2021, Vol. 20
2) Laboratory for Marine Drugs and Bioproducts of Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China
Brown algae is widely distributed throughout various seas around the world. At present, there are approximately 2000 species according to statistical reports (Thompson et al., 2019). It is well known for its richness in bioactive compounds, such as polysaccharides, polyphenols, omega-3 fatty acids, and carotenoids, which have considerable economic values (Wijesekara et al., 2011). Laminarin, the storage carbohydrate in brown algae, is also known as brown algal starch and is mainly formed by glucose monomers connected by β-1, 3-glucosidic bonds on its backbone and partial β-1, 6-glucosidic bonds on its branches (Kadam et al., 2015). It belongs to the family of β-glucans because of its single structure and connection method (Rioux et al., 2010). The laminarin content of brown algae is related to the species, growth environment, and harvest season. Generally, Saccharina, Laminarina, and Fucus spp. are the main sources of laminarin, and their laminarin content can be up to 62% of total dry weight at the highest. It has been reported that during the summer and autumn, laminarin accumulates and its content in Laminaria digitata increase, while during the winter, the content decreases due to the consumption of energy for new tissue growth (Adams et al., 2011). As a kind of functional marine algal polysaccharide, laminarin possesses a wide range of biological activities, including antitumor, antioxidant, anti-inflammatory, prebiotic, and other biofunctional activities (Kim et al., 2006; Kadam et al., 2015). In addition, it also plays an important role in the marine carbon cycle (Becker et al., 2020). As a relatively underexploited algal polysaccharide, laminarin also can be transformed into bioethanol through the bioprocess of fermentation (Lee and Lee, 2016). Therefore, laminarin possess an array of important applications in the fields of food, medicine, cosmetics, and energy.
Marine algal oligosaccharides can be obtained from marine algal polysaccharides through physical or chemical and enzymatic methods. Currently, marine algal oligosaccharides, such as alginate oligosaccharides, agar oligosaccharides, and carrageenan oligosaccharides, have received increasing attention due to their excellent solubility, bioavailability and prominent biological activities. Similarly, laminarin oligosaccharides, the degradation products of laminarin, can also be prepared by these strategies of physical hydrolysis, chemical hydrolysis, and enzymatic degradation. It has been reported that laminarin oligosaccharides have a significant effect on improving immunity and antitumor activity, and regulating the intestinal flora (Yvin et al., 1999; Kim et al., 2006; Kadam et al., 2015).
The present article reviews the preparation strategies, biofunctional activities, and potential applications of laminarin and laminarin oligosaccharides.
2 Preparation of LaminarinThe process of laminarin preparation can be divided into pre-treatment of raw materials, extraction, and purification. Generally, the raw materials need to be washed several times to remove epiphytes and sands, and dried thoroughly (Imbs et al., 2016). Traditionally, laminarin is extracted from dried brown algae with high temperature and mild acidic conditions. Nowadays, some environment-friendly green methods, including enzymatic extraction and microwave extraction, can also be exploited for laminarin preparation.
2.1 Traditional Laminarin Extraction StrategyDuring the traditional solvent extraction process, the appropriate concentration of ethanol can precipitate laminarin and separate some impurities. After ultrafiltration and dialysis, laminarin can be isolated (O'Shea et al., 2014). Most laminarin extraction methods use mild acidic or basic solvents. The type of acid solution and extraction temperature can affect the extraction efficiency of laminarin. Devillé et al. (2004) investigated the extraction of laminarin by different acid solutions. The results showed that HCL produces a higher extraction yield than H2SO4. Meanwhile, a high temperature can facilitate laminarin extraction and improve the yield. In fact, a high temperature was beneficial to the extraction of laminarin. Zha et al. (2012) extracted laminarin from Laminaria japonica at 4, 20, 40, 60, and 80℃ using water as the extraction solvent. The results showed that when the temperature was increased from 4 to 60℃, there was a corresponding increase in the quantity of laminarin. When the temperature was increased sequentially, the total sugar amount remained unchanged, and some extracted laminarin was degraded into laminarin oligosaccharides. Following the initial extraction, the obtained solution contained mixed polysaccharides such as laminarin, fucoidan, and alginate. CaCl2 or MnCl2 can be added to the solution to eliminate the alginate because alginate exhibits gel properties in the Ca2+ or Mn2+ solution (Cong et al., 2016). Rioux et al. (2010) used CaCl2 solution as a solvent to extract laminarin at 85℃ for 4 h. The same volume of sodium chloride solution (2%) and twice the volume of anhydrous ethanol were added to the extraction solution to precipitate the laminarin for 1 h at room temperature. Finally, laminarin can be further purified from the crude extract following the purification procedures described below (Cong et al., 2016).
