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Review Article

Traditional Chinese medicine improved diabetic kidney disease through targeting gut microbiota

, , , , , & show all
Pages 423-435 | Received 05 Dec 2023, Accepted 30 Apr 2024, Published online: 17 May 2024

References

  • Ahad A, Raish M, Ahmad A, Al-Jenoobi F, Al-Mohizea A. 2018. Development and biological evaluation of vesicles containing bile salt of telmisartan for the treatment of diabetic nephropathy. Artif Cells Nanomed Biotechnol. 46(sup1):532–539. doi: 10.1080/21691401.2018.1430700.
  • Ahmed S, Sparidans R, Lu J, Mihaila S, Gerritsen K, Masereeuw R. 2022. A robust, accurate, sensitive LC-MS/MS method to measure indoxyl sulfate, validated for plasma and kidney cells. Biomed Chromatogr. 36(5):e5307.
  • Alicic RZ, Rooney MT, Tuttle KR. 2017. Diabetic kidney disease: challenges, progress, and possibilities. Clin J Am Soc Nephrol. 12(12):2032–2045. doi: 10.2215/CJN.11491116.
  • Al-Obaide M, Singh R, Datta P, Rewers-Felkins K, Salguero M, Al-Obaidi I, Kottapalli K, Vasylyeva T. 2017. Gut microbiota-dependent trimethylamine-N-oxide and serum biomarkers in patients with T2DM and advanced CKD. J Clin Med. 6(9):86. doi: 10.3390/jcm6090086.
  • Anders H, Huber T, Isermann B, Schiffer M. 2018. CKD in diabetes: diabetic kidney disease versus nondiabetic kidney disease. Nat Rev Nephrol. 14(6):361–377. doi: 10.1038/s41581-018-0001-y.
  • Barrios C, Beaumont M, Pallister T, Villar J, Goodrich J, Clark A, Pascual J, Ley R, Spector T, Bell J, et al. 2015. Gut-microbiota-metabolite axis in early renal function decline. PLOS One. 10(8):e0134311. doi: 10.1371/journal.pone.0134311.
  • Cai K, Ma Y, Cai F, Huang X, Xiao L, Zhong C, Ren P, Luo Q, Chen J, Han F. 2022. Changes of gut microbiota in diabetic nephropathy and its effect on the progression of kidney injury. Endocrine. 76(2):294–303. doi: 10.1007/s12020-022-03002-1.
  • Cai T, Ye X, Li R, Chen H, Wang Y, Yong H, Pan M, Lu W, Tang Y, Miao H, et al. 2020. Resveratrol modulates the gut microbiota and inflammation to protect against diabetic nephropathy in mice. Front Pharmacol. 11:1249. doi: 10.3389/fphar.2020.01249.
  • Cao G, Miao H, Wang YN, Chen DQ, Wu XQ, Chen L, Guo Y, Zou L, Vaziri ND, Li P, et al. 2022. Intrarenal 1-methoxypyrene, an aryl hydrocarbon receptor agonist, mediates progressive tubulointerstitial fibrosis in mice. Acta Pharmacol Sin. 43(11):2929–2945. doi: 10.1038/s41401-022-00914-6.
  • Cao M, Peng Y, Lu Y, Zou Z, Chen J, Bottino R, Knoll M, Zhang H, Lin S, Pu Z, et al. 2021. Controls of hyperglycemia improves dysregulated microbiota in diabetic mice. Transplantation. 105(9):1980–1988. doi: 10.1097/TP.0000000000003603.
  • Chen Q, Ren D, Wu J, Yu H, Chen X, Wang J, Zhang Y, Liu M, Wang T. 2021. Shenyan Kangfu tablet alleviates diabetic kidney disease through ­attenuating inflammation and modulating the gut microbiota. J Nat Med. 75(1):84–98. doi: 10.1007/s11418-020-01452-3.
  • Chen Y, Chen D, Chen L, Liu J, Vaziri N, Guo Y, Zhao Y. 2019. Microbiome-metabolome reveals the contribution of gut-kidney axis on kidney disease. J Transl Med. 17(1):5. doi: 10.1186/s12967-018-1756-4.
  • Cheng X, Zhou T, He Y, Xie Y, Xu Y, Huang W. 2022. The role and mechanism of butyrate in the prevention and treatment of diabetic kidney disease. Front Microbiol. 13:961536. doi: 10.3389/fmicb.2022.961536.
  • Chi M, Ma K, Wang J, Ding Z, Li Y, Zhu S, Liang X, Zhang Q, Song L, Liu C. 2021. The immunomodulatory effect of the gut microbiota in kidney disease. J Immunol Res. 2021:5516035. doi: 10.1155/2021/5516035.
  • Chou C, Lin C, Chiu D, Chen I, Chen S. 2018. Tryptophan as a surrogate prognostic marker for diabetic nephropathy. J Diabetes Investig. 9(2):366–374. doi: 10.1111/jdi.12707.
  • Cuív P, Smith WJ, Pottenger S, Burman S, Shanahan ER, Morrison M. 2015. Isolation of genetically tractable most-wanted bacteria by metaparental mating. Sci Rep. 5(1):13282. doi: 10.1038/srep13282.
