Bioactivities of Ecklonia stolonifera Okamura

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Bioactivities of Ecklonia stolonifera Okamura

This entry is adapted from the peer-reviewed paper 10.3390/md20100607

Ecklonia stolonifera Okamura (ES) is mainly distributed in the coastal areas of the middle Pacific, around Korea and Japan, and has a long-standing edible value. It is rich in various compounds, such as polysaccharides, fatty acids, alginic acid, fucoxanthin, and phlorotannins, among which the polyphenol compound phlorotannins are the main active ingredients. Studies have shown that the extracts and active components of ES exhibit anti-cancer, antioxidant, anti-obesity, anti-diabetic, antibacterial, cardioprotective, immunomodulatory, and other pharmacological properties in vivo and in vitro. Although ES contains a variety of bioactive compounds, it is not widely known and has not been extensively studied. Based on its potential health benefits, it is expected to play an important role in improving the nutritional value of food both economically and medically. Therefore, ES needs to be better understood and developed so that it can be utilized in the development and application of marine medicines, functional foods, bioactive substances, and in many other fields.

Ecklonia stolonifera Okamura bioactive compound bioactivity

1. Introduction

Ecklonia stolonifera Okamura (ES) is a perennial benthic brown alga widely distributed in the middle Pacific coastal areas of Korea and Japan and belongs to the family Laminariaceae, order Laminariales ^[1]^[2]. It has strong reproductive ability and can adapt well to environmental changes. ES usually grows in the sea at a depth of 2–10 m ^[3]. The erect thalli length of ES is related to the underwater growth depth, and the length of ES grown, at a depth of 2 m, is significantly longer than that of ES at 1.0–1.5 m and 2.5–3.0 m ^[4]. The leaves can grow from 45.2 to 96.5 cm in length and 13.7 to 28.6 cm in width. The length and width of leaves are affected by different months; the leaves are longer from March to July, and their width is narrower in November. ES is an economical seaweed that is widely used in food and industry ^[5]. In the abalone farming industry, ES is considered an excellent candidate for abalone feed. Compared with other brown algae, ES can continue to grow when the water temperature increases in summer, providing a rich food source for the growth of abalone. Moreover, the shell color of farmed abalone can be more natural dark brown, which is more popular in the market ^[6]. In recent years, many studies have shown that ES has great development potential in functional foods and pharmaceuticals, and its extract contains a high content of phenolic compounds, showing high antioxidant capacity, including strong DPPH free radical-scavenging activity, ferrous reducing power, and superoxide radical-scavenging activity ^[7]. ES has a variety of biological activities and has attracted much attention because of its high concentration of polysaccharides, fucosterol, fatty acids, phlorotannins of eckol, diekcol, phlorofucofuroeckol A, eckstolonol, and phenolic compounds with antioxidant capacities ^[7]^[8]^[9]. Through gel filtration column and high-performance liquid chromatography (HPLC) analysis, Kuda et al. determined that the water extract of ES contained low molecular weight polysaccharides and that these polysaccharides were laminarin ^[7]. The results of sugar composition analysis indicated that the types of polysaccharides contained in ES cell walls were cellulose, fucoidan, and laminaran ^[10].

