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Anti-angiogenic properties of sulfated polysaccharides fucoidans and their analogs

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Abstract

In order to find efficient anticancer agents among natural sulfated polysaccharides and their analogs, we studied the anti-angiogenic capacity of natural fucoidans from brown algae Saccharina latissima (SL) and Chordaria flagelliformis (CF) along with chemically modified fucoidan from Punctaria plantaginea (MF) and synthetic completely sulfated fucooctasaccharide (OS) built of (1→3)-bonded residues of α-l-fucopyranose of exhibiting anti-angiogenic activity in vitro on the model of formation of capillary-like structures (precapillaries) by endothelial cells or their precursors, mesenchymal stem cells. The activity of the studied compounds was tested on cells of low-grade human breast cancer of the MDA-MB-231 line and multipotent mesenchymal stem cells (MSCs) of dogs. Fucoidan CF and its derivatives SL and MF in a concentration of 0.1 mg mL−1 reliably suppress the formation of closed circular structures by cancer cells. The formation of capillary-like structures of MSC is inhibited by fucoidan CF in concentrations of 0.1 and 0.01 mg mL−1. Modified fucoidan MF and synthetic oligosaccharide OS are somewhat less active, which can be due to their insufficiently high molecular weights and specific features of the sulfation character. The obtained data indicate that the search for anti-angiogenic agents in the series of sulfated oligosaccharides with the variation of the molecular size, structure, and sulfation pattern should be extended.

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References

  1. J. O. Jin, P. S. Chauhan, A. P. Arukha, V. Chavda, F. Dubey, D. Yadav, Mar. Drugs., 2021, 19, 265; DOI: https://doi.org/10.3390/md19050265.

    Article  CAS  Google Scholar 

  2. Y. Lin, X. Qi, H. Liu, K. Xue, S. Xu, Z. Tian, Cancer Cell Int., 2020, 20, 154; DOI: https://doi.org/10.1186/s12935-020-01233-8.

    Article  CAS  Google Scholar 

  3. F. Atashrazm, R. M. Lowenthal G. M, Woods, A. F. Holloway, J. L. Dickinson, Mar. Drugs., 2015, 13, 2327–2346; DOI: https://doi.org/10.3390/md130423275.

    Article  CAS  Google Scholar 

  4. H. Lee, J. S. Kim, E Kim, PLoS ONE, 2012, 7, e50624; DOI: https://doi.org/10.1371/journal.pone.0050624.

    Article  CAS  Google Scholar 

  5. H. Y. Hsu, T. Y. Lin, P. A. Hwang, L. M. Tseng, R. H. Chen, S. M. Tsao, J. Hsu, Carcinogenesis, 2013, 34, 874–884; DOI: https://doi.org/10.1093/carcin/bgs396.

    Article  CAS  Google Scholar 

  6. Z. Zhang, K. Teruya, T. Yoshida, H. Eto, S. Shirahata, Mar. Drugs., 2013, 11, 81–98; DOI: https://doi.org/10.3390/md11010081.

    Article  CAS  Google Scholar 

  7. T. V. Alekseyenko, S. Y. Zhanayeva, A. A. Venediktova, T. N. Zvyagintseva, T. A. Kuznetsova, N. N. Besednova, T. A. Korolenko, Bull. Exp. Biol. Med., 2007, 143, 730–732; DOI: https://doi.org/10.1007/s10517-007-0226-4.

    Article  CAS  Google Scholar 

  8. M. Zeng, X. Wu, F. Li, W. She, L. Zhou, B. Pi, Z. Xu, X. Huang, Exp. Toxicol. Pathol., 2017, 69, 527–532; DOI: https://doi.org/10.1016/j.etp.2017.03.005.

    Article  CAS  Google Scholar 

  9. W. Zhang, W. Wu, Y. Bao, X. Yan, F. Zhang, R. J. Linhardt, W. Jin, G. Mao, Food Funct., 2021, 12, 10644–10657; DOI: https://doi.org/10.1039/d1fo02062e.

