Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Esche...

Wen-Sing Liang, Tristan C. Liu, Chun-Ju Chang, Chorng-Liang Pan

Journal of Food and Nutrition Research

Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Escherichia coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII

Wen-Sing Liang1, 2, Tristan C. Liu1, Chun-Ju Chang1, Chorng-Liang Pan1, 2,

1Department of Food Science, National Taiwan Ocean University, Jhongjheng District, Keelung City, Taiwan

2Taiwan Algae Research Center, National Taiwan Ocean University, Jhongjheng District, Keelung City, Taiwan

Abstract

Oligosaccharides extracted from algae exhibit many bioactivities and are used as food additives and dietary supplements. In this study, β-1,3-xylan was extracted from the green algae Caulerpa lentillifera; this compound was hydrolyzed by β-1,3-xylanase XYLII to produce mixed < 3 kDa β-1,3-xylooligosaccharide (XOSmix), which was mainly composed of β-1,3-xylose, β-1,3-xylobiose, and β-1,3-xylotriose. The antioxidant and anticoagulant activities of XOSmix were then examined. Results revealed that the 2,2-diphenyl-1-pikryl-hydrazyl scavenging activity, reducing power, and total antioxidant status of 20 mg/mL XOSmix was equivalent to those of 8.7, 115.1, and 157.3 μg/mL trolox, respectively; whereas the ferrous ion chelating activity of 20 mg/mL XOSmix was equivalent to that of 64.3 μg/mL EDTA. Regarding the anticoagulant activity, XOSmix delayed the activated partial thromboplastin time. These results suggest that XOSmix exhibits potential for application in the food industry.

Cite this article:

  • Wen-Sing Liang, Tristan C. Liu, Chun-Ju Chang, Chorng-Liang Pan. Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Escherichia coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII. Journal of Food and Nutrition Research. Vol. 3, No. 7, 2015, pp 437-444. http://pubs.sciepub.com/jfnr/3/7/5
  • Liang, Wen-Sing, et al. "Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Escherichia coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII." Journal of Food and Nutrition Research 3.7 (2015): 437-444.
  • Liang, W. , Liu, T. C. , Chang, C. , & Pan, C. (2015). Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Escherichia coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII. Journal of Food and Nutrition Research, 3(7), 437-444.
  • Liang, Wen-Sing, Tristan C. Liu, Chun-Ju Chang, and Chorng-Liang Pan. "Bioactivity of β-1,3-xylan Extracted from Caulerpa lentillifera by Using Escherichia coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII." Journal of Food and Nutrition Research 3, no. 7 (2015): 437-444.

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At a glance: Figures

1. Introduction

Poly- and oligosaccharides obtained from marine algae exhibit many bioactivities, such as anticlotting, antioxidation, antiviral, antiinflammatory, and anticancer activities [1, 2, 3, 4]; these activities are affected by the molecular weight (MW) and bonding [5]. Algal polysaccharides are easily extractable bioingredient, and they abundantly vary in molecular chemistry. In recent years, oligosaccharides degraded from algal polysaccharides have been applied in chronic disease therapy [4]; however, comprehensive studies on such algal polysaccharides are required. The bioactivity of algal oligosaccharides also must be investigated.

Xylooligosaccharide can generally be obtained from acidic and enzymatic hydrolysis; both methods degrade xylan to xylooligosaccharides or xylose, thus increasing the availability and economic value [6, 7, 8]. Acidic hydrolysis is conducted under high temperature and pressure, and the cost of product recovery and instruments is exorbitant. Moreover, this method produces byproducts during processing, thus reducing the hydrolysis product of xylan [9, 10]. The enzymatic hydrolysis method provides high specificity, requires a mild processing condition, and yields easily recoverable products. This method is applied for producing xylooligosaccharides [10] and employed in the food and cosmetics industries, medical biotechnology, agriculture, environmental protection, and sewage treatment.

