Seaweed polysaccharides and their potential biomedical applications

Starch/Staerke

Volumn 67, Issue 5-6, 2015, Pages 381-390

  Venkatesan, Jayachandran ^a   Lowe, Baboucarr ^a   Anil, Sukumaran ^b   Manivasagan, Panchanathan ^a   Kheraif, Abdulaziz A Al ^c   Kang, Kyong Hwa ^a   Kim, Se Kwon ^a  

^a Pukyong National University   (South Korea)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Alginate; Biomedical applications; Carrageenan; Fucoidan; Seaweed

Indexed keywords

BIOCOMPATIBILITY; CELL ENGINEERING; CONTROLLED DRUG DELIVERY; MARINE APPLICATIONS; MEDICAL APPLICATIONS; SEAWEED; STEM CELLS; TARGETED DRUG DELIVERY; TISSUE; TISSUE REGENERATION;

BIOLOGICAL APPLICATIONS; BIOMEDICAL APPLICATIONS; CARRAGEENANS; CHONDROGENIC DIFFERENTIATION; EXTRACELLULAR MATRICES; FORMING PROPERTIES; FUCOIDANS; SULFATED POLYSACCHARIDES;

ALGINATE;

EID: 84929469257     PISSN: 00389056     EISSN: 1521379X     Source Type: Journal    
DOI: 10.1002/star.201400127     Document Type: Review

References (105)