2. Antibacterial Activity

Research and development of natural antibacterial agents is becoming a hot topic in the food industry. Marine algae have attracted much attention because of their richness in bioactive compounds such as phlorotannins and fucoidans ^[11]^[12]. Kuda et al. ^[11] studied the antibacterial properties of two boiled and four dried ES products and found that two of the four dried products showed antibacterial (Escherichia coli, Pseudomonas aeruginosa, Corynebacterium glutamicum, Staphylococcus aureus, and Bacillus cereus) activity, whereas the two products subjected to boiling treatment had no effect on various bacterial species, and the content and activity of bioactive compounds in ES brown algae were greatly reduced by processing and preservation methods. Boiling resulted in the loss of some phenolic compounds and water-soluble polysaccharides, such as phlorotannins, alginate, and fucoidan. Choi et al. ^[13] reported that the aqueous extract of ES exerted an inhibitory effect on microbial pathogens. Eom et al. ^[14] showed that the methanol extract of ES had significant antibacterial activity against methicillin-resistant Staphylococcus aureus (MRSA). To conduct a more detailed study of the antibacterial activity of the extract, the methanol extract was further fractionated with organic solvents such as EtOAc, CH₂Cl₂, hexane, and n-butanol, and it was determined that the hexane fraction had the strongest antibacterial activity against MRSA strains with minimum inhibitory concentrations ranging from 500 to 600 μg/mL. Lee et al. isolated 87 mg of dieckol in the EtOAc fraction (25.0 g) of ES methanolic extracts and investigated the synergistic effect of dieckol with β-lactams against methicillin-resistant Staphylococcus aureus. The results showed that the minimum inhibitory concentration of dieckol against standard MRSA and methicillin-susceptible S. aureus strains was 32–64 μg/mL. Furthermore, when ampicillin and penicillin were used in combination with dieckol (8 and 16 μg/mL), the fractional inhibitory concentration indices for all MRSA strains were 0.066–0.266 μg/mL. It showed that the combination of dieckol and β-lactam has an effective therapeutic effect on MRSA infection ^[15].

3. Tyrosinase Inhibition

Tyrosinase is a copper-containing oxidoreductase, also known as polyphenol oxidase, and is widely found in animals, plants, and microorganisms. It directly affects melanin synthesis, acting as the rate-limiting enzyme. Inhibition of tyrosinase activity can prevent skin darkening and melanin production, and tyrosinase inhibitors are widely used in medicine, cosmetics, and food ^[16]^[17]. ES is rich in polyphenols and its main component is phlorotannin ^[18]. Kang et al. ^[19] isolated five phloroglucinol derivatives from the methanolic extract of ES: dieckol, eckol, eckstolonol, phloroglucinol, and phlorofucofuroeckol A. These five compounds inhibited the oxidation of L-tyrosine catalyzed by mushroom tyrosinase, with IC₅₀ values of 2.16, 33.2, 126, 92.8, and 177 μg/mL, respectively. Compared with the tyrosinase inhibitors arbutin and kojic acid, their IC₅₀ values were 6.32 and 112 μg/mL, respectively. Using a Lineweaver–Burk plot, it was determined that there were differences in the inhibition modes of the five compounds. Among them, eckstolonol and phloroglucinol were competitive inhibitors, and the inhibition constants (Ki) were 3.1 × 10⁻⁴ and 2.3 × 10⁻⁴ M, respectively, while dieckol, eckol, and phlorofucofuroeckol A are noncompetitive inhibitors with Ki of 1.5 × 10⁻⁵, 1.9 × 10⁻⁵, and 1.4 × 10⁻³ M, respectively. Manandhar et al. ^[20] isolated a novel phlorotannin 974-A from ES and simultaneously detected three other known compounds: phlorofucofuroeckol A, eckol, and phloroglucinol. Compound 974-A can inhibit the activities of L-tyrosine and L-DOPA with IC₅₀ values of 1.57 ± 0.08 and 3.56 ± 0.22 µM, respectively. Phlorofucofuroeckol-A, eckol, and 974-A downregulated the expression of a tyrosinase-related protein (TRP)-1 and TRP-2, which are involved in melanin production in B16F10 melanoma cells. These results suggest that dieckol, eckol, eckstolonol, phloroglucinol, phlorofucofuroeckol A, and 974-A isolated from ES can be used as potent tyrosinase inhibitors and have potential applications in cosmetics, medicine, and food.

