Isosteviol Sodium Exerts Anti-Colitic Effects on BALB/c Mice with Dextran Sodium Sulfate-Induced Colitis Through Metabolic Reprogramming and Immune Response Modulation

References

• Chang JT. Pathophysiology of inflammatory bowel diseases. N Engl J Med. 2020;383:2652–2664. doi:10.1056/NEJMra2002697
   PubMed Web of Science ®Google Scholar
• Auerbach M, Gafter-Gvili A, Macdougall IC. Intravenous iron: a framework for changing the management of iron deficiency. Lancet Haematol. 2020;7:e342–e350. doi:10.1016/S2352-3026(19)30264-9
   PubMed Web of Science ®Google Scholar
• Zhao M, Gonczi L, Lakatos PL, Burisch J. The burden of inflammatory bowel disease in Europe in 2020. J Crohn’s & Colitis. 2021;15:1573–1587.
   PubMed Web of Science ®Google Scholar
• Ahlawat S, Kumar P, Mohan H, Goyal S, Sharma KK. Inflammatory bowel disease: tri-directional relationship between microbiota, immune system and intestinal epithelium. Crit Rev Microbiol. 2021;47:254–273. doi:10.1080/1040841X.2021.1876631
   PubMed Web of Science ®Google Scholar
• Aden K, Rehman A, Waschina S, et al. Metabolic functions of gut microbes associate with efficacy of tumor necrosis factor antagonists in patients with inflammatory bowel diseases. Gastroenterology. 2019;157:1279–1292. doi:10.1053/j.gastro.2019.07.025
   PubMed Web of Science ®Google Scholar
• Leppkes M, Neurath MF. Cytokines in inflammatory bowel diseases-update 2020. Pharmacol Res. 2020;158:104835. doi:10.1016/j.phrs.2020.104835
   PubMed Web of Science ®Google Scholar
• Na YR, Stakenborg M, Seok SH, Matteoli G. Macrophages in intestinal inflammation and resolution: a potential therapeutic target in IBD. Nat Rev Gastroenterol Hepatol. 2019;16:531–543. doi:10.1038/s41575-019-0172-4
   PubMed Web of Science ®Google Scholar
• Zhou X, Li W, Wang S, et al. YAP aggravates inflammatory bowel disease by regulating M1/M2 macrophage polarization and gut microbial homeostasis. Cell Rep. 2019;27:1176–1189. doi:10.1016/j.celrep.2019.03.028
   PubMed Web of Science ®Google Scholar
• Hall CHT, Lee JS, Murphy EM, et al. Creatine transporter, reduced in colon tissues from patients with inflammatory bowel diseases, regulates energy balance in intestinal epithelial cells, epithelial integrity, and barrier function. Gastroenterology. 2020;159:984–998. doi:10.1053/j.gastro.2020.05.033
   PubMed Web of Science ®Google Scholar
• Gui X, Li J, Ueno A, Iacucci M, Qian J, Ghosh S. Histopathologic features of inflammatory bowel disease are associated with different CD4+ T cell subsets in colonic mucosal lamina propria. J Crohn’s & Colitis. 2018;12:1448–1458.
   PubMedGoogle Scholar
• Jang YJ, Kim W-K, Han DH, Lee K, Ko G. Lactobacillus fermentum species ameliorate dextran sulfate sodium-induced colitis by regulating the immune response and altering gut microbiota. Gut Microbes. 2019;10:696–711. doi:10.1080/19490976.2019.1589281
   PubMed Web of Science ®Google Scholar
• Friedrich M, Pohin M, Powrie F. Cytokine networks in the pathophysiology of inflammatory bowel disease. Immunity. 2019;50:992–1006. doi:10.1016/j.immuni.2019.03.017
   PubMed Web of Science ®Google Scholar
• Nakase H, Uchino M, Shinzaki S, et al. Evidence-based clinical practice guidelines for inflammatory bowel disease 2020. J Gastroenterol. 2021;56:489–526. doi:10.1007/s00535-021-01784-1
   PubMed Web of Science ®Google Scholar
• Dart RJ, Ellul P, Scharl M, Lamb CA; Scientific Workshop Steering C. Results of the seventh scientific workshop of ECCO: precision medicine in IBD-challenges and future directions. J Crohn’s & Colitis. 2021;15:1407–1409.
