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Carrageenans from Sarcothalia crispata and Gigartina skottsbergii: Structural Analysis and Interpolyelectrolyte Complex Formation for Drug Controlled Release

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Abstract

The aims of the present study were to characterize for the first time the carrageenan extracted from cystocarpic stage of S. crispata collected in the Patagonian coast of Argentina, and to prepare interpolyelectrolytic complexes (IPECs) between the polysaccharide extracted from cystocarpic stage of Sarcothalia crispata and Gigartina skottsbergii thalli, and basic butylated methacrylate copolymer (Eudragit E), in order to test their potential for the controlled release of ibuprofen as model drug. The structural determination revealed that the polysaccharides extracted from S. crispata and G. skottsbergii were mainly constituted by κ-carrageenan, particularly in the case of G. skottsbergii; however, significant amounts of ι- and ν-carrageenan were also detected in both polygalactans. The differences in diad composition and possibly in their distribution along the polysaccharide chain of both carrageenans would favor a different arrangement in the resulting IPEC structure. The smaller pores observed by scanning electron microscopy in the IPEC of S. crispata suggest that the kinks in the polysaccharide backbone are evenly distributed, resulting in a slower ibuprofen release compared to the IPEC of G. skottsbergii.

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References

  • Bakaic E, Smeets NMB, Dorrington H, Hoare T (2015) “Off-the-shelf” thermoresponsive hydrogel design: tuning hydrogel properties by mixing precursor polymers with different lower-critical solution temperatures. RSC Adv 5:33364–33376

    Article  CAS  Google Scholar 

  • Barahona T, Prado HJ, Bonelli PR, Cukierman AL, Fissore EL, Gerschenson LN, Matulewicz MC (2015) Cationization of kappa- and iota-carrageenan. Characterization and properties of amphoteric polysaccharides. Carbohydr Polym 126:70–77

    Article  CAS  Google Scholar 

  • Campo VL, Kawano DF, da Silva DB Jr, Carvalho I (2009) Carrageenans: biological properties, chemical modifications and structural analysis—a review. Carbohydr Polym 77:167–180

    Article  CAS  Google Scholar 

  • Cases MR, Cerezo AS, Stortz CA (1995) Separation and quantitation of enantiomeric galactoses and their mono-O-methylethers as their diastereomeric acetylated 1-deoxy-1-(2-hydroxypropylamino) alditols. Carbohydr Res 269:333–341

    Article  CAS  Google Scholar 

  • Ciancia M, Matulewicz MC, Finch P, Cerezo AS (1993) Determination of the structures of cystocarpic carrageenans from Gigartina skottsbergii by methylation analysis and NMR spectroscopy. Carbohydr Res 238:241–248

    Article  CAS  Google Scholar 

  • Ciucanu I, Kerek K (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 134:209–217

    Article  Google Scholar 

  • Claridge TDW (1999) High-resolution NMR techniques in organic chemistry. Tetrahedron organic chemistry series, vol 19. Elsevier B.V., Amsterdam

    Chapter  Google Scholar 

  • Dalmoro A, Sitenkov AY, Cascone S, Lamberti G, Barba AA, Moustafine RI (2017) Hydrophilic drug encapsulation in shell-core microcarriers by two stage polyelectrolyte complexation method. Int J Pharm 518:50–58

    Article  CAS  Google Scholar 

  • Dautzenberg H, Gao Y, Hahn M (2000) Formation, structure, and temperature behavior of polyelectrolyte complexes between ionically modified thermosensitive polymers. Langmuir 16:9070–9081

    Article  CAS  Google Scholar 

  • Digimizer (2018) Image analysis software version 5.3.3. MedCalc Software bvba, Ostend, Belgium. https://www.digimizer.com/

  • Dodgson KS, Price RG (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Durako MJ, Dawes CJ (1980) A comparative seasonal study of two populations of Hypnea musciformis from the East and West Coasts of Florida, USA. I. Growth and chemistry. Mar Biol 59:151–156

    Article  CAS  Google Scholar 

  • Falshaw R, Bixler HJ, Johndro K (2001) Structure and performance of commercial kappa-2 carrageenan extracts 1. Structure analysis. Food Hydrocoll 15:441–452

    Article  CAS  Google Scholar 

  • Garbary DJ, Tompkins E, White K, Corey P, Kim JK (2011) Temporal and spatial variation in the distribution of life history phases of Chondrus crispus (Gigartinales, Rhodophyta). Algae 26:61–71

