Ultra-performance ion-pairing liquid chromatography with on-line electrospray ion trap mass spectrometry for heparin disaccharide analysis

Analytical Biochemistry

Volumn 415, Issue 1, 2011, Pages 59-66

  Yang, Bo ^a   Weyers, Amanda ^a   Baik, Jong Youn ^a,b   Sterner, Eric ^c   Sharfstein, Susan ^b   Mousa, Shaker A ^d   Zhang, Fuming ^c   Dordick, Jonathan S ^c   Linhardt, Robert J ^a,c,e  

^a Research Rensselaer Polytechnic Institute   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^d ALBANY COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

^e RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Biological samples; Disaccharide analysis; Heparan sulfate; Heparin; Heparin lyase; Mass spectrometry; Ultra performance liquid chromatography

Indexed keywords

ELECTROSPRAY IONIZATION; IONS; LIQUIDS; MASS SPECTROMETRY; POLYSACCHARIDES; PROTEINS; SULFUR COMPOUNDS;

BIOLOGICAL SAMPLES; DISACCHARIDE ANALYSIS; HEPARAN SULFATES; HEPARIN; HEPARIN LYASE; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

HIGH PRESSURE LIQUID CHROMATOGRAPHY;

HEPARAN SULFATE; HEPARIN LYASE; LOW MOLECULAR WEIGHT HEPARIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY FLUID; CARBOHYDRATE ANALYSIS; CHEMICAL STRUCTURE; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; ION PAIR CHROMATOGRAPHY; ION TRAP MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

EID: 79957686119     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2011.04.003     Document Type: Article

References (51)

