DOI QR코드

DOI QR Code

Reevaluation of bactericidal, cytotoxic, and macrophage-stimulating activities of commercially available Fucus vesiculosus fucoidan

  • Nishiguchi, Tomoki (Graduate School of Fisheries Science and Environmental Studies, Nagasaki University) ;
  • Jiang, Zedong (Graduate School of Fisheries Science and Environmental Studies, Nagasaki University) ;
  • Ueno, Mikinori (Graduate School of Fisheries Science and Environmental Studies, Nagasaki University) ;
  • Takeshita, Satoshi (Center for Industry, University and Government Cooperation, Nagasaki University) ;
  • Cho, Kichul (Joint Research Division, Korea University of Science and Technology) ;
  • Roh, Seong Woon (Jeju Center, Korea Basic Science Institute (KBSI)) ;
  • Kang, Kyong-Hwa (Department of Chemistry, Pukyong National University) ;
  • Yamaguchi, Kenichi (Graduate School of Fisheries Science and Environmental Studies, Nagasaki University) ;
  • Kim, Daekyung (Joint Research Division, Korea University of Science and Technology) ;
  • Oda, Tatsuya (Graduate School of Fisheries Science and Environmental Studies, Nagasaki University)
  • Received : 2014.05.01
  • Accepted : 2014.09.02
  • Published : 2014.09.15

Abstract

Polysaccharides prepared from marine algae sometimes contain contaminants such as polyphenols and endotoxins that may mislead their bona fide biological activities. In this study, we examined bioactive contaminants in commercially available fucoindan from Fucus vesiculosus, along with ascophyllan and fucoidan from Ascophyllum nodosum. F. vesiculosus fucoidan inhibited the growth of Vibrio alginolyticus in a concentration-dependent manner ($0-1,000{\mu}g\;mL^{-1}$). However, the antibacterial activity of the fucoidan significantly reduced after methanol-extraction, and the methanol-extract showed a potent antibacterial activity. The extract also showed cytotoxicity to RAW264.7 and U937 cells, and induced apoptotic nuclear morphological changes in U937 cells. These results suggest that the antibacterial activity of the fucoidan is partly due to the methanol-extractable contaminants that can also contribute to the cytotoxicity on RAW264.7 and U937 cells. On the other hand, the activities to induce secretion of nitric oxide and tumor necrosis factor-${\alpha}$ from RAW264.7 cells were observed in the fucoidan even after methanol extraction, and the extract had no such activities. Our observations suggest that commercially available fucoidan should be purified prior to biochemical use.

