Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins

Marine Drugs

Volumn 13, Issue 1, 2015, Pages 509-528

  Heffernan, Natalie ^a,b   Brunton, Nigel P ^c   FitzGerald, Richard J ^b   Smyth, Thomas J ^d  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY OF LIMERICK   (Ireland)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d Atlantic Technological University   (Ireland)

Author keywords

Antioxidant activity; Brown macroalgae; Isomerization; Metabolomic profiling; Phlorotannins; UPLC MS MS profiling

Indexed keywords

PHLOROGLUCINOL; PHLOROTANNIN; TANNIN DERIVATIVE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYSTOSEIRA NODICAULIS; FUCUS SERRATUS; FUCUS VESICULOSUS; HIMANTHALIA ELONGATA; IN VITRO STUDY; ISOMER; ISOMERIZATION; MACROALGA; MOLECULAR WEIGHT; MULTIPLE REACTION MONITORING; NONHUMAN; REACTION TIME; SPECIES COMPARISON; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; CHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; PROCEDURES; REVERSED PHASE LIQUID CHROMATOGRAPHY; SEAWEED; STEREOISOMERISM;

CYSTOSEIRA NODICAULIS; FUCUS SERRATUS; FUCUS VESICULOSUS; HIMANTHALIA ELONGATA; PHAEOPHYCEAE;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, REVERSE-PHASE; MOLECULAR STRUCTURE; MOLECULAR WEIGHT; SEAWEED; STEREOISOMERISM; TANDEM MASS SPECTROMETRY; TANNINS;

EID: 84921684187     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13010509     Document Type: Article

References (55)