  • Dai Y, Quan J, Xiong L, Luo Y, Yi B. 2022. Probiotics improve renal function, glucose, lipids, inflammation and oxidative stress in diabetic kidney disease: a systematic review and meta-analysis. Ren Fail. 44(1):862–880. doi: 10.1080/0886022X.2022.2079522.
  • Debnath N, Kumar R, Kumar A, Mehta P, Yadav A. 2021. Gut-microbiota ­derived bioactive metabolites and their functions in host physiology. Biotechnol Genet Eng Rev. 37(2):105–153. doi: 10.1080/02648725.2021.1989847.
  • Deng L, Yang Y, Xu G. 2022. Empagliflozin ameliorates type 2 diabetes mellitus-related diabetic nephropathy via altering the gut microbiota. Biochim Biophys Acta Mol Cell Biol Lipids. 1867(12):159234. doi: 10.1016/j.bbalip.2022.159234.
  • Du Y, Yang Y, Tang G, Jia J, Zhu N, Yuan W. 2020. Butyrate alleviates diabetic kidney disease by mediating the miR-7a-5p/P311/TGF-β1 pathway. FASEB J. 34(8):10462–10475. doi: 10.1096/fj.202000431R.
  • Ellis R, Small D, Vesey D, Johnson D, Francis R, Vitetta L, Gobe G, Morais C. 2016. Indoxyl sulphate and kidney disease: causes, consequences and interventions. Nephrology. 21(3):170–177. doi: 10.1111/nep.12580.
  • Fang Q, Zheng B, Liu N, Liu J, Liu W, Huang X, Zeng X, Chen L, Li Z, Ouyang D. 2021. Trimethylamine N-oxide exacerbates renal inflammation and fibrosis in rats with diabetic kidney disease. Front Physiol. 12:682482. doi: 10.3389/fphys.2021.682482.
  • Feng Y, Cao G, Chen D, Vaziri N, Chen L, Zhang J, Wang M, Guo Y, Zhao Y. 2019. Microbiome-metabolomics reveals gut microbiota associated with glycine-conjugated metabolites and polyamine metabolism in chronic kidney disease. Cell Mol Life Sci. 76(24):4961–4978. doi: 10.1007/s00018-019-03155-9.
  • Fernandes R, Viana S, Nunes S, Reis F. 2019. Diabetic gut microbiota dysbiosis as an inflammaging and immunosenescence condition that fosters progression of retinopathy and nephropathy. Biochim Biophys Acta Mol Basis Dis. 1865(7):1876–1897. doi: 10.1016/j.bbadis.2018.09.032.
  • Fiaccadori E, Cosola C, Sabatino A. 2020. Targeting the gut for early diagnosis, prevention, and cure of diabetic kidney disease: is the phenyl sulfate story another step forward? Am J Kidney Dis. 75(1):144–147. doi: 10.1053/j.ajkd.2019.07.001.
  • Fu X, Liu Z, Zhu C, Mou H, Kong Q. 2019. Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria. Crit Rev Food Sci Nutr. 59(sup1):S130–S152. doi: 10.1080/10408398.2018.1542587.
  • Gao J, Xu K, Liu H, Liu G, Bai M, Peng C, Li T, Yin Y. 2018. Impact of the gut microbiota on intestinal immunity mediated by tryptophan metabolism. Front Cell Infect Microbiol. 8:13. doi: 10.3389/fcimb.2018.00013.
  • Gao Y, Yang R, Guo L, Wang Y, Liu W, Ai S, Woon T, Wang Z, Zhai Y, Wang Z, et al. 2021. Qing-Re-Xiao-Zheng formula modulates gut microbiota and inhibits inflammation in mice with diabetic kidney disease. Front Med. 8:719950. doi: 10.3389/fmed.2021.719950.
  • Gembillo G, Ingrasciotta Y, Crisafulli S, Luxi N, Siligato R, Santoro D, Trifirò G. 2021. Kidney disease in diabetic patients: from pathophysiology to pharmacological aspects with a focus on therapeutic inertia. Int J Mol Sci. 22(9):4824. doi: 10.3390/ijms22094824.
  • Giordano L, Mihaila S, Eslami Amirabadi H, Masereeuw R. 2021. Microphysiological systems to recapitulate the gut-kidney axis. Trends Biotechnol. 39(8):811–823. doi: 10.1016/j.tibtech.2020.12.001.
  • Gonçalves P, Araújo J, Santo J. 2018. A cross-talk between microbiota-derived short-chain fatty acids and the host mucosal immune system regulates intestinal homeostasis and inflammatory bowel disease. Inflamm Bowel Dis. 24(3):558–572. doi: 10.1093/ibd/izx029.
  • Gooding J, Cao L, Ahmed F, Mwiza J, Fernander M, Whitaker C, Acuff Z, McRitchie S, Sumner S, Ongeri E. 2019. LC-MS-based metabolomics analysis to identify meprin-β-associated changes in kidney tissue from mice with STZ-induced type 1 diabetes and diabetic kidney injury. Am J Physiol Renal Physiol. 317(4):F1034–F1046. doi: 10.1152/ajprenal.00166.2019.