4. Antioxidant Activity

Antioxidants are substances that effectively inhibit the oxidative reaction of free radicals, thereby of preventing diseases, alleviating human aging, and maintaining the skin ^[21]. Marine organisms are rich in health value, among which marine algae are the most representative natural antioxidants with high free radical scavenging activity, and are rich in polyphenols, carotenoids, and chlorophyll ^[22]^[23]. Kim et al. ^[24] isolated and identified three phlorotannins (dioxinodehydroeckol, phlorofucofuroeckol A, and dieckol) with high antioxidant activity from the methanol extract of ES using gel, silica gel, and reversed-phase column chromatography, and determined their antioxidant activities by DPPH experiments. The EC₅₀ of dioxinodehydroeckol, phlorofucofuroeckol A, and dieckol were 8.8 ± 0.4, 4.7 ± 0.3, and 6.2 ± 0.4 μM, respectively. The antioxidant activities of these three phlorotannins were further determined in vitro, and the results showed that phlorofucofuroeckol A and dieckol inhibited reactive oxygen species (ROS) production in a concentration-dependent manner. Although dioxinodehydroeckol has high DPPH radical scavenging activity, it does not inhibit ROS. This may be because, compared with dioxinodehydroeckol, phlorofucofuroeckol A and dieckol can better penetrate cells and react with ROS, or are more easily involved in the antioxidant system in cells. The difference in antioxidant activity may not only depend on the phenol content of the sample but also on the characteristics of the phenolic compounds contained in the sample, their synergies, and the existence of other chemicals ^[25]^[26]. Jun et al. showed that eckol, a phlorotannin isolated from ES ethanolic extract, enhanced heme oxygenase-1 protein and mRNA expression in HepG2 cells by activating c-Jun NH₂-terminal kinase and PI3K/Akt signaling pathways ^[27]. Iwai et al. ^[28] investigated the inhibitory effect of ES on oxidative stress in a diabetic KK-Ay mouse model. In their study, the polyphenol content and free radical scavenging activity of the methanol extract of ES were much higher than those of the water extract, and the active polyphenols in ES extracts were determined to be phlorotannins by LC/MS and HPLC-PDA analysis. Kang et al. ^[29] determined the inhibitory effect of five compounds (dieckol, phlorofucofuroeckol A, eckol, eckstolonol, and phloroglucinol) in ES extract on total ROS generation, of which phloroglucinol had the highest ability to inhibit total ROS generation with an IC₅₀ value of 30.82 ± 2.53 μM. The content and activity of functional compounds in seaweed may vary depending on the preservation conditions and/or processing methods used. Boiling can lead to the loss of the content and activity of the compound because the compound will easily dissolve into the water during the boiling process, or the activity of the compound will be destroyed and reduced at high temperatures ^[11]. Kuda et al. ^[11] demonstrated that the total phenolic content and antioxidant activity of ES are affected by a variety of factors, including processing methods and product type. They determined the antioxidant activity of four dried and two boiled ES products, of which both dried and boiled products exhibited lower antioxidant activity. The amount and activity of a compound can be greatly affected by the processing and storage of the product. The active ingredient dieckol contained in the ES extract was nine times more active than the standard butylhydroxytoluene and six times more active than L-ascorbic acid ^[30].

