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Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Probiotics | Review

Microbiome–metabolome reveals the contribution of gut–kidney axis on kidney disease

Authors: Yuan-Yuan Chen, Dan-Qian Chen, Lin Chen, Jing-Ru Liu, Nosratola D. Vaziri, Yan Guo, Ying-Yong Zhao

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Dysbiosis represents changes in composition and structure of the gut microbiome community (microbiome), which may dictate the physiological phenotype (health or disease). Recent technological advances and efforts in metagenomic and metabolomic analyses have led to a dramatical growth in our understanding of microbiome, but still, the mechanisms underlying gut microbiome–host interactions in healthy or diseased state remain elusive and their elucidation is in infancy. Disruption of the normal gut microbiota may lead to intestinal dysbiosis, intestinal barrier dysfunction, and bacterial translocation. Excessive uremic toxins are produced as a result of gut microbiota alteration, including indoxyl sulphate, p-cresyl sulphate, and trimethylamine-N-oxide, all implicated in the variant processes of kidney diseases development. This review focuses on the pathogenic association between gut microbiota and kidney diseases (the gut–kidney axis), covering CKD, IgA nephropathy, nephrolithiasis, hypertension, acute kidney injury, hemodialysis and peritoneal dialysis in clinic. Targeted interventions including probiotic, prebiotic and symbiotic measures are discussed for their potential of re-establishing symbiosis, and more effective strategies for the treatment of kidney diseases patients are suggested. The novel insights into the dysbiosis of the gut microbiota in kidney diseases are helpful to develop novel therapeutic strategies for preventing or attenuating kidney diseases and complications.
Literature
1.
go back to reference De Sordi L, Khanna V, Debarbieux L. The gut microbiota facilitates drifts in the genetic diversity and infectivity of bacterial viruses. Cell Host Microbe. 2017;22(801–808):e803. De Sordi L, Khanna V, Debarbieux L. The gut microbiota facilitates drifts in the genetic diversity and infectivity of bacterial viruses. Cell Host Microbe. 2017;22(801–808):e803.
3.
go back to reference Li DY, Tang WHW. Contributory role of gut microbiota and their metabolites toward cardiovascular complications in chronic kidney disease. Semin Nephrol. 2018;38:193–205.PubMedCrossRefPubMedCentral Li DY, Tang WHW. Contributory role of gut microbiota and their metabolites toward cardiovascular complications in chronic kidney disease. Semin Nephrol. 2018;38:193–205.PubMedCrossRefPubMedCentral
4.
go back to reference Afsar B, Vaziri ND, Aslan G, Tarim K, Kanbay M. Gut hormones and gut microbiota: implications for kidney function and hypertension. J Am Soc Hypertens. 2016;10:954–61.PubMedCrossRef Afsar B, Vaziri ND, Aslan G, Tarim K, Kanbay M. Gut hormones and gut microbiota: implications for kidney function and hypertension. J Am Soc Hypertens. 2016;10:954–61.PubMedCrossRef
5.
go back to reference Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y, Shi J, Zhao S, Liu W, Wang X, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23:859–68.PubMedCrossRef Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y, Shi J, Zhao S, Liu W, Wang X, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23:859–68.PubMedCrossRef
6.
go back to reference Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Manneras-Holm L, Stahlman M, Olsson LM, Serino M, Planas-Felix M, et al. Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med. 2017;23:850–8.PubMedCrossRef Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Manneras-Holm L, Stahlman M, Olsson LM, Serino M, Planas-Felix M, et al. Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med. 2017;23:850–8.PubMedCrossRef
7.
go back to reference Imhann F, Vich Vila A, Bonder MJ, Fu J, Gevers D, Visschedijk MC, Spekhorst LM, Alberts R, Franke L, van Dullemen HM, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018;67:108–19.PubMedCrossRef Imhann F, Vich Vila A, Bonder MJ, Fu J, Gevers D, Visschedijk MC, Spekhorst LM, Alberts R, Franke L, van Dullemen HM, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018;67:108–19.PubMedCrossRef
8.
go back to reference Böhm M, Schumacher H, Teo KK, Lonn EM, Mahfoud F, Mann JFE, Mancia G, Redon J, Schmieder RE, Sliwa K, et al. Achieved blood pressure and cardiovascular outcomes in high-risk patients: results from ONTARGET and TRANSCEND trials. Lancet. 2017;389:2226–37.PubMedCrossRef Böhm M, Schumacher H, Teo KK, Lonn EM, Mahfoud F, Mann JFE, Mancia G, Redon J, Schmieder RE, Sliwa K, et al. Achieved blood pressure and cardiovascular outcomes in high-risk patients: results from ONTARGET and TRANSCEND trials. Lancet. 2017;389:2226–37.PubMedCrossRef
9.
go back to reference Levin A, Tonelli M, Bonventre J, Coresh J, Donner J-A, Fogo AB, Fox CS, Gansevoort RT, Heerspink HJL, Jardine M, et al. Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy. Lancet. 2017;390:1888–917.PubMedCrossRef Levin A, Tonelli M, Bonventre J, Coresh J, Donner J-A, Fogo AB, Fox CS, Gansevoort RT, Heerspink HJL, Jardine M, et al. Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy. Lancet. 2017;390:1888–917.PubMedCrossRef
10.
go back to reference Al Khodor S, Shatat IF. Gut microbiome and kidney disease: a bidirectional relationship. Pediatr Nephrol. 2017;32:921–31.PubMedCrossRef Al Khodor S, Shatat IF. Gut microbiome and kidney disease: a bidirectional relationship. Pediatr Nephrol. 2017;32:921–31.PubMedCrossRef
11.
go back to reference Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D. Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res. 2017;179:24–37.CrossRefPubMed Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D. Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res. 2017;179:24–37.CrossRefPubMed
12.
go back to reference Ramezani A, Massy ZA, Meijers B, Evenepoel P, Vanholder R, Raj DS. Role of the gut microbiome in uremia: a potential therapeutic target. Am J Kidney Dis. 2016;67:483–98.CrossRefPubMed Ramezani A, Massy ZA, Meijers B, Evenepoel P, Vanholder R, Raj DS. Role of the gut microbiome in uremia: a potential therapeutic target. Am J Kidney Dis. 2016;67:483–98.CrossRefPubMed
13.
go back to reference Di Iorio BR, Marzocco S, Nardone L, Sirico M, De Simone E, Di Natale G, Di Micco L. Urea and impairment of the gut–kidney axis in chronic kidney disease. G Ita Nefrol. 2017;34:1–11. Di Iorio BR, Marzocco S, Nardone L, Sirico M, De Simone E, Di Natale G, Di Micco L. Urea and impairment of the gut–kidney axis in chronic kidney disease. G Ita Nefrol. 2017;34:1–11.
