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Anti-Inflammatory Effects of Weigela Subsessilis Callus Extract

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Anti-Inflammatory Effects of Weigela Subsessilis Callus Extract plants Article Anti-Inflammatory Effects of Weigela subsessilis Callus Extract via Suppression of MAPK and NF-κB Signaling Hyeon-Ji Lim 1, Eun Yee Jie 2, In-Sun Park 1, Sang-Jun Kim 1, Woo Seok Ahn 2, Seung-Il Jeong 1, Suk Weon Kim 2,* and Chan-Hun Jung 1,* 1 Jeonju AgroBio-Materials Institute, Jeonju-si 54810, Jeollabuk-do, Korea; [email protected] (H.-J.L.); [email protected] (I.-S.P.); [email protected] (S.-J.K.); [email protected] (S.-I.J.) 2 Biological Resource Center, Korea Research Institute of Bioscience & Biotechnology, Jeoneup-si 56212, Jeollabuk-do, Korea; [email protected] (E.Y.J.); [email protected] (W.S.A.) * Correspondence: [email protected] (S.W.K.); [email protected] (C.-H.J.); Tel.: +82-63-570-5650 (S.W.K.); +82-63-711-1026 (C.-H.J.) Abstract: Weigela subsessilis is used in folk medicine to treat pain and allergic syndromes in Korea. However, the antibacterial and anti-inflammatory activities of W. subsessilis callus extract remain unexplored. In this study, we aimed to evaluate the W. subsessilis callus of pharmacological activity. Therefore, we first established in vitro calluses of W. subsessilis via plant tissue culture methods. We then evaluated the antioxidant and anti-inflammatory effects of W. subsessilis callus extract in lipopolysaccharide (LPS)-treated RAW264.7 macrophage cells. The W. subsessilis callus extract showed antioxidant and anti-inflammatory effects. These effects were regulated via suppression of mitogen- activated protein kinase signaling through LPS-induced translocation of nuclear factor kappa B (NF-κB) p65 from the cytoplasm to the nucleus. W. subsessilis callus extract also showed antibacterial Citation: Lim, H.-J.; Jie, E.Y.; Park, and anti-inflammatory activities in Propionibacterium acnes-treated HaCaT keratinocyte cells. These I.-S.; Kim, S.-J.; Ahn, W.S.; Jeong, S.-I.; Kim, S.W.; Jung, C.-H. results indicate that W. subsessilis callus extract has antioxidant, antibacterial and anti-inflammatory Anti-Inflammatory Effects of Weigela activities, suggesting its possible application in the treatment of inflammatory disorders. subsessilis Callus Extract via Suppression of MAPK and NF-κB Keywords: Weigela subsessilis; callus; antioxidant; antibacterial activity; anti-inflammatory; Signaling. Plants 2021, 10, 1635. inflammatory disorder https://doi.org/10.3390/plants10081635 Academic Editors: Luigi Milella and Mariangela Marrelli 1. Introduction Weigela subsessilis L. H. Bailey, a member of the family Caprifoliaceae, is widespread in Received: 20 July 2021 East Asian countries. W. subsessilis (WS) has been cultivated specifically in Korea and Japan. Accepted: 6 August 2021 It is used in folk medicine to treat pain and allergic syndromes in Korea. WS has various Published: 9 August 2021 pharmacological activities, including anti-complement activation effect, stimulation of melanogenesis, inhibition of low-density lipoprotein oxidation, stimulation of glucose up- Publisher’s Note: MDPI stays neutral take and anti-inflammatory activity [1–4]. Studies on the chemical constituents of WS have with regard to jurisdictional claims in published maps and institutional affil- shown the presence of flavonoids, coumarins, terpenoids, sterols and iridoids [5]. Among iations. the chemical constituents of WS, coumarins, terpenoids and iridoids have an equally broad spectrum of pharmacological functions, such as anti-cancer, anti-inflammatory and antibac- terial activities [6–9]. Other chemical constituents of WS, including flavonoids and sterols, also exhibit antioxidant activities [10–12]. Plant cell and tissue culture methods are efficient and powerful tools for the genetic Copyright: © 2021 by the authors. transformation of useful plant genotypes with high-value recombinant proteins and the Licensee MDPI, Basel, Switzerland. continuous production of plant-derived metabolites with commercial value [13,14]. Plant This article is an open access article distributed under the terms and cell or tissue cultures capable of producing useful metabolites offer several advantages conditions of the Creative Commons over traditional field cultivation [15]. Among them, the biggest advantage is that plant Attribution (CC BY) license (https:// cells can be easily proliferated for mass production under aseptic culture conditions. creativecommons.org/licenses/by/ Even though WS has various pharmacological activities, to the best of our knowledge, 4.0/). there have been no reports of in vitro proliferation or callus induction through plant tissue Plants 2021, 10, 1635. https://doi.org/10.3390/plants10081635 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 13 Plants 2021, 10, 1635 Even though WS has various pharmacological activities, to the best of 2 ofour 12 knowledge, there have been no reports of in vitro proliferation or callus induction through plant tissue culture. Therefore, this study aimed to evaluate whether the WS callus (WSC) culture. Therefore, this study aimed to evaluate whether the WS callus (WSC) extract extract retains the pharmacological activities of the parent plant after establishing in vitro retains the pharmacological activities of the parent plant after establishing in vitro callus callus cultures of WS to continuously produce materials of equal quality. cultures of WS to continuously produce materials of equal quality. 