Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING

Guimond SE, Puvirajesinghe TM, Skidmore MA, Kalus I, Dierks T, Yates EA, Turnbull JE (2009)
JOURNAL OF BIOLOGICAL CHEMISTRY 284(38): 25714-25722.

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Studies on glycosaminoglycans and proteoglycans (PGs) have been hampered by difficulties in isolation and analysis by traditional methods that are laborious and lack sensitivity and throughput. Here we demonstrate a simple method for rapid isolation of proteoglycans (RIP) employing phenol/guanidine/chloroform reagent to purify heparan sulfate (HS) PGs quantitatively from various tissues and cells. We further show that this generic purification methodology, when applied in concert with a BODIPY (TM) fluorescent label, permits structural analyses on RIP-purified HS at similar to 1,000-fold higher sensitivity than standard UV detection methods and similar to 10-100-fold higher sensitivity than previous fluorescence detection methods. The utility of RIP-BODIPY methodology was demonstrated by rapid profiling of HS structural composition from small tissue samples, multiple mouse organs, and as little as a few thousand cultured cells. It was also used to generate novel insights into in vivo structural changes in HS from Sulf1 knock-out mice for the first time that differed significantly from previous observations limited to tissue culture experiments. RIP was also applied to purify HS for bioassay testing, exemplified by cell assays of fibroblast growth factor signaling activation; this generated data from 2-O-sulfotransferase knock-out mice and revealed an unexpected deficiency in fibroblast growth factor activation by HS from heterozygous mice. These data demonstrate that RIP will underpin emerging efforts to develop glycomics profiling strategies for HS and other glycosaminoglycans to explore their structure-function relationships in complex biological systems.
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Guimond SE, Puvirajesinghe TM, Skidmore MA, et al. Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING. JOURNAL OF BIOLOGICAL CHEMISTRY. 2009;284(38):25714-25722.
Guimond, S. E., Puvirajesinghe, T. M., Skidmore, M. A., Kalus, I., Dierks, T., Yates, E. A., & Turnbull, J. E. (2009). Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING. JOURNAL OF BIOLOGICAL CHEMISTRY, 284(38), 25714-25722. doi:10.1074/jbc.M109.032755
Guimond, S. E., Puvirajesinghe, T. M., Skidmore, M. A., Kalus, I., Dierks, T., Yates, E. A., and Turnbull, J. E. (2009). Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING. JOURNAL OF BIOLOGICAL CHEMISTRY 284, 25714-25722.
Guimond, S.E., et al., 2009. Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING. JOURNAL OF BIOLOGICAL CHEMISTRY, 284(38), p 25714-25722.
S.E. Guimond, et al., “Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING”, JOURNAL OF BIOLOGICAL CHEMISTRY, vol. 284, 2009, pp. 25714-25722.
Guimond, S.E., Puvirajesinghe, T.M., Skidmore, M.A., Kalus, I., Dierks, T., Yates, E.A., Turnbull, J.E.: Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING. JOURNAL OF BIOLOGICAL CHEMISTRY. 284, 25714-25722 (2009).
Guimond, Scott E., Puvirajesinghe, Tania M., Skidmore, Mark A., Kalus, Ina, Dierks, Thomas, Yates, Edwin A., and Turnbull, Jeremy E. “Rapid Purification and High Sensitivity Analysis of Heparan Sulfate from Cells and Tissues TOWARD GLYCOMICS PROFILING”. JOURNAL OF BIOLOGICAL CHEMISTRY 284.38 (2009): 25714-25722.
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19 Citations in Europe PMC

Data provided by Europe PubMed Central.

