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Structural analysis of glycosaminoglycans from Oviductus ranae

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Abstract

Oviductus ranae (O.ran.) has been widely used as a tonic and a traditional animal-based Chinese medicine. O.ran. extracts have been reported to have numerous biological activities, including activities that are often associated with mammalian glycosaminoglycans such as anti-inflammatory, antiosteoperotic, and anti-asthmatic. Glycosaminoglycans are complex linear polysaccharides ubiquitous in mammals that possess a wide range of biological activities. However, their presence and possible structural characteristics within O.ran. were previously unknown. In this study, glycosaminoglycans were isolated from O.ran. and their disaccharide compositions were analyzed by liquid chromatography-ion trap/time-of-flight mass spectrometry (LC-MS-ITTOF). Heparan sulfate (HS)/heparin (HP), chondroitin sulfate (CS)/dermatan sulfate (DS) and hyaluronic acid (HA) were detected in O.ran. with varied disaccharide compositions. HS species contain highly acetylated disaccharides, and have various structures in their constituent chains. CS/DS chains also possess a heterogeneous structure with different sulfation patterns and densities. This novel structural information could help clarify the possible involvement of these polysaccharides in the biological activities of O.ran..

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Abbreviations

AMAC:

2-aminoacridone

CS:

chondroitin sulfate

DS:

dermatan sulfate

EIC:

extracted ion chromatogram

GAG:

glycosaminoglycan

GalNAc:

N-acetylgalatosamine

GlcA:

glucuronate

GlcNAc:

N-acetylglucosmine

GlcNS:

N-sulfated glucosamine

HA:

hyaluronic acid

HP:

heparin

HS:

heparan sulfate

IdoA:

iduronate

KS:

keratan sulphate

LC-MS-ITTOF:

liquid chromatography-ion trap/time-of-flight mass spectrometry

NaCl:

sodium chloride

ΔUA:

4,5-unsaturated uronate (generated by heparinases and chondroitinase excision)

O.ran. :

Oviductus ranae

SE-HPLC:

size-exclusion HPLC

References

  1. Wang, Y., Wang, L., Hu, Y., Zhang, L., Wang, Z.: Isolation and identification of two steroid compounds from Oviductus Ranae. Nat Prod Res. 24(16), 1518–1522 (2010). https://doi.org/10.1080/14786419.2010.484391

    Article  CAS  PubMed  Google Scholar 

  2. Xiao, J., Jiang, D.: On origin of Oviductus Ranae in Chinese Pharmacopoeia. China J. Chin. Mater. Med. 35(21), 2931–2933 (2010)

    Google Scholar 

  3. Guo, M., Cui, L., Zhai, M., Zhang, S., Wang, T., Xu, M., Weng, Q.: Promotion of spleen lymphocyte and macrophage functions induced by neutral protease hydrolysate of Oviductus Ranae protein. Sci. Technol. Food Ind. 35(01), 345–348 (2014)

  4. Ling, X.M., Zhang, X.H., Tan, Y., Yang, J.J., Ji, B., Wu, X.R., Yi, Y.K., Liang, L.: Protective effects of Oviductus Ranae-containing serum on oxidative stress-induced apoptosis in rat ovarian granulosa cells. J. Ethnopharmacol. 208, 138–148 (2017). https://doi.org/10.1016/j.jep.2017.05.035

    Article  PubMed  Google Scholar 

  5. Cui, J., Hu, Y.: Research of the mice burden swimming time was prolonged of Oviducts Rana capsule fatigue resistance. Food Science. 08, 373–375 (2005)

    Google Scholar 

  6. Qu, X., Li, Y., Zhang, H., Zhang, X., Wang, S., Zhao, Y.: Anti-oxidation of oviductus ranae water-insoluble part and hydrolysate. Food Sci. Technol. 37(10), 211–213 (2012)

  7. Wang, H., Zhao, Y., Zhang, M., Yang, S., Zhang, X.: Effect of oviductus ranae on reducing serum lipid and ability of anti-anoxia and anti-fatigue. Food Res Dev 33(08), 201–203 (2012). https://doi.org/10.3969/j.issn.1005-6521.2012.08.059