β-1,3-xylan is a component of D-xylose cell wall polysaccharides composed of β-1,3 bonds [11], and it is mainly observed in macroalgae, such as Caulerpa, Bryopsis, Bangia, Porphyra, and Palmaria spp. [12, 13]. Some reports have revealed antiinflammatory, antiviral, and anticancer activities of β-1,3-xylan [13, 14, 15]; however, few studies have addressed the bioactivity of β-1,3-xylooligosaccharide generated from β-1,3-xylan through enzymatic hydrolysis. In a previous study, the β-1,3-xylanase-producing marine bacteria Pseudomonas vesicularis MA103 was isolated, and the β-1,3-xylanase-producing gene was transferred to Escherichia coli ClearColi BL21(DE3), which hydrolyzed β-1,3-xylan on insertion (data not shown). This study aimed to evaluate the availability on β-1,3-xylooligosaccharide; therefore, the hydrolysis products of β-1,3-xylooligosaccharide were collected, and their antioxidant and anticlotting activities were evaluated.

2. Materials and Methods

Materials

Activated partial thromboplastin time-soluble activator (APTT–SA) reagent kit was purchased from Helena Laboratories (Beaumont, TX, USA). Arabinose, 2,2-diphenyl-1-pikryl-hydrazyl (DPPH), ethylenediaminetetraacetic acid (EDTA), trolox, galactose, glucose, heparin, mannose, rhamnose, xylose (X1), and other chemicals were purchased from Sigma–Aldrich Inc. (St. Louis, MO, USA). C. lentillifera was kindly provided by East Green BIO Corporation (Hualian, Taiwan). Furthermore, pure β-1,4-xylobiose (X2), β-1,4-xylotriose (X3), β-1,4-xylotetraose (X4), β-1,4-xylopentaose (X5), and β-1,4-xylohexaose (X6) were purchased from Qingdao BZ Oligo Biotech Co., Ltd (Qingdao, China). Rabbit coagulase plasma and all media for bacterial cultivation were purchased from Becton, Dickinson and Company (Sparks, MA, USA).

Chemical analyses

The sulfate content was determined using the barium chloride–gelatin method with Na2SO4 as standard [16]. The total phenolic content was determined using the Folin–Ciocalteu method with gallic acid as standard [17]. The protein concentration was measured using the Lowry method with bovine serum albumin as the standards [18]. Furthermore, the recombinant β-1,3-xylanase XYLII activity was measured by determining the amount of reducing sugars released form β-1,3-xylan through the dinitrosalicylic acid method [19] with X1 as standards. The enzyme activity was assayed at 35°C for 10 min by using 0.45% β-1,3-xylan as substrate in 20 mM phosphate buffer (pH 7.5). One unit (U) of β-1,3-xylanase XYLII activity was defined as the amount of enzyme required to release 1 μmol of reducing sugars from β-1,3-xylan in 1 min.

Preparation of mixed β-1,3-xylooligosaccharide

β-1,3-xylan was extracted from C. lentillifera according to the method published by Iriki et al. [11]. β-1,3-xylanase XYLII was extracted from P. vesicularis MA103 and was transferred to E. coli ClearColi BL21(DE3) pET-39b(+)-xylII prepared in our laboratory, which was induced by 0.0125 mM isopropyl-β-d-thiogalactopyranoside at 18°C for 24 hr. After induction, the solution was centrifuged at 6000 ×g for 30 min, and the pellet was collected, ultrasonicated (200 on–off cycles of 10 s each) on ice by using a Qsonica Q125 sonicator (Newtown, CT, USA), and centrifuged at 12,000 ×g for 30 min. Moreover, the supernatant (mainly contained β-1,3-xylanase XYLII) was filtered through a 30 kDa filter (MWCO 30 kDa, Millipore, NH, USA) and washed with a phosphate buffer (20 mM, pH 7.5) three times. The residues, which had a mass higher than 30 kDa, were collected, identified as β-1,3-xylanase XYLII (activity: 10.9 U/mL, MW = 91 kDa), and stored at –20°C until for further use.

The < 3 kDa mixed β-1,3-xylooligosaccharide (XOSmix) sample was prepared using the following steps. A 450 mL solution of 20 mM phosphate buffer (pH 7.5) containing 0.5% β-1,3-xylan was hydrolyzed using 50 mL of β-1,3-xylanase XYLII (10.9 U/mL) at 35°C for 72 hr. The solution was then filtered through a 3 kDa filter (MWCO 3 kDa, Millipore, NH, USA); the filtrate was considered XOSmix, which was stored at –20°C for further use. Figure 1 shows the flow diagram corresponding to this preparation of XOSmix.

