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Structural tailoring of fucoidan backbones for maximizing their benefits: Enzymatic, chemical, and physical strategies

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A Correction to this article was published on 07 March 2024

This article has been updated

Abstract

Fucoidans are a heterogenous class of sulfated, fucose-rich, and high molecular weight polysaccharides derived mainly from brown seaweeds. They have attracted particular interest in different scientific and industrial fields. Nevertheless, their applications are affected by various chemical properties, including molecular weight, sulfation pattern, and degree of sulphation. For instance, most of the reported bioactivities (e.g., immunomodulatory and cytotoxic activities) have been enhanced with more sulfated and low molecular weight fractions, in contrast to the anticoagulant effect. Additionally, high molecular weight fucoidans are unsuitable for nanomedicine formulation, oral absorption, and distribution to various body organs. Hence, different strategies have been developed as a subsequent stage of processing to modify the native fucoidans in order to produce more bioactive and efficiently formulated products. The current article highlights the various enzymatic (e.g., fucoidanase and fucoidan sulfatase), chemical, and other strategies used for structural modifications of native fucoidans accompanied by varied bioactivities. Interestingly, the enzymatic method has proved to be more specific and selective retaining the native sulfated chemical backbone efficiently. Hence, this review may help in tayloring new fucoidan derivatives for targeted homogenous production and maximized applications of fucoidans in the medical and pharmaceutical fields.

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Data Availability

The data is available from the corresponding author on request.

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References

  • Abdelkader DH, Elekhnawy E, Negm WA, El-Masry TA, Almukainzi M, Zayed A, Ulber R (2022) Insight into fucoidan-based PEGylated PLGA nanoparticles encapsulating methyl anthranilic acid: In vitro evaluation and in vivo anti-inflammatory study. Mari Drugs 20:694

    CAS  Google Scholar 

  • Ale MT, Mikkelsen JD, Meyer AS (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anastyuk SD, Shevchenko NM, Dmitrenok PS, Zvyagintseva TN (2011) Investigation of a sulfate transfer during autohydrolysis of a fucoidan from the brown alga Fucus evanescens by tandem ESIMS. Carbohydr Res 346:2975–2977

    CAS  PubMed  Google Scholar 

  • Anastyuk SD, Shevchenko NM, Nazarenko EL, Imbs TI, Gorbach VI, Dmitrenok PS, Zvyagintseva TN (2010) Structural analysis of a highly sulfated fucan from the brown alga Laminaria cichorioides by tandem MALDI and ESI mass spectrometry. Carbohydr Res 345:2206–2212

    CAS  PubMed  Google Scholar 

  • Anastyuk SD, Shevchenko NM, Usoltseva RV, Silchenko AS, Zadorozhny PA, Dmitrenok PS, Ermakova SP (2017) Structural features and anticancer activity in vitro of fucoidan derivatives from brown alga Saccharina cichorioides. Carbohydr Polym 157:1503–1510

    CAS  PubMed  Google Scholar 

  • Anisimova NY, Ustyuzhanina NE, Bilan MI, Donenko FV, Ushakova NA, Usov AI, Kiselevskiy MV, Nifantiev NE (2018) Influence of modified fucoidan and related sulfated oligosaccharides on hematopoiesis in cyclophosphamide-induced mice. Mar Drugs 16:333

    PubMed  PubMed Central  Google Scholar 

  • 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 anti-inflammatory effects of fucoidan: A review. Polymers 12:2338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arafuka S, Koshiba N, Takahashi D, Toshima K (2014) Systematic synthesis of sulfated oligofucosides and their effect on breast cancer MCF-7 cells. Chem Commun 50:9831–9834

    CAS  Google Scholar 

  • Arai Y, Shingu Y, Yagi H, Suzuki H, Ohshiro T (2022) Occurrence of different fucoidanase genes in Flavobacterium sp. SW and enzyme characterization. J Biosc Bioeng 134:187–194

    CAS  Google Scholar 

  • Bakunina IY, Nedashkovskaya OI, Alekseeva SA, Ivanova EP, Romanenko LA, Gorshkova NM, Isakov VV, Zvyagintseva TN, Mikhailov VV (2002) degradation of fucoidan by the marine proteobacterium Pseudoalteromonas citrea. Microbiology 71:41–47

    CAS  Google Scholar 

  • Bakunina IY, Shevchenko LS, Nedashkovskaya OI, Shevchenko NM, Alekseeva SA, Mikhailov VV, Zvyagintseva TN (2000) Screening of marine bacteria for fucoidanases. Microbiology 69:303–308

    CAS  Google Scholar 

  • Balboa EM, Rivas S, Moure A, Domínguez H, Parajó JC (2013) Simultaneous extraction and depolymerization of fucoidan from Sargassum muticum in aqueous media. Mar Drugs 11:4612–4627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bäumgen M, Dutschei T, Bornscheuer UT (2021) Marine polysaccharides: occurrence, enzymatic degradation and utilization. ChemBioChem 22:2247–2256

    PubMed  PubMed Central  Google Scholar 

  • Benslima A, Sellimi S, Hamdi M, Nasri R, Jridi M, Cot D, Li S, Nasri M, Zouari N (2021) Brown seaweed Cystoseira schiffneri as a promising source of sulfated fucans: Seasonal variability of structural, chemical, and antioxidant properties. Food Sci Nutr 9:1551–1563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bilan MI, Kusaykin MI, Grachev AA, Tsvetkova EA, Zvyagintseva TN, Nifantiev NE, Usov AI (2005) Effect of enzyme preparation from the marine mollusk Littorina kurila on fucoidan from the brown alga Fucus distichus. Biochemistry 70:1321–1326

