DOI QR코드

DOI QR Code

Functions and values of sulfated polysaccharides from seaweed

  • D. P. Nagahawatta (Department of Marine Life Sciences, Jeju National University) ;
  • N. M. Liyanage (Department of Marine Life Sciences, Jeju National University) ;
  • Thilina U. Jayawardena (Department of Chemistry, Biochemistry and Physics, Universite du Quebec a Trois-Rivieres) ;
  • Fengqi Yang (Department of Marine Life Sciences, Jeju National University) ;
  • H. H. A. C. K. Jayawardena (Department of Marine Life Sciences, Jeju National University) ;
  • M. J. M. S. Kurera (Department of Marine Life Sciences, Jeju National University) ;
  • Fahe Wang (State Key Laboratory of Marine Food Processing & Safety Control, Qingdao Bright Moon Seaweed Group Co., Ltd.) ;
  • Xiaoting Fu (College of Food Science and Engineering, Ocean University of China) ;
  • You-Jin Jeon (Department of Marine Life Sciences, Jeju National University)
  • 투고 : 2023.10.30
  • 심사 : 2023.12.01
  • 발행 : 2023.12.21

초록

Sulfated polysaccharides (SPs) isolated from seaweed have emerged as remarkable bioactive compounds with a wide spectrum of biological activities and have substantial value in the scientific and industrial domains. The current study explores the diverse biological activities of SPs and their relationship with their structures. This aids in an in-depth examination of the multifaceted biological activities of SPs, including anticoagulant, anti-inflammatory, antiviral, antioxidant, and immunomodulatory properties, which underpin their potential health benefits. Furthermore, the current study explores the complicated properties of SPs, with their extraction methodologies and techniques for precise characterization. Elucidation of the commercial significance of SPs derived from brown, red, and green seaweed by highlighting their potential applications has emphasized their importance in human well-being. Further, this review emphasizes the challenges needed to overcome research and industrial innovations for SPs. Collaboration among researchers, industry stakeholders, and regulatory authorities can overcome these challenges and elevate the potential of SPs to revolutionize industries such as pharmaceuticals, cosmeceuticals, food, and biotechnology.

키워드

과제정보

This work was supported by the Qingdao International Innovation Cooperation Project for Science and Technology (No. 22-3-6-ghgg-1-hz).

참고문헌

  1. Alboofetileh, M., Rezaei, M. & Tabarsa, M. 2019. Enzyme-assisted extraction of Nizamuddinia zanardinii for the recovery of sulfated polysaccharides with anticancer and immune-enhancing activities. J. Appl. Phycol. 31:1391-1402. https://doi.org/10.1007/s10811-018-1651-7
  2. Ale, M. T., Mikkelsen, J. D. & Meyer, A. S. 2011. Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar. Drugs 9:2106-2130. https://doi.org/10.3390/md9102106
  3. Amorim, R. d. N. d. S., Rodrigues, J. A. G., Holanda, M. L., Quindere, A. L. G., de Paula, R. C. M., Melo, V. M. M. & Benevides, N. M. B. 2012. Antimicrobial effect of a crude sulfated polysaccharide from the red seaweed Gracilaria ornata. Braz. Arch. Biol. Technol. 55:171-181. https://doi.org/10.1590/S1516-89132012000200001
  4. Anisha, G. S., Augustianath, T., Padmakumari, S., Singhania, R. R., Pandey, A. & Patel, A. K. 2023. Ulvan from green macroalgae: bioactive properties advancing tissue engineering, drug delivery systems, food industry, agriculture and water treatment. Bioresour. Technol. Rep. 22:101457.
  5. Anisha, G. S., Padmakumari, S., Patel, A. K., Pandey, A. & Singhania, R. R. 2022. Fucoidan from marine macroalgae: biological actions and applications in regenerative medicine, drug delivery systems and food industry. Bioengineering 9:472.
