Lycium barbarum polysaccharide alleviates DSS-induced chronic ulcerative colitis by restoring intestinal barrier function and modulating gut microbiota

References

• Dejban P, Rahimi N, Takzare N, et al. Biochemical and histopathological evidence for the beneficial effects of modafinil on the rat model of inflammatory bowel disease: involvement of nitric oxide pathway. Pharmacol Rep. 2020;72(1):1–17. doi: 10.1007/s43440-019-00054-5.
   PubMed Web of Science ®Google Scholar
• Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2017;390(10114):2769–2778. doi: 10.1016/S0140-6736(17)32448-0.
   PubMed Web of Science ®Google Scholar
• Kaplan GG. The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol. 2015;12(12):720–727. doi: 10.1038/nrgastro.2015.150.
   PubMed Web of Science ®Google Scholar
• Windsor JW, Kaplan GG. Evolving epidemiology of IBD. Curr Gastroenterol Rep. 2019;21(8):40. doi: 10.1007/s11894-019-0705-6.
   PubMedGoogle Scholar
• Shen B, Kochhar G, Navaneethan U, et al. Role of interventional inflammatory bowel disease in the era of biologic therapy: a position statement from the global interventional IBD group. Gastrointest Endosc. 2019;89(2):215–237. doi: 10.1016/j.gie.2018.09.045.
   PubMed Web of Science ®Google Scholar
• Algieri F, Rodriguez-Nogales A, Rodriguez-Cabezas ME, et al. Botanical drugs as an emerging strategy in inflammatory bowel disease: a review. Mediators Inflamm. 2015;2015:179616–179614. doi: 10.1155/2015/179616.
   PubMed Web of Science ®Google Scholar
• Ma ZF, Zhang H, Teh SS, et al. Goji berries as a potential natural antioxidant medicine: an insight into their molecular mechanisms of action. Oxid Med Cell Longev. 2019;2019:2437397–2437399. doi: 10.1155/2019/2437397.
   PubMed Web of Science ®Google Scholar
• Cao C, Wang Z, Gong G, et al. Effects of lycium barbarum polysaccharides on immunity and metabolic syndrome associated with the modulation of gut microbiota: a review. Foods. 2022;11(20):3177. doi: 10.3390/foods11203177.
   PubMed Web of Science ®Google Scholar
• Cao C, Wang L, Ai C, et al. Impact of lycium barbarum arabinogalactan on the fecal metabolome in a DSS-induced chronic colitis mouse model. Food Funct. 2022;13(16):8703–8716. doi: 10.1039/d2fo01283a.
   PubMed Web of Science ®Google Scholar
• Chen YS, Lian YZ, Chen WC, et al. Lycium barbarum polysaccharides and capsaicin inhibit oxidative stress, inflammatory responses, and pain signaling in rats with dextran sulfate Sodium-Induced colitis. Int J Mol Sci. 2022;23(5):2423. doi: 10.3390/ijms23052423.
   Web of Science ®Google Scholar
• Wang J, Gao H, Xie Y, et al. Lycium barbarum polysaccharide alleviates dextran sodium sulfate-induced inflammatory bowel disease by regulating M1/M2 macrophage polarization via the STAT1 and STAT6 pathways. Front Pharmacol. 2023;14:1044576. doi: 10.3389/fphar.2023.1044576.
   PubMed Web of Science ®Google Scholar
• Xiao Z, Deng Q, Zhou W, et al. Immune activities of polysaccharides isolated from lycium barbarum L. What do we know so far? [Pharmacol Ther. 2022;229:107921. doi: 10.1016/j.pharmthera.2021.107921.
   PubMed Web of Science ®Google Scholar
• Muller M, Hansmannel F, Arnone D, et al. Genomic and molecular alterations in human inflammatory bowel disease-associated colorectal cancer. United European Gastroenterol J. 2020;8(6):675–684. doi: 10.1177/2050640620919254.
   PubMed Web of Science ®Google Scholar
• Lavelle A, Sokol H. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2020;17(4):223–237. doi: 10.1038/s41575-019-0258-z.
   PubMed Web of Science ®Google Scholar
• Li W, Gao M, Han T. Lycium barbarum polysaccharides ameliorate intestinal barrier dysfunction and inflammation through the MLCK-MLC signaling pathway in caco-2 cells. Food Funct. 2020;11(4):3741–3748. doi: 10.1039/d0fo00030b.
   PubMed Web of Science ®Google Scholar
• Du L, Ha C. Epidemiology and pathogenesis of ulcerative colitis. Gastroenterol Clin North Am. 2020;49(4):643–654. doi: 10.1016/j.gtc.2020.07.005.