14.
go back to reference Ma SX, Shang YQ, Zhang HQ, Su W. Action mechanisms and therapeutic targets of renal fibrosis. J Nephrol Adv. 2018;1:4–14.CrossRef Ma SX, Shang YQ, Zhang HQ, Su W. Action mechanisms and therapeutic targets of renal fibrosis. J Nephrol Adv. 2018;1:4–14.CrossRef
15.
go back to reference Chen DQ, Hu HH, Wang YN, Feng YL, Cao G, Zhao YY. Natural products for the prevention and treatment of kidney disease. Phytomedicine. 2018;50:50–60.PubMedCrossRef Chen DQ, Hu HH, Wang YN, Feng YL, Cao G, Zhao YY. Natural products for the prevention and treatment of kidney disease. Phytomedicine. 2018;50:50–60.PubMedCrossRef
16.
go back to reference Lepage P, Leclerc MC, Joossens M, Mondot S, Blottiere HM, Raes J, Ehrlich D, Dore J. A metagenomic insight into our gut’s microbiome. Gut. 2013;62:146–58.PubMedCrossRef Lepage P, Leclerc MC, Joossens M, Mondot S, Blottiere HM, Raes J, Ehrlich D, Dore J. A metagenomic insight into our gut’s microbiome. Gut. 2013;62:146–58.PubMedCrossRef
17.
go back to reference Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 2007;35:D169–72.PubMedCrossRef Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 2007;35:D169–72.PubMedCrossRef
19.
go back to reference Zhao YY, Vaziri ND, Lin RC. Lipidomics: new insight into kidney disease. Adv Clin Chem. 2015;68:153–75.PubMedCrossRef Zhao YY, Vaziri ND, Lin RC. Lipidomics: new insight into kidney disease. Adv Clin Chem. 2015;68:153–75.PubMedCrossRef
21.
go back to reference Eghbalnia HR, Romero PR, Westler WM, Baskaran K, Ulrich EL, Markley JL. Increasing rigor in NMR-based metabolomics through validated and open source tools. Curr Opin Biotechnol. 2017;43:56–61.PubMedCrossRef Eghbalnia HR, Romero PR, Westler WM, Baskaran K, Ulrich EL, Markley JL. Increasing rigor in NMR-based metabolomics through validated and open source tools. Curr Opin Biotechnol. 2017;43:56–61.PubMedCrossRef
22.
go back to reference Zhao YY, Lin RC. UPLC-MSE application in disease biomarker discovery: the discoveries in proteomics to metabolomics. Chem Biol Interact. 2014;215:7–16.PubMedCrossRef Zhao YY, Lin RC. UPLC-MSE application in disease biomarker discovery: the discoveries in proteomics to metabolomics. Chem Biol Interact. 2014;215:7–16.PubMedCrossRef
23.
go back to reference Zhao YY, Wu SP, Liu S, Zhang Y, Lin RC. Ultra-performance liquid chromatography-mass spectrometry as a sensitive and powerful technology in lipidomic applications. Chem Biol Interact. 2014;220:181–92.PubMedCrossRef Zhao YY, Wu SP, Liu S, Zhang Y, Lin RC. Ultra-performance liquid chromatography-mass spectrometry as a sensitive and powerful technology in lipidomic applications. Chem Biol Interact. 2014;220:181–92.PubMedCrossRef
24.
go back to reference Zhao YY, Cheng XL, Vaziri ND, Liu S, Lin RC. UPLC-based metabonomic applications for discovering biomarkers of diseases in clinical chemistry. Clin Biochem. 2014;47:16–26.PubMedCrossRef Zhao YY, Cheng XL, Vaziri ND, Liu S, Lin RC. UPLC-based metabonomic applications for discovering biomarkers of diseases in clinical chemistry. Clin Biochem. 2014;47:16–26.PubMedCrossRef
25.
go back to reference Clayton TA, Baker D, Lindon JC, Everett JR, Nicholson JK. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci. 2009;106:14728.PubMedCrossRefPubMedCentral Clayton TA, Baker D, Lindon JC, Everett JR, Nicholson JK. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci. 2009;106:14728.PubMedCrossRefPubMedCentral
26.
go back to reference Zhao YY, Cheng XL, Lin RC, Wei F. Lipidomics applications for disease biomarker discovery in mammal models. Biomark Med. 2015;9:153–68.PubMedCrossRef Zhao YY, Cheng XL, Lin RC, Wei F. Lipidomics applications for disease biomarker discovery in mammal models. Biomark Med. 2015;9:153–68.PubMedCrossRef
27.
go back to reference Chen H, Miao H, Feng YL, Zhao YY, Lin RC. Metabolomics in dyslipidemia. Adv Clin Chem. 2014;66:101–19.PubMedCrossRef Chen H, Miao H, Feng YL, Zhao YY, Lin RC. Metabolomics in dyslipidemia. Adv Clin Chem. 2014;66:101–19.PubMedCrossRef
28.
go back to reference Zhao YY, Cheng XL, Lin RC. Lipidomics applications for discovering biomarkers of diseases in clinical chemistry. Int Rev Cell Mol Biol. 2014;313:1–26.PubMedCrossRef Zhao YY, Cheng XL, Lin RC. Lipidomics applications for discovering biomarkers of diseases in clinical chemistry. Int Rev Cell Mol Biol. 2014;313:1–26.PubMedCrossRef
29.
go back to reference Zhao YY, Miao H, Cheng XL, Wei F. Lipidomics: novel insight into the biochemical mechanism of lipid metabolism and dysregulation-associated disease. Chem Biol Interact. 2015;240:220–38.PubMedCrossRef Zhao YY, Miao H, Cheng XL, Wei F. Lipidomics: novel insight into the biochemical mechanism of lipid metabolism and dysregulation-associated disease. Chem Biol Interact. 2015;240:220–38.PubMedCrossRef
30.
go back to reference Wang M, Chen L, Liu D, Chen H, Tang DD, Zhao YY. Metabolomics highlights pharmacological bioactivity and biochemical mechanism of traditional Chinese medicine. Chem Biol Interact. 2017;273:133–41.PubMedCrossRef Wang M, Chen L, Liu D, Chen H, Tang DD, Zhao YY. Metabolomics highlights pharmacological bioactivity and biochemical mechanism of traditional Chinese medicine. Chem Biol Interact. 2017;273:133–41.PubMedCrossRef
31.
go back to reference Chen DQ, Chen H, Chen L, Tang DD, Miao H, Zhao YY. Metabolomic application in toxicity evaluation and toxicological biomarker identification of natural product. Chem Biol Interact. 2016;252:114–30.PubMedCrossRef Chen DQ, Chen H, Chen L, Tang DD, Miao H, Zhao YY. Metabolomic application in toxicity evaluation and toxicological biomarker identification of natural product. Chem Biol Interact. 2016;252:114–30.PubMedCrossRef
32.
go back to reference Rossi M, Johnson DW, Xu H, Carrero JJ, Pascoe E, French C, Campbell KL. Dietary protein-fiber ratio associates with circulating levels of indoxyl sulfate and p-cresyl sulfate in chronic kidney disease patients. Nutr Metab Cardiovasc Dis. 2015;25:860–5.PubMedCrossRef Rossi M, Johnson DW, Xu H, Carrero JJ, Pascoe E, French C, Campbell KL. Dietary protein-fiber ratio associates with circulating levels of indoxyl sulfate and p-cresyl sulfate in chronic kidney disease patients. Nutr Metab Cardiovasc Dis. 2015;25:860–5.PubMedCrossRef
33.
