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Compositional analysis and structural elucidation of glycosaminoglycans in chicken eggs

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Abstract

Glycosaminoglycans (GAGs) have numerous applications in the fields of pharmaceuticals, cosmetics, nutraceuticals, and foods. GAGs are also critically important in the developmental biology of all multicellular animals. GAGs were isolated from chicken egg components including yolk, thick egg white, thin egg white, membrane, calcified shell matrix supernatant, and shell matrix deposit. Disaccharide compositional analysis was performed using ultra high-performance liquid chromatography-mass spectrometry. The results of these analyses showed that all four families of GAGs were detected in all egg components. Keratan sulfate was found in egg whites (thick and thin) and shell matrix (calcified shell matrix supernatant and deposit) with high level. Chondroitin sulfates were much more plentiful in both shell matrix components and membrane. Hyaluronan was plentiful in both shell matrix components and membrane, but was only present in a trace of quantities in the yolk. Heparan sulfate was plentiful in the shell matrix deposit but was present in a trace of quantities in the egg content components (yolk, thick and thin egg whites). Most of the chondroitin and heparan sulfate disaccharides were present in the GAGs found in chicken eggs with the exception of chondroitin and heparan sulfate 2,6-disulfated disaccharides. Both CS and HS in the shell matrix deposit contained the most diverse chondroitin and heparan sulfate disaccharide compositions. Eggs might provide a potential new source of GAGs.

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References

  1. Capila, I., Linhardt, R.J.: Heparin–protein interactions. Angew. Chem. Int. Ed. 41, 391–412 (2002)

    Article  Google Scholar 

  2. Schaefer, L., Schaefer, R.M.: Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 339, 237–246 (2010)

    Article  CAS  PubMed  Google Scholar 

  3. Weyers, A., Yang, B., Solakyildirim, K., Yee, V., Li, L., Zhang, F., Linhardt, R.J.: Isolation of bovine corneal keratan sulfate and its growth factor and morphogen binding. FEBS J. 280, 2285–2293 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Trigkilidas, D., Anand, A.: The effectiveness of hyaluronic acid intra-articular injections in managing osteoarthritic knee pain. Ann. Royal Col. Surg. Engl. 95, 545–551 (2013)

    Article  CAS  Google Scholar 

  5. Abate, M., Schiavone, C., Salini, V.: The use of hyaluronic acid after tendon surgery and in tendinopathies. BioMed Res. Int. (2014)

  6. Arpicco, S., Milla, P., Stella, B., Dosio, F.: Hyaluronic acid conjugates as vectors for the active targeting of drugs, genes and nanocomposites in cancer treatment. Molecules 19, 3193–3230 (2014)

    Article  PubMed  Google Scholar 

  7. Chong, B.F., Blank, L.M., Mclaughlin, R., Nielsen, L.K.: Microbial hyaluronic acid production. Appl. Microbiol. Biotechnol. 66, 341–351 (2005)

    Article  CAS  PubMed  Google Scholar 

  8. Hamano, T., Mitsuhashi, Y., Acki, N., Yamamoto, S.: High-performance liquid chromatographic assay of chondroitin sulphate in food products. Analyst 114, 891–893 (1989)

    Article  CAS  Google Scholar 

  9. Yamada, S., Sugahara, K.: Potential therapeutic application of chondroitin sulfate/ dermatan sulfate. Curr. Drug Disc. Technol. 5, 289–301 (2008)

    Article  CAS  Google Scholar 

  10. Oschatz, C., Maas, C., Lecher, B., et al.: Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity 34(2), 258–268 (2011)

    Article  CAS  PubMed  Google Scholar 

  11. Linhardt, R.J.: Claude S Hudson award address in carbohydrate chemistry. Heparin: structure and activity. J. Med. Chem. 46(13), 2551–2564 (2003)

    Article  CAS  PubMed  Google Scholar 

  12. Barbosa, M.: What is the best treatment for a cancer patient with thrombosis? Clin. Med. Insights Oncol. 8, 49–55 (2014)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Amjadi, S., Mai, K., McCluskey, P., Wakefield, D.: The role of lumican in ocular disease. ISRN Ophthalmol. 1–7 (2013)

  14. Vázquez, J.A., Rodríguez-Amado, I., Montemayor, M., Fraguas, J., González, M.P., Murado, M.A.: Chondroitin sulfate, hyaluronic acid and chitin/chitosan production using marine waste sources: characteristics, applications and eco-friendly processes: a review. Mar. Drugs 11, 747–774 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  15. Lord, M.S., Whitelock, J.M.: Bioengineered heparin: Is there a future for this form of the successful therapeutic? Biogeosciences 5(4), 1–5 (2014)

    Google Scholar 

  16. Garnjanagoonchorn, W., Wongekalak, L., Engkagul, A.: Determination of chondroitin sulfate from different sources of cartilage. Chem. Eng. Proc. 46, 465–471 (2007)

