Abstract
Aqueous extraction of Ahnfeltia plicata collected in the Magellan ecoregion afforded agarose devoid of sulfate groups. This neutral agarose was subjected to sulfation with SO3-pyridine complex, giving an aqueous soluble derivative with 35.5 % sulfate groups. Analysis by Fourier transform infrared spectroscopy (FT-IR) and by 1H and 13C NMR spectroscopy indicated that this derivative was sulfated at positions C-6 of the β-galactopyranosyl residue and C-2 of the α-3,6-anhydrogalactopyranosyl residue and partially sulfated at position C-2 of the β residue. The antioxidant capacity of sulfated agarose was evaluated by the oxygen radical absorbance capacity (ORAC) method, ABTS radical cation, hydroxyl radicals, and chelating assays. This capacity of sulfated agarose toward peroxyl radicals was higher than that of commercial λ-carrageenan, while native agarose presented good activity, with an ORAC value similar to that of commercial κ-carrageenan. Sulfated agarose presented good antioxidant capacity toward other radicals. Copolymerization of sulfated agarose with acrylamide was achieved using ceric ammonium nitrate as initiator. NMR spectroscopy indicated grafting of polyacrylamide at position C-4 of β-galactopyranosyl residues.
Similar content being viewed by others
References
Alarcón E, Campos AM, Edwards AM, Lissi E, López-Alarcón C (2008) Antioxidant capacity of herbal infusions and tea extracts: a comparison of ORAC-fluorescein and ORAC-pyrogallol red methodologies. Food Chem 107:1114–1119
Barahona T, Chandía NP, Encinas MV, Matsuhiro B, Zúñiga EA (2011) Antioxidant capacity of sulfated polysaccharides from seaweeds. A kinetic approach. Food Hydrocoll 25:529–535
Barahona T, Encinas MV, Mansilla A, Matsuhiro B, Zúñiga EA (2012) A sulfated galactan with antioxidant capacity from the green variant of tetrasporic Gigartina skottsbergii (Gigartinales, Rhodophyta). Carbohydr Res 347:114–120
Cáceres PJ, Carlucci MC, Damonte EB, Matsuhiro B, Zúñiga EA (2000) Carrageenans from Chilean samples of Stenogramme interrupta (Phyllophoraceae): structural analysis and biological activity. Phytochemistry 53:81–86
Campo VL, Kawano DF, da Silva B, Jr D, Carvalho I (2009) Carragenans: biological properties, chemical modifications and structural analysis. A review. Carbohydr Polym 77:167–180
Chaplin MF (1986) Monosaccharides. In: Chaplin MF MF, Kennedy JF (eds) Carbohydrate analysis: a practical approach. IRL, Oxford, pp 1–36
De Araujo CA, Noseda MD, Cipriani TR, Gonçalves AG, Duarte MER, Ducatti DRB (2013) Selective sulfation of carrageenans and the influence of sulfate regiochemistry on anticoagulant properties. Carbohydr Polym 91:483–491
Decker E, Welch B (1990) Role of ferritin as a lipid oxidation catalyst in muscle food. J Agric Food Chem 38:674–677
Duckworth M, Yaphe W (1971) The structure of agar part I. Fractionation of a complex mixture of polysaccharides. Carbohyd Res 16:189–197
Guiseley KB (1987) Natural and synthetic derivatives of agarose and their use in biochemical separations. In: Yalpani M (ed) Industrial polysaccharides. Elsevier, Amsterdam, pp 139–147
Hosseinzadeh H (2009) Ceric-initiated free radical graft copolymerization of acrylonitrile onto kappa carrageenan. J Appl Polym Sci 114:404–412
Izumi K (1971) Chemical heterogeneity of the agar from Gelidium amansii. Carbohyd Res 17:227–230