2.2 Innovative Extraction Strategy of LaminarinIn addition to the traditional extraction methods, some environmentally friendly and efficient extraction methods, such as enzyme-assisted extraction (EAE), microwave-assisted extraction (MAE), and ultrasound-assisted extraction (UAE), have been used for the gradual extraction of laminarin (Chen et al., 2013).
EAE is a promising extraction strategy (Zhu et al., 2014). Charoensiddhi et al. (2016) used three commercial cell wall carbohydrate hydrolytic enzymes and three proteases to assist in the extraction of laminarin from the brown seaweed Ecklonia radiata at 50℃ for 24 h. During this process, the cell walls of the algae were broken up, and the polysaccharides containing laminarin were released. Subsequently, lyophilization and fractionation were employed for the isolation and purification of laminarin, and the molecular weight (Mw) of the purified laminarin was less than 65 kDa.
Microwaves have good penetrability and are effective for the extraction of active, heat sensitive substances (Pap et al., 2013). It was found that the amount of laminarin extracted increased with increasing microwave power during the MAE process (Gao et al., 2006). However, when the microwave power exceeded 400 W, the amount of laminarin extracted gradually decreased. It was speculated that excessive power can cause the degradation of laminarin. Therefore, it is necessary to control the power level in the MAE process to keep the yield and activity of laminarin. Many algal polysaccharides have been extracted with MAE up to now, such as fucoidan from Fucus vesiculosus, Undaria pinnatifida, and Ascophyllum nodosum (Quitain et al., 2013). Therefore, MAE shows good prospects for application in laminarin extraction.
UAE (ultrasound-assisted extraction) is another cost-effective laminarin extraction technology with great potential for large-scale industrialization (García-Vaquero et al., 2017). In addition to polysaccharide extraction, UAE has been used to extract functional components such as phycoerythrin, amino acids, and lipids from a variety of algae sources (Adam et al., 2012). Kadam et al. (2015) used UAE with an ultrasonic power amplitude of 69% to extract laminarin from Ascophyllum nodosum. The extracts were treated with 0.1 mol L−1 HCl for 15 min followed by solid-liquid extraction. Finally, the amount of laminarin obtained was estimated to be 5.82% of the dry weight of A. nodosum. The 1, 1-diphenyl-2-picryl-hydrazyl (DPPH) radical-scavenging activity of the extracted laminarin reached as high as 93.23%, demonstrating a good antioxidant activity.
These new extraction strategies lay an industrial foundation for the efficient extraction of polysaccharides and other active substances from marine algae. A comparison of these extraction strategies is outlined in Table 1.
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Table 1 Comparison of several strategies for extracting laminarin |
In order to remove impurities such as other polysaccharides, proteins, and phenolic compounds from the crude laminarin extract, it is necessary to further purify laminarin (Ale et al., 2011). In fact, the procedures of laminarin extraction and laminarin purification are sometimes not strictly distinguishable, because some extraction processes include certain purification steps. For example, the fractional precipitation of laminarin described in the extraction section can also be considered as a step of laminarin purification. The laminarin purification process described in this section mainly refers to the next step of separation and purification of pure laminarin to detect its biological activity. At present, the common methods of pure laminarin purification include size-exclusion chromatography (SEC) and affinity chromatography (AC).
SEC can be used to separate and purify polysaccharides according to their molecular weights (Mw). Thus, SEC is an efficient and convenient method for separating and purifying laminarin. Zhang et al. (2015) used this method with a Waters UltrahydrogelTM WATO 11530 size-exclusion column (300 mm × 7.8 mm) to separate algal polysaccharides and obtained 383.8 mg g−1 of laminarin, which showed a good purification effect. In addition, SEC can be used as an effective method to determine the Mw of polysaccharides (Gaborieau and Castignolles, 2011).
AC (affinity chromatography) is a powerful method to separate, purify, and analyze target compounds in a sample (Pohleven et al., 2012). Affinity columns can be used alone or together with other purification methods to purify laminarin (Hirabayashi et al., 2002). At present, AC has been used to successfully separate a variety of active substances, such as proteins, enzymes, antibodies, and polysaccharides (Hahn et al., 2016). This method is commonly used in the purification of sulfated polysaccharides (Mak et al., 2013). Labourel et al. (2015) combined both AC and SEC for the analysis of enzymatic products of laminarin and found that the laminarinase ZgLamCGH16 preferentially hydrolyzed branched laminarin.
