Acteoside alleviates dextran sulphate sodium‑induced ulcerative colitis via regulation of the HO‑1/HMGB1 signaling pathway

Guo,Wenjuan; Wang,Xiaodi; Liu,Fang; Chen,Shuo; Wang,Shuai; Zhang,Qingrui; Yuan,Lan; Du,Shiyu

doi:10.3892/mmr.2022.12877

Acteoside alleviates dextran sulphate sodium‑induced ulcerative colitis via regulation of the HO‑1/HMGB1 signaling pathway

Authors:
- Wenjuan Guo
- Xiaodi Wang
- Fang Liu
- Shuo Chen
- Shuai Wang
- Qingrui Zhang
- Lan Yuan
- Shiyu Du
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Affiliations: Department of Gastroenterology, China‑Japan Friendship Hospital, Beijing 100029, P.R. China, Peking University Medical and Health Analysis Center, Peking University Health Science Center, Beijing 100191, P.R. China
Published online on: October 21, 2022 https://doi.org/10.3892/mmr.2022.12877
Article Number: 360
Copyright: © Guo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Ulcerative colitis (UC) is a significant burden on human health, and the elucidation of the mechanism by which it develops has potential for the prevention and treatment of UC. It has been reported that acteoside (ACT) exhibits strong anti‑inflammatory activity. In the present study, it was hypothesized that ACT may exert a protective effect against UC. The effects of ACT on inflammation, oxidative stress and apoptosis were evaluated using dextran sulphate sodium (DSS)‑treated mice and DSS‑treated human colorectal adenocarcinoma Caco‑2 cells, which have an epithelial morphology. The results demonstrated that the ACT‑treated mice with DSS‑induced UC exhibited significantly reduced colon inflammation, as demonstrated by a reversal in body weight loss, colon shortening, disease activity index score, inflammation, oxidative stress and colonic barrier dysfunction. Further in vivo experiments demonstrated that ACT inhibited DSS‑induced apoptosis in colon tissues, as demonstrated by the results of the TUNEL assay and the altered protein expression levels of Bax, cleaved caspase‑3 and Bcl‑2. Furthermore, DSS significantly stimulated the protein expression levels of high mobility group box 1 protein (HMGB1), which serves a central role in the initiation and progression of UC, an effect which was markedly inhibited by ACT. Finally, DSS significantly decreased the protein expression levels of heme oxygenase‑1 (HO‑1) in colon tissues and the effect of ACT on GSH, apoptotic proteins and HMGB1 was markedly attenuated in the presence of the HO‑1 inhibitor tin protoporphyrin. In conclusion, ACT ameliorated colon inflammation through HMGB1 inhibition in a HO‑1‑dependent manner.