  6. Apostolova, E., Lukova, P., Baldzhieva, A., Katsarov, P., Nikolova, M., Iliev, I., Peychev, L., Trica, B., Oancea, F., Delattre, C. & Kokova, V. 2020. Immunomodulatory and antiinflammatory effects of fucoidan: a review. Polymers 12:2338.
  7. Barahona, T., Chandia, N. P., Encinas, M. V., Matsuhiro, B. & Zuniga, E. A. 2011. Antioxidant capacity of sulfated polysaccharides from seaweeds: a kinetic approach. Food Hydrocoll. 25:529-535. https://doi.org/10.1016/j.foodhyd.2010.08.004
  8. Bhardwaj, M., Padmavathy, T. K., Mani, S., Malarvizhi, R., Sali, V. K. & Vasanthi, H. R. 2020. Sulfated polysaccharide from Turbinaria ornata suppress lipopolysaccharide-induced inflammatory response in RAW 264.7 macrophages. Int. J. Biol. Macromol. 164:4299-4305. https://doi.org/10.1016/j.ijbiomac.2020.09.036
  9. Blakemore, W. R. & Harpell, A. R. 2009. Carrageenan. In Imeson, A. (Ed.) Food Stabilisers, Thickeners, and Gelling Agents. Blackwell Publishing Ltd., West Sussex, pp. 73-94.
  10. Campbell, R. & Hotchkiss, S. 2017. Carrageenan industry market overview. In Hurtado, A. Q., Critchley, A. T. & Neish, I. C. (Eds.) Tropical Seaweed Farming Trends, Problems and Opportunities: Focus on Kappaphycus and Eucheuma of Commerce. Springer International Publishing, Cham, pp. 193-205.
  11. Chi, Y., Zhang, M., Wang, X., Fu, X., Guan, H. & Wang, P. 2020. Ulvan lyase assisted structural characterization of ulvan from Ulva pertusa and its antiviral activity against vesicular stomatitis virus. Int. J. Biol. Macromol. 157:75-82. https://doi.org/10.1016/j.ijbiomac.2020.04.187
  12. Choi, J.-I. & Kim, H.-J. 2013. Preparation of low molecular weight fucoidan by gamma-irradiation and its anticancer activity. Carbohydr. Polym. 97:358-362. https://doi.org/10.1016/j.carbpol.2013.05.002
  13. Ciancia, M., Quintana, I. & Cerezo, A. S. 2010. Overview of anticoagulant activity of sulfated polysaccharides from seaweeds in relation to their structures, focusing on those of green seaweeds. Curr. Med. Chem. 17:2503-2529. https://doi.org/10.2174/092986710791556069
  14. Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. A., Camara, R. B. G., Nobre, L. T. D. B., Costa, M. S. S. P., Almeida-Lima, J., Farias, E. H. C., Leite, E. L. & Rocha, H. A. O. 2010. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed. Pharmacother. 64:21-28. https://doi.org/10.1016/j.biopha.2009.03.005
  15. da Silva, L. C. R. P., Todaro, V., do Carmo, F. A., Frattani, F. S., de Sousa, V. P., Rodrigues, C. R., Sathler, P. C. & Cabral, L. M. 2018. A promising oral fucoidan-based antithrombotic nanosystem: development, activity and safety. Nanotechnology 29:165102.
  16. de Araujo, I. W. F., Rodrigues, J. A. G., Quindere, A. L. G., de Fatima Teixeira Silva, J., de Freitas Maciel, G., Ribeiro, N. A., de Sousa Oliveira Vanderlei, E., Ribeiro, K. A., Chaves, H. V., Pereira, K. M. A., Bezerra, M. M. & Benevides, N. M. B. 2016. Analgesic and anti-inflammatory actions on bradykinin route of a polysulfated fraction from alga Ulva lactuca. Int. J. Biol. Macromol. 92:820-830. https://doi.org/10.1016/j.ijbiomac.2016.07.094
  17. Delma, C., Ramalingam, K., Pandian, V., Baskar, A., Savarimuthu, I., Thangavelu, B. & Somasundaram, S. 2014. Abstract A4: antagonistic effects of sulphated polysaccharides from Turbinaria conoides (J. Agardh) on tumor cell migration and angiogenesis. Cancer Prev. Res. 1:A4.