  • Gradisteanu G, Stoica R, Petcu L, Picu A, Suceveanu A, Salmen T, Stefan D, Serafinceanu C, Chifiriuc M, Stoian A. 2019. Microbiota signatures in type-2 diabetic patients with chronic kidney disease – a pilot study. J Mind Med Sci. 6(1):130–136. doi: 10.22543/7674.61.P130136.
  • Gryp T, Vanholder R, Vaneechoutte M, Glorieux G. 2017. p-Cresyl sulfate. Toxins. 9(2):52. doi: 10.3390/toxins9020052.
  • Han S, Chen M, Cheng P, Zhang Z, Lu Y, Xu Y, Wang Y. 2022. A systematic review and meta-analysis of gut microbiota in diabetic kidney disease: comparisons with diabetes mellitus, non-diabetic kidney disease, and healthy individuals. Front Endocrinol. 13:1018093. doi: 10.3389/fendo.2022.1018093.
  • Han S, Song H, Cha J, Han J, Kang Y, Cha D. 2021. Farnesoid X receptor (FXR) agonist ameliorates systemic insulin resistance, dysregulation of lipid metabolism, and alterations of various organs in a type 2 diabetic kidney animal model. Acta Diabetol. 58(4):495–503. doi: 10.1007/s00592-020-01652-z.
  • Hu ZB, Lu J, Chen PP, Lu CC, Zhang JX, Li XQ, Yuan BY, Huang SJ, Ruan XZ, Liu BC, et al. 2020. Dysbiosis of intestinal microbiota mediates tubulointerstitial injury in diabetic nephropathy via the disruption of cholesterol homeostasis. Theranostics. 10(6):2803–2816. doi: 10.7150/thno.40571.
  • Huang W, Man Y, Gao C, Zhou L, Gu J, Xu H, Wan Q, Long Y, Chai L, Xu Y, et al. 2020. Short-chain fatty acids ameliorate diabetic nephropathy via GPR43-mediated inhibition of oxidative stress and NF-κB signaling. Oxid Med Cell Longev. 2020:4074832.
  • Hwang Y, Kim S, Hur K, Cha B, Kim I, Park T, Baik S, Yoon K, Lee K, Lee I, et al. 2019. Predictive factors for efficacy of AST-120 treatment in diabetic nephropathy: a prospective single-arm, open-label, multi-center study. J Korean Med Sci. 34(15):e117. doi: 10.3346/jkms.2019.34.e117.
  • Janeiro M, Ramírez M, Milagro F, Martínez J, Solas M. 2018. Implication of trimethylamine N-oxide (TMAO) in disease: potential biomarker or new therapeutic target. Nutrients. 10(10):1398. doi: 10.3390/nu10101398.
  • Jb A, In B, Bi B, Mahk C, Zbz D, Arm E. 2021. Effect of probiotics on oxidative stress and inflammatory status in diabetic nephropathy: a systematic review and meta-analysis of clinical trials. Heliyon. 7(1):e05925.
  • Jiang H, Zhang Y, Xu D, Wang Q. 2021. Probiotics ameliorates glycemic control of patients with diabetic nephropathy: a randomized clinical study. J Clin Lab Anal. 35(4):e23650.
  • Johnson EL, Heaver SL, Walters WA, Ley RE. 2017. Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes. J Mol Med. 95(1):1–8. doi: 10.1007/s00109-016-1492-2.
  • Kalagi NA, Thota RN, Stojanovski E, Alburikan KA, Garg ML. 2023. Plasma trimethylamine N-oxide levels are associated with poor kidney function in people with type 2 diabetes. Nutrients. 15(4):812. doi: 10.3390/nu15040812.
  • Kikuchi K, Saigusa D, Kanemitsu Y, Matsumoto Y, Thanai P, Suzuki N, Mise K, Yamaguchi H, Nakamura T, Asaji K, et al. 2019. Gut microbiome-derived phenyl sulfate contributes to albuminuria in diabetic kidney disease. Nat Commun. 10(1):1835. doi: 10.1038/s41467-019-09735-4.
  • Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. 2016. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 165(6):1332–1345. doi: 10.1016/j.cell.2016.05.041.
  • Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F. 2015. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab. 22(6):971–982. doi: 10.1016/j.cmet.2015.10.001.
  • Krautkramer K, Fan J, Bäckhed F. 2021. Gut microbial metabolites as multi-kingdom intermediates. Nat Rev Microbiol. 19(2):77–94. doi: 10.1038/s41579-020-0438-4.
  • Kuka J, Videja M, Makrecka-Kuka M, Liepins J, Grinberga S, Sevostjanovs E, Vilks K, Liepinsh E, Dambrova M. 2020. Metformin decreases bacterial trimethylamine production and trimethylamine N-oxide levels in db/db mice. Sci Rep. 10(1):14555. doi: 10.1038/s41598-020-71470-4.
  • Kumar H, Kawai T, Akira S. 2011. Pathogen recognition by the innate immune system. Int Rev Immunol. 30(1):16–34. doi: 10.3109/08830185.2010.529976.
  • La Reau AJ, Suen G. 2018. The Ruminococci: key symbionts of the gut ecosystem. J Microbiol. 56(3):199–208. doi: 10.1007/s12275-018-8024-4.
