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Anti-Inflammatory Effects of Stearidonic Acid Mediated By

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Anti-Inflammatory Effects of Stearidonic Acid Mediated By Lipids (2017) 52:781–787 DOI 10.1007/s11745-017-4278-6 COMMUNICATION Anti‑Infammatory Efects of Stearidonic Acid Mediated by Suppression of NF‑κB and MAP‑Kinase Pathways in Macrophages Jeehye Sung1 · Heemang Jeon2 · In‑Hwan Kim3 · Heon Sang Jeong1 · Junsoo Lee1 Received: 21 November 2016 / Accepted: 13 July 2017 / Published online: 25 July 2017 © AOCS 2017 Abstract Stearidonic acid (SDA, 18:4n-3) is an omega-3 Abbreviations polyunsaturated fatty acid present in oils derived from ALA α-Linolenic acid plants of the Boraginaceae family. In this study, we deter- BSA Bovine serum albumin mined the anti-infammatory efects of SDA isolated from DHA Docosahexaenoic acid echium oil on lipopolysaccharide (LPS)-induced infamma- DMEM Dulbecco’s modifed Eagle’s medium tory responses in RAW 264.7 macrophages. SDA signif- FBS Foetal bovine serum cantly downregulated the levels of the inducible nitric oxide EPA Eicosapentaenoic acid synthase (iNOS) protein, thereby suppressing the produc- ERK Extracellular signal regulated kinase tion of nitric oxide (NO) in LPS-stimulated RAW 264.7 JNK c-jun N terminal kinase cells. In addition, SDA inhibited the nuclear translocation iNOS Inducible nitric oxide synthase and promoter activity of nuclear factor κB (NFκB) and IκB Inhibitor of κB the phosphorylation of mitogen-activated protein kinases LDH Lactate dehydrogenase (MAPK) such as extracellular signal regulated kinase 1/2, LPS Lipopolysaccharide c-jun N terminal kinase, and p38 in LPS-stimulated RAW MAPK Mitogen-activated protein kinases 264.7 cells. Our results showed that SDA exerted anti- MTT 3-(4,5-Dimethyl thiazol infammatory efects by suppressing iNOS-mediated NO 2-yl)-2,5-diphenyltetrazolium production via inactivation of NFκB and MAPK signaling NO Nitric oxide pathways. NFκB Nuclear factor κB n-3 PUFA Omega-3 polyunsaturated fatty acids Keywords Stearidonic acid · Echium oil · Anti- PBS Dulbecco’s phosphate-bufered saline infammatory · NFκB (nuclear factor κB) · MAPK SDA Stearidonic acid (mitogen-activated protein kinases) pathway Introduction * Junsoo Lee Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA), [email protected] primarily eicosapentaenoic acid (EPA; 20:5) and doco- 1 sahexaenoic acid (DHA; 22:6), are benefcial in preventing Division of Food and Animal Sciences, College chronic infammatory diseases, including cardiovascular of Agriculture, Life, and Environmental Sciences, Chungbuk National University, 1 Chungdae‑ro, Seowon‑gu, Cheongju, disease, coronary artery disease, and rheumatoid arthritis Chungbuk 28644, Korea [1, 2]. Most epidemiological studies show a strong asso- 2 Research and Innovation Center, Cosmax Bio Inc., ciation between higher levels of plasma n-3 PUFA and Seongnam, Gyeonggi 13486, Korea lower in the levels of infammatory mediators in the plasma 3 Department of Food and Nutrition, Korea University, [3–5]. It was reported that EPA and DHA reduced TNF-α Seoul 02841, Korea and IL-1β in LPS-activated human monocytes and murine 1 3Vol.:(0123456789) 782 Lipids (2017) 52:781–787 macrophages [6, 7]. Fish oils are the major dietary source macrophage cells have not been investigated. Therefore, of EPA and DHA; however, overfshing or pollution of the this study aimed to investigate the anti-infammatory efects marine environment has warranted the search for alterna- of SDA isolated from echium oil. tive plant-based n-3 PUFA [8, 9]. Stearidonic acid (SDA; 18:4, Fig. 1a) is a plant-based n-3 PUFA, which recently has received much attention Materials and methods because of its various physiological functions in the human body [10]. SDA has been reported to be more efective as Materials a protecting agent in tumorigenesis of breast cancer cells than another plant-based PUFA, α-linolenic acid (18:3) SDA (purity >99%) isolated from echium oil was provided [11]. Oils derived from the members of the Boraginaceae by Dr. Inhwan Kim from Korea University (Seoul, Korea) family, including Echium (viper’s bugloss) are rich in [13]. DHA, fatty acid-free bovine serum albumin (BSA), SDA. Echium oil is an alternative natural source of n-3 LPS, 3-(4,5-dimethyl thiazol 2-yl)-2,5-diphenyltetrazolium PUFA, particularly SDA, which accounts for approxi- (MTT), dimethyl sulfoxide (DMSO), and Griess reagent mately 15–22% of total fatty acids [12]. However, the were purchased from Sigma (St. Louis, MO, USA). Dul- efect of SDA on infammatory responses and its underly- becco’s modifed Eagle’s medium (DMEM), Dulbecco’s ing molecular mechanism in LPS-stimulated RAW 264.7 phosphate-bufered saline (PBS), foetal bovine serum (FBS), penicillin–streptomycin, and Lipofectamine 2000 were obtained from Invitrogen (Carlsbad, CA, USA). Anti- bodies for inducible nitric oxide synthase (iNOS), nuclear factor-kappa B (NFκB), proliferating cell nuclear antigen (PCNA), and β-actin were obtained from Santa Cruz Bio- technology (Santa Cruz, CA, USA). Anti-phospho or total antibodies to extracellular signal