1. Kurita, K., Chitin and chitosan: Functional biopolymers from marine crustaceans. Mar. Biotechnol. 2006, 8, 203-226.
2. Venugopal, V., Marine Polysaccharides: Food Applications. CRC Press, Boca Raton, Florida 2011.
3. d'Ayala, G. G., Malinconico, M., Laurienzo, P., Marine derived polysaccharides for biomedical applications: chemical modification approaches. Molecules 2008, 13, 2069-2106.
4. Gutowska, A., Jeong, B., Jasionowski, M., Injectable gels for tissue engineering. Anat. Rec. 2001, 263, 342-349.
5. Lee, K. Y., Mooney, D. J., Alginate: Properties and biomedical applications. Prog. Polym. Sci. 2012, 37, 106-126.
6. Lee, N. Y., Ermakova, S. P., Zvyagintseva, T. N., Kang, K. W., et al., Inhibitory effects of fucoidan on activation of epidermal growth factor receptor and cell transformation in JB6 Cl41 cells. Food Chem. Toxicol. 2008, 46, 1793-1800.
7. Prajapati, V. D., Maheriya, P. M., Jani, G. K., Solanki, H. K., Carrageenan: A natural seaweed polysaccharide and its applications. Carbohydr. Polym. 2014, 105, 97-112.
8. Wijesinghe, W., Jeon, Y-J., Biological activities and potential industrial applications of fucose rich sulfated polysaccharides and fucoidans isolated from brown seawe: A review. Carbohydr. Polym. 2012, 88, 13-20.
9. Li, B., Lu, F., Wei, X., Zhao, R., Fucoidan: Structure and bioactivity. Molecules 2008, 13, 1671-1695.
10. Cho, Y-S., Jung, W-K., Kim, J., Choi, I-W., Kim, S-K., Beneficial effects of fucoidan on osteoblastic MG-63 cell differentiation. Food Chem. 2009, 116, 990-994.
11. Renn, D., Biotechnology and the red seaweed polysaccharide industry: Status, needs and prospects. Trends Biotechnol. 1997, 15, 9-14.
12. Laurienzo, P., Marine polysaccharides in pharmaceutical applications: An overview. Mar. Drug. 2010, 8, 2435-2465.
13. Rowe, R. C., Sheskey, P. J., Owen, S. C., Association, A. P., Handbook of Pharmaceutical Excipients, Pharmaceutical press, London 2006.
14. De Ruiter, G.A., Rudolph, B., Carrageenan biotechnology. Trends Food Sci. Technol. 1997, 8, 389-395.
15. Fenoradosoa, T. A., Ali, G., Delattre, C., Laroche, C, et al., Extraction and characterization of an alginate from the brown seaweed Sargassum turbinarioides Grunow. J. Appl. Phycol. 2010, 22, 131-137.
16. Calumpong, H., Maypa, A., Magbanua, M., Sixteenth International Seaweed Symposium, Springer, Cebu City, Philippines 1999, pp 211-215.
17. Lin, L., Chow, K. L., Leng, Y., Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells. J. Biomed. Mater. Res. A 2009, 89, 326-335.
18. Venkatesan, J., Bhatnagar, I., Manivasagan, P., Kang, K-H., Kim, S-K., Alginate composites for bone tissue engineering: A review. Int. J. Biol. Macromol. 2015, 72, 269-281.
19. Valente, J., Valente, T., Alves, P., Ferreira, P, et al., Alginate based scaffolds for bone tissue engineering. Mater. Sci. Eng. C 2012, 32, 2596-2603.
20. Zhao, L., Weir, M. D., Xu, H. H., An injectable calcium phosphate-alginate hydrogel-umbilical cord mesenchymal stem cell paste for bone tissue engineering. Biomaterials 2010, 31, 6502-6510.
21. Bouhadir, K. H., Lee, K. Y., Alsberg, E., Damm, K., et al., Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol. Prog. 2001, 17, 945-950.
22. Moshaverinia, A., Chen, C., Akiyama, K., Ansari, S, et al., Alginate hydrogel as a promising scaffold for dental-derived stem cells: An in vitro study. J. Mater. Sci.: Mater. Med. 2012, 23, 3041-3051.
23. Tønnesen, H. H., Karlsen, J., Alginate in drug delivery systems. Drug Dev. Ind. Pharm. 2002, 28, 621-630.
24. George, M., Abraham, T. E., Polyionic hydrocolloids for the intestinal delivery of protein drugs: Alginate and chitosan-A review. J. Control. Release 2006, 114, 1-14.
25. Gombotz, W. R., Wee, S. F., Protein release from alginate matrices. Adv. Drug Deliver. Rev. 2012, 64, 194-205.