  • Larsen JM. 2017. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology. 151(4):363–374. doi: 10.1111/imm.12760.
  • Lau W, Chang Y, Vaziri N. 2021. The consequences of altered microbiota in immune-related chronic kidney disease. Nephrol Dial Transplant. 36(10):1791–1798. doi: 10.1093/ndt/gfaa087.
  • Lee GT, Ha H, Jung M, Li H, Hong SW, Cha BS, Lee HC, Cho YD. 2003. Delayed treatment with lithospermate B attenuates experimental diabetic renal injury. J Am Soc Nephrol. 14(3):709–720. doi: 10.1097/01.asn.0000051660.82593.19.
  • Lehto M, Groop P. 2018. The gut-kidney axis: putative interconnections between gastrointestinal and renal disorders. Front Endocrinol. 9:553. doi: 10.3389/fendo.2018.00553.
  • Leong S, Sirich T. 2016. Indoxyl sulfate-review of toxicity and therapeutic strategies. Toxins. 8(12):358. doi: 10.3390/toxins8120358.
  • Li L, Tao S, Ma L, Fu P. 2019. Roles of short-chain fatty acids in kidney diseases. Chin Med J. 132(10):1228–1232. doi: 10.1097/CM9.0000000000000228.
  • Li Y, Qin GQ, Wang WY, Liu X, Gao XQ, Liu JH, Zheng T, Zhang W, Cheng L, Yang K, et al. 2022. Short chain fatty acids for the risk of diabetic nephropathy in type 2 diabetes patients. Acta Diabetol. 59(7):901–909. doi: 10.1007/s00592-022-01870-7.
  • Li Y, Su X, Gao Y, Lv C, Gao Z, Liu Y, Wang Y, Li S, Wang Z. 2020b. The potential role of the gut microbiota in modulating renal function in experimental diabetic nephropathy murine models established in same environment. Biochim Biophys Acta Mol Basis Dis. 1866(6):165764. doi: 10.1016/j.bbadis.2020.165764.
  • Li YJ, Chen X, Kwan TK, Loh YW, Singer J, Liu Y, Ma J, Tan J, Macia L, Mackay CR, et al. 2020a. Dietary fiber protects against diabetic nephropathy through short-chain fatty acid-mediated activation of G protein-coupled receptors GPR43 and GPR109A. J Am Soc Nephrol. 31(6):1267–1281. doi: 10.1681/ASN.2019101029.
  • Lin JR, Wang ZT, Sun JJ, Yang YY, Li XX, Wang XR, Shi Y, Zhu YY, Wang RT, Wang MN, et al. 2022. Gut microbiota and diabetic kidney diseases: pathogenesis and therapeutic perspectives. World J Diabetes. 13(4):308–318. doi: 10.4239/wjd.v13.i4.308.
  • Liu J, Gao LD, Fu B, Yang HT, Zhang L, Che SQ, Xu Y, Du X, Liu ZC, Xue Y, et al. 2022. Efficacy and safety of Zicuiyin decoction on diabetic kidney disease: a multicenter, randomized controlled trial. Phytomedicine. 100:154079. doi: 10.1016/j.phymed.2022.154079.
  • Liu J, Miao H, Deng D, Vaziri N, Li P, Zhao Y. 2021. Gut microbiota-derived tryptophan metabolism mediates renal fibrosis by aryl hydrocarbon receptor signaling activation. Cell Mol Life Sci. 78(3):909–922. doi: 10.1007/s00018-020-03645-1.
  • Lopes R, Balbino K, Jorge M, Ribeiro A, Martino H, Alfenas R. 2018. Modulation of intestinal microbiota, control of nitrogen products and inflammation by pre/probiotics in chronic kidney disease: a systematic review. Nutr Hosp. 35(3):722–730. doi: 10.20960/nh.1642.
  • Lu C, Hu Z, Wang R, Hong Z, Lu J, Chen P, Zhang J, Li X, Yuan B, Huang S, et al. 2020. Gut microbiota dysbiosis-induced activation of the intrarenal renin-angiotensin system is involved in kidney injuries in rat diabetic nephropathy. Acta Pharmacol Sin. 41(8):1111–1118. doi: 10.1038/s41401-019-0326-5.
  • Lu C, Ma K, Ruan X, Liu B. 2018. Intestinal dysbiosis activates renal renin-angiotensin system contributing to incipient diabetic nephropathy. Int J Med Sci. 15(8):816–822. doi: 10.7150/ijms.25543.
  • Lu J, Chen P, Zhang J, Li X, Wang G, Yuan B, Huang S, Liu X, Jiang T, Wang M, et al. 2021. GPR43 deficiency protects against podocyte insulin resistance in diabetic nephropathy through the restoration of AMPKα activity. Theranostics. 11(10):4728–4742. doi: 10.7150/thno.56598.
  • Luo LP, Suo P, Ren LL, Liu HJ, Zhang Y, Zhao YY. 2021. Shenkang injection and its three anthraquinones ameliorates renal fibrosis by simultaneous targeting IƙB/NF-ƙB and Keap1/Nrf2 signaling pathways. Front Pharmacol. 12:800522. doi: 10.3389/fphar.2021.800522.