Jenkins DW, Hudson SM (2001) Review of vinyl graft copolymerization featuring recent advances toward controlled radical-based reactions and illustrated with chitin/chitosan trunk polymers. Chem Rev 101:3245–3273
Leal D, Matsuhiro B, Rossi M, Caruso F (2008) FT-IR spectra of alginic acid block fractions in three species of brown seaweeds. Carbohydr Res 343:308–316
Maciel S, Chavez L, Souza W, Texeira I, Freitas L, Feitosa P, De Paula C (2008) Structural characterization of cold extracted fraction of soluble sulfated polysaccharide from red seaweed Gracilaria birdiae. Carbohydr Polym 71:559–565
Mansilla A, Avila M, Yokoya NS (2012) Current knowledge on biotechnical interesting seaweeds from the Magellan region, Chile. Rev Bras Farmacogn 22:760–767
Mansilla A, Rodríguez JP, Souza JMC, Rosenfeld S, Ojeda J, Yokoya NS (2013) Growth responses to temperature, salinity and nutrient variations, and biomass variation and phenology of Ahnfeltia plicata (Rhodophyta, Ahnfeltiales): a commercially interesting agarophyte from the Magellanic region. Chile J Appl Phycol. doi:10.1007/s1081-013-0150-0
Matsuhashi T (1998) Agar. In: Dumitriu S (ed) Polysaccharides. Marcel Dekker, New York, pp 335–375
Matsuhiro B (1996) Vibrational spectroscopy of seaweed galactans. Hydrobiologia 326/327:481–489
Matsuhiro B, Rivas P (1993) Second-derivative Fourier transform infrared spectra of seaweed galactans. J Appl Phycol 5:45–51
Matsuhiro B, Zanlungo AB (1983) Colorimetric determination of 3,6-anhydrogalactose in polysaccharides from red seaweed. Carbohydr Res 118:276–279
Meena R, Prasad K, Mehta G, Siddhanta AK (2006) Synthesis of the copolymer hydrogel κ-carrageenan-graft-PAAm: evaluation of its absorbent and adhesive properties. J Appl Polym Sci 102:5144–5153
Mishra MM, Sand A, Mishra DK, Yadav M, Behari K (2010) Free radical graft copolymerization of N-vinyl-2-pyrrolidone onto κ-carrageenan in aqueous media and applications. Carbohydr Polym 82:424–431
Mourão PA (2004) Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr Pharm Design 10:967–981
Pereira MS, Melo FR, Mouraõ PA (2002) Is there a correlation between structure and anticoagulant action of sulfated galactans and sulfated fucans? Glycobiologia 12:573–580
Pourjavadi A, Amin-Fazl MS, Barzegar S (2008) Optimization of synthesis conditions of a novel carrageenan-based superabsorbent hydrogel by Taguchi method and investigation of its metal ions adsorption. J Appl Polym Sci 107:2970–2976
Rana V, Rai P, Tiwary AK, Singh RS, Kennedy JF, Knill CJ (2011) Modified gums: approaches and applications in drug delivery. Carbohydr Polym 83:1031–1047
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237
Rocha de Souza MC, Texeira Marquez C, Guerra Dore CM, Ferreira da Silva FR, Oliveira Rocha HA, Lisboa Leite E (2007) Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J Appl Phycol 19:153–160
Ruperez P, Abrazem O, Leal JA (2002) Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. J Agric Food Chem 50:840–845
Sand A, Mishra DK, Pandey VS, Mishra MM, Behari K (2012) Synthesis of graft copolymer (CgOH-g-AGA): physicochemical properties, characterization and application. Carbohydr Polym 90:901–907
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060
Sun Z, He Y, Liang Z, Zhou W, Niu T (2009) Sulfation of (1 → 3)-β-D-glucan from the fruiting bodies of Russula virescens and antitumor activities of the modifiers. Carbohydr Polym 77:628–633
