Protective effect of berberine against LPS-induced injury in the intestine: a review

References

• Cohen J. The immunopathogenesis of sepsis. Nature. 2002;420(6917):885–891.
   PubMed Web of Science ®Google Scholar
• Lever A, Mackenzie I. Sepsis: definition, epidemiology, and diagnosis. Bmj. 2007;335(7625):879–883.
   PubMed Web of Science ®Google Scholar
• Mayeux PR. Pathobiology of lipopolysaccharide. J Toxicol Environ Health. 1997 August 01;51(5):415–435.
   PubMed Web of Science ®Google Scholar
• Bowton D. CNS effects of sepsis. Crit Care Clin. 1989;5(4):785–792.
   PubMedGoogle Scholar
• Woźnica EA, Inglot M, Woźnica RK, et al. Liver dysfunction in sepsis. Adv Clin Exp Med. 2018;27(4):547–551.
   PubMed Web of Science ®Google Scholar
• Gill SE, Rohan M, Mehta S. Role of pulmonary microvascular endothelial cell apoptosis in murine sepsis-induced lung injury in vivo. Respir Res. 2015;16(1):1–13.
   PubMedGoogle Scholar
• Merx M, Weber C. Sepsis and the heart. Circulation. 2007;116(7):793–802.
   PubMed Web of Science ®Google Scholar
• Horn DL, Morrison DC, Opal SM, et al. What are the microbial components implicated in the pathogenesis of sepsis? Report on a symposium. Clin Infect Dis. 2000;31(4):851–858.
   PubMedGoogle Scholar
• Pålsson‐mcdermott EM, O’Neill LA. Signal transduction by the lipopolysaccharide receptor, Toll‐like receptor‐4. Immunology. 2004;113(2):153–162.
   PubMed Web of Science ®Google Scholar
• Miyake K, editor Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Seminars in immunology. Elsevier. 2007;19: 3–10.
   Google Scholar
• Park BS, Lee J-O. Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med. 2013;45(12):e66–e66.
   PubMedGoogle Scholar
• Appiah MG, Park EJ, Darkwah S, et al. Intestinal epithelium-derived luminally released extracellular vesicles in sepsis exhibit the ability to suppress TNF-α and IL-17A expression in mucosal inflammation. Int J Mol Sci. 2020;21(22):8445.
   Google Scholar
• Okumura R, Takeda K. Maintenance of intestinal homeostasis by mucosal barriers. Inflamm Regen. 2018;38(1):1–8.
   PubMedGoogle Scholar
• Meng M, Klingensmith NJ, Coopersmith CM. New insights into the gut as the driver of critical illness and organ failure. Curr Opin Crit Care. 2017;23(2):143.
   PubMed Web of Science ®Google Scholar
• Earley ZM, Akhtar S, Green SJ, et al. Burn injury alters the intestinal microbiome and increases gut permeability and bacterial translocation. PloS one. 2015;10(7):e0129996.
   PubMed Web of Science ®Google Scholar
• Yao P, Cui M, Li Y, et al. Effects of rhubarb on intestinal flora and toll-like receptors of intestinal mucosa in rats with severe acute pancreatitis. Pancreas. 2015;44(5):799–804.
   PubMedGoogle Scholar
• Chen F-Q, Xu W-Z, Gao H-Y, et al. Clinical effect of changweishu on gastrointestinal dysfunction in patients with sepsis. J Int Med Res. 2020;48(8):0300060520919579.
   PubMedGoogle Scholar
• Gu L, Li N, Li Q, et al. The effect of berberine in vitro on tight junctions in human Caco-2 intestinal epithelial cells. Fitoterapia. 2009;80(4):241–248.
   PubMedGoogle Scholar
• Li G-X, Wang X-M, Jiang T, et al. Berberine prevents intestinal mucosal barrier damage during early phase of sepsis in rat through the toll-like receptors signaling pathway. Korean J Physiol Pharmacol. 2015;19(1):1–7.
   PubMedGoogle Scholar
• Gu L, Li N, Gong J, et al. Berberine ameliorates intestinal epithelial tight-junction damage and down-regulates myosin light chain kinase pathways in a mouse model of endotoxinemia. J Infect Dis. 2011;203(11):1602–1612.