    Article  Google Scholar 

  • Hennink WE, van Nostrum CF (2012) Novel crosslinking methods to design hydrogels. Adv Drug Deliv Rev 64:223–236

    Article  Google Scholar 

  • Huang X, Brazel CS (2001) On the importance and mechanisms of burst release in matrix-controlled drug delivery systems. J Control Release 73:121–136

    Article  CAS  Google Scholar 

  • Jouanneau D, Boulenguer P, Mazoyer J, Helbert W (2011) Hybridity of carrageenans water- and alkali-extracted from Chondracanthus chamissoi, Mazzaella laminarioides, Sarcothalia crispata and Sarcothalia radula. J Appl Phycol 23:105–114

    Article  CAS  Google Scholar 

  • Khan AK, Saba AU, Nawazish S, Akhtar F, Rashid R, Mir S, Nasir B, Iqbal F, Afzal F, Pervaiz F, Murtaza G (2017) Carrageenan based bionanocomposites as drug delivery tool with special emphasis on the influence of ferromagnetic nanoparticles. Oxidative Med Cell Longev. 1–13

  • Knutsen SH, Myslabodski DE, Larsen B, Usov AI (1994) A modified system of nomenclature for red algal galactans. Bot Mar 37:163–169

    Article  CAS  Google Scholar 

  • Li L, Ni R, Shao Y, Mao S (2014) Carrageenan and its applications in drug delivery. Carbohydr Polym 103:1–11

    Article  CAS  Google Scholar 

  • Lowman MA (2000) In: Wise DL (ed) Handbook of pharmaceutical controlled release technology. Marcel Dekker, New York

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Martínez WA, Caves JM, Ravi S, Li W, Chaikof EL (2014) Effects of crosslinking on the mechanical properties, drug release and cytocompatibility of protein polymers. Acta Biomater 10:26–33

    Article  Google Scholar 

  • Matsuhiro B (1996) Vibrational spectroscopy of seaweed galactans. Hydrobiologia 326:481–489

    Article  Google Scholar 

  • Matulewicz MC, Ciancia M, Noseda MD, Cerezo AS (1989) The carrageenan system from tetrasporic and cystocarpic stages of Gigartina skottsbergii. Phytochemistry 28:2937–2941

    Article  CAS  Google Scholar 

  • Matulewicz MC, Ciancia M, Noseda MD, Cerezo AS (1990) Methylation analysis of carrageenans from tetrasporic and cystocarpic stages of Gigartina skottsbergii. Phytochemistry 29:3407–3410

    Article  CAS  Google Scholar 

  • McHugh DJ (2003) A guide to the seaweed industry FAO Fisheries Technical Paper 441. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Moustafine RI, Zaharov IM, Kemenova VA (2006) Physicochemical characterization and drug release properties of Eudragit® E PO/Eudragit® L 100-55 interpolyelectrolyte complexes. Eur J Pharm Biopharm 63:26–36

    Article  CAS  Google Scholar 

  • Moustafine RI, Salachova AR, Frolova ES, Kemenova VA, van den Mooter G (2009) Interpolyelectrolyte complexes of Eudragit E PO with sodium alginate as potential carriers for colonic drug delivery: monitoring of structural transformation and composition changes during swell ability and release evaluating. Drug Dev Ind Pharm 35:1439–1451

    Article  CAS  Google Scholar 

  • Moustafine RI, Sitenkova AY, Bukhovetsa AV, Nasibullina SF, Appeltans B, Kabanova TV, Khutoryanskiy VV, Van den Mooter G (2017) Indomethacin-containing interpolyelectrolyte complexes based on Eudragit1 E PO/S 100 copolymers as a novel drug delivery system. Int J Pharm 524:121–133

    Article  CAS  Google Scholar 

  • Navarro DA, Stortz CA (2003) Determination of the configuration of 3,6-anhydrogalactose and cyclizable α-galactose 6-sulfate units in red seaweed galactans. Carbohydr Res 338:211–218

    Article  Google Scholar 

  • Peppas NA (1985) Analysis of Fickian and non-Fickian drug release from polymers. Pharm Acta Helv 60:100–111

    Google Scholar 

  • Peppas NA, Sahlin JJ (1989) A simple equation for the description of solute release. III. Coupling of diffusion and relaxation. Int J Pharm 57:169–172