26. Liu, Z., Jiao, Y., Wang, Y., Zhou, C., Zhang, Z., Polysaccharides-based nanoparticles as drug delivery systems. Adv. Drug Deliver. Rev. 2008, 60, 1650-1662.
27. Reis, C. P., Neufeld, R. J., Vilela, S., Ribeiro, A. J., Veiga, F., Review and current status of emulsion/dispersion technology using an internal gelation process for the design of alginate particles. J. Microencapsul. 2006, 23, 245-257.
28. Shilpa, A., Agrawal, S., Ray, A. R., Controlled delivery of drugs from alginate matrix. J. Macromol. Sci. C 2003, 43, 187-221.
29. Patil, R., Speaker, T., Retention of trypsin activity in spermine alginate microcapsules. J. Microencapsul. 1997, 14, 469-474.
30. Holte, O., Tonnesen, H., Karlsen, J., Measurement of diffusion through calcium alginate gel matrices. Pharmazie 2006, 61, 30-34.
31. Florczyk, S. J., Leung, M., Jana, S., Li, Z, et al., Enhanced bone tissue formation by alginate gel-assisted cell seeding in porous ceramic scaffolds and sustained release of growth factor. J. Biomed. Mater. Res. A 2012, 100, 3408-3415.
32. Kim, G., Ahn, S., Kim, Y., Cho, Y., Chun, W., Coaxial structured collagen-alginate scaffolds: Fabrication, physical properties, and biomedical application for skin tissue regeneration. J. Mater. Chem. 2011, 21, 6165-6172.
33. Balakrishnan, B., Mohanty, M., Umashankar, P., Jayakrishnan, A., Evaluation of an in situ forming hydrogel wound dressing based on oxidized alginate and gelatin. Biomaterials 2005, 26, 6335-6342.
34. Chatfieid, S., A comparison of the efficacy of the alginate preparation, Gaviscon Advance, with placebo in the treatment of gastro-oesophageal reflux disease. Curr. Med. Res. Opin. 1999, 15, 152-159.
35. Draget, K. I., Taylor, C., Chemical, physical and biological properties of alginates and their biomedical implications. Food Hydrocolloid. 2011, 25, 251-256.
36. Lalau, J., Bresson, R., Charpentier, P., Coliche, V, et al., Efficacy and tolerance of calcium alginate versus vaseline gauze dressings in the treatment of diabetic foot lesions. Diabetes Metab. 2008, 28, 223-229.
37. Yuvarani, I., Kumar, S. S., Venkatesan, J., Kim, S-K., Sudha, P., Preparation and characterization of curcumin coated chitosan-alginate blend for wound dressing application. J. Biomater. Tissue Eng. 2012, 2, 54-60.
38. Lee, K. Y., Mooney, D. J., Hydrogels for tissue engineering. Chem. Rev. 2001, 101, 1869-1880.
39. Abu-Rabeah, K., Polyak, B., Ionescu, R. E., Cosnier, S., Marks, R. S., Synthesis and characterization of a pyrrole-alginate conjugate and its application in a biosensor construction. Biomacromolecules 2005, 6, 3313-3318.
40. Rawson, D. M., Willmer, A. J., Turner, A. P., Whole-cell biosensors for environmental monitoring. Biosensors 1989, 4, 299-311.
41. Polyak, B., Geresh, S., Marks, R. S., Synthesis and characterization of a biotin-alginate conjugate and its application in a biosensor construction. Biomacromolecules 2004, 5, 389-396.
42. Mousty, C., Lepellec, A., Cosnier, S., Novoa, A., Marks, R. S., Fabrication of organic phase biosensors based on multilayered polyphenol oxidase protected by an alginate coating. Electrochem. Commun. 2001, 3, 727-732.
43. Cosnier, S., Novoa, A., Mousty, C., Marks, R. S., Biotinylated alginate immobilization matrix in the construction of an amperometric biosensor: Application for the determination of glucose. Anal. Chim. Acta 2002, 453, 71-79.
44. Usov, A., Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocolloid. 1998, 12, 301-308.
45. Vázquez-Delfín, E., Robledo, D., Freile-Pelegrín, Y., Microwave-assisted extraction of the carrageenan from Hypnea musciformis (Cystocloniaceae, Rhodophyta). J. Appl. Phycol. 2014, 26, 901-907.
46. Liu, H., Cheng, J., Chen, F., Hou, F, et al., Biomimetic and cell-mediated mineralization of hydroxyapatite by carrageenan functionalized graphene oxide. ACS Appl. Mater. Interfaces 2014, 6, 3132-3140.