    CAS  PubMed  Google Scholar 

  • Bilan MI, Ustyuzhanina NE, Shashkov AS, Thanh TTT, Bui ML, Tran TTV, Bui VN, Nifantiev NE, Usov AI (2018) A sulfated galactofucan from the brown alga Hormophysa cuneiformis (Fucales, Sargassaceae). Carbohydr Res 469:48–54

    CAS  PubMed  Google Scholar 

  • Bilan MI, Ustyuzhanina NE, Shashkov AS, Thanh TTT, Bui ML, Tran TTV, Bui VN, Usov AI (2017) Sulfated polysaccharides of the Vietnamese brown alga Sargassum aquifolium (Fucales, Sargassaceae). Carbohydr Res 449:23–31

    CAS  PubMed  Google Scholar 

  • Borazjani NJ, Tabarsa M, You S, Rezaei M (2017) Improved immunomodulatory and antioxidant properties of unrefined fucoidans from Sargassum angustifolium by hydrolysis. J Food Sci Technol 54:4016–4025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao HTT, Mikkelsen MD, Lezyk MJ, Bui LM, Tran VTT, Silchenko AS, Kusaykin MI, Pham TD, Truong BH, Holck J, Meyer AS (2018) Novel enzyme actions for sulphated galactofucan depolymerisation and a new engineering strategy for molecular stabilisation of fucoidan degrading enzymes. Mar Drugs 16:422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L-M, Liu P-Y, Chen Y-A, Tseng H-Y, Shen P-C, Hwang P-A, Hsu H-L (2017) Oligo-fucoidan prevents IL-6 and CCL2 production and cooperates with p53 to suppress ATM signaling and tumor progression. Sci Rep 7:11864

    ADS  PubMed  PubMed Central  Google Scholar 

  • Chen MC, Hsu WL, Hwang PA, Chou TC (2015) Low molecular weight fucoidan inhibits tumor angiogenesis through downregulation of HIF-1/VEGF signaling under hypoxia. Mar Drugs 13:4436–4451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Ni L, Fu X, Wang L, Duan D, Huang L, Xu J, Gao X (2021) Molecular mechanism of anti-inflammatory activities of a novel sulfated galactofucan from Saccharina japonica. Mar Drugs 19:430

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chevolot L, Foucault A, Chaubet F, Kervarec N, Sinquin C, Fisher A-M, Boisson-Vidal C (1999) Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity. Carbohydr Res 319:154–165

    CAS  PubMed  Google Scholar 

  • Chevolot L, Mulloy B, Ratiskol J, Foucault A, Colliec-Jouault S (2001) A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr Res 330:529–535

    CAS  PubMed  Google Scholar 

  • Cho ML, Lee BY, You SG (2010) Relationship between oversulfation and conformation of low and high molecular weight fucoidans and evaluation of their in vitro anticancer activity. Molecules 16:291–297

    PubMed  PubMed Central  Google Scholar 

  • Choi J-i, Gu Lee S, Jong Han S, Cho M, Cheon Lee P (2014) Effect of gamma irradiation on the structure of fucoidan. Radiat Phys Chem 100:54–58

    ADS  CAS  Google Scholar 

  • Choi JI, Kim HJ (2013) Preparation of low molecular weight fucoidan by gamma-irradiation and its anticancer activity. Carbohydr Polym 97:358–362

    CAS  PubMed  Google Scholar 

  • Chollet L, Saboural P, Chauvierre C, Villemin JN, Letourneur D, Chaubet F (2016) Fucoidans in nanomedicine. Mar Drugs 14:145

    PubMed  PubMed Central  Google Scholar 

  • Colin S, Deniaud E, Jam M, Descamps V, Chevolot Y, Kervarec N, Yvin J-C, Barbeyron T, Michel G, Kloareg B (2006) Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology 16:1021–1032

    CAS  PubMed  Google Scholar 

  • Cunha L, Grenha A (2016) Sulfated seaweed polysaccharides as multifunctional materials in drug delivery applications. Mar Drugs 14:42

    PubMed  PubMed Central  Google Scholar 

  • da Silva LCRP, Todaro V, do Carmo FA, Frattani FS, de Sousa VP, Rodrigues CR, Sathler PC, Cabral LM (2018) A promising oral fucoidan-based antithrombotic nanosystem: Development, activity and safety. Nanotechnology 29:165102

  • de Jesus Raposo MF, de Morais AM, de Morais RM (2015) Marine polysaccharides from algae with potential biomedical applications. Mar Drugs 13:2967–3028

    PubMed  PubMed Central  Google Scholar 

  • Descamps V, Colin S, Lahaye M, Jam M, Richard C, Potin P, Barbeyron T, Yvin JC, Kloareg B (2006) Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar Biotechnol 8:27–39

    CAS  Google Scholar 

  • Ermakova SP, Menshova RV, Anastyuk SD, Malyarenko OS, Zakharenko AM, Thinh PD, Ly BM, Zvyagintseva TN (2016) Structure, chemical and enzymatic modification, and anticancer activity of polysaccharides from the brown alga Turbinaria ornata. J Appl Phycol 28:2495–2505

