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BioMed Research International
Volume 2014, Article ID 986594, 8 pages
http://dx.doi.org/10.1155/2014/986594
Research Article

Improvement of the Digestibility of Sulfated Hyaluronans by Bovine Testicular Hyaluronidase: A UV Spectroscopic and Mass Spectrometric Study

1Institute of Medical Physics and Biophysics, Medical Faculty, University of Leipzig, Härtelstraße 16-18, 04107 Leipzig, Germany
2INNOVENT e. V., Biomaterials Department, Pruessingstraße 27B, 07745 Jena, Germany

Received 27 January 2014; Accepted 24 April 2014; Published 27 May 2014

Academic Editor: Daniel Huster

Copyright © 2014 Katharina Lemmnitzer et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Schiller and D. Huster, “New methods to study the composition and structure of the extracellular matrix in natural and bioengineered tissues,” Biomatter, vol. 2, no. 3, pp. 115–131, 2012. View at Google Scholar
  2. B. Fuchs and J. Schiller, “Glycosaminoglycan degradation by selected reactive oxygen species,” Antioxidants and Redox Signaling, 2014. View at Publisher · View at Google Scholar
  3. K. E. Benders, P. R. van Weeren, S. F. Badylak et al., “Extracellular matrix scaffolds for cartilage and bone regeneration,” Trends in Biotechnology, vol. 31, no. 3, pp. 169–176, 2013. View at Google Scholar
  4. C. I. Gama and L. C. Hsieh-Wilson, “Chemical approaches to deciphering the glycosaminoglycan code,” Current Opinion in Chemical Biology, vol. 9, no. 6, pp. 609–619, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Schnabelrauch, D. Scharnweber, and J. Schiller, “Sulfated glycosaminoglycans as promising artificial extracellular matrix components to improve the regeneration of tissues,” Current Medicinal Chemistry, vol. 20, no. 20, pp. 2501–2523, 2013. View at Google Scholar
  6. H. Liu, Z. Zhang, and R. J. Linhardt, “Lessons learned from the contamination of heparin,” Natural Product Reports, vol. 26, no. 3, pp. 313–321, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Schiller, J. Becher, S. Möller, K. Nimptsch, T. Riemer, and M. Schnabelrauch, “Synthesis and characterization of chemically modified hyaluronan and chondroitin sulfate,” Mini-Reviews in Organic Chemistry, vol. 7, no. 4, pp. 290–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Hao, X. Ma, S. Fang et al., “Positive and negative-ion matrix-assisted laser desorption/ionization mass spectrometry of saccharides,” Rapid Communications in Mass Spectrometry, vol. 12, no. 7, pp. 345–348, 1998. View at Google Scholar
  9. A. Nimptsch, S. Schibur, M. Schnabelrauch, B. Fuchs, D. Huster, and J. Schiller, “Characterization of the quantitative relationship between signal-to-noise (S/N) ratio and sample amount on-target by MALDI-TOF MS: determination of chondroitin sulfate subsequent to enzymatic digestion,” Analytica Chimica Acta, vol. 635, no. 2, pp. 175–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Schiller, J. Arnhold, S. Benard, S. Reichl, and K. Arnold, “Cartilage degradation by hyaluronate lyase and chondroitin ABC lyase: a MALDI-TOF mass spectrometric study,” Carbohydrate Research, vol. 318, no. 1–4, pp. 116–122, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. I. Kakizaki, N. Ibori, K. Kojima, M. Yamaguchi, and M. Endo, “Mechanism for the hydrolysis of hyaluronan oligosaccharides by bovine testicular hyaluronidase,” FEBS Journal, vol. 277, no. 7, pp. 1776–1786, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Pichert, S. A. Samsonov, S. Theisgen et al., “Characterization of the interaction of interleukin-8 with hyaluronan, chondroitin sulfate, dermatan sulfate and their sulfated derivatives by spectroscopy and molecular modeling,” Glycobiology, vol. 22, no. 1, pp. 134–145, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Termeer, J. P. Sleeman, and J. C. Simon, “Hyaluronan—magic glue for the regulation of the immune response?” Trends in Immunology, vol. 24, no. 3, pp. 112–114, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Toida, Y. Ogita, A. Suzuki, H. Toyoda, and T. Imanari, “Inhibition of hyaluronidase by fully O-sulfonated glycosaminoglycans,” Archives of Biochemistry and Biophysics, vol. 370, no. 2, pp. 176–182, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. D. J. Langeslay, C. J. Jones, S. Beni, and