  18. Fabrowska, J., Ibanez, E., Leska, B. & Herrero, M. 2016. Supercritical fluid extraction as a tool to valorize underexploited freshwater green algae. Algal Res. 19:237-245. https://doi.org/10.1016/j.algal.2016.09.008
  19. Fernandez-Diaz, C., Coste, O. & Malta, E.-J. 2017. Polymer chitosan nanoparticles functionalized with Ulva ohnoi extracts boost in vitro ulvan immunostimulant effect in Solea senegalensis macrophages. Algal Res. 26:135-142. https://doi.org/10.1016/j.algal.2017.07.008
  20. Fitton, J. H., Stringer, D. N., Park, A. Y. & Karpiniec, S. S. 2019. Therapies from fucoidan: new developments. Mar. Drugs 17:571.
  21. Florez-Fernandez, N., Rodriguez-Coello, A., Latire, T., Bourgougnon, N., Torres, M. D., Bujan, M., Muinos, A., Muinos, A., Meijide-Failde, R., Blanco, F. J., Vaamonde-Garcia, C. & Dominguez, H. 2023. Anti-inflammatory potential of ulvan. Int. J. Biol. Macromol. 253:126936.
  22. Gereniu, C. R. N., Saravana, P. S. & Chun, B.-S. 2018. Recovery of carrageenan from Solomon Islands red seaweed using ionic liquid-assisted subcritical water extraction. Sep. Purif. Technol. 196:309-317. https://doi.org/10.1016/j.seppur.2017.06.055
  23. Hans, N., Malik, A. & Naik, S. 2021. Antiviral activity of sulfated polysaccharides from marine algae and its application in combating COVID-19: mini review. Bioresour. Technol. Rep. 13:100623.
  24. Hayashi, K., Nakano, T., Hashimoto, M., Kanekiyo, K. & Hayashi, T. 2008. Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection. Int. Immunopharmacol. 8:109-116. https://doi.org/10.1016/j.intimp.2007.10.017
  25. Hotchkiss, S., Brooks, M., Campbell, R., Philp, K. & Trius, A. 2016. The use of carrageenan in food. In Pereira, L. (Ed.) Carrageenans: Sources and Extraction Methods, Molecular Structure, Bioactive Properties and Health Effects. Nova Science Publishers, New York, NY, pp. 229-243.
  26. Huang, L., Shen, M., Morris, G. A. & Xie, J. 2019. Sulfated polysaccharides: immunomodulation and signaling mechanisms. Trends Food Sci. Technol. 92:1-11. https://doi.org/10.1016/j.tifs.2019.08.008
  27. Hwang, E. K., Boo, G. H., Graf, L., Yarish, C., Yoon, H. S. & Kim, J. K. 2022. Kelps in Korea: from population structure to aquaculture to potential carbon sequestratio. Algae 37:85-103. https://doi.org/10.4490/algae.2022.37.3.3
  28. Ibrahim, M. I. A., Amer, M. S., Ibrahim, H. A. H. & Zaghloul, E. H. 2022. Considerable production of ulvan from Ulva lactuca with special emphasis on its antimicrobial and anti-fouling properties. Appl. Biochem. Biotechnol. 194:3097-3118. https://doi.org/10.1007/s12010-022-03867-y
  29. Imeson, A. P. 2009. Carrageenan and furcellaran. In Phillips, G. O. & Williams, P. A. (Eds.) Handbook of Hydrocolloids. 2nd ed. Woodhead Publishing, Cambridge, pp. 164-185.
  30. Jaulneau, V., Lafitte, C., Jacquet, C., Fournier, S., Salamagne, S., Briand, X., Esquerre-Tugaye, M.-T. & Dumas, B. 2010. Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic scid signaling pathway. J. Biotechnol. 2010:525291.