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1	Hodson R: Inflammatory bowel disease. Nature. 540:S972016. View Article : Google Scholar : PubMed/NCBI
2	Chu H, Khosravi A, Kusumawardhani IP, Kwon AH, Vasconcelos AC, Cunha LD, Mayer AE, Shen Y, Wu WL, Kambal A, et al: Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science. 352:1116–1120. 2016. View Article : Google Scholar : PubMed/NCBI
3	Neurath MF: Cytokines in inflammatory bowel disease. Nat Rev Immunol. 14:329–342. 2014. View Article : Google Scholar : PubMed/NCBI
4	Zhang YZ and Li YY: Inflammatory bowel disease: Pathogenesis. World J Gastroenterol. 20:91–99. 2014. View Article : Google Scholar : PubMed/NCBI
5	Ungar B and Kopylov U: Advances in the development of new biologics in inflammatory bowel disease. Ann Gastroenterol. 29:243–248. 2016.PubMed/NCBI
6	Ng SC, Tang W, Ching JY, Wong M, Chow CM, Hui AJ, Wong TC, Leung VK, Tsang SW, Yu HH, et al: Incidence and phenotype of inflammatory bowel disease based on results from the Asia-pacific Crohn's and colitis epidemiology study. Gastroenterology. 145:158–165.e152. 2013. View Article : Google Scholar : PubMed/NCBI
7	Kaser A, Zeissig S and Blumberg RS: Inflammatory bowel disease. Annu Rev Immunol. 28:573–621. 2010. View Article : Google Scholar : PubMed/NCBI
8	Maloy KJ and Powrie F: Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 474:298–306. 2011. View Article : Google Scholar : PubMed/NCBI
9	Cho JH: The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol. 8:458–466. 2008. View Article : Google Scholar : PubMed/NCBI
10	Khor B, Gardet A and Xavier RJ: Genetics and pathogenesis of inflammatory bowel disease. Nature. 474:307–317. 2011. View Article : Google Scholar : PubMed/NCBI
11	Wang R, Luo Y, Lu Y, Wang D, Wang T, Pu W and Wang Y: Maggot extracts alleviate inflammation and oxidative stress in acute experimental colitis via the activation of Nrf2. Oxid Med Cell Longev. 2019:47032532019. View Article : Google Scholar : PubMed/NCBI
12	Saito M, Chen-Yoshikawa TF, Suetsugu K, Okabe R, Takahagi A, Masuda S and Date H: Pirfenidone alleviates lung ischemia-reperfusion injury in a rat model. J Thorac Cardiovasc Surg. 158:289–296. 2019. View Article : Google Scholar : PubMed/NCBI
13	Wang Y, Shou Z, Fan H, Xu M, Chen Q, Tang Q, Liu X, Wu H, Zhang M, Yu T, et al: Protective effects of oxymatrine against DSS-induced acute intestinal inflammation in mice via blocking the RhoA/ROCK signaling pathway. Biosci Rep. Jul 18–2019.(Epub ahead of print). View Article : Google Scholar
14	Wu X, He W, Zhang H, Li Y, Liu Z and He Z: Acteoside: A lipase inhibitor from the Chinese tea Ligustrum purpurascens kudingcha. Food Chem. 142:306–310. 2014. View Article : Google Scholar : PubMed/NCBI
15	Esposito E, Mazzon E, Paterniti I, Dal Toso R, Pressi G, Caminiti R and Cuzzocrea S: PPAR-alpha contributes to the anti-inflammatory activity of verbascoside in a model of inflammatory bowel disease in mice. PPAR Res. 2010:9173122010. View Article : Google Scholar : PubMed/NCBI
16	Gao H, Cui Y, Kang N, Liu X, Liu Y, Zou Y, Zhang Z, Li X, Yang S, Li J, et al: Isoacteoside, a dihydroxyphenylethyl glycoside, exhibits anti-inflammatory effects through blocking toll-like receptor 4 dimerization. Br J Pharmacol. 174:2880–2896. 2017. View Article : Google Scholar : PubMed/NCBI
17	Qiao Z, Tang J, Wu W, Tang J and Liu M: Acteoside inhibits inflammatory response via JAK/STAT signaling pathway in osteoarthritic rats. BMC Complement Altern Med. 19:2642019. View Article : Google Scholar : PubMed/NCBI
18	Jing W, Chunhua M and Shumin W: Effects of acteoside on lipopolysaccharide-induced inflammation in acute lung injury via regulation of NF-kappaB pathway in vivo and in vitro. Toxicol Appl Pharmacol. 285:128–135. 2015. View Article : Google Scholar : PubMed/NCBI
19	Hausmann M, Obermeier F, Paper DH, Balan K, Dunger N, Menzel K, Falk W, Schoelmerich J, Herfarth H and Rogler G: In vivo treatment with the herbal phenylethanoid acteoside ameliorates intestinal inflammation in dextran sulphate sodium-induced colitis. Clin Exp Immunol. 148:373–381. 2007. View Article : Google Scholar : PubMed/NCBI
20	Committee for the Update of the Guide for the Care and Use of Laboratory Animals, . Guide for the Care and Use of Laboratory Animals. 8th edition. The National Academies Press; Washington, DC: 2011