  • Lv Q, Li Z, Sui A, Yang X, Han Y, Yao R. 2022. The role and mechanisms of gut microbiota in diabetic nephropathy, diabetic retinopathy and cardiovascular diseases. Front Microbiol. 13:977187. doi: 10.3389/fmicb.2022.977187.
  • Lymperopoulos A, Suster MS, Borges JI. 2022. Short-chain fatty acid receptors and cardiovascular function. Int J Mol Sci. 23(6):3303. doi: 10.3390/ijms23063303.
  • Mafi A, Namazi G, Soleimani A, Bahmani F, Aghadavod E, Asemi Z. 2018. Metabolic and genetic response to probiotics supplementation in patients with diabetic nephropathy: a randomized, double-blind, placebo-controlled trial. Food Funct. 9(9): 4763–4770. doi: 10.1039/c8fo00888d.
  • Marquardt A, Al-Dabet M, Ghosh S, Kohli S, Manoharan J, ElWakiel A, Gadi I, Bock F, Nazir S, Wang H, et al. 2017. Farnesoid X receptor agonism protects against diabetic tubulopathy: potential add-on therapy for diabetic nephropathy. J Am Soc Nephrol. 28(11):3182–3189. doi: 10.1681/ASN.2016101123.
  • Meng X, Ma J, Kang A, Kang S, Jung H, Park Y. 2020a. A novel approach based on metabolomics coupled with intestinal flora analysis and network pharmacology to explain the mechanisms of action of Bekhogainsam Decoction in the improvement of symptoms of streptozotocin-induced diabetic nephropathy in mice. Front Pharmacol. 11:633. doi: 10.3389/fphar.2020.00633.
  • Meng X, Ma J, Kang S, Jung H, Park Y. 2020b. Jowiseungki decoction affects diabetic nephropathy in mice through renal injury inhibition as evidenced by network pharmacology and gut microbiota analyses. Chin Med. 15(1):24. doi: 10.1186/s13020-020-00306-0.
  • Miao H, Zhang YM, Yu XY, Zou L, Zhao YY. 2022. Membranous nephropathy: systems biology-based novel mechanism and traditional Chinese medicine therapy. Front Pharmacol. 13:969930. doi: 10.3389/fphar.2022.969930.
  • Miraghajani M, Zaghian N, Dehkohneh A, Mirlohi M, Ghiasvand R. 2019. Probiotic soy milk consumption and renal function among type 2 diabetic patients with nephropathy: a randomized controlled clinical trial. Probiotics Antimicrob Proteins. 11(1):124–132. doi: 10.1007/s12602-017-9325-3.
  • Miraghajani M, Zaghian N, Mirlohi M, Feizi A, Ghiasvand R. 2017. The impact of probiotic soy milk consumption on oxidative stress among type 2 diabetic kidney disease patients: a randomized controlled clinical trial. J Ren Nutr. 27(5):317–324. doi: 10.1053/j.jrn.2017.04.004.
  • Mishima E, Fukuda S, Mukawa C, Yuri A, Kanemitsu Y, Matsumoto Y, Akiyama Y, Fukuda N, Tsukamoto H, Asaji K, et al. 2017. Evaluation of the impact of gut microbiota on uremic solute accumulation by a CE-TOFMS-based metabolomics approach. Kidney Int. 92(3):634–645. doi: 10.1016/j.kint.2017.02.011.
  • Moon S, Tsay JJ, Lampert H, Md Dom ZI, Kostic AD, Smiles A, Niewczas MA. 2021. Circulating short and medium chain fatty acids are associated with normoalbuminuria in type 1 diabetes of long duration. Sci Rep. 11(1):8592. doi: 10.1038/s41598-021-87585-1.
  • Moravejolahkami AR, Kermani M, Zehi ZB, Mirenayat S, Mansourian M. 2021. The effect of probiotics on lipid profile & anthropometric indices in diabetic nephropathy; a systematic review and meta-analysis of clinical trials. J Diabetes Metab Disord. 20(1):893–904. doi: 10.1007/s40200-021-00765-8.
  • Mosterd C, Kanbay M, van den Born B, van Raalte D, Rampanelli E. 2021. Intestinal microbiota and diabetic kidney diseases: the role of microbiota and derived metabolites inmodulation of renal inflammation and disease progression. Best Pract Res Clin Endocrinol Metab. 35(3):101484. doi: 10.1016/j.beem.2021.101484.
  • Nagase N, Ikeda Y, Tsuji A, Kitagishi Y, Matsuda S. 2022. Efficacy of probiotics on the modulation of gut microbiota in the treatment of diabetic nephropathy. World J Diabetes. 13(3):150–160. doi: 10.4239/wjd.v13.i3.150.
  • Navid MA, Zahra ED, Hamid T, Reza SC, Alireza S, Zatollah A. 2019. The effects of probiotic honey consumption on metabolic status in patients with diabetic nephropathy: a randomized, double-blind, controlled trial. Probiotics Antimicrob Proteins. 11:1195–1201.
  • Ni Y, Zheng L, Nan S, Ke L, Fu Z, Jin J. 2022. Enterorenal crosstalks in diabetic nephropathy and novel therapeutics targeting the gut microbiota. Acta Biochim Biophys Sin. 54(10):1406–1420. doi: 10.3724/abbs.2022140.
