Methods of reducing the level of indoxyl sulfate – one of the most potent protein-bound uremic toxins

References

• Adelibieke Y, Shimizu H, Muteliefu G, et al. (2012). Indoxyl sulfate induces endothelial cell senescence by increasing reactive oxygen species production and p53 activity. J Ren Nutr 22:86–9
   PubMed Web of Science ®Google Scholar
• Adijiang A, Goto S, Uramoto S, et al. (2008). Indoxyl sulfate promotes aortic calcification with expression of osteoblast-specific proteins in hypertensive rats. Nephrol Dial Transplant 23:1892–901
   PubMed Web of Science ®Google Scholar
• Akiyama Y, Kikuchi K, Saigusa D, et al. (2013). Indoxyl sulfate down-regulates SLCO4C1 transporter through up-regulation of GATA3. PloS One 8:e66518. doi:10.1371/journal.pone.0066518
   PubMed Web of Science ®Google Scholar
• Al Suleimani YM, Al Za'abi M, Ramkumar A, et al. (2015). Influence of treatment with gum acacia on renal vascular responses in a rat model of chronic kidney disease. Eur Rev Med Pharmacol Sci 19:498–506
   PubMed Web of Science ®Google Scholar
• Ali BH, Al Za'abi M, Ramkumar A, et al. (2014). Anemia in adenine-induced chronic renal failure and the influence of treatment with gum acacia thereon. Physiol Res 63:351
   PubMed Web of Science ®Google Scholar
• Ali BH, Beegam S, Al-Lawati I, et al. (2013). Comparative efficacy of three brands of gum acacia on adenine-induced chronic renal failure in rats. Physiol Res 62:47
   PubMed Web of Science ®Google Scholar
• Ali BH, Inuwa I, Za'abi A, et al. (2014). Renal and myocardial histopathology and morphometry in rats with adenine – induced chronic renal failure: influence of gum acacia . Cell Physiol Biochem 34:818–28
   PubMed Web of Science ®Google Scholar
• Ali BH, Ziada A, Blunden G. (2009). Biological effects of gum arabic: a review of some recent research . Food Chem Toxicol 47:1–8
   PubMed Web of Science ®Google Scholar
• Anraku M, Fujii T, Kondo Y, et al. (2011). Antioxidant properties of high molecular weight dietary chitosan in vitro and in vivo. Carbohydr Polym 83:501–5
   Web of Science ®Google Scholar
• Anraku M, Tomida H, Michihara A, et al. (2012). Antioxidant and renoprotective activity of chitosan in nephrectomized rats. Carbohydr Polym 89:302–4
   PubMed Web of Science ®Google Scholar
• Anraku M, Tanaka M, Hiraga A, et al. (2014). Effects of chitosan on oxidative stress and related factors in hemodialysis patients. Carbohydr Polym 112:152–7
   PubMed Web of Science ®Google Scholar
• Basile C, Libutti P, Di Turo AL, et al. (2011). Removal of uremic retention solutes in standard bicarbonate hemodialysis and long-hour slow-flow bicarbonate hemodialysis. Nephrol Dial Transplant 26:1296–303
   PubMed Web of Science ®Google Scholar
• Bergesio F, Monzani G, Guasparini A, et al. (2005). Cardiovascular risk factors in severe chronic renal failure: the role of dietary treatment. Clin Nephrol 64:103–12
   PubMed Web of Science ®Google Scholar
• Brettschneider F, Tölle M, von der Giet M, et al. (2013). Removal of protein-bound, hydrophobic uremic toxins by a combined fractionated plasma separation and adsorption technique. Artif Org 37:409–16
   PubMed Web of Science ®Google Scholar
• Cha RH, Kang SW, Park CW, et al. (2016). A randomized, controlled trial of oral intestinal sorbent ast-120 on renal function deterioration in patients with advanced renal dysfunction. Clin J Am Soc Nephrol 11:559–67
   PubMed Web of Science ®Google Scholar