  31. Jayasinghe, P. S., Pahalawattaarachchi, V. & Ranaweera, K. K. D. S. 2016. Effect of extraction methods on the yield and physiochemical properties of polysaccharides extracted from seaweed available in Sri Lanka. Poult. Fish. Wildl. Sci. 4:1.
  32. Jayawardena, T. U., Nagahawatta, D. P., Fernando, I. P. S., Kim, Y.-T., Kim, J.-S., Kim, W.-S., Lee, J. S. & Jeon, Y.-J. 2022. A review on fucoidan structure, extraction techniques, and its role as an immunomodulatory agent. Mar. Drugs 20:755.
  33. Jayawardena, T. U., Sanjeewa, K. K. A., Lee, H.-G., Nagaha-watta, D. P., Yang, H.-W., Kang, M.-C. & Jeon, Y.-J. 2020a. Particulate matter-induced inflammation/oxidative stress in macrophages: fucosterol from Padina boryana as a potent protector, activated via NF-κB/MAPK pathways and Nrf2/HO-1 involvement. Mar. Drugs 18:628.
  34. Jayawardena, T. U., Sanjeewa, K. K. A., Nagahawatta, D. P., Lee, H.-G., Lu, Y.-A., Vaas, A. P. J. P., Abeytunga, D. T. U., Nanayakkara, C. M., Lee, D.-S. & Jeon, Y.-J. 2020b. Anti-inflammatory effects of sulfated polysaccharide from Sargassum swartzii in macrophages via blocking TLR/NF-Κb signal transduction. Mar. Drugs 18:601. https://doi.org/10.3390/md18120601
  35. Jayawardhana, H. H. A. C. K., Lee, H.-G., Liyanage, N. M., Nagahawatta, D. P., Ryu, B. & Jeon, Y.-J. 2023. Structural characterization and anti-inflammatory potential of sulfated polysaccharides from Scytosiphon lomentaria: attenuate inflammatory signaling pathways. J. Funct. Foods 102:105446.
  36. Jiksing, C., Ongkudon, M. M., Thien, V. Y., Rodrigues, K. F. & Yong, W. T. L. 2022. Recent advances in seaweed seedling production: a review of eucheumatoids and other valuable seaweeds. Algae 37:105-121. https://doi.org/10.4490/algae.2022.37.5.11
  37. Karnjanapratum, S. & You, S. 2011. Molecular characteristics of sulfated polysaccharides from Monostroma nitidum and their in vitro anticancer and immunomodulatory activities. Int. J. Biol. Macromol. 48:311-318. https://doi.org/10.1016/j.ijbiomac.2010.12.002
  38. Kidgell, J. T., Glasson, C. R. K., Magnusson, M., Vamvounis, G., Sims, I. M., Carnachan, S. M., Hinkley, S. F. R., Lopata, A. L., de Nys, R. & Taki, A. C. 2020. The molecular weight of ulvan affects the in vitro inflammatory response of a murine macrophage. Int. J. Biol. Macromol. 150:839-848. https://doi.org/10.1016/j.ijbiomac.2020.02.071
  39. Kikionis, S., Koromvoki, M., Tagka, A., Polichronaki, E., Stratigos, A., Panagiotopoulos, A., Kyritsi, A., Karalis, V., Vitsos, A., Rallis, M., Ioannou, E. & Roussis, V. 2022. Ulvan-based nanofibrous patches enhance wound healing of skin trauma resulting from cryosurgical treatment of keloids. Mar. Drugs 20:551.
