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Biosprospecting potential of kelp (Laminariales, Phaeophyceae) from Baja California Peninsula: phenolic content, antioxidant properties, anti-inflammatory, and cell viability

  • Paola A. Tenorio-Rodríguez
  • Hugo Esquivel-Solis
  • Jesús I. Murillo-Álvarez
  • Felipe Ascencio
  • Ángel I. Campa-CórdovaEmail author
  • Carlos AnguloEmail author
Article

Abstract

To explore the potential of two kelps as natural sources of bioactive compounds, this study evaluated total phenolic content, antioxidant properties, anti-inflammatory, and cell viability activities of polyphenol-enriched fractions from Eisenia arborea and Macrocystis pyrifera. Overall, the fractions from E. arborea had higher antioxidant properties than M. pyrifera. However, two fractions from E. arborea and M. pyrifera showed the strongest antioxidant activities among 12 fractions tested by polyphenol content, 1,1-diphenyl-2-picryl-hydrazyl (DPPH), and Ferric reducing antioxidant power (FRAP) assays. Several fractions upregulated IL-10 gene expression and downregulated TNF-α and iNOS mRNA in RAW 264.7 cells. Remarkably, most of the fractions at the highest concentration (1280 μg mL−1) showed non-toxic effect on L9S29 cell line. Analysis of fractions by Fourier transformed infrared from attenuated total reflectance (FTIR-ATR) and by ultra-performance liquid chromatography coupled to electrospray ionization quadrupole time of flight mass spectrometry (UPLC-ESI-Q-TOF-MS) suggested the presence of phlorotannins, such as phloroeckol, fucophloroethol, and phlorofucofuroeckol. In conclusion, the polyphenol content (phlorotannins) varied among fractions of macroalgal species and influencing their biological properties, which represent natural sources for health promotion.

Keywords

Eisenia arborea Macrocystis pyrifera Phlorotannins Antioxidant activity Anti-inflammatory effects Polyphenols 

