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ISSN : 1598-5504(Print)
ISSN : 2383-8272(Online)
Journal of Agriculture & Life Science Vol.56 No.2 pp.17-24
DOI : https://doi.org/10.14397/jals.2022.56.2.17

Zanthoxylum coreanum Essential Oil Inhibits DNP-BSA-Induced β-hexosaminidase Release and Overproduction of Intracellular Active Oxygen and Nitric Oxide

Si-Young Ha1, Ji-Young Jung2, Jae-Kyung Yang3*
1Ph.D candidate, Division of Environmental Forest Science/Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, 52828, Republic of Korea
2Ph.D research professor, Division of Environmental Forest Science/Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, 52828, Republic of Korea
3Ph.D professor, Division of Environmental Forest Science/Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, 52828, Republic of Korea
* Corresponding author: Jae-Kyung Yang (Tel.) +82-55-772-1862 (E-mail) jkyang68@gmail.com
September 8, 2021 April 14, 2022

Abstract


Plant-derived compounds have been reported to possess anti-inflammatory abilities contained inhibited β-hexosaminidase, ROS and NO release. Essential oils are natural volatile complex compounds that are characterized by a strong scent and produced by aromatic plants as various plant-derived compounds. The essential oil extracted from Zanthoxylum coreanum Nakai (Z. coreanum) has various functional properties; however, little information is available regarding its anti-allergic inflammatory. A total of 17 compounds were detected in Z. coreanum oil, and the main component was estragole (50.86%). The tested Z. coreanum oil and estragole statistically inhibited the release of β-hexosaminidase induced by antigen stimulation in RBL-2H3 cells. This Z. coreanum oil and estragole may stimulate the secretion of active oxygen (ROS) or nitric oxide (NO) which are considered to involved in anti-inflammatory events. Moreover, it is suggested that Z. coreanum oil and estragole may negatively control the production of SNARE proteins (VAMP7) at the tran-scriptional and translational levels in common. These results demonstrate that Z. coreanum oil and its major component, estragole, possess potent anti-inflammatory abilities that are coupled with antioxidant properties.



초록


    Introduction

    Inflammation is a complex mechanism that involves the activation and deactivation of immune cells. This can result in cellular and tissue damages that subsequently cause chronic diseases (Alessandri et al., 2013).

    Plant-derived compounds, including eugenol (Hancı et al., 2016), and the recently characterized sub-stance of camphor (Santos et al., 2021) reportedly exhibit anti-inflammatory properties and inhibit β-hexosaminidase, reactive oxygen species (ROS), and nitric oxide (NO) release.

    Essential oils are natural volatile complex compounds characterized by a strong scent and produced by aromatic plants (Bakkali et al., 2008). Essential oils have largely been used owing to their well-known natural antitumor, anti-inflammatory, antioxidant, and antibacterial properties (Woollard et al., 2007). Furthermore, studies on the anti-inflammatory activity of essential oils from various plants (lemon, eucalyptus, marjoram, juniper, thyme, lavender, mentha, rosemary, geranium, pine, and salvia), monoterpenes 1,8-cineole, menthol, citral, α-pinene, limonene, linalool, thymol, camphor, and borneol showed that pine and lemon oils have the strong-est anti-inflammatory activity, while α-pinene has the strongest activity among the mono-terpenes (Silveira e Sá et al., 2013). Similarly, Standen et al. (2006) performed in vitro experiments using a selection of essential oils obtained from Matricaria recutita, and Thymus vulgaris and found that the monoterpenes α-pinene, (S)-(−)-limonene, linalool, geraniol, thymol, 1,8-cineole, linalyl acetate, and (+)-terpinen-4-ol, which have potential anti-inflammatory activity, inhibit β-hexosaminidase release and significantly inhibit ROS and NO release.

    Zanthoxylum coreanum Nakai, also called the wang-cho-pi tree, is a Korean lime tree, a rare shrub that grows only in Korea and China. In Korea, the essential oil of Z. coreanum has been used as a crude medicine for the treatment of ozena, rheumatoid arthritis, nasal sinusitis, and sore throat. Moreover, Z. coreanum has shown to have antiviral activity against picornaviruses (Choi et al., 2016). However, studies on the anti-allergic inflammatory effect of Z. coreanum are limited.