    CAS  Google Scholar 

  • Etman SM, Elnaggar YSR, Abdallah OY (2020) Fucoidan, a natural biopolymer in cancer combating: From edible algae to nanocarrier tailoring. Int J Biol Macromol 147:799–808

    CAS  PubMed  Google Scholar 

  • Flórez-Fernández N, Torres MD, González-Muñoz MJ, Domínguez H (2018) Potential of intensification techniques for the extraction and depolymerization of fucoidan. Algal Res 30:128–148

    Google Scholar 

  • Furukawa S-I, Fujikawa T, Koga D, A I (1992a) Production of fucoidan-degrading enzymes, fucoidanase, and fucoidan sulfatase by Vibrio sp. N-5. Nippon Suisan Gakkaishi 58:1499–1503

  • Furukawa S-i, Fujikawa T, Koga D, Ide A (1992b) Purification and Some properties of exo-type fucoidanases from Vibrio sp. N-5. Biosci Biotech Biochem 56:1829–1834

  • Gao L, Xu C, Tao X, Zuo Z, Ning Z, Wang L, Zhao J (2022) Structure elucidation of fucan sulfate from sea cucumber Holothuria fuscopunctata through a bottom-up strategy and the antioxidant activity analysis. Int J Mol Sci 23:4488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghebouli R, Loyau S, Maire M, Saboural P, Collet JP, Jandrot-Perrus M, Letourneur D, Chaubet F, Michel JB (2018) Amino-fucoidan as a vector for rtPA-induced fibrinolysis in experimental thrombotic events. Thromb Haemost 118:42–53

    PubMed  Google Scholar 

  • Guo X, Ye X, Sun Y, Wu D, Wu N, Hu Y, Chen S (2014) Ultrasound effects on the degradation kinetics, structure, and antioxidant activity of sea cucumber fucoidan. J Agric Food Chem 62:1088–1095

    CAS  PubMed  Google Scholar 

  • Hahn T, Lang S, Ulber R, Muffler K (2012) Novel procedures for the extraction of fucoidan from brown algae. Process Biochemy 47:1691–1698

    CAS  Google Scholar 

  • Hanisch FG, Aydogan C, Schroten H (2021) Fucoidan and derived oligo-fucoses: structural features with relevance in competitive inhibition of gastrointestinal norovirus binding. Mar Drugs 19:591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haroun-Bouhedja F, Ellouali M, Sinquin C, Boisson-Vidal C (2000) Relationship between sulfate groups and biological activities of fucans. Thrombosis Res 100:453–459

    CAS  Google Scholar 

  • Hentati F, Tounsi L, Djomdi D, Pierre G, Delattre C, Ursu AV, Fendri I, Abdelkafi S, Michaud P (2020) Bioactive polysaccharides from seaweeds. Molecules 25:3152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holtkamp AD, Kelly S, Ulber R, Lang S (2009) Fucoidans and fucoidanases-focus on techniques for molecular structure elucidation and modification of marine polysaccharides. Appl Microbiol Biotechnol 82:1–11

    CAS  PubMed  Google Scholar 

  • Hou Y, Wang J, Jin W, Zhang H, Zhang Q (2012) Degradation of Laminaria japonica fucoidan by hydrogen peroxide and antioxidant activities of the degradation products of different molecular weights. Carbohydr Polym 87:153–159

    CAS  PubMed  Google Scholar 

  • Hsiao HH, Wu TC, Tsai YH, Kuo CH, Huang RH, Hong YH, Huang CY (2021) Effect of oversulfation on the composition, structure, and in vitro anti-lung cancer activity of fucoidans extracted from Sargassum aquifolium. Mar Drugs 19:215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu S, Chen S, Zhu H, Du M, Jiang W, Liu Y, Gao X, Su L, Xu Y (2021) Low molecular weight, 4-O-sulfation, and sulfation at meta-fucose positively promote the activities of sea cucumber fucoidans on improving insulin resistance in HFD-fed mice. Mar Drugs 20:37

  • Huang Y-C, Li R-Y (2014) Preparation and characterization of antioxidant nanoparticles composed of chitosan and fucoidan for antibiotics delivery. Mar Drugs 12:4379–4398

    CAS  Google Scholar 

  • Imbs TI, Shevchenko NM, Semenova TL, Sukhoverkhov SV, Zvyagintseva TN (2011) Compositional heterogeneity of sulfated polysaccharides synthesized by the brown alga Costaria costata. Chem Nat Compd 47:96–97

    CAS  Google Scholar 

  • Jo BW, Choi S-K (2014) Degradation of fucoidans from Sargassum fulvellum and their biological activities. Carbohydr Polym 111:822–829

    CAS  PubMed  Google Scholar 

  • Kasai A, Arafuka S, Koshiba N, Takahashi D, Toshima K (2015) Systematic synthesis of low-molecular weight fucoidan derivatives and their effect on cancer cells. Org Biomol Chem 13:10556–10568

    CAS  PubMed  Google Scholar 

  • Kimura R, Rokkaku T, Takeda S, Senba M, Mori N (2013) Cytotoxic effects of fucoidan nanoparticles against osteosarcoma. Mar Drugs 11:4267–4278

