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Rhododendron Album Blume Extract Inhibits TNF-Α/IFN-Γ-Induced Chemokine Production Via Blockade of NF-Κb and JAK/STAT Activation in Human Epidermal Keratinocytes

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Rhododendron Album Blume Extract Inhibits TNF-Α/IFN-Γ-Induced Chemokine Production Via Blockade of NF-Κb and JAK/STAT Activation in Human Epidermal Keratinocytes 3642 INTERNATIONAL JOURNAL OF MOleCular meDICine 41: 3642-3652, 2018 Rhododendron album Blume extract inhibits TNF-α/IFN-γ-induced chemokine production via blockade of NF-κB and JAK/STAT activation in human epidermal keratinocytes JI‑WON PARK1, HAN-SOL LEE1,2, YOURIM LIM1,2, JIN‑HYUB PAIK3, OK‑KYOUNG KWON1, JUNG‑HEE KIM1, IMAM PARYANTO4, PRASETYAWAN YUNIANTO4, SANGHO CHOI3, SEI‑RYANG OH1 and KYUNG‑SEOP AHN1 1Natural Medicine Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Cheongju, Chungbuk 28116; 2College of Pharmacy, Chungbuk National University, Cheongju, Chungcheongbuk 28644; 3International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon 34141, Republic of Korea; 4Center for Pharmaceutical and Medical Technology, Kawasan Puspiptek Serpong, LAPTIAB, Tangerang, Banten 15314, Indonesia Received October 25, 2017; Accepted February 27, 2018 DOI: 10.3892/ijmm.2018.3556 Abstract. Rhododendron album Blume (RA) has traditionally TNF-α/IFN-γ‑induced expression of IL‑6, IL‑8, TARC, and been used as an herbal medicine and is considered to have MDC. In addition, RAME treatment inhibited the activation of anti‑inflammatory properties. It is a well‑known medicine for NF-κB and the JAK/STAT pathway in TNF‑α/IFN-γ-induced treatment of allergic or atopic diseases. In the present study, HaCaT cells. These results suggest that RAME decreases the the biological effects of an RA methanol extract (RAME) on production of chemokines and pro‑inflammatory cytokines inflammation were investigated in tumor necrosis factor‑α by suppressing the NF‑κB and the JAK/STAT pathways. (TNF-α)/interferon‑γ (IFN-γ)‑stimulated human keratino- Consequently, RAME may potentially be used for treatment cytes. The present study aimed to investigate the potential of atopic dermatitis. mechanisms by which R A ME in hibited TN F‑α/IFN-γ-induced expression of chemokines [thymus‑ and activation‑regulated Introduction chemokine (TARC) and macrophage‑derived chemokine (MDC)] and cytokines [interleukin (IL)‑6 and IL‑8] through Atopic dermatitis (AD) is a chronic inflammatory skin disorder the nuclear factor‑κB (NF-κB) pathway in human keratino- and persistent inflammatory skin disease accompanied by cytes. The effects of RAME treatment on cell viability were eczematous lesions and severe itching. It is caused by environ- investigated in TNF‑α/IFN-γ‑stimulated HaCaT cells. The mental and genetic factors, including microbial infection and expression of TARC, MDC, IL‑6 and IL‑8 was assessed environmental pollutants (1‑3). AD results from a combination using reverse transcription‑quantitative polymerase chain of severe pruritus, epidermal barrier abnormalities, imbal- reaction analysis or ELISA, and its effect on the inhibitory anced immune responses and genetic predisposition (4,5). mitogen‑activated protein kinase pathway was also studied The diagnosis of AD is based on the following clinical using western blot analysis. TNF‑α/IFN-γ induced the expres- phenotypes: Erythematous papules, eczematous skin, and sion of IL‑6, IL‑8, TARC and MDC in a dose‑dependent severe pruritus (6,7). manner through NF‑κB and Janus kinase/signal transducers Chemokines are a large group of small cytokines and activators of transcription (JAK/STAT) activation. produced by various types of cell, and are separated into the Notably, treatment with RAME significantly suppressed CX3C, CXC, CC, and C subfamilies based on NH2-terminal cysteine‑motifs. On the basis of the categorization of these subfamilies, a methodical nomenclature system of the chemo- kine ligands has been devised in previous studies (8). The main function of chemokines is the control of inflammatory Correspondence to: Dr Kyung‑Seop Ahn, Natural Medicine cell recruitment, including macrophages, T cells, eosinophils Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), 30 Yeongudanji‑ro, Ochang‑eup, and the trafficking of dendritic cells (DC) at sites of inflam- Cheongwon‑gu, Cheongju, Chungbuk 28116, Republic of Korea mation and infection (9). The thymus and activation‑regulated E‑mail: [email protected] chemokines (TARC/CCL17) are CC chemokines that are constitutively expressed and produced by monocyte‑derived Key words: Rhododendron album, HaCaT, Thymus- and keratinocytes and dendritic cells (10,11). Macrophage‑derived activation‑regulated chemokine, macrophage‑derived chemokine, chemokines (MDC/CCL22) are also the specific ligands for nuclear factor‑κB C‑C chemokine receptor type 4 (CCR4). MDC/CCL22 is constitutively produced by epithelial cells, B cells, kerati- nocytes, macrophages and dendritic cells (10,12). MDC and PARK et al: ANTI-ATOPIC EFFECTS OF RHODODENDRON ALBUM BLUME 3643 TARC may serve an important function in increasing the 36.5 kHz using Ultrasonic Cleaning Bath (Branson Ultrasonics; incidence of certain skin diseases, including