Inhibition of the Wnt/β‑catenin signaling pathway and SOX9 by XAV939 did not alleviate inflammation in a dextran sulfate sodium‑induced ulcerative colitis model
- Authors:
- Shao-Jie Liang
- Kun Wang
- Da-Bin Mao
- Li-Wei Xie
- Da-Jian Zhu
-
Affiliations: Maternal and Children's Health Research Institute, Shunde Women and Children's Hospital, Guangdong Medical University, Foshan, Guangdong 528300, P.R. China, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, Guangdong 510075, P.R. China - Published online on: November 26, 2024 https://doi.org/10.3892/etm.2024.12774
- Article Number: 24
-
Copyright: © Liang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Le Berre C, Honap S and Peyrin-Biroulet L: Ulcerative colitis. Lancet. 402:571–584. 2023.PubMed/NCBI View Article : Google Scholar | |
Wang M, Fu R, Xu D, Chen Y, Yue S, Zhang S and Tang Y: Traditional Chinese Medicine: A promising strategy to regulate the imbalance of bacterial flora, impaired intestinal barrier and immune function attributed to ulcerative colitis through intestinal microecology. J Ethnopharmacol. 318(116879)2024.PubMed/NCBI View Article : Google Scholar | |
Hassan SA, Kapur N, Sheikh F, Fahad A and Jamal S: Disease clearance in ulcerative colitis: A new therapeutic target for the future. World J Gastroenterol. 30:1801–1809. 2024.PubMed/NCBI View Article : Google Scholar | |
Le Berre C, Roda G, Nedeljkovic Protic M, Danese S and Peyrin-Biroulet L: Modern use of 5-aminosalicylic acid compounds for ulcerative colitis. Expert Opin Biol Ther. 20:363–378. 2020.PubMed/NCBI View Article : Google Scholar | |
De Deo D, Dal Buono A, Gabbiadini R, Spaggiari P, Busacca A, Masoni B, Ferretti S, Bezzio C and Armuzzi A: Management of proctitis in ulcerative colitis and the place of biological therapies. Expert Opin Biol Ther. 24:443–453. 2024.PubMed/NCBI View Article : Google Scholar | |
Heimann TM, Swaminathan S, Slater GI and Kurtz RJ: Perianal fistula after ileoanal pouch in patients with ulcerative colitis: A review of 475 patients operated on at a major IBD center. Dis Colon Rectum. 65:76–82. 2022.PubMed/NCBI View Article : Google Scholar | |
Hou Q, Huang J, Ayansola H, Masatoshi H and Zhang B: Intestinal stem cells and immune cell relationships: Potential therapeutic targets for inflammatory bowel diseases. Front Immunol. 11(623691)2021.PubMed/NCBI View Article : Google Scholar | |
Quandt J, Arnovitz S, Haghi L, Woehlk J, Mohsin A, Okoreeh M, Mathur PS, Emmanuel AO, Osman A, Krishnan M, et al: Wnt-β-catenin activation epigenetically reprograms Treg cells in inflammatory bowel disease and dysplastic progression. Nat Immunol. 22:471–484. 2021.PubMed/NCBI View Article : Google Scholar | |
Swafford D, Shanmugam A, Ranganathan P, Manoharan I, Hussein MS, Patel N, Sifuentes H, Koni PA, Prasad PD, Thangaraju M and Manicassamy S: The Wnt-β-catenin-IL-10 signaling axis in intestinal APCs protects mice from colitis-associated colon cancer in response to gut microbiota. J Immunol. 205:2265–2275. 2020.PubMed/NCBI View Article : Google Scholar | |
Chang M, Chang L, Chang HM and Chang F: Intestinal and extraintestinal cancers associated with inflammatory bowel disease. Clin Colorectal Cancer. 17:e29–e37. 2018.PubMed/NCBI View Article : Google Scholar | |
Hirano T, Hirayama D, Wagatsuma K, Yamakawa T, Yokoyama Y and Nakase H: Immunological mechanisms in inflammation-associated colon carcinogenesis. Int J Mol Sci. 21(3062)2020.PubMed/NCBI View Article : Google Scholar | |
Li F, Yan H, Jiang L, Zhao J, Lei X and Ming J: Cherry polyphenol extract ameliorated dextran sodium sulfate-induced ulcerative colitis in mice by suppressing Wnt/β-catenin signaling pathway. Foods. 11(49)2021.PubMed/NCBI View Article : Google Scholar | |