  40. Knoop, J., Barrento, S., Lewis, R., Walter, B. & Griffin, J. N. 2022. Incorporating concepts of biodiversity into modern aquaculture: macroalgal species richness enhances bioremediation efficiency in a lumpfish hatchery. Algae 37:213-226. https://doi.org/10.4490/algae.2022.37.5.12
  41. Lahaye, M. & Robic, A. 2007. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765-1774. https://doi.org/10.1021/bm061185q
  42. Lee, H.-G., Nagahawatta, D. P., Liyanage, N. M., Jayawardhana, H. H. A. C. K., Yang, F., Je, J.-G., Kang, M.-C., Kim, H.-S. & Jeon, Y.-J. 2022. Structural characterization and anti-inflammatory activity of fucoidan isolated from Ecklonia maxima stipe. Algae 37:239-247. https://doi.org/10.4490/algae.2022.37.9.12
  43. Lee, J.-B., Yamagaki, T., Maeda, M. & Nakanishi, H. 1998. Rhamnan sulfate from cell walls of Monostroma latissimum. Phytochemistry 48:921-925. https://doi.org/10.1016/S0031-9422(97)00927-8
  44. Li, Q., Wang, X., Wan, Y., Hu, X., Liu, J. & Wang, J. 2023. In vivo immunomodulatory activity offucoidan from brown alga Undaria pinnatifida in sarcoma 180-bearing mice. J. Funct. Foods 103:105486.
  45. Li, R., Zhou, Q.-L., Chen, S.-T., Tai, M.-R., Cai, H.-Y., Ding, R., Liu, X.-F., Chen, J.-P., Luo, L.-X. & Zhong, S.-Y. 2022. Chemical characterization and immunomodulatory activity of fucoidan from Sargassum hemiphyllum. Mar. Drugs 21:18.
  46. Li, W., Jiang, N., Li, B., Wan, M., Chang, X., Liu, H., Zhang, L., Yin, S., Qi, H. & Liu, S. 2018. Antioxidant activity of purified ulvan in hyperlipidemic mice. Int. J. Biol. Macromol. 113:971-975. https://doi.org/10.1016/j.ijbiomac.2018.02.104
  47. Lin, Y., Qi, X., Liu, H., Xue, K., Xu, S. & Tian, Z. 2020. The anticancer effects of fucoidan: a review of both in vivo and in vitro investigations. Cancer Cell Int. 20:154.
  48. Little, S. M., Senhorinho, G. N. A., Saleh, M., Basiliko, N. & Scott, J. A. 2021. Antibacterial compounds in green microalgae from extreme environments: a review. Algae 36:61-72. https://doi.org/10.4490/algae.2021.36.3.6
  49. Liyanage, N. M., Nagahawatta, D. P., Jayawardena, T. U. & Jeon, Y.-J. 2023a. The role of seaweed polysaccharides in gastrointestinal health: protective effect against inflammatory bowel disease. Life 13:1026.
  50. Liyanage, N. M., Nagahawatta, D. P., Jayawardena, T. U., Sanjeewa, K. K. A., Jayawrdhana, H. H. A. C. K., Kim, J.-I. & Jeon, Y.-J. 2023b. Sulfated polysaccharides from seaweeds: a promising strategy for combatting viral diseases. A review. Mar. Drugs 21:461.
  51. Luning, K. & Pang, S. 2003. Mass cultivation of seaweeds: current aspects and approaches. J. Appl. Phycol. 15:115-119. https://doi.org/10.1023/A:1023807503255
  52. Lu, W., Yang, Z., Chen, J., Wang, D. & Zhang, Y. 2021. Recent advances in antiviral activities and potential mechanisms of sulfated polysaccharides. Carbohydr. Polym. 272:118526.