5. Anti-Obesity Activity

A clinical trial material made from ES extract significantly inhibited adipogenesis in 3T3-L1 cells and significantly reduced body weight gain, liver weight, white adipose tissue (WAT) weight, and adipocyte size in high-fat diet-induced obese mice. It also improved serum levels of total cholesterol, triglycerides, and LDL cholesterol, and increased HDL cholesterol. Western blot analysis showed that a clinical trial test material made of ES extract reduced the protein expression of C/EBP-α, PPAR-γ, and aP2 to inhibit adipocyte differentiation while promoting the expression of UCP-1 and CPT-1 in adipocytes to increase energy expenditure and play a key role in improving obesity ^[31]. Jin et al. ^[32] fed C57BL/6J mice with ES extract at a concentration of 150 mg/kg for six weeks, and the results showed that ES extract significantly reduced body weight gain and WAT weight in mice. In addition, ES extract can promote WAT browning and lipolysis in mice, with excellent anti-obesity effects. Lee et al. ^[33] isolated the sterol metabolite fucosterol from ES. Fucosterol exhibits an anti-adipogenic ability in vitro, which inhibits adipocyte differentiation and lipid accumulation by downregulating SREBP-1, PPAR-γ, and C/EBP-α, as well as the regulation of multiple signaling pathways (phosphoinositide 3-kinase/Akt and extracellular signal-regulated kinase-dependent forkhead box protein O signaling pathway) that play an anti-obesity role. The anti-adipogenic effect of ES has been demonstrated in a study by Jung et al. ^[2] in which it was reported that fucosterol, isolated from the methanolic extract of ES, reduced lipid accumulation in a concentration-dependent manner. This analyzed the active ingredients contained in the ES extract, and the results showed that the ES extract mainly contained five phlorotannins: phlorofucofuroeckol A, dioxinodehydroeckol, eckol, phloroglucinol, and dieckol. Among them, phlorofucofuroeckol A, eckol, and phloroglucinol exhibited concentration-dependent inhibition of lipid accumulation in adipocytes at concentrations ranging from 12.5–100 μM ^[34]. In a male Sprague–Dawley rat model of alcoholic fatty liver disease, ES extract decreased the expression of the triglyceride synthesis-related gene SREBP-1 and promoted the expression of PPAR-α and CPT-1 fatty acid oxidation-related genes to inhibit fat synthesis. It also reduces the blood levels of alanine aminotransferase, triglycerides, aspartate aminotransferase, and total cholesterol ^[35].

6. Anti-Diabetic Activity

Diabetes mellitus is a worldwide epidemic characterized by hyperglycemia, and its prevalence is increasing daily ^[36]. It is mainly caused by defective insulin secretion, impaired biological action, or both ^[37]. Long-term hyperglycemia leads to chronic damage and dysfunction of various tissues, especially of the eyes, kidneys, heart, blood vessels, and nerves ^[38]. Many studies have demonstrated that ES can effectively prevent and treat diabetes and its complications ^[28]^[39]^[40]. Iwai ^[28] identified ES as an effective diabetes preventive agent based on in vitro and in vivo studies. ES methanol extract containing 303.0 mg/g total polyphenol showed a strong inhibitory effect on α-glucosidase in vitro. In vivo, ES methanol extract was taken orally at 81.20 mg/day and plasma glucose levels were significantly reduced in KK-A Y diabetic mice after 4 weeks. Five phlorotannins, eckol, phlorofucofuroeckol-A, dieckol, phloroglucinol, and dioxinodehydroeckol were isolated from ES ethanolic extract. Among them, phlorofucofuroeckel-A, dieckol, eckol, and dioxinodehydroeckol all showed inhibition of amyloid-β_25–35 Self-Aggregation at the concentration of 10 μM. In addition, phlorofucofuroeckol-A inhibited D-glucose and D-ribose induced non-enzymatic insulin glycosylation in a dose-dependent manner ^[41]. Lee and Jeon isolated three phlorotannins 7-Phloroeckol, Dieckol, and phlorofucofuroeckol-A from ES methanolic extracts, which were able to inhibit the activity of the α-glucosidase enzyme ^[42]. Various phlorotannins such as phlorofucofuroeckol-A, dieckol, and eckol contained in ES had significant inhibitory effects on the activity of angiotensin-converting enzyme with IC₅₀ of 12.74 ± 0.15 μm, 34.25 ± 3.56 μm, and 70.82 ± 0.25 μm, respectively ^[43]. Jung et al. ^[40] isolated fucosterol from ES and reported that this compound showed moderate inhibitory activity against human recombinant aldose reductase and rat lens aldose reductase and was a mixed-type inhibitor. It was determined by the Autodock program that fucosterol could bind tightly to the enzymatic active site on aldose reductase, thus inhibiting its activity of aldose reductase. Six phlorotannins, 7-phloroeckol, dieckol, phloroglucinol, eckol, phlorofurofucoeckol-A, and dioxinodehydroeckol, were isolated from ES. Among these, 7-phloroeckol, dieckol, and phlorofurofucoeckol-A significantly inhibited α-glucosidase, with IC₅₀ values ranging from 1.37 to 6.13 µM. ES and its six phlorotannins also show significant inhibitory activity against protein tyrosine phosphatase 1 B ^[39].