1. Lopes, G.; Sousa, C.; Silva, L. R.; Pinto, E.; Andrade, P. B.; Bernardo, J.; Mouga, T.; Valentão, P. Can phlorotannins purified extracts constitute a novel pharmacological alternative for microbial infections with associated inflammatory conditions? PLoS One 2012, 7, e31145, doi:10.1371/journal.pone.0031145.
2. Thomas, N. V.; Kim, S. K. Potential pharmacological applications of polyphenolic derivatives from marine brown algae. Environ. Toxicol. Pharmacol. 2011, 32, 325-335.
3. Wang, T.; Jónsdóttir, R.; Liu, H.; Gu, L.; Kristinsson, H. G.; Raghavan, S.; Ólafsdóttir, G. Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J. Agric. Food Chem. 2012, 60, 5874-5883.
4. Audibert, L.; Fauchan, M.; Blanc, N.; Hauchard, D.; ArGalla, E. Phenolic compounds in the brown seaweed Ascophyllum nodosum: Distribution and radical scavenging activities. Phytochem. Anal. 2010, 21, 399-405.
5. Li, Y. X.; Wijeseker, I.; Li, Y.; Kim, S. K. Phlorotannins as bioactive agents from brown algae. Process Biochem. 2011, 46, 2219-2224.
6. Zubia, M.; Robledo, D.; Freile-Pelegrin, Y. Antioxidant activities in tropical marine macroalgae from the Yucatan Penisula, Mexico. J. Appl. Phycol. 2007, 19, 449-458.
7. Sailler, B.; Glombitza, K. W. Phlorethols and fucophlorethols from the brown alga Cystophoroa retroflexa. Phytochemistry 1999, 50, 869-881.
8. Boettcher, A. A.; Targett, N. M. Role of polyphenolic molecular-size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 1993, 74, 891-903.
9. McClintock, J. B.; Baker, B. J. Marine Chemical Ecology; CRC Press: Boca Ratopm, FA, USA, 2001.
10. Schoenwaelder, M. E. A.; Clayton, M. N. Secretion of phenolic substances into the zygote wall and cellplate in embryos of Hormosira and Acrocarpia (fucales, phaeophyceae). J. Phycol. 1998, 34, 969-980.
11. Mazid, M.; Khan, T. A.; Mohammad, F. Role of secondary metabolites in defense mechanisms of plants. Biol. Med. 2011, 3, 232-249.
12. Steinberg, P. D. Algal chemical defense against herbivores: Allocation of phenolic compounds in the kelp Alaria marginata. Science 1984, 223, 405-407.
13. Targett, N. M.; Arnold, T. M. Effects on secondary metabolites on digestion in marine herbivores. In Marine Chemical Ecology; McClinlock, J. B., Baker, B. J., Eds.; CRC Press: Boca Ratopm, FL, USA, 2001; pp. 391-412.
14. Waterman, P. G.; Mole, S. Analysis of Phenolic Plant Metabolities; Blackwell Scientific Publication: Oxford, UK, 1994; pp. 85-87.
15. Pavia, H.; Toth, G. B. Inducible chemical resistance to herbivory in the brown seaweed Acophyllum nodosum. Ecology 2000, 81, 3212-3225.
16. Pavia, H.; Cervin, G.; Lindgren, A.; Åberg, P. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 1997, 157, 139-146.
17. Davis, A. R.; Tagett, N. M.; McConnell, O. J.; Young, C. M. Epibiosis of marine algae and benthic invertebrates: Natural products chemistry and other mechanisms inhibiting settlement and growth. In Biorganic Marine Chemistry; Schever, P. J., Ed.; Springer Verlag: Berlin/Heidelberg, Germany, 1989; Volume 3, pp. 85-114.
18. Schoenwaelder, M. E. A. The occurrence and cellular significance of physodes in brown algae. Phycologia 2002, 41, 125-139.
19. Arnold, T. M.; Targett, N. M. To grow and defend: Lack of trade-offs for brown algal phlorotannins. Oikas 2003, 100, 406-408.
20. Shibata, T.; Ishimaru, K.; Kawaguchi, S.; Yoshikawa, H.; Hama, Y. Antioxidant activities of phlorotannins isolated from Japanese Laminariceae. J. Appl. Phycol. 2008, 20, 705-711.
21. Tierney, M. S.; Soler-Vila, A.; Croft, A. K.; Hayes, M. Antioxidant Activity of the Brown Macroalgae Fucus spiralis Linnaeus Harvested from the West Coast of Ireland. Curr. Res. J. Biol. Sci. 2013, 5, 81-90.
22. Tierney, M. S.; Smyth, T. J.; Hayes, M.; Soler-Vila, A.; Croft, A. K.; Brunton, N. Influence of pressurized liquid extraction and solid liquid extraction methods on the phenolic content and antioxidant activities of Irish macroalgae. Int. J. Food Technol. 2013, 48, 860-869.
23. Li, Y.; Lee, S. H.; Le, Q. T.; Kim, M. M.; Kim, S. K. Anti-allergic effects of phlorotannins on histamine release via binding inhibition between IgE and Fc epsilon RI. J. Agric. Food Chem. 2008, 56, 12073-12080.
24. Kim, A. R.; Shin, T. S.; Lee, M. S.; Park, J. Y.; Park, K. E.; Yoon, N. Y.; Kim, J. S.; Choi, J. S.; Jang, B. C.; Byun, D. S.; et al. Isolation and identification of phlorotannins from Ecklonia stolonifera with antioxidant and anti-inflammatory properties. J. Agric. Food Chem. 2009, 57, 3483-3489.
25. Artan, M.; Li, Y.; Karadeniz, F.; Lee, S. H.; Kim, M. M.; Kim, S. K. Anti-HIV-1 activity of phloroglucinol derivative 6, 6'-bieckol, from Ecklonia cava. Bio-organ Med. Chem. 2008, 16, 7921-7926.
26. Kong, C. S.; Kim, J. A.; Yoon, N. Y.; Kim, S. K. Induction of apoptosis by phloroglucinol derivative from Ecklonia cava in MCF-7 human breast cancer cells. Food Chem. Toxicol. 2009, 47, 1653-1658.
27. Okada, Y.; Ishimaru, A.; Suzuki, R.; Okuyama, T. A new phloroglucinol derivative from the brown algae Eisenia bicyclis: Potential for the effective treatment of diabetic complications. J. Nat. Prod. 2004, 67, 103-105, doi:101021/np030323j.
28. Lordan, S.; Smyth, T. J.; Soler-Vila, A.; Stanton, C.; Ross, R. P. The a-amylase and a-glucosidase inhibitory effects of Irish seaweed extracts. Food Chem. 2013, 141, 2170-2176.
29. Hwang, H.; Chen, T.; Nines, R. G.; Shin, H. C.; Stoner, G. D. Photochemoprevention of UVBinduced skin carcinogenesis in SKH-1 mice by brown algae polyphenols. Int. J. Cancer 2006, 119, 2742-2749.
