541
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Yi-Shen-Hua-Shi regulates intestinal microbiota dysbiosis and protects against proteinuria in patients with chronic kidney disease: a randomized controlled study

, , , , ORCID Icon, , & show all
Pages 356-366 | Received 07 Aug 2023, Accepted 15 Apr 2024, Published online: 09 May 2024

References

  • Alexander M, Ang QY, Nayak RR, Bustion AE, Sandy M, Zhang B, Upadhyay V, Pollard KS, Lynch SV, Turnbaugh PJ. 2022. Human gut bacterial metabolism drives Th17 activation and colitis. Cell Host Microbe. 30(1):17–30.e9. doi:10.1016/j.chom.2021.11.001.
  • Bakris GL, Molitch M. 2014. Microalbuminuria as a risk predictor in diabetes: the continuing saga. Diabetes Care. 37(3):867–875. doi:10.2337/dc13-1870.
  • Balakrishnan B, Luckey D, Taneja V. 2019. Autoimmunity-associated gut commensals modulate gut permeability and immunity in humanized mice. Mil Med. 184(Suppl 1):529–536. doi:10.1093/milmed/usy309.
  • Barzilay JI, Buzkova P, Shlipak MG, Bansal N, Garimella P, Mukamal KJ. 2020. Hospitalization rates in older adults with albuminuria: the Cardiovascular Health Study. J Gerontol A Biol Sci Med Sci. 75(12):2426–2433. doi:10.1093/gerona/glaa020.
  • Cai YY, Huang FQ, Lao X, Lu Y, Gao X, Alolga RN, Yin K, Zhou X, Wang Y, Liu B, et al. 2022. Integrated metagenomics identifies a crucial role for trimethylamine-producing Lachnoclostridium in promoting atherosclerosis. NPJ Biofilms Microbiomes. 8(1):11. doi:10.1038/s41522-022-00273-4.
  • Chen S, Gui R, Zhou XH, Zhang JH, Jiang HY, Liu HT, Fu YF. 2022. Combined microbiome and metabolome analysis reveals a novel interplay between intestinal flora and serum metabolites in lung cancer. Front Cell Infect Microbiol. 12:885093. doi:10.3389/fcimb.2022.885093.
  • Chen X, Sun H, Jiang F, Shen Y, Li X, Hu X, Shen X, Wei P. 2020. Alteration of the gut microbiota associated with childhood obesity by 16S rRNA gene sequencing. PeerJ. 8:e8317. doi:10.7717/peerj.8317.
  • Christovich A, Luo XM. 2022. Gut microbiota, leaky gut, and autoimmune diseases. Front Immunol. 13:946248. doi:10.3389/fimmu.2022.946248.
  • Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L, Hayes RB, Ahn J. 2015. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 10(4):e0124599. doi:10.1371/journal.pone.0124599.
  • Dong Y, Xu T, Xiao G, Hu Z, Chen J. 2022. Opportunities and challenges for synthetic biology in the therapy of inflammatory bowel disease. Front Bioeng Biotechnol. 10:909591. doi:10.3389/fbioe.2022.909591.
  • Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. 2012. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 48(4):612–626. doi:10.1016/j.molcel.2012.08.033.
  • Du Y, Neng Q, Li Y, Kang Y, Guo L, Huang X, Chen M, Yang F, Hong J, Zhou S, et al. 2021. Gastrointestinal autonomic neuropathy exacerbates gut microbiota dysbiosis in adult patients with type 2 diabetes mellitus. Front Cell Infect Microbiol. 11:804733. doi:10.3389/fcimb.2021.804733.
  • Felizardo RJ, Castoldi A, Andrade-Oliveira V, Câmara NO. 2016. The microbiota and chronic kidney diseases: a double-edged sword. Clin Transl Immunol. 5(6):e86.
  • GBD Chronic Kidney Disease Collaboration. 2020. Global, regional, and national burden of chronic kidney disease, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 395(10225):709–733.
  • Huang Y, Xin W, Xiong J, Yao M, Zhang B, Zhao J. 2022. The intestinal microbiota and metabolites in the gut-kidney-heart axis of chronic kidney disease. Front Pharmacol. 13:837500. doi:10.3389/fphar.2022.837500.