47. Pawelec, K., Husmann, A., Best, S. M., Cameron, R. E., Ice-templated structures for biomedical tissue repair: From physics to final scaffolds. Appl. Phys. Rev. 2014, 1, 021301.
48. Santo, V. E., Frias, A. M., Carida, M., Cancedda, R, et al., Carrageenan-based hydrogels for the controlled delivery of PDGF-BB in bone tissue engineering applications. Biomacromolecules 2009, 10, 1392-1401.
49. Li, L., Ni, R., Shao, Y., Mao, S., Carrageenan, and its applications in drug delivery. Carbohydr. Polym. 2014, 103, 1-11.
50. Karavas, E., Koutris, E., Papadopoulos, A. G., Sigalas, M., et al., Application of density functional theory in combination with FTIR and DSC to characterise polymer drug interactions for the preparation of sustained release formulations between fluvastatin and carrageenans. Int. J. Pharm. 2014, 466, 211-222.
51. Grenha, A., Gomes, M. E., Rodrigues, M., Santo, V., et al., Development of new chitosan/carrageenan nanoparticles for drug delivery applications. J. Biomed. Mater. Res. A 2010, 92, 1265-1272.
52. Kulkarni, R. V., Boppana, R., Krishna Mohan, G, Mutalik, S., Kalyane, N. V., pH-responsive interpenetrating network hydrogel beads of poly (acrylamide)-g-carrageenan and sodium alginate for intestinal targeted drug delivery: Synthesis, in vitroand in vivo evaluation. J. Colloid Interface Sci. 2012, 367, 509-517.
53. Rocha, P. M., Santo, V. E., Gomes, M. E., Reis, R. L., Mano, J. F., Encapsulation of adipose-derived stem cells and transforming growth factor-β1 in carrageenan-based hydrogels for cartilage tissue engineering. J. Bioact. Compat. Polym. 2011, 26, 493-507.
54. Beneke, C. E., Viljoen, A. M., Hamman, J. H., Polymeric plant-derived excipients in drug delivery. Molecules 2009, 14, 2602-2620.
55. Şen, M., Avci, E. N., Radiation synthesis of poly (N-vinyl-2-pyrrolidone)-κ-carrageenan hydrogels and their use in wound dressing applications. I. Preliminary laboratory tests. J. Biomed. Mater. Res. A 2005, 74, 187-196.
56. Campanella, L., Favero, G., Persi, L., Tomassetti, M., New biosensor for superoxide radical used to evidence molecules of biomedical and pharmaceutical interest having radical scavenging properties. J. Pharm. Biomed. Anal. 2000, 23, 69-76.
57. Campanella, L., Favero, G., Sammartino, M., Tomassetti, M., Enzymatic immobilisation in kappa-carrageenan gel suitable for organic phase enzyme electrode (OPEE) assembly. J. Mol. Catal. B: Enzym. 1999, 7, 101-113.
58. Medina, M. B., Binding interaction studies of the immobilized Salmonella typhimurium with extracellular matrix and muscle proteins, and polysaccharides. Int. J. Food Microbiol. 2004, 93, 63-72.
59. Campanella, L., De Luca, S., Favero, G., Persi, L., Tomassetti, M., Superoxide dismutase biosensors working in non-aqueous solvent. Fresenius. J. Anal. Chem. 2001, 369, 594-600.
60. Silva, T. H., Alves, A., Popa, E. G., Reys, L. L., et al., Marine algae sulfated polysaccharides for tissue engineering and drug delivery approaches. Biomatter 2012, 2, 278-289.
61. Campanella, L., Bonanni, A., Finotti, E., Tomassetti, M., Biosensors for determination of total and natural antioxidant capacity of red and white wines: Comparison with other spectrophotometric and fluorimetric methods. Biosens. Bioelectron. 2004, 19, 641-651.
62. Campanella, L., Pacifici, F., Sammartino, M., Tomassetti, M., Analysis of lecithin in pharmaceutical products and diet integrators using a new biosensor operating directly in non aqueous solvent. J. Pharm. Biomed. Anal. 1998, 18, 597-604.
63. Campanella, L., Gabbianelli, R., Gatta, T., Mazzone, E., Tomassetti, M., Sensors, Springer, Rome 2014, pp 131-135.
64. Calas-Blanchard, C., Catanante, G., Noguer, T., Electrochemical sensor and biosensor strategies for ROS/RNS detection in biological systems. Electroanalysis 2014, 26, 1277-1286.
65. Choi, D. Y., Jung, S. W., Lee, D. S., Lee, S. J., Fabrication and characteristics of microbial time temperature indicators from bio-paste using screen printing method. Packag. Technol. Sci. 2014, 27, 303-312.