2.2. Results Results and and Discussion Discussion 2.1.2.1. In In Vitro Vitro Proliferation Proliferation of of W. W. subsessilis subsessilis Callus CallusesCalluses were were successfully successfully induced induced from from stem stem explants explants of of WS by culturing on 1/2MS1B03D1/2MS1B03D medium medium after after four four weeks weeks of of incu incubation.bation. The The calluses calluses were were then then transferred toto the the same same fresh medium and sub-cultured every four weeks (Figure1 1b).b). ProliferatedProliferated callusescalluses obtained obtained from from the the subculture subculture were were collected collected carefully carefully and and freeze-dried for for the antioxidant,antioxidant, antibacterial antibacterial and and anti-inflammatory anti-inflammatory assays. assays. Next, Next, to to confirm confirm the the quality of thisthis plant plant material, material, the the chemical chemical constituents constituents of of WSC WSC and and leaves leaves of of WS WS were compared usingusing a a high-performance high-performance liquid liquid chromatograp chromatographyhy (HPLC) (HPLC) with with diode diode array array detector detector anal- anal- ysis.ysis. As As shown shown in in Figure Figure 11c,c, wewe confirmedconfirmed thatthat WSCWSC containedcontained scopolinscopolin andand scopoletinscopoletin (Supplementary(Supplementary Figure S1). To To prepare WSC ex extract,tract, 500 mg of of the the dried dried WS WS calluses calluses were were dissolveddissolved in in 1 1 mL mL of of DMSO DMSO and and extracted extracted by by sonication sonication for for 1 1 h, and the supernatant was usedused in in further further studies studies after after centrifugation centrifugation at at 12,000 rpm for 5 min. (a) (b) (c) Figure 1. 1. EstablishmentEstablishment of of an an inin vitro vitro proliferproliferationation system system from from stem stem explants explants of ofW.W. subsessilis subsessilis: (a:() Fielda) Field grown grown plant plant of W. of subsessilisW. subsessilis; (b;() Inb) vitroIn vitro growngrown calluses calluses of ofW.W. subsessilis subsessilis. Scale. Scale bar, bar, 1 1cm; cm; (c ()c )HPLC HPLC chromatograms chromatograms of of scopolin scopolin (1) (1) and scopoletin (2) in extracts of W. subsessilis. A methanol extract of W. subsessilis callus was analyzed compared to standard peaks with octadecyl-silica analytical column (A), standard; (B), callus of W. subsessilis;(C), leaves of W. subsessilis). Plants 2021, 10, x FOR PEER REVIEW 3 of 13 scopoletin (2) in extracts of W. subsessilis. A methanol extract of W. subsessilis callus was analyzed compared to standard peaks with octadecyl-silica analytical column (A), standard; (B), callus of W. subsessilis; (C), leaves of W. subsessilis). Plants 2021, 10, 1635 3 of 12 2.2. Antioxidant Effect and Viability of W. subsessilis Callus Extract in RAW264.7 Cells 2.2. AntioxidantA previous Effect study and reported Viability ofthat W. the subsessilis flower Callusextract Extract of WS in has RAW264.7 antioxidant Cells and anti- inflammatoryA previous effects study [4]. reported However, that the the antioxidant flower extract and ofanti-inflammatory WS has antioxidant effects and of anti-WSC inflammatoryremain unknown. effects We [4 ].found However, that the the DPPH antioxidant (2,2-diphenyl-1-picryl-hydrazyl-hydrate) and anti-inflammatory effects of WSC rad- remainical scavenging unknown. and We SOD found (superoxide that the dismutase) DPPH (2,2-diphenyl-1-picryl-hydrazyl-hydrate) inhibition activities of WSC extract oc- radicalcurred scavenging in a dose-dependent and SOD (superoxide manner (Figure dismutase) 2). The inhibition half-maximal activities inhibitory of WSC extractconcentra- oc- curredtions of in WS a dose-dependent extract were 66 manner ± 2.56 μ (Figureg/mL in2). the The DPPH half-maximal assay and inhibitory 20.0 ± 3.33 concentrations μg/mL in the ofSOD WS extractassay. These were 66findings± 2.56 indicateµg/mL inthat the the DPPH WSC assay extract and has 20.0 significant± 3.33 µg/mL antioxidant in the SODactiv- assay.ity. These findings indicate that the WSC extract has significant antioxidant activity. (a) (b) FigureFigure 2. 2.Antioxidant Antioxidant
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