   PubMed Web of Science ®Google Scholar
• Magro F, Cordeiro G, Dias AM, Estevinho MM. Inflammatory bowel disease-non-biological treatment. Pharmacol Res. 2020;160:105075. doi:10.1016/j.phrs.2020.105075
   PubMed Web of Science ®Google Scholar
• Naganuma M, Sugimoto S, Mitsuyama K, et al. Efficacy of indigo naturalis in a multicenter randomized controlled trial of patients with ulcerative colitis. Gastroenterology. 2018;154:935–947. doi:10.1053/j.gastro.2017.11.024
   PubMed Web of Science ®Google Scholar
• Jing W, Dong S, Luo X, et al. Berberine improves colitis by triggering AhR activation by microbial tryptophan catabolites. Pharmacol Res. 2021;164:105358. doi:10.1016/j.phrs.2020.105358
   PubMed Web of Science ®Google Scholar
• Zhang Y, Yan T, Sun D, et al. Rutaecarpine inhibits KEAP1-NRF2 interaction to activate NRF2 and ameliorate dextran sulfate sodium-induced colitis. Free Radic Biol Med. 2020;148:33–41. doi:10.1016/j.freeradbiomed.2019.12.012
   PubMed Web of Science ®Google Scholar
• Fiocchi C, Dragoni G, Iliopoulos D, et al. Results of the seventh scientific workshop of ECCO: precision medicine in IBD-what, why, and how. J Crohn’s Colitis. 2021;1–65.
   Google Scholar
• Gallagher K, Catesson A, Griffin JL, Holmes E, Williams HRT. Metabolomic analysis in inflammatory bowel disease: a systematic review. J Crohn’s Colitis. 2021;15:813–826. doi:10.1093/ecco-jcc/jjaa227
   Google Scholar
• Ding NS, McDonald JAK, Perdones-Montero A, et al. Metabonomics and the gut microbiome associated with primary response to anti-TNF therapy in Crohn’s disease. J Crohn’s Colitis. 2020;14:1090–1102. doi:10.1093/ecco-jcc/jjaa039
   Google Scholar
• Tang S-G, Liu X-Y, Ye J-M, et al. Isosteviol ameliorates diabetic cardiomyopathy in rats by inhibiting ERK and NF-κB signaling pathways. J Endocrinol. 2018;238:47–60. doi:10.1530/JOE-17-0681
   PubMed Web of Science ®Google Scholar
• Hu H, Sun X, Tian F, Zhang H, Liu Q, Tan W. Neuroprotective effects of isosteviol sodium injection on acute focal cerebral ischemia in rats. Oxid Med Cell Longev. 2016;2016:1379162. doi:10.1155/2016/1379162
   PubMed Web of Science ®Google Scholar
• Chen Y, Beng H, Su H, et al. Isosteviol prevents the development of isoprenaline induced myocardial hypertrophy. Int J Mol Med. 2019;44:1932–1942. doi:10.3892/ijmm.2019.4342
   PubMed Web of Science ®Google Scholar
• Li T, Wang C, Liu Y, et al. Neutrophil extracellular traps induce intestinal damage and thrombotic tendency in inflammatory bowel disease. J Crohn’s Colitis. 2020;14:240–253. doi:10.1093/ecco-jcc/jjz132
   Google Scholar
• Shen FC, Zhang HJ, Zhao XD, Cao RS, Shi RH. Purine analogues compared with mesalamine or 5-ASA for the prevention of postoperative recurrence in Crohn’s disease: a meta-analysis. Int J Clin Pract. 2012;66:758–766. doi:10.1111/j.1742-1241.2012.02965.x
   PubMed Web of Science ®Google Scholar
• Assa A, Matar M, Turner D, et al. Proactive monitoring of Adalimumab trough concentration associated with increased clinical remission in children with Crohn’s disease compared with reactive monitoring. Gastroenterology. 2019;157:985–996. doi:10.1053/j.gastro.2019.06.003
   PubMed Web of Science ®Google Scholar
• Colombel JF, Loftus EV, Tremaine WJ, et al. The safety profile of infliximab in patients with Crohn’s disease: the Mayo clinic experience in 500 patients. Gastroenterology. 2004;126:19–31. doi:10.1053/j.gastro.2003.10.047
   PubMed Web of Science ®Google Scholar
• Wang S, Tan KS, Beng H, et al. Protective effect of isosteviol sodium against LPS-induced multiple organ injury by regulating of glycerophospholipid metabolism and reducing macrophage-driven inflammation. Pharmacol Res. 2021;172:105781. doi:10.1016/j.phrs.2021.105781
   PubMed Web of Science ®Google Scholar
• Zhang H, Lu M, Zhang X, et al. Isosteviol sodium protects against ischemic stroke by modulating microglia/macrophage polarization via disruption of GAS5/miR-146a-5p sponge. Sci Rep. 2019;9:12221. doi:10.1038/s41598-019-48759-0
   PubMed Web of Science ®Google Scholar
• Dawson PA, Huxley S, Gardiner B, et al. Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut. 2009;58:910–919. doi:10.1136/gut.2007.147595
   PubMed Web of Science ®Google Scholar
• Wang S, Liu F, Tan KS, et al. Effect of (R)-salbutamol on the switch of phenotype and metabolic pattern in LPS-induced macrophage cells. J Cell Mol Med. 2019;24:722–736. doi:10.1111/jcmm.14780
   PubMed Web of Science ®Google Scholar
• Broeckling CD, Prenni JE. Stacked injections of biphasic extractions for improved metabolomic coverage and sample throughput. Anal Chem. 2018;90:1147–1153. doi:10.1021/acs.analchem.7b03654
   PubMed Web of Science ®Google Scholar
• Ashrafi F, Kowsari F, Darakhshandeh A, Adibi P. Composite lymphoma in a patient with ulcerative colitis: a case report. Int J Hematol Oncol Stem Cell Res. 2014;8:45–48.
