The Structure of Sulfated Polysaccharides from the Sea Cucumber  Holothuria  ( Stauropora )  fuscocinerea

M. I. Bilan; Билан М. И.; A. I. Usov; Усов А. И.; Tran Thi Thanh Van; Van Tran Thi Thanh; Dinh Thanh Trung; Trung Dinh Thanh; Pham Duc Thinh; Thinh Pham Duc; Cao Thi Thuy Hang; Hang Cao Thi Thuy; N. E. Ustyuzhanina; Устюжанина Н. Е.; E. A. Tsvetkova; Цветкова Е. А.; S. P. Nikogosova; Никогосова С. П.; A. S. Dmitrenok; Дмитренок А. С.; N. E. Nifantiev; Нифантьев Н. Э.

doi:10.31857/S0132342323040309

The Structure of Sulfated Polysaccharides from the Sea Cucumber Holothuria (Stauropora) fuscocinerea

Authors: Bilan M.I.¹, Usov A.I.¹, Van T.T.², Trung D.T.², Thinh P.D.², Hang C.T.², Ustyuzhanina N.E.¹, Tsvetkova E.A.¹, Nikogosova S.P.¹, Dmitrenok A.S.¹, Nifantiev N.E.¹
Affiliations:
1. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences
2. NhaTrang Institute of Technology Research and Application, Vietnam Academy of Science and Technology
Issue: Vol 49, No 4 (2023)
Pages: 392-402
Section: Articles
URL: https://journals.rcsi.science/0132-3423/article/view/139173
DOI: https://doi.org/10.31857/S0132342323040309
EDN: https://elibrary.ru/ODDRCN
ID: 139173

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Abstract

Fucosylated chondroitin sulfate FCS-Hf and preparations of fucan sulfates Hf-Fuc1 and Hf-Fuc2 were isolated from the Vietnamese sea cucumber Holothuria (Stauropora) fuscocinerea. Separation of the polysaccharides was carried out using anion-exchange chromatography on DEAE-Sephacel. The structure of polysaccharides was established by determinations of the content of monosaccharides and sulfate, as well as by NMR spectra. It was shown that FCS-Hf was built of the repeating trisaccharide fragments, with alternating 3‑linked N-acetyl-β-D-galactosamine and 4-linked β-D-glucuronic acid residues forming the main polymer chain, which carries α-L-fucose residues as side branches attached to O3 of glucuronic acid. The regular structure of polymer is masked by an uneven distribution of sulfate groups attached to fucose residues (2,4-disulfate, 3,4-disulfate and 4-monosulfate in a ratio of 2 : 2 : 1) and galactosamine residues (4,6-disulfate and 4-monosulfate in a ratio of 3 : 1). It was also shown that fucan sulfate Hf-Fuc1 contained predominantly linear molecules built of 4-linked α-L-fucose 3-sulfate residues, while Hf-Fuc2 appeared to be a mixture of several related linear and branched fucan sulfates containing 3-linked and 4-linked α-L-Fuc residues sulfated at different positions.

Keywords

Holothuria (Stauropora) fuscocinerea, sea cucumber, polysaccharides, fucosylated chondroitin sulfate, fucan sulfate

