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

  • Roberto T. Abdala DíazEmail author
  • V. Casas Arrojo
  • M. A. Arrojo Agudo
  • C. Cárdenas
  • S. Dobretsov
  • F. L. Figueroa
Original Article

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.

Keywords

Antioxidant activity Immunomodulator Macroalgae Seaweeds Sulfated polysaccharides 

Notes

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.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there are no conflicts of interest.

Ethical Approval

Consent was obtained from all participants of the study.

References

  1. 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 23:523–528CrossRefGoogle Scholar
  2. 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 42:271–288CrossRefGoogle Scholar
  3. Amano H, Noda H (1993) Natural occurrence of denatured phycoerythrin during Porphyra cultivation. Hydrobiologia 261:535–539CrossRefGoogle Scholar
  4. 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 22:197–205CrossRefGoogle Scholar
  5. 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 21:1124–1125CrossRefGoogle Scholar
  6. Brand-Williams W, C ME, B C (1995) Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 30:25–30CrossRefGoogle Scholar
  7. 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 63:1–11CrossRefGoogle Scholar
  8. Castro R, Piazzon MC, Zarra I, Leiro J, Noya M, Lamas J (2006) Stimulation of turbot phagocytes by Ulva rigida C. agardh polysaccharides. Aquaculture 254:9–20CrossRefGoogle Scholar
  9. Chen YH, Tu CJ, Wu HT (2004) Growth-inhibitory effects of the red alga Gelidium amansii on cultured cells. Biol Pharm Bull 27:180–184CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 64:21–28CrossRefGoogle Scholar
  12. 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 17:541–552CrossRefGoogle Scholar
  13. 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 10:812–833CrossRefGoogle Scholar
  14. 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 119:913–917CrossRefGoogle Scholar
  15. 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 10:353–359CrossRefGoogle Scholar
  16. 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 55:541–548CrossRefGoogle Scholar
  17. Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144CrossRefGoogle Scholar
  18. Jeong TS, Kim YS, Oh KK (2011) Two-stage acid saccharification of fractionated Gelidium amansii minimizing the sugar decomposition. Bioresour Technol 102:10529–10534CrossRefGoogle Scholar
  19. Jiao G, Yu G, Zhang J, Ewart H (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223CrossRefGoogle Scholar
  20. 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 41:443–453CrossRefGoogle Scholar
  21. Kim S-K (2012) Handbook of marine macroalgae biotechnology and applied phycology. John Wiley &Sons, Ltd, Oxford, pp 592Google Scholar
  22. 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 146:645–654CrossRefGoogle Scholar
  23. 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 50:233–241CrossRefGoogle Scholar
  24. 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):543–553CrossRefGoogle Scholar
  25. 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 72:145–171CrossRefGoogle Scholar
  26. 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 171:4750–4757CrossRefGoogle Scholar
  27. 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 24:1537–1546CrossRefGoogle Scholar
  28. 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 30:734–738CrossRefGoogle Scholar
  29. Pereira BMR, da Silva BP, Pereira NA, Parente JP (2000) Anti-inflammatory and immunologically active polysaccharides of Periandra mediterranea. Phytochemistry 54:409–413CrossRefGoogle Scholar
  30. 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 23:1903–1909CrossRefGoogle Scholar
  31. 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 2013:1–7CrossRefGoogle Scholar
  32. 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 37:195–199CrossRefGoogle Scholar
  33. 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 26:1231–1237CrossRefGoogle Scholar
  34. 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 27:1599–1605CrossRefGoogle Scholar
  35. 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 19:153–160CrossRefGoogle Scholar
  36. Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354CrossRefGoogle Scholar
  37. 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 50:840–845CrossRefGoogle Scholar
  38. 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 85:439–444CrossRefGoogle Scholar
  39. Schepetkin IA, Quinn MT (2006) Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol 6:317–333CrossRefGoogle Scholar
  40. Schepetkin IA, Faulkner CL, Nelson-Overton LK, Wiley JA, Quinn MT (2005) Macrophage immunomodulatory activity of polysaccharides isolated from Juniperus scopolorum. Int Immunopharmacol 5:1783–1799CrossRefGoogle Scholar
  41. Sladkova T, Kostolansky F (2006) The role of cytokines in the immune response to influenza A virus infection. Acta Virol 50:151–162Google Scholar
  42. 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 1–37Google Scholar
  43. Teruya T, Takeda S, Tamaki Y, Tako M (2010) Fucoidan isolated from Laminaria angustata var. longissima induced macrophage activation. Biosci Biotechnol Biochem 74:1960–1962CrossRefGoogle Scholar
  44. Thomas NV, Kim S-K (2013) Beneficial effects of marine algal compounds in cosmeceuticals. Mar Drugs 11:146–164CrossRefGoogle Scholar
  45. Tiwari BK, Troy DJ (2015) Seaweed sustainability: food and non food applications, 1st edn. Academic Press, Amsterdam, pp 1–470Google Scholar
  46. 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–S896CrossRefGoogle Scholar
  47. 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 46:6–12CrossRefGoogle Scholar
  48. 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 29:949–982CrossRefGoogle Scholar
  49. 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 197:217–219CrossRefGoogle Scholar
  50. Yan Z, Hansson GK (2007) Innate immunity, macrophage activation, and atherosclerosis. Immunol Rev 219:187–203CrossRefGoogle Scholar
  51. Yan XJ, Nagata T, Fan X (1998) Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 52:253–262CrossRefGoogle Scholar
  52. 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 57:1862–1866CrossRefGoogle Scholar
  53. 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):117–122CrossRefGoogle Scholar
  54. 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+CrossRefGoogle Scholar
  55. Zhao X, Xue C, Cai Y, Wang D, Fang Y (2005) Study of antioxidant activities of fucoidan from Laminaria japonica. High Technol Lett 11:91–94Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Roberto T. Abdala Díaz
    • 1
    Email author
  • V. Casas Arrojo
    • 1
  • M. A. Arrojo Agudo
    • 1
  • C. Cárdenas
    • 2
  • S. Dobretsov
    • 3
    • 4
  • F. L. Figueroa
    • 1
  1. 1.Ecology Department, Faculty of SciencesMalaga UniversityMalagaSpain
  2. 2.Biochemistry Department, Faculty of SciencesMalaga UniversityMalagaSpain
  3. 3.Department of Marine Science and Fisheries, College of Agricultural and Marine SciencesSultan Qaboos UniversityAl KhoudOman
  4. 4.Center of Excellence in Marine BiotechnologySultan Qaboos UniversityAl KhoudOman

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