Figure 1. Schematic diagram of the preparation of XOSmix

Monosaccharide composition and degrees of polymerization assay

The monosaccharide composition was examined using a method described by Konishi et al. [20]; 25 mg of sample was mixed with 2 mL 2 M trifluoroacetic acid (TFA) and hydrolyzed at 121°C for 3 hr under vacuum. The hydrolyzed solution was vacuum dried and neutralized using double-distilled water (ddH2O) for eliminating TFA. The neutralized monosaccharide was diluted to 5 mg/mL, and the monosaccharide composition was analyzed through high performance liquid chromatography (HPLC). The HPLC system comprised a pump PU-2080 (Jasco, Tokyo, Japan), a Carbo Sep CHO-682 Pb column (7.8 × 300 mm, 7 μm; Transgenomic, Inc., Omaha, NE), and an ERC-7515 A RI detector (ERC Inc., Saitama, Japan). The mobile phase was ddH2O with a constant flow rate of 0.4 mL/min at 80°C. Six monosaccharides (glucose, X1, rhamnose, galactose, arabinose, and mannose) were used as the standards.

The degree of polymerization (DP) was analyzed. XOSmix was hydrolyzed using the aforementioned steps, and the products were analyzed though HPLC on the same column. The mobile phase was ddH2O with a constant flow rate of 0.4 mL/min at 90°C, and X1–X6 were used as the standards.

Fourier transform infrared and electrospray ionization mass spectrometry

The chemical groups of all compounds were analyzed using a Fourier transform infrared spectrometer (FTIR; FTS 155 Win-ir, Bio-Rad, CA, USA). Infrared spectra of potassium bromide (KBr) and sample mixtures were obtained over the frequency range of 400 to 4,000 cm1 at a resolution of 8 cm1. The sample was thoroughly mixed with KBr (100:1, v:v), dried, ground, and pressed to obtain a sample disk [21].

The XOSmix fraction was analyzed through electrospray ionization mass spectrometry (ESI-MS) using ESI-Orbitrap MS (Exactive, Thermo Scientific, Bremen, Germany) at the Instrumentation Center of National Taiwan University (Taipei, Taiwan).

Antioxidation methods

Total antioxidant status assay

The total antioxidant status (TAS) of each extract was tested using TAS kit (Randox Labs, Crumlin, UK) according to the manufacturer’s protocol. TAS of varying concentrations of XOSmix (1, 3, 5, 10, and 20 mg/mL) were expressed as μg/mL of trolox equivalent.

α,α-diphenyl-β-picrythydrazyl assay

The free radical scavenging activity of each extract was tested using DPPH as described by Shimada et al. [22]. Furthermore, 200 μL of varying concentrations of XOSmix (1, 3, 5, 10, and 20 mg/mL) was mixed with 200 μL of 0.1 mM DPPH, reacted at room temperature for 30 minute, and then measured at 517 nm. Trolox was used as the standard. The percentage of DPPH scavenging activity (%) was calculated as follows:

DPPH scavenging activity (%) = [(A0 − A1)/(A0 − A2)] × 100%, where A0 and A1 are the absorbance of the control and sample, respectively, and A2 is the 100% DPPH scavenging absorbance.

The trolox equivalent of XOSmix was calculated using the following equation:

Trolox equivalent (μg/mL) = (A1 − 0.003)/−0.00217, where R2 = 0.9942.

Chelating effects on ferrous ions

The ferrous ion (Fe2+) chelating activity for each extract was calculated a modification of a method published by Dinis et al. [23]. Furthermore, 250 μL of varying concentrations of XOSmix (1, 3, 5, 10, and 20 mg/mL) was mixed with 925 μL of methanol and 25μL of FeCl2·4H2O (2 mM) for 30 s. After the reaction, 50 μL of ferrozine (5 mM) was added and reacted for 10 min; the absorbance was tested at 562 nm. EDTA was used as the standard, and the percentage of the chelating effect (%) was calculated as follows.