66. Chevolot, L., Mulloy, B., Ratiskol, J., Foucault, A., Colliec-Jouault, S., A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydrate Research 2001, 330, 529-535.
67. Chung, H. J., Jeun, J., Houng, S. J., Jun, H., et al., Toxicological evaluation of fucoidan from Undaria pinnatifidain vitro and in vivo. Phytother. Res. 2010, 24, 1078-1083.
68. Huang, Y-C., Liu, T-J., Mobilization of mesenchymal stem cells by stromal cell-derived factor-1 released from chitosan/tripolyphosphate/fucoidan nanoparticles. Acta biomater. 2012, 8, 1048-1056.
69. Ponce, N., Pujol, C. A., Damonte, E. B., Flores, M. a. L., Stortz, C. A., Fucoidans from the brown seaweed Adenocystis utricularis: Extraction methods, antiviral activity and structural studies. Carbohydr. Res. 2003, 338, 153-165.
70. Bilan, M. I., Grachev, A. A., Ustuzhanina, N. E., Shashkov, A. S., et al., Structure of a fucoidan from the brown seaweed Fucus evanescensC. Ag. Carbohydr. Res. 2002, 337, 719-730.
71. Senni, K., Pereira, J., Gueniche, F., Delbarre-Ladrat, C, et al., Marine polysaccharides: A source of bioactive molecules for cell therapy and tissue engineering. Mar. Drug. 2011, 9, 1664-1681.
72. Thébaud, N-B., Pierron, D., Bareille, R., Le Visage, C, et al., Human endothelial progenitor cell attachment to polysaccharide-based hydrogels: A pre-requisite for vascular tissue engineering. J. Mater. Sci. Mater. Med. 2007, 18, 339-345.
73. Jeong, H-S., Venkatesan, J., Kim, S-K., Hydroxyapatite-fucoidan nanocomposites for bone tissue engineering. Inter. J. Biol. Macromol. 2013, 57, 138-141.
74. Song, M. Y., Ku, S. K., Han, J. S., Genotoxicity testing of low molecular weight fucoidan from brown seaweeds. Food Chem. Toxicol. 2012, 50, 790-796.
75. Song, M. Y., Ku, S. K., Kim, H. J., Han, J. S., Low molecular weight fucoidan ameliorating the chronic cisplatin-induced delayed gastrointestinal motility in rats. Food Chem. Toxicol. 2012, 50, 4468-4478.
76. Hamidi, S., Letourneur, D., Aid-Launais, R., Di Stefano, A, et al., Fucoidan promotes early step of cardiac differentiation from human embryonic stem cells and long-term maintenance of beating areas. Tissue Eng. A 2014, 20, 1285-1294.
77. Changotade, S., Korb, G., Bassil, J., Barroukh, B, et al., Potential effects of a low-molecular-weight fucoidan extracted from brown algae on bone biomaterial osteoconductive properties. J. Biomed. Mater. Res. A 2008, 87, 666-675.
78. Lee, H. M., Kim, J-K., Cho, T-S., Applications of ophthalmic biomaterials embedded with fucoidan. J. Indus. Eng. Chem. 2012, 18, 1197-1201.
79. Lee, J. S., Jin, G. H., Yeo, M. G., Jang, C., et al., Fabrication of electrospun biocomposites comprising polycaprolactone/fucoidan for tissue regeneration. Carbohyd. Polym. 2012, 90, 181-188.
80. Nakamura, S., Nambu, M., Ishizuka, T., Hattori, H, et al., Effect of controlled release of fibroblast growth factor-2 from chitosan/fucoidan micro complex-hydrogel on in vitro and in vivo vascularization. J. Biomed. Mater. Res. A 2008, 85, 619-627.
81. Murakami, K., Aoki, H., Nakamura, S., Nakamura, S.-i., et al., Hydrogel blends of chitin/chitosan, fucoidan and alginate as healing-impaired wound dressings. Biomaterials 2010, 31, 83-90.
82. Sezer, A. D., Hatipoglu, F., Cevher, E., Oʇurtan, Z, et al., Chitosan film containing fucoidan as a wound dressing for dermal burn healing: preparation and in vitro/in vivo evaluation. AAPS Pharm. Sci. Tech. 2007, 8, E94-E101.
83. Senni, K., Gueniche, F., Foucault-Bertaud, A., Igondjo-Tchen, S, et al., Fucoidan a sulfated polysaccharide from brown algae is a potent modulator of connective tissue proteolysis. Arch. Biochem. Biophys. 2006, 445, 56-64.
84. Ale, M. T., Mikkelsen, J. D., Meyer, A. S., 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 2011, 9, 2106-2130.