Notes

Acknowledgments

The authors are grateful for the financial support by CONACYT Mexico (INFR-2014-01/225924 and PDCPN2014-01/248033). P.A.T.R. is a recipient of a study fellowship (CONACYT); to D. Fischer for editorial services in English.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Arvizu DL, Rodríguez YE, Hernández G, Murillo JI (2007) Chemical constituents of Eisenia arborea Areschoug from Baja California Sur, Mexico. Investig Mar 35:63–66CrossRefGoogle Scholar
  2. Ashley NT, Weil ZM, Nelson RJ (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385–406CrossRefGoogle Scholar
  3. Benzie IF, Strain JJ (1996) Ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefGoogle Scholar
  4. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 28:25–30CrossRefGoogle Scholar
  5. Caamal-Fuentes E, Chale-Dzul J, Moo-Puc R, Freile-Pelegrin Y, Robledo D (2013) Bioprospecting of brown seaweed (Ochrophyta) from the Yucatan Peninsula: cytotoxic, antiproliferative, and antiprotozoal activities. J Appl Phycol 26:1009–1017CrossRefGoogle Scholar
  6. Chan PM, Tan YS, Chua KH, Sabaratnam V, Kuppusamy UR (2015) Attenuation of inflammatory mediators (TNF-α and nitric oxide) and up-regulation of IL-10 by wild and domesticated basidiocarps of Amauroderma rugosum (Blume and T. Nees) Torrend in LPS-stimulated RAW264.7 cells. PLoS One 10:e0139593CrossRefGoogle Scholar
  7. Číž M, Čížová H, Denev P, Kratchanova M, Slavov A, Lojek A (2010) Different methods for control and comparison of the antioxidant properties of vegetables. Food Control 21:518–523CrossRefGoogle Scholar
  8. Coates J (2000) Interpretation of infrared spectra, a practical approach. Encyclopedia of analytical chemistry. In: R.A Meyers (ed) John Wiley & Sons Ltd Chichester UK pp 10815–10837Google Scholar
  9. Ferreres F, Lopes G, Gil-Izquierdo A, Andrade PB, Sousa C, Mouga T, Valentão P (2012) Phlorotannins extracts from Fucales profiled by HPLC-DAD-ESI-MSn: approaches to hyaluronidase inhibitory capacity and antioxidant properties. Mar Drugs 10:2766–2278CrossRefGoogle Scholar
  10. Gambato G, Baroni EG, García CS, Frassini R, Frozza COS, Pereira CMP, Fujii MT, Colepicolo P, Lambert APF, Henriques JAP, Roesch-Ely M (2014) Brown algae Himantothallus grandifolius (Desmarestiales, Phaeophyceae) suppresses proliferation and promotes apoptosis-mediated cell death in tumor cells. Adv Biol Chem 4:98–108CrossRefGoogle Scholar
  11. Giustarini D, Rossi R, Milzani A, Dalle-Donne I (2008) Nitrite and nitrate measurement by Griess reagent in human plasma: evaluation of interferences and standardization. Methods Enzymol 440:361–380CrossRefGoogle Scholar
  12. Heffernan N, Smyth TJ, Soler-Villa A, Fitzgerald RJ, Brunton NP (2015) Phenolic content and antioxidant activity of fractions obtained from selected Irish macroalgae species (Laminaria digitata, Fucus serratus, Gracilaria gracilis, and Codium fragile). J Appl Phycol 27:519–530CrossRefGoogle Scholar
  13. Hemat RAS (2007) Fat and muscle dysfunction. In: Hemat RAS (ed) Andropathy. Urotext, Dublin, pp 83–85Google Scholar
  14. Hernández-Carmona G, García O, Robledo D, Foster M (2000) Restoration techniques for Macrocystis pyrifera (Phaeophyceae) populations at the southern limit of their distribution in Mexico. Bot Mar 43:273–284CrossRefGoogle Scholar
  15. Hernández-Carmona G, Carrillo-Domínguez S, Arvizu-Higuera DL, YE Rodriguez-Montesinos YE, Murillo-Álvarez JI, Muñoz-Ochoa M, Castillo-Domínguez RM (2009) Monthly variation in the chemical composition of Eisenia arborea J.E. Areschoug. J Appl Phycol 21:607–616CrossRefGoogle Scholar
  16. Hou X, Zhang J, Ahmad H, Zhang H, Xu Z, Wang T (2014) Evaluation of antioxidant activities of ampelopsin and its protective effect in lipopolysaccharide-induced oxidative stress piglets. PLoS One 9:e108314CrossRefGoogle Scholar
  17. International Organization for Standardization (2009) Biological evaluation of medical devices-part 5: tests for in vitro cytotoxicity GenevaGoogle Scholar
  18. Jung WK, Heo SJ, Jeon YJ, Lee CM, Park YM, Byun HG, Choi YH, Park SG, Choi IW (2009) Inhibitory effects and molecular mechanism of dieckol isolated from marine brown alga on COX-2 and iNOS in microglial cells. J Agric Food Chem 57:4439–4446CrossRefGoogle Scholar
  19. Kellogg J, Grace MH, Lila MA (2014) Phlorotannins from Alaskan seaweed inhibit carbolytic enzyme activity. Mar Drugs 12:5277–5294CrossRefGoogle Scholar