  • Oliphant K, Allen-Vercoe E. 2019. Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome. 7(1):91. doi: 10.1186/s40168-019-0704-8.
  • Patel D, Bose M, Cooper M. 2020. Glucose and blood pressure-dependent pathways-the progression of diabetic kidney disease. Int J Mol Sci. 21(6):2218. doi: 10.3390/ijms21062218.
  • Paul P, Kaul R, Chaari A. 2022. Renal health improvement in diabetes through microbiome modulation of the gut-kidney axis with biotics: a systematic and narrative review of randomized controlled trials. Int J Mol Sci. 23(23):14838. doi: 10.3390/ijms232314838.
  • Persson P, Palm F. 2017. Hypoxia-inducible factor activation in diabetic kidney disease. Curr Opin Nephrol Hypertens. 26(5):345–350. doi: 10.1097/MNH.0000000000000341.
  • Phull AR, Ali A, Rafiq M, Tahir T, Majid A, Seo SY, Park HJ. 2021. Antioxidant potential, urease and acetylcholine esterase inhibitory activity and phytochemical analysis of selected medicinal plants from the Republic of Korea. Exp Res Hypot Med. 6:51–59.
  • Pugin B, Barcik W, Westermann P, Heider A, Wawrzyniak M, Hellings P, Akdis C, O’Mahony L. 2017. A wide diversity of bacteria from the human gut produces and degrades biogenic amines. Microb Ecol Health Dis. 28(1):1353881. doi: 10.1080/16512235.2017.1353881.
  • Qi C, Mao X, Zhang Z, Wu H. 2017. Classification and differential diagnosis of diabetic nephropathy. J Diabetes Res. 2017(2017):8637138–8637137. doi: 10.1155/2017/8637138.
  • Rysz J, Franczyk B, Ławiński J, Olszewski R, Ciałkowska-Rysz A, Gluba-Brzózka A. 2021. The impact of CKD on uremic toxins and gut microbiota. Toxins. 13(4):252. doi: 10.3390/toxins13040252.
  • Saleem T, Dahpy M, Ezzat G, Abdelrahman G, Abdel-Aziz E, Farghaly R. 2019. The profile of plasma free amino acids in type 2 diabetes mellitus with insulin resistance: association with microalbuminuria and macroalbuminuria. Appl Biochem Biotechnol. 188(3):854–867. doi: 10.1007/s12010-019-02956-9.
  • Salguero M, Al-Obaide M, Singh R, Siepmann T, Vasylyeva T. 2019. Dysbiosis of gram-negative gut microbiota and the associated serum lipopolysaccharide exacerbates inflammation in type 2 diabetic patients with chronic kidney disease. Exp Ther Med. 18(5):3461–3469. doi: 10.3892/etm.2019.7943.
  • Sato E, Hosomi K, Sekimoto A, Mishima E, Oe Y, Saigusa D, Ito S, Abe T, Sato H, Kunisawa J, et al. 2020. Effects of the oral adsorbent AST-120 on fecal p-cresol and indole levels and on the gut microbiota composition. Biochem Biophys Res Commun. 525(3):773–779. doi: 10.1016/j.bbrc.2020.02.141.
  • Seong CN, Kang JW, Lee JH, Seo SY, Woo JJ, Park C, Bae KS, Kim MS. 2018. Taxonomic hierarchy of the phylum Firmicutes and novel Firmicutes species originated from various environments in Korea. J Microbiol. 56(1):1–10. doi: 10.1007/s12275-018-7318-x.
  • Shi R, Tao Y, Tang H, Wu C, Fei J, Ge H, Gu HF, Wu J. 2022. Abelmoschus manihot ameliorates the levels of circulating metabolites in diabetic nephropathy by modulating gut microbiota in non-obese diabetes mice. Microb Biotechnol. 16(4):813–826. doi: 10.1111/1751-7915.14200.
  • Singh H, Miyamoto S, Darshi M, Torralba M, Kwon K, Sharma K, Pieper R. 2020. Gut microbial changes in diabetic db/db mice and recovery of microbial diversity upon Pirfenidone treatment. Microorganisms. 8(9):1347. doi: 10.3390/microorganisms8091347.
  • Snelson M, Tan S, Higgins G, Lindblom R, Coughlan M. 2020. Exploring the role of the metabolite-sensing receptor GPR109a in diabetic nephropathy. Am J Physiol Renal Physiol. 318(3):F835–F842. doi: 10.1152/ajprenal.00505.2019.
  • Su X, Yu W, Liu A, Wang C, Li X, Gao J, Liu X, Jiang W, Yang Y, Lv S. 2021. San-Huang-Yi-Shen capsule ameliorates diabetic nephropathy in rats through modulating the gut microbiota and overall metabolism. Front Pharmacol. 12:808867. doi: 10.3389/fphar.2021.808867.
  • Sun G, Yin Z, Liu N, Bian X, Yu R, Su X, Zhang B, Wang Y. 2017. Gut microbial metabolite TMAO contributes to renal dysfunction in a mouse model of diet-induced obesity. Biochem Biophys Res Commun. 493(2):964–970. doi: 10.1016/j.bbrc.2017.09.108.