30. Fukuyama, Y.; Kodama, M.; Miura, I.; Kinzyo, Z.; Mori, H.; Nakayama, Y.; Takahashi, M. Anti-plasmin Inhibitor V. Structures of novel dimeric eckols isolated from the brown alga Ecklonia kurome OKAMURA. Chem. Pharm. Bull. 1989, 37, 2438-2440.
31. Shibata, T.; Fujimoto, K.; Nagayama, K.; Yamaguchi, K.; Nakamura, T. Inhibitory activity of brown algal phlorotannins against hyaluronidase. Int. J. Food Sci. Technol. 2002, 37, 703-709.
32. Fujii, Y.; Tanaka, R.; Miyake, H.; Tamaru, Y.; Ueda, M.; Shibata, T. Evaluation for antioxidative properties of phlorotannins isolated from the brown alga Eisenia bicyclis, by the HORAC method. Food Nutr. Sci. 2013, 4, 478-482.
33. Ferreres, F.; Lopes, G.; Gil-Izquierdo, A.; Andrade, P. B.; Sousa, C.; Mouga, T.; Valentao, P. Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESI-MS; Approaches to hyaluronidase inhibitory capacity and antioxidant properties. Mar. Drugs 2012, 10, 2766-2781.
34. Montero, L.; Herrero, M.; Ibánez, E.; Cifuentes, A. Separation and characterization of phlorotannins from brown algae Cystoseira abies-marina by comprehensive two-dimensional liquid chromatography. Electrophoresis 2014, 35, 1644-1651.
35. Steevensz, A. J.; MacKinnon, S. L.; Hankinson, R.; Craft, C.; Connan, S.; Stengel, D. B.; Melansona, J. E. Profiling phlorotannina in brown macroalgae by Liquid Chromatography-High Resolution Mass Spectrometry. Phytochem. Anal. 2012, 23, 547-553.
36. Tierney, M. S.; Soler-Vila, A.; Rai, D. K.; Croft, A. K.; Brunton, N. P.; Smyth, T. J. UPLC-MS profiling of low molecular weight phlorotannin polymers in Ascophyllum nodosum, Pelvetia canaliculata and Fucus spiralis. Metabolomics 2014, 10, 524-535.
37. Wang, T.; Jónsdóttir, R.; Ólafsdóttir, G. Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem. 2009, 116, 240-248.
38. Heffernan, N.; Smyth, T.; Soler-Villa, A.; Fitz Gerald, R. J.; Brunton, N. P. Phenolic content and antioxidant activity of fractions obtained from selected Irish macroalgae species (Laminaria digitata, Fucusserratus, Gracilaria gracilis and Codium fragile). J. Appl. Phycol. 2014, 26, doi:10.1007/s10811-01-029-9.
39. Koivikko, R.; Loponen, J.; Pihlaja, K.; Jormalainen, V. High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochem. Anal. 2007, 18, 326-332.
40. Hagerman, A. E.; Riedl, K. M.; Jones, G. A.; Sovik, K. N.; Ritchard, N. T.; Hartzfeld, P. W.; Riechel, T. L. High molecular weight plant polyphenolics (tannins) as biological antioxidants. J. Agric. Food Chem. 1998, 46, 1887-1892.
41. Fan, X.; Yan, X.; Fang, G.; Chen, Y.; Lou, G. Antioxidative properties of high molecular weight polyphenols from brown seaweed. Acta Hydrobiol. Sinica 1999, 5, 494-499.
42. Wei, Y. X.; Xu, Z. H. Studies on antioxidative activity of high molecular weight polyphenols from two kinds of brown algae. Chin. Tradit. Herb. Drugs 2003, 34, 317-319.
43. Glombitza, K. W.; Pauli, K. Fucols and Phloretols from the Brown alga Scytothaminus australis Hook. Et Harv (Chnoosporaceae). Bot. Mar. 2003, 46, 315-320.
44. Grosse-Damhues, J.; Glombitza, K. W.; Schulter, H. R. An eight-ring phlorotannin from the brown alga Himanthalia elongata. Phytochemistry 1983, 22, 2043-2046.
45. Glombitza, K. W.; Grobe-Damhues, J. Antibiotics from algae XXXIII. Phlorotannins of the brown alga Himanthalia elongata. Planta Medica 1985, 1, 42-46.
46. Pary, S.; Kehraus, S.; Krick, A.; Glombitza, K. W.; Carmeli, S.; Klimo, K.; Gerhäuser, C.; König, G. M. In vitro chemopreventative potential of fucophlorethols from the brown alga Fucus vesiculosus L.by antioxidant activity and inhibition of selected cytochrome P450 enzymes. Phytochemistry 2010, 71, 221-229.
47. Koivikko, R. Brown Algal Phlorotannins: Improving and Applying Chemical Methods (Annales Universitatis Turkvensis A1 381). Ph. D. Thesis, University of Turku, Turku, Finland, February 2008.
48. Liu, H.; Cu, L. Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation end products by scavenging reactive carbonyls. J. Agric. Food Chem. 2012, 60, 1326-1334.
49. Heffernan, N.; Smyth, T. J.; Fitz Gerald, R. J.; Soler-Vila, A.; Brunton, N. Antioxidant activity and phenolic content of pressurized liquid and solid liquid extracts from four Irish origin macroalgae. Int. J. Food Sci. Technol. 2014, 49, 1765-1771.
50. Kang, M. C.; Kim, E. A.; Kang, S. M.; Wijesinghe, W. A. J. P.; Yang, X.; Kang, N.; Jeon, Y. J. Thermostability of a marine polyphenolic antioxidant dieckol, derived from the brown seaweed Ecklonia cava. Algae 2012, 27, 205-213.
51. Singleton, V. L.; Orthofer, R.; Lamuela-Raventos, R. M. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1999, 299, 152-178
52. Stratil, P.; Klejdus, B.; Kuban, V. Determination of total content of phenolic compounds and their antioxidant activity in vegetables evaluation of spectrophotometric methods. J. Agric. Food Chem. 2006, 54, 607-616.
53. Goupy, P.; Hughes, M.; Boivin, P.; Amiot, M. J. Antioxidant composition and activity of barley (Hordeum vulgare) and malt extracts and of isolated phenolic compounds. J. Sci. Food Agric. 1999, 79, 1625-1634.
54. Ollanketo, M.; Peltoketo, A.; Hartonen, K.; Hiltunen, R.; Riekkola, M. L. Extraction of sage (Salvia officinalis) by pressurized hot water and conventional methods: Antioxidant activity of the extracts. Eur. Food Res. Technol. 2002, 215, 158-163.
55. Brand-Williams, W.; Culvelier, M. E.; Berset, C. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol. 1995, 28, 25-30