   PubMed Web of Science ®Google Scholar
• Landy J, Ronde E, English N, et al. Tight junctions in inflammatory bowel diseases and inflammatory bowel disease associated colorectal cancer. World J Gastroenterol. 2016;22(11):3117–3126. doi: 10.3748/wjg.v22.i11.3117.
   PubMed Web of Science ®Google Scholar
• Ren X, Zhu Y, Gamallat Y, et al. E. coli O124 K72 alters the intestinal barrier and the tight junctions proteins of Guinea pig intestine. Biomed Pharmacother. 2017;94:468–473. doi: 10.1016/j.biopha.2017.07.123.
   PubMed Web of Science ®Google Scholar
• Wirtz S, Popp V, Kindermann M, et al. Chemically induced mouse models of acute and chronic intestinal inflammation. Nat Protoc. 2017;12(7):1295–1309. doi: 10.1038/nprot.2017.044.
   PubMed Web of Science ®Google Scholar
• Cho CW, Ahn S, Lim TG, et al. Cynanchum wilfordii polysaccharides suppress dextran sulfate Sodium-Induced acute colitis in mice and the production of inflammatory mediators from macrophages. Mediators Inflamm. 2017;2017:3859856–3859814. doi: 10.1155/2017/3859856.
   PubMed Web of Science ®Google Scholar
• Dieleman LA, Palmen MJ, Akol H, et al. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol. 1998;114(3):385–391. doi: 10.1046/j.1365-2249.1998.00728.x.
   PubMed Web of Science ®Google Scholar
• Pedersen J, Coskun M, Soendergaard C, et al. Inflammatory pathways of importance for management of inflammatory bowel disease. World J Gastroenterol. 2014;20(1):64–77. doi: 10.3748/wjg.v20.i1.64.
   PubMed Web of Science ®Google Scholar
• Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–9071. doi: 10.1073/pnas.1219451110.
   PubMed Web of Science ®Google Scholar
• Geirnaert A, Steyaert A, Eeckhaut V, et al. Butyricicoccus pullicaecorum, a butyrate producer with probiotic potential, is intrinsically tolerant to stomach and small intestine conditions. Anaerobe. 2014;30:70–74. doi: 10.1016/j.anaerobe.2014.08.010.
   PubMed Web of Science ®Google Scholar
• Caruso R, Mathes T, Martens EC, et al. A specific gene-microbe interaction drives the development of Crohn’s disease-like colitis in mice. Sci Immunol. 2019;4(34):eaaw4341. doi: 10.1126/sciimmunol.aaw4341.
   PubMed Web of Science ®Google Scholar
• Kaakoush NO. Sutterella species, IgA-degrading bacteria in ulcerative colitis. Trends Microbiol. 2020;28(7):519–522. doi: 10.1016/j.tim.2020.02.018.
   PubMed Web of Science ®Google Scholar
• Kang Y, Yang G, Zhang S, et al. Goji berry modulates gut microbiota and alleviates colitis in IL-10-deficient mice. Mol Nutr Food Res. 2018;62(22):e1800535. doi: 10.1002/mnfr.201800535.
   PubMed Web of Science ®Google Scholar
• Parada VD, De la Fuente MK, Landskron G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:1486. doi: 10.3389/fimmu.2019.01486.
   PubMed Web of Science ®Google Scholar
• Li C, Cai YY, Yan ZX. Brain-derived neurotrophic factor preserves intestinal mucosal barrier function and alters gut microbiota in mice. Kaohsiung J Med Sci. 2018;34(3):134–141. doi: 10.1016/j.kjms.2017.11.002.
   PubMed Web of Science ®Google Scholar
• Borisova MA, Achasova KM, Morozova KN, et al. Mucin-2 knockout is a model of intercellular junction defects, mitochondrial damage and ATP depletion in the intestinal epithelium. Sci Rep. 2020;10(1):21135. doi: 10.1038/s41598-020-78141-4.
   PubMed Web of Science ®Google Scholar
• Ding Y, Yan Y, Chen D, et al. Modulating effects of polysaccharides from the fruits of Lycium barbarum on the immune response and gut microbiota in cyclophosphamide-treated mice. Food Funct. 2019;10(6):3671–3683. doi: 10.1039/c9fo00638a.
   PubMed Web of Science ®Google Scholar
• Khor TO, Huang MT, Kwon KH, et al. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res. 2006;66(24):11580–11584. doi: 10.1158/0008-5472.CAN-06-3562.