  • Huang Y, Zhou J, Wang S, Xiong J, Chen Y, Liu Y, Xiao T, Li Y, He T, Li Y, et al. 2020. Indoxyl sulfate induces intestinal barrier injury through IRF1-DRP1 axis-mediated mitophagy impairment. Theranostics. 10(16):7384–7400. doi:10.7150/thno.45455.
  • Ichii O, Otsuka-Kanazawa S, Nakamura T, Ueno M, Kon Y, Chen W, Rosenberg AZ, Kopp JB. 2014. Podocyte injury caused by indoxyl sulfate, a uremic toxin and aryl-hydrocarbon receptor ligand. PLoS One. 9(9):e108448. doi:10.1371/journal.pone.0108448.
  • Jackson MA, Jeffery IB, Beaumont M, Bell JT, Clark AG, Ley RE, O’Toole PW, Spector TD, Steves CJ. 2016. Signatures of early frailty in the gut microbiota. Genome Med. 8(1):8. doi:10.1186/s13073-016-0262-7.
  • Jha V, Garcia-Garcia G, Iseki K, Li Z, Naicker S, Plattner B, Saran R, Wang AY, Yang CW. 2013. Chronic kidney disease: global dimension and perspectives. Lancet. 382(9888):260–272. doi:10.1016/S0140-6736(13)60687-X.
  • Jiang S, Xie S, Lv D, Zhang Y, Deng J, Zeng L, Chen Y. 2016. A reduction in the butyrate producing species Roseburia spp. and Faecalibacterium prausnitzii is associated with chronic kidney disease progression. Antonie Van Leeuwenhoek. 109(10):1389–1396. doi:10.1007/s10482-016-0737-y.
  • Josefsdottir KS, Baldridge MT, Kadmon CS, King KY. 2017. Antibiotics impair murine hematopoiesis by depleting the intestinal microbiota. Blood. 129(6):729–739. doi:10.1182/blood-2016-03-708594.
  • Karbach SH, Schönfelder T, Brandão I, Wilms E, Hörmann N, Jäckel S, Schüler R, Finger S, Knorr M, Lagrange J, et al. 2016. Gut microbiota promote angiotensin ii-induced arterial hypertension and vascular dysfunction. J Am Heart Assoc. 5(9):e003698. doi: 10.1161/JAHA.116.003698.
  • Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, et al. 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe. 17(5):662–671. doi:10.1016/j.chom.2015.03.005.
  • Kelly JR, Keane VO, Cryan JF, Clarke G, Dinan TG. 2019. Mood and microbes: gut to brain communication in depression. Gastroenterol Clin North Am. 48(3):389–405. doi:10.1016/j.gtc.2019.04.006.
  • Kidney Disease: Improving Global Outcomes (KDIGO) Diabetes Work Group. 2020. KDIGO 2020 clinical practice guideline for diabetes management in chronic kidney disease. Kidney Int. 98(4s):S1–s115.
  • 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.
  • Li W, Tan L, Li X, Zhang X, Wu X, Chen H, Hu L, Wang X, Luo X, Wang F, et al. 2019. Identification of a p.Trp403* nonsense variant in PHEX causing X-linked hypophosphatemia by inhibiting p38 MAPK signaling. Hum Mutat. 40(7):879–885.
  • Liang M, Zhu X, Zhang D, He W, Zhang J, Yuan S, He Q, Jin J. 2022. Yi-Shen-Hua-Shi granules inhibit diabetic nephropathy by ameliorating podocyte injury induced by macrophage-derived exosomes. Front Pharmacol. 13:962606. doi:10.3389/fphar.2022.962606.
  • Liu F, Sheng J, Hu L, Zhang B, Guo W, Wang Y, Gu Y, Jiang P, Lin H, Lydia B, et al. 2022. Salivary microbiome in chronic kidney disease: what is its connection to diabetes, hypertension, and immunity? J Transl Med. 20(1):387. doi:10.1186/s12967-022-03602-5.