    PubMed  PubMed Central  Google Scholar 

  • Kitamura K, Matsuo M, Tsuneo Y (1992) Enzymic degradation of fucoidan by fucoidanase from the hepatopancreas of Patinopecten yessoensis. Biosci Biotechnol Biochem 56:490–494

    CAS  PubMed  Google Scholar 

  • Koh HSA, Lu J, Zhou W (2019) Structure characterization and antioxidant activity of fucoidan isolated from Undaria pinnatifida grown in New Zealand. Carbohydr Polym 212:178–185

    CAS  PubMed  Google Scholar 

  • Koike T, Sugimoto A, Kosono S, Komaba S, Kanno Y, Kitamura T, Anzai I, Watanabe T, Takahashi D, Toshima K (2021) Synthesis of low-molecular weight fucoidan derivatives and their binding abilities to SARS-CoV-2 spike proteins. RSC Med Chem 12:2016–2021

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Krylova NV, Ermakova SP, Lavrov VF, Leneva IA, Kompanets GG, Iunikhina OV, Nosik MN, Ebralidze LK, Falynskova IN, Silchenko AS, Zaporozhets TS (2020) The comparative analysis of antiviral activity of native and modified fucoidans from brown algae Fucus evanescens in vitro and in vivo. Mar Drugs 18:224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kusaykin MI, Silchenko AS, Zakharenko AM, Zvyagintseva TN (2016) Fucoidanases. Glycobiology 26:3–12

    CAS  PubMed  Google Scholar 

  • Lahrsen E, Liewert I, Alban S (2018a) Gradual degradation of fucoidan from Fucus vesiculosus and its effect on structure, antioxidant and antiproliferative activities. Carbohydr Polym 192:208–216

    CAS  PubMed  Google Scholar 

  • Lahrsen E, Schoenfeld AK, Alban S (2018b) Size-dependent pharmacological activities of differently degraded fucoidan fractions from Fucus vesiculosus. Carbohydr Polym 189:162–168

    CAS  PubMed  Google Scholar 

  • Leal D, Mansilla A, Matsuhiro B, Moncada-Basualto M, Lapier M, Maya JD, Olea-Azar C, De Borggraeve WM (2018) Chemical structure and biological properties of sulfated fucan from the sequential extraction of subAntarctic Lessonia sp (Phaeophyceae). Carbohydr Polym 199:304–313

    CAS  PubMed  Google Scholar 

  • Lee ZH, Lee MF, Chen JH, Tsou MH, Wu ZY, Lee CZ, Huang YY, Lin SM, Lin HM (2022) Fucoidan with three functions extracted from Sargassum aquifolium integrated rice-husk synthesis dual-imaging mesoporous silica nanoparticle. J Nanobiotechnol 20:298

    CAS  Google Scholar 

  • Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: Structure and bioactivity. Molecules 13:1671–1695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lim J-M, Yoo H, Lee K-W (2022) High molecular weight fucoidan restores intestinal integrity by regulating inflammation and tight junction loss induced by methylglyoxal-derived hydroimidazolone-1. Mar Drugs 20:580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd PF, Lloyd KO (1963) Sulphatases and sulphated polysaccharides in the viscera of marine molluscs. Nature 199:287–287

    ADS  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucl Acids Res 42:D490-495

    CAS  PubMed  Google Scholar 

  • Lu C, Shao Z, Zhang P, Duan D (2020) Genome-wide analysis of the Saccharina japonica sulfotransferase genes and their transcriptional profiles during whole developmental periods and under abiotic stresses. BMC Plant Biol 20:271

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luthuli S, Wu S, Cheng Y, Zheng X, Wu M, Tong H (2019) Therapeutic effects of fucoidan: A review on recent studies. Mar Drugs 17:487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mensah EO, Kanwugu ON, Panda PK, Adadi P (2023) Marine fucoidans: Structural, extraction, biological activities and their applications in the food industry. Food Hydrocoll 142:108784

  • Mikkelsen MD, Cao HTT, Roret T, Rhein-Knudsen N, Holck J, Tran VTT, Nguyen TT, Tran VHN, Lezyk MJ, Muschiol J, Pham TD, Czjzek M, Meyer AS (2021) A novel thermostable prokaryotic fucoidan active sulfatase PsFucS1 with an unusual quaternary hexameric structure. Sci Rep 11:19523

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen MS, Mikkelsen MD, Ptak SH, Hejbøl EK, Ohmes J, Thi TN, Nguyen Ha VT, Fretté X, Fuchs S, Meyer A, Schrøder HD, Ding M (2022) Efficacy of marine bioactive compound fucoidan for bone regeneration and implant fixation in sheep. J Biomed Mater Res A 110:861–872

    CAS  PubMed  Google Scholar 

  • Obluchinskaya ED, Pozharitskaya ON, Shikov AN (2022a) In vitro anti-inflammatory activities of fucoidans from five species of brown seaweeds. Mar Drugs 20:606

    CAS  PubMed  PubMed Central  Google Scholar 

  • Obluchinskaya ED, Pozharitskaya ON, Zakharov DV, Flisyuk EV, Terninko II, Generalova YE, Smekhova IE, Shikov AN (2022b) The biochemical composition and antioxidant properties of Fucus vesiculosus from the Arctic region. Mar Drugs 20:193