• De Loor H, Meijers BK, Meyer TW, et al. (2009). Sodium octanoate to reverse indoxyl sulfate and p-cresyl sulfate albumin binding in uremic and normal serum during sample preparation followed by fluorescence liquid chromatography. J Chromatogr 1216:4684–8
   Web of Science ®Google Scholar
• De Smet R, Dhondt A, Eloot S, et al. (2007). Effect of the super-flux cellulose triacetate dialyzer membrane on the removal of non-protein-bound and protein-bound uremic solutes. Nephrol Dial Transplant 22:2006–12
   PubMed Web of Science ®Google Scholar
• Devine E, Krieter DH, Rüth M, et al. (2014). Binding affinity and capacity for the uremic toxin indoxyl sulfate. Toxins 6:416–29
   PubMed Web of Science ®Google Scholar
• Duranton F, Cohen G, De Smet R, et al. (2012). Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol 23:1258–70
   PubMed Web of Science ®Google Scholar
• Ellis RJ, Small DM, Vesey DA, et al. (2016). Indoxyl sulphate and kidney disease: causes, consequences and interventions. Nephrology (Carlton) 21:170–7
   PubMed Web of Science ®Google Scholar
• Eloot S, Vanholder R, Dequidt C, Van Biesen W. (2015). Removal of different classes of uremic toxins in APD vs CAPD: a randomized cross-over study. Perit Dial Int 35:436–42
   PubMed Web of Science ®Google Scholar
• Fagugli RM, De Smet R, Buoncristiani U, et al. (2002). Behavior of non-protein-bound and protein-bound uremic solutes during daily hemodialysis. Am J Kidney Dis 40:339–47
   PubMed Web of Science ®Google Scholar
• Gao X, Huang L, Grosjean F, et al. (2011). Low-protein diet supplemented with ketoacids reduces the severity of renal disease in 5/6 nephrectomized rats: a role for KLF15. Kidney Int 79:987–96
   PubMed Web of Science ®Google Scholar
• Gondouin B, Cerini C, Dou L, et al. (2013). Indolic uremic solutes increase tissue factor production in endothelial cells by the aryl hydrocarbon receptor pathway. Kidney Int 84:733–44
   PubMed Web of Science ®Google Scholar
• Guo X, Meng Q, Liu Q, et al. (2013). JBP485 improves gentamicin-induced acute renal failure by regulating the expression and function of Oat1 and Oat3 in rats. Toxicol Appl Pharmacol 271:285–95
   PubMed Web of Science ®Google Scholar
• Hyun HS, Paik KH, Cho HY. (2013). p-Cresyl sulfate and indoxyl sulfate in pediatric patients on chronic dialysis. Korean J Pediatr 56:159–64
   PubMedGoogle Scholar
• Iida S, Kohno K, Yoshimura J, et al. (2006). Carbonic-adsorbent AST-120 reduces overload of indoxyl sulfate and the plasma level of TGF-beta1 in patients with chronic renal failure. Clin Exp Nephrol 10:262–7
   PubMedGoogle Scholar
• Ito S, Higuchi Y, Yagi Y, et al. (2013). Reduction of indoxyl sulfate by AST-120 attenuates monocyte inflammation related to chronic kidney disease. J Leukoc Biol 93:837–45
   PubMed Web of Science ®Google Scholar
• Itoh Y, Ezawa A, Kikuchi K, et al. (2012). Protein-bound uremic toxins in hemodialysis patients measured by liquid chromatography/tandem mass spectrometry and their effects on endothelial ROS production. Anal Bioanal Chem 403:1841–50
   PubMed Web of Science ®Google Scholar
• Iwasaki Y, Yamato H, Nii-Kono T, et al. (2006). Administration of oral charcoal adsorbent (AST-120) suppresses low-turnover bone progression in uraemic rats. Nephrol Dial Transplant 21:2768–74
   PubMed Web of Science ®Google Scholar
• Kim YH, Kwak KA, Gil HW, et al. (2013). Indoxyl sulfate promotes apoptosis in cultured osteoblast cells. BMC Pharmacol Toxicol 14:60. doi:10.1186/2050-6511-14-60
   PubMed Web of Science ®Google Scholar