    Article  CAS  Google Scholar 

  8. Yang, S., Zhao, Y., Zhang, M., Wang, H., Lin, Y.: Pharmacological research on non-water-soluble hydrolysates of Oviductus Ranae. Food Sci. Technol. 37(04), 44–47 (2012)

  9. Sui, X., Li, X.H., Duan, M.H., Jia, A.L., Wang, Y., Liu, D., Li, Y.P., Qiu, Z.D.: Investigation of the anti-glioma activity of Oviductus ranae protein hydrolysate. Biomed Pharmacother. 81, 176–181 (2016). https://doi.org/10.1016/j.biopha.2016.04.015

    Article  CAS  PubMed  Google Scholar 

  10. Zhang, Y., Wang, Y., Li, M., Liu, S., Yu, J., Yan, Z., Zhou, H.: Traditional uses, bioactive constituents, biological functions, and safety properties of Oviductus ranae as functional foods in China. Oxidative Med. Cell. Longev. 2019 (2019). https://doi.org/10.1155/2019/4739450

  11. Li, Y., Zheng, W., Wang, R., Su, X.: Nutritive material of Rana chensinensis by multivariation analysis methods. Food Sci. 12, 472–475 (2007)

    Google Scholar 

  12. Wang, S., Xu, Y., Wang, Y., Yang, H., Lv, Z., Jin, X., Wang, Y.: Simultaneous determination of six active components in oviductus ranae via quantitative analysis of multicomponents by single marker. J. Anal. Methods Chem. 2017 (2017). https://doi.org/10.1155/2017/9194847

  13. Hou, Z., Zhao, H., Yu, B., Cui, B.: Comprehensively analysis of components in Oviductus ranae. Sci. Technol. Food Ind. 38(04), 348–352 (2017). https://doi.org/10.13386/j.issn1002-0306.2017.04.057

    Article  Google Scholar 

  14. Esko, J.D., Lindahl, U.: Molecular diversity of heparan sulfate. J. Clin. Invest. 108(2), 169–173 (2001). https://doi.org/10.1172/JCI13530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002). https://doi.org/10.1146/annurev.biochem.71.110601.135458

    Article  CAS  PubMed  Google Scholar 

  16. Bulow, H.E., Hobert, O.: The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22, 375–407 (2006). https://doi.org/10.1146/annurev.cellbio.22.010605.093433

    Article  CAS  PubMed  Google Scholar 

  17. Whistler, R.L., Olson, E.J.: The biosynthesis of hyaluronic acid. Adv Carbohydr Chem. 12, 299–319 (1957). https://doi.org/10.1016/s0096-5332(08)60211-8

    Article  CAS  PubMed  Google Scholar 

  18. Schaefer, L., Schaefer, R.M.: Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 339(1), 237–246 (2010). https://doi.org/10.1007/s00441-009-0821-y

    Article  CAS  PubMed  Google Scholar 

  19. Iozzo, R.V.: Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 6(8), 646–656 (2005). https://doi.org/10.1038/nrm1702

    Article  CAS  PubMed  Google Scholar 

  20. Couchman, J.R.: Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26, 89–114 (2010). https://doi.org/10.1146/annurev-cellbio-100109-104126

    Article  CAS  PubMed  Google Scholar 

  21. Iozzo, R.V., Sanderson, R.D.: Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 15(5), 1013–1031 (2011). https://doi.org/10.1111/j.1582-4934.2010.01236.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mizumoto, S., Yamada, S., Sugahara, K.: Molecular interactions between chondroitin-dermatan sulfate and growth factors/receptors/matrix proteins. Curr. Opin. Struct. Biol. 34, 35–42 (2015). https://doi.org/10.1016/j.sbi.2015.06.004

    Article  CAS  PubMed  Google Scholar 

  23. Bukhari, S.N.A., Roswandi, N.L., Waqas, M., Habib, H., Hussain, F., Khan, S., Sohail, M., Ramli, N.A., Thu, H.E., Hussain, Z.: Hyaluronic acid, a promising skin rejuvenating biomedicine: A review of recent updates and pre-clinical and clinical investigations on cosmetic and nutricosmetic effects. Int. J. Biol. Macromol. 120, 1682–1695 (2018). https://doi.org/10.1016/j.ijbiomac.2018.09.188