    Therefore, this study sought to investigate the chemical composition of Z. coreanum using gas chromatography-mass spectrometry (GC-MS) and examine its anti-allergic inflammatory effect. In particular, we analyzed the effects of Z. coreanum on cell degranulation, inhibition of β-hexosaminidase release from RBL-2H3 cells, production of inflammatory cytokines such as ROS and NO, and SNAP23 expression levels in LPS-induced RAW264.7 macrophages.

    Materials and Methods

    1. Essential oils

    Z. coreanum fruit was purchased from Hwacheonmin Sancho, Inc. (Hwacheon-gun, Gangwon Province, South Korea). The extraction was performed as described previously, with slight modifications (Lee et al., 2001). Briefly, Z. coreanum fruit was placed in a vessel and extracted by distillation for 4 h. The vapors were cooled by a closed cooling system, and the resulting liquid was collected in a container. The oil was at the top of the distilled liquid, whereas the water settled into the lower phase of the liquid; thus, the essential oils were obtained by simply removing the upper phase of the liquid, which contained the desired oils.

    2. Chemicals

    Dulbecco’s modified Eagle’s medium (DMEM), minimum essential medium, fetal bovine serum (FBS), L-glutamine, and penicillin-streptomycin were purchased from Invitrogen Life Technologies (Carlsbad, CA, USA). Quercetin, 1-Chloro-2,4-dinitrobenzene (DNCB), dimethyl sulfoxide (DMSO), and dexamethasone were obtained from Sig-ma-Aldrich (St. Louis, MO, USA). Albumin from bovine serum and DNP-BSA were pur-chased from Invitrogen by Thermo Fisher Scientific (Eugene, OR, USA). β-actin, SNAP23, Syntaxin4, VAMP7, and VAMP8 were procured from R&D Systems Inc. (Minneapolis, MN, USA).

    3. GC-MS analysis

    Z. coreanum oil was analyzed by GC-MS (Clarus 600 GC-MS, PerkinElmer, USA). The analysis column was PerkinElmer Elite-5ms (30 mm × 0.3 mm × 0.25 μm), helium gas was used as the mobile phase, and the movement speed was 1.0 mL/min. The oven temperature was increased from 40 °C to 100 °C at a rate of 10 °C/min and then maintained for 1 min. Then, the temperature was raised to 230 °C at a rate of °C/min and then maintained for 5 min. The temperature of the injector was set to 200 °C, and the temperature of the detector was set to 250 °C. The 2005 version of the National Institute of Standards and Technology (NIST) MS spectral database was used for a mass spectrum database search and to compare the MS fragmentation patterns with the fragmentation patterns of pure components.

    4. Cell cultures

    The rat cell line RBL-2H3 was obtained from the Korean Cell Line Bank (Seoul, South Korea). RBL-2H3 cells were cultured in DMEM (Gibco, Burlington, Ontario, Canada) supplemented with 10% FBS (Gibco, Rockville, MD, USA) and 1% penicillin-streptomycin in an atmosphere of 5% CO2 in a humidified 37 °C incubator. RAW264.7 macrophages were purchased from American Type Culture Collection (Manassas, VA, USA) and cultured in DMEM containing 10% FBS and 1% penicillin- streptomycin. The cells were maintained in a humidified 5% CO2 incubator at 37 °C and sub-cultured every 3–4 days to maintain logarithmic growth.

    5. Cell viability

    Cell viability was assessed using the MTT colorimetric assay. RBL-2H3 cells were treated with different concentrations of Z. coreanum oil (25–100 ppm) or estragole (25–100 ppm) for 24 h followed by MTT (5 mg/mL) in serum-free DMEM. After a 3 h incubation at 37 °C and 5% CO2, 100 μL of 100% DMSO was added to dissolve an insoluble purple formazan product into a colored solution. Absorbance was measured at 540 nm using an absorbance microplate reader (SpectraMax 190, Molecular Devices LLC, CA, USA).