SEC can be combined with many purification methods for further separation and purification of the target products. AC is mainly used to separate biomacromolecules such as proteins according to their different chemical structures. SEC and AC have been applied successfully in the purification of many polysaccharides (García-Vaquero et al., 2017). However, high cost remains the main factor limiting their large-scale application. In addition to the above chromatography methods, there are other purification methods, such as ultrafiltration and membrane filtration (Oda et al., 2016). Ultrafiltration and membrane filtration can be used to separate diverse solutions and are suitable for polysaccharide purification on an industrial scale, but the product purity is relatively low. Therefore, the appropriate purification methods are usually selected according to actual needs.
These methods can be chosen to further characterize the biological activity of laminarin. The processes of laminarin extraction and purification are presented in Fig. 1.
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Fig. 1 Laminarin extraction and purification processes. |
In general, laminarin oligosaccharides can be prepared
by depolymerization of laminarin (chemical, physical, and enzymatic hydrolysis) (Iji and Tivey, 1998). Furthermore, laminarin oligosaccharides can also be produced by synthesis from disaccharide or monosaccharide substrates.
3.1 Laminarin Oligosaccharide Preparation by Chemical and Physical HydrolysisMany algal polysaccharides, such as fucoidan, carrageenan, and agarose, can be degraded into oligosaccharides by acidic hydrolysis at high temperatures due to the cleavage of glycosidic bonds (Chen et al., 2005). Laminarin oligosaccharides can also be produced by partial acid hydrolysis and then separated by size-fractionation and reversed-phase high-performance liquid chromatography (Natsuka et al., 2018). As an effective method of degrading polysaccharides, acid hydrolysis can help us to understand the specific structure of polysaccharides. Graiff et al. (2016) explored the preparation of laminarin oligosaccharides by using 0.5 mol L−1 H2SO4 to hydrolyze commercial laminarin. The hydrolysis temperature was 121℃, and the ionexclusion chromatography results showed that when the hydrolysis time was 5 min, there were oligosaccharides in the hydrolytic products. When the hydrolysis time was extended to 180 min, the chromatogram showed only glucose and sulfuric acid without oligosaccharides in the products (Renard et al., 1997).
Radiolysis, such as ultraviolet light and gamma rays, can induce the degradation of polysaccharides by breaking glycosidic bonds and is the main physical treatment for oligosaccharide preparation (Ramani and Ranganathaiah, 2000). Gamma irradiation has been applied to the acquisition of oligosaccharides (Nagasawa et al., 2000). Choi et al. (2011) used gamma irradiation to obtain laminarin oligosaccharides, and the results of Nuclear Magnetic Resonance (NMR) analysis indicated that the glycosidic bonds of laminarin were randomly broken. The antioxidant activity of the prepared laminarin oligosaccharides was higher than that of laminarin. Unlike chemical methods, physical hydrolysis for laminarin oligosaccharide production is eco-friendly. However, laminarin oligosaccharides with the desired degree of polymerization (DP) cannot be produced by physical irradiation of polysaccharides, and long exposure times to physical radiation may cause damage to the structures of oligosaccharides (Delattre et al., 2005).
3.2 Laminarin Oligosaccharide Preparation by Enzymatic DegradationSome enzymes can efficiently and specifically hydrolyze laminarin into laminarin oligosaccharides under mild conditions. Enzymes that can specifically hydrolyze laminarin include endo-β-1, 3-glucanase (laminarinase, EC 3.2.1.39) and exo-β-1, 3-glucanase (EC 3.2.1.58) (Santos et al., 1979). Laminarinase can randomly cleave (1→3)-β-linkages within laminarin glycoside bonds to release oligosaccharides, while exo-β-1, 3-glucanases can hydrolyze laminarin by sequentially cleaving glucose residues from the non-reducing end and release glucose (Bara et al., 2003). There are many reports about laminarinases from bacteria, fungi, higher plants, and archaea isolated from soil and marine environments (Tschiggerl et al., 2008). These glycoside hydrolases can be used not only to prepare oligosaccharides, but also to accurately quantify laminarin in marine organic matter. Becker et al. (2017) used laminarinase to digest glycans selectively and quantify laminarin in particulate organic matter.