   PubMed Web of Science ®Google Scholar
• Gong C, Hu X, Xu Y, et al. Berberine inhibits proliferation and migration of colorectal cancer cells by downregulation of GRP78. Anticancer Drugs. 2020;31(2):141–149.
   PubMed Web of Science ®Google Scholar
• Jin F, Xie T, Huang X, et al. Berberine inhibits angiogenesis in glioblastoma xenografts by targeting the VEGFR2/ERK pathway. Pharm Biol. 2018;56(1):665–671.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang S. Berberine suppresses growth and metastasis of endometrial cancer cells via miR-101/COX-2. Biomed Pharmacother. 2018;103:1287–1293.
   PubMed Web of Science ®Google Scholar
• Yu Y, Liu L, Wang X, et al. Modulation of glucagon-like peptide-1 release by berberine: in vivo and in vitro studies. Biochem Pharmacol. 2010;79(7):1000–1006.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li X, Zou D, et al. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J Clin Endocrinol Metab. 2008;93(7):2559–2565.
   PubMed Web of Science ®Google Scholar
• Zhang H, Wei J, Xue R, et al. Berberine lowers blood glucose in type 2 diabetes mellitus patients through increasing insulin receptor expression. Metabolism. 2010;59(2):285–292.
   PubMed Web of Science ®Google Scholar
• Kim WS, Lee YS, Cha SH, et al. Berberine improves lipid dysregulation in obesity by controlling central and peripheral AMPK activity. Am J Physiol Endocrinol Metab. 2009;296(4):E812–E819.
   PubMedGoogle Scholar
• Derosa G, Maffioli P, Cicero AF. Berberine on metabolic and cardiovascular risk factors: an analysis from preclinical evidences to clinical trials. Expert Opin Biol Ther. 2012;12(8):1113–1124.
   PubMed Web of Science ®Google Scholar
• Wang K, Chen Q, Wu N, et al. Berberine ameliorates spatial learning memory impairment and modulates cholinergic anti-inflammatory pathway in diabetic rats. Front Pharmacol. 2019;10:1003.
   PubMedGoogle Scholar
• Yarmohammadi F, Karbasforooshan H, Hayes AW, et al. Inflammation suppression in doxorubicin-induced cardiotoxicity: natural compounds as therapeutic options. Naunyn-Schmiedeberg’s Arch Pharmacol. 2021 October 01;394(10):2003–2011.
   Google Scholar
• Habtemariam S. Berberine pharmacology and the gut microbiota: a hidden therapeutic link. Pharmacol Res. 2020;155:104722.
   PubMed Web of Science ®Google Scholar
• Wu S-J, Don T-M, Lin C-W, et al. Delivery of berberine using chitosan/fucoidan-taurine conjugate nanoparticles for treatment of defective intestinal epithelial tight junction barrier. Mar Drugs. 2014;12(11):5677–5697.
   PubMed Web of Science ®Google Scholar
• Feng A-W, Gao W, Zhou G-R, et al. Berberine ameliorates COX-2 expression in rat small intestinal mucosa partially through PPARγ pathway during acute endotoxemia. Int Immunopharmacol. 2012;12(1):182–188.
   PubMedGoogle Scholar
• Shan C, Yang J, Kong Y, et al. Alteration of the intestinal barrier and GLP2 secretion in berberine-treated type 2 diabetic rats. J Endocrinol. 2013;218(3):255–262.
   PubMedGoogle Scholar
• Liu C-S, Zheng Y-R, Zhang Y-F, et al. Research progress on berberine with a special focus on its oral bioavailability. Fitoterapia. 2016;109:274–282.
   PubMed Web of Science ®Google Scholar
• Lu Y-C, Yeh W-C, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine. 2008;42(2):145–151.
   PubMed Web of Science ®Google Scholar
• Frey E, Miller D, Jahr TG, et al. Soluble CD14 participates in the response of cells to lipopolysaccharide. J Exp Med. 1992;176(6):1665–1671.
   PubMed Web of Science ®Google Scholar
• Shimazu R, Akashi S, Ogata H, et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med. 1999;189(11):1777–1782.