  53. Manikandan, R., Parimalanandhini, D., Mahalakshmi, K., Beulaja, M., Arumugam, M., Janarthanan, S., Palanisamy, S., You, S. & Prabhu, N. M. 2020. Studies on isolation, characterization of fucoidan from brown algae Turbinaria decurrens and evaluation of it's in vivo and in vitro anti-inflammatory activities. Int. J. Biol. Macromol. 160:1263-1276. https://doi.org/10.1016/j.ijbiomac.2020.05.152
  54. Maray, S. O., Abdel-Kareem, M. S. M., Mabrouk, M. E. M., El-Halmouch, Y. & Makhlof, M. E. M. 2023. In vitro assessment of antiviral, antimicrobial, antioxidant and anticancer activities of ulvan extracted from the green sea-weed Ulva lactuca. Thalassas Int. J. Mar. Sci. 39:779-790. https://doi.org/10.1007/s41208-023-00584-z
  55. Mauray, S., Sternberg, C., Theveniaux, J., Millet, J., Sinquin, C., Tapon-Bretaudiere, J. & Fischer, A. M. 1995. Venous antithrombotic and anticoagulant activities of a fucoidan fraction. Thromb. Haemost. 74:1280-1285. https://doi.org/10.1055/s-0038-1649927
  56. Moawad, M. N., El-Sayed, A. A. M., Abd El Latif, H. H., ElNaggar, N. A., El-Din, N. G. S. & Tadros, H. R. Z. 2022. Chemical characterization and biochemical activity of polysaccharides isolated from Egyptian Ulva fasciata Delile. Oceanologia 64:117-130. https://doi.org/10.1016/j.oceano.2021.09.008
  57. Moran-Santibanez, K., Cruz-Suarez, L. E., Ricque-Marie, D., Robledo, D., Freile-Pelegrin, Y., Pena-Hernandez, M. A., Rodriguez-Padilla, C. & Trejo-Avila, L. M. 2016. Synergistic effects of sulfated polysaccharides from Mexican seaweeds against measles virus. Biomed Res. Int. 2016:8502123.
  58. Muthukumar, J., Chidambaram, R. & Sukumaran, S. 2021. Sulfated polysaccharides and its commercial applications in food industries: a review. J. Food Sci. Technol. 58:2453-2466. https://doi.org/10.1007/s13197-020-04837-0
  59. Nagahawatta, D., Sanjeewa, K. K. A., Jayawardena, T. U., Kim, H.-S., Yang, H.-W., Jiang, Y., Je, J.-G., Lee, T.-K. & Jeon, Y.-J. 2021. Drying seaweeds using hybrid hot water Goodle dryer (HHGD): comparison with freeze-dryer in chemical composition and antioxidant activity. Fish Aquat Sci. 24:19-31. https://doi.org/10.47853/FAS.2021.e3
  60. Nagahawatta, D. P., Liyanage, N. M., Jayawardhana, H. H. A. C. K., Lee, H.-G., Jayawardena, T. U. & Jeon, Y.-J. 2022. Anti-fine dust effect of fucoidan extracted from Ecklonia maxima leaves in macrophages via inhibiting inflammatory signaling pathways. Mar. Drugs 20:413.
  61. Ortega-Barria, E. & Boothroyd, J. C. 1999. A toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J. Biol. Chem. 274:1267-1276. https://doi.org/10.1074/jbc.274.3.1267
  62. Palanisamy, S., Vinosha, M., Marudhupandi, T., Rajasekar, P. & Prabhu, N. M. 2017. Isolation of fucoidan from Sargassum polycystum brown algae: structural characterization, in vitro antioxidant and anticancer activity. Int. J. Biol. Macromol. 102:405-412. https://doi.org/10.1016/j.ijbiomac.2017.03.182
  63. Park, H. Y., Han, M. H., Park, C., Jin, C.-Y., Kim, G.-Y., Choi, I.-W., Kim, N. D., Nam, T.-J., Kwon, T. K. & Choi, Y. H. 2011. Anti-inflammatory effects of fucoidan through inhibition of NF-κB, MAPK and Akt activation in lipopoly-saccharide-induced BV2 microglia cells. Food Chem. Toxicol. 49:1745-1752. https://doi.org/10.1016/j.fct.2011.04.020
  64. Piriz, M. L., Eyras, M. C. & Rostagno, C. M. 2003. Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia. J. Appl. Phycol. 15:67-74. https://doi.org/10.1023/A:1022959005072
  65. Pradhan, B., Patra, S., Nayak, R., Behera, C., Dash, S. R., Nayak, S., Sahu, B. B., Bhutia, S. K. & Jena, M. 2020. Multifunctional role of fucoidan, sulfated polysaccharides in human health and disease: a journey under the sea in pursuit of potent therapeutic agents. Int. J. Biol. Macromol. 164:4263-4278. https://doi.org/10.1016/j.ijbiomac.2020.09.019
  66. Rodriguez-Jasso, R. M., Mussatto, S. I., Pastrana, L., Aguilar, C. N. & Teixeira, J. A. 2011. Microwave-assisted extraction of sulfated polysaccharides (fucoidan) from brown seaweed. Carbohydr. Polym. 86:1137-1144. https://doi.org/10.1016/j.carbpol.2011.06.006
  67. Salehi, B., Sharifi-Rad, J., Seca, A. M. L., Pinto, D. C. G. A., Michalak, I., Trincone, A., Mishra, A. P., Nigam, M., Zam, W. & Martins, N. 2019. Current trends on seaweeds: looking at chemical composition, phytopharmacology, and cosmetic applications. Molecules 24:4182.