7. Anti-Inflammatory Activity

In RAW 264.7, phlorofucofuroeckol A isolated from ES significantly inhibited the inflammatory response induced by lipopolysaccharide (LPS) and reduced the mRNA expression levels of inflammation-related proteins inducible nitric oxide synthase (iNOS) and cyclooxygenase-2 (COX-2), as well as the pro-inflammatory factors interleukin-1β, IL-6, and tumor necrosis factor-α. Phlorofucofuroeckol A also inhibits the activities of nuclear factor-κB (NF-κB) and AP-1 transcription factor promoters ^[44]. In LPS-stimulated RAW 264.7 cells, the ethanolic extract of ES decreased the expression of NF-κB by inhibiting the degradation of inhibitor κB-α and blocking the phosphorylation of mitogen-activated protein kinases and protein kinase B. Simultaneously, the ethanolic ES extract further downregulated the expression of inflammatory markers (IL-6, iNOS, TNF-α, COX-2, and IL-1β) by inhibiting the NF-κB pathway. The main anti-inflammatory components in the ethanolic extract were identified as phlorofucofuroeckol A and B by HPLC analysis ^[45]. Kim et al. ^[24] isolated three phlorotannins, dioxinodehydroeckol, dieckol, and phlorofucofuroeckol A, from ES using a series of column chromatography methods. Among these, only phlorofucofuroeckol A exhibited significant anti-inflammatory activity. Additionally, it further inhibited the production of NO and prostaglandin E2 by inhibiting the protein expression of iNOS and COX-2. In a study by Wei et al. ^[46], ES was first extracted using ethanol, followed by fractional distillation of the extract. The EtOAc fraction inhibited the production of prostaglandin E2 and nitric oxide in a dose-dependent manner and inhibited the expression of IL-6, TNF-α, and IL-1β pro-inflammatory cytokines. The main anti-inflammatory components in ES were identified by HPLC as 974-B, phlorofucofuroeckol A, 2′-phloroeckol, phlorofucofuroeckol B, and 6,6′-bieckol. Methanol: chloroform (1:2, v/v) was used to obtain the ES extract. It inhibits the activities of degranulated enzymes (lipoxygenase and hyaluronidase) in rat basophilic leukemia-2H3 cells in a dose-dependent manner, which may play a role in the treatment of allergic and inflammatory symptoms ^[47].

8. Treat Neurological Disorders

Alzheimer’s disease is a degenerative disease of the central nervous system that occurs in old age and pre-senile age and is characterized by progressive cognitive impairment and behavioral impairment and clinically manifested as memory impairment, aphasia, personality, and behavioral changes ^[48]. Hae et al. isolated eight phlorotannins, 7-phloroeckol, 2-phloroeckol, triphlorethol-A, dieckol, phlorofucofuroeckol-A, eckol, eckstolonol, and phloroglucinol, from the EtOAc fraction of ES ethanolic extract. Two sterols, fucosterol and 24-hydroperoxy 24-vinylcholesterol, were isolated from the n-hexane fraction. The compounds eckstolonol and phlorofucofuroeckol-A both exhibited inhibitory activities against acetylcholinesterase and butyrylcholinesterase with IC₅₀ values of 42.66 ± 8.48, 230.27 ± 3.52 μM, and 4.89 ± 2.28, 136.71 ± 3.33 μM, respectively. These results indicated that phlorotannins and sterols contained in ES have potential therapeutic effects in the treatment of Alzheimer’s disease ^[49]. In a study by Seong et al., four phlorotannins were isolated from ES ethanolic extract: phlorofucofuroeckol-A, dieckol, phloroglucinol, and dioxinodehydroeckol. Among them, phlorofucofuroeckol-A showed the highest inhibitory activity against human monoamine oxidase-A and B, with IC₅₀ values of 9.22 ± 0.19 and 4.89 ± 0.32 μm, respectively. In addition, Dieckol and phlorofucofuroeckol-A exhibited a multi-target combination of dopamine D3/D4 receptor agonism and antagonism of dopamine D1/serotonin/neurokinin-1. This suggests that the phlorotannins contained in ES are potential drugs for the treatment of neuronal diseases ^[50].