   PubMed Web of Science ®Google Scholar
• Zhao C, Wang Y, Yuan X, et al. Berberine inhibits lipopolysaccharide-induced expression of inflammatory cytokines by suppressing TLR4-mediated NF-ĸB and MAPK signaling pathways in rumen epithelial cells of Holstein calves. J Dairy Res. 2019;86(2):171–176.
   PubMed Web of Science ®Google Scholar
• Nyati KK, Masuda K, Zaman MM, et al. TLR4-induced NF-κB and MAPK signaling regulate the IL-6 mRNA stabilizing protein Arid5a. Nucleic Acids Res. 2017 Mar 17;45(5):2687–2703. PubMed PMID: 28168301; PubMed Central PMCID: PMCPMC5389518. eng
   PubMedGoogle Scholar
• Chu M, Ding R, Chu Z-Y, et al. Role of berberine in anti-bacterial as a high-affinity LPS antagonist binding to TLR4/MD-2 receptor. BMC Complement Altern Med. 2014;14(1):1–9.
   PubMedGoogle Scholar
• Li H-M, Wang Y-Y, Wang H-D, et al. Berberine protects against lipopolysaccharide-induced intestinal injury in mice via alpha 2 adrenoceptor-independent mechanisms. Acta Pharmacol Sin. 2011;32(11):1364–1372.
   PubMedGoogle Scholar
• Xu X, Zhang L, Zhao Y, et al. Anti‑inflammatory mechanism of berberine on lipopolysaccharide‑induced IEC‑18 models based on comparative transcriptomics. Mol Med Rep. 2020;22(6):5163–5180.
   PubMed Web of Science ®Google Scholar
• Xu G, Wan H, Yi L, et al. Berberine administrated with different routes attenuates inhaled LPS-induced acute respiratory distress syndrome through TLR4/NF-κB and JAK2/STAT3 inhibition. Eur J Pharmacol. 2021;908:174349.
   PubMedGoogle Scholar
• Chen H, Liu Q, Liu X, et al. Berberine attenuates septic cardiomyopathy by inhibiting TLR4/NF-κB signalling in rats. Pharm Biol. 2021;59(1):121–128.
   PubMed Web of Science ®Google Scholar
• Hu Y, Chen X, Duan H, et al. Chinese herbal medicinal ingredients inhibit secretion of IL-6, IL-8, E-selectin and TXB2 in LPS-induced rat intestinal microvascular endothelial cells. Immunopharmacol Immunotoxicol. 2009;31(4):550–555.
   PubMed Web of Science ®Google Scholar
• Zhu Z, Xueying L, Chunlin L, et al. Effect of berberine on LPS-induced expression of NF-κ B/MAPK signalling pathway and related inflammatory cytokines in porcine intestinal epithelial cells. Innate Immun. 2020;26(7):627–634.
   PubMed Web of Science ®Google Scholar
• Pahl HL. Activators and target genes of Rel/NF-κB transcription factors. Oncogene. 1999;18(49):6853–6866.
   PubMed Web of Science ®Google Scholar
• Detmer K, Wang Z, Warejcka D, et al. Endotoxin stimulated cytokine production in rat vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2001;281(2):H661–H668.
   PubMedGoogle Scholar
• Vardam TD, Zhou L, Appenheimer MM, et al. Regulation of a lymphocyte–endothelial–IL-6 trans-signaling axis by fever-range thermal stress: hot spot of immune surveillance. Cytokine. 2007;39(1):84–96.
   PubMedGoogle Scholar
• Duan H, Zhang Y, Xu J, et al. Effect of anemonin on NO, ET-1 and ICAM-1 production in rat intestinal microvascular endothelial cells. J Ethnopharmacol. 2006;104(3):362–366.
   PubMedGoogle Scholar
• Kucharzik T, Hudson JT, Lügering A, et al. Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut. 2005;54(11):1565–1572.
   PubMed Web of Science ®Google Scholar
• Pfeffer K. Biological functions of tumor necrosis factor cytokines and their receptors. Cytokine Growth Factor Rev. 2003;14(3–4):185–191.