go back to reference Liang H, Dai Z, Liu N, Ji Y, Chen J, Zhang Y, Yang Y, Li J, Wu Z, Wu G. Dietary l-tryptophan modulates the structural and functional composition of the intestinal microbiome in weaned piglets. Front Microbiol. 2018;9:1736.PubMedPubMedCentralCrossRef Liang H, Dai Z, Liu N, Ji Y, Chen J, Zhang Y, Yang Y, Li J, Wu Z, Wu G. Dietary l-tryptophan modulates the structural and functional composition of the intestinal microbiome in weaned piglets. Front Microbiol. 2018;9:1736.PubMedPubMedCentralCrossRef
34.
go back to reference Vanholder R, De Smet R, Glorieux G, Argiles A, Baurmeister U, Brunet P, Clark W, Cohen G, De Deyn PP, Deppisch R, et al. Review on uremic toxins: classification, concentration, and interindividual variability. Kidney Int. 2003;63:1934–43.CrossRefPubMed Vanholder R, De Smet R, Glorieux G, Argiles A, Baurmeister U, Brunet P, Clark W, Cohen G, De Deyn PP, Deppisch R, et al. Review on uremic toxins: classification, concentration, and interindividual variability. Kidney Int. 2003;63:1934–43.CrossRefPubMed
35.
go back to reference Maciel RA, Rempel LC, Bosquetti B, Finco AB, Pecoits-Filho R, Souza WM, Stinghen AE. p-cresol but not p-cresyl sulfate stimulate MCP-1 production via NF-kappaB p65 in human vascular smooth muscle cells. J Bras Nefrol. 2016;38:153–60.PubMedCrossRef Maciel RA, Rempel LC, Bosquetti B, Finco AB, Pecoits-Filho R, Souza WM, Stinghen AE. p-cresol but not p-cresyl sulfate stimulate MCP-1 production via NF-kappaB p65 in human vascular smooth muscle cells. J Bras Nefrol. 2016;38:153–60.PubMedCrossRef
36.
go back to reference Zeisel SH, Warrier M. Trimethylamine N-oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr. 2017;37:157–81.PubMedCrossRef Zeisel SH, Warrier M. Trimethylamine N-oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr. 2017;37:157–81.PubMedCrossRef
37.
go back to reference Vaziri ND. CKD impairs barrier function and alters microbial flora of the intestine: a major link to inflammation and uremic toxicity. Curr Opin Nephrol Hypertens. 2012;21:587–92.PubMedPubMedCentralCrossRef Vaziri ND. CKD impairs barrier function and alters microbial flora of the intestine: a major link to inflammation and uremic toxicity. Curr Opin Nephrol Hypertens. 2012;21:587–92.PubMedPubMedCentralCrossRef
38.
go back to reference Vaziri ND, Goshtasbi N, Yuan J, Jellbauer S, Moradi H, Raffatellu M, Kalantar-Zadeh K. Uremic plasma impairs barrier function and depletes the tight junction protein constituents of intestinal epithelium. Am J Nephrol. 2012;36:438–43.PubMedCrossRef Vaziri ND, Goshtasbi N, Yuan J, Jellbauer S, Moradi H, Raffatellu M, Kalantar-Zadeh K. Uremic plasma impairs barrier function and depletes the tight junction protein constituents of intestinal epithelium. Am J Nephrol. 2012;36:438–43.PubMedCrossRef
39.
go back to reference Nakabayashi I, Nakamura M, Kawakami K, Ohta T, Kato I, Uchida K, Yoshida M. Effects of synbiotic treatment on serum level of p-cresol in haemodialysis patients: a preliminary study. Nephrol Dial Transplant. 2011;26:1094–8.PubMedCrossRef Nakabayashi I, Nakamura M, Kawakami K, Ohta T, Kato I, Uchida K, Yoshida M. Effects of synbiotic treatment on serum level of p-cresol in haemodialysis patients: a preliminary study. Nephrol Dial Transplant. 2011;26:1094–8.PubMedCrossRef
40.
go back to reference Odenwald MA, Turner JR. The intestinal epithelial barrier: a therapeutic target? Nat Rev Gastroenterol Hepatol. 2017;14:9–21.PubMedCrossRef Odenwald MA, Turner JR. The intestinal epithelial barrier: a therapeutic target? Nat Rev Gastroenterol Hepatol. 2017;14:9–21.PubMedCrossRef
41.
go back to reference Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr. 2011;141:769–76.PubMedCrossRef Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr. 2011;141:769–76.PubMedCrossRef
42.
go back to reference Ramezani A, Raj DS. The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol. 2014;25:657–70.PubMedCrossRef Ramezani A, Raj DS. The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol. 2014;25:657–70.PubMedCrossRef
43.
go back to reference Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology. 2007;132:1359–74.PubMedCrossRef Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology. 2007;132:1359–74.PubMedCrossRef
44.
go back to reference Vaziri ND, Yuan J, Norris K. Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease. Am J Nephrol. 2013;37:1–6.PubMedCrossRef Vaziri ND, Yuan J, Norris K. Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease. Am J Nephrol. 2013;37:1–6.PubMedCrossRef
45.
go back to reference Al-Sadi R, Boivin M, Ma T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci. 2009;14:2765–78.PubMedCentralCrossRef Al-Sadi R, Boivin M, Ma T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci. 2009;14:2765–78.PubMedCentralCrossRef
46.
go back to reference Sabatino A, Regolisti G, Brusasco I, Cabassi A, Morabito S, Fiaccadori E. Alterations of intestinal barrier and microbiota in chronic kidney disease. Nephrol Dial Transplant. 2015;30:924–33.PubMedCrossRef Sabatino A, Regolisti G, Brusasco I, Cabassi A, Morabito S, Fiaccadori E. Alterations of intestinal barrier and microbiota in chronic kidney disease. Nephrol Dial Transplant. 2015;30:924–33.PubMedCrossRef
47.
go back to reference Xu X, Su J, Diao Z, Wei W. Reduction in estimated glomerular filtration gate in patients with elevated blood urea nitrogen but normal for any other markers of kidney damage. J Nephrol Adv. 2015;1:58–61. Xu X, Su J, Diao Z, Wei W. Reduction in estimated glomerular filtration gate in patients with elevated blood urea nitrogen but normal for any other markers of kidney damage. J Nephrol Adv. 2015;1:58–61.
