Maackiain Protects the Kidneys of Type 2 Diabetic Rats via Modulating the Nrf2/HO-1 and TLR4/NF-κB/Caspase-3 Pathways

References

• International Diabetes Federation. IDF Diabetes Atlas. 8th ed. Brussels, Belgium: International Diabetes Federation; 2017.
   Google Scholar
• SaeediP, SalpeaP, KarurangaS, etal. Mortality attributable to diabetes in 20–79 years old adults, 2019 estimates: results from the International Diabetes Federation Diabetes Atlas. Diabetes Res Clin Pract. 2020;162:108086. doi:10.1016/j.diabres.2020.10808632068099
   PubMed Web of Science ®Google Scholar
• AndersH-J, HuberTB, IsermannB, SchifferM. CKD in diabetes: diabetic kidney disease versus nondiabetic kidney disease. Nat Rev Nephrol. 2018;14(6):361–377.29654297
   PubMed Web of Science ®Google Scholar
• Anguiano GómezL, LeiY, Kumar DevarapuS, AndersH. The diabetes pandemic suggests unmet needs for ‘CKD with diabetes’ in addition to ‘diabetic nephropathy’—implications for pre-clinical research and drug testing. Nephrol Dial Transplant. 2018;33(8):1292–1304.28992221
   PubMed Web of Science ®Google Scholar
• Al HroobAM, AbukhalilMH, AlghonmeenRD, MahmoudAM. Ginger alleviates hyperglycemia-induced oxidative stress, inflammation and apoptosis and protects rats against diabetic nephropathy. Biomed Pharmacother. 2018;106:381–389.29966984
   PubMed Web of Science ®Google Scholar
• FernandesSM, CordeiroPM, WatanabeM, FonsecaCD, VattimoMF. The role of oxidative stress in streptozotocin-induced diabetic nephropathy in rats. Arch Endocrinol Metabol. 2016;60(5):443–449. doi:10.1590/2359-3997000000188
   PubMed Web of Science ®Google Scholar
• MahmoodniaL, AghadavodE, BeigrezaeiS, Rafieian-KopaeiM. An update on diabetic kidney disease, oxidative stress and antioxidant agents. JRenal Injury Prev. 2017;6(2):153.
   PubMed Web of Science ®Google Scholar
• VomundS, SchäferA, ParnhamMJ, BrüneB, Von KnethenA. Nrf2, the master regulator of anti-oxidative responses. IntJMol Sci. 2017;18(12):2772. doi:10.3390/ijms18122772
   Web of Science ®Google Scholar
• JiangT, HuangZ, LinY, ZhangZ, FangD, ZhangDD. The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes. 2010;59(4):850–860.20103708
   PubMed Web of Science ®Google Scholar
• BaoL, LiJ, ZhaD, etal. Chlorogenic acid prevents diabetic nephropathy by inhibiting oxidative stress and inflammation through modulation of the Nrf2/HO-1 and NF-ĸB pathways. IntImmunopharmacol. 2018;54:245–253.
   PubMed Web of Science ®Google Scholar
• Donate-CorreaJ, Luis-RodríguezD, Martín-NúñezE, etal. Inflammatory targets in diabetic nephropathy. JClin Med. 2020;9(2):458.
   PubMed Web of Science ®Google Scholar
• SuryavanshiSV, KulkarniYA. NF-κβ: apotential target in the management of vascular complications of diabetes. Front Pharmacol. 2017;8:798.29163178
   PubMed Web of Science ®Google Scholar
• SuQ, LvX, SunY, etal. Role of TLR4/MyD88/NF-κB signaling pathway in coronary microembolization-induced myocardial injury prevented and treated with nicorandil. Biomed Pharmacother. 2018;106:776–784.29990871
   PubMed Web of Science ®Google Scholar
• ModakM, DixitP, LondheJ, GhaskadbiS, DevasagayamTP. Recent advances in Indian herbal drug research guest editor: Thomas Paul Asir Devasagayam Indian herbs and herbal drugs used for the treatment of diabetes. Nutrition. 2007;40(3):163–173.