Tao YZ, Zhang L, Peter CK (2006) Physicochemical properties and antitumor activities of water-soluble native and sulfated hyperbranched mushroom polysaccharides. Carbohyd Res 341:2261–2269
Telles CBS, Sabry DA, Almeida-Lima J, Costa MSSP, Melo-Silveoira RF, Trindade ES, Sassaki GL, Wisbeck E, Furlan SA, Leite EA, Rocha HAO (2011) Sulfation of the extracellular polysaccharide produced by the edible mushroom Pleurotus sajor-caju alters its antioxidant, anticoagulant and antiproliferative properties in vitro. Carbohydr Polym 85:514–521
Truus K, Tuvikene R, Vaher M, Kailas T, Toomik P, Pehk T (2006) Structural and compositional characteristics of gelling galactan from the red alga Ahnfeltia tobuchiensis (Ahnfeltiales, the Sea of Japan). Carbohydr Polym 63:130–135
Usov AI (2011) Polysaccharides of red algae. Adv Carbohydr Chem Biochem 65:115–217
Usov AI, Yarotsky SV, Shaskov AS (1980) 13C NMR spectroscopy of red algal galactans. Biopolymers 19:977–990
Vogl H, Paper DH, Franz G (2000) Preparation of a sulfated linear (1 → 4)-β-D-galactan with variable degrees of sulfation. Carbohyd Polym 41:185–190
Wang L, Li XX, Chen ZH (2009a) Sulfated modification of the polysaccharides obtained from defatted rice bran and their antitumor activities. Int J Biol Macromol 44:211–214
Wang J, Liu L, Zhang Q, Zhang Z, Qi H, Li P (2009b) Synthesized oversulphated, acetylated and benzoylated derivatives of fucoidan extracted from Laminaria japonica and their potential antioxidant activity in vitro. Food Chem 114:1285–1290
Wang X, Wang J, Zhang J, Zhao B, Yao J, Wang Y (2010) Structure-antioxidant relationships of sulfated galactomannan from guar gum. Int J Biol Macromol 46:59–66
Wijesekara I, Pangestuti R, Kiqim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21
Yadav M, Sand A, Mishra MM, Tripathy J, Pandey VS (2012) Synthesis, characterization and applications of graft copolymer (κ-carrageenan-g-vinylsulfonic acid). Int J Biol Macromol 50:826–832
Zhang Q, Li N, Zhou G, Lu X, Xu Z, Li Z (2003) In vivo antioxidant activity of polysaccharide fraction from Porphyra haitanensis (Rhodophyta) in aging mice. Pharmacol Res 48:151–155
Zhang Z, Zhang Q, Wang J, Song H, Zhang H, Niu X (2010) Regioselective syntheses of sulfated porphyrans from Porphyra haitanensis and their antioxidant and anticoagulant activities in vitro. Carbohydr Polym 79:1124–1129
Zhao X, Xue CH, Li ZJ, Cai YP, Liu HY, Qi HT (2004) Antioxidant and hepatoprotective activities of low molecular weight sulfated polysaccharide from Laminaria japonica. J Appl Phycol 16:111–115
Zhao X, Xue CH, Li BF (2008) Study of antioxidant activities of sulfated polysaccharides from Laminaria japonica. J Appl Phycol 20:431–436
Acknowledgments
Financial support by the Dirección de Investigaciones Científicas y Tecnológicas (DICYT) of the Universidad de Santiago de Chile, Fondef-UMAG DO811163, Millennium Scientific Initiative (Grant No. P05-002), and the Basal Financing Program of the Comisión Nacional de Investigaciones Científicas y Tecnológicas (CONICYT) (Grant N°PFB-23) Chile is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuhiro, B., Barahona, T., Encinas, M.V. et al. Sulfation of agarose from subantarctic Ahnfeltia plicata (Ahnfeltiales, Rhodophyta): studies of its antioxidant and anticoagulant properties in vitro and its copolymerization with acrylamide. J Appl Phycol 26, 2011–2019 (2014). https://doi.org/10.1007/s10811-014-0297-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-014-0297-3