    Article  CAS  Google Scholar 

  10. M. Xue, Y. Ge, J. Zhang, PLoS ONE, 2012, 7, e43483; DOI: https://doi.org/10.1371/journal.pone.0043483.

    Article  CAS  Google Scholar 

  11. X. Rui, H. F. Pan, S. L. Shao, BMC Complement Altern. Med., 2017, 17, 378; DOI: https://doi.org/10.1186/s12906-017-1885-y.

    Article  Google Scholar 

  12. L. M. Cao, Z. X. Sun, E. C. Makale, G. K. Du, W. F. Long, H. R. Huang, Transl. Cancer Res., 2021, 10, 5390–5405. DOI: https://doi.org/10.21037/tcr-21-173.

    Article  CAS  Google Scholar 

  13. S. Nishimoto, J. Intl. Soc. Life Info. Sci., 2015, 33, 25–37; DOI: https://doi.org/10.18936/islis.33.1_25.

    Google Scholar 

  14. H. L. Tsai, C. J. Tai, C. W. Huang, F. R. Chang, J. Y. Wang, Mar. Drugs., 2017, 15, 122; DOI: https://doi.org/10.3390/md15040122.

    Article  Google Scholar 

  15. H. Y. Hsu, T. Y. Lin, C. H. Hu, D. T. F. Shu, M. K. Lu, Cancer Lett., 2018, 432, 120–112; DOI: https://doi.org/10.1016/j.canlet.2018.05.006.

    Article  Google Scholar 

  16. X. Rui, H. F. Pan, S. L. Shao, X. M. Xu, BMC Complement Altern. Med., 2017, 17, 378; DOI: https://doi.org/10.1186/s12906-017-1885-y.

    Article  Google Scholar 

  17. Y. Lin, X. Qi, H. Liu, K. Xue, S. Xu, Z. Tian, Cancer Cell Int., 2020, 20, 154; DOI: https://doi.org/10.1186/s12935-020-01233-8.

    Article  CAS  Google Scholar 

  18. M. C. Chen, W. L. Hsu, P. A. Hwang, T. C. Chou, Mar. Drugs., 2015, 13, 4436–4451; DOI: https://doi.org/10.3390/md13074436.

    Article  CAS  Google Scholar 

  19. G. Morales-Guadarrama, R. García-Becerra, E. A. Méndez-Pérez, J. García-Quiroz, E. Avila, L. Díaz, Cells, 2021, 10, 1758; DOI: https://doi.org/10.3390/cells10071758.

    Article  CAS  Google Scholar 

  20. K. Shirakawa, H. Tsuda, Y. Heike, K. Kato, R. Asada, M. Inomata, H. Sasaki, F. Kasumi, M. Yoshimoto, T. Iwanaga, Cancer Res., 2001, 61, 445–451; PMID: 11212228.

    CAS  Google Scholar 

  21. K. Shirakawa, H. Wakasugi, Y. Heike, I. Watanabe, S. Yamada, K. Saito, F. Konishi, Int. J. Cancer., 2002, 99, 821–828; DOI: https://doi.org/10.1002/ijc.10423.

    Article  CAS  Google Scholar 

  22. A. A. Vartanian, Biochemistry (Moscow), 2012, 77, 1044–1055; DOI: https://doi.org/10.1134/S000629791209012X.

    Article  CAS  Google Scholar 

  23. K. Matsubara, C. Xue, X. Zhao, M. Mori, T. Sugawara, T. Hirata, Int. J. Mol. Med., 2000, 15, 695–699; PMID: 15754034.

    Google Scholar 

  24. W. J. Hsu, M. H. Lin, T. C. Kuo, C. M. Chou, F. L. Mi, C. H. Cheng, C. W. Lin, Int. J. Biol. Macromol., 2020, 149, 600–608; DOI: https://doi.org/10.1016/j.ibiomac.2020.01.256.