   Google Scholar
• WangJ, FengB, XiongX. Chinese herbal medicine for the treatment of obesity-related hypertension. Evid Based Complement Altern Med. 2013;2013. doi:10.1155/2013/757540
   Web of Science ®Google Scholar
• HeX, FangJ, HuangL, WangJ, HuangXJ. Traditional usage, phytochemistry and pharmacology of an important traditional Chinese medicine. Sophora Flavescens Ait. 2015;172:10–29.
   Google Scholar
• CaoX, HeQ. Anti-tumor activities of bioactive phytochemicals in sophora flavescens for breast cancer. Research. 2020;12:1457.
   Google Scholar
• NariaiY, MizuguchiH, OgasawaraT, etal. Disruption of heat shock protein 90 (Hsp90)-protein kinase Cδ (PKCδ) interaction by (−)-maackiain suppresses histamine H1 receptor gene transcription in HeLa cells. JBiol Chem. 2015;290(45):27393–27402.26391399
   PubMed Web of Science ®Google Scholar
• LeeHW, RyuHW, KangM-G, etal. Potent selective monoamine oxidase Binhibition by maackiain, apterocarpan from the roots of Sophora flavescens. Bioorgan Med Chem Lett. 2016;26(19):4714–4719.
   Web of Science ®Google Scholar
• MaH, HuangQ, QuW, etal. In vivo and invitro anti-inflammatory effects of Sophora flavescens residues. JEthnopharmacol. 2018;224:497–503.29913301
   PubMed Web of Science ®Google Scholar
• SrinivasanK, ViswanadB, AsratL, KaulC, RamaraoP. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: amodel for type 2 diabetes and pharmacological screening. Pharmacol Res. 2005;52(4):313–320.15979893
   PubMed Web of Science ®Google Scholar
• MahmoudAM, AshourMB, Abdel-MoneimA, AhmedOM. Hesperidin and naringin attenuate hyperglycemia-mediated oxidative stress and proinflammatory cytokine production in high fat fed/streptozotocin-induced type 2 diabetic rats. JDiabetes Complicat. 2012;26(6):483–490.
   PubMed Web of Science ®Google Scholar
• Organisation for Economic Co-operation and Development. Test No.425: Acute Oral Toxicity: Up-And-Down Procedure. OECD Publishing; 2008.
   Google Scholar
• MizuguchiH, NariaiY, KatoS, etal. Maackiain is anovel antiallergic compound that suppresses transcriptional upregulation of the histamine H1 receptor and interleukin‐4 genes. Pharmacol Res Perspect. 2015;3(5):e00166.26516579
   PubMedGoogle Scholar
• RuntuweneJ, ChengK-C, AsakawaA, etal. Rosmarinic acid ameliorates hyperglycemia and insulin sensitivity in diabetic rats, potentially by modulating the expression of PEPCK and GLUT4. Drug Design Dev Ther. 2016;10:2193.
   PubMed Web of Science ®Google Scholar
• YelumalaiS, GiribabuN, Kamarulzaman KarimSZO, SallehNB, SallehNB. In vivo administration of quercetin ameliorates sperm oxidative stress, inflammation, preserves sperm morphology and functions in streptozotocin-nicotinamide induced adult male diabetic rats. Archiv Med Sci. 2019;15(1):240. doi:10.5114/aoms.2018.81038
   Web of Science ®Google Scholar
• GiribabuN, KarimK, KilariEK, SallehN. Phyllanthus niruri leaves aqueous extract improves kidney functions, ameliorates kidney oxidative stress, inflammation, fibrosis and apoptosis and enhances kidney cell proliferation in adult male rats with diabetes mellitus. JEthnopharmacol. 2017;205:123–137. doi:10.1016/j.jep.2017.05.00228483637
   PubMed Web of Science ®Google Scholar
• KhalilASM, GiribabuN, YelumalaiS, ShahzadH, KilariEK, SallehN. Myristic acid defends against testicular oxidative stress, inflammation, apoptosis: restoration of spermatogenesis, steroidogenesis in diabetic rats. Life Sci. 2021;278:119605. doi:10.1016/j.lfs.2021.11960533989665
   PubMed Web of Science ®Google Scholar
• HudishLI, ReuschJE, SusselL. β cell dysfunction during progression of metabolic syndrome to type 2 diabetes. JClin Investig. 2019;129(9):4001–4008.31424428
   PubMed Web of Science ®Google Scholar
• QiY, MaJ, LiS, WL. Applicability of adipose-derived mesenchymal stem cells in treatment of patients with type 2 diabetes. Stem Cell Res Ther. 2019;10(1):274.31455405
   PubMed Web of Science ®Google Scholar
• GirijaR, ArunaS, SangeethaR. In silico molecular modelling and docking studies of sophora flavescens derived flavonoids against SGLT2 for type 2 diabetes mellitus. IntJBioinform Biol Sci. 2018;6(2):71–76.