  68. Sanchez, R. A. R., Matulewicz, M. C. & Ciancia, M. 2022. NMR spectroscopy for structural elucidation of sulfated polysaccharides from red seaweeds. Int. J. Biol. Macromol. 199:386-400. https://doi.org/10.1016/j.ijbiomac.2021.12.080
  69. Saravana, P. S., Cho, Y.-N., Patil, M. P., Cho, Y.-J., Kim, G.-D., Park, Y. B., Woo, H.-C. & Chun, B.-S. 2018. Hydrothermal degradation of seaweed polysaccharide: characterization and biological activities. Food Chem. 268:179-187. https://doi.org/10.1016/j.foodchem.2018.06.077
  70. Shao, P., Chen, M., Pei, Y. & Sun, P. 2013. In intro antioxidant activities of different sulfated polysaccharides from chlorophytan seaweeds Ulva fasciata. Int. J. Biol. Macromol. 59:295-300. https://doi.org/10.1016/j.ijbiomac.2013.04.048
  71. Shen, P., Yin, Z., Qu, G. & Wang, C. 2018. Fucoidan and its health benefits. In Qin, Y. (Ed.) Bioactive Seaweeds for Food Applications. Academic Press, London, pp. 223-238.
  72. Snethlage, J. S., de Koning, S., Giesbers, E., Veraart, J. A., Debrot, A. O., Harkes, I., van den Burg, S. W. K. & Hamon, K. G. 2023. Knowledge needs in realising the full potential of seaweed for world food provisioning. Glob. Food Sec. 37:100692.
  73. Song, Y., He, P., Rodrigues, A. L., Datta, P., Tandon, R., Bates, J. T., Bierdeman, M. A., Chen, C., Dordick, J., Zhang, F. & Linhardt, R. J. 2021. Anti-SARS-CoV-2 activity of rhamnan sulfate from Monostroma nitidum. Mar. Drugs 19:685.
  74. Therkelsen, G. H. 1993. Carrageenan. In Whistler, R. L. & Bemiller, J. N. (Eds.) Industrial Gums. 3rd ed. Academic Press, London, pp. 145-180.
  75. Tran, T. T. V., Truong, H. B., Tran, N. H. V., Quach, T. M. T., Nguyen, T. N., Bui, M. L., Yuguchi, Y. & Thanh, T. T. T. 2018. Structure, conformation in aqueous solution and antimicrobial activity of ulvan extracted from green seaweed Ulva reticulata. Nat. Prod. Res. 32:2291-2296. https://doi.org/10.1080/14786419.2017.1408098
  76. Tziveleka, L.-A., Pippa, N., Ioannou, E., Demetzos, C. & Roussis, V. 2022. Development of ulvan-containing liposomes as antibacterial drug delivery platforms. J. Funct. Biomater. 13:186.