The main sources of laminarinase include bacteria (such as Bacillus circulans, Flavobacterium johnsoniae, Paenibacillus sp., Rhodothermus marinus, and Thermotoga maritima), fungi (such as Candida albicans, Saccharomyces cerevisiae, and Yarrowia lipolytica), and algae (such as L. digitata) (Sandini et al., 2007; Li et al., 2009; Kim et al., 2011; Kusaykin et al., 2017). According to sequence information, endo-β-1, 3-glucanases can be grouped into six glycoside hydrolase (GH) families including GH16, GH17, GH55, GH64, GH81, and GH128 in the CAZy database (http://www.cazy.org/) (Sakamoto et al., 2011). Similarly, exo-β-1, 3-glucanases can be classified into GH3, GH5, GH17, GH55, and GH132 in the CAZy database (Kumar et al., 2018). Based on amino acid sequence divergence, most laminarinases derived from bacteria are categorized into GH16, while laminarinases originating from plants are all assigned to GH17 (Sandini et al., 2007). Diverse laminarinases have been employed for the preparation of laminarin oligosaccharides. The characteristics and hydrolysis products of laminarinases from different GH families are listed in Table 2.
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Table 2 Action patterns, hydrolysis products, optimum pH, and temperature of laminarinases |
Most of the characterized laminarinases belonging to the GH16 family have conserved sequences. For example, the conserved sequences of the laminarinase from the marine bacterium Formosa algae KMM 3553 include the sequences WPAXWXL (substrate binding site) and EIDXXE (catalytic active site) (Kusaykin et al., 2017). Until now, crystal structures of different laminarinases from the GH16 family have been analyzed, and their crystal structures share a β-jelly-roll fold, and the inner β-fold bends outward to form a long catalytic groove (Dong et al., 2015) (Fig. 2A). The laminarinase from P. rolfsii c3-2(1) IBRL belongs to the GH16 family, and it is a thermostable laminarinase that can hydrolyze laminarin to laminaribiose and glucose at 70℃ (Lee et al., 2014). The heat resistance of this laminarinase and its product characteristics indicate its application in the preparation of laminarin oligosaccharides. Recently, Badur et al. (2020) reported three laminarinases from Vibrio breoganii 1C10 belong to the GH16 family. As a member of these laminarinases, laminarinase VbGH16C can hydrolyze laminarin to oligosaccharides of DP8 and DP9. This characteristic of the hydrolysate can be applied in the preparation of relatively large laminarin oligosaccharides.
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Fig. 2 Three-dimensional structures of laminarinases, including laminarinase ZgLamC of the GH16 family (PDB: 4CTE), laminarinase of the GH17 family (PDB: 2CYG), laminarinase LPHase of the GH64 family (PDB: 3GD9), and laminarinase ZgLamC of the GH81 family (PDB: 4K35). |
The laminarinases derived from plants that have been reported so far belong to GH17 (Badur et al., 2020). Their crystal structures have a typical (roll) 8 TIM-barrel structure, which consists of eight α-helices and eight β-sheets. Laminarinases of GH17 share many conserved sequences, which encode many α-helices, η-helices, β-sheets, and strict β-turns (Ezzine et al., 2016). Receveur-Bréchot et al. (2006) revealed a crystal structure at 1.45-Å resolution of the β-1, 3-glucanase Ban-Gluc from banana. Its three-dimensional structure consists of an internal crown of eight β-strands connected by extended loops to an outer crown of eight α-helices, which exhibit the typical (α/β) 8 TIM-barrel motif (Fig. 2B). There are a few reports on these laminarinases about the preparation of laminarin oligosaccharides, some of which even lack the degradation activity of laminarin (Menu-Bouaouiche et al., 2003). Recently, the laminarinase VbGH17A belonging to GH17 family was identified from V. breoganii 1C10 by Badur et al. (2020). It can hydrolyze laminarin into a series of laminarin oligosaccharides (DP4-DP9). In contrast, complex laminarin oligosaccharide products with different DP may cause difficulties in the separation and purification of laminarin oligosaccharides at a later stage, which is not conducive to the production of laminarin oligosaccharides.
Compared with laminarinases belonging to GH16 and GH17, there have been fewer studies on laminarinases of GH55, GH64, and GH81. Until now, only the crystal structures of laminarinases belonging to GH64 and GH81 have been reported (Ezzine et al., 2016; Badur et al., 2020).
Wu et al. (2009) revealed the essential amino acid residues and crystal structure at 1.80 Å resolution of the laminarinase LPHase of GH64 from S. matensis DIC-108. Its conserved sequences include two strictly conserved carboxylates (Glu154 and Asp170) and several saccharidelinked residues (Thr156, Thr167, Trp163, Asn165, and Val169). The LPHase structure consists of a barrel domain and a mixed (α/β) domain, and its main hydrolysate is laminaripentaose (Fig. 2C). The homogeneous product of enzymatic hydrolysis is conducive to the preparation of laminarin oligosaccharides.