Keywords

References

  1. Ahmed, S. A., Gogal, R. M. Jr. & Walsh, J. E. 1994. A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [$^{3}H$]thymidine incorporation assay. J. Immunol. Methods 170:211-224. https://doi.org/10.1016/0022-1759(94)90396-4
  2. Baba, M., Schols, D., Pauwels, R., Nakashima, H. & De Clercq, E. 1990. Sulfated polysaccharides as potent inhibitors of HIV-induced syncytium formation: a new strategy towards AIDS chemotherapy. J. Acquir. Immune Defic. Syndr. 3:493-499.
  3. Chotigeat, W., Tongsupa, S., Supamataya, K. & Phongdara, A. 2004. Effect of fucoidan on disease resistance of black tiger shrimp. Aquaculture 233:23-30. https://doi.org/10.1016/j.aquaculture.2003.09.025
  4. Clement, M. J., Tissot, B., Chevolot, L., Adjadj, E., Du, Y., Curmi, P. A. & Daniel, R. 2010. NMR characterization and molecular modeling of fucoidan showing the importance of oligosaccharide branching in its anticomplementary activity. Glycobiology 20:883-894. https://doi.org/10.1093/glycob/cwq046
  5. Collins, L. & Franzblau, S. G. 1997. Microplate alamar blue assay versus BACTEC 460 system for high-throughput screening of compounds against Mycobacterium tuberculosis and Mycobacterium avium. Antimicrob. Agents Chemother. 41:1004-1009.
  6. Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. A., Camara, R. B., Nobre, L. T., Costa, M. S., Almeida- Lima, J., Farias, E. H., Leite, E. L. & Rocha, H. A. 2010. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed. Pharmacother. 64:21-28. https://doi.org/10.1016/j.biopha.2009.03.005
  7. Croci, D. O., Cumashi, A., Ushakova, N. A., Preobrazhenskaya, M. E., Piccoli, A., Totani, L., Ustyuzhanina, N. E., Bilan, M. I., Usov, A. I., Grachev, A. A., Morozevich, G. E., Berman, A. E., Sanderson, C. J., Kelly, M., Di Gregorio, P., Rossi, C., Tinari, N., Iacobelli, S., Rabinovich, G. A., Nifantiev, N. E. & Consorzio Interuniversitario Nazionale per la Bio-Oncologia (CINBO), Italy. 2011. Fucans, but not fucomannoglucuronans, determine the biological activities of sulfated polysaccharides from Laminaria saccharina brown seaweed. PLoS One 6:e17283. https://doi.org/10.1371/journal.pone.0017283
  8. Cumashi, A., Ushakova, N. A., Preobrazhenskaya, M. E., D'Incecco, A., Piccoli, A., Totani, L., Tinari, N., Morozevich, G. E., Berman, A. E., Bilan, M. I., Usov, A. I., Ustyuzhanina, N. E., Grachev, A. A., Sanderson, C. J., Kelly, M., Rabinovich, G. A., Iacobelli, S., Nifantiev, N. E. & Consorzio Interuniversitario Nazionale per la Bio-Oncologia (CINBO), Italy. 2007. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17:541-552.
  9. Damonte, E. B., Matulewicz, M. C. & Cerezo, A. S. 2004. Sulfated seaweed polysaccharides as antiviral agents. Curr. Med. Chem. 11:2399-2419. https://doi.org/10.2174/0929867043364504
  10. De Souza, M. C. R., Marques, C. T., Dore, C. M. G., Da Silva, F. R. F., Rocha, H. A. O. & Leite, E. L. 2007. Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J. Appl. Phycol. 19:153-160. https://doi.org/10.1007/s10811-006-9121-z
  11. Ellouali, M., Boisson-Vidal, C., Durand, P. & Jozefonvicz, J. 1993. Antitumor activity of low molecular weight fucans extracted from brown seaweed Ascophyllum nodosum. HeliAnticancer Res. 13:2011-2019.
  12. Heinzelmann, M., Polk, H. C. Jr. & Miller, F. N. 1998. Modulation of lipopolysaccharide-induced monocyte activation by heparin-binding protein and fucoidan. Infect. Immun. 66:5842-5847.
  13. Jiang, Z., Okimura, T., Yamaguchi, K. & Oda, T. 2011. The potent activity of sulfated polysaccharide, ascophyllan, isolated from Ascophyllum nodosum to induce nitric oxide and cytokine production from mouse macrophage RAW264.7 cells: comparison between ascophyllan and fucoidan. Nitric Oxide 25:407-415. https://doi.org/10.1016/j.niox.2011.10.001
