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Research Article

Stevioside attenuates bleomycin-induced pulmonary fibrosis by activating the Nrf2 pathway and inhibiting the NF-κB and TGF-β1/Smad2/3 pathways

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Pages 205-219 | Received 02 Jun 2023, Accepted 16 Nov 2023, Published online: 03 Dec 2023

References

  • Kolb M, Bonella F, Wollin L. Therapeutic targets in idiopathic pulmonary fibrosis. Respir Med. 2017;131:49–57. doi:10.1016/j.rmed.2017.07.062.
  • Mojiri-Forushani H, Hemmati AA, Dehghani MA, et al. Effects of herbal extracts and compounds and pharmacological agents on pulmonary fibrosis in animal models: a review. J Integr Med. 2017;15(6):433–441. doi:10.1016/S2095-4964(17)60363-7.
  • Selman M, King TE, Pardo A. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med. 2001;134(2):136–151. doi:10.7326/0003-4819-134-2-200101160-00015.
  • Mastruzzo C, Crimi N, Vancheri C. Role of oxidative stress in pulmonary fibrosis. Monaldi Arch Chest Dis. 2002;57(3–4):173–176.
  • Niture SK, Khatri R, Jaiswal AK. Regulation of Nrf2-an update. Free Radic Biol Med. 2014;66:36–44. doi:10.1016/j.freeradbiomed.2013.02.008.
  • Lin C, Zhao X, Sun D, et al. Transcriptional activation of follistatin by Nrf2 protects pulmonary epithelial cells against silica nanoparticle-induced oxidative stress. Sci Rep. 2016;6(1):21133–21143. doi:10.1038/srep21133.
  • Alam J, Stewart D, Touchard C, et al. Nrf2, a Cap’n’Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem. 1999;274(37):26071–26078. doi:10.1074/jbc.274.37.26071.
  • Swamy SM, Rajasekaran NS, Thannickal VJ. Nuclear factor-erythroid-2-related factor 2 in aging and lung fibrosis. Am J Pathol. 2016;186(7):1712–1723. doi:10.1016/j.ajpath.2016.02.022.
  • Chien LH, Deng JS, Jiang WP, et al. Evaluation of lung protection of Sanghuangporus sanghuang through TLR4/NF-κB/MAPK, keap1/Nrf2/HO-1, CaMKK/AMPK/Sirt1, and TGF-β/SMAD3 signaling pathways mediating apoptosis and autophagy. Biomed Pharmacother. 2023;165:115080–115082. doi:10.1016/j.biopha.2023.115080.
  • Cheng HS, Sivachandran N, Lau A, et al. MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways. EMBO Mol Med. 2013;5(7):1017–1034. doi:10.1002/emmm.201202318.
  • Ghisletti S, Meda C, Maggi A, et al. 17beta-estradiol inhibits inflammatory gene expression by controlling NF-κappaB intracellular localization. Mol Cell Biol. 2005;25(8):2957–2968. doi:10.1128/MCB.25.8.2957-2968.
  • Liu M, Ning X, Li R, et al. Signalling pathways involved in hypoxia-induced renal fibrosis. J Cell Mol Med. 2017;21(7):1248–1259. doi:10.1111/jcmm.13060.
  • Kim JY, Jeon S, Yoo YJ, et al. The Hsp27-mediated IκBα-NFκB signaling axis promotes radiation-induced lung fibrosis. Clin Cancer Res. 2019;25(17):5364–5375. doi:10.1158/1078-0432.CCR-18-3900.
  • Gong J, Gong H, Liu Y, et al. Calcipotriol attenuates liver fibrosis through the inhibition of vitamin D receptor-mediated NF-κB signaling pathway. Bioengineered. 2022;13(2):2658–2672. doi:10.1080/21655979.2021.2024385.
  • Roksandic Milenkovic M, Klisic A, Ceriman V, et al. Oxidative stress and inflammation parameters-novel biomarkers for idiopathic pulmonary fibrosis. Eur Rev Med Pharmacol Sci. 2022;26(3):927–934. doi:10.26355/eurrev_202202_28002.
  • Cheng D, Xu Q, Wang Y, et al. Metformin attenuates silica-induced pulmonary fibrosis via AMPK signaling. J Transl Med. 2021;19(1):349–358. doi:10.1186/s12967-021-03036-5.
  • Park SH, Kim JY, Kim JM, et al. PM014 attenuates radiation-induced pulmonary fibrosis via regulating NF-κB and TGF-b1/NOX4 pathways. Sci Rep. 2020;10(1):16112–16123. doi:10.1038/s41598-020-72629-9.
  • Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15(3):178–196. doi:10.1038/nrm3758.