Chelating effect (%) = [(A0 − A1)/(A0 − A2)] × 100%, where A0 and A1 are the absorbance of the control and sample, respectively, and A2 is the 100% Fe2+ chelating absorbance.

The EDTA equivalent of XOSmix was calculated using the following equation:

EDTA equivalent (µg/mL) = (A1 − 0.0059)/−0.0085, where R2 = 0.9991.

Reducing power

The reducing power of each extract was determined according to the method described by Wang et al. [24]. Moreover, 250 μL of varying concentrations of XOSmix (1, 3, 5, 10, and 20 mg/mL) was mixed with 250 μL of 0.2 M phosphate buffer (pH 6.6) and 250 μL of 1% potassium ferricyanide [K3Fe(CN)6] and reacted at 50°C for 20 min. After the reaction, the solution was cooled to room temperature, and 1 mL of 10% trichloroacetic acid and 100 L of 0.1% FeCl3·6H2O were added. After reaction for 10 min in the dark, the absorbance of the test sample was measured at 700 nm. Trolox was used as the standard to evaluate the equivalent of each extract, which was calculated using the following equation:

Trolox equivalent (μg/mL) = (OD700nm + 0.0014)/0.0067, where R2 = 0.998.

Anticoagulant activity assay

The anticoagulant activity was calculated as described by Matsubara et al. [25]. Rabbit plasma (90 μL) was mixed with varying concentrations of XOSmix (1, 3, 5, 10, and 20 mg/mL) and was reacted at 37°C for 1 min. The solution was then mixed with 100 μL of APTT (preheated at 37°C for 10 min) for 5 min; 100 μL of CaCl2 (0.025 M) was added, and the absorbance was tested at 660 nm in different clotting time assays. Heparin and ddH2O were used as positive and negative control, respectively. The heparin equivalent of XOSmix was calculated using the following equation:

Heparin equivalent (μg/mL) = [clotting time (s) − 14.516)/3.3871], where R2 = 0.9876.

Statistical analyses

Data were presented as the mean ± standard deviation. The differences between the mean values were analyzed using the one-way analysis of variance followed by the Duncan test at p = 0.05. Statistical analysis was performed using the SPSS 12.0 software (SPSS Inc., Chicago, IL, USA).

3. Results and Discussion

XOSmix characterization

β-1,3-xylan is mainly extracted using alkali treatments [11, 12]. In this study, β-1,3-xylan was extracted from C. lentillifera by using alkali, and the chemical composition of XOSmix was analyzed. Table 1 presents the obtained yield of β-1,3-xylan (24.93%) and XOSmix (46.07%). The sulfate content of β-1,3-xylan and XOSmix were 0.69% and 0.74%, respectively. Jiao et al. [1] indicated that algal polysaccharide generally contain a sulfate group. In accordance, in our study, β-1,3-xylan extracted from C. lentillifera contained a sulfate group. After enzymatic hydrolysis, the final product XOSmix retained the sulfate group, and the total phenolic content was not detected in this study. The protein content of XOSmix was 2.43%; however, phenol was not detected in β-1,3-xylan, possibly because of protein degradation during enzymatic hydrolysis.

The monosaccharide composition indicated that β-1,3-xylan and XOSmix were mainly composed of glucose and X1. The glucose content of β-1,3-xylan and XOSmix were 2.58% and 3.45%, respectively, whereas the X1 content of β-1,3-xylan and XOSmix were 97.42% and 96.55%, respectively (Table 1). Previous studies have revealed that the polysaccharide extracted from Caulerpa spp. not only contained xylose but also glucose and galactose [14, 20, 26]. These results suggest that the chemical composition of algal polysaccharides varies depending on the species, region, and season as well as environmental factors [27]. Extracts obtained from the same algal species by using the same procedures exhibited difference chemical compositions depending on the region [20].

Structural properties of XOSmix

Figure 2 shows the DP of XOSmix determined using HPLC; three major peaks were observed in the spectrum. In contrast to the components of β-1,4-xylooligosaccharide (X1−X6), the main oligomer products in XOSmix were identified as xylose, xylobiose, and xylotriose, with some xylotetraose. Yamaura et al. [28] analyzed β-1,3-xylan hydrolyzed by the marine bacteria Pseudomonas sp. PT-5, which produced β-1,3-xylanase, and indicated that xylose and xylobiose were produced after 6 hr of hydrolysis.