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohmes J, Mikkelsen MD, Nguyen TT, Tran VHN, Meier S, Nielsen MS, Ding M, Seekamp A, Meyer AS, Fuchs S (2022) Depolymerization of fucoidan with endo-fucoidanase changes bioactivity in processes relevant for bone regeneration. Carbohydr Polym 286:119286

    CAS  PubMed  Google Scholar 

  • Park E-J, Choi J-I (2017) Melanogenesis inhibitory effect of low molecular weight fucoidan from Undaria pinnatifida. J Appl Phycol 29:2213–2217

  • Park HY, Han MH, Park C, Jin CY, Kim GY, Choi IW, Kim ND, Nam TJ, Kwon TK, Choi YH (2011) Anti-inflammatory effects of fucoidan through inhibition of NF-κB, MAPK and Akt activation in lipopolysaccharide-induced BV2 microglia cells. Food Chem Toxicol 49:1745–1752

    CAS  PubMed  Google Scholar 

  • Park MH, Hong JT (2016) Roles of NF-κB in cancer and inflammatory diseases and their therapeutic approaches. Cells 5:15

    PubMed  PubMed Central  Google Scholar 

  • Pielesz A, Biniaś W, Paluch J (2011) Mild acid hydrolysis of fucoidan: characterization by electrophoresis and FT-Raman spectroscopy. Carbohydr Res 346:1937–1944

    CAS  PubMed  Google Scholar 

  • Pinheiro AC, Bourbon AI, Cerqueira MA, Maricato É, Nunes C, Coimbra MA, Vicente AA (2015) Chitosan/fucoidan multilayer nanocapsules as a vehicle for controlled release of bioactive compounds. Carbohydr Polym 115:1–9

    CAS  PubMed  Google Scholar 

  • Ponce NMA, Stortz CA (2020) A comprehensive and comparative analysis of the fucoidan compositional data across the Phaeophyceae. Front Plant Sci 11:556312

    PubMed  PubMed Central  Google Scholar 

  • Pradhan B, Nayak R, Patra S, Bhuyan PP, Behera PK, Mandal AK, Behera C, Ki JS, Adhikary SP, MubarakAli D, Jena M (2022) A state-of-the-art review on fucoidan as an antiviral agent to combat viral infections. Carbohydr Polym 291:119551

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Y, Wang L, You Y, Sun X, Wen C, Fu Y, Song S (2022) Preparation of low-molecular-weight fucoidan with anticoagulant activity by photocatalytic degradation method. Foods 11:822

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qianqian W, Shuang M, Hourong X, Min Z, Jingmin C (2011) Purification and the secondary structure of fucoidanase from Fusarium sp. LD8. Evid Based Complement Alternat Med 2011:196190

  • Qiu Y, Jiang H, Dong Y, Wang Y, Hamouda HI, Balah MA, Mao X (2022) Expression and biochemical characterization of a novel fucoidanase from Flavobacterium algicola with the principal product of fucoidan-derived disaccharide. Foods 11:1025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos-de-la-Peña AM, Contreras-Esquivel JC, Aguilar O, González-Valdez J (2022) Structural and bioactive roles of fucoidan in nanogel delivery systems. A review. Carbohydr Polym Technol Appl 4:100235

    Google Scholar 

  • Rasin AB, Silchenko AS, Kusaykin MI, Malyarenko OS, Zueva AO, Kalinovsky AI, Airong J, Surits VV, Ermakova SP (2020) Enzymatic transformation and anti-tumor activity of Sargassum horneri fucoidan. Carbohydr Polym 246:116635

    CAS  PubMed  Google Scholar 

  • Sakai T, Ishizuka K, Shimanaka K, Ikai K, Kato I (2003a) Structures of oligosaccharides derived from Cladosiphon okamuranus fucoidan by digestion with marine bacterial enzymes. Mar Biotechnol 5:536–544

    CAS  Google Scholar 

  • Sakai T, Kawai T, Kato I (2004) Isolation and characterization of a fucoidan-degrading marine bacterial strain and its fucoidanase. Mar Biotechnol 6:335–346

    CAS  Google Scholar 

  • Sakai T, Kimura H, Kato I (2002) A marine strain of Flavobacteriaceae utilizes brown seaweed fucoidan. Mar Biotechnol 4:399–405

    CAS  Google Scholar 

  • Sakai T, Kimura H, Kato I (2003b) Purification of sulfated fucoglucuronomannan lyase from bacterial strain of Fucobacter marina and study of appropriate conditions for its enzyme digestion. Mar Biotechnol 5:380–387

    CAS  Google Scholar 

  • Santinon C, Ochi D, Beppu MM, Vieira MGA (2022) Chemical modifications in the structure of seaweed polysaccharides as a viable antimicrobial application: A current overview and future perspectives. Algal Res 66:102796

    Google Scholar 

  • Sasaki K, Sakai T, Kojima K, Nakayama S, Nakanishi Y, Kato I (1996) Partial purification and characterization of an enzyme releasing 2-sulfo-α-L-fucopyranose from 2-sulfo-α-L-fucopyranosyl-(1→2) pyridylaminated fucose from a sea urchin, Strongylocentrotus nudus. Biosci Biotech Biochem 60:666–668

    CAS  Google Scholar 

  • Shao Z, Duan D (2022) The cell wall polysaccharides biosynthesis in seaweeds: A molecular perspective. Front Plant Sci 13:902823

