Fluorescent-tagged heparan sulfate precursor oligosaccharides to probe the enzymatic action of heparitinase I

Analytical Biochemistry

Volumn 396, Issue 1, 2010, Pages 124-132

  Babu, Ponnusamy ^a   Kuberan, Balagurunathan ^a,b,c  

^a UNIVERSITY OF UTAH   (United States)

^b Department of Electrical and Computer Engineering   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

AMAC labeling; Heparan sulfate; Heparitinase; Heparosan oligosaccharides; Mass spectrometry

Indexed keywords

ELECTROPHORESIS; ENZYMES; FLUORESCENCE; MASS SPECTROMETRY; SULFUR COMPOUNDS;

2-AMINOACRIDONE; ENZYMATIC ACTION; HEPARAN SULFATES; HEPARITINASE; MECHANISM OF ACTION; QUANTITATIVE METHODOLOGY; ROBUST STRATEGY; STRUCTURAL INFORMATION;

OLIGOSACCHARIDES;

GLYCOSAMINOGLYCAN POLYSULFATE; HEPARAN SULFATE; HEPARITINASE I; LYASE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SUBSTRATE; FLUORESCENCE; MASS SPECTROMETRY; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS;

EID: 70449687903     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2009.08.036     Document Type: Article

References (33)

1. Esko J.D., and Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71 (2002) 435-471
2. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., and Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68 (1999) 729-777
3. Korn E.D., and Payza A.N. The degradation of heparin by bacterial enzymes. II. Acetone powder extracts. J. Biol. Chem. 223 (1956) 859-864
4. Linker A., and Hovingh P. The enzymatic degradation of heparin and heparitin sulfate. I. The fractionation of a crude heparinase from flavobacteria. J. Biol. Chem. 240 (1965) 3724-3728
5. Linker A., and Hovingh P. The enzymatic degradation of heparitin sulfate. II. Isolation and characterization of non-sulfated oligosaccharides. Biochim. Biophys. Acta 165 (1968) 89-96
6. Hovingh P., and Linker A. The enzymatic degradation of heparin and heparitin sulfate. III. Purification of a heparitinase and a heparinase from flavobacteria. J. Biol. Chem. 245 (1970) 6170-6175
7. Yang V.C., Linhardt R.J., Bernstein H., Cooney C.L., and Langer R. Purification and characterization of heparinase from Flavobacterium heparinum. J. Biol. Chem. 260 (1985) 1849-1857
8. 13C NMR spectroscopy. J. Biol. Chem. 265 (1990) 16807-16813
9. Lohse D.L., and Linhardt R.J. Purification and characterization of heparin lyases from Flavobacterium heparinum. J. Biol. Chem. 267 (1992) 24347-24355
10. Sasisekharan R., Bulmer M., Moremen K.W., Cooney C.L., and Langer R. Cloning and expression of heparinase I gene from Flavobacterium heparinum. Proc. Natl. Acad. Sci. USA 90 (1993) 3660-3664
11. Godavarti R., Davis M., Venkataraman G., Cooney C., Langer R., and Sasisekharan R. Heparinase III from Flavobacterium heparinum: cloning and recombinant expression in Escherichia coli. Biochem. Biophys. Res. Commun. 225 (1996) 751-758
12. Rosenberg R.D., and Lam L. Correlation between structure and function of heparin. Proc. Natl. Acad. Sci. USA 76 (1979) 1218-1222
13. Lindahl U., Backstrom G., Hook M., Thunberg L., Fransson L.A., and Linker A. Structure of the antithrombin-binding site in heparin. Proc. Natl. Acad. Sci. USA 76 (1979) 3198-3202
14. Linhardt R.J., Turnbull J.E., Wang H.M., Loganathan D., and Gallagher J.T. Examination of the substrate specificity of heparin and heparan sulfate lyases. Biochemistry 29 (1990) 2611-2617