48.
go back to reference Ehsan A, Lone A, Sabir O, Tareef N, Riaz S, Tanvir I. Refractory anaemia with hyperoxalurea. J Nephrol Adv. 2015;1:1–5.CrossRef Ehsan A, Lone A, Sabir O, Tareef N, Riaz S, Tanvir I. Refractory anaemia with hyperoxalurea. J Nephrol Adv. 2015;1:1–5.CrossRef
49.
go back to reference Chen DQ, Feng YL, Cao G, Zhao YY. Natural products as a source for antifibrosis therapy. Trends Pharmacol Sci. 2018;39:937–52.PubMedCrossRef Chen DQ, Feng YL, Cao G, Zhao YY. Natural products as a source for antifibrosis therapy. Trends Pharmacol Sci. 2018;39:937–52.PubMedCrossRef
50.
go back to reference Wing MR, Patel SS, Ramezani A, Raj DS. Gut microbiome in chronic kidney disease. Exp Physiol. 2016;101:471–7.CrossRefPubMed Wing MR, Patel SS, Ramezani A, Raj DS. Gut microbiome in chronic kidney disease. Exp Physiol. 2016;101:471–7.CrossRefPubMed
51.
go back to reference Chaves LD, McSkimming DI, Bryniarski MA, Honan AM, Abyad S, Thomas SA, Wells S, Buck M, Sun Y, Genco RJ, et al. Chronic kidney disease, uremic milieu, and its effects on gut bacterial microbiota dysbiosis. Am J Physiol Renal Physiol. 2018;315:F487–502.PubMedCrossRefPubMedCentral Chaves LD, McSkimming DI, Bryniarski MA, Honan AM, Abyad S, Thomas SA, Wells S, Buck M, Sun Y, Genco RJ, et al. Chronic kidney disease, uremic milieu, and its effects on gut bacterial microbiota dysbiosis. Am J Physiol Renal Physiol. 2018;315:F487–502.PubMedCrossRefPubMedCentral
52.
go back to reference Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, DeSantis TZ, Ni Z, Nguyen TH, Andersen GL. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013;83:308–15.PubMedCrossRef Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, DeSantis TZ, Ni Z, Nguyen TH, Andersen GL. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013;83:308–15.PubMedCrossRef
53.
go back to reference Hida M, Aiba Y, Sawamura S, Suzuki N, Satoh T, Koga Y. Inhibition of the accumulation of uremic toxins in the blood and their precursors in the feces after oral administration of Lebenin, a lactic acid bacteria preparation, to uremic patients undergoing hemodialysis. Nephron. 1996;74:349–55.CrossRefPubMed Hida M, Aiba Y, Sawamura S, Suzuki N, Satoh T, Koga Y. Inhibition of the accumulation of uremic toxins in the blood and their precursors in the feces after oral administration of Lebenin, a lactic acid bacteria preparation, to uremic patients undergoing hemodialysis. Nephron. 1996;74:349–55.CrossRefPubMed
54.
go back to reference Lau WL, Savoj J, Nakata MB, Vaziri ND. Altered microbiome in chronic kidney disease: systemic effects of gut-derived uremic toxins. Clin Sci. 2018;132:509–22.CrossRef Lau WL, Savoj J, Nakata MB, Vaziri ND. Altered microbiome in chronic kidney disease: systemic effects of gut-derived uremic toxins. Clin Sci. 2018;132:509–22.CrossRef
55.
go back to reference Mahmoodpoor F, Rahbar Saadat Y, Barzegari A, Ardalan M, Zununi Vahed S. The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharmacother. 2017;93:412–9.PubMedCrossRef Mahmoodpoor F, Rahbar Saadat Y, Barzegari A, Ardalan M, Zununi Vahed S. The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharmacother. 2017;93:412–9.PubMedCrossRef
56.
go back to reference Sampaio-Maia B, Simoes-Silva L, Pestana M, Araujo R, Soares-Silva IJ. The role of the gut microbiome on chronic kidney disease. Adv Appl Microbiol. 2016;96:65–94.PubMedCrossRef Sampaio-Maia B, Simoes-Silva L, Pestana M, Araujo R, Soares-Silva IJ. The role of the gut microbiome on chronic kidney disease. Adv Appl Microbiol. 2016;96:65–94.PubMedCrossRef
57.
go back to reference Jiang S, Xie S, Lv D, Wang P, He H, Zhang T, Zhou Y, Lin Q, Zhou H, Jiang J, et al. Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep. 2017;7:2870.PubMedPubMedCentralCrossRef Jiang S, Xie S, Lv D, Wang P, He H, Zhang T, Zhou Y, Lin Q, Zhou H, Jiang J, et al. Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep. 2017;7:2870.PubMedPubMedCentralCrossRef
58.
go back to reference Zhao YY, Wang HL, Cheng XL, Wei F, Bai X, Lin RC, Vaziri ND. Metabolomics analysis reveals the association between lipid abnormalities and oxidative stress, inflammation, fibrosis, and Nrf2 dysfunction in aristolochic acid-induced nephropathy. Sci Rep. 2015;5:12936.PubMedPubMedCentralCrossRef Zhao YY, Wang HL, Cheng XL, Wei F, Bai X, Lin RC, Vaziri ND. Metabolomics analysis reveals the association between lipid abnormalities and oxidative stress, inflammation, fibrosis, and Nrf2 dysfunction in aristolochic acid-induced nephropathy. Sci Rep. 2015;5:12936.PubMedPubMedCentralCrossRef
59.
go back to reference Chen DQ, Chen H, Chen L, Vaziri ND, Wang M, Li XR, Zhao YY. The link between phenotype and fatty acid metabolism in advanced chronic kidney disease. Nephrol Dial Transplant. 2017;32:1154–66.PubMedCrossRef Chen DQ, Chen H, Chen L, Vaziri ND, Wang M, Li XR, Zhao YY. The link between phenotype and fatty acid metabolism in advanced chronic kidney disease. Nephrol Dial Transplant. 2017;32:1154–66.PubMedCrossRef
60.
go back to reference Wang Z, Koonen D, Hofker M, Fu JY. Gut microbiome and lipid metabolism: from associations to mechanisms. Curr Opin Lipidol. 2016;27:216–24.PubMedCrossRef Wang Z, Koonen D, Hofker M, Fu JY. Gut microbiome and lipid metabolism: from associations to mechanisms. Curr Opin Lipidol. 2016;27:216–24.PubMedCrossRef
61.
go back to reference Xu KY, Xia GH, Lu JQ, Chen MX, Zhen X, Wang S, You C, Nie J, Zhou HW, Yin J. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci Rep. 2017;7:1445.PubMedPubMedCentralCrossRef Xu KY, Xia GH, Lu JQ, Chen MX, Zhen X, Wang S, You C, Nie J, Zhou HW, Yin J. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci Rep. 2017;7:1445.PubMedPubMedCentralCrossRef
62.
go back to reference Vaziri ND, Yuan J, Nazertehrani S, Ni Z, Liu S. Chronic kidney disease causes disruption of gastric and small intestinal epithelial tight junction. Am J Nephrol. 2013;38:99–103.PubMedCrossRef Vaziri ND, Yuan J, Nazertehrani S, Ni Z, Liu S. Chronic kidney disease causes disruption of gastric and small intestinal epithelial tight junction. Am J Nephrol. 2013;38:99–103.PubMedCrossRef
63.
