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Biological and Therapeutic Properties of the Seaweed Polysaccharides Leonel Pereira1*

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Biological and Therapeutic Properties of the Seaweed Polysaccharides Leonel Pereira1* Pereira L. International Biology Review, vol. 2, issue 2, June 2018 Page 1 of 50 REVIEW ARTICLE Biological and therapeutic properties of the seaweed polysaccharides Leonel Pereira1* Author’s affiliations: 1. MARE (Marine and Environmental Sciences Centre), Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal * Corresponding author: Leonel Pereira, E-mail: [email protected] Abstract Seaweed polysaccharides isolated from the cell walls of various species of algae, possess immunomodulatory, anti-inflammatory, antiviral, antitumor, antithrombotic, anticoagulant and antioxidant bioactivities. Within the group of polysaccharides extracted from algae there are the phycocolloids. Collo- ids are extracted compounds that form colloidal solutions, an intermediate state between a solution and a suspension; they can be used commercially as thickeners, gelling agents and stabilizers for suspensions and emulsions. Hydrocolloids are carbohydrates that when dis- solved in water form viscous solutions. Sulfated galactans (e.g. agars, carrageenans, porphyrans) can be obtained from red algae, (e.g. ulvans) from green algae, alginates and other sulfated polysaccharides (e.g. ascophyl- lan, laminaran and fucoidan) are obtained from selected brown algae. The historic origin of the main phycocolloids and other seaweed polysaccharides (e.g. agar, carrageenan, alginic acid - alginates), their chemistry, uses and bioactivities are described in this review. Keywords: Macroalgae; Hydrocolloids; Sulfated galactans; Sulfate content; Bioactivities 1. Introduction a) the green algae are included in the phy- lum Chlorophyta and their pigmentation is Seaweeds (or macroalgae) are aquatic pho- identical to that of terrestrial plants (chloro- tosynthetic organisms belonging to the do- phyll a, b and carotenoids); main Eukarya and to kingdoms Plantae (green and red algae) and Chromista (brown b) the red algae belong to the phylum Rho- algae). Although classification systems dophyta and their photosynthetic pigments have varied greatly over time and according are chlorophyll a, phycobilins (R-phyco- to the authors, it is generally agreed that: cyanin and R-phycoerythrin) and caroteno- Copyright 2018 KEI Journals. All Rights Reserved http://journals.ke-i.org/index.php/IBR Pereira L. International Biology Review, vol. 2, issue 2, June 2018 Page 2 of 50 ids, mostly β-carotene, lutein and zeaxan- amount from the algae. All these polysac- thin; charides are water soluble and could be extracted with hot water or alkaline solution c) the brown algae are included in the phy- [11]. lum Ochrophyta (or Heterokontophyta), class Phaeophyceae and their pigments en- The historic origin of the main phycocollo- close chlorophylls a, c and carotenoids, ids (agar, carrageenan, and alginate) and dominated by fucoxanthin [1-3]. other seaweed polysaccharides (e.g. ulvan, porphyran, fucoidan, laminaran, ascophyl- Macroalgae are known to be enriched in lan), their chemistry, uses and bioactivities polysaccharides, with concentrations that are described in this review. can vary in the range of 4% to 76% of dry weight [4]. Globally, these are mainly struc- tural cell wall polysaccharides, although 2. Polysaccharides from green algae considerable amounts of mucopolysaccha- (Chlorophyta) rides and storage polysaccharides can occur in specific species [3,5,6]. 2.1. Ulvan The seaweed hydrocolloids, associated with Ulvan is a sulfated, water-soluble polysac- the cell wall and intercellular spaces, are charide which have physio-chemical and mainly produced by red and brown algae. biological features of great potentials in Several species of red algae (Rhodophyta) food, pharmaceutical, agricultural, and produce galactans (e.g. carrageenans and chemical applications [12,13]. agars) and of brown algae (Phaeophyceae) Ulvan may represent 8 - 29% of algal dry produce uronates (alginates) [7-10]. weight and is produced by some species Sulfated galactans (e.g. agars and carragee- belonging to the Phylum Chlorophyta nans) can be obtained from red algae, and (green algae), mostly belonging to the Class alginates and other sulfated polysaccharides Ulvophyceae [14]. It is mainly made up of (e.g. laminaran and fucoidan) are obtained disaccharide repeating sequences composed from brown algae. Phycocolloids are used of sulfated rhamnose and glucuronic acid, in food industries as natural additives and iduronic acid, or xylose [15,16]. have different European codes: E400 (al- The two major repeating disaccharides are ginic acid), E401 (sodium alginate), E402 aldobiuronic acids designated as: type A, (potassium alginate), E403 (ammonium ulvanobiuronic acid 