Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts
Introduction
Over the last decades, products liable to promote health and well-being have aroused a huge interest among consumers and food industrialists. These food items are, nowadays, gathered under the generic name of functional food; in addition to their nutritional or energetic benefits, these items can be also worth for the physiology of humans by exerting an antihypertensive, antioxidant or anti-inflammatory effect (Herrero, Cifuentes, & Ibáñez, 2006). The beneficial action exerted by functional food is usually ascribed to a given functional component (e.g. vitamins, minerals or micronutrients such as ω-3 fatty acids), which is either missing in the analogous conventional food or present at lower concentrations (Plaza, Cifuentes, & Ibañez, 2008).
Due to their low content in lipids, high concentration in polysaccharides, natural richness in minerals, polyunsaturated fatty acids and vitamins as well as their content in bioactive molecules, e.g. phenolic compounds or more specifically phlorotannins, terpenes, alkaloids, (Kornprobst, 2005), marine algae are known to be a source of healthy food. Among them, microalgae have attracted considerable attention from functional food industrialists because of their high contents in polyunsaturated fatty acids, β-carotene and other pigments, sterols (Herrero et al., 2006). Macroalgae are mainly traded as food items in particular in Asia (e.g. sushi wrappings, seasonings, condiments and vegetables) and employed in the phycocolloid industry. Over the last years, the development of innovative projects for the agri-food industry and/or pharmaceutical and para-pharmaceutical applications has been at the origin of a great expansion in the demand for macroalgae. Indeed, the potential offered by macroalgae in functional foods or ingredients industries is huge because of their exceptional richness in bioactive compounds liable to be endowed with antioxidant, antimicrobial, anti-inflammatory, antitumoural activities (Kornprobst, 2005, Smit, 2004).
Among the most relevant compounds found in the algae, antioxidants are probably the substances that have attracted major interest. Antioxidants are considered key-compounds in the fight against various diseases (e.g. cancer, chronic inflammation, atherosclerosis and cardiovascular disorder) and ageing processes (Kohen & Nyska, 2002). Moreover, the relevance of using antioxidants from natural sources has been considerably enhanced by consumer’s preference for natural products and concerns about the toxic effects by synthetic antioxidants (Ito et al., 1986). Algae, as photosynthetic organisms, are exposed to a combination of light and high oxygen concentration at the origin of the formation of free radicals and other oxidative reagents. But, the awareness of the lack of structural damage in their organs has led the scientific community to consider that their protection against oxidation comes from their natural content, or production under stress, in antioxidant substances. Indeed, macroalgae are particularly rich in natural antioxidants, e.g. phlorotannins, ascorbic acid, tocopherols and carotenoids, and a literature search shows that most investigation has been devoted to the phlorotannins that play an essential role in the photoprotection of the brown algae.
Another area of focus is the search for anticancer drugs since marine molecules have led to promising results in trials at different phases of cancer diseases (Mayer & Gustafson, 2006). Numerous macroalgae have shown potent cytotoxic activities (see reviews in Mayer and Gustafson, 2006, Smit, 2004), and certain authors have suggested to consume algae as a chemopreventive agent against several cancers (Yuan & Walsh, 2006). Dehydrothyrsiferol and halomon extracted from Laurencia viridis sp. nov. (Pec et al., 2003) and Portieria hornemanii (Egorin et al., 1997) respectively, have been tested in the preclinical phase. Concerning brown algae, polysaccharides (Aisa et al., 2005, Dias et al., 2005, Kwon and Nam, 2007) and terpenoids (Culioli et al., 2004, Duran et al., 1997) are considered as promising bioactive molecules in the search for anticancer drugs.
With about 700 identified species (Dizerbo & Herpé, 2003), the coasts of Brittany (France) are acknowledged for their particular richness in macroalgae. Among them, only few species, mainly brown algae, have been investigated for their antioxidant capacities (Cerantola et al., 2006, Connan et al., 2006, Connan et al., 2007, Le Lann et al., 2008), their anti-fouling (Hellio et al., 2000, Hellio et al., 2004, Plouguerné et al., 2008) and antitumoural (Moreau et al., 2006) activities. These studies have highlighted the great potential of brown macroalgae in the search for bioactive molecules.
The present study was aimed at assessing the antioxidative and antitumoural capabilities of 10 brown algae settled along the shoreline of Brittany. To gain more insight into antioxidant processes, the antioxidative activities of extracts were characterised by three biochemical methods (DPPH radical-scavenging activity, reducing activity and β-carotene–linoleic acid system), and their total phenolic contents were quantified. This led us to further select some crude extracts for fractionation in order to determine the antioxidant activity and total phenolic content of each fraction to analyse relationships between both parameters. A cytotoxic assay was also conducted with three different tumoural cells lines (Daudi, Jurkat and K562) to determine the antitumoural activities of the crude extracts.