go back to reference Vaziri ND, Yuan J, Rahimi A, Ni Z, Said H, Subramanian VS. Disintegration of colonic epithelial tight junction in uremia: a likely cause of CKD-associated inflammation. Nephrol Dial Transplant. 2012;27:2686–93.PubMedCrossRef Vaziri ND, Yuan J, Rahimi A, Ni Z, Said H, Subramanian VS. Disintegration of colonic epithelial tight junction in uremia: a likely cause of CKD-associated inflammation. Nephrol Dial Transplant. 2012;27:2686–93.PubMedCrossRef
64.
go back to reference Rossi M, Campbell KL, Johnson DW, Stanton T, Vesey DA, Coombes JS, Weston KS, Hawley CM, McWhinney BC, Ungerer JP, Isbel N. Protein-bound uremic toxins, inflammation and oxidative stress: a cross-sectional study in stage 3–4 chronic kidney disease. Arch Med Res. 2014;45:309–17.PubMedCrossRef Rossi M, Campbell KL, Johnson DW, Stanton T, Vesey DA, Coombes JS, Weston KS, Hawley CM, McWhinney BC, Ungerer JP, Isbel N. Protein-bound uremic toxins, inflammation and oxidative stress: a cross-sectional study in stage 3–4 chronic kidney disease. Arch Med Res. 2014;45:309–17.PubMedCrossRef
65.
go back to reference Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, Vaziri ND. 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. 2014;39:230–7.PubMedCrossRef Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, Vaziri ND. 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. 2014;39:230–7.PubMedCrossRef
66.
go back to reference Zhao YY, Cheng XL, Wei F, Xiao XY, Sun WJ, Zhang Y, Lin RC. Serum metabonomics study of adenine-induced chronic renal failure in rats by ultra performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry. Biomarkers. 2012;17:48–55.PubMedCrossRef Zhao YY, Cheng XL, Wei F, Xiao XY, Sun WJ, Zhang Y, Lin RC. Serum metabonomics study of adenine-induced chronic renal failure in rats by ultra performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry. Biomarkers. 2012;17:48–55.PubMedCrossRef
67.
go back to reference Zhao YY, Cheng XL, Cui JH, Yan XR, Wei F, Bai X, Lin RC. Effect of ergosta-4,6,8(14),22-tetraen-3-one (ergone) on adenine-induced chronic renal failure rat: a serum metabonomic study based on ultra performance liquid chromatography/high-sensitivity mass spectrometry coupled with MassLynx i-FIT algorithm. Clin Chim Acta. 2012;413:1438–45.PubMedCrossRef Zhao YY, Cheng XL, Cui JH, Yan XR, Wei F, Bai X, Lin RC. Effect of ergosta-4,6,8(14),22-tetraen-3-one (ergone) on adenine-induced chronic renal failure rat: a serum metabonomic study based on ultra performance liquid chromatography/high-sensitivity mass spectrometry coupled with MassLynx i-FIT algorithm. Clin Chim Acta. 2012;413:1438–45.PubMedCrossRef
68.
go back to reference Zhao YY, Feng YL, Bai X, Tan XJ, Lin RC, Mei Q. Ultra performance liquid chromatography-based metabonomic study of therapeutic effect of the surface layer of Poria cocos on adenine-induced chronic kidney disease provides new insight into anti-fibrosis mechanism. PLoS ONE. 2013;8:e59617.PubMedPubMedCentralCrossRef Zhao YY, Feng YL, Bai X, Tan XJ, Lin RC, Mei Q. Ultra performance liquid chromatography-based metabonomic study of therapeutic effect of the surface layer of Poria cocos on adenine-induced chronic kidney disease provides new insight into anti-fibrosis mechanism. PLoS ONE. 2013;8:e59617.PubMedPubMedCentralCrossRef
69.
go back to reference Zhang ZH, Vaziri ND, Wei F, Cheng XL, Bai X, Zhao YY. An integrated lipidomics and metabolomics reveal nephroprotective effect and biochemical mechanism of Rheum officinale in chronic renal failure. Sci Rep. 2016;6:22151.PubMedPubMedCentralCrossRef Zhang ZH, Vaziri ND, Wei F, Cheng XL, Bai X, Zhao YY. An integrated lipidomics and metabolomics reveal nephroprotective effect and biochemical mechanism of Rheum officinale in chronic renal failure. Sci Rep. 2016;6:22151.PubMedPubMedCentralCrossRef
70.
go back to reference Dou F, Miao H, Wang JW, Chen L, Wang M, Chen H, Wen AD, Zhao YY. An integrated lipidomics and phenotype study reveals protective effect and biochemical mechanism of traditionally used Alisma orientale Juzepzuk in chronic renal disease. Front Pharmacol. 2018;9:53.PubMedPubMedCentralCrossRef Dou F, Miao H, Wang JW, Chen L, Wang M, Chen H, Wen AD, Zhao YY. An integrated lipidomics and phenotype study reveals protective effect and biochemical mechanism of traditionally used Alisma orientale Juzepzuk in chronic renal disease. Front Pharmacol. 2018;9:53.PubMedPubMedCentralCrossRef
71.
go back to reference Zhao YY, Zhang L, Long FY, Cheng XL, Bai X, Wei F, Lin RC. UPLC-Q-TOF/HSMS/MSE-based metabonomics for adenine-induced changes in metabolic profiles of rat faeces and intervention effects of ergosta-4,6,8(14),22-tetraen-3-one. Chem Biol Interact. 2013;201:31–8.PubMedCrossRef Zhao YY, Zhang L, Long FY, Cheng XL, Bai X, Wei F, Lin RC. UPLC-Q-TOF/HSMS/MSE-based metabonomics for adenine-induced changes in metabolic profiles of rat faeces and intervention effects of ergosta-4,6,8(14),22-tetraen-3-one. Chem Biol Interact. 2013;201:31–8.PubMedCrossRef
72.
go back to reference Zhao YY, Feng YL, Du X, Xi ZH, Cheng XL, Wei F. Diuretic activity of the ethanol and aqueous extracts of the surface layer of Poria cocos in rat. J Ethnopharmacol. 2012;144:775–8.PubMedCrossRef Zhao YY, Feng YL, Du X, Xi ZH, Cheng XL, Wei F. Diuretic activity of the ethanol and aqueous extracts of the surface layer of Poria cocos in rat. J Ethnopharmacol. 2012;144:775–8.PubMedCrossRef
73.
go back to reference Chen H, Cao G, Chen DQ, Wang M, Vaziri ND, Zhang ZH, Mao JR, Bai X, Zhao YY. Metabolomics insights into activated redox signaling and lipid metabolism dysfunction in chronic kidney disease progression. Redox Biol. 2016;10:168–78.PubMedPubMedCentralCrossRef Chen H, Cao G, Chen DQ, Wang M, Vaziri ND, Zhang ZH, Mao JR, Bai X, Zhao YY. Metabolomics insights into activated redox signaling and lipid metabolism dysfunction in chronic kidney disease progression. Redox Biol. 2016;10:168–78.PubMedPubMedCentralCrossRef
74.