9. Other Functionalities

Dieckol, isolated from ES, reduced the increase in the number of human hepatocellular carcinoma Hep3B cells and induced apoptosis in a dose-dependent manner. Dieckol increases the permeability of the mitochondrial membrane, promotes the release of the apoptotic factor cytochrome c, and induces apoptosis in Hep3B cells ^[51]. ES extract inhibited the expression of matrix metalloproteinase-1 in human dermal fibroblasts and also had a significant inhibitory effect on NF-κB and AP-1. HPLC analysis identified eckol and dieckol as effective anti-photoaging components in the extract by HPLC analysis ^[52]. Jun et al. prepared ES gold nanoparticles (GNPs) by mixing ES extract (2 mg/mL) with 1 mM gold (III) chloride solution with vigorous stirring and then incubating at 25 °C for 15 min. The antisenescence effect of ES-GNPs in a human dermal fibroblasts (HDF) senescence model induced by ultraviolet A (UVA) irradiation was investigated. The results showed that ES-GNPs exerted antisenescence effects on UVA-irradiated HDF by inhibiting MMP-1/-3 expression and SA-β-galactosidase activity ^[53]. In addition, fucosterol extracted from ES down-regulated the expression of glucose-regulated protein 78 to alleviate soluble amyloid beta peptide_1–42-induced cognitive impairment in aging rats ^[54]. In vitro, ES extract (1000 µg/mL) significantly reduced phenylephrine-induced cardiomyocyte hypertrophy and directly inhibited the activity of p300-HAT as well as the acetylation of histone H3K9. In in vivo experiments, treatment of mice with myocardial infarction with ES extract showed that ES significantly inhibited the increase in myocardial cell diameter, vascular fibrosis, and histone H3K9 acetylation ^[9]. The ES formulation can significantly inhibit liver injury induced by carbon tetrachloride in rats, promote an increase in antioxidant enzymes, and inhibit the activity of CYP2E1 in a dose-dependent manner ^[55]. The ethanolic extract of ES (163.93 μg/mL) showed inhibitory properties on angiotensin-converting enzyme with an inhibition rate of more than 50% ^[56]. The methanol extract of ES and four phlorotannins (7-phloroeckol, dieckol, phlorofucofuroeckol A, and eckol) isolated from ES effectively inhibited the Cu2+-induced oxidation of low-density lipoprotein ^[57]. Fucosterol, isolated from the leafy thalli of ES, significantly ameliorated the increase in ROS levels and decrease in glutathione levels induced by tert-butyl hydroperoxide and tacrine ^[58]. Vo et al. isolated a novel phlorotannin fucofuroeckol-A (F-A) from ES extracts—and investigated the protective effect of FA on ultraviolet B (UVB)-induced allergic reactions in RBL-2H3 mast cells. They found that F-A (50 μM) could prevent mast cell degranulation by promoting the elevation of intracellular Ca²⁺ and inhibiting the release of histamine and showed inhibitory effects on the production of TNF-α and IL-1β, which could effectively prevent the occurrence of allergic reactions caused by UVB ^[59].

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Xiao Men

Xionggao Han

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Geon Oh

Heegu Jin

Hyun-Ji Oh

Eunjin Kim

Jongwook Kim

Boo-Yong Lee

Sun-Il Choi

Ok-Hwan Lee

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