regulated kinase (ERK) 1/2, c-jun N terminal kinase (JNK), and p38 were pur- chased from Cell Signaling Technology Inc. (Danvers, MA, USA). Peroxidase-conjugated secondary antibodies, NE- PER® nuclear extraction kit and SuperSignal® West Pico chemiluminescent substrate were obtained from Thermo Scientifc (Tewksbury, MA, USA). Cell Culture and Treatment RAW 264.7 cells (Koran Cell Line Bank, Seoul, Korea) were grown in DMEM supplemented with 10% FBS, 50 μg/mL streptomycin, and 100 unit/mL penicillin and incubated at 37 °C in a humidifed atmosphere of 5% CO 2. SDA (10 mM) or DHA (10 mM) as a positive control [7] were conjugated to 10% fatty acid-free BSA to ensure an even distribution in the cell culture media and were used for the treatment of cells. All stock solutions were fltered through a 0.2 µm syringe flter and stored at −20 °C. Cell Viability and Cytotoxicity Fig. 1 Efect of stearidonic acid (SDA) on the cell viability and cyto- To determine cell viability, after treatment with SDA and toxicity in RAW 264.7 macrophages. a Chemical structure of SDA DHA in the presence or absence of LPS (1 µg/mL) for 18 h, and docosahexaenoic acid (DHA). b RAW 264.7 cells were treated with diferent concentrations of SDA in the absence or presence of cells were incubated in DMEM medium containing 0.5 mg/ 1 µg/mL lipopolysaccharide (LPS) for 18 h. DHA (100 µM) was used mL MTT for an additional 4 h at 37 °C; subsequently, as a positive control. Cell viability and cytotoxicity were determined DMSO was added to dissolve formazan. The absorbance using the MTT and LDH assays, respectively. Each value is presented was measured using a microplate reader (BioTek, Inc., as the mean ± standard error (n = 3). NS not signifcant. Diferent letters among groups indicate signifcant diferences obtained using Winooski, VT, USA). To measure cytotoxicity, the con- Duncan’s test (P < 0.05) centration of lactate dehydrogenase (LDH) was estimated 1 3 Lipids (2017) 52:781–787 783 using an LDH cytotoxicity detection kit (Roche Applied Statistical Analysis Science, IN, USA). The results are reported as mean ± standard error (SE). Statistical comparisons were made using one-way analysis Cellular Fatty Acid Analysis of variance (ANOVA) using SAS version 9.4 (SAS Insti- tute, Cary, NC, USA), followed by Duncan’s multiple com- Total lipids in RAW 264.7 cell lysates were extracted with parison test. A p value <0.05 was considered statistically chloroform/methanol (2:1, v/v). Fatty acid methyl esters signifcant for all analyses. by BF3-catalyzed transesterifcation were separated and quantifed with a Hewlett-Packard 6890 gas chromatograph equipped with a fused-silica capillary column (SP-WAX, Results and Discussion 60 m × 0.25 mm i.d., Supelco, Bellefonte, PA, USA), auto injector, and fame-ionization detector (Hewlett-Packard, Efects of SDA on Cell Viability and Cytotoxicity Anondale, PA, USA), as previously described [14]. in LPS‑Stimulated RAW 264.7 Cells The MTT assay measures the mitochondrial activity of Nitrite Determination cells, which is an indicator of cell viability. The LDH leakage assay indicates membrane integrity, and this The levels of nitrite, a stable metabolite of NO, was meas- assay has been used as an indicator of cytotoxicity in ured using a colorimetric assay based on the Griess reac- various cell lines [16]. In this study, treatment with SDA tion, as previously described [15]. did not afect the viability and did not induce cytotox- icity in RAW 264.7 macrophages (Fig. 1b). Although treatment with 200 µM SDA and 100 µM DHA in the Western Blotting presence of LPS induced a signifcant decrease in the cell viability of RAW 264.7 cells, the percentage of via- To obtain whole cell extracts, the cells were washed with ble cells was more than 80%, and; thus, this treatment PBS and lysed in a Pro-Prep™ sample bufer (iNtRON was non-cytotoxic [17]. Previous studies reported that Biotechonology, Seongnam, Korea). For nuclear extraction, the n-3 PUFA, such as DHA and SDA, were not cyto- cells were prepared using the NE-PER® nuclear extraction toxic at concentrations up to 200 μM in various cell kit according to the manufacturer’s guidelines. The protein culture systems [12, 18]. In addition, it was reported concentration was quantifed using the Take3™ Multivol- that 400 μM of SDA was non-cytotoxic to healthy dog ume Plate (BioTek, Inc., Winooski, VT, USA) and equal peripheral blood mononuclear cells [19]. Similar dietary amounts of proteins were electrophoretically transferred fatty acids such as EPA and DHA in humans could attain onto a nitrocellulose membrane following separation on a up to 500 uM in plasma after oral intake in diet [20, 10% sodium dodecylsulphate (SDS)-polyacrylamide gel. 21]. Thus, the efects of using SDA at 200 μM can be The membranes were blocked with 5% non-fat milk in Tris- expected in vivo. bufered saline-Tween 20 (TBST) and subsequently incu- bated with various primary antibodies followed by addition Efects of SDA on NO Production and iNOS Protein of horseradish peroxidase-conjugated secondary antibod- Expression in LPS‑Stimulated RAW 264.7 Cells ies.
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