   PubMedGoogle Scholar
• Chassaing B, Ley RE, Gewirtz AT. Intestinal epithelial cell toll-like receptor 5 regulates the intestinal microbiota to prevent low-grade inflammation and metabolic syndrome in mice. Gastroenterology. 2014;147:1363–1377. doi:10.1053/j.gastro.2014.08.033
   PubMed Web of Science ®Google Scholar
• Kobia FM, Preusse K, Dai Q, et al. Notch dimerization and gene dosage are important for normal heart development, intestinal stem cell maintenance, and splenic marginal zone B-cell homeostasis during mite infestation. PLoS Biol. 2020;18:e3000850. doi:10.1371/journal.pbio.3000850
   PubMed Web of Science ®Google Scholar
• Zhang A, Sun H, Wang X. Mass spectrometry-driven drug discovery for development of herbal medicine. Mass Spectrom Rev. 2018;37:307–320. doi:10.1002/mas.21529
   PubMed Web of Science ®Google Scholar
• Johnson CH, Ivanisevic J, Siuzdak G. Metabolomics: beyond biomarkers and towards mechanisms. Nat Rev Mol Cell Biol. 2016;17:451–459. doi:10.1038/nrm.2016.25
   PubMed Web of Science ®Google Scholar
• Brand S. Crohn’s disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn’s disease. Gut. 2009;58:1152–1167. doi:10.1136/gut.2008.163667
   PubMed Web of Science ®Google Scholar
• Mehandru S, Colombel JF. The intestinal barrier, an arbitrator turned provocateur in IBD. Nat Rev Gastroenterol Hepatol. 2021;18:83–84. doi:10.1038/s41575-020-00399-w
   PubMed Web of Science ®Google Scholar
• Tang B, Zhu J, Zhang B, et al. Therapeutic potential of triptolide as an anti-inflammatory agent in dextran sulfate sodium-induced murine experimental colitis. Front Immunol. 2020;11:592084. doi:10.3389/fimmu.2020.592084
   PubMed Web of Science ®Google Scholar
• Yang H, Cai R, Kong Z, et al. Teasaponin ameliorates murine colitis by regulating gut microbiota and suppressing the immune system response. Front Med. 2020;7:584369. doi:10.3389/fmed.2020.584369
   Web of Science ®Google Scholar
• Li Y, Pan X, Yin M, Li C, Han L. Preventive effect of lycopene in dDextran sulfate sodium-induced ulcerative colitis mice through the regulation of TLR4/TRIF/NF-κB signaling pathway and tight junctions. J Agric Food Chem. 2021;69:13500–13509. doi:10.1021/acs.jafc.1c05128
   PubMed Web of Science ®Google Scholar
• Lee MW, Pourmorady JS, Laine L. Use of fecal occult blood testing as a diagnostic tool for clinical indications: a systematic review and meta-analysis. Am J Gastroenterol. 2020;115:662–670. doi:10.14309/ajg.0000000000000495
   PubMed Web of Science ®Google Scholar
• Basseri RJ, Nemeth E, Vassilaki ME, et al. Hepcidin is a key mediator of anemia of inflammation in Crohn’s disease. J Crohn’s Colitis. 2013;7:e286–e291. doi:10.1016/j.crohns.2012.10.013
   Google Scholar
• Breugelmans T, Van Spaendonk H, De Man JG, et al. In-depth study of transmembrane mucins in association with intestinal barrier dysfunction during the course of T cell transfer and DSS-induced colitis. J Crohn’s Colitis. 2020;14:974–994. doi:10.1093/ecco-jcc/jjaa015
   Google Scholar
• Koelink PJ, Bloemendaal FM, Li B, et al. Anti-TNF therapy in IBD exerts its therapeutic effect through macrophage IL-10 signalling. Gut. 2020;69:1053–1063. doi:10.1136/gutjnl-2019-318264
   PubMed Web of Science ®Google Scholar
• Joosten LA, Netea MG, Dinarello CA. Interleukin-1β in innate inflammation, autophagy and immunity. Semin Immunol. 2013;25:416–424. doi:10.1016/j.smim.2013.10.018
   PubMed Web of Science ®Google Scholar
• Kaplanski G. Interleukin-18: biological properties and role in disease pathogenesis. Immunol Rev. 2018;281:138–153. doi:10.1111/imr.12616
   PubMed Web of Science ®Google Scholar