85. Athukorala, Y., Jung, W.-K., Vasanthan, T., Jeon, Y.-J., An anticoagulative polysaccharide from an enzymatic hydrolysate of Ecklonia cava. Carbohyd. Polym. 2006, 66, 184-191.
86. Bachelet, L., Bertholon, I., Lavigne, D., Vassy, R, et al., Affinity of low molecular weight fucoidan for P-selectin triggers its binding to activated human platelets. Biochim. Biophys. Acta 2009, 1790, 141-146.
87. Choi, J-i., Kim, H-J., Preparation of low molecular weight fucoidan by gamma-irradiation and its anticancer activity. Carbohydr. Polym. 2013, 97, 358-362.
88. Anastyuk, S. D., Shevchenko, N. M., Ermakova, S. P., Vishchuk, O. S., et al., Anticancer activity in vitro of a fucoidan from the brown alga Fucus evanescens and its low-molecular fragments, structurally characterized by tandem mass-spectrometry. Carbohydr. Polym. 2012, 87, 186-194.
89. Fedorov, S. N., Ermakova, S. P., Zvyagintseva, T. N., Stonik, V. A., Anticancer and cancer preventive properties of marine polysaccharides: some results and prospects. Mar. Drugs 2013, 11, 4876-4901.
90. Wang, J., Liu, H., Li, N., Zhang, Q., Zhang, H., The protective effect of fucoidan in rats with streptozotocin-induced diabetic nephropathy. Mar. Drugs 2014, 12, 3292-3306.
91. Moon, H. J., Park, K. S., Ku, M. J., Lee, M. S., et al., Effect of Costaria costata fucoidan on expression of matrix metalloproteinase-1 promoter, mRNA, and protein. J. Nat. Prod. 2009, 72, 1731-1734.
92. Alves, A., Sousa, R. A., Reis, R. L., A practical perspective on ulvan extracted from green algae. J. Appl. Phycol. 2013, 25, 407-424.
93. Raveendran, S., Yoshida, Y., Maekawa, T., Kumar, D. S., Pharmaceutically versatile sulfated polysaccharide based bionano platforms. Nanomed. Nanotechnol. 2013, 9, 605-626.
94. Patel, S., Therapeutic importance of sulfated polysaccharides from seawe: Updating the recent findings. 3 Biotech 2012, 2, 171-185.
95. Yaich, H., Garna, H., Besbes, S., Barthélemy, J.-P, et al., Impact of extraction procedures on the chemical, rheological and textural properties of ulvan from Ulva lactuca of Tunisia coast. Food Hydrocolloid. 2014, 40, 53-63.
96. Dash, M., Samal, S. K., Bartoli, C., Morelli, A, et al., Biofunctionalization of ulvan scaffolds for bone tissue engineering. ACS Appl. Mater. Inter. 2014, 6, 3211-3218.
97. Toskas, G., Heinemann, S., Heinemann, C., Cherif, C, et al., Ulvan and ulvan/chitosan polyelectrolyte nanofibrous membranes as a potential substrate material for the cultivation of osteoblasts. Carbohydr. Polym. 2012, 89, 997-1002.
98. Alves, A., Sousa, R. A., Reis, R. L., Processing of degradable ulvan 3D porous structures for biomedical applications. J. Biomed. Mater. Res. A 2013, 101, 998-1006.
99. Rossi, F., van Griensven, M., Polymer functionalization as a powerful tool to improve scaffold performances. Tissue Eng. A 2013, 20, 2043-2051.
100. Barros, A., Alves, A., Nunes, C., Coimbra, M. A., et al., Carboxymethylation of ulvan and chitosan and their use as polymeric components of bone cements. Acta Biomater. 2013, 9, 9086-9097.
101. Alves, A., Pinho, E. D., Neves, N. M., Sousa, R. A., Reis, R. L., Processing ulvan into 2D structures: Cross-linked ulvan membranes as new biomaterials for drug delivery applications. Int. J. Pharm. 2012, 426, 76-81.
102. Chiellini, F., Morelli, A., Ulvan: A versatile platform of biomaterials from renewable resources. Biomaterials-Physics and Chemistry 2011, InTech, Rijeka. DOI: 10.5772/24901
103. Lahaye, M., Robic, A, Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 2007, 8, 1765-1774.
104. Alves, A., Sousa, R. A., Reis, R. L., In vitro cytotoxicity assessment of ulvan, a polysaccharide extracted from green algae. Phytother. Res. 2013, 27, 1143-1148.
105. Matsubara, K., Matsuura, Y., Hori, K., Miyazawa, K., An anticoagulant proteoglycan from the marine green alga, Codium pugniformis. J. Appl. Phycol. 2000, 12, 9-14.