Skip to main content
Log in

Immunomodulatory and Antioxidant Activities of Sulfated Polysaccharides from Laminaria ochroleuca, Porphyra umbilicalis, and Gelidium corneum

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Seaweeds of the genera Laminaria, Gelidium, and Porphyra have been used in both food and non-food industries due to their unique properties and characteristic biological activity. This study assesses the antioxidant activity and immunomodulatory properties of the acidic polysaccharides extracted from Laminaria ochroleuca, Porphyra umbilicalis, and Gelidium corneum collected in the Atlantic coast of Tarifa (Cadiz, Spain). The proliferation of murine cell line RAW 264 decreased with increasing concentration of polysaccharides of the three algal species. The highest both antioxidant (25.69 μmol TE g−1 DW) and immunomodulatory activities were observed in the sulfated polysaccharides of L. ochroleuca compared to that of P. umbilicalis and G. corneum. Sulfated polysaccharides of L. ochroleuca presented high potential anticancer activity in cell lines of human colon cancer HTC-116 (IC50 = 0.44 mg mL−1), human malignant melanoma G-361 (IC50 = 5.42 mg mL−1), breast adenocarcinoma human MCF-7 (IC50 = 8.32 mg mL−1), and human leukemia U-937 (IC50 = 3.72 mg mL−1). It is concluded that metabolites of L. ochroleuca can offer significant advantages for the pharmaceutical industry, particularly when macrophage activation is required.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abdala-Díaz RT, Chabrillón M, Cabello-Pasini A et al (2011) Characterization of polysaccharides from Hypnea spinella (Gigartinales) and Halopithys incurva (Ceramiales) and their effect on RAW 264.7 macrophage activity. J Appl Phycol 23:523–528

    Article  CAS  Google Scholar 

  • Álvarez-Gómez F, Korbee N, Figueroa FL (2016) Analysis of antioxidant capacity and bioactive compounds in marine macroalgal and lichenic extracts using different solvents and evaluation methods. Cienc Mar 42:271–288

    Article  CAS  Google Scholar 

  • Amano H, Noda H (1993) Natural occurrence of denatured phycoerythrin during Porphyra cultivation. Hydrobiologia 261:535–539

    Article  Google Scholar 

  • Ann-Chang Cheng C-WT (2007) The immunostimulatory effects of sodium alginate and iota-carrageenan on orange-spotted grouper Epinephelus coicoides and its resistance against Vibrio alginolyticus. Fish Shellfish Immunol 22:197–205

    Article  CAS  PubMed  Google Scholar 

  • Bonneville M, Saint-Mezard P, Benetiere J, Hennino A, Pernet I, Denis A, Nicolas JF (2007) Laminaria ochroleuca extract reduces skin inflammation. J Eur Acad Dermatol Venereol 21:1124–1125

    Article  CAS  PubMed  Google Scholar 

  • Brand-Williams W, C ME, B C (1995) Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 30:25–30

    Article  Google Scholar 

  • Cabassi F, Casu B, Perlin AS (1978) Infrared absorption and Raman scattering of sulfate groups of heparin and related glycosaminoglycans in aqueous solution. Carbohydr Res 63:1–11

    Article  CAS  Google Scholar 

  • Castro R, Piazzon MC, Zarra I, Leiro J, Noya M, Lamas J (2006) Stimulation of turbot phagocytes by Ulva rigida C. agardh polysaccharides. Aquaculture 254:9–20

    Article  CAS  Google Scholar 

  • Chen YH, Tu CJ, Wu HT (2004) Growth-inhibitory effects of the red alga Gelidium amansii on cultured cells. Biol Pharm Bull 27:180–184

    Article  CAS  PubMed  Google Scholar 

  • Cofrades S, López-López I, Bravo L et al (2010) Nutritional and antioxidant properties of different brown and red Spanish edible seaweeds. Food Sci Technol Int 16:361–370. https://doi.org/10.1177/1082013210367049A

    Article  CAS  PubMed  Google Scholar 

  • Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DA, Ciara RBG, Nobre LTDB, Costa MSSP, Almeida-Lima J, Farias EHC, Leite EL, Rocha HAO (2010) Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother 64:21–28

    Article  CAS  Google Scholar 

  • Cumashi NA, Ushakova ME, Preobrazhenskaya A, D’Incecco A, Piccoli L, Totani N, Tinari GE, Morozevich AE, Berman MI, Bilan (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17:541–552

    Article  CAS  PubMed  Google Scholar 

  • D’Orazio N, Gammone MA, Gemello E, de Girolamo M, Cusenza S, Riccioni G (2012) Marine bioactives: pharmacological properties and potential applications against inflammatory diseases. Mar Drugs 10:812–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denis C, Morançais M, Li M, Deniaud E, Gaudin P, Wielgosz-Collin G, Barnathan G, Jaouen P, Fleurence J (2010) Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chem 119:913–917