AD. Previous Emerson Electric Co., St. Louis, MO, USA) and incubated for researchers have reported that serum concentrations of MDC 2 h at room temperature. This procedure was repeated 30 times and TARC are positively correlated with disease gravity in for 3 days to produce an extract. The methanol extract (360 mg) patients with AD patients (13). Considering all these factors, was suspended in distilled water, the same amount of n‑hexane MDC and TARC may be involved in the pathogenesis of AD. was added and mixed, and then the n‑hexane soluble fraction and Tumor necrosis factor (TNF) is a pro‑inflammatory cyto- the water‑soluble fraction were separated. This was performed kine with multiple biological functions, including cytostatic three times, followed by cotton wool filtration and concentration and cytotoxic effects, differentiation and proliferation in under reduced pressure to obtain an n‑hexane fraction (yield, various types of tumor cell. The antitumor effects of TNF are 17.2 mg). Then, the n‑hexane fraction was removed and the enhanced by interferons (IFNs) (14). The nuclear transcrip- same amount of chloroform was added to the remaining water tion factor, nuclear factor (NF)‑κB has been reported to be layer. A chloroform fraction (yield, 21.0 mg) was obtained in an anti‑apoptotic factor that serves a major function in cell the same manner. The same amount of ethyl acetate was added survival during apoptosis induced by cytokines, including to the remaining water later, and an ethyl acetate fraction TNF-α/IFN-γ, and various chemotherapeutic agents (15,16). (yield, 14.0 mg) was obtained in the same manner. Finally, an In addition, the phosphorylation of the Janus kinase/signal equivalent amount of butanol was added to the water layer, and transducers and activators of transcription (JAK/STAT) a butanol fraction (yield, 47.3 mg) was obtained in the same pathway has been reported to be an important anti‑inflam- manner. The remaining water layer was then concentrated to matory factor. JAK activation stimulates cell differentiation, obtain a water fraction (yield, 235.5 mg). proliferation, cell migration and apoptosis. Kimura et al (14) reported that a combination of TNF‑α and IFN-γ treatment Cell culture. The human keratinocyte HaCaT cell line (ATCC; resulted in an upregulated immune response in murine American Type Culture Collection, Manassas, VA, USA) was fibroblasts (14). In addition, this TNF‑α/IFN-γ combined cultured in high glucose Dulbecco's modified Eagle's medium treatment also increased the in vitro and in vivo induction of (DMEM) supplemented with 10% fetal bovine serum (FBS) human inflammation (17,18). Based on these observations, and antibiotics (100 U/ml penicillin and 100 µg/ml strepto- our group hypothesized that the synergism of atopic derma- mycin) at 37˚C in a humidified 5% CO2 incubator. Prior to titis and immune responses results in the downregulation of further association studies, the growth medium was changed TNF-α/IFN-γ‑induced cell survival mechanisms. to serum‑free medium. Cells in the control group were treated Rhododendron album Blume (RA) is a species of plant with dimethyl sulfoxide (DMSO, 0.1% per 100 µl) alone. that belongs to the family Ericaceae. It is primarily found in DMEM, FBS, penicillin, streptomycin, and PBS (pH 7.4) humid primeval forests at high altitudes throughout western were purchased from Gibco; Thermo Fisher Scientific, Inc. and central Java. RA is 1‑2 m tall, and the leaves (5‑12 cm long, (Waltham, MA, USA). Recombinant TNF‑α (10 ng/ml) was and 2‑3 cm wide) are stiff, with a brown, scaly underside. The purchased from Invitrogen; Thermo Fisher Scientific, Inc. corolla is widely campanulate, and is pale yellow in colour and IFN-γ (10 ng/ml) was purchased from Merck KGaA with scattered brown scales. RA is endemic to Java and is (Darmstadt, Germany). The HaCaT cells were pretreated rare in the wild. However, RA is grown widely in nurseries with RAME (2.5, 5, 10, 20 µg/ml) for 1 h and subsequently throughout the world, particularly in the United States. Certain treated with TNF‑α (10 ng/ml) and IFN‑γ (10 ng/ml), and plants belonging to the genus Rhododendron have documented incubated for 24 h at 37˚C. In another set of cultures, the cells anti‑cancer (19,20) and antioxidant functions (21). Therefore, were co‑incubated with 5 µM Bay11‑7082, a nuclear factor RA may also exert anti‑atopic or anti‑inflammatory activity. of κ light polypeptide gene enhancer in B‑cells inhibitor, The present study focused on the anti‑inflammatory effects of α (IκB-α) inhibitor, 10 µM SB203580, a p38 inhibitor, and RA methanol (MeOH) extract (RAME) (22). At present, there 10 µM SP600125, a c‑Jun N‑terminal kinase (JNK) inhibitor are no data on the anti‑inflammatory activity of this plant. (Calbiochem; EMD Millipore, Billerica, MA, USA) for 1 h at Therefore, the purpose of the present study was to evaluate 37˚C in a humidified 5% CO2 incubator. the anti‑inflammatory and anti‑atopic dermatitis activity of RAME in HaCaT keratinocyte cells. Cell viability. To confirm the effect of RAME on HaCaT cells, the reduction of MTT (Amresco, Inc., Solon, OH, USA) by Materials and methods viable cells was measured.
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