Dong LN, Wang M, Guo J and Wang JP: Influences of probiotics combined with sulfasalazine on rats with ulcerative colitis via the Wnt/β-catenin signaling pathway. Eur Rev Med Pharmacol Sci. 23:6371–6378. 2019.PubMed/NCBI View Article : Google Scholar | |
Jang J, Jung Y, Chae S, Bae T, Kim SM, Shim YJ, Chung SI and Yoon Y: XAV939, a Wnt/β-catenin pathway modulator, has inhibitory effects on LPS-induced inflammatory response. Immunopharmacol Immunotoxicol. 41:394–402. 2019.PubMed/NCBI View Article : Google Scholar | |
Yao YY, Bian LG, Yang P, Sui Y, Li R, Chen YL, Sun L, Ai QL, Zhong LM and Lu D: Gastrodin attenuates proliferation and inflammatory responses in activated microglia through Wnt/β-catenin signaling pathway. Brain Res. 1717:190–203. 2019.PubMed/NCBI View Article : Google Scholar | |
Takahashi T: Roles of nAChR and Wnt signaling in intestinal stem cell function and inflammation. Int Immunopharmacol. 81(106260)2020.PubMed/NCBI View Article : Google Scholar | |
Hiramatsu Y, Fukuda A, Ogawa S, Goto N, Ikuta K, Tsuda M, Matsumoto Y, Kimura Y, Yoshioka T, Takada Y, et al: Arid1a is essential for intestinal stem cells through Sox9 regulation. Proc Natl Acad Sci USA. 116:1704–1713. 2019.PubMed/NCBI View Article : Google Scholar | |
Moparthi L and Koch S: Wnt signaling in intestinal inflammation. Differentiation. 108:24–32. 2019.PubMed/NCBI View Article : Google Scholar | |
Parikh K, Antanaviciute A, Fawkner-Corbett D, Jagielowicz M, Aulicino A, Lagerholm C, Davis S, Kinchen J, Chen HH, Alham NK, et al: Colonic epithelial cell diversity in health and inflammatory bowel disease. Nature. 567:49–55. 2019.PubMed/NCBI View Article : Google Scholar | |
Wei P, He Q, Liu T, Zhang J, Shi K, Zhang J and Liu S: Baitouweng decoction alleviates dextran sulfate sodium-induced ulcerative colitis by suppressing leucine-related mTORC1 signaling and reducing oxidative stress. J Ethnopharmacol. 304(116095)2023.PubMed/NCBI View Article : Google Scholar | |
Zhang H, Lang W, Li S, Xu C, Wang X, Li Y, Zhang Z, Wu T and Feng M: Corynoline ameliorates dextran sulfate sodium-induced colitis in mice by modulating Nrf2/NF-κB pathway. Immunopharmacol Immunotoxicol. 45:26–34. 2023.PubMed/NCBI View Article : Google Scholar | |
Distler A, Deloch L, Huang J, Dees C, Lin NY, Palumbo-Zerr K, Beyer C, Weidemann A, Distler O, Schett G and Distler JH: Inactivation of tankyrases reduces experimental fibrosis by inhibiting canonical Wnt signalling. Ann Rheum Dis. 72:1575–1580. 2013.PubMed/NCBI View Article : Google Scholar | |
Anders S, Pyl PT and Huber W: HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics. 31:166–169. 2015.PubMed/NCBI View Article : Google Scholar | |
Lachmann A, Clarke DJB, Torre D, Xie Z and Ma'ayan A: Interoperable RNA-Seq analysis in the cloud. Biochim Biophys Acta Gene Regul Mech. 1863(194521)2020.PubMed/NCBI View Article : Google Scholar | |
Robinson MD, McCarthy DJ and Smyth GK: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26:139–140. 2010.PubMed/NCBI View Article : Google Scholar | |
McDermaid A, Monier B, Zhao J, Liu B and Ma Q: Interpretation of differential gene expression results of RNA-seq data: Review and integration. Brief Bioinform. 20:2044–2054. 2019.PubMed/NCBI View Article : Google Scholar | |
Mi JX, Zhang YN, Lai Z, Li W, Zhou L and Zhong F: Principal component analysis based on nuclear norm minimization. Neural Netw. 118:1–16. 2019.PubMed/NCBI View Article : Google Scholar | |
Yoo YE, Lee S, Kim W, Kim H, Chung C, Ha S, Park J, Chung Y, Kang H and Kim E: Early chronic memantine treatment-induced transcriptomic changes in wild-type and Shank2-mutant mice. Front Mol Neurosci. 14(712576)2021.PubMed/NCBI View Article : Google Scholar | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001.PubMed/NCBI View Article : Google Scholar | |