    6. The assay of β-hexosaminidase

    Briefly, RBL-2H3 cells were seeded into 24-well plates at a density of 5 × 105 cells/well and cultured overnight. The medium was changed and the cells were treated with 50 ng/mL of DNP-specific IgE. The cells were sensitized by incubating for 4 h at 37 °C in 5% CO2. Then, the cells were washed twice with 500 μL of piperazine-N, N-bis-(2-ethanesulfonic acid) (PIPES) buffer and incubated in PIPES buffer containing glucose, CaCl2, and 0.1% BSA for an additional 10 min at 37 °C. Then, the cells were treated with Z. coreanum oil (25–100 ppm), estragole (25–100 ppm) or the positive control quercetin (20 μM), challenged with test materials for 20 min at 37 °C, and activated by treating with 25 ng/mL of the antigen DNP-BSA for 30 min at 37 °C. The supernatant was transferred to a 96-well plate and incubated with a substrate (1 mM p-nitrophenyl- N-acetyl-β-D-glucosaminide) for 1 h at 37 °C. The reaction was stopped by adding 0.1 M Na2CO3/NaHCO2 or 2 M glycine. Absorbance was measured at 405 nm using a microplate reader (SpectraMax 190, Molecular Devices LLC).

    7. The assay of ROS

    Intracellular ROS levels were determined using DCFH-DA as described previously (Onodera et al., 2015). RAW264.7 cells were cultured in 96-well plates (5×104 cells/well). After 24 h, the cells were treated with different concentrations of Z. coreanum oil (25–100 ppm), estragole (25–100 ppm) or the positive control Bay 11-7082 (20 μM) for 72 h. Then, DCFH-DA was added to the cells and incubated for 30 min. The intensities were read using a microplate reader (SpectraMax 190, Molecular Devices LLC) at an excitation wavelength of 504 nm and an emission wavelength of 524 nm.

    8. The assay of NO

    The level of NO was determined using the Griess reaction, which indirectly measures NO levels via the accumulation of sodium nitrite. RAW264.7 cells were seeded in 96-well plates and treated with different concentrations of Z. coreanum oil (25–100 ppm), estragole (25–100 ppm) or the positive control Bay 11-7082 (20 μM) for 72 h. Then, the supernatant was isolated, mixed with the Griess reagent at room temperature for 5 min, and the absorbance was read using a microplate reader (SpectraMax 190, Molecular Devices LLC) (Davis et al., 2005).

    9. Phosphorylation assay of SNARE proteins

    Enrichment and separation of phosphorylated SNARE proteins from cell lysates were conducted using a Phosphoprotein Purification Kit (Qiagen Hilden, Germany) according to the manufacturer's instructions (Hiramatsu et al., 2010). RBL-2H3 cells were pretreated with Z. coreanum oil or estragole of 100 ppm for 8 h at 37 °C in a CO2 incubator. Then, 1 × 105 RBL-2H3 cells were washed with HEPES buffer and stimulated for 15 min at 37 °C. Western blotting was performed using primary antibodies against β-actin (1:1000), SNAP23 (1:1000), Syntaxin4 (1:2000), VAMP7 (1:1000), and VAMP8 (1:1000). Immunore-activity was detected using anti-rabbit IgG conjugated with horseradish peroxidase (1:1000, Santa Cruz Biotechnology). Blots were visualized with Super Signal West Pico Chemiluminescent Substrate (Pierce, Rockford, IL, USA) using a LAS-3000 mini.

    10. Statistical analyses

    All experiments were repeated at least three times, and data were obtained at least in triplicate. The statistical significance of the differences between the control and experimental results was estimated by t-test using R (version 2.6.1).

    Results and Discussion

    1. Identification and quantification of Z. coreanum oil components

    We examined the chemical composition of Z. coreanum oil using GC-MS (Table 1). In total, 17 components were detected in Z. coreanum oil. Of note, Z. coreanum oil was of South Korean origin. The origin is important because the chemical composition differs depending on its origin. GC-MS analysis revealed a composition that was not significantly different from those reported previously (Kim et al., 2018). The main components were estragole (50.86%), camphor (30.68%), and R(+)-limonene (3.75%), along with other minor components such as elemol (1.89%), linalool (1.10%), and cyclotetrasiloxane (0.95%). In addition, limonene, camphene, and estragole were also detected; these components are found in many Zanthoxylum species (Lee, 2016).

    2. Effects of Z. coreanum oil and estragole on cell viability

    The effect of Z. coreanum oil and estragole on RBL-2H3 cell viability was evaluated using 3-(4,5-dimethyl-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay to confirm whether its anti-allergic inflammatory effects were not due to cell death. Treatment with Z. coreanum oil and estragole for 24 h at concentrations of 25–100 ppm showed no significant cytotoxic effects (Fig. 1).