15. Desai U.R., Wang H.M., and Linhardt R.J. Specificity studies on the heparin lyases from Flavobacterium heparinum. Biochemistry 32 (1993) 8140-8145
16. Wei Z., Lyon M., and Gallagher J.T. Distinct substrate specificities of bacterial heparinases against N-unsubstituted glucosamine residues in heparan sulfate. J. Biol. Chem. 280 (2005) 15742-15748
17. Lauer M.E., Hascall V.C., and Wang A. Heparan sulfate analysis from diabetic rat glomeruli. J. Biol. Chem. 282 (2007) 843-852
18. Linhardt R.J., Fitzgerald G.L., Cooney C.L., and Langer R. Mode of action of heparin lyase on heparin. Biochim. Biophys. Acta 702 (1982) 197-203
19. Rhomberg A.J., Ernst S., Sasisekharan R., and Biemann K. Mass spectrometric and capillary electrophoretic investigation of the enzymatic degradation of heparin-like glycosaminoglycans. Proc. Natl. Acad. Sci. USA 95 (1998) 4176-4181
20. Rhomberg A.J., Shriver Z., Biemann K., and Sasisekharan R. Mass spectrometric evidence for the enzymatic mechanism of the depolymerization of heparin-like glycosaminoglycans by heparinase II. Proc. Natl. Acad. Sci. USA 95 (1998) 12232-12237
21. Jandik K.A., Gu K., and Linhardt R.J. Action pattern of polysaccharide lyases on glycosaminoglycans. Glycobiology 4 (1994) 289-296
22. Tissot B., Ceroni A., Powell A.K., Morris H.R., Yates E.A., Turnbull J.E., Gallagher J.T., Dell A., and Haslam S.M. Software tool for the structural determination of glycosaminoglycans by mass spectrometry. Anal. Chem. 80 (2008) 9204-9212
23. Shi X., and Zaia J. Organ-specific heparan sulfate structural phenotypes. J. Biol. Chem. 284 (2009) 11806-11814
24. Zhang Z., Xie J., Liu H., Liu J., and Linhardt R.J. 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
25. Korir A.K., Limtiaco J.F., Gutierrez S.M., and Larive C.K. 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
26. Meissen J.K., Sweeney M.D., Girardi M., Lawrence R., Esko J.D., and Leary J.A. Differentiation of 3-O-sulfated heparin disaccharide isomers: identification of structural aspects of the heparin CCL2 binding motif. J. Am. Soc. Mass Spectrom. 20 (2009) 652-657
27. Kuberan B., Lech M., Zhang L., Wu Z.L., Beeler D.L., and 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. 124 (2002) 8707-8718
28. Lyon M., Deakin J.A., Lietha D., Gherardi E., and Gallagher J.T. The interactions of hepatocyte growth factor/scatter factor and its NK1 and NK2 variants with glycosaminoglycans using a modified gel mobility shift assay: elucidation of the minimal size of binding and activatory oligosaccharides. J. Biol. Chem. 279 (2004) 43560-43567
29. Ambrosius M., Kleesiek K., and Gotting C. Quantitative determination and comparison of the glycosaminoglycan Δ-disaccharide composition in 22 different human cell lines. Cell Biol. Int. 33 (2009) 848-852
30. Turnbull J.E., Fernig D.G., Ke Y., Wilkinson M.C., and Gallagher J.T. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267 (1992) 10337-10341
31. Sasisekharan R., Moses M.A., Nugent M.A., Cooney C.L., and Langer R. Heparinase inhibits neovascularization. Proc. Natl. Acad. Sci. USA 91 (1994) 1524-1528
32. Deakin J.A., and Lyon M. 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
33. Charlwood J., Birrell H., Organ A., and Camilleri P. A chromatographic and mass spectrometric strategy for the analysis of oligosaccharides: determination of the glycan structures in porcine thyroglobulin. Rapid Commun. Mass Spectrom. 13 (1999) 716-723