  14. Jiang, Z., Okimura, T., Yokose, T., Yamasaki, Y., Yamaguchi, K. & Oda, T. 2010. Effects of sulfated fucan, ascophyllan, from the brown alga Ascophyllum nodosum on various cell lines: a comparative study on ascophyllan and fucoidan. J. Biosci. Bioeng. 110:113-117. https://doi.org/10.1016/j.jbiosc.2010.01.007
  15. Jin, J. -O., Song, M. -G., Kim, Y. -N., Park, J. -I. & Kwak, J. -Y. 2010. The mechanism of fucoidan-induced apoptosis in leukemic cells: involvement of ERK1/2, JNK, glutathione, and nitric oxide. Mol. Carcinog. 49:771-782.
  16. Kang, S. -M., Kim, K. -N., Lee, S. -H., Ahn, G., Cha, S. -H., Kim, A. -D., Yang, X. -D., Kang, M. -C. & Jeon, Y. -J. 2011. Anti-inflammatory activity of polysaccharide purified from AMG-assistant extract of Ecklonia cava in LPS-stimulated RAW 264.7 macrophages. Carbohydr. Polym. 85:80-85. https://doi.org/10.1016/j.carbpol.2011.01.052
  17. Karmakar, P., Pujol, C. A., Damonte, E. B., Ghosh, T. & Ray, B. 2010. Polysaccharides from Padina tetrastromatica: structural features, chemical modification and antiviral activity. Carbohydr. Polym. 80:513-520. https://doi.org/10.1016/j.carbpol.2009.12.014
  18. Kim, E. J., Park, S. Y., Lee, J. -Y. & Park, J. H. 2010. Fucoidan present in brown algae induces apoptosis of human colon cancer cells. BMC Gastroenterol. 10:96. https://doi.org/10.1186/1471-230X-10-96
  19. Kloareg, B., Demarty, M. & Mabeau, S. 1986. Polyanionic characteristics of purified sulphated homofucans from brown algae. Int. J. Biol. Macromol. 8:380-386. https://doi.org/10.1016/0141-8130(86)90060-7
  20. Koyanagi, S., Tanigawa, N., Nakagawa, H., Soeda, S. & Shimeno, H. 2003. Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem. Pharmacol. 65:173-179. https://doi.org/10.1016/S0006-2952(02)01478-8
  21. Kusaykin, M., Bakunina, I., Sova, V., Ermakova, S., Kuznetsova, T., Besednova, N., Zaporozhets, T. & Zvyagintseva, T. 2008. Structure, biological activity, and enzymatic transformation of fucoidans from the brown seaweeds. Biotechnol. J. 3:904-915. https://doi.org/10.1002/biot.200700054
  22. Leiro, J. M., Castro, R., Arranz, J. A. & Lamas, J. 2007. Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh. Int. Immunopharmacol. 7:879-888. https://doi.org/10.1016/j.intimp.2007.02.007
  23. Li, L. -Y., Li, L. -Q. & Guo, C. -H. 2010. Evaluation of in vitro antioxidant and antibacterial activities of Laminaria japonica polysaccharides. J. Med. Plants Res. 4:2194-2198.
  24. Lins, K. O., Bezerra, D. P., Alves, A. P., Alencar, N. M., Lima, M. W., Torres, V. M., Farias, W. R., Pessoa, C., De Moraes, M. O. & Costa- Lotufo, L. V. 2009. Antitumor properties of a sulfated polysaccharide from the red seaweed Champia feldmannii (Diaz-Pifferer). J. Appl. Toxicol. 29:20-26. https://doi.org/10.1002/jat.1374
  25. Lustigman, B. & Brown, C. 1991. Antibiotic production by marine algae isolated from the New York/New Jersey coast. Bull. Environ. Contam. Toxicol. 46:329-335. https://doi.org/10.1007/BF01688928
  26. Medcalf, D. G. & Larsen, B. 1977. Fucose-containing polysaccharides in the brown algae Ascophyllum nodosum and Fucus vesiculosus. Carbohydr. Res. 59:531-537. https://doi.org/10.1016/S0008-6215(00)83190-0
  27. Nagayama, K., Iwamura, Y., Shibata, T., Hirayama, I. & Nakamura, T. 2002. Bactericidal activity of phlorotannins from the brown alga Ecklonia kurome. J. Antimicrob. Chemother. 50:889-893. https://doi.org/10.1093/jac/dkf222
  28. Nakayasu, S., Soegima, R., Yamaguchi, K. & Oda, T. 2009. Biological activities of fucose-containing polysaccharide ascophyllan isolated from the brown alga Ascophyllum nodosum. Biosci. Biotechnol. Biochem. 73:961-964. https://doi.org/10.1271/bbb.80845