1. U. Hacker, K. Nybakken, N. Perrimon, Heparan sulphate proteoglycans: the sweet side of development, Nat. Rev. Mol. Cell Biol. 6 (2005) 530-541. (Pubitemid 40943044)
2. S. Tumova, A. Woods, J.R. Couchman, Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions, Int. J. Biochem. Cell Biol. 32 (2000) 269-288. (Pubitemid 30069970)
3. M. Petitou, J.P. Herault, A. Bernat, P.A. Driguez, P. Duchaussoy, J.C. Lormeau, J.M. Herbert, Synthesis of thrombin-inhibiting heparin mimetics without side effects, Nature 398 (1999) 417-422. (Pubitemid 29180373)
4. L. Wang, M. Fuster, P. Sriramarao, J.D. Esko, Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses, Nat. Immunol. 6 (2005) 902-910.
5. I. Capila, R.J. Linhardt, Heparin-protein interactions, Angew. Chem. Int. Ed. Engl. 41 (2002) 391-412.
6. L. Muszbek, Z. Bereczky, B. Kovacs, I. Komaromi, Antithrombin deficiency and its laboratory diagnosis, Clin. Chem. Lab. Med. 48 (2010) S67-S78 (review).
7. M. Guerrini, D. Beccati, Z. Shriver, A. Naggi, K. Viswanathan, A. Bisio, I. Capila, J.C. Lansing, S. Guglieri, B. Fraser, A. Al-Hakim, N.S. Gunay, Z. Zhang, L. Robinson, L. Buhse, M. Nasr, J. Woodcock, R. Langer, G. Venkataraman, R.J. Linhardt, B. Casu, G. Torri, R. Sasisekharan, Oversulfated chondroitin sulfate is a contaminant in heparin associated with adverse clinical events, Nat. Biotechnol. 26 (2008) 669-675.
8. A.M. Brustkern, L.F. Buhse, M. Nasr, A. Al-Hakim, D.A. Keire, Characterization of currently marketed heparin products: reversed-phase ion-pairing liquid chromatography mass spectrometry of heparin digests, Anal. Chem. 82 (2010) 9865-9870.
9. A.K. Korir, J.F. Limtiaco, S.M. Gutierrez, C.K. Larive, Ultraperformance ion-pair liquid chromatography coupled to electrospray time-of-flight mass spectrometry for compositional profiling and quantification of heparin and heparan sulfate, Anal. Chem. 80 (2008) 1297-1306.
10. 1H-NMR and PAGE, J. Pharm. Sci. 98 (2009) 4017-4026.
11. M. Bernfield, M. Gotte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, M. Zako, Functions of cell surface heparan sulfate proteoglycans, Annu. Rev. Biochem. 68 (1999) 729-777. (Pubitemid 29449208)
12. J.G. Martin, M. Gupta, Y. Xu, S. Akella, J. Liu, J.S. Dordick, R.J. Linhardt, Toward an artificial Golgi: redesigning the biological activities of heparan sulfate on a digital microfluidic chip, J. Am. Chem. Soc. 131 (2009) 11041-11048.
13. D.L. Rabenstein, Heparin and heparan sulfate: structure and function, Nat. Prod. Rep. 19 (2002) 312-331. (Pubitemid 34656777)
14. K.A. Jandik, D. Kruep, M. Cartier, R.J. Linhardt, Accelerated stability studies of heparin, J. Pharm. Sci. 85 (1996) 45-51.
15. D.M. Cohen, R.J. Linhardt, Randomness in the heparin polymer: computer simulations of alternative action patterns of heparin lyase, Biopolymers 30 (1990) 733-741.
16. Z. Xiao, B.R. Tappen, M. Ly, W. Zhao, L.P. Canova, H. Guan, R.J. Linhardt, Heparin mapping using heparin lyases and the generation of a novel low molecular weight heparin, J. Med. Chem. 54 (2011) 603-610.
17. K.G. Rice, Y.S. Kim, A.C. Grant, Z.M. Merchant, R.J. Linhardt, High-performance liquid chromatographic separation of heparin-derived oligosaccharides, Anal. Biochem. 150 (1985) 325-331.
18. S. Yamada, K. Sakamoto, H. Tsuda, K. Yoshida, M. Sugiura, K. Sugahara, Structural studies of octasaccharides derived from the low-sulfated repeating disaccharide region and octasaccharide serines derived from the protein linkage region of porcine intestinal heparin, Biochemistry 38 (1999) 838-847.
19. W.L. Chuang, H. McAllister, L. Rabenstein, Chromatographic methods for product-profile analysis and isolation of oligosaccharides produced by heparinase-catalyzed depolymerization of heparin, J. Chromatogr. A 932 (2001) 65-74. (Pubitemid 32938187)
20. R.E. Hileman, A.E. Smith, T. Toida, R.J. Linhardt, Preparation and structure of heparin lyase-derived heparan sulfate oligosaccharides, Glycobiology 7 (1997) 231-239. (Pubitemid 27168778)
21. A. Pervin, C. Gallo, K.A. Jandik, X.J. Han, R.J. Linhardt, Preparation and structural characterization of large heparin-derived oligosaccharides, Glycobiology 5 (1995) 83-95.
22. N. Volpi, F. Maccari, R.J. Linhardt, Quantitative capillary electrophoresis determination of oversulfated chondroitin sulfate as a contaminant in heparin preparations, Anal. Biochem. 388 (2009) 140-145.
23. a, and electrophoretic mobility measurements, Anal. Chem. 81 (2009) 7406-7415.
24. 1H NMR spectroscopy, J. Pharm. Biomed. Anal. 49 (2009) 1060-1064.
25. 1H NMR spectroscopy of tetra-, hexa-, and octa-saccharides of porcine intestinal heparin, Carbohydr. Res. 269 (1995) 139-156.
26. W. Chai, J. Luo, C.K. Lim, A.M. Lawson, Characterization of heparin oligosaccharide mixtures as ammonium salts using electrospray mass spectrometry, Anal. Chem. 70 (1998) 2060-2066.
27. J. Zaia, C.E. Costello, Compositional analysis of glycosaminoglycans by electrospray mass spectrometry, Anal. Chem. 73 (2001) 233-239.