Sulf1 and Sulf2 Differentially Modulate Heparan Sulfate Proteoglycan Sulfation during Postnatal Cerebellum Development: Evidence for Neuroprotective and Neurite Outgrowth Promoting Functions.
Kalus I, Rohn S, Puvirajesinghe TM, Guimond SE, Eyckerman-Kolln PJ, Ten Dam G, van Kuppevelt TH, Turnbull JE, Dierks T., PLoS ONE 10(10), 2015
PMID: 26448642
2-O Heparan Sulfate Sulfation by Hs2st Is Required for Erk/Mapk Signalling Activation at the Mid-Gestational Mouse Telencephalic Midline.
Chan WK, Howe K, Clegg JM, Guimond SE, Price DJ, Turnbull JE, Pratt T., PLoS ONE 10(6), 2015
PMID: 26075383
Discovery of a heparan sulfate 3-O-sulfation specific peeling reaction.
Huang Y, Mao Y, Zong C, Lin C, Boons GJ, Zaia J., Anal. Chem. 87(1), 2015
PMID: 25486437
The role of heparan sulfate as determining pathogenic factor in complement factor H-associated diseases.
Loeven MA, Rops AL, Berden JH, Daha MR, Rabelink TJ, van der Vlag J., Mol. Immunol. 63(2), 2015
PMID: 25246018
Recent advances in cellular glycomic analyses.
Furukawa J, Fujitani N, Shinohara Y., Biomolecules 3(1), 2013
PMID: 24970165
Mass spectral profiling of glycosaminoglycans from histological tissue surfaces.
Shao C, Shi X, Phillips JJ, Zaia J., Anal. Chem. 85(22), 2013
PMID: 24099043
New targets for glycosaminoglycans and glycosaminoglycans as novel targets.
Gesslbauer B, Theuer M, Schweiger D, Adage T, Kungl AJ., Expert Rev Proteomics 10(1), 2013
PMID: 23414361
Cell-Based Microscale Isolation of Glycoaminoglycans for Glycomics Study.
Zhao X, Yang B, Datta P, Gasmili L, Zhang F, Linhardt RJ., J Carbohydr Chem 31(4-6), 2012
PMID: 24068855
Heparin and heparan sulfate: analyzing structure and microheterogeneity.
Shriver Z, Capila I, Venkataraman G, Sasisekharan R., Handb Exp Pharmacol (207), 2012
PMID: 22566225
Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry.
Yang B, Chang Y, Weyers AM, Sterner E, Linhardt RJ., J Chromatogr A 1225(), 2012
PMID: 22236563
Analysis of Glycosaminoglycans Using Mass Spectrometry.
Staples GO, Zaia J., Curr Proteomics 8(4), 2011
PMID: 25705143
Genetic analysis of the heparan modification network in Caenorhabditis elegans.
Townley RA, Bulow HE., J. Biol. Chem. 286(19), 2011
PMID: 21454666
Glycosaminoglycan characterization by electrospray ionization mass spectrometry including fourier transform mass spectrometry.
Laremore TN, Leach FE 3rd, Solakyildirim K, Amster IJ, Linhardt RJ., Meth. Enzymol. 478(), 2010
PMID: 20816475
Proteoglycomics: recent progress and future challenges.
Ly M, Laremore TN, Linhardt RJ., OMICS 14(4), 2010
PMID: 20450439
Generating heparan sulfate saccharide libraries for glycomics applications.
Powell AK, Ahmed YA, Yates EA, Turnbull JE., Nat Protoc 5(5), 2010
PMID: 20379137

39 References

Data provided by Europe PubMed Central.

Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development.
Brickman YG, Ford MD, Gallagher JT, Nurcombe V, Bartlett PF, Turnbull JE., J. Biol. Chem. 273(8), 1998
PMID: 9468484
Structural comparison of fibroblast growth factor-specific heparan sulfates derived from a growing or differentiating neuroepithelial cell line.
Brickman YG, Nurcombe V, Ford MD, Gallagher JT, Bartlett PF, Turnbull JE., Glycobiology 8(5), 1998
PMID: 9597544
Variant heparan sulfates synthesized in developing mouse brain differentially regulate FGF signaling.
Ford-Perriss M, Guimond SE, Greferath U, Kita M, Grobe K, Habuchi H, Kimata K, Esko JD, Murphy M, Turnbull JE., Glycobiology 12(11), 2002
PMID: 12460940
The molecular phenotype of heparan sulfate in the Hs2st-/- mutant mouse.
Merry CL, Bullock SL, Swan DC, Backen AC, Lyon M, Beddington RS, Wilson VA, Gallagher JT., J. Biol. Chem. 276(38), 2001
PMID: 11457822
Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4.
Guimond S, Maccarana M, Olwin BB, Lindahl U, Rapraeger AC., J. Biol. Chem. 268(32), 1993
PMID: 7693696
A strategy for rapid sequencing of heparan sulfate and heparin saccharides.
Turnbull JE, Hopwood JJ, Gallagher JT., Proc. Natl. Acad. Sci. U.S.A. 96(6), 1999
PMID: 10077574
Laser-induced fluorescence as a powerful detection tool for capillary electrophoretic analysis of heparin/heparan sulfate disaccharides.
Militsopoulou M, Lecomte C, Bayle C, Couderc F, Karamanos NK., Biomed. Chromatogr. 17(1), 2003
PMID: 12583004
Glycomics approach to structure-function relationships of glycosaminoglycans.
Sasisekharan R, Raman R, Prabhakar V., Annu Rev Biomed Eng 8(), 2006
PMID: 16834555
Emerging glycomics technologies.
Turnbull JE, Field RA., Nat. Chem. Biol. 3(2), 2007
PMID: 17235338
A chip-based amide-HILIC LC/MS platform for glycosaminoglycan glycomics profiling.
Staples GO, Bowman MJ, Costello CE, Hitchcock AM, Lau JM, Leymarie N, Miller C, Naimy H, Shi X, Zaia J., Proteomics 9(3), 2009
PMID: 19137549
Preparation of unsaturated disaccharides by eliminative cleavage of heparin and heparan sulfate with heparitinases.
Kariya Y, Yoshida K, Morikawa K, Tawada A, Miyazono H, Kikuchi H, Tokuyasu K., Comp. Biochem. Physiol., B 103(2), 1992
PMID: 1424575

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