Section snippets
Chemicals
Ascorbic acid, α-tocopherol, β-carotene, BHT (butylated hydroxytoluene) and BHA (butylated hydroxyanisole), DPPH (2,2-diphenyl-1-picryhydrazyl radical), Folin–Ciocalteu’s phenol reagent, linoleic acid, phloroglucinol, potassium ferricyanide [K3Fe(CN)6], trichloroacetic acid and Tween-40 were purchased from Sigma–Aldrich Co. (France). The organic solvents (chloroform, dichloromethane, formol, ethanol and methanol) were from VWR (France); Fontainebleau sand was from Grosseron (France). The other
Crude extracts
Fig. 1, Table 2, Table 3 show the main results of the assessment by the DPPH radical-scavenging activity, the reducing activity and the β-carotene–linoleic acid system, respectively, of the antioxidative activities displayed by the crude extracts under study. All of the species collected for this study showed DPPH radical-scavenging activities (Fig. 1). By exhibiting the lowest EC50 (0.21 ± 0.00 mg ml−1), the crude extract from Halidrys siliquosa proved to be endowed with a very strong antioxidant
Antioxidant activities
In order to by-pass the inability of a one-dimensional test of antioxidant capacity to accurately mirror the in vivo complexity of interactions between antioxidants, in this study the antioxidative activities displayed by algal crude extracts were characterised by three simple, fast and reliable biochemical methods (Frankel & Meyer, 2000). DPPH radical-scavenging activity, reducing activity and β-carotene–linoleic acid system assays proved to be relevant, here, in the assessment of the total
Conclusions
This study constituted the largest screening of antioxidant and antitumoural activities in brown macroalgae from Brittany coasts achieved till now. It emphasised the great antioxidant potential of H. siliquosa, which was found to be equivalent to the antioxidant activity of all of the commercial antioxidant molecules assessed in the same study. Moreover, two other Sargassaceae species (B. bifurcata and C. tamariscifolia) and one Fucaceae (F. ceranoides) demonstrated a high antioxidant activity.
Acknowledgements
The authors thank Erwan Ar Gall and Michel Le Duff (LEBHAM EA3877/IUEM/UBO) for their help with identification of the macroalgal species and Marie-Paule Friocourt for advices in the English writing of this paper.
References (48)
- et al.
Use of a free radical method to evaluate antioxidant activity
Food Science and Technology – Lebensmittel-Wissenschaft and Technologie
(1995) - et al.
Influence of day-night and tidal cycles on phenol content and antioxidant capacity in three temperate intertidal brown seaweeds
Journal of Experimental Marine Biology and Ecology
(2007) - et al.
Does measurement of oxidative damage to DNA have clinical significance?
Clinica Chimica Acta
(2006) - et al.
Trihydroxylated linear diterpenes from the brown alga Bifurcaria bifurcata
Phytochemistry
(2004) - et al.
New diterpenoids from the alga Dictyota dichotoma
Tetrahedron
(1997) - et al.
Antioxidant activity of phenolic meroditerpenoids from marine algae
Journal of Photochemistry and Photobiology B: Biology
(1994) - et al.
Sub- and super-critical fluid extraction of functional ingredients from different natural sources: Plants, food-by-products, algae and microalgae – A review
Food Chemistry
(2006) - et al.
Studies on antioxidants: Their carcinogenic and modifying effects on chemical carcinogenesis
Food Chemistry Toxicology
(1986) - et al.
Diterpenes from the Far-eastern brown alga Dictyota dichotoma
Phytochemistry
(2006) - et al.
Antioxidant properties of dried ‘kayamo-nori’, a brown alga Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae)
Food Chemistry
(2005)
A polysaccharide of the marine alga Capsosiphon fulvescens induces apoptosis in AGS gastric cancer cells via an IGF-IR-mediated PI3K/Akt pathway
Cell Biology International
Marine pharmacology in 2003–2004: Antitumour and cytotoxic compounds
European Journal of Cancer
Inudction of apoptosis in estrogen dependent and independent breast cancer cells by the marine terpenoid dehydrothyrsiferol
Biochemistry Pharmacology
In the search of new functional food ingredients from algae
Trends Food Science and Technology
Meroterpenes from Cystoseira usneoides II
Phytochemistry
Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds
Food and Chemical Toxicology
Antioxidant and prooxidant roles for β-carotene, α-tocopherol and ascorbic acid in human lung cells
Toxicology In Vitro
Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta)
Marine Biology
Fucoidan induces apoptosis of human HS-Sultan cells accompanied by activation of caspase-3 and down-regulation of ERK pathways
American Journal of Hematology
Cytotoxic hydroazulene diterpenes from the brown alga Cystoseira myrica
Zeitschrift für Naturforschung C – A Journal of Biosciences
Guide des algues des mers d’Europe
Co-occurrence and antioxidant activities of fucol and fucophlorethol classes of polymeric phenols in Fucus spiralis
Botanica Marina
Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters
Botanica Marina
New chromenols from the brown alga Desmarestia menziesii
Natural Product Letters
Cited by (211)
Effects of UV radiation on photosynthesis of Sargassum muticum
2023, Journal of Experimental Marine Biology and EcologyAntioxidant capacity of seaweeds: In vitro and in vivo assessment
2023, Marine Phenolic Compounds: Science and Engineering