Zhou et al. (2013) reported essential residues and a crystal structure to resolutions of 2.3 and 2.0 Å of the laminarinase as a member of GH81 from Rhizomucor miehei. The conserved amino acid residues (251–343 aa) may be involved in the stabilization of the whole structure. The overall structure of the laminarinase mainly consists of a β-sandwich domain and a C-terminal (α/α)6 domain (as shown Fig. 2D). Kumar et al. (2018) reported a thermostable laminarinase belonging to GH81 from C. thermocellum, and its hydrolysates are a series of oligosaccharides (DP2 to DP7).
3.3 Laminarin Oligosaccharide Preparation by Synthesis StrategiesSeveral algal oligosaccharides, such as alginate oligosaccharides and fucose oligosaccharides, can be produced by organic synthesis and biosynthesis (Mong et al., 2003). These synthesis strategies have also been applied in the preparation of laminarin oligosaccharides. He et al. (2003) reported an organic synthesis strategy. He used a 4, 6-Obenzylidenated acceptor for β-(1→3) bond formation to avoid the predominant generation of α glycosides. Eventually, a homogeneous laminarin oligosaccharide (DP4) with α-(1→3) and α-(1→6) bonds was prepared, and the yield was up to 43%. However, the operational steps were cumbersome and costly, and the synthesis of oligosaccharides was accompanied by the introduction of other glycosidic bonds. In contrast, the biosynthesis of laminarin oligosaccharides can be accomplished with other methods at a low cost. Sun et al. (2019) designed an in vitro multienzyme catalytic system consisting of α-glucan phosphorylase and laminaribiose phosphorylase. This catalytic system could convert low-value starch and glucose into highvalue laminaribiose, which can be used to synthesize hyaluronic acid.
In contrast to the degradation of polysaccharides, oligosaccharide synthesis is based on oligosaccharides with smaller Mw (Boons, 1996). However, there are only a few studies on the biosynthesis of laminarin oligosaccharides, and only a few laminarin oligosaccharides with a specific DP can be synthesized. Table 3 presents strategies for laminarin oligosaccharide preparation, specific methods, production, advantages, and disadvantages of each strategy.
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Table 3 Strategies for laminarin oligosaccharides preparation, specific methods, production, advantages and disadvantages of each strategy |
Laminarin and laminarin oligosaccharides have been widely reported for their biological functions. Like other algal polysaccharides, laminarin has prebiotic, antioxidant, and anti-inflammatory activities (Kim et al., 2006; Kadam et al., 2015). In addition, due to its unique triple helical structure, laminarin also exhibits excellent antitumor and anticancer activities, which can be applied to drug development (Novak and Vetvicka, 2008). The biological activities of laminarin and laminarin oligosaccharides are considered to depend on their molecular structure, such as the DP, the introduction of sulfate groups, and the side chain branches (Pang et al., 2005; Menshova et al., 2014; Zargarzadeh et al., 2020). Therefore, appropriate structural modification of laminarin can significantly improve its biological activities.
4.1 Antitumor and Anticancer ActivitiesTo date, many studies have shown that laminarin and laminarin oligosaccharides have significant antitumor and anticancer activities (Park et al., 2012). The mechanisms of antitumor and anticancer activities of laminarin and laminarin oligosaccharides include apoptosis and inhibition of cancer cell colony formation (Zargarzadeh et al., 2020). For instance, the capacity of laminarin to induce apoptosis in HT-29 colon cancer cells was investigated by Park et al. (2013). The results demonstrated that laminarin extracted from Laminaria digitate could not only induce apoptosis in HT-29 colon cancer cells through an apoptotic pathway involving growth factors, but also regulate the ErbB signaling pathway. Ji et al. (2012) used different concentrations of laminarin to treat human colon cancer LOVO cells at different times. The intracellular reactive oxygen species (ROS), pH, intracellular calcium ion concentration, mitochondrion permeability transition pore, mitochondrial membrane potential, and expression levels of Cyt-C, Caspase-9, and Caspase-3 were detected and analyzed. It was found that laminarin could induce human colon cancer LOVO cell apoptosis through a mitochondrial pathway. Subsequently, the relationship between laminarin-induced apoptosis and the death receptor-mediated (DR-mediated) pathway in human colon cancer LOVO cells was illuminated by Ji and Ji (2014). The structural characteristics and antitumor activity of laminarin from Eisenia bicyclis were determined and analyzed by Ermakova et al. (2013). Laminarin exhibited no direct cytotoxicity and showed significant antitumor activity against SK-MEL-28 human melanoma cells.