  20. Khanavi M, Nabavi M, Sadati N, Shams Ardekani M, Sohrabipour J, Nabavi SM, Ghaeli P, Ostad SN (2010) Cytotoxic activity of some marine brown algae against cancer cell lines. Biol Res 43:31–37CrossRefGoogle Scholar
  21. Kim AR, Lee MS, Shin TS, Hua H, Jang BC, Choi JS, Byun DS, Utsuki T, Ingram D, Kim HR (2011) Phlorofucofuroeckol A inhibits the LPS-stimulated iNOS and COX-2 expressions in macrophages via inhibition of NF-jB, Akt, and p38 MAPK. Toxicol in Vitro 25:1789–1795CrossRefGoogle Scholar
  22. Kindleysides S, Quek SY, Miller MR (2012) Inhibition of fish oil oxidation and the radical scavenging activity of New Zealand seaweed extracts. Food Chem 133:1624–1631CrossRefGoogle Scholar
  23. Kuda T, Kunii T, Goto H, Suzuki T, Yano T (2007) Varieties of antioxidant and antibacterial properties of Ecklonia stolonifera and Ecklonia kurome products harvested and processed in the Noto Peninsula, Japan. Food Chem 103:900–905CrossRefGoogle Scholar
  24. Kwon TH, Kim TW, Kim CG, Park NH (2013) Antioxidant activity of various solvent fractions from edible brown alga, Eisenia bicyclis and its active compounds. J Food Sci 78C:679–684CrossRefGoogle Scholar
  25. Leyton A, Pezoa-Conte R, Barriga A, Buschmann AH, Mäki-Arvela P, Mikkola JP, Lienqueo ME (2016) Identification and efficient extraction method of phlorotannins from the brown seaweed Macrocystis pyrifera using an orthogonal experimental design. Algal Res 16:201–208CrossRefGoogle Scholar
  26. Li HB, Cheng KW, Wong CC, Fan KW, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776CrossRefGoogle Scholar
  27. Li Y, Qian ZJ, Ryu B, Lee SH, Kim MM, Kim SK (2009) Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg Med Chem 17:1963–1973CrossRefGoogle Scholar
  28. Lim SN, Cheung PCK, Ooi VEC, Ang PO (2002) Evaluation of antioxidative activity of extracts from a brown seaweed, Sargassum siliquastrum. J Agric Food Chem 50:3862–3866CrossRefGoogle Scholar
  29. Machu L, Misurcova L, Ambrozova JA, Orsavova J, Mlcek J, Sochor J, Jurikova T (2015) Phenolic content and antioxidant capacity in algal food products. Molecules 20:1118–1133CrossRefGoogle Scholar
  30. Matanjun P, Mohamed S, Mustapha NM, Muhamad K, Ming CH (2008) Antioxidant activites and phenolics content of eight species of seaweeds from North Borneo. J Appl Phycol 20:367–373CrossRefGoogle Scholar
  31. Meenakshi S, Umayaparvathi S, Arumugam M, Balasubramanian T (2012) In vitro antioxidant properties and FTIR analysis of two seaweeds of Gulf of Mannar. Asian Pac J Trop Biomed 1:S66–70Google Scholar
  32. Mueller-Harvey I (2001) Analysis of hydrolysable tannins. Anim Feed Sci Tech 91:3–20CrossRefGoogle Scholar
  33. Muñoz-Ochoa M, Murillo-Álvarez JI, Zermeño-Cervantes LA (2010) Screening of extracts of algae from Baja California Sur, Mexico as reversers of the antibiotic resistance of some pathogenic bacteria. Eur Rev Med Pharmacol Sci 14:739–747Google Scholar
  34. O’Sullivan AM, O’Callaghan YC, O’Grady MN, Queguineur B, Hanniffy D, Troy DJ, Kerry JP, O’Brien NM (2011) In vitro and cellular antioxidant activities of seaweed extracts prepared from five brown seaweeds harvested in spring from the west coast of Ireland. Food Chem 12:1064–1070CrossRefGoogle Scholar
  35. Ozgen M, Reese RN, Tulio AZ, Miller AR, Scheerens JC (2006) Modified 2,2-Azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-Diphenyl-1-picrylhydrazyl (DPPH) methods. J Agric Food Chem 54:1151–1157CrossRefGoogle Scholar
  36. Park EJ, Pezzuto JM (2013) Antioxidant marine products in cancer chemoprevention. Antioxid Redox Signal 19:115–138CrossRefGoogle Scholar
  37. Pokornỳ JP (2007) Are natural antioxidants better—and safer—than synthetic antioxidants. Eur J Lipid Sci Technol 109:629–642CrossRefGoogle Scholar
  38. Raja R, Hemaiswarya S, Arunkumar K, Carvalho IS (2016) Antioxidant activity and lipid profile of three seaweeds of Faro, Portugal. Braz J Bot 39:9–17CrossRefGoogle Scholar
  39. Rajauria G, Jaiswal AK, Abu-Ghannam N, Gupta S (2010) Effect of hydrothermal processing on colour, antioxidant and free radical scavenging capacities of edible Irish brown seaweeds. Int J Food Sci Technol 45:2485–2493CrossRefGoogle Scholar
  40. Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159CrossRefGoogle Scholar