• Mu Q, Chen L, Gao X, et al. The role of iron homeostasis in remodeling immune function and regulating inflammatory disease. Sci Bull. 2021;66:1806–1816. doi:10.1016/j.scib.2021.02.010
   PubMed Web of Science ®Google Scholar
• Xu S, He Y, Lin L, Chen P, Chen M, Zhang S. The emerging role of ferroptosis in intestinal disease. Cell Death Dis. 2021;12:1–12. doi:10.1038/s41419-020-03229-8
   PubMed Web of Science ®Google Scholar
• Leuti A, Fazio D, Fava M, Piccoli A, Oddi S, Maccarrone M. Bioactive lipids, inflammation and chronic diseases. Adv Drug Deliv Rev. 2020;159:133–169. doi:10.1016/j.addr.2020.06.028
   PubMed Web of Science ®Google Scholar
• Collison LW, Murphy EJ, Jolly CA. Glycerol-3-phosphate acyltransferase-1 regulates murine T-lymphocyte proliferation and cytokine production. Am J Physiol Cell Physiol. 2008;295:C1543–C1549. doi:10.1152/ajpcell.00371.2007
   PubMed Web of Science ®Google Scholar
• Solverson P, Murali SG, Brinkman AS, et al. Glycomacropeptide, a low-phenylalanine protein isolated from cheese whey, supports growth and attenuates metabolic stress in the murine model of phenylketonuria. Am J Physiol Endocrinol Metab. 2012;302:E885–E895. doi:10.1152/ajpendo.00647.2011
   PubMed Web of Science ®Google Scholar
• Yu LM, Zhao KJ, Wang SS, Wang X, Lu B. Gas chromatography/mass spectrometry based metabolomic study in a murine model of irritable bowel syndrome. World J Gastroenterol. 2018;24:894–904. doi:10.3748/wjg.v24.i8.894
   PubMed Web of Science ®Google Scholar
• Zhou ZY, Zhao WR, Xiao Y, Zhang J, Tang JY, Lee SM. Mechanism study of the protective effects of sodium tanshinone IIA sulfonate against atorvastatin-induced cerebral hemorrhage in zebrafish: transcriptome analysis. Front Pharmacol. 2020;11:551745. doi:10.3389/fphar.2020.551745
   PubMed Web of Science ®Google Scholar
• von Martels JZH, Bourgonje AR, Klaassen MAY, et al. Riboflavin supplementation in patients with Crohn’s disease [the RISE-UP study]. J Crohn’s Colitis. 2020;14:595–607. doi:10.1093/ecco-jcc/jjz208
   Google Scholar
• Salvador P, Macias-Ceja DC, Gisbert-Ferrandiz L, et al. CD16+ macrophages mediate fibrosis in inflammatory bowel disease. J Crohn’s Colitis. 2018;12:589–599. doi:10.1093/ecco-jcc/jjx185
   Google Scholar
• Yang F, Wang D, Li Y, et al. Th1/Th2 balance and Th17/Treg-mediated immunity in relation to murine resistance to dextran sulfate-induced colitis. J Immunol Res. 2017;2017:7047201. doi:10.1155/2017/7047201
   PubMed Web of Science ®Google Scholar
• Pushparaj PN, Li D, Komai-Koma M, et al. Interleukin-33 exacerbates acute colitis via interleukin-4 in mice. Immunology. 2013;140:70–77. doi:10.1111/imm.12111
   PubMed Web of Science ®Google Scholar
• Lee S, Park K, Kim J, Min H, Seong RH. Foxp3 expression in induced regulatory T cells is stabilized by C/EBP in inflammatory environments. EMBO Rep. 2018;19:e45995. doi:10.15252/embr.201845995
   PubMed Web of Science ®Google Scholar
• Das P, Goswami P, Das TK, et al. Comparative tight junction protein expressions in colonic Crohn’s disease, ulcerative colitis, and tuberculosis: a new perspective. Virchows Arch. 2012;460:261–270. doi:10.1007/s00428-012-1195-1
   PubMed Web of Science ®Google Scholar
• Rosing N, Salvador E, Guntzel P, et al. Neuroprotective effects of isosteviol sodium in murine brain capillary cerebellar endothelial cells (cerebEND) after Hypoxia. Front Cell Neurosci. 2020;14:573950. doi:10.3389/fncel.2020.573950
   PubMed Web of Science ®Google Scholar
• Zhao L, Xiong Q, Stary CM, et al. Bidirectional gut-brain-microbiota axis as a potential link between inflammatory bowel disease and ischemic stroke. J Neuroinflammation. 2018;15:1–11. doi:10.1186/s12974-018-1382-3
   PubMed Web of Science ®Google Scholar