References

Sea Cucumbers. A Global Review of Fisheries and Trade / Eds. Toral-Granda V., Lovatelli A., Vasconcellos M. Rome: FAO, 2008. 317 p.
Khotimchenko Y. // Int. J. Mol. Sci. 2018. V. 19. P. 1342. https://doi.org/10.3390/ijms19051342
Pomin V.H. // Mar. Drugs. 2014. V. 12. P. 232–254. https://doi.org/10.3390/md12010232
Ustyuzhanina N.E., Bilan M.I., Nifantiev N.E., Usov A.I. // Pure Appl. Chem. 2019. V. 91. P. 1065–1071. https://doi.org/10.1515/pac-2018-1211
Liu X., Zhang Z., Mao H., Wang P., Zuo Z., Gao L., Shi X., Yin R., Gao N., Zhao J. // Mar. Drugs. 2020. V. 18. P. 286. https://doi.org/10.3390/md18060286
Yang J., Wang Y., Jiang T., Lv Z. // Int. J. Biol. Macromol. 2015. V. 72. P. 911–918. https://doi.org/10.1016/j.ijbiomac.2014.10.010
Ustyuzhanina N.E., Bilan M.I., Dmitrenok A.S., Shashkov A.S., Kusaykin M.I., Stonik V.A., Nifantiev N.E., Usov A.I. // Glycobiology. 2016. V. 26. P. 449–459. https://doi.org/10.1093/glycob/cwv119
Mao H., Cai Y., Li S., Sun H., Lin L., Pan Y., Yang W., He Z., Chen R., Zhou L., Wang W., Yin R., Zhao J. // Carbohydr. Polym. 2020. V. 245. P. 116503. https://doi.org/10.1016/j.carbpol.2020.116503
Li S., Zhong W., Pan Y., Lin L., Cai Y., Mao H., Zhang T., Li S., Chen R., Zhou L., Wang W., Cui Q., Yin R., Huang S., Zhao J. // Carbohydr. Polym. 2021. V. 269. P. 118290. https://doi.org/10.1016/j.carbpol.2021.118290
Yin R., Zhou L., Gao N., Lin L., Sun H., Chen D., Cai Y., Zuo Z., Hu K., Huang S., Liu J., Zhao J. // Biomacromolecules. 2021. V. 22. P. 1244–1255. https://doi.org/10.1021/acs.biomac.0c01739
Yin R., Pan Y., Cai Y., Yang F., Gao N., Ruzemaimaiti D., Zhao J. // Carbohydr. Polym. 2022. V. 294. P. 119826. https://doi.org/10.1016/j.carbpol.2022.119826
Qiu P., Wu F., Yi L., Chen L., Jin Y., Ding X., Ouyang Y., Yao Y., Jiang Y., Zhang Z. // Carbohydr. Polym. 2020. V. 240. P. 116337. https://doi.org/10.1016/j.carbpol.2020.116337
Ustyuzhanina N.E., Bilan M.I., Panina E.G., Sanamyan N.P., Dmitrenok A.S., Tsvetkova E.A., Ushakova N.A., Shashkov A.S., Nifantiev N.E., Usov A.I. // Mar. Drugs. 2018. V. 16. P. 389. https://doi.org/10.3390/md16100389
Vieira R.P., Mulloy B., Mourão P.A.S. // J. Biol. Chem. 1991. V. 266. P. 13530–13536. https://doi.org/10.1016/S0021-9258(18)92730-4
Ustyuzhanina N.E., Bilan M.I., Dmitrenok A.S., Nifantiev N.E., Usov A.I. // Carbohydr. Polym. 2017. V. 164. P. 8–12. https://doi.org/10.1016/j.carbpol.2017.01.034
Li H., Yuan Q., Lv K., Ma H., Gao C., Liu Y., Zhang S., Zhao L. // Carbohydr. Polym. 2021. V. 251. P. 117034. https://doi.org/10.1016/j.carbpol.2020.117034
Ustyuzhanina N.E., Anisimova N.Y., Bilan M.I., Donenko F.V., Morozevich G.E., Yashunskiy D.V., Usov A.I., Siminyan N.G., Kirgisov K.I., Varfolomeeva S.R., Kiselevskiy M.V., Nifantiev N.E. // Pharmaceuticals. 2021. V. 14. P. 1074. https://doi.org/10.3390/ph14111074
Киселевский М.В., Анисимова Н.Ю., Билан М.И., Усов А.И., Устюжанина Н.Е., Петкевич А.А., Шубина И.Ж., Морозевич Г.Е., Нифантьев Н.Э. // Биоорг. химия. 2022. Т. 48. С. 633–647. [Kiselevskiy M.V., Anisimova N.Yu., Bilan M.I., Usov A.I., Ustyuzhanina N.E., Petkevich A.A., Shubina I.Zh., Morosevich G.E., Nifantiev N.E. // Russ. J. Bioorg. Chem. 2022. V. 39. P. 1109–1122.] https://doi.org/10.1134/S1068162022060152
Pereira M.S., Mulloy B., Mourão P.A.S. // J. Biol. Chem. 1999. V. 274. P. 7656–7667. https://doi.org/10.1074/jbc.274.12.7656