   PubMed Web of Science ®Google Scholar
• Cao S, Du J, Hei Q. Lycium barbarum polysaccharide protects against neurotoxicity via the Nrf2-HO-1 pathway. Exp Ther Med. 2017;14(5):4919–4927. doi: 10.3892/etm.2017.5127.
   PubMed Web of Science ®Google Scholar
• Singh R, Chandrashekharappa S, Bodduluri SR, et al. Enhancement of the gut barrier integrity by a microbial metabolite through the Nrf2 pathway. Nat Commun. 2019;10(1):89. doi: 10.1038/s41467-018-07859-7.
   PubMedGoogle Scholar
• Kaplan GG, Windsor JW. The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2021;18(1):56–66. doi: 10.1038/s41575-020-00360-x.
   PubMed Web of Science ®Google Scholar
• Ng WK, Wong SH, Ng SC. Changing epidemiological trends of inflammatory bowel disease in Asia. Intest Res. 2016;14(2):111–119. doi: 10.5217/ir.2016.14.2.111.
   PubMed Web of Science ®Google Scholar
• Philippe D, Brahmbhatt V, Foata F, et al. Anti-inflammatory effects of Lacto-Wolfberry in a mouse model of experimental colitis. World J Gastroenterol. 2012;18(38):5351–5359. doi: 10.3748/wjg.v18.i38.5351.
   PubMed Web of Science ®Google Scholar
• Kang Y, Xue Y, Du M, et al. Preventive effects of goji berry on dextran-sulfate-sodium-induced colitis in mice. J Nutr Biochem. 2017;40:70–76. doi: 10.1016/j.jnutbio.2016.10.009.
   PubMed Web of Science ®Google Scholar
• Rath T, Atreya R, Neurath MF. A spotlight on intestinal permeability and inflammatory bowel diseases. Expert Rev Gastroenterol Hepatol. 2023;17(9):893–902. doi: 10.1080/17474124.2023.2242772.
   PubMed Web of Science ®Google Scholar
• Capaldo CT. Claudin barriers on the brink: how conflicting tissue and cellular priorities drive IBD pathogenesis. Int J Mol Sci. 2023;24(10):8562. doi: 10.3390/ijms24108562.
   PubMed Web of Science ®Google Scholar
• Fizanne L, Villard A, Benabbou N, et al. Faeces-derived extracellular vesicles participate in the onset of barrier dysfunction leading to liver diseases. J Extracell Vesicles. 2023;12(2):e12303. doi: 10.1002/jev2.12303.
   PubMed Web of Science ®Google Scholar
• Zhou W, Kan X, Chen G, et al. The polysaccharides from the fruits of Lycium barbarum L. modify the gut community profile and alleviate dextran sulfate sodium-induced colitis in mice. Int J Biol Macromol. 2022;222(Pt B):2244–2257. doi: 10.1016/j.ijbiomac.2022.10.015.
   PubMedGoogle Scholar
• Poplawska M, Dutta D, Jayaram M, et al. Genes modulating intestinal permeability and microbial community are dysregulated in sickle cell disease. Ann Hematol. 2022;101(5):1009–1013. doi: 10.1007/s00277-022-04794-y.
   PubMed Web of Science ®Google Scholar
• Barrett KE. Claudin-2 pore causes leak that breaches the dam in intestinal inflammation. J Clin Invest. 2020;130(10):5100–5101. doi: 10.1172/JCI140528.
   PubMed Web of Science ®Google Scholar
• Rankin CR, Lokhandwala ZA, Huang R, et al. Linear and circular CDKN2B-AS1 expression is associated with inflammatory bowel disease and participates in intestinal barrier formation. Life Sci. 2019;231:116571. doi: 10.1016/j.lfs.2019.116571.
   PubMed Web of Science ®Google Scholar
• Woo JK, Choi S, Kang JH, et al. Fermented barley and soybean (BS) mixture enhances intestinal barrier function in dextran sulfate sodium (DSS)-induced colitis mouse model. BMC Complement Altern Med. 2016;16(1):498. doi: 10.1186/s12906-016-1479-0.
   PubMedGoogle Scholar
• Peng S, Shen L, Yu X, et al. The role of Nrf2 in the pathogenesis and treatment of ulcerative colitis. Front Immunol. 2023;14:1200111. doi: 10.3389/fimmu.2023.1200111.
   PubMed Web of Science ®Google Scholar
• Liu Y, Bao Z, Xu X, et al. Extracellular Signal-Regulated kinase/nuclear factor-Erythroid2-like2/heme oxygenase-1 pathway-Mediated mitophagy alleviates traumatic brain injury-induced intestinal mucosa damage and epithelial barrier dysfunction. J Neurotrauma. 2017;34(13):2119–2131. doi: 10.1089/neu.2016.4764.