go back to reference Zhang ZH, Chen H, Vaziri ND, Mao JR, Zhang L, Bai X, Zhao YY. Metabolomic signatures of chronic kidney disease of diverse etiologies in the rats and humans. J Proteome Res. 2016;15:3802–12.PubMedCrossRef Zhang ZH, Chen H, Vaziri ND, Mao JR, Zhang L, Bai X, Zhao YY. Metabolomic signatures of chronic kidney disease of diverse etiologies in the rats and humans. J Proteome Res. 2016;15:3802–12.PubMedCrossRef
75.
go back to reference Chen H, Chen L, Liu D, Chen DQ, Vaziri ND, Yu XY, Zhang L, Su W, Bai X, Zhao YY. Combined clinical phenotype and lipidomic analysis reveals the impact of chronic kidney disease on lipid metabolism. J Proteome Res. 2017;16:1566–78.PubMedCrossRef Chen H, Chen L, Liu D, Chen DQ, Vaziri ND, Yu XY, Zhang L, Su W, Bai X, Zhao YY. Combined clinical phenotype and lipidomic analysis reveals the impact of chronic kidney disease on lipid metabolism. J Proteome Res. 2017;16:1566–78.PubMedCrossRef
77.
go back to reference El Bardai G, Dami F, Hanin H, Kabbali N, Arrayhani M, Sqalli HT. Bedside lung ultrasound in the assessment of volume status in chronic hemodialysis patients. J Nephrol Adv. 2015;1:48–57. El Bardai G, Dami F, Hanin H, Kabbali N, Arrayhani M, Sqalli HT. Bedside lung ultrasound in the assessment of volume status in chronic hemodialysis patients. J Nephrol Adv. 2015;1:48–57.
78.
go back to reference Zhang ZH, Mao JR, Chen H, Su W, Zhang Y, Zhang L, Chen DQ, Zhao YY, Vaziri ND. Removal of uremic retention products by hemodialysis is coupled with indiscriminate loss of vital metabolites. Clin Biochem. 2017;50:1078–86.PubMedCrossRef Zhang ZH, Mao JR, Chen H, Su W, Zhang Y, Zhang L, Chen DQ, Zhao YY, Vaziri ND. Removal of uremic retention products by hemodialysis is coupled with indiscriminate loss of vital metabolites. Clin Biochem. 2017;50:1078–86.PubMedCrossRef
79.
go back to reference Borges NA, Barros AF, Nakao LS, Dolenga CJ, Fouque D, Mafra D. Protein-bound uremic toxins from gut microbiota and inflammatory markers in chronic kidney disease. J Ren Nutr. 2016;26:396–400.PubMedCrossRef Borges NA, Barros AF, Nakao LS, Dolenga CJ, Fouque D, Mafra D. Protein-bound uremic toxins from gut microbiota and inflammatory markers in chronic kidney disease. J Ren Nutr. 2016;26:396–400.PubMedCrossRef
80.
go back to reference Shen W-C, Liang C-J, Huang T-M, Liu C-W, Wang S-H, Young G-H, Tsai J-S, Tseng Y-C, Peng Y-S, Wu V-C, Chen Y-L. Indoxyl sulfate enhances IL-1β-induced E-selectin expression in endothelial cells in acute kidney injury by the ROS/MAPKs/NFκB/AP-1 pathway. Arch Toxicol. 2016;90:2779–92.PubMedCrossRef Shen W-C, Liang C-J, Huang T-M, Liu C-W, Wang S-H, Young G-H, Tsai J-S, Tseng Y-C, Peng Y-S, Wu V-C, Chen Y-L. Indoxyl sulfate enhances IL-1β-induced E-selectin expression in endothelial cells in acute kidney injury by the ROS/MAPKs/NFκB/AP-1 pathway. Arch Toxicol. 2016;90:2779–92.PubMedCrossRef
81.
go back to reference Crespo-Salgado J, Vehaskari VM, Stewart T, Ferris M, Zhang Q, Wang G, Blanchard EE, Taylor CM, Kallash M, Greenbaum LA, Aviles DH. Intestinal microbiota in pediatric patients with end stage renal disease: a Midwest Pediatric Nephrology Consortium study. Microbiome. 2016;4:50.PubMedPubMedCentralCrossRef Crespo-Salgado J, Vehaskari VM, Stewart T, Ferris M, Zhang Q, Wang G, Blanchard EE, Taylor CM, Kallash M, Greenbaum LA, Aviles DH. Intestinal microbiota in pediatric patients with end stage renal disease: a Midwest Pediatric Nephrology Consortium study. Microbiome. 2016;4:50.PubMedPubMedCentralCrossRef
82.
go back to reference Wang IK, Lai HC, Yu CJ, Liang CC, Chang CT, Kuo HL, Yang YF, Lin CC, Lin HH, Liu YL, et al. Real-time PCR analysis of the intestinal microbiotas in peritoneal dialysis patients. Appl Environ Microbiol. 2012;78:1107–12.PubMedPubMedCentralCrossRef Wang IK, Lai HC, Yu CJ, Liang CC, Chang CT, Kuo HL, Yang YF, Lin CC, Lin HH, Liu YL, et al. Real-time PCR analysis of the intestinal microbiotas in peritoneal dialysis patients. Appl Environ Microbiol. 2012;78:1107–12.PubMedPubMedCentralCrossRef
83.
go back to reference Szeto CC, Chow VC, Chow KM, Lai RW, Chung KY, Leung CB, Kwan BC, Li PK. Enterobacteriaceae peritonitis complicating peritoneal dialysis: a review of 210 consecutive cases. Kidney Int. 2006;69:1245–52.PubMedCrossRef Szeto CC, Chow VC, Chow KM, Lai RW, Chung KY, Leung CB, Kwan BC, Li PK. Enterobacteriaceae peritonitis complicating peritoneal dialysis: a review of 210 consecutive cases. Kidney Int. 2006;69:1245–52.PubMedCrossRef
84.
go back to reference De Angelis M, Montemurno E, Piccolo M, Vannini L, Lauriero G, Maranzano V, Gozzi G, Serrazanetti D, Dalfino G, Gobbetti M, Gesualdo L. Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS ONE. 2014;9:e99006.PubMedPubMedCentralCrossRef De Angelis M, Montemurno E, Piccolo M, Vannini L, Lauriero G, Maranzano V, Gozzi G, Serrazanetti D, Dalfino G, Gobbetti M, Gesualdo L. Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS ONE. 2014;9:e99006.PubMedPubMedCentralCrossRef
85.
go back to reference Piccolo M, De Angelis M, Lauriero G, Montemurno E, Di Cagno R, Gesualdo L, Gobbetti M. Salivary microbiota associated with immunoglobulin A nephropathy. Microb Ecol. 2015;70:557–65.PubMedCrossRef Piccolo M, De Angelis M, Lauriero G, Montemurno E, Di Cagno R, Gesualdo L, Gobbetti M. Salivary microbiota associated with immunoglobulin A nephropathy. Microb Ecol. 2015;70:557–65.PubMedCrossRef
86.