Similarly, Usoltseva et al. (2016) also found that laminarin extracted from Alaria angusta and A. angusta had no cytotoxicity in vitro and could effectively inhibit colony formation in HT-29 cells. Tian et al. (2020) elucidated the anticancer effect of laminarin from L. japonica on Human HCC cell lines (Bel-7404 and HepG2). The results revealed that laminarin could inhibit the proliferation of Bel-7404 and HepG2 cells in a dose-dependent manner, and the expression levels of SMP-30 in laminarin-treated cells were lower than those in the control LO2 cells. Thus, it is speculated that laminarin can inhibit cancer cells by regulating the expression levels of SMP-30.
Laminarin oligosaccharides also showed obvious anticancer activity (Pang et al., 2005; Menshova et al., 2014). The human tissue lymphoma cell line (U937 cells) was treated with the hydrolytic products of laminarin oligosaccharides LB and LI, respectively (Pang et al., 2005). The results suggested that LB can inhibit the proliferation of U937 cells by stimulating monocytes to produce cytokines. Moreover, it was revealed that specific enzymatic products (laminarin oligosaccharides with DP 9-23) with a high content of 1, 6-linked glucose residues showed significant anticancer activity, and they could inhibit colony formation in melanoma and colon cancer cells (Menshova et al., 2014). This also provides new ideas to produce laminarin products with high antitumor activity through enzymatic hydrolysis.
Additionally, laminarin can be modified to enhance its antitumor and anticancer activities. Ji et al. (2013) applied the chlorosulfonic acid-pyridine method for laminarinsulfated modification and obtained a sulfated laminarin (LAMS) with a sulfate content of 45.92%. The main sulfate substitution site was at the hydroxyl groups of C2 and C6. The MTT assay (MTT) results showed that LAMS had more obvious inhibition effects than laminarin on LoVo cell growth, which suggested that LAMS had better antitumor activity. It was hypothesized that the introduction of sulfate groups can not only change the molecular structure and spatial conformation of laminarin, but also enhance its anion repulsion to stretch the sugar chains and form hydrogen bonds. These changes lead to the formation of a helical structure and adoption of an active conformation, which enhances the antitumor activity of laminarin (Zargarzadeh et al., 2020). This means that some specific structural modifications such as sulfated modification is an effective method to enhance the antitumor activity of laminarin. Nanoparticle modification of polysaccharide structure is another strategy to improve its physical and chemical properties. Laminarin decorated with selenium nanoparticles (LP-SeNPs) was prepared by Cui et al. (2019). Laminarin with nano modification can induce mitochondria-mediated apoptosis of tumor cells (HepG2 cells) by promoting the expression of Bax and decreasing the expression of Bcl-2.
4.2 Prebiotic ActivityIt has been well documented that many algal polysaccharides and their functional oligosaccharides play an important role in regulating human intestinal health, which is considered as a prebiotic activity (Ramnani et al., 2012). The prebiotic activities of laminarin and laminarin oligosaccharides have also aroused the interest of many scholars. It was confirmed that neither in vitro hydrochloric acid under physiological conditions nor in vitro homogenates of the human digestive system can hydrolyze laminarin and laminarin oligosaccharides (Walsh et al., 2013; Kadam et al., 2015). Laminarin and laminarin oligosaccharides are resistant to hydrolytic enzymes in the human upper gastrointestinal tract (Devillé et al., 2004). However, the intestinal microflora can utilize laminarin and laminarin oligosaccharides (Devillé et al., 2007). Therefore, laminarin and laminarin oligosaccharides cannot be degraded and absorbed by host. Thus they can become prebiotics potentially. This beneficial effects of laminarin on intestinal microorganisms were demonstrated by Nguyen et al. (2016). With the supplementation of laminarin in the diets of mice, a significant increase in Bacteroides and a significant decrease in Firmicutes were observed. The results suggested that laminarin could enhance the high energy metabolism of the gut microbiota to reduce the side effects of a high-fat diet. Zaporozhets et al. (2014) proposed the prebiotic properties of laminarin. Moreover, it was shown that laminarin could regulate intestinal metabolism via its effect on mucus composition, the intestinal pH, and short-chain fatty acids (SCFA) (Devillé et al., 2007). Leal et al. (2017) found that laminarin oligosaccharides were beneficial to the growth of Bifidobacterium animalis and Lactobacillus casei, and could increase their production of SCFA, such as lactic acid and acetic acid.