   PubMed Web of Science ®Google Scholar
• Liu D, Zhang Y, Liu Y, et al. Berberine modulates gut microbiota and reduces insulin resistance via the TLR4 signaling pathway. Exp Clin Endocrinol Diabetes. 2018;126(8):513–520.
   PubMedGoogle Scholar
• Li F, WANG H, LU D, et al. Neutral sulfate berberine modulates cytokine secretion and increases survival in endotoxemic mice 1. Acta Pharmacol Sin. 2006;27(9):1199–1205.
   PubMedGoogle Scholar
• Schlegel N, Leweke R, Meir M, et al. Role of NF-κB activation in LPS-induced endothelial barrier breakdown. Histochem Cell Biol. 2012;138(4):627–641.
   PubMedGoogle Scholar
• Ma TY, Boivin MA, Ye D, et al. Mechanism of TNF-α modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol. 2005;288(3):G422–G430.
   PubMed Web of Science ®Google Scholar
• Al-Sadi R, Ye D, Dokladny K, et al. Mechanism of IL-1β-induced increase in intestinal epithelial tight junction permeability. J Immunol. 2008;180(8):5653–5661.
   PubMed Web of Science ®Google Scholar
• Gatica-Andrades M, Vagenas D, Kling J, et al. WNT ligands contribute to the immune response during septic shock and amplify endotoxemia-driven inflammation in mice. Blood Adv. 2017;1(16):1274–1286.
   PubMedGoogle Scholar
• Ranaivo HR, Carusio N, Wangensteen R, et al. Protection against endotoxic shock as a consequence of reduced nitrosative stress in MLCK210-null mice. Am J Pathol. 2007;170(2):439–446.
   PubMedGoogle Scholar
• Shen L, Black ED, Witkowski ED, et al. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci. 2006;119(10):2095–2106.
   PubMed Web of Science ®Google Scholar
• Li C, Yu J, Ai K, et al. IκBα phosphorylation and associated NF-κB activation are essential events in lymphocyte activation, proliferation, and anti-bacterial adaptive immune response of Nile tilapia. Dev Comp Immunol. 2020;103:103526.
   PubMedGoogle Scholar
• Cui L, Wang H, Lin J, et al. Progesterone inhibits inflammatory response in E. coli-or LPS-Stimulated bovine endometrial epithelial cells by NF-κB and MAPK pathways. Dev Comp Immunol. 2020;105:103568.
   PubMedGoogle Scholar
• Mahmoudi M, Zamani Taghizadeh Rabe S, Balali-Mood M, et al. Immunotoxicity induced in mice by subacute exposure to berberine. J Immunotoxicol. 2016;13(2):255–262.
   PubMed Web of Science ®Google Scholar
• Yarmohammadi F, Hayes AW, Karimi G. Possible protective effect of resolvin D1 on inflammation in atrial fibrillation: involvement of ER stress mediated the NLRP3 inflammasome pathway. Naunyn-Schmiedeberg’s Arch Pharmacol. 2021 August 01;394(8):1613–1619.
   Google Scholar
• Hou Q, Zhu S, Zhang C, et al. Berberine improves intestinal epithelial tight junctions by upregulating A20 expression in IBS-D mice. Biomed Pharmacother. 2019;118:109206.
   PubMedGoogle Scholar
• Guo M, Cao J, Chen M, et al. Berberine maintains intestinal homeostasis through modulating TLR4/NF-κB/MTORC pathway and autophagy in cats. 2022.
   Google Scholar
• Coulombe P, Meloche S. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim Biophys Acta-Mol Cell Res. 2007;1773(8):1376–1387.
   PubMed Web of Science ®Google Scholar
• Yang S-H, Sharrocks AD, Whitmarsh AJ. MAP kinase signalling cascades and transcriptional regulation. Gene. 2013;513(1):1–13.
   PubMed Web of Science ®Google Scholar
• Roskoski Jr R. ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol Res. 2012;66(2):105–143.
   PubMedGoogle Scholar
• He S, Hou X, Xu X, et al. Quantitative proteomic analysis reveals heat stress-induced injury in rat small intestine via activation of the MAPK and NF-κB signaling pathways. Mol Biosyst. 2015;11(3):826–834.