    PubMed  PubMed Central  Google Scholar 

  • Shen J, Chang Y, Zhang Y, Mei X, Xue C (2020) Discovery and characterization of an endo-1,3-fucanase from marine bacterium Wenyingzhuangia fucanilytica: A novel glycoside hydrolase family. Front Microbiol 11:1674

    PubMed  PubMed Central  Google Scholar 

  • Shevchenko NM, Anastyuk SD, Menshova RV, Vishchuk OS, Isakov VI, Zadorozhny PA, Sikorskaya TV, Zvyagintseva TN (2015) Further studies on structure of fucoidan from brown alga Saccharina gurjanovae. Carbohydr Polym 121:207–216

    CAS  PubMed  Google Scholar 

  • Shi D, Qi J, Zhang H, Yang H, Yang Y, Zhao X (2019) Comparison of hydrothermal depolymerization and oligosaccharide profile of fucoidan and fucosylated chondroitin sulfate from Holothuria floridana. Int J Biol Macromol 132:738–747

    CAS  PubMed  Google Scholar 

  • Sichert A, Le Gall S, Klau LJ, Laillet B, Rogniaux H, Aachmann FL, Hehemann JH (2021) Ion-exchange purification and structural characterization of five sulfated fucoidans from brown algae. Glycobiology 31:352–357

    CAS  PubMed  Google Scholar 

  • Silchenko AS, Kusaykin MI, Kurilenko VV, Zakharenko AM, Isakov VV, Zaporozhets TS, Gazha AK, Zvyagintseva TN (2013) Hydrolysis of fucoidan by fucoidanase isolated from the marine bacterium, Formosa algae. Mar Drugs 11:2413–2430

    PubMed  PubMed Central  Google Scholar 

  • Silchenko AS, Kusaykin MI, Zakharenko AM, Menshova RV, Khanh HHN, Dmitrenok PS, Isakov VV, Zvyagintseva TN (2014) Endo-1,4-fucoidanase from Vietnamese marine mollusk Lambis sp. which producing sulphated fucooligosaccharides. J Mol Catal B 102:154–160

    CAS  Google Scholar 

  • Silchenko AS, Rasin AB, Kusaykin MI, Kalinovsky AI, Miansong Z, Changheng L, Malyarenko O, Zueva AO, Zvyagintseva TN, Ermakova SP (2017a) Structure, enzymatic transformation, anticancer activity of fucoidan and sulphated fucooligosaccharides from Sargassum horneri. Carbohydr Polym 175:654–660

    CAS  PubMed  Google Scholar 

  • Silchenko AS, Rasin AB, Kusaykin MI, Malyarenko OS, Shevchenko NM, Zueva AO, Kalinovsky AI, Zvyagintseva TN, Ermakova SP (2018a) Modification of native fucoidan from Fucus evanescens by recombinant fucoidanase from marine bacteria Formosa algae. Carbohydr Polym 193:189–195

    CAS  PubMed  Google Scholar 

  • Silchenko AS, Rasin AB, Zueva AO, Kusaykin MI, Zvyagintseva TN, Kalinovsky AI, Kurilenko VV, Ermakova SP (2018b) Fucoidan sulfatases from marine bacterium Wenyingzhuangia fucanilytica CZ1127(T). Biomolecules 8:98

    PubMed  PubMed Central  Google Scholar 

  • Silchenko AS, Rasin AB, Zueva AO, Kusaykin MI, Zvyagintseva TN, Rubtsov NK, Ermakova SP (2021) Discovery of a fucoidan endo-4O-sulfatase: Regioselective 4O-desulfation of fucoidans and its effect on anticancer activity in vitro. Carbohydr Polym 271:118449

    CAS  PubMed  Google Scholar 

  • Silchenko AS, Ustyuzhanina NE, Kusaykin MI, Krylov VB, Shashkov AS, Dmitrenok AS, Usoltseva RV, Zueva AO, Nifantiev NE, Zvyagintseva TN (2017b) Expression and biochemical characterization and substrate specificity of the fucoidanase from Formosa algae. Glycobiology 27:254–263

    CAS  PubMed  Google Scholar 

  • Song C, You Y, Wen C, Fu Y, Yang J, Zhao J, Song S (2023) Characterization and gel properties of low-molecular-weight carrageenans prepared by photocatalytic degradation. Polymers 15:602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Ai C, Wen C, Peng H, Yang J, Cui Y, Song S (2023) Inhibitory effects of fucoidan from Laminaria japonica against some pathogenic bacteria and SARS-CoV-2 depend on its large molecular weight. Int J Biol Macromol 229:413–421

    CAS  PubMed  Google Scholar 

  • Suprunchuk V (2021) Ultrasonic-treated fucoidan as a promising therapeutic agent. Polim Med 51:85–90

    PubMed  Google Scholar 

  • Suprunchuk VE (2019) Low-molecular-weight fucoidan: Chemical modification, synthesis of its oligomeric fragments and mimetics. Carbohydr Res 485:107806

    CAS  PubMed  Google Scholar 

  • Takayama M, Koyama N, Sakai T, Kato I (2002) Enzymes capable of degrading a sulfated-fucose-containing polysaccharide and their encoding genes. United States Patent US648955B1