Figure 2. Analysis of mixed < 3 kDa β-1,3-xylooligosaccharide through high-performance liquid chromatography
Figure 3. Fourier transform infrared spectroscopy of mixed < 3 kDa β-1,3-xylooligosaccharide

β-1,3-Xylan hydrolyzed by β-1,3-xylanase purified from Vibrio sp. XY-214 yielded xylose, xylobiose, and xylotriose [29]. In this study, β-1,3-xylanase XYLII extracted from P. vesicularis MA103-transformed E. coli ClearColi BL21(DE3) hydrolyzed β-1,3-xylan and produced β-1,3-xylooligosaccharid. XOSmix was then analyzed through FTIR, and the spectrum is shown in Figure 3. The major peaks observed in the spectrum were located in 899, 1050, 1247, 1636, 2903, and 3369 cm−1. Furthermore, the absorbance of 3600−3000 cm−1 represented the O–H group, whereas the absorbance of approximately 1166−1000 cm−1 represented the C–O, C–C or C–OH group in hemicelluloses [30]. Samanta et al. [31] used FTIR to analyze alkali-extracted xylan from corncob and reported a spectrum similar to that observed in the present study, suggesting that XOSmix contains the xylan group. The FTIR spectrum of XOSmix also revealed peaks at 2903 cm−1 and 1636 cm−1, indicating a C–H group, and the peak at 899 cm−1 represented the β-glycosidic bonds between molecules. These results are in accordance with those previous studies [32, 33]. Jayapal et al. [30] and Ayoub et al. [32] indicated that a peak at 1642 cm−1 represents water molecules in the xylan structure. Gómez-Ordóñez and Rupérez [34] indicated that apeak at 1220–1260 cm−1 represents the S=O group. In this study, XOSmix exhibited similar features in the FTIR spectrum.

XOSmix was purified through HPLC, and the X1–X3 fractions were collected. These fractions were analyzed in the positive ion mode of ESI-MS, and the DP and MW of each fraction were detected (Figure 4). In the ESI-MS spectrum, the m/z ratios of X3 (Figure 4A), X2 (Figure 4B), and X1 (Figure 4C) were 173.0, 305.1, and 437.1, respectively. These results are in concordance with those of previous studies [26, 35], indicating that XOSmix contains β-1,3-xylose, β-1,3-xylobiose, and β-1,3-xylotriose.

Figure 4. Electrospray ionization mass spectrometry spectrum of mixed < 3 kDa β-1,3-xylooligosaccharide

Antioxidant assay

The total antioxidant status assay is used for testing the ABTS radical cation (ABTS+) scavenging activities. As can be seen in Figure 5A, the total antioxidant status was 0, 114.4, 166.9, 146.4, and 157.3 μg/mL for 1, 3, 5, 10, and 20 mg/mL sample concentrations, respectively. The 5 mg/mL sample concentrations exhibited the highest TAS activity. The ABTS scavenging activities of 20 mg/mL XOSmix was equivalent to that of 157.3 μg/mL trolox.

The DPPH scavenging assay is used for testing the antioxidant and scavenging activities of peroxy radicals [22]. Figure 5B presents the healthy benefit potential of XOSmix in a concentration-dependen manner. The scavenging activity was 1.4%, 56.3%, 76.7%, 79.7%, and 79.5% for 1, 3, 5, 10, and 20 mg/mL sample concentrations, respectively. These results were equivalent to those of 8.7 μg/mL trolox when the sample concentration was 20 mg/mL.

Figure 5. Antioxidant activity of varying concentrations of mixed < 3 kDa β-1,3-xylooligosaccharide

Many metal ions accelerate lipid oxidation and act as pro-oxidant. Thus, the chelating activity affects the antioxidation activity of XOSmix. Figure 5C shows the Fe2+ chelating activity of XOSmix, which increased with increasing sample concentration and was 63.5%, 67.4%, 73.6%, and 88.3% for 3, 5, 10, and 20 mg/mL sample concentrations, respectively. Chelating activity was not detected when the sample concentration was 1 mg/mL; however, optimal activity was observed when the sample concentration was 20 mg/mL and was equivalent to that of 64.3 μg/mL EDTA.