   PubMedGoogle Scholar
• Tang M, Yuan D, Liao P. Berberine improves intestinal barrier function and reduces inflammation, immunosuppression, and oxidative stress by regulating the NF-κB/MAPK signaling pathway in deoxynivalenol-challenged piglets. Environ Pollut. 2021;289:117865.
   PubMedGoogle Scholar
• Hla T. Sphingosine 1-phosphate in coagulation and inflammation. Semin Immunopathol. 2012;34(1):73–91.
   PubMedGoogle Scholar
• Ding R, Han J, Tian Y, et al. Sphingosine-1-phosphate attenuates lung injury induced by intestinal ischemia/reperfusion in mice: role of inducible nitric-oxide synthase. Inflammation. 2012;35(1):158–166.
   PubMed Web of Science ®Google Scholar
• Frej C, Linder A, Happonen KE, et al. Sphingosine 1‐phosphate and its carrier apolipoprotein M in human sepsis and in Escherichia coli sepsis in baboons. J Cell Mol Med. 2016;20(6):1170–1181.
   PubMedGoogle Scholar
• Sorribas M, Jakob MO, Yilmaz B, et al. FXR modulates the gut-vascular barrier by regulating the entry sites for bacterial translocation in experimental cirrhosis. J Hepatol. 2019;71(6):1126–1140.
   PubMed Web of Science ®Google Scholar
• Vermette D, Hu P, Canarie MF, et al. Tight junction structure, function, and assessment in the critically ill: a systematic review. Intensive Care Med Exp. 2018;6(1):1–18.
   Google Scholar
• Li Y, Zhou J, Qiu J, et al. Berberine reduces gut-vascular barrier permeability via modulation of ApoM/S1P pathway in a model of polymicrobial sepsis. Life Sci. 2020;261:118460.
   PubMed Web of Science ®Google Scholar
• Spadoni I, Pietrelli A, Pesole G, et al. Gene expression profile of endothelial cells during perturbation of the gut vascular barrier. Gut Microbes. 2016;7(6):540–548.
   PubMed Web of Science ®Google Scholar
• Spadoni I, Zagato E, Bertocchi A, et al. A gut-vascular barrier controls the systemic dissemination of bacteria. Science. 2015;350(6262):830–834.
   PubMed Web of Science ®Google Scholar
• Wilkerson BA, Grass GD, Wing SB, et al. Sphingosine 1-phosphate (S1P) carrier-dependent regulation of endothelial barrier: high density lipoprotein (HDL)-S1P prolongs endothelial barrier enhancement as compared with albumin-S1P via effects on levels, trafficking, and signaling of S1P1. J Biol Chem. 2012;287(53):44645–44653.
   PubMed Web of Science ®Google Scholar
• Garcia JG, Liu F, Verin AD, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001;108(5):689–701.
   PubMed Web of Science ®Google Scholar
• Zhang X, Jiang B, Luo G, et al. Hyperglycemia down-regulates apolipoprotein M expression in vivo and in vitro. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids. 2007;1771(7):879–882.
   PubMedGoogle Scholar
• Jiang B, Zhang X, Di D, et al. Hyperglycemia-induced downregulation of apolipoprotein M expression is not via the hexosamine pathway. Lipids Health Dis. 2015;14(1):1–6.
   PubMedGoogle Scholar
• Silva-García O, Valdez-Alarcón JJ, Baizabal-Aguirre VM. Wnt/β-catenin signaling as a molecular target by pathogenic bacteria. Front Immunol. 2019;10:2135.
   PubMedGoogle Scholar
• Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20(1):781–810.
   PubMedGoogle Scholar
• Pai SG, Carneiro BA, Mota JM, et al. Wnt/beta-catenin pathway: modulating anticancer immune response. J Hematol Oncol. 2017;10(1):1–12.
   PubMedGoogle Scholar
• Srinivasan B, Kolli AR, Esch MB, et al. TEER measurement techniques for in vitro barrier model systems. J Lab Autom. 2015;20(2):107–126.
   PubMedGoogle Scholar
• He Y, Yuan X, Zuo H, et al. Berberine exerts a protective effect on gut-vascular barrier via the modulation of the Wnt/beta-catenin signaling pathway during sepsis. Cell Physiol Biochem. 2018;49(4):1342–1351.