  • Meng XM, Nikolic-Paterson DJ, Lan HY. TGF-β: the master regulator of fibrosis. Nat Rev Nephrol. 2016;12(6):325–338. doi:10.1038/nrneph.2016.48.
  • Han Q, Lin L, Zhao B, et al. Inhibition of mTOR ameliorates bleomycin-induced pulmonary fibrosis by regulating epithelial-mesenchymal transition. Biochem Biophys Res Commun. 2018;500(4):839–845. doi:10.1016/j.bbrc.2018.04.148.
  • Alavala S, Sangaraju R, Nalban N, et al. Stevioside, a diterpenoid glycoside, shows anti-inflammatory property against Dextran Sulphate Sodium-induced ulcerative colitis in mice. Eur J Pharmacol. 2019;855:192–201. doi:10.1016/j.ejphar.2019.05.015.
  • Dandin E, Üstündağ ÜV, Ünal İ, et al. Stevioside ameliorates hyperglycemia and glucose intolerance, in a diet-induced obese zebrafish model, through epigenetic, oxidative stress and inflammatory regulation. Obes Res Clin Pract. 2022;16(1):23–29. doi:10.1016/j.orcp.2022.01.002.
  • Chen C, Na X, Wang L, et al. High-throughput screening identifies stevioside as a potent agent to induce apoptosis in bladder cancer cells. Biochem Pharmacol. 2022;203:115166–115176. doi:10.1016/j.bcp.2022.115166.
  • Wang J, Shen W, Zhang JY, et al. Stevioside attenuates isoproterenol-induced mouse myocardial fibrosis through inhibition of the myocardial NF-κB/TGF-β1/Smad signaling pathway. Food Funct. 2019;10(2):1179–1190. doi:10.1039/c8fo01663a.
  • Shen W, Fan K, Zhao Y, et al. Stevioside inhibits unilateral ureteral obstruction-induced kidney fibrosis and upregulates renal PPARγ expression in mice. J Food Biochem. 2020;44(12):e13520–e13528. doi:10.1111/jfbc.13520.
  • Casas-Grajales S, Alvarez-Suarez D, Ramos-Tovar E, et al. Stevioside inhibits experimental fibrosis by down-regulating profibrotic Smad pathways and blocking hepatic stellate cell activation. Basic Clin Pharmacol Toxicol. 2019;124(6):670–680. doi:10.1111/bcpt.13194.
  • Tong B, Fu L, Hu B, et al. Tauroursodeoxycholic acid alleviates pulmonary endoplasmic reticulum stress and epithelial-mesenchymal transition in bleomycin-induced lung fibrosis. BMC Pulm Med. 2021;21(1):149–159. doi:10.1186/s12890-021-01514-6.
  • Wu G, Wei Q, Yu D, et al. Neonatal genistein exposure disrupts ovarian and uterine development in the mouse by inhibiting cellular proliferation. J Reprod Dev. 2019;65(1):7–17. doi:10.1262/jrd.2018-070.
  • Zhang S, Yu D, Wang M, et al. FGF21 attenuates pulmonary fibrogenesis through a meliorating oxidative stress in vivo and in vitro. Biomed Pharmacother. 2018;103:1516–1525. doi:10.1016/j.biopha.2018.03.100.
  • Ley B, Collard HR, King TE Jr. Clinical course and prediction of survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;183(4):431–440. doi:10.1164/rccm.201006-0894CI.
  • King CS, Nathan SD. Idiopathic pulmonary fibrosis: effects and optimal management of comorbidities. Lancet Respir Med. 2017;5(1):72–84. doi:10.1016/S2213-2600(16)30222-3.
  • Collard HR, Ward AJ, Lanes S, et al. Burden of illness in idiopathic pulmonary fibrosis. J Med Econ. 2012;15(5):829–835. doi:10.3111/13696998.2012.680553.
  • Raghu G, Chen SY, Hou Q, et al. Incidence and prevalence of idiopathic pulmonary fibrosis in US adults 18-64 years old. Eur Respir J. 2016;48(1):179–186. doi:10.1183/13993003.01653-2015.
  • Zhang Y, Lu P, Qin H, et al. Traditional Chinese medicine combined with pulmonary drug delivery system and idiopathic pulmonary fibrosis: rationale and therapeutic potential. Biomed Pharmacother. 2021;133:111072–111083. doi:10.1016/j.biopha.2020.111072.
  • Geuns JM. Stevioside. Phytochemistry. 2003;64(5):913–921. doi:10.1016/s0031-9422(03)00426-6.
  • Perrier JD, Mihalov JJ, Carlson SJ. FDA regulatory approach to steviol glycosides. Food Chem Toxicol. 2018;122:132–142. doi:10.1016/j.fct.2018.09.062.