    Article  CAS  PubMed  Google Scholar 

  24. Liu, D.F., Shriver, Z., Venkataraman, G., El Shabrawi, Y., Sasisekharan, R.: Tumor cell surface heparan sulfate as cryptic promoters or inhibitors of tumor growth and metastasis. Proc. Natl Acad. Sci. USA 99(2), 568–573 (2002). https://doi.org/10.1073/pnas.012578299

    Article  CAS  PubMed  Google Scholar 

  25. Perrimon, N., Bernfield, M.: Specificities of heparan sulphate proteoglycans in developmental processes. Nature. 404(6779), 725–728 (2000). https://doi.org/10.1038/35008000

    Article  CAS  PubMed  Google Scholar 

  26. El Masri, R., Cretinon, Y., Gout, E., Vives, R.R.: HS and inflammation: a potential playground for the sulfs? Front. Immunol. 11, 570 (2020). https://doi.org/10.3389/fimmu.2020.00570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Honvo, G., Bruyere, O., Geerinck, A., Veronese, N., Reginster, J.Y.: Efficacy of chondroitin sulfate in patients with knee osteoarthritis: a comprehensive meta-analysis exploring inconsistencies in randomized, placebo-controlled trials. Adv. Ther. 36(5), 1085–1099 (2019). https://doi.org/10.1007/s12325-019-00921-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Signorelli, S.S., Scuto, S., Marino, E., Giusti, M., Xourafa, A., Gaudio, A.: Anticoagulants and osteoporosis. Int. J. Mol. Sci. 20(21) (2019). https://doi.org/10.3390/ijms20215275

  29. Wang, X., Sharp, J.S., Handel, T.M., Prestegard, J.H.: Chemokine oligomerization in cell signaling and migration. Prog. Mol. Biol. Transl. Sci. 117, 531–578 (2013). https://doi.org/10.1016/B978-0-12-386931-9.00020-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Vasvani, S., Kulkarni, P., Rawtani, D.: Hyaluronic acid: A review on its biology, aspects of drug delivery, route of administrations and a special emphasis on its approved marketed products and recent clinical studies. Int. J. Biol. Macromol. 151, 1012–1029 (2020). https://doi.org/10.1016/j.ijbiomac.2019.11.066

    Article  CAS  PubMed  Google Scholar 

  31. Wigen, J., Elowsson-Rendin, L., Karlsson, L., Tykesson, E., Westergren-Thorsson, G.: Glycosaminoglycans: a link between development and regeneration in the lung. Stem Cells Dev. 28(13), 823–832 (2019). https://doi.org/10.1089/scd.2019.0009

    Article  PubMed  Google Scholar 

  32. Du, J., Liu, S., Liang, Q., Lin, J., Jiang, L., Chen, F., Wei, Z.: Analysis of Heparan sulfate/heparin from Colla corii asini by liquid chromatography-electrospray ion trap mass spectrometry. Glycoconj. J. 36(3), 211–218 (2019). https://doi.org/10.1007/s10719-019-09868-0

    Article  CAS  PubMed  Google Scholar 

  33. Huang, H., Liu, S., Du, J., Lin, J., Liang, Q., Liu, S., Wei, Z.: Structural analysis of glycosaminoglycans from Colla corii asini by liquid chromatography-electrospray ion trap mass spectrometry. Glycoconj. J. 37(2), 201–207 (2020). https://doi.org/10.1007/s10719-019-09904-z

    Article  CAS  PubMed  Google Scholar 

  34. Liang, Q.T., Xiao, X.M., Lin, J.H., Wei, Z.: A new sequencing approach for N-unsubstituted heparin/heparan sulfate oligosaccharides. Glycobiology. 25(7), 714–725 (2015). https://doi.org/10.1093/glycob/cwv011