   PubMedGoogle Scholar
• Duan Y, Liao AP, Kuppireddi S, et al. β-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest. 2007;87(6):613–624.
   PubMed Web of Science ®Google Scholar
• Grishin A, Wang J, Hackam D, et al. p38 MAP kinase mediates endotoxin-induced expression of cyclooxygenase-2 in enterocytes. Surgery. 2004;136(2):329–335.
   PubMedGoogle Scholar
• Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010;10(2):131–144.
   PubMed Web of Science ®Google Scholar
• Grishin AV, Wang J, Potoka DA, et al. Lipopolysaccharide induces cyclooxygenase-2 in intestinal epithelium via a noncanonical p38 MAPK pathway. J Immunol. 2006;176(1):580–588.
   PubMedGoogle Scholar
• Singer II, Kawka DW, Schloemann S, et al. Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology. 1998;115(2):297–306.
   PubMed Web of Science ®Google Scholar
• Unno N, Wang H, Menconi MJ, et al. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology. 1997;113(4):1246–1257.
   PubMed Web of Science ®Google Scholar
• Short SS, Wang J, Castle SL, et al. Low doses of celecoxib attenuate gut barrier failure during experimental peritonitis. Lab Invest. 2013;93(12):1265–1275.
   PubMedGoogle Scholar
• Hsu W-H, Hsieh Y-S, Kuo H-C, et al. Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL. Arch Toxicol. 2007;81(10):719–728.
   PubMed Web of Science ®Google Scholar
• Tanabe T, Tohnai N. Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat. 2002;68:95–114.
   PubMedGoogle Scholar
• Bottone Jr FG, Martinez JM, Alston-Mills B, et al. Gene modulation by Cox-1 and Cox-2 specific inhibitors in human colorectal carcinoma cancer cells. Carcinogenesis. 2004;25(3):349–357.
   PubMedGoogle Scholar
• Guo Y-S, Hellmich MR, Wen XD, et al. Activator protein-1 transcription factor mediates bombesin-stimulated cyclooxygenase-2 expression in intestinal epithelial cells. J Biol Chem. 2001;276(25):22941–22947.
   PubMedGoogle Scholar
• Feng A-W, Yu C, Mao Q, et al. Berberine hydrochloride attenuates cyclooxygenase-2 expression in rat small intestinal mucosa during acute endotoxemia. Fitoterapia. 2011;82(7):976–982.
   PubMedGoogle Scholar
• Baeuerle PA, Baltimore D. NF-κB: ten years after. Cell. 1996;87(1):13–20.
   PubMed Web of Science ®Google Scholar
• Kojima M, Morisaki T, Izuhara K, et al. Lipopolysaccharide increases cyclo-oxygenase-2 expression in a colon carcinoma cell line through nuclear factor-κB activation. Oncogene. 2000;19(9):1225–1231.
   PubMed Web of Science ®Google Scholar
• Granado M, Martín AI, Villanúa MÁ, et al. Experimental arthritis inhibits the insulin-like growth factor-I axis and induces muscle wasting through cyclooxygenase-2 activation. Am J Physiol Endocrinol Metab. 2007;292(6):E1656–E1665.
   PubMedGoogle Scholar
• Priego T, Ibáñez de Cáceres I, Martín AI, et al. NO plays a role in LPS-induced decreases in circulating IGF-I and IGFBP-3 and their gene expression in the liver. Am J Physiol Endocrinol Metab. 2004;286(1):E50–E56.
   PubMedGoogle Scholar
• Onnureddy K, Onteru SK, Singh D. IGF-1 attenuates LPS induced pro-inflammatory cytokines expression in buffalo (Bubalus bubalis) granulosa cells. Mol Immunol. 2015;64(1):136–143.
   PubMedGoogle Scholar
• Haydon AM, MacInnis RJ, English DR, et al. Physical activity, insulin-like growth factor 1, insulin-like growth factor binding protein 3, and survival from colorectal cancer. Gut. 2006;55(5):689–694.
   PubMedGoogle Scholar
• Zhang W, Frankel WL, Adamson WT, et al. Insulin-like growth factor-I improves mucosal structure and function in transplanted rat small intestine. Transplantation. 1995;59(5):755–761.