  • Thanassi NM, Nakada HI (1967) Enzymic degradation of fucoidan by enzymes from the hepatopancreas of abalone, Haliotus species. Arch Biochem Biophys 118:172–177

    CAS  Google Scholar 

  • Thinh PD, Menshova RV, Ermakova SP, Anastyuk SD, Ly BM, Zvyagintseva TN (2013) Structural characteristics and anticancer activity of fucoidan from the brown alga Sargassum mcclurei. Mar Drugs 11:1456–1476

    CAS  PubMed  Google Scholar 

  • Tran VHN, Nguyen TT, Meier S, Holck J, Cao HTT, Van TTT, Meyer AS, Mikkelsen MD (2022) The endo-α(1,3)-fucoidanase Mef2 releases uniquely branched oligosaccharides from Saccharina latissima fucoidans. Mar Drugs 20:305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trang VTD, Mikkelsen MD, Vuillemin M, Meier S, Cao HTT, Muschiol J, Perna V, Nguyen TT, Tran VHN, Holck J, Van TTT, Khanh HHN, Meyer AS (2022) The endo-α(1,4) specific fucoidanase Fhf2 from Formosa haliotis releases highly sulfated fucoidan oligosaccharides. Front Plant Sci 13:823668

    PubMed  PubMed Central  Google Scholar 

  • Ustyuzhanina NE, Bilan MI, Gerbst AG, Ushakova NA, Tsvetkova EA, Dmitrenok AS, Usov AI, Nifantiev NE (2016) Anticoagulant and antithrombotic activities of modified xylofucan sulfate from the brown alga Punctaria plantaginea. Carbohydr Polym 136:826–833

    CAS  PubMed  Google Scholar 

  • van Weelden G, Bobiński M, Okła K, van Weelden WJ, Romano A, Pijnenborg JMA (2019) Fucoidan structure and activity in relation to anti-cancer mechanisms. Mar Drugs 17:32

    PubMed  PubMed Central  Google Scholar 

  • Venkatesan J, Anil S, Kim S-K, Shim MS (2016) Seaweed polysaccharide-based nanoparticles: preparation and applications for drug delivery. Polymers 8:30

    PubMed  PubMed Central  Google Scholar 

  • Venkatesan J, Murugan SS, Seong GH (2022) Fucoidan-based nanoparticles: Preparations and applications. Int J Biol Macromol 217:652–667

    CAS  PubMed  Google Scholar 

  • Vuillemin M, Silchenko AS, Cao HTT, Kokoulin MS, Trang VTD, Holck J, Ermakova SP, Meyer AS, Mikkelsen MD (2020) Functional characterization of a new GH107 endo-α-(1,4)-fucoidanase from the marine bacterium Formosa haliotis. Mar Drugs 18:562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Giardino GJ, Chen R, Yang C, Niu J, Wang D (2023a) Photocatalytic depolymerization of native lignin toward chemically recyclable polymer networks. ACS Cent Sci 9:48–55

    CAS  PubMed  Google Scholar 

  • Wang J, Liu Z, Pan X, Wang N, Li L, Du Y, Li J, Li M (2022a) Structural and biochemical analysis reveals catalytic mechanism of fucoidan lyase from Flavobacterium sp. SA-0082. Mar Drugs 20:533

  • Wang J, Zhang Q (2017) Chemical modification of fucoidan and their application. In: Venkatesan J, Anil S, Kim S-K (eds) Seaweed Polysaccharides. Elsevier, Oxford, pp 157–173

    Google Scholar 

  • Wang J, Zhang Q, Zhang Z, Zhang H, Niu X (2010) Structural studies on a novel fucogalactan sulfate extracted from the brown seaweed Laminaria japonica. Int J Biol Macromol 47:126–131

    CAS  PubMed  Google Scholar 

  • Wang L, Wang L, Yan C, Ai C, Wen C, Guo X, Song S (2022b) Two Ascophyllum nodosum fucoidans with different molecular weights inhibit inflammation via blocking of TLR/NF-κB signaling pathway discriminately. Foods 11:2381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Veeraperumal S, Zhong S, Cheong KL (2023b) Fucoidan-derived functional oligosaccharides: Recent developments, preparation, and potential applications. Foods 12:878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Kankala RK, Fan J, Long R, Liu Y, Wang S (2018) Poly-L-ornithine/fucoidan-coated calcium carbonate microparticles by layer-by-layer self-assembly technique for cancer theranostics. J Mater Sci 29:68

    Google Scholar 

  • Wang SH, Huang CY, Chen CY, Chang CC, Huang CY, Dong CD, Chang JS (2020) Structure and biological activity analysis of fucoidan isolated from Sargassum siliquosum. ACS Omega 5:32447–32455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Xing M, Cao Q, Ji A, Liang H, Song S (2019) Biological activities of fucoidan and the factors mediating its therapeutic effects: A review of recent studies. Mar Drugs 17:183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu M, Xu L, Zhao L, Xiao C, Gao N, Luo L, Yang L, Li Z, Chen L, Zhao J (2015) Structural analysis and anticoagulant activities of the novel sulfated fucan possessing a regular well-defined repeating unit from sea cucumber. Mar Drugs 13:2063–2084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Q, Zhang M, Wu K, Liu B, Cai J, Pan R (2011) Purification and characteristics of fucoidanase obtained from Dendryphiella arenaria TM94. J Appl Phycol 23:197–203