C. K. Larive, “Glycosaminoglycans: oligosaccharide analysis by liquid chromatography, capillary electrophoresis, and specific labeling,” Methods in Molecular Biology, vol. 836, pp. 131–144, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. V. Hintze, S. Moeller, M. Schnabelrauch et al., “Modifications of hyaluronan influence the interaction with human bone morphogenetic protein-4 (hBMP-4),” Biomacromolecules, vol. 10, no. 12, pp. 3290–3297, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. J. L. Reissig, J. L. Storminge, and L. F. Leloir, “A modified colorimetric method for the estimation of N-acetylamino sugars,” The Journal of Biological Chemistry, vol. 217, no. 2, pp. 959–966, 1955. View at Google Scholar · View at Scopus
  18. I. Muckenschnabel, G. Bernhardt, T. Spruss, B. Dietl, and A. Buschauer, “Quantitation of hyaluronidases by the Morgan-Elson reaction: comparison of the enzyme activities in the plasma of tumor patients and healthy volunteers,” Cancer Letters, vol. 131, no. 1, pp. 13–20, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Asteriou, B. Deschrevel, B. Delpech et al., “An improved assay for the N-acetyl-D-glucosamine reducing ends of polysaccharides in the presence of proteins,” Analytical Biochemistry, vol. 293, no. 1, pp. 53–59, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Nagaraju, K. S. Girish, Y. Pan, K. A. Easely, and K. Kemparaju, “Estimation of serum hyaluronidase activity overcoming the turbidity interference,” Clinical Laboratory Science, vol. 24, no. 3, pp. 172–177, 2011. View at Google Scholar · View at Scopus
  21. P. B. O'Connor, K. Dreisewerd, K. Strupat, and F. Hillenkamp, “MALDI mass spectrometry instrumentation,” in MALDI MS—A Practical Guide to Instrumentation, Methods, and Applications, F. Hillenkamp and J. Peter-Katalinic, Eds., pp. 41–104, Wiley-VCH, Weinheim, Germany, 2nd edition, 2013. View at Google Scholar
  22. K. Busse, M. Averbeck, U. Anderegg, K. Arnold, J. C. Simon, and J. Schiller, “The signal-to-noise ratio as a measure of HA oligomer concentration: a MALDI-TOF MS study,” Carbohydrate Research, vol. 341, no. 8, pp. 1065–1070, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Sun, K. Yang, Z. Zhao, S. Guan, X. Han, and R. W. Gross, “Matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis of cellular glycerophospholipids enabled by multiplexed solvent dependent analyte-matrix interactions,” Analytical Chemistry, vol. 80, no. 19, pp. 7576–7585, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Nimptsch, R. Süß, M. Schnabelrauch, A. Nimptsch, and J. Schiller, “Positive ion MALDI-TOF mass spectra are more suitable than negative ion spectra to characterize sulphated glycosaminoglycan oligosaccharides,” International Journal of Mass Spectrometry, vol. 310, pp. 72–76, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Volpi, J. Schiller, R. Stern, and L. Šoltés, “Role, metabolism, chemical modifications and applications of hyaluronan,” Current Medicinal Chemistry, vol. 16, no. 14, pp. 1718–1745, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Stern, G. Kogan, M. J. Jedrzejas, and L. Šoltés, “The many ways to cleave hyaluronan,” Biotechnology Advances, vol. 25, no. 6, pp. 537–557, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. “Enzyme Nomenclature,” Academic Press, San Diego, Calif, USA, 1992, http://www.chem.qmul.ac.uk/iubmb/enzyme.
  28. E. Sisu, C. Flangea, A. Serb, and A. D. Zamfir, “Modern developments in mass spectrometry of chondroitin and dermatan sulfate glycosaminoglycans,” Amino Acids, vol. 41, no. 2, pp. 235–256, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Zaia, “Glycosaminoglycan glycomics using mass spectrometry,” Molecular and Cellular Proteomics, vol. 12, no. 4, pp. 885–892, 2013. View at Google Scholar
  30. T. N. Laremore and R. J. Linhardt, “Improved matrix-assisted laser desorption/ionization mass spectrometric detection of glycosaminoglycan disaccharides as cesium salts,” Rapid Communications in Mass Spectrometry, vol. 21, no. 7, pp. 1315–1320, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Kovensky, “Sulfated oligosaccharides: new targets for drug development?” Current Medicinal Chemistry, vol. 16, no. 18, pp. 2338–2344, 2009. View at Publisher · View at Google Scholar · View at Scopus