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Sigesbeckia Glabrescens Makino Extract Ma et al. Chin Med (2020) 15:91 https://doi.org/10.1186/s13020-020-00372-4 Chinese Medicine RESEARCH Open Access Sigesbeckia glabrescens Makino extract attenuated the collagen-induced arthritis through inhibiting the synovial hyperplasia and infammation Qiu Shuo Ma1†, Ke‑Gang Linghu1†, Tian Zhang1, Guan Ding Zhao1, Wei Xiong1, Shi Hang Xiong1, Mingming Zhao1, Wei Xu2, Juan Yu3 and Hua Yu1,2,4* Abstract Background: Sigesbeckia glabrescens Makino (SG) has been traditionally used for rheumatism and joint protection. However, the anti‑arthritic efects and underling mechanisms of SG have not been demonstrated. In this study, we investigated the anti‑arthritic efects and mechanisms of SG extract (SGE) on collagen‑induced arthritic rats and inter‑ leukin (IL)‑1β‑stimulated human synovial SW982 cells. Methods: Rats were induced to arthritis by collagen for 15 days and then received SGE treatment for 35 days. The body weight and arthritis severity score of the rats were monitored weekly. At the end of the experiment, the radio‑ graphic and histological changes of rats’ hind paw were obtained; the serum C‑reactive protein was detected by enzyme‑linked immunosorbent assay (ELISA); the expression levels of interleukin (IL)‑ 1β, IL6 and IL‑10 in the joint muscles were determined by ELISA and immunohistochemical staining; and the level of regulatory T cells (Tregs) in the spleen was detected using fow cytometry. In addition, 3‑(4,5‑Dimethylthiazol‑2‑yl)‑2,5‑diphenyltetrazolium bromide (MTT) assay and scratch wound healing assay were used to evaluate the proliferation of SW982 synovial cells. ELISA, western blot and immunofuorescence staining were used to investigate the anti‑infammatory mechanisms of SGE on IL‑1β‑induced SW982 cells and joint muscles of CIA rats. Results: SGE attenuated the collagen‑induced hind paw swelling, cartilage damage and bone erosion. SGE inhibited the synovial hyperplasia to the articular cavity in the toe joint and ankle. Moreover, SGE decreased the production of C‑reactive protein in serum and the expression of IL‑6, IL‑1β, cyclooxygenase‑2 (COX‑2) and phosphorylation of NF‑κB p65 in the joint muscles. SGE also recovered the decreased Tregs. Results from the in vitro experiments showed that SGE not only inhibited the proliferation and migration of human synovial cell but also inhibited the IL‑1β‑induced expression of IL‑6 and IL‑8. Similarly, SGE inhibited the activation of NF‑κB and the expression of COX‑2. Conclusions: SGE attenuated the collagen‑induced arthritis through inhibiting the synovial hyperplasia and infammation. Keywords: Rheumnnatoid arthritis, Synovial hyperplasia, Infammation, Sigesbeckia glabrescens Makino, SW982, Nuclear transcription factor‑kappa B *Correspondence: [email protected] †Qiu Shuo Ma and Ke‑Gang Linghu contributed equally to this work 1 Institute of Chinese Medical Sciences, State Key Laboratory of Quality Research in Chinese Medicine, University of Macau, Room 8008, Building N22, Avenida da Universidade, Taipa, Macao, SAR, China Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ma et al. Chin Med (2020) 15:91 Page 2 of 12 Background Chemicals and reagents Rheumatoid arthritis (RA) is an autoimmune disease 3-[4, 5-Dimethyl-2-thiazolyl]-2, 5-diphenyltetrazolium characterized by chronic infammation, synovial tis- bromide (MTT), dimethyl sulfoxide (DMSO), indo- sue proliferation, cartilage damaging and bone erosion. methacin (IND) and lipopolysaccharides (LPS, Escheri- Almost all RA patients lost the joint function fnally, chia coli O111:B4) were purchased from Sigma-Aldrich which highly afects the life quality of the patients, and (St. Louis, MO, United States). FITC anti-rat CD4, PE ® leads to serious social problems and a tremendous eco- anti-rat CD25, Alexa Fluor 647 anti-mouse/rat/human ® nomic burden [1]. FOXP3, (Alexa Fluor 647, PE and FITC) Mouse IgG1, Etiology and the pathogenesis of RA are complex, κ isotype ctrl and True-Nuclear™ Transcription Factor referring to various types of cells such as macrophages, Bufer Set were obtained from Biolegend (San Diego, T/B cells and fbroblasts [2]. As an important compo- CA, USA). Fetal bovine serum (FBS), 0.25% Trypsin– nent of synovial tissue, the synovial fbroblasts, also called EDTA (w/v), dulbecco’s modifed eagle’s medium fbroblast-like synoviocytes (FLS), play critical role dur- (DMEM), penicillin–streptomycin (10,000 U/mL, P/S) ing the progress of joint destruction through secreting and phosphate-bufered saline (PBS) were purchased various cytokines, proteases