    Article  CAS  Google Scholar 

  • Pereira L, Amado AM, Critchley AT, van de Velde F, Ribeiro-Claro PJA (2011) Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocoll 23:1903–1909

    Article  Google Scholar 

  • Pérez Recalde M, Canelón DJ, Compagnone RS, Matulewicz MC, Cerezo AS, Ciancia M (2016) Carrageenan and agaran structures from the red seaweed Gymnogongrus tenuis. Carbohydr Polym 136:1370–1378

    Article  CAS  Google Scholar 

  • Piriz ML (1996) Phenology of a Gigartina skottsbergii Setchell et Gardner population in Chubut Province (Argentina). Bot Mar 39:311–316

    Article  Google Scholar 

  • Prado HJ, Matulewicz MC (2014) Cationization of polysaccharides; a path to greener derivatives with many industrial applications. Eur Polym J 52:53–75

    Article  CAS  Google Scholar 

  • Prado HJ, Matulewicz MC, Bonelli P, Cukierman AL (2008a) Basic butylated methacrylate copolymer/kappa-carrageenan interpolyelectrolyte complex: preparation, characterization and drug release behaviour. Eur J Pharm Biopharm 70:171–178

    Article  CAS  Google Scholar 

  • Prado HJ, Ciancia M, Matulewicz MC (2008b) Agarans from the red seaweed Polysiphonia nigrescens (Rhodomelaceae, Ceramiales). Carbohydr Res 343:711–718

    Article  CAS  Google Scholar 

  • Prado HJ, Matulewicz MC, Bonelli P, Cukierman AL (2009) Preparation and characterization of a novel starch-based interpolyelectrolyte complex as matrix for controlled drug release. Carbohydr Res 344:1325–1331

    Article  CAS  Google Scholar 

  • Rees DA, Morris ER, Thom D, Marden JK (1982) In: Aspinall GO (ed) The polysaccharides, vol 1. Academic Press, Inc, New York

  • Reis RP, Yoneshigue-Valentin Y, Pereira dos Santos C (2008) Spatial and temporal variation of Hypnea musciformis carrageenan (Rhodophyta–Gigartinales) from natural beds in Rio de Janeiro State, Brazil. J Appl Phycol 20:1–8

    Article  Google Scholar 

  • Rinaudo M (2008) Main properties and current applications of some polysaccharides as biomaterials. Polym Int 57:397–430

    Article  CAS  Google Scholar 

  • Siepmann J, Siepmann F (2012) Modeling diffusion controlled drug delivery. J Control Release 161:351–362

    Article  CAS  Google Scholar 

  • Stevenson TT, Furneaux RH (1991) Chemical methods for the analysis of sulphated galactans from red algae. Carbohydr Res 210:277–298

    Article  CAS  Google Scholar 

  • Stortz CA, Cerezo AS (2000) Novel findings in carrageenans, agaroids and “hybrid” red seaweed galactans. Curr Top Phytochem 4:121–134

    CAS  Google Scholar 

  • Usov AI (2011) Polysaccharides of red algae. Adv Carbohydr Chem Biochem 65:115–217

    Article  CAS  Google Scholar 

  • Wen JL, Sun SL, Xue BL, Sun RC (2013) Recent advances in characterization of lignin polymer by solution-state nuclear magnetic resonance (NMR) methodology. Materials 6:359–391

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are indebted to Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET) PIP 112-201101-00208 and 112-2015 01-00510, Secretaría de Ciencia y Tecnología de la Universidad Nacional del Sur, PGI 24/B246 and Secretaría de Ciencia y Técnica, Universidad de Buenos Aires, UBACyT 20020130100216BA. MHH is a Fellow Member of CONICET. HJP, PIL, and MCM are Research Members of CONICET.

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Correspondence to María Cristina Matulewicz.

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Fig. S1

FTIR of the carrageenans from S. crispata (SC), G. skottsbergii (GS), Eudragit E (EE) and the corresponding IPECs (PNG 237 kb)

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Hughes, M.H., Prado, H.J., Rodríguez, M.C. et al. Carrageenans from Sarcothalia crispata and Gigartina skottsbergii: Structural Analysis and Interpolyelectrolyte Complex Formation for Drug Controlled Release. Mar Biotechnol 20, 706–717 (2018). https://doi.org/10.1007/s10126-018-9842-4

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