Microbiome perturbation by oral vancomycin reduces plasma concentration of two gut-derived uremic solutes, indoxyl sulfate and p -cresyl sulfate, in end-stage renal disease

Nephrology Dialysis Transplantation

Volumn 32, Issue 11, 2017, Pages 1809-1817

  Nazzal, Lama ^a   Roberts, Julia ^a   Singh, Prabhjot ^a   Jhawar, Sachin ^a   Matalon, Albert ^a   Gao, Zhan ^a   Holzman, Robert ^a   Liebes, Len ^a   Blaser, Martin J ^a   Lowenstein, Jerome ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

atherosclerosis; chronic renal failure; gut microbiome; indoxyl sulfate; p cresyl sulfate

Indexed keywords

4 CRESYL SULFATE; INDICAN; RNA 16S; SULFUR DERIVATIVE; UNCLASSIFIED DRUG; VANCOMYCIN; 4-CRESOL SULFATE; ANTIINFECTIVE AGENT; BIOLOGICAL MARKER; CRESOL; SULFATE;

ADULT; AGED; ARTICLE; BLOOD LEVEL; CLINICAL ARTICLE; FECES; FEMALE; GENUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INTESTINE FLORA; MALE; MASS SPECTROMETRY; MICROBIAL DIVERSITY; MIDDLE AGED; NONHUMAN; PHYLUM; PILOT STUDY; PRIORITY JOURNAL; SINGLE DRUG DOSE; BLOOD; CHRONIC KIDNEY FAILURE; DRUG EFFECT; GENETICS; METAGENOME; MOLECULAR TYPING; ORAL DRUG ADMINISTRATION;

ADMINISTRATION, ORAL; ADULT; AGED; ANTI-BACTERIAL AGENTS; BIOMARKERS; CRESOLS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INDICAN; KIDNEY FAILURE, CHRONIC; MALE; METAGENOME; MIDDLE AGED; MOLECULAR TYPING; PILOT PROJECTS; RNA, RIBOSOMAL, 16S; SULFURIC ACID ESTERS; VANCOMYCIN;

EID: 85030989745     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfx029     Document Type: Article

References (40)