• Krieter DH, Hackl A, Rodriguez A, et al. (2010). Protein-bound uremic toxin removal in hemodialysis and post-dilution haemodiafiltration. Nephrol Dial Transplant 25:212–8
   PubMed Web of Science ®Google Scholar
• Lauri K, Arund J, Tanner R, et al. (2010). Behavior of uremic toxins and UV absorbance in respect to low and high flux dialyzers. Estonian J Eng 16:95–106
   Google Scholar
• Ledebo I. (1998). Principles and practice of hemofiltration and hemodiafiltration. Artif Organs 22:20–5
   PubMed Web of Science ®Google Scholar
• Lee CT, Kuo CC, Chen YM, et al. (2010). Factors associated with blood concentrations of indoxyl sulfate and p-cresol in patients undergoing peritoneal dialysis. Perit Dial Int 30:456–63
   PubMed Web of Science ®Google Scholar
• Lee CT, Hsu CY, Tain YL, et al. (2014). Effects of AST-120 on blood concentrations of protein-bound uremic toxins and biomarkers of cardiovascular risk in chronic dialysis patients. Blood Purif 37:76–83
   PubMed Web of Science ®Google Scholar
• Lesaffer G, De Smet R, Lameire N, et al. (2000). Intradialytic removal of protein-bound uremic toxins: role of solute characteristics and of dialyzer membrane. Nephrol Dial Transplant 15:50–7
   PubMed Web of Science ®Google Scholar
• Lin CJ, Chen HH, Pan CF, et al. (2011). p-Cresylsulfate and indoxyl sulfate level at different stages of chronic kidney disease. J Clin Lab Anal 25:191–7
   PubMed Web of Science ®Google Scholar
• Liu S, Wang BH, Kompa AR, et al. (2012). Antagonists of organic anion transporters 1 and 3 ameliorate adverse cardiac remodelling induced by uremic toxin indoxyl sulfate. Int J Cardiol 158:457–8
   PubMed Web of Science ®Google Scholar
• Luo FJG, Patel KP, Marquez IO, et al. (2009). Effect of increasing dialyzer mass transfer area coefficient and dialysate flow on clearance of protein-bound solutes: a pilot crossover trial. Am J Kidney Dis 53:1042–9
   PubMed Web of Science ®Google Scholar
• Marzocco S, Dal Piaz F, Di Micco L, et al. (2013). Very low protein diet reduces indoxyl sulfate levels in chronic kidney disease. Blood Purif 35:196–201
   PubMed Web of Science ®Google Scholar
• Meert N, Eloot S, Waterloos MA, et al. (2009). Effective removal of protein-bound uremic solutes by different convective strategies: a prospective trial. Nephrol Dial Transplant 24:562–70
   PubMed Web of Science ®Google Scholar
• Meyer TW, Leeper EC, Bartlett DW, et al. (2004). Increasing dialysate flow and dialyzer mass transfer area coefficient to increase the clearance of protein-bound solutes. J Am Soc Nephrol15:1927–35
   PubMed Web of Science ®Google Scholar
• Meyer TW, Peattie JW, Miller JD, et al. (2007). Increasing the clearance of protein-bound solutes by addition of a sorbent to the dialysate. J Am Soc Nephrol18:868–74
   PubMed Web of Science ®Google Scholar
• Miyazaki T, Aoyama I, Ise M, et al. (2000). An oral sorbent reduces overload of indoxyl sulphate and gene expression of TGF-beta1 in uraemic rat kidneys . Nephrol Dial Transplant15:1773–81
   PubMed Web of Science ®Google Scholar
• Mozar A, Louvet L, Godin C, et al. (2012). Indoxyl sulfate inhibits osteoclast differentiation and function. Nephrol Dial Transplant 27:217–81
   Web of Science ®Google Scholar
• Namekawa K, Schreiber MT, Aoyagi T, Ebara M. (2014). Fabrication of zeolite–polymer composite nanofibers for removal of uremic toxins from kidney failure patients. Biomater Sci 2:674–9
   Web of Science ®Google Scholar
• Nasir O. (2013). Renal and extrarenal effects of gum arabic (Acacia senegal)-what can be learned from animal experiments? Kidney Blood Press Res 37:269–79.