go back to reference Brito JS, Borges NA, Dolenga CJ, Carraro-Eduardo JC, Nakao LS, Mafra D. Is there a relationship between tryptophan dietary intake and plasma levels of indoxyl sulfate in chronic kidney disease patients on hemodialysis? J Bras Nefrol. 2016;38:396–402.PubMedCrossRef Brito JS, Borges NA, Dolenga CJ, Carraro-Eduardo JC, Nakao LS, Mafra D. Is there a relationship between tryptophan dietary intake and plasma levels of indoxyl sulfate in chronic kidney disease patients on hemodialysis? J Bras Nefrol. 2016;38:396–402.PubMedCrossRef
87.
go back to reference Han L, Fang X, He Y, Ruan XZ. ISN forefronts symposium 2015: IgA nephropathy, the gut microbiota, and gut–kidney crosstalk. Kidney International Reports. 2016;1:189–96.PubMedCentralCrossRef Han L, Fang X, He Y, Ruan XZ. ISN forefronts symposium 2015: IgA nephropathy, the gut microbiota, and gut–kidney crosstalk. Kidney International Reports. 2016;1:189–96.PubMedCentralCrossRef
88.
go back to reference Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 2016;6:34712.PubMedPubMedCentralCrossRef Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 2016;6:34712.PubMedPubMedCentralCrossRef
89.
go back to reference Siva S, Barrack ER, Reddy GP, Thamilselvan V, Thamilselvan S, Menon M, Bhandari M. A critical analysis of the role of gut Oxalobacter formigenes in oxalate stone disease. BJU Int. 2009;103:18–21.PubMedCrossRef Siva S, Barrack ER, Reddy GP, Thamilselvan V, Thamilselvan S, Menon M, Bhandari M. A critical analysis of the role of gut Oxalobacter formigenes in oxalate stone disease. BJU Int. 2009;103:18–21.PubMedCrossRef
90.
go back to reference Jalanka-Tuovinen J, Salonen A, Nikkila J, Immonen O, Kekkonen R, Lahti L, Palva A, de Vos WM. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS ONE. 2011;6:e23035.PubMedPubMedCentralCrossRef Jalanka-Tuovinen J, Salonen A, Nikkila J, Immonen O, Kekkonen R, Lahti L, Palva A, de Vos WM. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS ONE. 2011;6:e23035.PubMedPubMedCentralCrossRef
91.
go back to reference Ivanovski O, Drueke TB. A new era in the treatment of calcium oxalate stones? Kidney Int. 2013;83:998–1000.PubMedCrossRef Ivanovski O, Drueke TB. A new era in the treatment of calcium oxalate stones? Kidney Int. 2013;83:998–1000.PubMedCrossRef
92.
go back to reference Siener R, Bangen U, Sidhu H, Honow R, von Unruh G, Hesse A. The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int. 2013;83:1144–9.PubMedCrossRef Siener R, Bangen U, Sidhu H, Honow R, von Unruh G, Hesse A. The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int. 2013;83:1144–9.PubMedCrossRef
93.
go back to reference Stern JM, Moazami S, Qiu Y, Kurland I, Chen Z, Agalliu I, Burk R, Davies KP. Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis. 2016;44:399–407.PubMedCrossRefPubMedCentral Stern JM, Moazami S, Qiu Y, Kurland I, Chen Z, Agalliu I, Burk R, Davies KP. Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis. 2016;44:399–407.PubMedCrossRefPubMedCentral
94.
go back to reference Zheng X, Zhao A, Xie G, Chi Y, Zhao L, Li H, Wang C, Bao Y, Jia W, Luther M, et al. Melamine-induced renal toxicity is mediated by the gut microbiota. Sci Transl Med. 2013;5:172ra122. Zheng X, Zhao A, Xie G, Chi Y, Zhao L, Li H, Wang C, Bao Y, Jia W, Luther M, et al. Melamine-induced renal toxicity is mediated by the gut microbiota. Sci Transl Med. 2013;5:172ra122.
95.
go back to reference Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331–40.PubMedCrossRef Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331–40.PubMedCrossRef
96.
go back to reference Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, Wu S, Liu W, Cui Q, Geng B, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5:14.PubMedPubMedCentralCrossRef Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, Wu S, Liu W, Cui Q, Geng B, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5:14.PubMedPubMedCentralCrossRef
97.
go back to reference Wanchai K, Pongchaidecha A, Chatsudthipong V, Chattipakorn SC, Chattipakorn N, Lungkaphin A. Role of gastrointestinal microbiota on kidney injury and the obese condition. Am J Med Sci. 2017;353:59–69.PubMedCrossRef Wanchai K, Pongchaidecha A, Chatsudthipong V, Chattipakorn SC, Chattipakorn N, Lungkaphin A. Role of gastrointestinal microbiota on kidney injury and the obese condition. Am J Med Sci. 2017;353:59–69.PubMedCrossRef
98.
go back to reference Poesen R, Windey K, Neven E, Kuypers D, De Preter V, Augustijns P, D’Haese P, Evenepoel P, Verbeke K, Meijers B. The influence of CKD on colonic microbial metabolism. J Am Soc Nephrol. 2016;27:1389–99.PubMedCrossRef Poesen R, Windey K, Neven E, Kuypers D, De Preter V, Augustijns P, D’Haese P, Evenepoel P, Verbeke K, Meijers B. The influence of CKD on colonic microbial metabolism. J Am Soc Nephrol. 2016;27:1389–99.PubMedCrossRef
99.
go back to reference Mafra D, Barros AF, Fouque D. Dietary protein metabolism by gut microbiota and its consequences for chronic kidney disease patients. Future Microbiol. 2013;8:1317–23.PubMedCrossRef Mafra D, Barros AF, Fouque D. Dietary protein metabolism by gut microbiota and its consequences for chronic kidney disease patients. Future Microbiol. 2013;8:1317–23.PubMedCrossRef
100.
go back to reference Ranganathan N, Ranganathan P, Friedman EA, Joseph A, Delano B, Goldfarb DS, Tam P, Rao AV, Anteyi E, Musso CG. Pilot study of probiotic dietary supplementation for promoting healthy kidney function in patients with chronic kidney disease. Adv Ther. 2010;27:634–47.PubMedCrossRef Ranganathan N, Ranganathan P, Friedman EA, Joseph A, Delano B, Goldfarb DS, Tam P, Rao AV, Anteyi E, Musso CG. Pilot study of probiotic dietary supplementation for promoting healthy kidney function in patients with chronic kidney disease. Adv Ther. 2010;27:634–47.PubMedCrossRef
101.