  • Liu W, Luo Z, Zhou J, Sun B. 2022. Gut microbiota and antidiabetic drugs: perspectives of personalized treatment in type 2 diabetes mellitus. Front Cell Infect Microbiol. 12:853771. doi:10.3389/fcimb.2022.853771.
  • Liu Z, Li J, Liu H, Tang Y, Zhan Q, Lai W, Ao L, Meng X, Ren H, Xu D, et al. 2019. The intestinal microbiota associated with cardiac valve calcification differs from that of coronary artery disease. Atherosclerosis. 284:121–128. doi:10.1016/j.atherosclerosis.2018.11.038.
  • Lun H, Yang W, Zhao S, Jiang M, Xu M, Liu F, Wang Y. 2019. Altered gut microbiota and microbial biomarkers associated with chronic kidney disease. Microbiologyopen. 8(4):e00678. doi:10.1002/mbo3.678.
  • 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.
  • Madan S, Mehra MR. 2020. Gut dysbiosis and heart failure: navigating the universe within. Eur J Heart Fail. 22(4):629–637. doi:10.1002/ejhf.1792.
  • McDermott AJ, Huffnagle GB. 2014. The microbiome and regulation of mucosal immunity. Immunology. 142(1):24–31. doi:10.1111/imm.12231.
  • Oshi M, Sarkar J, Wu R, Tokumaru Y, Yan L, Nakagawa K, Ishibe A, Matsuyama R, Endo I, Takabe K. 2022. Intratumoral density of regulatory T cells is a predictor of host immune response and chemotherapy response in colorectal cancer. Am J Cancer Res. 12(2):490–503.
  • Ramakrishna C, Kujawski M, Chu H, Li L, Mazmanian SK, Cantin EM. 2019. Bacteroides fragilis polysaccharide A induces IL-10 secreting B and T cells that prevent viral encephalitis. Nat Commun. 10(1):2153. doi:10.1038/s41467-019-09884-6.
  • Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD, Gasbarrini A, Mele MC. 2019. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 7(1):14. doi:10.3390/microorganisms7010014.
  • Rooks MG, Garrett WS. 2016. Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 16(6):341–352. doi:10.1038/nri.2016.42.
  • Santos-Marcos JA, Haro C, Vega-Rojas A, Alcala-Diaz JF, Molina-Abril H, Leon-Acuña A, Lopez-Moreno J, Landa BB, Tena-Sempere M, Perez-Martinez P, et al. 2019. Sex differences in the gut microbiota as potential determinants of gender predisposition to disease. Mol Nutr Food Res. 63(7):e1800870.
  • Santos-Marcos JA, Rangel-Zuñiga OA, Jimenez-Lucena R, Quintana-Navarro GM, Garcia-Carpintero S, Malagon MM, Landa BB, Tena-Sempere M, Perez-Martinez P, Lopez-Miranda J, et al. 2018. Influence of gender and menopausal status on gut microbiota. Maturitas. 116:43–53. doi:10.1016/j.maturitas.2018.07.008.
  • Seldin MM, Meng Y, Qi H, Zhu W, Wang Z, Hazen SL, Lusis AJ, Shih DM. 2016. Trimethylamine N-oxide promotes vascular inflammation through signaling of mitogen-activated protein kinase and nuclear factor-κB. J Am Heart Assoc. 5(2):e002767. doi:10.1161/JAHA.115.002767.
  • Shivani S, Kao CY, Chattopadhyay A, Chen JW, Lai LC, Lin WH, Lu TP, Huang IH, Tsai MH, Teng CH, et al. 2022. Uremic toxin-producing bacteroides species prevail in the gut microbiota of Taiwanese CKD patients: an analysis using the new Taiwan microbiome baseline. Front Cell Infect Microbiol. 12:726256. doi:10.3389/fcimb.2022.726256.
  • Song M, Chan AT, Sun J. 2020. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 158(2):322–340. doi:10.1053/j.gastro.2019.06.048.
  • Su WY, Wu PY, Huang JC, Chen SC, Chang JM. 2020. Increased proteinuria is associated with increased aortic arch calcification, cardio-thoracic ratio, rapid renal progression and increased overall and cardiovascular mortality in chronic kidney disease. Int J Med Sci. 17(8):1102–1111. doi:10.7150/ijms.45470.