21	Liu YJ, Tang B, Wang FC, Tang L, Lei YY, Luo Y, Huang SJ, Yang M, Wu LY, Wang W, et al: Parthenolide ameliorates colon inflammation through regulating Treg/Th17 balance in a gut microbiota-dependent manner. Theranostics. 10:5225–5241. 2020. View Article : Google Scholar : PubMed/NCBI
22	Eichele DD and Kharbanda KK: Dextran sodium sulfate colitis murine model: An indispensable tool for advancing our understanding of inflammatory bowel diseases pathogenesis. World J Gastroenterol. 23:6016–6029. 2017. View Article : Google Scholar : PubMed/NCBI
23	Park YH, Kim N, Shim YK, Choi YJ, Nam RH, Choi YJ, Ham MH, Suh JH, Lee SM, Lee CM, et al: Adequate dextran sodium sulfate-induced colitis model in mice and effective outcome measurement method. J Cancer Prev. 20:260–267. 2015. View Article : Google Scholar : PubMed/NCBI
24	Chen Z, Yu K, Zhu F and Gorczynski R: Over-expression of CD200 protects mice from dextran sodium sulfate induced colitis. PLoS One. 11:e01466812016. View Article : Google Scholar : PubMed/NCBI
25	Dutton JW III, Artwohl JE, Huang X and Fortman JD: Assessment of pain associated with the injection of sodium pentobarbital in laboratory mice (mus musculus). J Am Assoc Lab Anim Sci. 58:373–379. 2019. View Article : Google Scholar : PubMed/NCBI
26	Ren J, Su D, Li L, Cai H, Zhang M, Zhai J, Li M, Wu X and Hu K: Anti-inflammatory effects of aureusidin in LPS-stimulated RAW264.7 macrophages via suppressing NF-κB and activating ROS- and MAPKs-dependent Nrf2/HO-1 signaling pathways. Toxicol Appl Pharmacol. 387:1148462020. View Article : Google Scholar : PubMed/NCBI
27	Lien GS, Wu MS, Bien MY, Chen CH, Lin CH and Chen BC: Epidermal growth factor stimulates nuclear factor-κB activation and heme oxygenase-1 expression via c-Src, NADPH oxidase, PI3K, and Akt in human colon cancer cells. PLoS One. 9:e1048912014. View Article : Google Scholar : PubMed/NCBI
28	Tsoyi K, Lee TY, Lee YS, Kim HJ, Seo HG, Lee JH and Chang KC: Heme-oxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high-mobility group box 1 release in vitro and improve survival of mice in LPS- and cecal ligation and puncture-induced sepsis model in vivo. Mol Pharmacol. 76:173–182. 2009. View Article : Google Scholar : PubMed/NCBI
29	Reinke D, Kritas S, Polychronopoulos P, Skaltsounis AL, Aligiannis N and Tran CD: Herbal substance, acteoside, alleviates intestinal mucositis in mice. Gastroenterol Res Pract. 2015:3278722015. View Article : Google Scholar : PubMed/NCBI
30	Tian T, Wang Z and Zhang J: Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies. Oxid Med Cell Longev. 2017:45351942017. View Article : Google Scholar : PubMed/NCBI
31	Xia D, Zhang Z and Zhao Y: Acteoside attenuates oxidative stress and neuronal apoptosis in rats with focal cerebral ischemia-reperfusion injury. Biol Pharm Bull. 41:1645–1651. 2018. View Article : Google Scholar : PubMed/NCBI
32	Peerzada KJ, Faridi AH, Sharma L, Bhardwaj SC, Satti NK, Shashi B and Tasduq SA: Acteoside-mediates chemoprevention of experimental liver carcinogenesis through STAT-3 regulated oxidative stress and apoptosis. Environ Toxicol. 31:782–798. 2016. View Article : Google Scholar : PubMed/NCBI
33	Nakov R: New markers in ulcerative colitis. Clin Chim Acta. 497:141–146. 2019. View Article : Google Scholar : PubMed/NCBI
34	Palone F, Vitali R, Cucchiara S, Pierdomenico M, Negroni A, Aloi M, Nuti F, Felice C, Armuzzi A and Stronati L: Role of HMGB1 as a suitable biomarker of subclinical intestinal inflammation and mucosal healing in patients with inflammatory bowel disease. Inflamm Bowel Dis. 20:1448–1457. 2014. View Article : Google Scholar : PubMed/NCBI
35	Chen Y, Wu D and Sun L: Clinical significance of high-mobility group box 1 protein (HMGB1) and Nod-like receptor protein 3 (NLRP3) in patients with ulcerative colitis. Med Sci Monit. 26:e9195302020.PubMed/NCBI
36	Hu Z, Wang X, Gong L, Wu G, Peng X and Tang X: Role of high-mobility group box 1 protein in inflammatory bowel disease. Inflamm Res. 64:557–563. 2015. View Article : Google Scholar : PubMed/NCBI
37	Long H, Ruan J, Zhang M, Wang C and Huang Y: Gastrodin alleviates Tourette syndrome via Nrf-2/HO-1/HMGB1/NF-small ka, CyrillicB pathway. J Biochem Mol Toxicol. 33:e223892019. View Article : Google Scholar : PubMed/NCBI
38	Wang J, Hu X, Xie J, Xu W and Jiang H: Beta-1-adrenergic receptors mediate Nrf2-HO-1-HMGB1 axis regulation to attenuate hypoxia/reoxygenation-induced cardiomyocytes injury in vitro. Cell Physiol Biochem. 35:767–777. 2015. View Article : Google Scholar : PubMed/NCBI