Ustyuzhanina N.E., Bilan M.I., Dmitrenok A.S., Borodina E.Y., Nifantiev N.E., Usov A.I. // Carbohydr. Res. 2018. V. 456. P. 5–9. https://doi.org/10.1016/j.carres.2017.12.001
Shang S., Mou R., Zhang Z., Gao N., Lin L., Li Z., Wu M., Zhao J. // Carbohydr. Polym. 2018. V. 195. P. 257–266. https://doi.org/10.1016/j.carbpol.2018.04.117
Ustyuzhanina N.E., Bilan M.I., Dmitrenok A.S., Tsvetkova E.A., Nikogosova S.P., Cao T.T.H., Pham D.T., Dinh T.T., Tran T.T.V., Shashkov A.S., Usov A.I., Nifantiev N.E. // Mar. Drugs. 2022. V. 20. P. 380. https://doi.org/10.3390/md20060380
Ning Z., Wang P., Zuo Z., Tao X., Gao L., Xu C., Wang Z., Wu B., Gao N., Zhao J. // Mar. Drugs. 2022. V. 20. P. 377. https://doi.org/10.3390/md20060377
Mourão P.A.S. // Mar. Drugs. 2015. V. 13. P. 2770–2784. https://doi.org/10.3390/md13052770
Fonseca R.J.C., Mourão P.A.S. // Mar. Drugs. 2021. V. 19. P. 425. https://doi.org/10.3390/md19080425
Lu W., Yang Z., Chen J., Wang D., Zhang Y. // Carbohydr. Polym. 2021. V. 272. P. 118526. https://doi.org/10.1016/j.carbpol.2021.118526
Pham D.T., Ly B.M., Usoltseva R.V., Shevchenko N.M., Rasin A.V., Anastyuk S.D., Malyarenko O.S., Zvyagintseva T.N., San P.T., Ermakova S.P. // Int. J. Biol. Macromol. 2018. V. 117. P. 1101–1109. https://doi.org/10.1016/j.ijbiomac.2018.06.017
Teo S., Ng C.S.L., Loh K.S. // Nat. Singapore. 2010. V. 3. P. 133–137.
Maya-Alvarado B., Calva-Benítez L.G., Granja- Fernández R., Pérez-López J., López-Pérez A. // Rev. Biol. Tropical. 2021. V. 69 (S1). P. 66–79. https://doi.org/10.15517/rbt.v69isuppl.1.46328
Gao N., Chen R., Mou R., Xiang J., Zhou K., Li Z., Zhao J. // Int. J. Biol. Macromol. 2020. V. 164. P. 3421–3428. https://doi.org/10.1016/j.ijbiomac.2020.08.150
Ma Y., Gao N., Zuo Z., Li S., Zheng W., Shi X., Liu Q., Ma T., Yin R., Li X., Zhao J. // Int. J. Biol. Macromol. 2021. V. 186. P. 535–543. https://doi.org/10.1016/j.ijbiomac.2021.07.049
Pomin V.H. // Carbohydr. Res. 2015. V. 413. P. 41–50. https://doi.org/10.1016/j.carres.2015.05.004
Ustyuzhanina N.E., Bilan M.I., Dmitrenok A.S., Borodina E.Y., Stonik V.A., Nifantiev N.E., Usov A.I. // Carbohydr. Polym. 2017. V. 167. P. 20–26. https://doi.org/10.1016/j.carbpol.2017.02.101
Ustyuzhanina N.E., Bilan M.I., Nifantiev N.E., Usov A.I. // Carbohydr. Res. 2019. V. 476. P. 8–11. https://doi.org/10.1016/j.carres.2019.02.008
Ustyuzhanina N.E., Bilan M.I., Anisimova N.Y., Dmitrenok A.S., Tsvetkova E.A., Kiselevskiy M.V., Nifantiev N.E., Usov A.I. // Carbohydr. Polym. 2022. V. 281. P. 119072. https://doi.org/10.1016/j.carbpol.2021.119072
Bilan M.I., Grachev A.A., Ustuzhanina N.E., Shashkov A.S., Nifantiev N.E., Usov A.I. // Carbohydr. Res. 2002. V. 337. P. 719–730. https://doi.org/10.1016/S0008-6215(02)00053-8
Билан М.И., Захарова А.Н., Грачев А.А., Шашков А.С., Нифантьев Н.Э., Усов А.И. // Биоорг. химия. 2007. Т. 33. С. 44–53. [Bilan M.I., Zakharova A.N., Grachev A.A., Shashkov A.S., Nifantiev N.E., Usov A.I. // Russ. J. Bioorg. Chem. 2007. V. 33. P. 38–46.] https://doi.org/10.1134/S1068162007010049
Usov A.I., Bilan M.I., Klochkova N.G. // Bot. Mar. 1995. V. 38. P. 43–51. https://doi.org/10.1515/botm.1995.38.1-6.43
Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith, F. // Anal. Chem. 1956. V. 28. P. 350–356. https://doi.org/10.1021/ac60111a017