    3. Effects of Z. coreanum oil and estragole on the hexosaminidase activity in dinitrophenylated bovine serum albumin (DNP-BSA)-stimulated RBL-2H3 cells

    Histamine, which is released from mast cells stimulated by an antigen or a degranulation inducer, is a common degranulation marker for in vitro experiments on immediate allergic reactions. β-hexosaminidase is also stored in the secretory granules of mast cells and is released concomitantly with histamine upon immunological activation of mast cells (Matsuda et al., 2016). Therefore, β-hexosaminidase is also considered a degranulation marker of mast cells. Here, we examined the effects of Z. coreanum oil constituents on the DNP-BSA-induced release of β-hexosaminidase from RBL-2H3 cells. RBL-2H3 cells were treated with Z. coreanum oil and estragole, together with quercetin as a positive control, to evaluate their inhibitory effects on the release of β-hexosaminidase. All the test samples significantly inhibited the release of β -hexosaminidase from antigen-stimulated RBL-2H3 cells (Fig. 2). Among them, Z. coreanum oil showed remarkable inhibitory effects on β-hexosaminidase activity at concentrations ranging between 50 and 100 ppm. Ergosterol showed a trend similar to that of Z. coreanum oil. The capacity of both Z. coreanum oil and estragole to suppress the β-hexosaminidase enzyme release from RBL-2H3 mast cells is demonstrated in the dose-response curves (Fig. 2A, B). Z. coreanum oil and estragole significantly reduced the release of the enzyme at all concentrations tested when compared with cells treated with DNP-IgE and DNP-BSA. Both Z. coreanum oil and estragole at 100 ppm showed the greatest inhibitory effects (p < 0.001). Cell viability measured by MTT assay revealed that none of the tested components had any significant cytotoxicity to RBL-2H3 cells at concentrations that inhibited the release of β-hexosaminidase (Fig. 1).

    4. Effects of Z. coreanum oil and estragole on ROS level

    Overproduction of free radicals during inflammatory proc-esses is involved in signal transduction and NF-κB activation (Akanda & Park, 2017). The effects of Z. coreanum oil and estragole on in-tracellular free radical production in LPS-stimulated RAW 264.7 cells was analyzed. The level of ROS was similar to that of the positive control Bay 11–7082 (Fig. 3). LPS stimulation increased ROS production, which was significantly decreased upon treatment with different concentrations of Z. coreanum oil and estragole (25–100 ppm). These results suggest that Z. coreanum oil and estragole, which are considered to be involved in anti-inflammatory events, may stimulate the secretion of ROS.

    5. Z. coreanum oil and estragole suppress LPS-stimulated NO production

    As NO is known to be a representative toxic and pro-inflammatory mediator in several acute and chronic inflammatory diseases as well as in normal defense reactions (Naik & Wala, 2013), we next examined whether Z. coreanum oil or estragole modulates NO production in LPS-activated macrophages. Z. coreanum oil dose-dependently inhibited NO production compared to the control in RAW264.7 macrophages (Fig. 4A). In particular, the inhibitory effect of Z. coreanum oil appeared to be strongest at 50 ppm and 100 ppm. Similarly, estragole dose-dependently inhibited NO production compared to the control (Fig. 4B). Collectively, the suppressive effect of Z. coreanum oil and estragole on NO production is similar to that of Bay 11-7082, and do not display strong cytotoxicity (Fig. 1).

    6. Z. coreanum oil and estragole differentially regulate LPS-induced expression of soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins

    SNARE proteins, such as SNAP23, Syntaxin4, VAMP7, and VAMP8, are involved in a multitude of biological activities that are linked to normal defense responses and the immunopathology of acute or chronic inflammatory diseases (Pham, 2008). Therefore, we examined whether Z. coreanum oil and estragole are capable of effectively regulating SNARE proteins in RAW264.7 cells. As shown in Fig. 5A, 100 ppm Z. coreanum oil blocked the production of VAMP7 and VAMP8 in RAW264.7 cells. This suppressive effect was not observed at the transcriptional level as indicated by a weak inhibition of VAMP7 and VAMP8 mRNAs (Fig. 5A), suggesting a more favorable inhibition at the translational level. The effect of 100 ppm estragole on the mRNA expression of other SNARE proteins was extensively examined. As shown in Fig. 5B, the expression of VAMP7 was strongly inhibited by estragole. Therefore, it is suggested that Z. coreanum oil and estragole may negatively control the production of SNARE proteins, particularly VAMP7, at the transcriptional and translational levels.