   PubMed Web of Science ®Google Scholar
• Scopa CD, Koureleas S, Tsamandas AC, et al. Beneficial effects of growth hormone and insulin-like growth factor I on intestinal bacterial translocation, endotoxemia, and apoptosis in experimentally jaundiced rats. J Am Coll Surg. 2000;190(4):423–431.
   PubMedGoogle Scholar
• Lorenzo-Zuñiga V, Rodriguez-Ortigosa CM, Bartoli R, et al. Insulin-like growth factor I improves intestinal barrier function in cirrhotic rats. Gut. 2006;55(9):1306–1312.
   PubMed Web of Science ®Google Scholar
• Zhao T-Y, Su L-P, Ma C-Y, et al. IGF-1 decreases portal vein endotoxin via regulating intestinal tight junctions and plays a role in attenuating portal hypertension of cirrhotic rats. BMC Gastroenterol. 2015;15(1):1–10.
   PubMedGoogle Scholar
• Hatakeyama N, Kojima T, Iba K, et al. IGF-I regulates tight-junction protein claudin-1 during differentiation of osteoblast-like MC3T3-E1 cells via a MAP-kinase pathway. Cell Tissue Res. 2008;334(2):243–254.
   PubMedGoogle Scholar
• Hwa V, Oh Y, Rosenfeld RG. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev. 1999;20(6):761–787.
   PubMed Web of Science ®Google Scholar
• Chen K, Okuma T, Okamura K, et al. Insulin‐like growth factor‐I prevents gut atrophy and maintains intestinal integrity in septic rats. J Parenteral Enteral Nutr. 1995;19(2):119–124.
   PubMedGoogle Scholar
• He Y, Yuan X, Zhou G, et al. Activation of IGF-1/IGFBP-3 signaling by berberine improves intestinal mucosal barrier of rats with acute endotoxemia. Fitoterapia. 2018;124:200–205.
   PubMedGoogle Scholar
• Fukuda K, Hibiya Y, Mutoh M, et al. Inhibition by berberine of cyclooxygenase-2 transcriptional activity in human colon cancer cells. J Ethnopharmacol. 1999;66(2):227–233.
   PubMed Web of Science ®Google Scholar
• Torra P, Gervois P, Staels B. Peroxisome proliferator-activated receptor alpha in metabolic disease, inflammation, atherosclerosis and aging. Curr Opin Lipidol. 1999;10(2):151–159.
   PubMedGoogle Scholar
• Berger J, Moller DE. The mechanisms of action of PPARs. Annu Rev Med. 2002;53(1):409–435.
   PubMed Web of Science ®Google Scholar
• Michalik L, Auwerx J, Berger JP, et al. International union of pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol Rev. 2006;58(4):726–741.
   PubMed Web of Science ®Google Scholar
• Baregamian N, Mourot JM, Ballard AR, et al. PPAR-γ agonist protects against intestinal injury during necrotizing enterocolitis. Biochem Biophys Res Commun. 2009;379(2):423–427.
   PubMedGoogle Scholar
• Ricote M, Huang J, Fajas L, et al. Expression of the peroxisome proliferator-activated receptor γ (PPARγ) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc Nat Acad Sci. 1998;95(13):7614–7619.
   PubMedGoogle Scholar
• Huin C, Corriveau L, Bianchi A, et al. Differential expression of peroxisome proliferator-activated receptors (PPARs) in the developing human fetal digestive tract. J Histochem Cytochem. 2000;48(5):603–611.
   PubMedGoogle Scholar
• Su CG, Wen X, Bailey ST, et al. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammatory response. J Clin Invest. 1999;104(4):383–389.
   PubMed Web of Science ®Google Scholar
• Chinetti G, Fruchart J-C, Staels B. Peroxisome proliferator-activated receptors (PPARs): nuclear receptors at the crossroads between lipid metabolism and inflammation. Inflammation Res. 2000;49(10):497–505.
   PubMed Web of Science ®Google Scholar
• Eun CS, Han DS, Lee SH, et al. Attenuation of colonic inflammation by PPARγ in intestinal epithelial cells: effect on toll-like receptor pathway. Dig Dis Sci. 2006;51(4):693–697.