  • Sun M, Wu W, Chen L, Yang W, Huang X, Ma C, Chen F, Xiao Y, Zhao Y, Ma C, et al. 2018. Microbiota-derived short-chain fatty acids promote Th1 cell IL-10 production to maintain intestinal homeostasis. Nat Commun. 9(1):3555. doi:10.1038/s41467-018-05901-2.
  • Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS. 2016. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 6(1):34712. doi:10.1038/srep34712.
  • Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA, Agatisa-Boyle B, Li XS, Levison BS, Hazen SL. 2015. Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res. 116(3):448–455. doi:10.1161/CIRCRESAHA.116.305360.
  • Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. 2013. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 368(17):1575–1584. doi:10.1056/NEJMoa1109400.
  • Thota VR, Dacha S, Natarajan A, Nerad J. 2011. Eggerthella lenta bacteremia in a Crohn’s disease patient after ileocecal resection. Future Microbiol. 6(5):595–597. doi:10.2217/fmb.11.31.
  • Tilg H, Adolph TE, Gerner RR, Moschen AR. 2018. The intestinal microbiota in colorectal cancer. Cancer Cell. 33(6):954–964. doi:10.1016/j.ccell.2018.03.004.
  • Van Treuren W, Dodd D. 2020. Microbial contribution to the human metabolome: implications for health and disease. Annu Rev Pathol. 15(1):345–369. doi:10.1146/annurev-pathol-020117-043559.
  • Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, DeSantis TZ, Ni Z, Nguyen TH, Andersen GL. 2013. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 83(2):308–315. doi:10.1038/ki.2012.345.
  • Vaziri ND, Zhao YY, Pahl MV. 2016. Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment. Nephrol Dial Transplant. 31(5):737–746. doi:10.1093/ndt/gfv095.
  • Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, Vaziri ND. 2014. Expansion of urease- and uricase-containing, indole- and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am J Nephrol. 39(3):230–237. doi:10.1159/000360010.
  • 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 T, Richards EM, Pepine CJ, Raizada MK. 2018. The gut microbiota and the brain-gut-kidney axis in hypertension and chronic kidney disease. Nat Rev Nephrol. 14(7):442–456. doi:10.1038/s41581-018-0018-2.
  • Yu X, Zheng Q, He Y, Yu D, Chang G, Chen C, Bi L, Lv J, Zhao M, Lin X, et al. 2022. Associations of gut microbiota and fatty metabolism with immune thrombocytopenia. Front Med (Lausanne). 9:810612. doi:10.3389/fmed.2022.810612.
  • 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, Luo D, Lin Z, Zhou W, Rao J, Li Y, Wu J, Peng H, Lou T. 2020. Dysbiosis of gut microbiota in adult idiopathic membranous nephropathy with nephrotic syndrome. Microb Pathog. 147:104359. doi:10.1016/j.micpath.2020.104359.
  • Zhang L, Lu QY, Wu H, Cheng YL, Kang J, Xu ZG. 2023. The intestinal microbiota composition in early and late stages of diabetic kidney disease. Microbiol Spectr. 11(4):e0038223. doi:10.1128/spectrum.00382-23.
  • Zhang L, Wang F, Wang L, Wang W, Liu B, Liu J, Chen M, He Q, Liao Y, Yu X, et al. 2012. Prevalence of chronic kidney disease in China: a cross-sectional survey. Lancet. 379(9818):815–822. doi:10.1016/S0140-6736(12)60033-6.
  • Zhao J, Chan YC, He B, Duan TT, Yu ZL. 2019. A patent herbal drug Yi-Shen-Hua-Shi granule ameliorates C-BSA-induced chronic glomerulonephritis and inhabits TGFβ signaling in rats. J Ethnopharmacol. 236:258–262. doi:10.1016/j.jep.2019.02.044.
  • Zhao T, Li M, Xiang Q, Lie B, Chen D, Wang W, Li X, Xu T, Zhang X, Li Y, et al. 2022. Yishen Huashi granules ameliorated the development of diabetic nephropathy by reducing the damage of glomerular filtration barrier. Front Pharmacol. 13:872940. doi:10.3389/fphar.2022.872940.