    CAS  Google Scholar 

  • Wu SY, Yang WY, Cheng CC, Hsiao MC, Tsai SL, Lin HK, Lin KH, Yuh CH (2020a) Low molecular weight fucoidan prevents radiation-induced fibrosis and secondary tumors in a Zebrafish model. Cancers 12:1608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu T-C, Hong Y-H, Tsai Y-H, Hsieh S-L, Huang R-H, Kuo C-H, Huang C-Y (2020b) Degradation of Sargassum crassifolium fucoidan by ascorbic acid and hydrogen peroxide, and compositional, structural, and in vitro anti-Lung cancer analyses of the degradation products. Mar Drugs 18:334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J-K, Wang Y-Y, Ma H-L, Wang Z-B (2016) Ultrasonic effects on the degradation kinetics, preliminary characterization and antioxidant activities of polysaccharides from Phellinus linteus mycelia. Ultrason Sonochem 29:251–257

    CAS  PubMed  Google Scholar 

  • Yang X, Wang S, Trangle SS, Li Y, White WL, Li J, Ying T, Kong Q, Zhao Y, Lu J (2018) Investigation of different molecular weight fucoidan fractions derived from New Zealand Undaria pinnatifida in combination with GroA therapy in prostate cancer cell lines. Mar Drugs 16:454

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo HJ, You DJ, Lee KW (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Li Q, Wu J, Yang X, Yang S, Zhu W, Liu Y, Tang W, Nie S, Hassouna A, White WL, Zhao Y, Lu J (2021) Fucoidan extracted from sporophyll of Undaria pinnatifida grown in Weihai, China - Chemical composition and comparison of antioxidant activity of different molecular weight fractions. Front Nutr 8:636930

    PubMed  PubMed Central  Google Scholar 

  • Zayed A, Avila-Peltroche J, El-Aasr M, Ulber R (2022a) Sulfated galactofucans: An outstanding class of fucoidans with promising bioactivities. Mar Drugs 20:412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zayed A, Dienemann C, Giese C, Krämer R, Ulber R (2018) An immobilized perylene diimide derivative for fucoidan purification from a crude brown algae extract. Process Biochem 65:233–238

    CAS  Google Scholar 

  • Zayed A, El-Aasr M, Ibrahim AS, Ulber R (2020) Fucoidan characterization: determination of purity and physicochemical and chemical properties. Mar Drugs 18:571

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zayed A, Haggag Y, Ezzat SM, Salem MA, Ulber R (2022b) Fucoidans as nanoparticles: pharmaceutical and biomedical applications. In: Venkatesan J, Kim S-K, Anil S, Rekha PD (eds) Polysaccharide Nanoparticles: Preparation and Biomedical Applications Micro and Nano Technologies. Elsevier, Amsterdam, pp 413–455

  • Zayed A, Muffler K, Hahn T, Rupp S, Finkelmeier D, Burger-Kentischer A, Ulber R (2016) Physicochemical and biological characterization of fucoidan from Fucus vesiculosus purified by dye affinity chromatography. Mar Drugs 14:79

    PubMed  PubMed Central  Google Scholar 

  • Zayed A, Ulber R (2019) Fucoidan production: Approval key challenges and opportunities. Carbohydr Polym 211:289–297

    CAS  PubMed  Google Scholar 

  • Zayed A, Ulber R (2020) Fucoidans: Downstream processes and recent applications. Mar Drugs 18:170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zueva AO, Silchenko AS, Rasin AB, Kusaykin MI, Usoltseva RV, Kalinovsky AI, Kurilenko VV, Zvyagintseva TN, Thinh PD, Ermakova SP (2020) Expression and biochemical characterization of two recombinant fucoidanases from the marine bacterium Wenyingzhuangia fucanilytica CZ1127T. Int J Biol Macromol 164:3025–3037

    CAS  PubMed  Google Scholar 

  • Zueva AO, Silchenko AS, Rasin AB, Malyarenko OS, Kusaykin MI, Kalinovsky AI, Ermakova SP (2023) Production of high- and low-molecular weight fucoidan fragments with defined sulfation patterns and heightened in vitro anticancer activity against TNBC cells using novel endo-fucanases of the GH107 family. Carbohydr Polymers

  • Zvyagintseva TN, Shevchenko NM, Chizhov AO, Krupnova TN, Sundukova EV, Isakov VV (2003) Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J Exp Mar Biol Ecol 294:1–13

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Conceptualization, A.Z. and R.U.; writing original draft, A.Z., H.C. and V.T.; writing review and editing, A.Z. and R.U.; supervision, A.Z. and R.U.; project administration, A.Z. and R.U.; funding acquisition, R.U. and A.Z. All authors have read and agreed to the published version of the manuscript.

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The original online version of this article was revised: In this article the affiliation 'NhaTrang Institute of Technology Research and Application, Vietnam Academy of Science and Technology, 02 Hung Vuong Street, Nhatrang 650000, Vietnam' for Authors Dr. Cao and Dr. Trang was missing.

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Zayed, A., Cao, H.T.T., Trang, V.T.D. et al. Structural tailoring of fucoidan backbones for maximizing their benefits: Enzymatic, chemical, and physical strategies. J Appl Phycol 35, 2445–2462 (2023). https://doi.org/10.1007/s10811-023-03036-6

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