1. Vanholder R, De Smet R, Glorieux G et al. Review on uremic toxins: classification, concentration, and interindividual variability. Kidney Int 2003; 63: 1934-1943
2. Sekine T, Miyazaki H, Endou H. Molecular physiology of renal organic anion transporters. Am J Physiol Renal Physiol 2006; 290: F251-F261
3. Masereeuw R,Mutsaers HA, Toyohara T et al. The kidney and uremic toxin removal: glomerulus or tubule? Semin Nephrol 2014; 34: 191-208
4. Grantham JJ, Irwin RL, Qualizza PB et al. Fluid secretion in isolated proximal straight renal tubules. Effect of human uremic serum. J Clin Invest 1973; 52: 2441-2450
5. Marquez IO, Tambra S, Luo FY et al. Contribution of residual function to removal of protein-bound solutes in hemodialysis. Clin J Am Soc Nephrol 2011; 6: 290-296
6. Lindner A, Charra B, Sherrard DJ et al. Accelerated atherosclerosis in prolonged maintenance hemodialysis. NEngl J Med 1974; 290: 697-701
7. Sciarretta S, Valenti V, Tocci G et al. Association of renal damage with cardiovascular diseases is independent of individual cardiovascular risk profile in hypertension: data from the Italy-Developing Education and awareness on MicroAlbuminuria in patients with hypertensive Disease study. J Hypertens 2010; 28: 251-258
8. Weiner DE, Tighiouart H, Amin MG et al. Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: a pooled analysis of community-based studies. J Am SocNephrol 2004; 15: 1307-1315
9. Jhawar S, Singh P, Torres D et al. Functional genomic analysis identifies indoxyl sulfate as a major, poorly dialyzable uremic toxin in end-stage renal disease. PLoS One 2015; 10: e0118703
10. Gondouin B, Cerini C, Dou L et al. Indolic uremic solutes increase tissue factor production in endothelial cells by the aryl hydrocarbon receptor pathway. Kidney Int 2013; 84: 733-744
11. Shivanna S, Kolandaivelu K, ShasharMet al. The aryl hydrocarbon receptor is a critical regulator of tissue factor stability and an antithrombotic target in uremia. J Am Soc Nephrol 2016; 27: 189-201
12. Meijers B, Glorieux G, Poesen R et al. Nonextracorporeal methods for decreasing uremic solute concentration: a future way to go? Semin Nephrol 2014; 34: 228-243
13. Meijers BK, Evenepoel P. The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression. Nephrol Dial Transplant 2011; 26: 759-761
14. Evenepoel P, Meijers BK, Bammens BR et al. Uremic toxins originating from colonicmicrobial metabolism. Kidney Int Suppl 2009: S12-S19
15. Aronov PA, Luo FJ, Plummer NS et al. Colonic contribution to uremic solutes. J Am Soc Nephrol 2011; 22: 1769-1776
16. Meyer TW, Hostetter TH. Uremic solutes from colon microbes. Kidney Int 2012; 81: 949-954
17. Wikoff WR, Anfora AT, Liu J et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA 2009; 106: 3698-3703
18. Butler MS, Hansford KA, Blaskovich MA et al. Glycopeptide antibiotics: back to the future. J Antibiot (Tokyo) 2014; 67: 631-644
19. Yap IK, Li JV, Saric J et al. Metabonomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse. J Proteome Res 2008; 7: 3718-3728
20. Caporaso JG, Lauber CL, Walters WA et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6: 1621-1624
21. Caporaso JG, Kuczynski J, Stombaugh J et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335-336
22. Lozupone C, Lladser ME, Knights D et al. UniFrac: an effective distance metric for microbial community comparison. ISME J 2011; 5: 169-172
23. Langille MG, Zaneveld J, Caporaso JG et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013; 31: 814-821
24. Segata N, Izard J, Waldron L et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011; 12: R60
25. Suchy-Dicey AM, Laha T, Hoofnagle A et al. Tubular secretion in CKD. J Am Soc Nephrol 2016; 27: 2148-2155
26. The R Project for Statistical Computing. https://www.r-project.org
27. Bates D,M€achlerM, Bolker B et al. Fitting linearmixed-effects models using lme4. J Stat Softw 2015; 67: 1-48
28. lmerTest: Tests in Linear Mixed Effects Models. https://cran.r-project.org/ web/packages/lmerTest/index.html
29. Lenth RV. Least-squares means: the R package lsmeans. J Stat Softw 2016; 69: 1-33
30. Wong J, Piceno YM, Desantis TZ et al. Expansion of urease-and uricasecontaining, indole-and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am J Nephrol 2014; 39: 230-237
31. Dethlefsen L, Huse S, Sogin ML et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6: e280
32. Meijers BK, De Loor H, Bammens B et al. p-Cresyl sulfate and indoxyl sulfate in hemodialysis patients. Clin J AmSoc Nephrol 2009; 4: 1932-1938
33. Lowenstein J, Grantham JJ. The rebirth of interest in renal tubular function. Am J Physiol Renal Physiol 2016; 310: F1351-F1355
34. Beyenbach KW. Kidneys sans glomeruli. Am J Physiol Renal Physiol 2004; 286: F811-F827
35. Wu IW, Hsu KH, Lee CC et al. p-Cresyl sulphate and indoxyl sulphate predict progression of chronic kidney disease. Nephrol Dial Transplant 2011; 26: 938-947
36. Sekula P, Goek ON, Quaye L et al. A metabolome-wide association study of kidney function and disease in the general population. J Am Soc Nephrol 2016; 27: 1175-1188
37. Ramezani A, Raj DS. The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol 2014; 25: 657-670
38. Meijers BK, De Preter V, Verbeke K et al. p-Cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructoseenriched inulin. Nephrol Dial Transplant 2010; 25: 219-224
39. RossiM, Johnson DW,MorrisonMet al. Synbiotics Easing Renal Failure by Improving Gut Microbiology (SYNERGY): a randomized trial. Clin J Am Soc Nephrol 2016; 11: 199-201
40. Eknoyan G, Beck GJ, Cheung AK et al. Effect of dialysis dose andmembrane flux in maintenance hemodialysis. NEngl JMed 2002; 347: 2010-2019