    Article  CAS  Google Scholar 

  • Galland-Irmouli A-V, Fleurence J, Lamghari R, Luçon M, Rouxel C, Barbaroux O, Bronowicki JP, Villaume C, Guéant JL (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J Nutr Biochem 10:353–359

    Article  CAS  PubMed  Google Scholar 

  • Islam MN, Ishita IJ, Jin SE, Choi RJ, Lee CM, Kim YS, Jung HA, Choi JS (2013) Anti-inflammatory activity of edible brown alga Saccharina japonica and its constituents pheophorbide a and pheophytin a in LPS-stimulated RAW 264.7 macrophage cells. Food ChemToxicol 55:541–548

    Article  CAS  Google Scholar 

  • Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144

    Article  CAS  Google Scholar 

  • Jeong TS, Kim YS, Oh KK (2011) Two-stage acid saccharification of fractionated Gelidium amansii minimizing the sugar decomposition. Bioresour Technol 102:10529–10534

    Article  CAS  PubMed  Google Scholar 

  • Jiao G, Yu G, Zhang J, Ewart H (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karsten U, Sawall T, Hanelt D, Bischop K, Flores-Moya A, Figueroa FL, Wiencke C (1998) Contents of UV absorbing mycosporine-like aminoacids in macroalgae from polar to warm-temperate regions. Bot Mar 41:443–453

    Article  CAS  Google Scholar 

  • Kim S-K (2012) Handbook of marine macroalgae biotechnology and applied phycology. John Wiley &Sons, Ltd, Oxford, pp 592

  • Korbee N, Huovinen P, Figueroa FL, Aguilera J, Karsten U (2005) Availability of ammonium influences photosynthesis and the accumulation of mycosporine-like aminoacids in two Porphyra species (Bangiales, Rhodophyta). Mar Biol 146:645–654

    Article  CAS  Google Scholar 

  • Lourenço SO, Barbarino E, De-Paula JC, Pereira LO d S, Marquez UML (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241

    Article  Google Scholar 

  • Malyarenko OS, Usoltseva RV, Shevchenko NM, Isakov VV, Zvyagintseva TN, Ermakova SP (2017) In vitro anticancer activity of the laminarans from Far Eastern brown seaweeds and their sulfated derivatives. J Appl Phycol 29(1):543–553

    Article  CAS  Google Scholar 

  • Moure A, Cruz JM, Franco D, Domı́nguez JM, Sineiro J, Domı́nguez H, José Núñez Ḿ, Parajó JC (2001) Natural antioxidants from residual sources. Food Chem 72:145–171

    Article  CAS  Google Scholar 

  • Nagabhushanam V, Solache A, Ting LM, Escaron CJ, Zhang JY, Ernst JD (2003) Innate inhibition of adaptive immunity: Mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN-gamma. J Immunol 171:4750–4757

    Article  CAS  PubMed  Google Scholar 

  • Parages ML, Rico RM, Abdala-Díaz RT, Chabrillón M, Sotiroudis TG, Jiménez C (2012) Acidic polysaccharides of Arthrospira (Spirulina) platensis induce the synthesis of TNF-α in RAW macrophages. J Appl Phycol 24:1537–1546

    Article  CAS  Google Scholar 

  • Park H-K, Kim I-H, Kim J, Nam T-J (2012) Induction of apoptosis by laminarin, regulating the insulin-like growth factor-IR signaling pathways in HT-29 human colon cells. Int J Mol Med 30:734–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira BMR, da Silva BP, Pereira NA, Parente JP (2000) Anti-inflammatory and immunologically active polysaccharides of Periandra mediterranea. Phytochemistry 54:409–413

    Article  CAS  PubMed  Google Scholar 

  • Pereira L, Amado AM, Critchley AT, van de Velde F, Ribeiro-Claro PJA (2009) Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocoll 23:1903–1909

    Article  CAS  Google Scholar 

  • Pereira L, Gheda SF, Ribeiro-Claro PJA (2013) Analysis by vibrational spectroscopy of seaweed polysaccharides with potential use in food, pharmaceutical, and cosmetic industries. Int J Carbohydr Chem 2013:1–7

    Article  CAS  Google Scholar 

  • Qi HM, Zhang QB, Zhao TT, Chen R, Zhang H, Niu X, Li Z (2005) Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. Int J Biol Macromol 37:195–199

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rengasamy KRR, Amoo SO, Aremu AO, Stirk WA, Gruz J, Šubrtová M, Doležal K, van Staden J (2015) Phenolic profiles, antioxidant capacity, and acetyl cholinesterase inhibitory activity of eight South African seaweeds. J Appl Phycol 27:1599–1605

    Article  CAS  Google Scholar 

  • Rocha de Souza MC, Marques CT, Guerra-Dore CM et al (2007) Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J Appl Phycol 19:153–160

    Article  CAS  Google Scholar 

  • Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354

    Article  Google Scholar 

  • Rupérez P, Ahrazem 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

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Article  CAS  Google Scholar 