   PubMed Web of Science ®Google Scholar
• Ng HY, Yisireyili M, Saito S, et al. (2014). Indoxyl sulfate downregulates expression of Mas receptor via OAT3/AhR/Stat3 pathway in proximal tubular cells. PloS One 9:e91517. doi:10.1371/journal.pone.0091517
   PubMed Web of Science ®Google Scholar
• Nii-Kono T, Iwasaki Y, Uchida M, et al. (2007). Indoxyl sulfate induces skeletal resistance to parathyroid hormone in cultured osteoblastic cells. Kidney Int 71:738–43
   PubMed Web of Science ®Google Scholar
• Nishikawa M, Ishimori N, Takada S, et al. (2015). AST-120 ameliorates lowered exercise capacity and mitochondrial biogenesis in the skeletal muscle from mice with chronic kidney disease via reducing oxidative stress. Nephrol Dial Transplant 30:934–42
   PubMed Web of Science ®Google Scholar
• Niwa T. (2010a). Indoxyl sulfate is a nephro-vascular toxin. J Renal Nutr 20:2–6
   PubMed Web of Science ®Google Scholar
• Niwa T. (2010b). Uremic toxicity of indoxyl sulfate. Nagoya J Med Sci 72:1–11
   PubMed Web of Science ®Google Scholar
• Patel KP, Luo FJG, Plummer NS, et al. (2012). The production of p-cresol sulfate and indoxyl sulfate in vegetarians versus omnivores. Clin J Am Soc Nephrol 7:982–8
   PubMed Web of Science ®Google Scholar
• Rossi M, Campbell K, Johnson D, et al. (2014). Uraemic toxins and cardiovascular disease across the chronic kidney disease spectrum: an observational study. Nutr Metab Cardiovasc Dis 24:1035–42
   PubMed Web of Science ®Google Scholar
• Rossi M, Klein K, Johnson DW, Campbell KL. (2012). Pre-, pro-, and synbiotics: do they have a role in reducing uremic toxins? A systematic review and meta-analysis. Int J Nephrol 2012:673631. doi:10.1155/2012/673631
   PubMedGoogle Scholar
• Rossi M, Campbell KL, Johnson DW. (2013). Indoxyl sulfate and p-cresyl sulfate: therapeutically modifiable nephrovascular toxins. OA Nephrol 1:13
   Google Scholar
• Rossi M, Johnson DW, Morrison M, et al. (2014). SYNbiotics Easing Renal failure by improving Gut microbiologY (SYNERGY): a protocol of placebo-controlled randomized cross-over trial. BMC Nephrol 15:1. doi:10.1186/1471-2369-15-106
   PubMed Web of Science ®Google Scholar
• Rueth M, Lemke HD, Preisinger C, et al. (2015). Guanidinylations of albumin decreased binding capacity of hydrophobic metabolites. Acta Physiol (Oxford, England) 215:13–23
   PubMed Web of Science ®Google Scholar
• Saito S, Shimizu H, Yisireyili M, et al. (2014). Indoxyl sulfate-induced activation of (pro)renin receptor is involved in expression of TGF-β1 and α-smooth muscle actin in proximal tubular cells. Endocrinology 155:1899–907
   PubMed Web of Science ®Google Scholar
• Sandeman SR, Howell CA, Phillips GJ, et al. (2005). Assessing the in vitro biocompatibility of a novel carbon device for the treatment of sepsis. Biomaterials 26:7124–31
   PubMed Web of Science ®Google Scholar
• Sandeman S, Petersson M, Wiezell S, et al. (2012). Characterizing nanoporous carbon adsorbents for biological application to chronic kidney disease. J Biomater Tissue Eng 2:40–7
   Web of Science ®Google Scholar
• Sandeman SR, Howell CA, Phillips GJ, et al. (2014). An adsorbent monolith device to augment the removal of uraemic toxins during haemodialysis. J Mater Sci Mater Med 25:1589–97
   PubMed Web of Science ®Google Scholar
• Schulman G, Agarwal R, Acharya M, et al. (2006). A multicenter, randomized, double-blind, placebo-controlled, dose-ranging study of AST-120 (Kremezin) in patients with moderate to severe CKD. Am J Kidney Dis 47:565–77
   PubMed Web of Science ®Google Scholar
• Schulman G, Berl T, Beck GJ, et al. (2015). Randomized placebo-controlled EPPIC trials of AST-120 in CKD. J Am Soc Nephrol 26:1732–46
   PubMed Web of Science ®Google Scholar
• Shimizu H, Saito S, Higashiyama Y, et al. (2013). CREB, NF-κB, and NADPH oxidase coordinately upregulate indoxyl sulfate-induced angiotensinogen expression in proximal tubular cells. Am J Physiol-Cell Physiol 304:685–92
   PubMed Web of Science ®Google Scholar