go back to reference Natarajan R, Pechenyak B, Vyas U, Ranganathan P, Weinberg A, Liang P, Mallappallil MC, Norin AJ, Friedman EA, Saggi SJ. Randomized controlled trial of strain-specific probiotic formulation (Renadyl) in dialysis patients. Biomed Res Int. 2014;2014:568571.PubMedPubMedCentral Natarajan R, Pechenyak B, Vyas U, Ranganathan P, Weinberg A, Liang P, Mallappallil MC, Norin AJ, Friedman EA, Saggi SJ. Randomized controlled trial of strain-specific probiotic formulation (Renadyl) in dialysis patients. Biomed Res Int. 2014;2014:568571.PubMedPubMedCentral
102.
go back to reference Vaziri ND, Zhao YY, Pahl MV. Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment. Nephrol Dial Transplant. 2016;31:737–46.PubMedCrossRef Vaziri ND, Zhao YY, Pahl MV. Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment. Nephrol Dial Transplant. 2016;31:737–46.PubMedCrossRef
103.
go back to reference Rossi M, Johnson DW, Morrison M, Pascoe EM, Coombes JS, Forbes JM, Szeto CC, McWhinney BC, Ungerer JP, Campbell KL. Synbiotics easing renal failure by improving gut microbiology (SYNERGY): a randomized trial. Clin J Am Soc Nephrol. 2016;11:223–31.PubMedPubMedCentralCrossRef Rossi M, Johnson DW, Morrison M, Pascoe EM, Coombes JS, Forbes JM, Szeto CC, McWhinney BC, Ungerer JP, Campbell KL. Synbiotics easing renal failure by improving gut microbiology (SYNERGY): a randomized trial. Clin J Am Soc Nephrol. 2016;11:223–31.PubMedPubMedCentralCrossRef
104.
go back to reference Lau WL, Kalantar-Zadeh K, Vaziri ND. The gut as a source of inflammation in chronic kidney disease. Nephron. 2015;130:92–8.PubMedCrossRef Lau WL, Kalantar-Zadeh K, Vaziri ND. The gut as a source of inflammation in chronic kidney disease. Nephron. 2015;130:92–8.PubMedCrossRef
105.
go back to reference Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G Jr, Goh YJ, Hamaker B, Martens EC, Mills DA, Rastal RA, et al. Prebiotics: why definitions matter. Curr Opin Biotechnol. 2016;37:1–7.PubMedCrossRef Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G Jr, Goh YJ, Hamaker B, Martens EC, Mills DA, Rastal RA, et al. Prebiotics: why definitions matter. Curr Opin Biotechnol. 2016;37:1–7.PubMedCrossRef
106.
go back to reference Meijers BK, De Preter V, Verbeke K, Vanrenterghem Y, Evenepoel P. p-Cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin. Nephrol Dial Transplant. 2010;25:219–24.PubMedCrossRef Meijers BK, De Preter V, Verbeke K, Vanrenterghem Y, Evenepoel P. p-Cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin. Nephrol Dial Transplant. 2010;25:219–24.PubMedCrossRef
107.
go back to reference Vaziri ND, Liu SM, Lau WL, Khazaeli M, Nazertehrani S, Farzaneh SH, Kieffer DA, Adams SH, Martin RJ. High amylose resistant starch diet ameliorates oxidative stress, inflammation, and progression of chronic kidney disease. PLoS ONE. 2014;9:e114881.PubMedPubMedCentralCrossRef Vaziri ND, Liu SM, Lau WL, Khazaeli M, Nazertehrani S, Farzaneh SH, Kieffer DA, Adams SH, Martin RJ. High amylose resistant starch diet ameliorates oxidative stress, inflammation, and progression of chronic kidney disease. PLoS ONE. 2014;9:e114881.PubMedPubMedCentralCrossRef
108.
go back to reference Kieffer DA, Piccolo BD, Vaziri ND, Liu S, Lau WL, Khazaeli M, Nazertehrani S, Moore ME, Marco ML, Martin RJ, Adams SH. Resistant starch alters gut microbiome and metabolomic profiles concurrent with amelioration of chronic kidney disease in rats. Am J Physiol Renal Physiol. 2016;310:F857–71.PubMedPubMedCentralCrossRef Kieffer DA, Piccolo BD, Vaziri ND, Liu S, Lau WL, Khazaeli M, Nazertehrani S, Moore ME, Marco ML, Martin RJ, Adams SH. Resistant starch alters gut microbiome and metabolomic profiles concurrent with amelioration of chronic kidney disease in rats. Am J Physiol Renal Physiol. 2016;310:F857–71.PubMedPubMedCentralCrossRef
109.
go back to reference Sirich TL, Plummer NS, Gardner CD, Hostetter TH, Meyer TW. Effect of increasing dietary fiber on plasma levels of colon-derived solutes in hemodialysis patients. Clin J Am Soc Nephrol. 2014;9:1603–10.PubMedPubMedCentralCrossRef Sirich TL, Plummer NS, Gardner CD, Hostetter TH, Meyer TW. Effect of increasing dietary fiber on plasma levels of colon-derived solutes in hemodialysis patients. Clin J Am Soc Nephrol. 2014;9:1603–10.PubMedPubMedCentralCrossRef
110.
go back to reference Guida B, Germano R, Trio R, Russo D, Memoli B, Grumetto L, Barbato F, Cataldi M. Effect of short-term synbiotic treatment on plasma p-cresol levels in patients with chronic renal failure: a randomized clinical trial. Nutr Metab Cardiovasc Dis. 2014;24:1043–9.PubMedCrossRef Guida B, Germano R, Trio R, Russo D, Memoli B, Grumetto L, Barbato F, Cataldi M. Effect of short-term synbiotic treatment on plasma p-cresol levels in patients with chronic renal failure: a randomized clinical trial. Nutr Metab Cardiovasc Dis. 2014;24:1043–9.PubMedCrossRef
111.
go back to reference Viramontes-Horner D, Marquez-Sandoval F, Martin-del-Campo F, Vizmanos-Lamotte B, Sandoval-Rodriguez A, Armendariz-Borunda J, Garcia-Bejarano H, Renoirte-Lopez K, Garcia-Garcia G. Effect of a symbiotic gel (Lactobacillus acidophilus + Bifidobacterium lactis + inulin) on presence and severity of gastrointestinal symptoms in hemodialysis patients. J Ren Nutr. 2015;25:284–91.PubMedCrossRef Viramontes-Horner D, Marquez-Sandoval F, Martin-del-Campo F, Vizmanos-Lamotte B, Sandoval-Rodriguez A, Armendariz-Borunda J, Garcia-Bejarano H, Renoirte-Lopez K, Garcia-Garcia G. Effect of a symbiotic gel (Lactobacillus acidophilus + Bifidobacterium lactis + inulin) on presence and severity of gastrointestinal symptoms in hemodialysis patients. J Ren Nutr. 2015;25:284–91.PubMedCrossRef
Metadata
Title
Microbiome–metabolome reveals the contribution of gut–kidney axis on kidney disease
Authors
Yuan-Yuan Chen
Dan-Qian Chen
Lin Chen
Jing-Ru Liu
Nosratola D. Vaziri
Yan Guo
Ying-Yong Zhao
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-018-1756-4

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