   Google Scholar
• ShaoJ, LiuY, WangH, LuoY, ChenLJ. An integrated fecal microbiome and metabolomics in T2DM rats reveal antidiabetes effects from host-microbial metabolic axis of EtOAc extract from Sophora flavescens. Oxid Med Cell Longev. 2020;2020:1–25. doi:10.1155/2020/1805418
   Web of Science ®Google Scholar
• HuangY, HaoJ, TianD, etal. Antidiabetic activity of a flavonoid-rich extract from Sophora davidii (Franch.) Skeels in KK-Ay mice via activation of AMP-activated protein kinase. Front Pharmacol. 2018;9:760.30061831
   PubMed Web of Science ®Google Scholar
• MatsuzakaT, ShimanoHJ. New perspective on type 2 diabetes, dyslipidemia and non‐alcoholic fatty liver disease. JDiabetes Investig. 2020;11(3):532–534.
   Web of Science ®Google Scholar
• KawanamiD, MatobaK, UtsunomiyaK. Dyslipidemia in diabetic nephropathy. Renal Replacement Ther. 2016;2(1):16. doi:10.1186/s41100-016-0028-0
   Google Scholar
• BurkhardtRJ. Hyperlipidemia and cardiovascular disease: new insights on lipoprotein (a). Curr Opin Lipidol. 2019;30(3):260–261.31045609
   PubMed Web of Science ®Google Scholar
• QuispeR, MartinSS, JonesSR. Triglycerides to high-density lipoprotein–cholesterol ratio, glycemic control and cardiovascular risk in obese patients with type 2 diabetes. Diabetes Obes. 2016;23(2):150–156.
   Google Scholar
• FerenceBA, KasteleinJJ, RayKK, etal. Association of triglyceride-lowering LPL variants and LDL-C–lowering LDLR variants with risk of coronary heart disease. JAMA. 2019;321(4):364–373.30694319
   PubMed Web of Science ®Google Scholar
• XuY, HeZ, KingGL. Introduction of hyperglycemia and dyslipidemia in the pathogenesis of diabetic vascular complications. Curr Diabetes Rep. 2005;5(2):91–97.