    Article  CAS  Google Scholar 

  25. F. Wang, Y. Xiao, S. Neupane, S. H. Ptak, R. Römer, J. Xiong, J. Ohmes, A. Seekamp, X. Fretté, S. Alban, S. Fuchs, Mar. Drugs., 2021, 19, 194; DOI: https://doi.org/10.3390/md19040194.

    Article  CAS  Google Scholar 

  26. A. Cumashi, N. A. Ushakova, M. E. Preobrazhenskaya, A. D’Incecco, A. Piccoli, L. Totani, N. Tinari, G. E. Morozevich, A. E. Berman, M. I. Bilan, A. I. Usov, N. E. Ustyuzhanina, A. A. Grachev, C. J. Sanderson, M. Kelly, G. A. Rabinovich, S. Iacobelli, N. E. Nifantiev, Glycobiology, 2007, 17, 541–552; DOI:https://doi.org/10.1093/glycob/cwm014.

    Article  CAS  Google Scholar 

  27. N. E. Ustyuzhanina, M. I. Bilan, N. A. Ushakova, A. I. Usov, M. V. Kiselevskiy, N. E. Nifantiev, Glycobiology, 2014, 24, 1265–1274; DOI: https://doi.org/10.1093/glycob/cwu063.

    Article  CAS  Google Scholar 

  28. M. I. Bilan, A. A. Grachev, A. S. Shashkov, M. Kelly, C. J. Sanderson, N. E. Nifantiev, A. I. Usov, Carbohydr. Res., 2010, 345, 2038–2047; DOI: https://doi.org/10.1016/j.carres.2010.07.009.

    Article  CAS  Google Scholar 

  29. M. I. Bilan, E. V. Vinogradova, E. A. Tsvetkova, A. A. Grachev, A. S. Shashkov, N. E. Nifantiev, A. I. Usov, Carbohydr. Res., 2008, 343, 2605–2612; DOI: https://doi.org/10.1016/j.carres.2008.06.001.

    Article  CAS  Google Scholar 

  30. N. E. Ustyuzhanina, M. I. Bilan, A. G. Gerbst, N. A. Ushakova, E. A. Tsvetkova, A. S. Dmitrenok, A. I. Usov, N. E. Nifantiev, Carbohydr. Polym., 2016, 136, 826–833; DOI: https://doi.org/10.1016/j.carbpol.2015.09.102.

    Article  CAS  Google Scholar 

  31. V. B. Krylov, Z. M. Kaskova, D. Z. Vinnitskiy, N. E. Ustyuzhanina, A. A. Grachev, A. O. Chizhov, N. E. Nifantiev, Carbohydr. Res., 2011, 346, 540–550; DOI: https://doi.org/10.1016/j.carres.2011.01.005.

    Article  CAS  Google Scholar 

  32. M. V. Kiselevskiy, N. Y. Anisimova, E. A. Kornushenkov, A. D. Shepelev, S. N. Chvalun, B. E. Polotskiy, M. I. Davydov, Modern Technol. Med., 2016, 8, No. 1, 6–13; DOI: https://doi.org/10.17691/stm2016.8.1.01.

    Google Scholar 

  33. M. Berridge, A. Tan, Arch. Biochem. Biophys., 1993, 303, 474–482; DOI: https://doi.org/10.1006/abbi.1993.1311.

    Article  CAS  Google Scholar 

  34. B. Ye, J. Ma, Z. Li, Y. Li, X. Han, Front. Oncol., 2022, 12:939646; DOI: https://doi.org/10.3389/fonc.2022.939646.

    Article  Google Scholar 

  35. G. Morales-Guadarrama, R. García-Becerra, E. A. Méndez-Pérez, J. García-Quiroz, E. Avila, L. Díaz, Cells, 2021, 10, 1758; DOI: https://doi.org/10.3390/cells10071758.