4.3 Antioxidant ActivityLaminarin and laminarin oligosaccharides present good antioxidant activity (Zhou et al., 2009). Jia et al. (2010) separated and purified laminarin from L. Japonica by gel chromatography and obtained two components with Mw of 5.5 × 104 and 2.7 × 104 Da. The results indicated that the laminarin with 5.5 × 104 Da had a good scavenging effect on the hydroxyl free radical, superoxide anion free radical, and diphenyl generation of free radical.
When laminarin oligosaccharides were prepared by gamma irradiation of laminarin (Choi et al., 2012), they showed higher ferric reducing antioxidant potential values and greater DPPH radical-scavenging than that of nonirradiated laminarin. This means that proper reduction of the DP of laminarin can enhance its antioxidant activity. However, the mechanism remains to be further explored.
4.4 Anti-Inflammatory ActivityStudies have confirmed that several algal polysaccharides and their oligosaccharides exhibited excellent antiinflammatory activity (Dore et al., 2013). Dectin-1 is a receptor related to extracellular pathogen recognition. Previous studies found it was associated with anti-inflammatory activity (Karsten et al., 2012). Smith et al. (2018) tested the biological activity of five different laminarin preparations and identified some of them as either Dectin-1 antagonists or agonists. Kim et al. (2006) prepared laminarin with Mw between 5 and 10 kDa and laminarin oligosaccharides derived by enzymatic hydrolysis. Both laminarin and laminarin oligosaccharides showed good results for suppression of apoptosis and extension of cell survival in culture. A mouse cDNA microarray indicated that the genes coding immune response proteins were induced in the process, which showed potential for application as new immunopotentiating substances of laminarin and laminarin oligosaccharides.
In addition, laminarin and laminarin oligosaccharides can also be prepared as a drug for treating inflammatory diseases induced by non-specific inflammatory responses (Yvin et al., 2006).
4.5 Applications in CosmeticsSkin protection and repair functions of laminarin have been proven (Yvin et al., 1999; Li et al., 2013). Yvin et al. (1999) found that laminarin and laminarin oligosaccharides had stimulating, regenerating, modulatory, and energizing effects on human dermis fibroblasts and human epidermis keratinocytes, which is useful in cosmetics. Li et al. (2013) explored the effect of laminarin on matrix metalloproteinase activity in photoaging skin. The results indicated that laminarin can regulate the metabolism of lightaged skin collagen by regulating matrix metalloproteinase activity. In addition, laminarin has a positive effect on wound healing (Choi et al., 2013).
4.6 Applications in Plant Disease Control and Growth PromotionThe fruit, leaves, and crowns of plants are vulnerable to pathogens such as Botrytis cinerea and Aspergillus flavus, causing huge economic losses. Chemical control of plant disease not only causes environmental pollution but also is harmful to human health (Hirooka and Ishii, 2013). Algal polysaccharides can increase basal metabolism and cell division as well as the level of essential oils or biomolecules in plants, which can trigger protection against pathogens (González et al., 2013). Laminarin has been applied in the control of strawberry leaf spot and powdery mildew under field conditions. The results showed that laminarin can reduce the incidences of leaf spot and powdery mildew by 50% and 70% – 80%, respectively. Its effectiveness at inhibiting B. cinerea infection was also obvious, and the inhibition rate was as high as 80% (Meszka and Bielenin, 2011). Aflatoxin contamination has been a worldwide problem. Laminarin extracted from L. digitata had inhibitory effects on growth and toxin production of A. flavus (Hu et al., 2012). Laminarin also can be used as a plant growth-promoting agent. For instance, laminarin could stimulate the germination of seeds through interfering with pathways that can lead to α-amylase formation (Yvin et al., 1998). In another study, transcriptome analysis indicated that laminarin can regulate the DEFL-mediated pathway, thus affecting abiotic stress tolerance in plants (Wu et al., 2016).