  • Tan Y, Gao Y, Teo G, Koh H, Tai E, Khoo C, Choi K, Zhou L, Choi H. 2021. Plasma metabolome and lipidome associations with type 2 diabetes and diabetic nephropathy. Metabolites. 11(4):228. doi: 10.3390/metabo11040228.
  • Tang G, Du Y, Guan H, Jia J, Zhu N, Shi Y, Rong S, Yuan W. 2022. Butyrate ameliorates skeletal muscle atrophy in diabetic nephropathy by enhancing gut barrier function and FFA2-mediated PI3K/Akt/mTOR signals. Br J Pharmacol. 179(1):159–178. doi: 10.1111/bph.15693.
  • Thomas RJ, Kim H, Maillard P, Decarli CS, Heckman EJ, Karjadi C, Fang T, Ang A, Au R. 2021. Digital sleep measures and white matter health in the Framingham Heart Study. Explor Med. 2(3):253–267. doi: 10.37349/emed.2021.00045.
  • Tofte N, Vogelzangs N, Mook-Kanamori D, Brahimaj A, Nano J, Ahmadizar F, van Dijk K, Frimodt-Møller M, Arts I, Beulens J, et al. 2020. Plasma metabolomics identifies markers of impaired renal function: a meta-analysis of 3089 persons with type 2 diabetes. J Clin Endocrinol Metab. 105(7):2275–2287. doi: 10.1210/clinem/dgaa173.
  • Toyohara T, Suzuki T, Morimoto R, Akiyama Y, Souma T, Shiwaku H, Takeuchi Y, Mishima E, Abe M, Tanemoto M, et al. 2009. SLCO4C1 transporter eliminates uremic toxins and attenuates hypertension and renal inflammation. J Am Soc Nephrol. 20(12):2546–2555. doi: 10.1681/ASN.2009070696.
  • Velasquez MT, Ramezani A, Manal A, Raj DS. 2016. Trimethylamine N-oxide: the good, the bad and the unknown. Toxins. 8(11):326. doi: 10.3390/toxins8110326.
  • Vlachou E, Ntikoudi A, Govina O, Lavdaniti M, Kotsalas N, Tsartsalis A, Dimitriadis G. 2020. Effects of probiotics on diabetic nephropathy: a systematic review. Curr Clin Pharmacol. 15(3):234–242. doi: 10.2174/1574884715666200303112753.
  • Walker A, Schmitt-Kopplin P. 2021. The role of fecal sulfur metabolome in inflammatory bowel diseases. Int J Med Microbiol. 311(5):151513. doi: 10.1016/j.ijmm.2021.151513.
  • Wang P, Wang T, Zheng X, Cui W, Shang J, Zhao Z. 2021. Gut microbiota, key to unlocking the door of diabetic kidney disease. Nephrology. 26(8):641–649. doi: 10.1111/nep.13874.
  • Wang X, Edelstein M, Gafter U, Qiu L, Luo Y, Dobrinskikh E, Lucia S, Adorini L, D’Agati V, Levi J, et al. 2016. G protein-coupled bile acid receptor TGR5 activation inhibits kidney disease in obesity and diabetes. J Am Soc Nephrol. 27(5):1362–1378. doi: 10.1681/ASN.2014121271.
  • Wang X, Wang D, Luo Y, Myakala K, Dobrinskikh E, Rosenberg A, Levi J, Kopp J, Field A, Hill A, et al. 2018. FXR/TGR5 dual agonist prevents progression of nephropathy in diabetes and obesity. J Am Soc Nephrol. 29(1):118–137. doi: 10.1681/ASN.2017020222.
  • Wang Y, Liu H, Ren L, Suo P, Zou L, Zhang Y, Yu X, Zhao Y. 2022a. Shenkang injection improves chronic kidney disease by inhibiting multiple renin-angiotensin system genes by blocking the Wnt/β-catenin signalling pathway. Front Pharmacol. 13:964370. doi: 10.3389/fphar.2022.964370.
  • Wang Y, Zhang Z, Liu H, Guo Z, Zou L, Zhang Y, Zhao Y. 2022b. Integrative phosphatidylcholine metabolism through phospholipase A2 in rats with chronic kidney disease. Acta Pharmacol Sin. 44(2):393–405. doi: 10.1038/s41401-022-00947-x.
  • Wang Y, Zhao J, Qin Y, Yu Z, Zhang Y, Ning X, Sun S. 2022c. the specific alteration of gut microbiota in diabetic kidney diseases–a systematic review and meta-analysis. Front Immunol. 13:908219. doi: 10.3389/fimmu.2022.908219.
  • Wei H, Wang L, An Z, Xie H, Liu W, Du Q, Guo Y, Wu X, Li S, Shi Y, et al. 2021. QiDiTangShen granules modulated the gut microbiome composition and improved bile acid profiles in a mouse model of diabetic nephropathy. Biomed Pharmacother. 133:111061. doi: 10.1016/j.biopha.2020.111061.
  • Wexler HM. 2007. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 20(4):593–621. doi: 10.1128/CMR.00008-07.