and arachidonic acid metab- from Termo Fisher Scientifc (Waltham, MA, USA). olites [3]. Activation of FLS promotes the clinical symp- Interleukin (IL)-1β protein and enzyme-linked immuno- toms and the process of RA [3]. Excessive proliferation sorbent assay (ELISA) kits were supplied by Neobiosci- and invasion of FLS have been reported to be involved in ence Technology Co., Ltd. (Shenzhen, China). Safranin the pathogenesis of RA. Blocking the activation of FLS to O, Fast Green FCF and Streptavidin Peroxidase immu- reduce the production of cytokines has become a prom- nohistochemistry kit were obtained from Solarbio (Bei- ising RA therapy [4]. Terefore, FLS becomes a critical jing, China). Primary antibodies against IL-1β, IL-6 and target cell for studying the treatment and pathogenesis of IL-10 were purchased from Beyotime Biotechnology RA. (Shanghai, China) and were diluted with 1:100, 1:100, Sigesbeckiae Herba (SH), a traditional anti-infam- and 1:50 respectively. Primary antibodies against NF-κB matory herbal medicine, had been used for rheumatism p65, phosphorylation (P)-p65, COX-2 and GAPDH from Tang dynasty in China [5]. Currently, the ofcially (glyceraldehyde-3-phosphate dehydrogenase) and the authorized plant origins for SH include Sigesbeckia secondary antibody were purchased from Cell Signaling pubescens Makino (SP), S. glabrescens Makino (SG), and Technology (Danvers, MA, United States), all antibodies S. orientalis L. (SO). SO had been reported to attenuate were diluted with 1:1000. λ-carrageenan-induced paw edema and LPS-induced systemic infammation in mice [6]. SP had shown thera- Herbs and herbal extracts peutic efect on collagenase-induced osteoarthritis by Te herb of Sigesbeckia glabrescens Makino (SG) was inhibiting cartilage damaging in rabbits [7]. Although collected from Jinyun (Zhejiang province, China; lon- there are growing number of reports about the pharma- gitude: 120.61, latitude: 28.66) and authenticated by cological properties of SG in vitro, such as anti-infam- Dr. Hua Yu (the corresponding author). Te voucher mation [8], immunomodulation [9], and anti-tumor specimen (No. SG-03) was deposited at the Institute of [10], it has not been demonstrated about the pharma- Chinese Medical Sciences, University of Macau, Macao cological properties of SG on arthritis in vivo. In this SAR, China. study, we investigated the therapeutic efects of SG in Te SG extract (SGE) used in this study is a part of collagen-induced arthritic rats, and further revealed the the extract prepared previously using the herbal mate- anti-proliferation and anti-infammatory mechanisms rial of SG-03 [11]. Te contents of fve components in of SG on interleukin -1β-stimulated human synovial the SGE were determined to be 4.37% (kirenol), 6.30% SW982 cells. Our work suggests the therapeutic efects (3-O-methylquercetin), 1.09% (3,7-dimethyl-5,3′,4′- of SG on RA treatment, and provides better understand- trihydroxyfavone), 0.43% (darutoside) and 1.02% (Leco- ing for rational applications of SP, SO and SG in clinics. carpinolide B), respectively, by UPLC-PDA analysis. Methods Experimental animals and treatments Te Minimum Standards of Reporting Checklist contains Male Wistar rats (7–8 weeks old) were fed on a stand- details of the experimental design, and statistics, and ard animal laboratory environment (free access to water resources used in this study (Additional fle 1). and food, 20–22 °C, relative humidity of 50% and 12-h Ma et al. Chin Med (2020) 15:91 Page 3 of 12 light/dark cycle). All the experimental protocols were separated into two parts and fxed in 10% neutral phos- in accordance with the National Institutes of Health phate-bufered formalin respectively. 24 h later, the guidelines for the Care of Use of Laboratory Animals muscles were used to detect the expression levels of and approved by the Animal Research Ethics Committee IL-6, IL-1β and IL-10 with immunohistochemical stain- (reference No: UMARE-029-2016), University of Macau, ing as previously [13]; 7 days later, the bone specimens Macao SAR, China. were decalcifed in mixed acid solution (8% hydrochlo- Te model of collagen-induced arthritis (CIA) in rats ric acid, v/v; 5% acetic acid, v/v; 10% salicylic acid, m/v) was established using emulsifed bovine type II col- for 2–3 weeks. Te decalcifed bones were used for his- lagen in incomplete Freund’s adjuvant according to topathological evaluation on the joint injury with hema- the protocol of manufacture (Chondrex, Inc., NE Red- toxylin & eosin staining and proteoglycan assessment on mond, WA 98052).
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