Liang B, Jiang Y, Song S, Jing W, Yang H, Zhao L, Chen Y, Tang Q, Li X, Zhang L, et al: ASPP2 suppresses tumour growth and stemness characteristics in HCC by inhibiting Warburg effect via WNT/β-catenin/HK2 axis. J Cell Mol Med. 27:659–671. 2023.PubMed/NCBI View Article : Google Scholar | |
Ming Z, Vining B, Bagheri-Fam S and Harley V: SOX9 in organogenesis: Shared and unique transcriptional functions. Cell Mol Life Sci. 79(522)2022.PubMed/NCBI View Article : Google Scholar | |
Kitamura S, Miyazaki Y, Shinomura Y, Kondo S, Kanayama S and Matsuzawa Y: Peroxisome proliferator-activated receptor gamma induces growth arrest and differentiation markers of human colon cancer cells. Jpn J Cancer Res. 90:75–80. 1999.PubMed/NCBI View Article : Google Scholar | |
Centonze M, Berenschot EJW, Serrati S, Susarrey-Arce A and Krol S: The fast track for intestinal tumor cell differentiation and in vitro intestinal models by inorganic topographic surfaces. Pharmaceutics. 14(218)2022.PubMed/NCBI View Article : Google Scholar | |
Yang C and Merlin D: Unveiling colitis: A journey through the dextran sodium sulfate-induced model. Inflamm Bowel Dis. 30:844–853. 2024.PubMed/NCBI View Article : Google Scholar | |
Zhong Y, Wang K, Zhang Y, Yin Q, Li S, Wang J, Zhang X, Han H and Yao K: Ocular Wnt/β-catenin pathway inhibitor XAV939-loaded liposomes for treating alkali-burned corneal wound and neovascularization. Front Bioeng Biotechnol. 9(753879)2021.PubMed/NCBI View Article : Google Scholar | |
Liu J, Kang R and Tang D: Lipopolysaccharide delivery systems in innate immunity. Trends Immunol. 45:274–287. 2024.PubMed/NCBI View Article : Google Scholar | |
So T and Ishii N: The TNF-TNFR family of co-signal molecules. Adv Exp Med Biol. 1189:53–84. 2019.PubMed/NCBI View Article : Google Scholar | |
Shi J, Ma C, Hao X, Luo H and Li M: Reserve of Wnt/β-catenin signaling alleviates mycoplasma pneumoniae P1-C-induced Inflammation in airway epithelial cells and lungs of mice. Mol Immunol. 153:60–74. 2023.PubMed/NCBI View Article : Google Scholar | |
Chen T, Zhou R, Chen Y, Fu W, Wei X, Ma G, Hu W and Lu C: Curcumin ameliorates IL-1β-induced apoptosis by activating autophagy and inhibiting the NF-κB signaling pathway in rat primary articular chondrocytes. Cell Biol Int. 45:976–988. 2021.PubMed/NCBI View Article : Google Scholar | |
Zhou J, Wu H, Hou J, Wang J, Wang J, Li M, Yao X, Gao J and Zhang Q: Daurisoline alleviated experimental colitis in vivo and in vitro: Involvement of NF-κB and Wnt/β-catenin pathway. Int Immunopharmacol. 108(108714)2022.PubMed/NCBI View Article : Google Scholar | |
Ma B and Hottiger MO: Crosstalk between Wnt/β-catenin and NF-κB signaling pathway during inflammation. Front Immunol. 7(378)2016.PubMed/NCBI View Article : Google Scholar | |
Caioni G, Viscido A, d'Angelo M, Panella G, Castelli V, Merola C, Frieri G, Latella G, Cimini A and Benedetti E: Inflammatory bowel disease: New insights into the interplay between environmental factors and PPARγ. Int J Mol Sci. 22(985)2021.PubMed/NCBI View Article : Google Scholar | |
Wang N, Kong R, Han W, Bao W, Shi Y, Ye L and Lu J: Honokiol alleviates ulcerative colitis by targeting PPAR-γ-TLR4-NF-κB signaling and suppressing gasdermin-D-mediated pyroptosis in vivo and in vitro. Int Immunopharmacol. 111(109058)2022.PubMed/NCBI View Article : Google Scholar | |
Fang J, Wang H, Xue Z, Cheng Y and Zhang X: PPARγ: The central mucus barrier coordinator in ulcerative colitis. Inflamm Bowel Dis. 27:732–741. 2021.PubMed/NCBI View Article : Google Scholar | |
Venkataraman B, Ojha S, Belur PD, Bhongade B, Raj V, Collin PD, Adrian TE and Subramanya SB: Phytochemical drug candidates for the modulation of peroxisome proliferator-activated receptor γ in inflammatory bowel diseases. Phytother Res. 34:1530–1549. 2020.PubMed/NCBI View Article : Google Scholar | |