  • Winther S, Øllgaard J, Tofte N, Tarnow L, Wang Z, Ahluwalia T, Jorsal A, Theilade S, Parving H, Hansen T, et al. 2019. Utility of plasma concentration of trimethylamine N-oxide in predicting cardiovascular and renal complications in individuals with type 1 diabetes. Diabetes Care. 42(8):1512–1520. doi: 10.2337/dc19-0048.
  • Winther SA, Øllgaard JC, Hansen TW, von Scholten BJ, Reinhard H, Ahluwalia TS, Wang Z, Gæde P, Parving HH, Hazen S, et al. 2021. Plasma trimethylamine N-oxide and its metabolic precursors and risk of mortality, cardiovascular and renal disease in individuals with type 2-diabetes and albuminuria. PLOS One. 16(3):e0244402. doi: 10.1371/journal.pone.0244402.
  • Wu C, Fei J, Xu Q, Tao Y, Zhou Z, Wang Y, Wu J, Gu HF. 2022. Interaction between plasma metabolomics and intestinal microbiome in db/db mouse, an animal model for study of type 2 diabetes and diabetic kidney disease. Metabolites. 12(9):775. doi: 10.3390/metabo12090775.
  • Xiao H, Sun X, Liu R, Chen Z, Lin Z, Yang Y, Zhang M, Liu P, Quan S, Huang H. 2020. Gentiopicroside activates the bile acid receptor Gpbar1 (TGR5) to repress NF-kappaB pathway and ameliorate diabetic nephropathy. Pharmacol Res. 151:104559. doi: 10.1016/j.phrs.2019.104559.
  • Xu KY, Xia GH, Lu JQ, Chen MX, Zhen X, Wang S, You C, Nie J, Zhou HW, Yin J. 2017. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci Rep. 7(1):1445. doi: 10.1038/s41598-017-01387-y.
  • Yang MX, Zhang R, Zhuang CF, Wu YY, Yang Q, Yu ZY, Liu J, Zha BB, Gong QH, Yang B, et al. 2021. Serum trimethylamine N-oxide and the diversity of the intestinal microbial flora in type 2 diabetes complicated by diabetic kidney disease. Clin Lab. 68(5):2373–2382. doi: 10.7754/Clin.Lab.2021.210836.
  • Yu XY, Sun Q, Zhang YM, Zou L, Zhao YY. 2022. TGF-β/Smad signaling pathway in tubulointerstitial fibrosis. Front Pharmacol. 13:860588. doi: 10.3389/fphar.2022.860588.
  • Zaky A, Glastras SJ, Wong MYW, Pollock CA, Saad S. 2021. The role of the gut microbiome in diabetes and obesity-related kidney disease. Int J Mol Sci. 22(17):9641. doi: 10.3390/ijms22179641.
  • Zhang J, Fu Y, Li L, Liu Y, Zhang C, Yu D, Ma Y, Xiao Y. 2019. Pharmacokinetic comparisons of major bioactive components after oral administration of raw and steamed rhubarb by UPLC-MS/MS. J Pharm Biomed Anal. 171:43–51. doi: 10.1016/j.jpba.2019.04.002.
  • Zhang L, Wang Z, Zhang X, Zhao L, Chu J, Li H, Sun W, Yang C, Wang H, Dai W, et al. 2022. Alterations of the gut microbiota in patients with diabetic nephropathy. Microbiol Spectr. 10(4):e0032422. doi: 10.1128/spectrum.00324-22.
  • Zhao J, Zhang Q, Shen J, Wang K, Liu J. 2019. Magnesium lithospermate B improves the gut microbiome and bile acid metabolic profiles in a mouse model of diabetic nephropathy. Acta Pharmacol Sin. 40(4):507–513. doi: 10.1038/s41401-018-0029-3.
  • Zhao T, Zhang H, Yin X, Zhao H, Ma L, Yan M, Peng L, Wang Q, Dong X, Li P. 2020. Tangshen formula modulates gut microbiota and reduces gut-derived toxins in diabetic nephropathy rats. Biomed Pharmacother. 129:110325. doi: 10.1016/j.biopha.2020.110325.
  • Zhao YY. 2022. Recent advances of gut microbiota in chronic kidney disease patients. Explor Med. 3:260–274. doi: 10.37349/emed.2022.00090.
  • Zhong C, Bai X, Chen Q, Ma Y, Li J, Zhang J, Luo Q, Cai K. 2022. Gut microbial products valerate and caproate predict renal outcome among the patients with biopsy-confirmed diabetic nephropathy. Acta Diabetol. 59(11):1469–1477. doi: 10.1007/s00592-022-01948-2.
  • Zhong C, Dai Z, Chai L, Wu L, Li J, Guo W, Zhang J, Zhang Q, Xue C, Lin H, et al. 2021. The change of gut microbiota-derived short-chain fatty acids in diabetic kidney disease. J Clin Lab Anal. 35(12):e24062.
  • Zhou Q, Yang F, Li Z, Qu Q, Zhao C, Liu X, Yang P, Han L, Shi Y, Shi X. 2022. Paecilomyces cicadae-fermented Radix Astragali ameliorate diabetic nephropathy in mice by modulating the gut microbiota. J Med Microbiol. 71(5):1–10.