detachment dissociation. Anal. Chem. 79, 2015-2022
15. Leach, F. E., 3rd, Wolff, J. J., Laremore, T. N., Linhardt, R. J., and Amster, I. J. (2008) Evaluation of the experimental parameters which control electron detachment dissociation, and their effect on the fragmentation efficiency of glycosaminoglycan carbohydrates. Int. J. Mass Spectrom. 276, 110-115
16. Wolff, J. J., Laremore, T. N., Aslam, H., Linhardt, R. J., and Amster, I. J. (2008) Electron-induced dissociation of glycosaminoglycan tetrasaccharides. J. Am. Soc. Mass. Spectrom. 19, 1449-1458
17. Wolff, J. J., Laremore, T. N., Busch, A. M., Linhardt, R. J., and Amster, I. J. (2008) Influence of charge state and sodium cationization on the electron detachment dissociation and infrared multiphoton dissociation of glyco-saminoglycan oligosaccharides. J. Am. Soc. Mass. Spectrom. 19, 790-798
18. Wolff, J. J., Laremore, T. N., Busch, A. M., Linhardt, R. J., and Amster, I. J. (2008) Electron detachment dissociation of dermatan sulfate oligosac-charides. J. Am. Soc. Mass. Spectrom. 19, 294-304
19. Wolff, J. J., Leach, F. E., 3rd, Laremore, T. N., Kaplan, D. A., Easterling, M. L., Linhardt, R. J., and Amster, I. J. (2010) Negative electron transfer dissociation of glycosaminoglycans. Anal. Chem. 82, 3460-3466
20. Leach, F. E., Wolff, J. J., Xiao, Z., Ly, M., Laremore, T. N., Arungundram, S., Al-Mafraji, K., Venot, A., Boons, G.-J., Linhardt, R. J., and Amster, I. J. (2011) Negative electron transfer dissociation Fourier transform mass spectrometry of glycosaminoglycan carbohydrates. Eur. J. Mass Spectrom. 17, 167-176
21. Leach, F. E., 3rd, Xiao, Z., Laremore, T. N., Linhardt, R. J., and Amster, I. J. (2011) Electron detachment dissociation and infrared multiphoton dissociation of heparin tetrasaccharides. Int. J. Mass Spectrom. 308, 253-259
22. Oh, H. B., Leach, F. E., 3rd, Arungundram, S., Al-Mafraji, K., Venot, A., Boons, G.-J., and Amster, I. J. (2011) Multivariate analysis of electron detachment dissociation and infrared multiphoton dissociation mass spectra of heparan sulfate tetrasaccharides differing only in hexuronic acid stereochemistry. J. Am. Soc. Mass. Spectrom. 22, 582-590
23. Zaia, J., McClellan, J. E., and Costello, C. E. (2001) Tandem mass spec- trometric determination of the 4S/6S sulfation sequence in chondroitin sulfate oligosaccharides. Anal. Chem. 73, 6030-6039
24. McClellan, J. E., Costello, C. E., O'Connor, P. B., and Zaia, J. (2002) Influence of charge state on product ion mass spectra and the determination of 4S/6S sulfation sequence of chondroitin sulfate oligosaccha-rides. Anal. Chem. 74, 3760-3771
25. Zaia, J., and Costello, C. E. (2003) Tandem mass spectrometry of sulfated heparin-like glycosaminoglycan oligosaccharides. Anal. Chem. 75, 2445-2455
26. Zaia, J., Li, X. Q., Chan, S. Y, and Costello, C. E. (2003) Tandem mass spectrometric strategies for determination of sulfation positions and uronic acid epimerization in chondroitin sulfate oligosaccharides. J. Am. Soc. Mass. Spectrom. 14, 1270-1281
27. Naggar, E. F., Costello, C. E., and Zaia, J. (2004) Competing fragmentation processes in tandem mass spectra of heparin-like glycosaminoglycans. J. Am. Soc. Mass. Spectrom. 15, 1534-1544
28. Miller, M. J., Costello, C. E., Malmström, A., and Zaia, J. (2006) A tandem mass spectrometric approach to determination of chondroitin/dermatan sulfate oligosaccharide glycoforms. Glycobiology 16, 502-513
29. Bielik, A. M., and Zaia, J. (2011) Multistage tandem mass spectrometry of chondroitin sulfate and dermatan sulfate. Int. J. Mass Spectrom. 305, 131-137
30. Saad, O. M., and Leary, J. A. (2004) Delineating mechanisms of dissociation for isomeric heparin disaccharides using isotope labeling and ion trap tandem mass spectrometry. J. Am. Soc. Mass. Spectrom. 15, 1274-1286
31. n with HOST: A heparin/HS oligosaccharide sequencing tool. Anal. Chem. 77, 5902-5911
32. Ly, M., Leach, F. E., 3rd, Laremore, T. N., Toida, T., Amster, I. J., and Linhardt, R. J. (2011) The proteoglycan bikunin has a defined sequence. Nat. Chem. Biol. 7, 827-833