  29. Nishino, T., Nishioka, C., Ura, H. & Nagumo, T. 1994. Isolation and partial characterization of a novel amino sugar-containing fucan sulfate from commercial Fucus vesiculosus fucoidan. Carbohydr. Res. 255:213-224. https://doi.org/10.1016/S0008-6215(00)90980-7
  30. Niwano, Y., Sato, E., Kohno, M., Matsuyama, Y., Kim, D. & Oda, T. 2007. Antioxidant properties of aqueous extracts from red tide plankton cultures. Biosci. Biotechnol. Biochem. 71:1145-1153. https://doi.org/10.1271/bbb.60593
  31. Noda, H., Amano, H., Arashima, K. & Nisizawa, K. 1990. Antitumor activity of marine algae. Hydrobiologia 204/205:577-584. https://doi.org/10.1007/BF00040290
  32. Pereira, M. S., Mulloy, B. & Mourao, P. A. 1999. Structure and anticoagulant activity of sulfated fucans: comparison between the regular, repetitive, and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. J. Biol. Chem. 274:7656- 7667. https://doi.org/10.1074/jbc.274.12.7656
  33. Pierre, G., Sopena, V., Juin, C., Mastouri, A., Graber, M. & Maugard, T. 2011. Antibacterial activity of a sulfated galactan extracted from the marine alga Chaetomorpha aerea against Staphylococcus aureus. Biotechnol. Bioprocess. Eng. 16:937-945. https://doi.org/10.1007/s12257-011-0224-2
  34. Raghavendran, H. R., Srinivasan, P. & Rekha, S. 2011. Immunomodulatory activity of fucoidan against aspirin-induced gastric mucosal damage in rats. Int. Immunopharmacol. 11:157-163. https://doi.org/10.1016/j.intimp.2010.11.002
  35. Shibata, H., Kimura-Takagi, I., Nagaoka, M., Hashimoto, S., Sawada, H., Ueyama, S. & Yokokura, T. 1999. Inhibitory effect of Cladosiphon fucoidan on the adhesion of Helicobacter pylori to human gastric cells. J. Nutr. Sci. Vitaminol. (Tokyo) 45:325-336. https://doi.org/10.3177/jnsv.45.325
  36. Sinha, S., Astani, A., Ghosh, T., Schnitzler, P. & Ray, B. 2010. Polysaccharides from Sargassum tenerrimum: structural features, chemical modification and anti-viral activity. Phytochemistry 71:235-242. https://doi.org/10.1016/j.phytochem.2009.10.014
  37. Tissot, B. & Daniel, R. 2003. Biological properties of sulfated fucans: the potent inhibiting activity of algal fucoidan against the human compliment system. Glycobiology 13:29G-30G. https://doi.org/10.1093/glycob/cwg126
  38. Wang, H., Chiu, L. C. M., Ooi, V. E. C. & Ang, P. O. Jr. 2010. A potent antitumor polysaccharide from the edible brown seaweed Hydroclathrus clathratus. Bot. Mar. 53:265-274.
  39. Witvrouw, M. & De Clercq, E. 1997. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen. Pharmacol. Vasc. Syst. 29:497-511. https://doi.org/10.1016/S0306-3623(96)00563-0
  40. Yoon, J. -S., Yadunandam, A. K., Kim, S. -J., Woo, H. -C., Kim, H. -R. & Kim, G. -D. 2013. Dieckol, isolated from Ecklonia stolonifera, induces apoptosis in human hepatocellular carcinoma Hep3B cells. J. Nat. Med. 67:519-527. https://doi.org/10.1007/s11418-012-0709-0

Cited by

  1. Effect of seaweed on gastrointestinal microbiota isolated from Norwegian White sheep vol.66, pp.3, 2016, https://doi.org/10.1080/09064702.2017.1310287
  2. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae vol.32, pp.1, 2017, https://doi.org/10.4490/algae.2017.32.12.1
  3. Potential Antibacterial Activity of Marine Macroalgae against Pathogens Relevant for Aquaculture and Human Health vol.11, pp.4, 2014, https://doi.org/10.22207/jpam.11.4.07
  4. Extraction Improvement of the Bioactive Blue-Green Pigment “Marennine” from Diatom Haslea ostrearia ’s Blue Water: A Solid-Phase Method Based on Graphitic Matrices vol.18, pp.12, 2020, https://doi.org/10.3390/md18120653