   Google Scholar
• ErejuwaOO, NwobodoNN, AkpanJL, etal. Nigerian honey ameliorates hyperglycemia and dyslipidemia in alloxan-induced diabetic rats. Nutrients. 2016;8(3):95. doi:10.3390/nu803009526927161
   PubMed Web of Science ®Google Scholar
• IrondiEA, ObohG, AkindahunsiAA. Antidiabetic effects of Mangifera indica Kernel Flour-supplemented diet in streptozotocin-induced type 2 diabetes in rats. Food Sci Nutr. 2016;4(6):828–839. doi:10.1002/fsn3.34827826432
   PubMed Web of Science ®Google Scholar
• HiranoT. Abnormal lipoprotein metabolism in diabetic nephropathy. Clin Exp Nephrol. 2014;18(2):206–209. doi:10.1007/s10157-013-0880-y24132562
   PubMed Web of Science ®Google Scholar
• KimHY, JeongDM, JungHJ, JungYJ, YokozawaT, ChoiJS. Hypolipidemic effects of Sophora flavescens and its constituents in poloxamer 407-induced hyperlipidemic and cholesterol-fed rats. Biol Pharm Bull. 2008;31(1):73–78. doi:10.1248/bpb.31.7318175945
   PubMed Web of Science ®Google Scholar
• Al-SawalhaNA, AlSariRR, KhabourOF, AlzoubiKH. Influence of prenatal waterpipe tobacco smoke exposure on renal biomarkers in adult offspring rats. Inhal Toxicol. 2019;31(5):171–179. doi:10.1080/08958378.2019.162489731179778
   PubMed Web of Science ®Google Scholar
• SeverinMJ, CampagnoRV, BrandoniA, TorresAM. Time evolution of methotrexate-induced kidney injury: acomparative study between different biomarkers of renal damage in rats. Clin Exp Pharmacol Physiol. 2019;46(9):828–836. doi:10.1111/1440-1681.1312231187885
   PubMed Web of Science ®Google Scholar
• WenW, LinY, TiZ. Antidiabetic, antihyperlipidemic, antioxidant, anti-inflammatory activities of ethanolic seed extract of Annona reticulata L.in streptozotocin induced diabetic rats. Front Endocrinol (Lausanne). 2019;10:716. doi:10.3389/fendo.2019.0071631708869
   PubMed Web of Science ®Google Scholar
• DuniA, LiakopoulosV, RoumeliotisS, PeschosD, DounousiE. Oxidative stress in the pathogenesis and evolution of chronic kidney disease: untangling Ariadne’s thread. IntJMol Sci. 2019;20(15):3711. doi:10.3390/ijms20153711
   Web of Science ®Google Scholar
• LeeSJ, KangJS, KimHM, etal. CCR2 knockout ameliorates obesity-induced kidney injury through inhibiting oxidative stress and ER stress. PLoS One. 2019;14(9):e0222352. doi:10.1371/journal.pone.022235231498850
   PubMed Web of Science ®Google Scholar
• AlotaibiMF, Bin-JumahM, ElgebalyH, MahmoudAM, MahmoudAM. Olea europaea leaf extract up-regulates Nrf2/ARE/HO-1 signaling and attenuates cyclophosphamide-induced oxidative stress, inflammation and apoptosis in rat kidney. Biomed Pharmacother. 2019;111:676–685. doi:10.1016/j.biopha.2018.12.11230611992
   PubMed Web of Science ®Google Scholar
• AbdelhalimMAK, QaidHA, Al-MohyYH, GhannamMM. The protective roles of vitamin eand α-lipoic acid against nephrotoxicity, lipid peroxidation, and inflammatory damage induced by gold nanoparticles. IntJNanomedicine. 2020;15:729–734. doi:10.2147/IJN.S192740
   PubMed Web of Science ®Google Scholar
• ParkWS, ParkMS, KangSW, etal. Hesperidin shows protective effects on renal function in ischemia-induced acute kidney injury (Sprague-Dawley Rats). Transplant Proc. 2019;51(8):2838–2841. doi:10.1016/j.transproceed.2019.02.05531493919
   PubMed Web of Science ®Google Scholar
• MaheshwariR, BalaramanR, SenAK, ShuklaD, SethA. Effect of concomitant administration of coenzyme Q10 with sitagliptin on experimentally induced diabetic nephropathy in rats. Ren Fail. 2017;39(1):130–139. doi:10.1080/0886022X.2016.125465927841100
   PubMed Web of Science ®Google Scholar