Selim MA, Mosaad SM and El-Sayed NM: Lycopene protects against Bisphenol A induced toxicity on the submandibular salivary glands via the upregulation of PPAR-γ and modulation of Wnt/β-catenin signaling. Int Immunopharmacol. 112(109293)2022.PubMed/NCBI View Article : Google Scholar | |
Jeon KI, Phipps RP, Sime PJ and Huxlin KR: Antifibrotic actions of peroxisome proliferator-activated receptor γ ligands in corneal fibroblasts are mediated by β-catenin-regulated pathways. Am J Pathol. 187:1660–1669. 2017.PubMed/NCBI View Article : Google Scholar | |
Oda M, Hatano Y and Sato T: Intestinal epithelial organoids: Regeneration and maintenance of the intestinal epithelium. Curr Opin Genet Dev. 76(101977)2022.PubMed/NCBI View Article : Google Scholar | |
Dunleavy KA, Raffals LE and Camilleri M: Intestinal barrier dysfunction in inflammatory bowel disease: Underpinning pathogenesis and therapeutics. Dig Dis Sci. 68:4306–4320. 2023.PubMed/NCBI View Article : Google Scholar | |
Rath T, Atreya R and Neurath MF: A spotlight on intestinal permeability and inflammatory bowel diseases. Expert Rev Gastroenterol Hepatol. 17:893–902. 2023.PubMed/NCBI View Article : Google Scholar | |
Li G, Zhang B, Hao J, Chu X, Wiestler M, Cornberg M, Xu CJ, Liu X and Li Y: Identification of novel population-specific cell subsets in chinese ulcerative colitis patients using single-cell RNA sequencing. Cell Mol Gastroenterol Hepatol. 12:99–117. 2021.PubMed/NCBI View Article : Google Scholar | |
Liang SJ, Li XG and Wang XQ: Notch signaling in mammalian intestinal stem cells: Determining cell fate and maintaining homeostasis. Curr Stem Cell Res Ther. 14:583–590. 2019.PubMed/NCBI View Article : Google Scholar | |
Zipper L, Jassmann D, Burgmer S, Görlich B and Reiff T: Ecdysone steroid hormone remote controls intestinal stem cell fate decisions via the PPARγ-homolog Eip75B in Drosophila. Elife. 9(e55795)2020.PubMed/NCBI View Article : Google Scholar | |
Kong L, Pokatayev V, Lefkovith A, Carter GT, Creasey EA, Krishna C, Subramanian S, Kochar B, Ashenberg O, Lau H, et al: The landscape of immune dysregulation in Crohn's disease revealed through single-cell transcriptomic profiling in the ileum and colon. Immunity. 56:444–458.e5. 2023.PubMed/NCBI View Article : Google Scholar | |
Smillie CS, Biton M, Ordovas-Montanes J, Sullivan KM, Burgin G, Graham DB, Herbst RH, Rogel N, Slyper M, Waldman J, et al: Intra- and inter-cellular rewiring of the human colon during ulcerative colitis. Cell. 178:714–730.e22. 2019.PubMed/NCBI View Article : Google Scholar | |
Zhou S and Shu Y: Transcriptional regulation of solute carrier (SLC). Drug transporters. Drug Metab Dispos. 50:1238–1250. 2022.PubMed/NCBI View Article : Google Scholar | |
Chen L, Jiao T, Liu W, Luo Y, Wang J, Guo X, Tong X, Lin Z, Sun C, Wang K, et al: Hepatic cytochrome P450 8B1 and cholic acid potentiate intestinal epithelial injury in colitis by suppressing intestinal stem cell renewal. Cell Stem Cell. 29:1366–1381.e9. 2022.PubMed/NCBI View Article : Google Scholar | |
Kapur N, Alam MA, Hassan SA, Patel PH, Wempe LA, Bhogoju S, Goretsky T, Kim JH, Herzog J, Ge Y, et al: Enhanced mucosal mitochondrial function corrects dysbiosis and OXPHOS metabolism in IBD. bioRxiv [Preprint]: 2024.03.14.584471, 2024. | |
Yin X, Farin HF, van Es JH, Clevers H, Langer R and Karp JM: Niche-independent high-purity cultures of Lgr5+ intestinal stem cells and their progeny. Nat Methods. 11:106–112. 2014.PubMed/NCBI View Article : Google Scholar | |
Hageman JH, Heinz MC, Kretzschmar K, van der Vaart J, Clevers H and Snippert HJG: Intestinal regeneration: Regulation by the microenvironment. Dev Cell. 54:435–446. 2020.PubMed/NCBI View Article : Google Scholar |