    Article  CAS  PubMed  Google Scholar 

  35. Fu, L., Sun, X., He, W., Cai, C., Onishi, A., Zhang, F., Linhardt, R.J., Liu, Z.: Keratan sulfate glycosaminoglycan from chicken egg white. Glycobiology. 26(7), 693–700 (2016). https://doi.org/10.1093/glycob/cww017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Funderburgh, J.L.: Mini Review Keratan sulfate: structure, biosynthesis, and function. Glycobiology. 10, 951–958 (2000). https://doi.org/10.1093/glycob/10.10.951

    Article  CAS  PubMed  Google Scholar 

  37. Du, J.Y., Chen, L.R., Liu, S., Lin, J.H., Liang, Q.T., Lyon, M., Wei, Z.: Ion-pairing liquid chromatography with on-line electrospray ion trap mass spectrometry for the structural analysis of N-unsubstituted heparin/heparan sulfate. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1028, 71–76 (2016). https://doi.org/10.1016/j.jchromb.2016.06.006

    Article  CAS  PubMed  Google Scholar 

  38. 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). https://doi.org/10.1016/j.chroma.2011.12.063

    Article  CAS  PubMed  Google Scholar 

  39. Gallagher, J.T.: Heparan sulphate: a heparin in miniature. Handb. Exp. Pharmacol. 207, 347–360 (2012). https://doi.org/10.1007/978-3-642-23056-1_15

    Article  CAS  Google Scholar 

  40. Wei, Z., Lyon, M., Gallagher, J.T.: Distinct substrate specificities of bacterial heparinases against N-unsubstituted glucosamine residues in heparan sulfate. J. Biol. Chem. 280(16), 15742–15748 (2005). https://doi.org/10.1074/jbc.M501102200

    Article  CAS  PubMed  Google Scholar 

  41. Kim, S.Y., Kundu, J., Williams, A., Yandulskaya, A.S., Monaghan, J.R., Carrier, R.L., Linhardt, R.J.: Glycosaminoglycans compositional analysis of Urodele axolotl (Ambystoma mexicanum) and Porcine Retina. Glycoconj. J. 36(2), 165–174 (2019). https://doi.org/10.1007/s10719-019-09863-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Trowbridge, J.M., Gallo, R.L.: Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology. 12(9), 117r-125r (2002). https://doi.org/10.1093/glycob/cwf066

  43. Thelin, M.A., Bartolini, B., Axelsson, J., Gustafsson, R., Tykesson, E., Pera, E., Oldberg, A., Maccarana, M., Malmstrom, A.: Biological functions of iduronic acid in chondroitin/dermatan sulfate. FEBS J. 280(10), 2431–2446 (2013). https://doi.org/10.1111/febs.12214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Neuman, M.G., Nanau, R.M., Oruna-Sanchez, L., Coto, G.: Hyaluronic acid and wound healing. J. Pharm. Pharm. Sci. 18(1), 53–60 (2015). https://doi.org/10.18433/j3k89d

    Article  CAS  PubMed  Google Scholar 

  45. Gupta, R.C., Lall, R., Srivastava, A., Sinha, A.: Hyaluronic acid: molecular mechanisms and therapeutic trajectory. Front. Vet. Sci. 6 (2019). https://doi.org/10.3389/fvets.2019.00192

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Acknowledgements

This work was supported by Chinese National Funding Grants 21576051.

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Authors and Affiliations

  1. Institute of Glycobiochemistry, National Engineering Research Centre of Chemical Fertilizer Catalyst, Fu Zhou University, Fu Zhou, 350002, People’s Republic of China

    Haiyue Huang, Jin Mao, Jianghui Lin, Lilong Jiang & Zheng Wei

  2. College of Biological Science and Engineering, Fu Zhou University, Fu Zhou, 350002, People’s Republic of China

    Quntao Liang & Shutao Liu

  3. Department of BioMolecular Sciences, Department of Chemistry and Biochemistry, University of Mississippi, Oxford, MS, 38655, USA

    Joshua S. Sharp

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  1. Haiyue Huang
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Huang, H., Mao, J., Liang, Q. et al. Structural analysis of glycosaminoglycans from Oviductus ranae. Glycoconj J 38, 25–33 (2021). https://doi.org/10.1007/s10719-020-09962-8

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