3-sulfate (A3s) and alginate), E404 (calcium alginate), E405 type B, ulvanobiuronic acid 3-sulfate (B3s) (propylene glycol alginate), E406 (agar), (Figure 1). Partially sulfated xylose residues E407 (carrageenan) and E407a (semi- at O-2 can also occur in place of uronic refined carrageenan or ―processed Eucheu- acids. Low proportions of galactose, glu- ma seaweed‖) [10]. Agar, alginates and cose, mannose and protein were also gener- carrageenans are the ones with the highest ally described as components of ulvan. Ad- economic and commercial significance, ditionally, minor repeating units were being since these polysaccharides exhibit high reported to contain sulfated xylose, replac- molecular weights, high viscosity and ex- ing the iduronic acid or glucuronic acid cellent gelling, stabilizing and emulsifying components [12,13,17]. properties. They are extracted in fairly high Copyright 2018 KEI Journals. All Rights Reserved http://journals.ke-i.org/index.php/IBR Pereira L. International Biology Review, vol. 2, issue 2, June 2018 Page 3 of 50 (ulvanobiuronic acid – type A) (ulvanobiuronic acid – type B) Figure 1 - Idealized structure of the chemical units of Ulvan. Ulvan have exhibited strong antioxidant stable supramolecular structures via elec- [18,19], anticoagulant, antithrombotic [20], trostatic interactions and could also form antitumor [21], immune-stimulatory [22], stabilized membranes. Ulvan/chitosan poly- anti-inflammatory [22,23], antiviral [24,25], electrolytes were found to mimics the antibacterial [26], antiprotozoal [12], anti- extracellular matrix structure providing hypercholesterolemic [27], and antihyperli- points of attachment for osteoblasts, be- pidemic [28] activities; used also for hyper- lieved to be enhanced by the nanofibrous plasia prevention, gastrointestinal, rege- structure of this construct. It is suggested nerative and nanomedicine applications that this construct could be a suitable scaf- [29,30]. fold for applications in tissue engineering [32,33]. Alves et al. [31] determined the cytotoxicity of ulvan via MTT test (Methyl Thiazolyl Tetrazolium - colorimetric assay for assess- 3. Polysaccharides from red algae (Rho- ing cell metabolic activity), using fibrob- dophyta) last-like cells were incubated with ulvan, in vitro. Quantified protein and total DNA 3.1. Carrageenans stands data were directly correlated with Carrageenan has been used in Europe and hyaluronic acid use as control (non- Asia for centuries as a thickening and stabi- cytotoxic); in the studies conducted by lizing agent in food. In Europe, the use of these researchers [31], ulvan showed en- carrageenan began in Ireland more than 600 couraging results in terms of cytotoxicity. years ago when, in the small village on the Meanwhile, cytotoxicity is one of the most southern coast of Ireland, called "Carrag- important factors to determine the use of a hen", the flans were made by cooking "Irish biomaterial for medical purposes, as in tis- Moss" (Irish Moss - Chondrus crispus) in sue engineering and wound healing [32]. milk. The name carrageenin, the ancient Ulvan can be used in biomedical applica- name of carrageenan, was first used in 1862 tions, especially in tissue engineering. Bio- to designate the extract obtained from C. functionalized ulvan hydrogels with ALP crispus, in reference to the name of the (Alkaline Phosphatase) enzyme served as small Irish town [36]. The procedure for the inducers of mineralization in osteoblastic extraction of carrageenans was described differentiation [32,33] and the cytocompa- for the first time by Schmidt in 1844 [37]. tibility of ulvan as well as it relative mem- The name was later changed to carrageenan brane are promising features for scaffold to comply with the ―-an‖ suffix for the development [34,35]. The inter-molecular names of polysaccharides. charges of ulvan and chitosan (i.e. anionic and cationic charges respectively) produced Copyright 2018 KEI Journals. All Rights Reserved http://journals.ke-i.org/index.php/IBR Pereira L. International Biology Review, vol. 2, issue 2, June 2018 Page 4 of 50 The Irish moss has been used in industry sausages, patties and low-fat hamburgers since the 19th Century, in the clarification of [7,9,37,46-48]. beer [39]. The industrial extraction of car- rageenan had its start in 1930 in New- The most commonly used commercial car- England, from Chondrus crispus and Mas- rageenans are extracted from Kappaphycus tocarpus stellatus thalli, for the preparation alvarezii and Eucheuma denticulatum [45]. of chocolate milk. The interruption of agar Primarily wild-harvested genera such as imports during World War II, led to its re- Chondrus, Furcellaria, Gigartina, Chon- placement by carrageenan. This situation dracanthus, Sarcothalia, Mazzaella, Iri- was the starting point of a booming industry daea, Mastocarpus, and Tichocarpus are [40].
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