   PubMedGoogle Scholar
• Carvalho M, Gonçalves-de-albuquerque CF, Silva AR. PPAR gamma: from definition to molecular targets and therapy of lung diseases. Int J Mol Sci. 2021;22(2):805.
   Google Scholar
• Feng A, Zhou G, Yuan X, et al. Inhibitory effect of baicalin on iNOS and NO expression in intestinal mucosa of rats with acute endotoxemia. PloS one. 2013;8(12):e80997.
   PubMedGoogle Scholar
• Rangwala SM, Rhoades B, Shapiro JS, et al. Genetic modulation of PPARγ phosphorylation regulates insulin sensitivity. Dev Cell. 2003;5(4):657–663.
   PubMedGoogle Scholar
• Diradourian C, Girard J, Pégorier J-P. Phosphorylation of PPARs: from molecular characterization to physiological relevance. Biochimie. 2005;87(1):33–38.
   PubMedGoogle Scholar
• Guan C, Qiao S, Lv Q, et al. Orally administered berberine ameliorates bleomycin-induced pulmonary fibrosis in mice through promoting activation of PPAR-γ and subsequent expression of HGF in colons. Toxicol Appl Pharmacol. 2018;343:1–15.
   PubMed Web of Science ®Google Scholar
• Mahmoud AM, Hozayen WG, Ramadan SM. Berberine ameliorates methotrexate-induced liver injury by activating Nrf2/HO-1 pathway and PPARγ, and suppressing oxidative stress and apoptosis in rats. Biomed Pharmacother. 2017 October 01;94:280–291.
   PubMed Web of Science ®Google Scholar
• He Y, Yuan X, Zuo H, et al. Berberine induces ZIP14 expression and modulates zinc redistribution to protect intestinal mucosal barrier during polymicrobial sepsis. Life Sci. 2019;233:116697.
   PubMedGoogle Scholar
• Guthrie GJ, Aydemir TB, Troche C, et al. Influence of ZIP14 (slc39A14) on intestinal zinc processing and barrier function. Am J Physiol Gastrointest Liver Physiol. 2015;308(3):G171–G178.
   PubMedGoogle Scholar
• Aydemir TB, Cousins RJ. The multiple faces of the metal transporter ZIP14 (SLC39A14). J Nutr. 2018;148(2):174–184.
   PubMedGoogle Scholar
• Zhang Q, Piao X-L, Piao X-S, et al. Preventive effect of Coptis chinensis and berberine on intestinal injury in rats challenged with lipopolysaccharides. Food Chem Toxicol. 2011;49(1):61–69.
   PubMed Web of Science ®Google Scholar
• Rao A. Efficacy of berberine hydrochloride on biochemical parameters in Indian type 2 diabetic patients. Endocr Pract. 2017;23(1):18A.
   Google Scholar
• Zeng X-H, Zeng X-J, Li -Y-Y. Efficacy and safety of berberine for congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am J Cardiol. 2003;92(2):173–176.
   PubMed Web of Science ®Google Scholar
• Wang L, Peng L, Wei G, et al. Therapeutic effects of berberine capsule on patients with mild hyperlipidemia. Zhongguo Zhong xi yi jie he za zhi Zhongguo Zhongxiyi jiehe zazhi= Chinese j integrated trad Western med. 2016;36(6):681–684.
   PubMedGoogle Scholar
• Li G-H, Wang D-L, Hu Y-D, et al. Berberine inhibits acute radiation intestinal syndrome in human with abdomen radiotherapy. Med Oncol. 2010;27(3):919–925.
   PubMedGoogle Scholar
• Jiang X-W, Zhang Y, Zhu Y-L, et al. Effects of berberine gelatin on recurrent aphthous stomatitis: a randomized, placebo-controlled, double-blind trial in a Chinese cohort. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013;115(2):212–217.
   PubMedGoogle Scholar
• Chen C, Tao C, Liu Z, et al. A randomized clinical trial of berberine hydrochloride in patients with diarrhea‐predominant irritable bowel syndrome. Phytother Res. 2015;29(11):1822–1827.
   PubMed Web of Science ®Google Scholar