• Shimoishi K, Anraku M, Kitamura K, et al. (2007). An oral adsorbent, AST-120 protects against the progression of oxidative stress by reducing the accumulation of indoxyl sulfate in the systemic circulation in renal failure. Pharmaceut Res 24:1283–9
   PubMed Web of Science ®Google Scholar
• Six I, Gross P, Rémond MC, et al. (2015). Deleterious vascular effects of indoxyl sulfate and reversal by oral adsorbent AST-120. Atherosclerosis 243:248–56
   PubMed Web of Science ®Google Scholar
• Takayama F, Taki K, Niwa T. (2003). Bifidobacterium in gastro-resistant seamless capsule reduces serum levels of indoxyl sulfate in patients on hemodialysis. Am J Kidney Dis 41:142–5
   PubMed Web of Science ®Google Scholar
• Tange Y, Takesawa S, Yoshitake S. (2015). Dialysate with high dissolved hydrogen facilitates dissociation of indoxyl sulfate from albumin. Nephro-Urol Monthly 7:e26847. do:10.5812/numonthly.26847
   Google Scholar
• Tao X, Thijssen S, Levin N, et al. (2015). Enhanced indoxyl sulfate dialyzer clearance with the use of binding competitors. Blood Purif 39:323–30
   PubMed Web of Science ®Google Scholar
• Tao X, Thijssen S, Kotanko P, et al. (2016). Improved dialytic removal of protein-bound uremic toxins with use of albumin binding competitors: an in vitro human whole blood study. Sci Rep 6:23389. doi:10.1038/srep23389
   PubMed Web of Science ®Google Scholar
• Tattersall JE, Ward RA, EUDIAL group. (2013). Online haemodiafiltration: definition, dose quantification and safety revisited. Nephrol Dial Transplant 28:542–50
   PubMed Web of Science ®Google Scholar
• Vanholder R, De Smet R, Glorieux G, et al. (2003). Review on uremic toxins: classification, concentration, and interindividual variability. Kidney Int 63:1934–43
   PubMed Web of Science ®Google Scholar
• Watanabe H, Noguchi T, Miyamoto Y, et al. (2012). Interaction between two sulfate-conjugated uremic toxins, p-cresyl sulfate and indoxyl sulfate, during binding with human serum albumin. Drug Metab Dispos 40:1423–8
   PubMed Web of Science ®Google Scholar
• Watanabe I, Tatebe J, Namba S, et al. (2013). Activation of aryl hydrocarbon receptor mediates indoxyl sulfate-induced monocyte chemoattractant protein-1 expression in human umbilical vein endothelial cells. Circ J 77:224–30
   PubMed Web of Science ®Google Scholar
• Wernert V, Schäf O, Ghobarkar H, Denoyel R. (2005). Adsorption properties of zeolites for artificial kidney applications. Micropor Mesopor Mater 83:101–13
   Web of Science ®Google Scholar
• Wu IW, Hsu KH, Lee CC, et al. (2011). p-Cresyl sulfate and indoxyl sulfate predict progression of chronic kidney disease. Nephrol Dial Transplant 26:938–47
   PubMed Web of Science ®Google Scholar
• Yamamoto KI, Eguchi K, Kaneko I, et al. (2013). In vitro study of removal of protein-bound toxins. Blood Purif 35:51–4
   PubMed Web of Science ®Google Scholar
• Yamamoto S, Kazama JJ, Omori K, et al. (2015). Continuous reduction of protein-bound uremic toxins with improved oxidative stress by using the oral charcoal adsorbent ast-120 in hemodialysis patients. Sci Rep 5:14381. doi:10.1038/srep14381
   PubMed Web of Science ®Google Scholar
• Yang K, Xu X, Nie L, et al. (2015). Indoxyl sulfate induces oxidative stress and hypertrophy in cardiomyocytes by inhibiting the AMPK/UCP2 signaling pathway. Toxicol Lett 234:110–9
   PubMed Web of Science ®Google Scholar
• Yorioka N, Ito T, Masaki T, et al. (2002). Dose-dependent effect of an oral adsorbent, AST-120, in patients with early chronic renal failure. J Int Med Res 30:467–75
   PubMed Web of Science ®Google Scholar
• Yu M, Kim YJ, Kang DH. (2011). Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress. Clin J Am Soc Nephrol 6:30–9
   PubMed Web of Science ®Google Scholar
• Zhang QL, Rothenbacher D. (2008). Prevalence of chronic kidney disease in population-based studies: systematic review. BMC Public Health 8:117. doi:10.1186/1471-2458-8-117
   PubMed Web of Science ®Google Scholar