  77. Usov, A. I. 1992. Sulfated polysaccharides of the red seaweeds. Food Hydrocoll. 6:9-23. https://doi.org/10.1016/S0268-005X(09)80055-6
  78. Venkatesan, J., Singh, S. K., Anil, S., Kim, S.-K. & Shim, M. S. 2018. Preparation, characterization and biological applications of biosynthesized silver nanoparticles with chitosan-fucoidan coating. Molecules 23:1429.
  79. Wang, J., Zhang, Q., Zhang, Z. & Li, Z. 2008. Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int. J. Biol. Macromol. 42:127-132. https://doi.org/10.1016/j.ijbiomac.2007.10.003
  80. Wang, L., Oh, J.-Y., Kim, Y.-S., Lee, H.-G., Lee, J.-S. & Jeon, Y.-J. 2020. Anti-photoaging and anti-melanogenesis effects of fucoidan isolated from Hizikia fusiforme and its underlying mechanisms. Mar. Drugs 18:427. https://doi.org/10.3390/md18080427
  81. Wei, Q., Fu, G., Wang, K., Yang, Q., Zhao, J., Wang, Y., Ji, K. & Song, S. 2022. Advances in research on antiviral activities of sulfated polysaccharides from seaweeds. Pharmaceuticals 15:581.
  82. Weiner, M. L. 2014. Food additive carrageenan: part II: a critical review of carrageenan in vivo safety studies. Crit. Rev. Toxicol. 44:244-269. https://doi.org/10.3109/10408444.2013.861798
  83. Wiencke, C. & Bischof, K. 2012. Seaweed biology. Vol. 219. Springer, Heidelberg, 507 pp.
  84. Wijesinghe, W. A. J. P. & Jeon, Y.-J. 2012. Biological activities and potential industrial applications of fucose rich sulfated polysaccharides and fucoidans isolated from brown seaweeds: a review. Carbohydr. Polym. 88:13-20. https://doi.org/10.1016/j.carbpol.2011.12.029
  85. Wu, G.-J., Shiu, S.-M., Hsieh, M.-C. & Tsai, G.-J. 2016. Anti-inflammatory activity of a sulfated polysaccharide from the brown alga Sargassum cristaefolium. Food Hydrocoll. 53:16-23. https://doi.org/10.1016/j.foodhyd.2015.01.019
  86. Yang, M. Y. & Kim, M. S. 2022. Phylogeography of the economic seaweeds Chondrus (Gigartinales, Rhodophyta) in the northwest Pacific based on rbcL and COI-5P genes. Algae 37:135-147. https://doi.org/10.4490/algae.2022.37.5.29
  87. Yoo, H. J., You, D.-J. & Lee, K.-W. 2019. Characterization and immunomodulatory effects of high molecular weight fucoidan fraction from the sporophyll of Undaria pinnatifida in cyclophosphamide-induced immunosuppressed mice. Mar. Drugs 17:447.
  88. Zayed, A., Avila-Peltroche, J., El-Aasr, M. & Ulber, R. 2022. Sulfated galactofucans: an outstanding class of fucoidans with promising bioactivities. Mar. Drugs 20:412.
  89. Zhang, L., Wang, X., Hua, Q., Wang, J., Liu, J. & Yang, Y. 2020. Synthesis and immunomodulatory activity of the sulfated tetrasaccharide motif of type B ulvanobiuronic acid 3-sulfate. Org. Biomol. Chem. 18:7932-7935. https://doi.org/10.1039/D0OB01852J
  90. Zhao, X., Guo, F., Hu, J., Zhang, L., Xue, C., Zhang, Z. & Li, B. 2016. Antithrombotic activity of oral administered low molecular weight fucoidan from Laminaria japonica. Thromb. Res. 144:46-52. https://doi.org/10.1016/j.thromres.2016.03.008
  91. Zhao, Y., Zheng, Y., Wang, J., Ma, S., Yu, Y., White, W. L., Yang, S., Yang, F. & Lu, J. 2018. Fucoidan extracted from Undaria pinnatifida: source for nutraceuticals/functional foods. Mar. Drugs 16:321.