    Allergic diseases are inflammatory disorders which have become a worldwide clinical health problem. With the allergy patients increasing annually due to various factors, approximately 10 - 20% of the world population is affected by allergies (Bousquet et al., 2005;Cecchi et al., 2018;Zhang and Zhang, 2019). Mast cells express a high-affinity IgE receptor on membranes, which is important to the pro-inflammatory allergic response (Pastwińska et al., 2017;Utomo et al., 2018;Martínez et al., 2019). Also, a combined treatment with DNP-BSA has been used widely for mast cell activation, because they are known to induce the generation of inflammatory cytokines (Majewska-Szczepanik et al., 2012;Tang et al., 2015;Jiang et al., 2016). β-hexosaminidase, a granuleas-sociated exo-glycosidase, is stored in secretory granules of mast cells, and has been used to monitor mast cell degranulation just as histamine has been used (Mizuno et al., 2007;Ringvall et al., 2008). During the pathogenesis of allergic disease, SNARE protein is also crucial for the induction of IgE synthesis and mast cell development (Suzuki & Verma, 2008;Yang et al., 2013). Lipopolysaccharide (LPS), a principle component of the outer membrane of Gram-negative bacteria, could induce the macro-phage cells’ inflammation reaction, and stimulate the production of inflammatory mediators such as ROS and NO (Lau et al., 2007;Lee & Yang, 2012). This could be used to assess the anti-inflammatory activities of samples. The genus Zanthoxylum is a well-known medicinal plant. It has been well documented that oils from Zanthoxylum species have many medicinal efficacies, including anti-inflammatory and analgesic effects (Fu et al., 2020). These pharmacological effects may have been derived from the components of the oil. Our results verified that Z. coreanum oil and estragole significantly suppressed the production of pro-inflammatory markers β-hexosaminidase induced by DNP-BSA from RBL-2H3 cells. From our result, we tentatively conclude that Z. coreanum oil and estragole could inhibition inflammation from harmful factors like VAMP7. So, we considered that the estragole was major biologically active compounds in Z. coreanum oil. Existing research on anti-inflammation of Z. coreanum oil is insufficient, so it can be used as important basic data for future research on main ingredients showing anti-inflammation efficacy and mechanism of action.

    Acknowledgements

    This study was carried out with the support of ´R&D Program for Forest Science Technology (Project No. "2020186D10-2122- AA02)´ provided by Korea Forest Service(Korea Forestry Promotion Institute).

    Figure

    JALS-56-2-17_F1.gif

    The effects of Z. coreanum oil (A) and estragole (B) on the cell viability of RBL-2H3 mast cell, respectively. The data are represented as the mean ± S.D. of three independent experiments. * indicates a significant difference (p<0.05) compared with the untreated group.

    JALS-56-2-17_F2.gif

    The effects of Z. coreanum oil (A) and estragole (B) on β-hexosaminidase induced by DNP-BSA from RBL-2H3 cells, respectively. The data are represented as the mean ± S.D. of three independent experiments. +++ indicates a significant difference (p<0.001) compared with the DNP-IgE; ** indicates a significant difference (p<0.01) compared with the DNP-BSA; *** indicates a significant difference (p<0.001) compared with the DNP-BSA.

    JALS-56-2-17_F3.gif

    The effects of Z. coreanum oil (A) and estragole (B) on the ROS of RAW 264.7 cell, respectively. The data are represented as the mean ± S.D. of three independent experiments. +++ indicates a significant difference (p<0.001) compared with the untreated group; * indicates a significant difference (p<0.05) compared with the LPS; ** indicates a significant difference (p<0.01) compared with the LPS; *** indicates a significant difference (p<0.001) compared with the LPS.

    JALS-56-2-17_F4.gif

    The effects of Z. coreanum oil (A) and estragole (B) on the NO of RAW 264.7 cell, respectively. The data are represented as the mean ± S.D. of three independent experiments. +++ indicates a significant difference (p<0.001) compared with the untreated group; * indicates a significant difference (p<0.05) compared with the LPS; ** indicates a significant difference (p<0.01) compared with the LPS; *** indicates a significant difference (p<0.001) compared with the LPS.

    JALS-56-2-17_F5.gif

    The effects of Z. coreanum oil (A) and estragole (B) on the SNARE protein of RBL-2H3 mast cells, respectively. *** indicates a significant difference (p<0.001) compared with the control.

    Table

    The gas chromatography-mass spectrometry (GC/MS) analysis of Z. coreanum oil

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