  • Abdel-Rahman A, Anyangwe N, Carlacci L, et al. The safety and regulation of natural products used as foods and food ingredients. Toxicol Sci. 2011;123(2):333–348. doi:10.1093/toxsci/kfr198.
  • Xu Y, Liu X, Zhang Z. STV-Na attenuates lipopolysaccharide-induced lung injury in mice via the TLR4/NF-kB pathway. Immun Inflamm Dis. 2023;11(1):e770–e781. doi:10.1002/iid3.770.
  • Latha S, Chaudhary S, Ray RS. Hydroalcoholic extract of Stevia rebaudiana bert. leaves and stevioside ameliorates lipopolysaccharide induced acute liver injury in rats. Biomed Pharmacother. 2017;95:1040–1050. doi:10.1016/j.biopha.2017.08.082.
  • Shen W, Huang H, Xue J, Xie M-L. et al. Stevioside inhibits lipopolysaccharide-induced epithelial-to-mesenchymal transition of NRK-52E cells by PPARγactivation. Immunopharmacol Immunotoxicol. 2022;44(2):287–294. doi:10.1080/08923973.2022.2039935.
  • Liu T, De Los Santos FG, Phan SH. The bleomycin model of pulmonary fibrosis. Methods Mol Biol. 2017;1627:27–42. doi:10.1007/978-1-4939-7113-8_2.
  • Andersson-Sjöland A, Karlsson JC, Rydell-Törmänen K. ROS-induced endothelial stress contributes to pulmonary fibrosis through pericytes and Wnt signaling. Lab Invest. 2016;96(2):206–217. doi:10.1038/labinvest.2015.100.
  • Carnesecchi S, Deffert C, Donati Y, et al. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal. 2011;15(3):607–619. [Database] doi:10.1089/ars.2010.3829.
  • Kabel AM, Estfanous RS, Alrobaian MM. Targeting oxidative stress, proinflammatory cytokines, apoptosis and toll like receptor 4 by empagliflozin to ameliorate bleomycin-induced lung fibrosis. Respir Physiol Neurobiol. 2020;273:103316–103348. doi:10.1016/j.resp.2019.103316.
  • Bellezza I, Giambanco I, Minelli A, et al. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res. 2018;1865(5):721–733. doi:10.1016/j.bbamcr.2018.02.010.
  • Kumari S, Badana AK, G MM, et al. Reactive oxygen species: A key constituent in cancer survival. Biomark Insights. 2018;13:1177271918755391–1177271918755399. doi:10.1177/1177271918755391.
  • Liu B, Rong Y, Sun D, et al. Costunolide inhibits pulmonary fibrosis via regulating NF-κB and TGF-β1/Smad2/Nrf2-NOX4 signaling pathways. Biochem Biophys Res Commun. 2019;510(2):329–333. doi:10.1016/j.bbrc.2019.01.104.
  • Jiang J, Qi L, Lv Z, et al. Dietary stevioside supplementation alleviates lipopolysaccharide-induced intestinal mucosal damage through anti-inflammatory and intioxidant effects in broiler chickens. Antioxidants (Basel). 2019;8(12):575–594. doi:10.3390/antiox8120575.
  • Nie YJ, Wu SH, Xuan YH, et al. Role of IL-17 family cytokines in the progression of IPF from inflammation to fibrosis. Mil Med Res. 2022;9(1):21–29. doi:10.1186/s40779-022-00382-3.
  • Fielding CA, Jones GW, McLoughlin RM, et al. Interleukin-6 signaling drives fibrosis in unresolved inflammation. Immunity. 2014;40(1):40–50. doi:10.1016/j.immuni.2013.10.022.
  • Mack M. Inflammation and fibrosis. Matrix Biol. 2018;68-69:106–121. doi:10.1016/j.matbio.2017.11.010.
  • Karin M. The beginning of the end: IκB kinase (IKK) and NF-κB activation. J Biol Chem. 1999;274(39):27339–27342. [Database] doi:10.1074/jbc.274.39.27339.
  • Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[κ]B activity. Annu Rev Immunol. 2000;18(1):621–663. doi:10.1146/annurev.immunol.18.1.621.
  • Salton F, Volpe MC, Confalonieri M. Epithelial-mesenchymal transition in the pathogenesis of idiopathic pulmonary fibrosis. Medicina (Kaunas). 2019;55(4):83–89. doi:10.3390/medicina55040083.
  • Zhang C, Zhu X, Hua Y, et al. YY1 mediates TGF-β1-induced EMT and pro-fibrogenesis in alveolar epithelial cells. Respir Res. 2019;20(1):249–259. doi:10.1186/s12931-019-1223-7.
  • Hu HH, Chen DQ, Wang YN, et al. New insights into TGF-β/Smad signaling in tissue fibrosis. Chem Biol Interact. 2018;292:76–83. doi:10.1016/j.cbi.2018.07.008.