Figure 5D presents the reducing power results of XOSmix. In this experiment, the sample exhibited antioxidant activity and reduced K3Fe(CN)6 to potassium hexacyanoferrate [K4Fe(CN)6]; K4Fe(CN)6 interacted with ferric ions to generate Prussian blue, which showed strong absorbance at 700 nm [36]. Furthermore, XOSmix revealed exhibited activity at all concentrations; absorbance was observed at 0.01, 0.15, 0.24, 0.45, and 0.77 nm for 1, 3, 5, 10, and 20 mg/mL sample concentrations, respectively. The reducing power of 20 mg/mL XOSmix was equivalent to that of 115.1 μg/mL trolox.

In previous study, oligosaccharides contained phenol compounds, which represent the DPPH scavenging activity [37]. In this study, soluble polyphenol was not detected in XOSmix; however, effective DPPH scavenging activity was still observed. O’Sullivan et al. [38] used methanol for extracting five types of brown algae and examined their DPPH scavenging activity; their results indicated no positive correlation between DPPH scavenging activity and polyphenol concentrations. Previous studies have indicated that -OH, -COOH and some spatial structure in carbohydrates enhance the antioxidant activity [39, 40][39, 40]; thus, algal polyphenol is not the only substance representing the DPPH scavenging activity. Some researchers exacted polysaccharides from Enteromorpha prolifera and indicated that the Fe2+ chelating and reducing activity were revesed MWs [41]. As compared with high-MW oligosaccharide, low-MW oligosaccharides have superior activity in chelating transition ion metals, such as cuprous ions or Fe2+, in spatial structures [37]. In addition, Wang et al. [42] indicated that low-MW sulfated polysaccharides more efficiently enter cells and contribute H+ ions.

Anticoagulant activity

Previous studies have indicated that the anticoagulant activity of algal extract is attributable to sulfite ion-containing polysaccharides. In addition to a negative charge, the anticoagulant activity is related to structural specificities, such as the sulfate group position, the monosaccharide from, and glycosidic bonding [43, 44]. Table 1 and Figure 3 illustrate that XOSmix contained sulfate groups; therefore, we further tested the activated partial thromboplastin time by using rabbit plasma against varying XOSmix concentrations.

Table 1. Chemical composition analysis of β-1,3-xylan and mixed < 3 kDa β-1,3-xylooligosaccharide

Table 2 shows prolonged activated partial thromboplastin times of 27, 30, 26, and 25 s for 3, 5, 10, and 20 mg/mL sample concentrations, respectively. The heparin equivalents were 3.8, 4.2, 3.4, and 3.2 μg/mL for 3, 5, 10, and 20 mg/mL XOSmix concentrations, respectively. By contrast, varying the XOSmix concentration did not significantly affect the prothrombin and thrombin times (data not shown). In general, many factors affect the coagulating mechanism. The sulfate group was a factor, and the underlying mechanism was similar to that of heparin, which stimulated the antithrombin activity to inhibit the inner coagulating factors IXa, XIa, and XIIa, thus delaying thrombosis [45].

Table 2. Anticoagulant activity of varying concentrations of mixed < 3 kDa β-1,3-xylooligosaccharide

4. Conclusion

In this study, β-1,3-xylan was extracted from C. lentillifera through alkali extraction; the compound was then hydrolyzed by E. coli ClearColi BL21(DE3)-β-1,3-xylanase XYLII to obtain low-MW XOSmix. XOSmix was composed of β-1,3-xylose, β-1,3-xylobiose, and β-1,3-xylotriose and exhibited antioxidant and anticoagulant activities. This study provides an efficient method for producing XOSmix with a low DP, and XOSmix can be applied in producing dietary supplements and antioxidant and functional nutrient additives.

Acknowledgment

The authors are grateful for the financial support from Ministry of Science and Technology (102-2313-B-019-012-MY3) and Ministry of Economic Affairs (102-EC-17-A-17-S1-210), Taiwan, R.O.C.

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