4.7 Applications in Feed AdditivesLaminarin can be used as a high-value feed additive, which can effectively improve growth performance, enhance the immune response, and regulate the gut microbiota of animals. Researchers found that the developmental competence of early-stage porcine embryos could be dramatically improved when laminarin was used as a feed additive (Jiang et al., 2018). Some important physiological parameters, such as the blastocyst formation rate, hatching rate, and total cell number in the blastocyst significantly increased when 20 mg mL−1 of laminarin was used as a food additive during the in vitro culture period of early-stage porcine embryos (Jiang et al., 2018). Walsh et al. (2013) confirmed that the supplementation of laminarin could suppress the secretion of pro-inflammatory cytokines, which could be helpful for the growth performance of pigs. After laminarin extracted from L. digitate was added to the diets of pigs, intestinal bacterial populations, volatile fatty acid concentrations, and the expression levels of cytokines and mucin genes in the ileum and colon were determined and analyzed by Smith et al. (2011). The results indicated that laminarin can improve gut health in the pig. In addition, dietary supplementation with laminarin and fucoidan could enhance pork meat quality through reducing saturated fatty acids and lowering lipid oxidation in longissimus thoracis and lumborum muscle of pig (Moroney et al., 2015).
Similarly, laminarin has been used as a feed additive in fish breeding. After growth performance, biochemical parameters, and the expression levels of immune-related genes in Epinephelus coioides fed with laminarin were measured, the results indicated that laminarin could regulate the immune response and promote the growth of fish (Yin et al., 2014).
4.8 Applications in Bioethanol ProductionBioethanol, a clean fuel, is considered as an important solution to the current fossil fuel energy crisis (Amin, 2009). Although technologies for ethanol production through yeast fermentation are relatively mature, production costs remain the main barrier to bioethanol application. Due to its abundant resources, algal polysaccharide can be one of the ideal feedstocks for bioethanol production. Remarkably, laminarin is composed of glucose, which is the preferable fermentable sugar in bioethanol producers such as S. cerevisiae and Zymomonas mobilis (Al Abdallah et al., 2016). Therefore, laminarin may emerge as a potential substrate for bioethanol production. For example, an optimized combination of laminarinase and β-glucosidase-displaying yeasts could directly transform laminarin into bioethanol, and the bioethanol yield was 5.2 g L−1 (Motone et al., 2016). A two-stage bioprocess using an immobilized laminarinase and a marine-derived yeast for bioethanol production from laminarin was established by Mitsuya et al. (2017). Finally, 0.51–0.58 g L−1 bioethanol was yielded from the saccharified solution prepared via the immobilized laminarinase. Fig. 3 shows the biological activities and potential applications of laminarin and laminarin oligosaccharides.
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Fig. 3 The biological activities and potential applications of laminarin and laminarin oligosaccharides. |
As one of the important marine algal polysaccharides derived from brown algae, laminarin has many biofunctional activities. With the development and progress of the extraction process, EAE-, MAE-, and UAE-assisted extraction methods are becoming promising extraction strategies for laminarin as they are environmentally friendly and efficient (Chen et al., 2013).
Laminarin has many excellent health beneficial effects. The mechanisms of antitumor and anticancer activities of laminarin, such as apoptosis (ErbB signaling pathway, mitochondrial pathway, and DR-mediated pathway) and inhibition of cancer cell colony formation (SMP-30), have been summarized and discussed in this review. Laminarin oligosaccharides possess higher antioxidant and antitumor activities than laminarin (Menshova et al., 2014), while the differences of other biological activities between laminarin oligosaccharides and laminarin, such as prebiotic activity and anti-inflammatory activity, have not been studied in detail thus far. Therefore, large-scale preparation of laminarin oligosaccharides and evaluation of their more specific biological activities are a focus of research. Enzymatic degradation of laminarin by using laminarinases is one of the most promising approaches to produce laminarin oligosaccharide because of the mild reaction conditions, low energy consumption, high output, and clear laminarin oligosaccharide composition. In total, typical crystal structures of laminarinases from four GH families have been identified, which will benefit our understanding of the catalytic mechanisms and targeted production of laminarin oligosaccharides.
Moreover, modifications of laminarin such as sulfation, nanoparticle modification, and branched-chain modification can enhance some specific functional activities of laminarin (Ji et al., 2013; Cui et al., 2019). For example, specific bit sulfated modification (C2 and C6) and increase the content of side chains are effective methods to enhance the antitumor activity of laminarin. However, the detailed mechanism requires further illustration. Thus, the production of laminarin with specific structural modifications and laminarin oligosaccharides with homogeneous DP and the illumination of their structure-activity relationship will become another research focus in the near future.
AcknowledgementsThis work was supported by the National Natural Science Foundation of China (No. 31922072), the National Key Research and Development Program of China (Nos. 2019YFD0901902 and 2019YFD090 1904), the Taishan Scholar Project of Shandong Province (No. tsqn2018120 20), and the Fundamental Research Funds for the Central Universities (No. 201941002).
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