    Article  CAS  Google Scholar 

  17. Stern, R., Asari, A.A., Sugahara, K.N.: Hyaluronan fragments: an information-rich system. Eur. J. Cell Biol. 85(8), 699–715 (2006)

    Article  CAS  PubMed  Google Scholar 

  18. Jiang, D., Liang, J., Noble, P.W.: Hyaluronan in tissue injury and repair. Ann. Rev. Cell Dev. Biol. 23, 435–461 (2007)

    Article  CAS  Google Scholar 

  19. Abdou, A.M., Kim, M., Sato K.: Functional proteins and peptides of hen’s egg origin. In Hernández-Ledesma, B., Hsieh, C.C. (Ed.): Bioactive food peptides in health and disease, InTech (JanezaTrdine 9, 51000 Rijeka, Croatia). 115–144 (2013)

  20. Arias, J.L., Fink, D.J., Xiao, S.Q., Heuer, A.H., Caplan, A.I.: Biomineralization and eggshells: cell-mediated acellular compartments of mineralized extracellular matrix. Int. Rev. Cytol. 145, 217–250 (1993)

    Article  CAS  PubMed  Google Scholar 

  21. Solomon, S.E.: Egg and eggshell quality. Wolfe Publ, Ltd, London (1991)

    Google Scholar 

  22. Baker, J.R., Balch, D.A.: A study of the organic material of hen’s eggshell. Biochem. J. 82, 352–361 (1962)

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Heaney, R.K., Robinson, D.S.: The isolation and characterization of hyaluronic acid in eggshell. Biochim. Biophys. Acta 451, 133–142 (1976)

    Article  CAS  PubMed  Google Scholar 

  24. Leach, R.M.: Biochemistry of the organic matrix of the eggshell. Poult. Sci. 61, 2040–2047 (1982)

    Article  CAS  Google Scholar 

  25. Nakano, T., Ikawa, N.I., Ozimek, L.: Chemical composition of chicken eggshell and shell membranes. Poult. Sci. 82, 510–514 (2003)

    Article  CAS  PubMed  Google Scholar 

  26. Carrino, D.A., Dennis, J.E., Wu, T.M., Arias, J.L., Fernandez, M.S., Rodriguez, J.P., Fink, D.J., Heuer, A.H., Caplan, A.I.: The avian eggshell extracellular matrix as a model for biomineralization. Connect. Tissue Res. 35(1), 325–329 (1996)

    Article  CAS  PubMed  Google Scholar 

  27. Yang, B., Chang, Y., Weyers, A.M., Sterner, E., Linhardt, R.J.: Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry. J. Chromatogr. A 1225, 91–98 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Plaas, A.H.K., West, L.A., Midura, R.J.: Keratan sulfate disaccharide composition determined by FACE analysis of keratanase II and endo-β-galactosidase digestion products. Glycobiology 11(10), 779–790 (2001)

    Article  CAS  PubMed  Google Scholar 

  29. Wang, P.L., Wang, S.H., Liu, Z.G.: Structural characterizations of pimpled eggshells. Chin. J. Anim. Husb. 50(1), 79–83 (2014)

    CAS  Google Scholar 

  30. Carrino, D.A., Rodriguez, J.P., Caplan, A.I.: Dermatan sulfate proteoglycans from the mineralized matrix of the avian eggshell. Connect. Tissue Res. 36(3), 175–193 (1997)

    Article  CAS  PubMed  Google Scholar 

  31. Ucakturk, E., Cai, C., Li, L., Li, G., Zhang, F., Linhardt, R.J.: Capillary electrophoresis for total glycosaminoglycan analysis. Anal. Bioanal. Chem. 406(19), 4617–26 (2014)

    Article  CAS  PubMed  Google Scholar 

  32. Yamada, S., Sugahara, K.: Potential therapeutic application of chondroitin sulfate/ dermatan sulphate. Curr. Drug. Discov. Technol. 5, 289–301 (2008)

    Article  CAS  PubMed  Google Scholar 

  33. Feinberg, R.N., Beebe, D.C.: Hyaluronate in vasculogenesis. Science 220(4602), 1177–1179 (1983)

    Article  CAS  PubMed  Google Scholar 

  34. West, D.C., Hampson, I.N., Arnold, F., Kumar, S.: Angiogenesis induced by degradation products of hyaluronic acid. Science 228(4705), 1324–1326 (1985)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the US National Institutes of Health (HL62244, HL094463, HL096972, GM102137), the National Natural Science Foundation of China (NSFC 31372303, 30700567) and Zhejiang Provincial Natural Science Foundation of China (LY12C17002) for supporting this research.

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Correspondence to Robert J. Linhardt.

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Liu, Z., Zhang, F., Li, L. et al. Compositional analysis and structural elucidation of glycosaminoglycans in chicken eggs. Glycoconj J 31, 593–602 (2014). https://doi.org/10.1007/s10719-014-9557-3

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  • DOI: https://doi.org/10.1007/s10719-014-9557-3

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