   PubMed Web of Science ®Google Scholar
• Huang Y, Zhou F, Shen C, et al. LBP reduces the inflammatory injury of kidney in septic rat and regulates the Keap1-Nrf2∕ARE signaling pathway1. Acta Cir Bras. 2019;34(1):e631258493. doi: 10.1590/s0102-865020190010000003.
   Web of Science ®Google Scholar
• Zheng G, Ren H, Li H, et al. Lycium barbarum polysaccharide reduces hyperoxic acute lung injury in mice through Nrf2 pathway. Biomed Pharmacother. 2019;111:733–739. doi: 10.1016/j.biopha.2018.12.073.
   PubMed Web of Science ®Google Scholar
• Xiong GF, Li DW, Zheng MB, et al. The effects of Lycium barbarum polysaccharide (LBP) in a mouse model of Cerulein-Induced acute pancreatitis. Med Sci Monit. 2019;25:3880–3886. doi: 10.12659/MSM.913820.
   PubMed Web of Science ®Google Scholar
• Khan I, Ullah N, Zha L, et al. Alteration of gut microbiota in inflammatory bowel disease (IBD): cause or consequence? IBD treatment targeting the gut microbiome. Pathogens. 2019;8(3):126. doi: 10.3390/pathogens8030126.
   PubMed Web of Science ®Google Scholar
• Derrien M, Belzer C, de Vos WM. Akkermansia muciniphila and its role in regulating host functions. Microb Pathog. 2017;106:171–181. doi: 10.1016/j.micpath.2016.02.005.
   PubMed Web of Science ®Google Scholar
• Zakerska-Banaszak O, Tomczak H, Gabryel M, et al. Dysbiosis of gut microbiota in polish patients with ulcerative colitis: a pilot study. Sci Rep. 2021;11(1):2166. doi: 10.1038/s41598-021-81628-3.
   PubMed Web of Science ®Google Scholar
• Devriese S, Eeckhaut V, Geirnaert A, et al. Reduced mucosa-associated butyricicoccus activity in patients with ulcerative colitis correlates with aberrant claudin-1 expression. J Crohns Colitis. 2017;11(2):229–236. doi: 10.1093/ecco-jcc/jjw142.
   PubMed Web of Science ®Google Scholar
• Steppe M, Van Nieuwerburgh F, Vercauteren G, et al. Safety assessment of the butyrate-producing Butyricicoccus pullicaecorum strain 25-3(T), a potential probiotic for patients with inflammatory bowel disease, based on oral toxicity tests and whole genome sequencing. Food Chem Toxicol. 2014;72:129–137. doi: 10.1016/j.fct.2014.06.024.
   PubMed Web of Science ®Google Scholar
• Meijer BJ, Dieleman LA. Probiotics in the treatment of human inflammatory bowel diseases: update 2011. J Clin Gastroenterol. 2011;45 Suppl(Suppl):S139–S144. doi: 10.1097/MCG.0b013e31822103f7.
   PubMedGoogle Scholar
• Zhu W, Zhou S, Liu J, et al. Prebiotic, immuno-stimulating and gut microbiota-modulating effects of lycium barbarum polysaccharide. Biomed Pharmacother. 2020;121:109591. doi: 10.1016/j.biopha.2019.109591.
   PubMed Web of Science ®Google Scholar
• Zhou F, Jiang X, Wang T, et al. Lyciumbarbarum polysaccharide (LBP): a novel prebiotics candidate for bifidobacterium and lactobacillus. Front Microbiol. 2018;9:1034. doi: 10.3389/fmicb.2018.01034.
   PubMed Web of Science ®Google Scholar
• Orlando A, Linsalata M, Bianco G, et al. Lactobacillus rhamnosus GG protects the epithelial barrier of wistar rats from the pepsin-trypsin-digested gliadin (PTG)-induced enteropathy[J]. Nutrients. 2018;10(11):1698. doi: 10.3390/nu10111698.
   PubMed Web of Science ®Google Scholar
• Wang R, Yang X, Liu J, et al. Gut microbiota regulates acute myeloid leukaemia via alteration of intestinal barrier function mediated by butyrate. Nat Commun. 2022;13(1):2522. doi: 10.1038/s41467-022-30240-8.
   PubMed Web of Science ®Google Scholar
• Peng L, Li ZR, Green RS, et al. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in caco-2 cell monolayers. J Nutr. 2009;139(9):1619–1625. doi: 10.3945/jn.109.104638.
   PubMed Web of Science ®Google Scholar