• JungHJ, KangSS, WooJJ, ChoiJS. Anew lavandulylated flavonoid with free radical and ONOO- scavenging activities from Sophora flavescens. Arch Pharm Res. 2005;28(12):1333–1336. doi:10.1007/BF0297789716392664
   PubMed Web of Science ®Google Scholar
• TsaiRT, TsaiCW, LiuSP, etal. Maackiain ameliorates 6-hydroxydopamine and SNCA pathologies by modulating the PINK1/parkin pathway in models of Parkinson’s disease in Caenorhabditis elegans and the SH-SY5Y cell line. IntJMol Sci. 2020;21(12):4455. doi:10.3390/ijms21124455
   Web of Science ®Google Scholar
• LiX, ZouY, XingJ, etal. Pretreatment with roxadustat (FG-4592) attenuates folic acid-induced kidney injury through antiferroptosis via Akt/GSK-3β/Nrf2 pathway. Oxid Med Cell Longev. 2020;2020:6286984.32051732
   PubMed Web of Science ®Google Scholar
• AshrafizadehM, AhmadiZ, SamarghandianS, etal. MicroRNA-mediated regulation of Nrf2 signaling pathway: implications in disease therapy and protection against oxidative stress. Life Sci. 2020;244:117329. doi:10.1016/j.lfs.2020.11732931954747
   PubMed Web of Science ®Google Scholar
• ChoiBH, KangKS, KwakMK. Effect of redox modulating NRF2 activators on chronic kidney disease. Molecules (Basel, Switzerland). 2014;19(8):12727–12759. doi:10.3390/molecules190812727
   PubMed Web of Science ®Google Scholar
• PedruzziLM, CardozoLF, DalepraneJB, etal. Systemic inflammation and oxidative stress in hemodialysis patients are associated with down-regulation of Nrf2. JNephrol. 2015;28(4):495–501. doi:10.1007/s40620-014-0162-025585822
   PubMed Web of Science ®Google Scholar
• TanJ, WanL, ChenX, etal. Conjugated linoleic acid ameliorates high fructose-induced hyperuricemia and renal inflammation in rats via NLRP3 inflammasome and TLR4 signaling pathway. Mol Nutr Food Res. 2019;63(12):e1801402. doi:10.1002/mnfr.20180140230913372
   PubMed Web of Science ®Google Scholar
• ZhuS, TangS, SuF. Dioscin inhibits ischemic stroke-induced inflammation through inhibition of the TLR4/MyD88/NF-κB signaling pathway in arat model. Mol Med Rep. 2018;17(1):660–666.29115455
   PubMed Web of Science ®Google Scholar
• LeeW, KuS-K, BaeJ. Anti-inflammatory effects of Baicalin, Baicalein, and Wogonin invitro and in vivo. Inflammation. 2015;38(1):110–125.25249339
   PubMed Web of Science ®Google Scholar
• KandemirFM, YildirimS, KucuklerS, CaglayanC, MahamaduA, DortbudakMB. Therapeutic efficacy of zingerone against vancomycin-induced oxidative stress, inflammation, apoptosis and aquaporin 1permeability in rat kidney. Biomed Pharmacother. 2018;105:981–991. doi:10.1016/j.biopha.2018.06.04830021393
   PubMed Web of Science ®Google Scholar
• ChenX, WeiW, LiY, HuangJ, CiX. Hesperetin relieves cisplatin-induced acute kidney injury by mitigating oxidative stress, inflammation and apoptosis. Chem Biol Interact. 2019;308:269–278. doi:10.1016/j.cbi.2019.05.04031153982
   PubMed Web of Science ®Google Scholar
• LingappanK. NF-κB in oxidative stress. Curr Opin Toxicol. 2018;7:81–86. doi:10.1016/j.cotox.2017.11.00229862377
   PubMedGoogle Scholar
• FuchsY, StellerH. Live to die another way: modes of programmedcell death and the signals emanating from dying cells. Nat Rev Mol Cell Biol. 2015;16(6):329–344. doi:10.1038/nrm399925991373
   PubMed Web of Science ®Google Scholar
• MarquesC, MegaC, GonçalvesA, etal. Sitagliptin prevents inflammation and apoptotic cell death in the kidney of type 2 diabetic animals. Mediators Inflamm. 2014;2014:538737. doi:10.1155/2014/53873724817793
   PubMed Web of Science ®Google Scholar
• KimHY, JeonH, KimH, KooS, KimS. Sophora flavescens aiton decreases MPP(+)-induced mitochondrial dysfunction in SH-SY5Y cells. Front Aging Neurosci. 2018;10:119. doi:10.3389/fnagi.2018.0011929740311
   PubMed Web of Science ®Google Scholar