33. Lohse, D. L., and Linhardt, R. J. (1992) Purification and characterization of heparin lyases from Flavobacterium heparinum. J. Biol. Chem. 267, 24347-24355
34. Conrad, H. E. (2001) Nitrous acid degradation of glycosaminoglycans. Curr. Protoc. Mol. Biol. 2001 May Chapter 17, Unit 17.22A
35. Takagaki, K., Kojima, K., Majima, M., Nakamura, T., Kato, I., and Endo, M. (1992) Ion-spray mass-spectrometric analysis of glycosaminoglycan oligosaccharides. Glycoconj. J. 9, 174-179
36. Jones, C. J., Beni, S., Limtiaco, J. F., Langeslay, D. J., and Larive, C. K. (2011) Heparin characterization: Challenges and solutions. Annu. Rev. Anal. Chem. 4, 439-465
37. Meissen, J. K., Sweeney, M. D., Girardi, M., Lawrence, R., Esko, J. D., and Leary, J. A. (2009) Differentiation of 3-O-sulfated heparin disaccharide isomers: Identification of structural aspects of the heparin CCL2-binding motif. J. Am. Soc. Mass. Spectrom. 20, 652-657
38. Orlando, R., Allen Bush, C., and Fenselau, C. (1990) Structural analysis of oligosaccharides by tandem mass spectrometry: Collisional activation of sodium adduct ions. Biol. Mass Spectrom. 19, 747-754
39. Staempfli, A., Zhou, Z., and Leary, J. A. (1992) Gas-phase dissociation mechanisms of dilithiated disaccharides: tandem mass spectrometry and semiempirical calculations. J. Org. Chem. 57, 3590-3594
40. Desaire, H., and Leary, J. A. (2001) The effects of coordination number and ligand size on the gas phase dissociation and stereochemical differentiation of cobalt-coordinated monosaccharides. Int. J. Mass Spectrom. 209, 171-184
41. n in a quadrupole ion trap. J. Am. Soc. Mass Spectrom. 10, 269-272
42. Harvey, D. (2001) Ionization and collision-induced fragmentation of N- linked and related carbohydrates using divalent cations. J. Am. Soc. Mass Spectrom. 12, 926-937
43. Zhou, Z., Ogden, S., and Leary, J. A. (1990) Linkage position determination in oligosaccharides: mass spectrometry (MS/MS) study of lithium-cationized carbohydrates. J. Org. Chem. 55, 5444-5446
44. Tissot, B., Gasiunas, N., Powell, A. K., Ahmed, Y., Zhi, Z.-L., Haslam, S. M., Morris, H. R., Turnbull, J. E., Gallagher, J. T., and Dell, A. (2007) Toward GAG glycomics: Analysis of highly sulfated heparins by MALDI-TOF mass spectrometry. Glycobiology 17, 972-982
45. Zhang, Z., and Linhardt, R. J. (2009) Sequence analysis of native oligosac- charides using negative ESI tandem MS. Curr. Anal. Chem. 5, 225-237
46. Kailemia, M. J., Li, L., Ly, M., Linhardt, R. J., and Amster, I. J. (2012) Complete mass spectral characterization of a synthetic ultralow-molecular-weight heparin using collision-induced dissociation. Anal. Chem. 84, 5475-5478
47. Xiao, Z., Zhao, W., Yang, B., Zhang, Z., Guan, H., and Linhardt, R. J. (2011) Heparinase 1 selectivity for the 3,6-di-O-sulfo-2-deoxy-2-sulfamido- α-D-glucopyranose(1,4)2-O-sulfo-α-L-idopyranosyluronic acid (GlcNS3S6S-IdoA2S) linkages. Glycobiology 21, 13-22
48. Liu, R., Xu, Y., Chen, M., Weïwer, M., Zhou, X., Bridges, A. S., DeAngelis, P. L., Zhang, Q., Linhardt, R. J., and Liu, J. (2010) Chemoenzymatic design of heparan sulfate oligosaccharides. J. Biol. Chem. 285, 34240-34249
49. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. (2008) GlycoWorkbench: A tool for the computer-assisted annotation of mass spectra of glycans. J. Proteome Res. 7, 1650-1659
50. Domon, B., and Costello, C. E. (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS MS spectra of glycoconjugates. Glycoconj. J. 5, 397-409
51. Hofmeister, G. E., Zhou, Z., and Leary, J. A. (1991) Linkage position determination in lithium-cationized disaccharides: tandem mass spectrometry and semiempirical calculations. J. Am. Chem. Soc. 113, 5964-5970
52. Spengler, B., Dolce, J. W., and Cotter, R. J. (1990) Infrared laser desorption mass spectrometry of oligosaccharides: fragmentation mechanisms and isomer analysis. Anal. Chem. 62, 1731-1737
53. Leymarie, N., and Zaia, J. (2012) Effective use of mass spectrometry for glycan and glycopeptide structural analysis. Anal. Chem. 84, 3040-3048