    Article  CAS  Google Scholar 

  36. D. Leal, A. Mansilla, B. Matsuhiro, M. Moncada-Basualto, M. Lapier, J. D. Maya, C. Olea-Azar, W. M. De Borggraeve, Carbohydr. Polym., 2018, 199, 304–313; DOI: https://doi.org/10.1016/j.carbpol.2018.07.012.

    Article  CAS  Google Scholar 

  37. E. Lahrsen, A. K. Schoenfeld, S. Alban, Carbohydr. Polym., 2018, 189, 162–168; DOI: https://doi.org/10.1016/j.carbpol.2018.02.035.

    Article  CAS  Google Scholar 

  38. E. Lahrsen, A. K. Schoenfeld, S. Alban, ACS Biomater. Sci. Eng., 2019, 5, 1200–1214; DOI: https://doi.org/10.1021/acsbiomaterials.8b01113.

    Article  CAS  Google Scholar 

  39. A. Zayed, R. Ulber, Carbohydr. Polym., 2019, 211, 289–297; DOI: https://doi.org/10.1016/j.carbpol.2019.01.

    Article  CAS  Google Scholar 

  40. E. A. Khatuntseva, N. E. Ustuzhanina, G. V. Zatonskii, A. S. Shashkov, A. I. Usov, N. E. Nifant’ev, J. Carbohydr. Chem., 2000, 19, 1151–1173; DOI: https://doi.org/10.1080/07328300008544140.

    Article  CAS  Google Scholar 

  41. N. E. Ustuzhanina, V. B. Krylov, A. A. Grachev, A. G. Gerbst, N. E. Nifantiev, Synthesis, 2006, 4017–4031; DOI: https://doi.org/10.1055/s-2006-950333.

  42. N. E. Ustyuzhanina, N. A. Ushakova, M. E. Preobrazhenskaya, M. I. Bilan, E. N. Tsvetkova, V. B. Krylov, N. A. Anisimova, M. V. Kiselevskiy, V. N. Krukovskaya, C. Li, G. Yu, S. Saran, R. K. Saxena, A. I. Usov, N. E. Nifantiev, Pure Appl. Chem., 2014, 86, 1365–1375; DOI: https://doi.org/10.1515/pac-2014-0404.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. N. N. Blokhin National Medical Research Center of Oncology, Ministry of Health Protection, 24 Kashirskoe sh., 115478, Moscow, Russian Federation

    N. Yu. Anisimova & M. V. Kiselevskiy

  2. N. D. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 47 Leninsky prosp., 119991, Moscow, Russian Federation

    N. E. Ustyuzhanina, M. I. Bilan & N. E. Nifantiev

  3. V. N. Orekhovich Research Institute of Biomedical Chemistry, 10 ul. Pogodinskaya, 119121, Moscow, Russian Federation

    G. E. Morozevich & A. I. Usov

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  1. N. Yu. Anisimova
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  2. N. E. Ustyuzhanina
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Correspondence to N. Yu. Anisimova, N. E. Nifantiev or M. V. Kiselevskiy.

Additional information

This work was financially supported by the Russian Foundation for Basic Research (Projects Nos 17-00-00494, 17-00-00495, and 17-00-00496).

All procedures involving animals corresponded to the ethical standards of the institution at which the research was performed and to legal documents of the Russian Federation and international organizations.

No human or animal subjects were used in this research.

The authors declare no competing interests.

Published in Russian in Izvestiya Akademii Nauk. Seriya Khimicheskaya, No. 11, pp. 2505–2514, November, 2022.

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Anisimova, N.Y., Ustyuzhanina, N.E., Bilan, M.I. et al. Anti-angiogenic properties of sulfated polysaccharides fucoidans and their analogs. Russ Chem Bull 71, 2505–2514 (2022). https://doi.org/10.1007/s11172-022-3680-2

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