28. C. Thanawiroon, K.G. Rice, T. Toida, R.J. Linhardt, Liquid chromatography/mass spectrometry sequencing approach for highly sulfated heparin-derived oligosaccharides, J. Biol. Chem. 279 (2004) 2608-2615.
29. Z. Zhang, J. Xie, H. Liu, J. Liu, R.J. Linhardt, Quantification of heparan sulfate disaccharides using ion-pairing reversed-phase microflow high-performance liquid chromatography with electrospray ionization trap mass spectrometry, Anal. Chem. 81 (2009) 4349-4355.
30. B. Kuberan, M. Lech, L. Zhang, Z.L. Wu, D.L. Beeler, R.D. Rosenberg, 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. 124 (2002) 8707-8718. (Pubitemid 34791042)
31. N. Volpi, R.J. Linhardt, High-performance liquid chromatography-mass spectrometry for mapping and sequencing glycosaminoglycan-derived oligosaccharides, Nat. Protoc. 5 (2010) 993-1004.
32. M.E. Swartz, UPLC: an introduction and review, J. Liq. Chromatogr. Related Technol. 28 (2005) 1253-1263.
33. J.E. MacNair, K.C. Lewis, J.W. Jorgenson, Ultra-high-pressure reversed-phase liquid chromatography in packed capillary columns, Anal. Chem. 69 (1997) 983-989.
34. C.J. Jones, N. Membreno, C.K. Larive, Insights into the mechanism of separation of heparin and heparan sulfate disaccharides by reverse-phase ion-pair chromatography, J. Chromatogr. A 1217 (2010) 479-488.
35. E. Yoshida, S. Arakawa, T. Matsunaga, S. Toriumi, S. Tokuyama, K. Morikawa, Y. Tahara, Cloning, sequencing, and expression of the gene from Bacillus circulans that codes for a heparinase that degrades both heparin and heparan sulfate, Biosci. Biotechnol. Biochem. 66 (2002) 1873-1879.
36. D. Shaya, A. Tocilj, Y. Li, J. Myette, G. Venkataraman, R. Sasisekharan, M. Cygler, Crystal structure of heparinase II from Pedobacter heparinus and its complex with a disaccharide product, J. Biol. Chem. 281 (2006) 15525-15535.
37. R. Godavarti, M. Davis, G. Venkataraman, C. Cooney, R. Langer, R. Sasisekharan, Heparinase III from Flavobacterium heparinum: cloning and recombinant expression in Escherichia coli, Biochem. Biophys. Res. Commun. 225 (1996) 751-758. (Pubitemid 26319178)
38. B. Li, P.W. Ryan, B.H. Ray, K.J. Leister, N.M. Sirimuthu, A.G. Ryder, Rapid characterization and quality control of complex cell culture media solutions using Raman spectroscopy and chemometrics, Biotechnol. Bioeng. 107 (2010) 290-301.
39. F. Zhang, P. Sun, E. Munoz, L. Chi, S. Sakai, T. Toida, H. Zhang, S. Mousa, R.J. Linhardt, Microscale isolation and analysis of heparin from plasma using an anion-exchange spin column, Anal. Biochem. 353 (2006) 284-286.
40. B. Li, H. Liu, Z. Zhang, H.E. Stansfield, J.S. Dordick, R.J. Linhardt, Analysis of glycosaminoglycans in stem cell glycomics, Methods Mol. Biol. 690 (2011) 285-300.
41. T. Cecchi, P. Passamonti, Retention mechanism for ion-pair chromatography with chaotropic reagents, J. Chromatogr. A 1216 (2009) 1789-1797.
42. T. Cecchi, F. Pucciarelli, P. Passamonti, Extended thermodynamic approach to ion interaction chromatography, Anal. Chem. 73 (2001) 2632-2639.
43. K. Solakyildirim, Z. Zhang, R.J. Linhardt, Ultra-performance liquid chromatography with electrospray ionization ion trap mass spectrometry for chondroitin disaccharide analysis, Anal. Biochem. 397 (2010) 24-28.
44. S.A. Wren, P. Tchelitcheff, UPLC/MS for the identification of beta-blockers, J. Pharm. Biomed. Anal. 40 (2006) 571-580.
45. R.J. Linhardt, Heparin: structure and activity [2003 Claude S. Hudson Award address in carbohydrate chemistry], J. Med. Chem. 46 (2003) 2551-2564.
46. S. Yamada, H. Morimoto, T. Fujisawa, K. Sugahara, Glycosaminoglycans in Hydra magnipapillata (Hydrozoa, Cnidaria): demonstration of chondroitin in the developing nematocyst, the sting organelle, and structural characterization of glycosaminoglycans, Glycobiology 17 (2007) 886-894.
47. J.A. Deakin, M. Lyon, A simplified and sensitive fluorescent method for disaccharide analysis of both heparan sulfate and chondroitin/dermatan sulfates from biological samples, Glycobiology 18 (2008) 483-491. (Pubitemid 351753552)
48. R. Lawrence, S.K. Olson, R.E. Steele, L. Wang, R. Warrior, R.D. Cummings, J.D. Esko, Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling, J. Biol. Chem. 283 (2008) 33674-33684.
49. K. Cuellar, H. Chuong, S.M. Hubbell, M.E. Hinsdale, Biosynthesis of chondroitin and heparan sulfate in Chinese hamster ovary cells depends on xylosyltransferase II, J. Biol. Chem. 282 (2007) 5195-5200.
50. D.R. Garud, V.M. Tran, X.V. Victor, M. Koketsu, B. Kuberan, Inhibition of heparan sulfate and chondroitin sulfate proteoglycan biosynthesis, J. Biol. Chem. 283 (2008) 28881-28887.
51. M. Warda, E.M. Gouda, T. Toida, L. Chi, R.J. Linhardt, Isolation and characterization of raw heparin from dromedary intestine: evaluation of a new source of pharmaceutical heparin, Comp. Biochem. Physiol. C 136 (2003) 357-365. (Pubitemid 38167573)