  • Schepetkin IA, Quinn MT (2006) Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol 6:317–333

    Article  CAS  PubMed  Google Scholar 

  • Schepetkin IA, Faulkner CL, Nelson-Overton LK, Wiley JA, Quinn MT (2005) Macrophage immunomodulatory activity of polysaccharides isolated from Juniperus scopolorum. Int Immunopharmacol 5:1783–1799

    Article  CAS  PubMed  Google Scholar 

  • Sladkova T, Kostolansky F (2006) The role of cytokines in the immune response to influenza A virus infection. Acta Virol 50:151–162

    CAS  PubMed  Google Scholar 

  • Stengel DB, Connan S (2015) Marine algae: a source of biomass for biotechnological applications. In: Stengel DB, Connan S (eds) Natural products from marine algae, vol 1308. Springer, New York, pp 1–37

  • Teruya T, Takeda S, Tamaki Y, Tako M (2010) Fucoidan isolated from Laminaria angustata var. longissima induced macrophage activation. Biosci Biotechnol Biochem 74:1960–1962

    Article  CAS  PubMed  Google Scholar 

  • Thomas NV, Kim S-K (2013) Beneficial effects of marine algal compounds in cosmeceuticals. Mar Drugs 11:146–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari BK, Troy DJ (2015) Seaweed sustainability: food and non food applications, 1st edn. Academic Press, Amsterdam, pp 1–470

  • Vijayabaskar P, Vaseela N (2012) In vitro antioxidant properties of sulfated polysaccharide from brown marine algae Sargassum tenerrimum. Asian Pac J Trop Dis 2:S890–S896

    Article  CAS  Google Scholar 

  • Wang J, Zhang Q, Zhang Z, Song H, Li P (2010) Potential antioxidant and anticoagulant capacity of low molecular weight fucoidan fractions extracted from Laminaria japonica. Int J Biol Macromol 46:6–12

    Article  CAS  PubMed  Google Scholar 

  • Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982

    Article  CAS  PubMed  Google Scholar 

  • Wiencke C, Gómez I, Pakker H, Flores-Moya A, Alatamirano M, Hanelt D, Bischof K, Figueroa FL (2000) Impact of UV radiation on viability, photosynthetic characteristics and DNA on algal zoospores: implications for depth zonation. Mar Ecol Prog Ser 197:217–219

    Article  Google Scholar 

  • Yan Z, Hansson GK (2007) Innate immunity, macrophage activation, and atherosclerosis. Immunol Rev 219:187–203

    Article  CAS  PubMed  Google Scholar 

  • Yan XJ, Nagata T, Fan X (1998) Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 52:253–262

    Article  CAS  PubMed  Google Scholar 

  • Yoshizawa Y, Enomoto A, Todoh H, Ametani A, Kaminogawa S (1993) Activation of murine macrophages by polysaccharide fractions from marine-algae (Porphyra-yezoensis). Biosci Biotechnol Biochem 57:1862–1866

    Article  CAS  PubMed  Google Scholar 

  • Zhai Q, Li X, Yang Y, Yu L, Yao Y (2014) Antitumor activity of a polysaccharide fraction from Laminaria japonica on U14 cervical carcinoma-bearing mice. Tumor Biol 35(1):117–122

    Article  CAS  Google Scholar 

  • Zhang QB, Li N, Liu XG, Zhao Z, Li Z, Xu Z (2004) The structure of a sulfated galactan from Porphyra haitanensis and its in vivo antioxidant activity. Carbohydr Res 339:105–10+

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Xue C, Cai Y, Wang D, Fang Y (2005) Study of antioxidant activities of fucoidan from Laminaria japonica. High Technol Lett 11:91–94

    Google Scholar 

Download references

Acknowledgements

We want to express our gratitude to the Photobiology and Biotechnology of Aquatic Organisms (FYBOA) research group (RNM-295) for their financial support. We also want to thank Dr. Luis Alemany and Dr. María de los Ángeles Vargas (Chemical Engineering Department, UMA) for their technical assistance in the FT-IR analysis and D. Augusto Martínez García, Technical Manager of the Chemical Analysis and Material Characterization Area: Elemental and Thermal Analysis Unit of the SCAI (Central Research Support Service) of the University of Malaga, for the technical assistance in the elementary analysis of the samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roberto T. Abdala Díaz.

Ethics declarations

Conflict of Interest

The authors declare that there are no conflicts of interest.

Ethical Approval

Consent was obtained from all participants of the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdala Díaz, R.T., Casas Arrojo, V., Arrojo Agudo, M.A. et al. Immunomodulatory and Antioxidant Activities of Sulfated Polysaccharides from Laminaria ochroleuca, Porphyra umbilicalis, and Gelidium corneum. Mar Biotechnol 21, 577–587 (2019). https://doi.org/10.1007/s10126-019-09905-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09905-x

Keywords

Navigation