  41. Ryu B, Kim S-K (2012) Pharmacological potential of phlorotannins from marine brown algae marine pharmacognosy. In: Kim S-K (ed) Marine pharmacognosy: trends and allications. CRC Press, Boca Raton, pp 153–160CrossRefGoogle Scholar
  42. Schmittgen TD, Livak KJ (2008) Analazing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108CrossRefGoogle Scholar
  43. Schofield P, Mbugua DM, Pell AN (2001) Analysis of condensed tannins: a review. Anim Feed Sci Technol 91:21–40CrossRefGoogle Scholar
  44. Shahidi F, Zhong Y (2015) Measurement of antioxidant activity. J Funct Foods B 18:757–781CrossRefGoogle Scholar
  45. Shanura IPF, Jae-Woon N, You-Jin J (2016) Potential anti-inflammatory natural products from marine algae. Environ Toxicol Pharmacol 48:22–30CrossRefGoogle Scholar
  46. Shibata T, Fujimoto K, Nagayama K, Yamaguchi K, Nakamura T (2002) Inhibitory activity of brown algal phlorotannins against hyaluronidase. Int J Food Sci Technol 37:703–709CrossRefGoogle Scholar
  47. Shibata T, Ishimaru K, Kawaguchi S, Yoshikawa H, Hama Y (2008) Antioxidant activities of phlorotannins isolated from Japanese Laminariaceae. J Appl Phycol 20:705–711CrossRefGoogle Scholar
  48. Steevensz AJ, Mackinnon SL, Hankinson R, Craft C, Connan S, Stengel DB, Melanson JE (2012) Profiling phlorotannins in brown macroalgae by liquid chromatography-high resolution mass spectrometry. Phytochem Anal 23:547–553CrossRefGoogle Scholar
  49. Sugiura Y, Matsuda K, Yamada Y, Nishikawa M, Shioya K, Katsuzaki H, Imai K, Amano H (2007) Isolation of a new anti-allergic phlorotannin, phlorofucofuroeckol-B, from an edible brown alga Eisenia arborea. Biosci Biotechnol Biochem 70:2807–2281CrossRefGoogle Scholar
  50. Tenorio-Rodríguez PA, Murillo-Álvarez JI, Campa-Córdova AI, Angulo C (2017) Antioxidant screening and phenolic content of ethanol extracts of selected Baja California Peninsula macroalgae. J Food Sci Technol 54:422–429CrossRefGoogle Scholar
  51. Tierney MS, Soler-Vila A, Croft AK, Hayes M (2013) Antioxidant activity of the brown macroalgae Fucus spiralis Linnaeus harvested from the west coast of Ireland. Curr Res J Biol Sci 5:81–90CrossRefGoogle Scholar
  52. Vizetto-Duarte C, Custódio L, Acosta G, Lago JHG, Morais TR, Bruno de Sousa C, Gangadhar KN, Rodrigues MJ, Pereira H, Lima RT, Vasconcelos MH, Barreira L, Rauter AP, Albericio F, Varela J (2016) Can macroalgae provide promising anti-tumoral compounds? A closer look at Cystoseira tamariscifolia as a source for antioxidant and anti-hepatocarcinoma compounds. PeerJ 4:e1704CrossRefGoogle Scholar
  53. Wang T, Jónsdóttir R, Liu H, Gu L, Kristinsson HG, Raghavan S, Ólafsdóttir G (2012) Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J Agric Food Chem 60:5874–5883CrossRefGoogle Scholar
  54. Wei R, Lee MS, Lee B, Oh CW, Choi CG, Kim HR (2016) Isolation and identification of anti-inflammatory compounds from ethyl acetate fraction of Ecklonia stolonifera and their anti-inflammatory action. J Appl Phycol 28:3535–3545CrossRefGoogle Scholar
  55. Xie PJ, Huang LX, Zhang CH, Zhang YL (2015) Phenolic compositions, and antioxidant performance of olive leaf and fruit (Olea europaea L.) extracts and their structure– activity relationships. J Funct Foods 16:460–471CrossRefGoogle Scholar
  56. Yoon JS, Kasin Yadunandam A, Kim SJ, Woo HC, Kim HR, Kim GD (2012) Dieckol, isolated from Ecklonia stolonifera, induces apoptosis in human hepatocellular carcinoma Hep3B cells. J Nat Med 67:519–527CrossRefGoogle Scholar
  57. Yotsu-Yamashita M, Kondo S, Segawa S, Lin YC, Toyohara H, Ito H, Konoki K, Cho Y, Uchida T (2013) Isolation and structural determination of two novel phlorotannins from the brown alga Ecklonia kurome Okamura, and their radical scavenging activities. Mar Drugs 11:165–183CrossRefGoogle Scholar
  58. Zubia M, Fabre MS, Kerjean V, Lann KL, Stiger-Pouvreau V, Fauchon M, Deslandes E (2009) Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts. Food Chem 116:693–701CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Immunology & Vaccinology Group, Centro de Investigaciones Biológicas del Noroeste (CIBNOR)La PazMexico
  2. 2.Unidad de Biotecnología Médica y Farmacéutica, Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, CIATEJGuadalajaraMexico
  3. 3.Centro Interdisciplinario de Ciencias Marinas-IPN (CICIMAR)La PazMexico

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