Protein-bound uremic toxins, inflammation and oxidative stress: A cross-sectional study in stage 3-4 chronic kidney disease

Archives of Medical Research

Volumn 45, Issue 4, 2014, Pages 309-317

  Rossi, Megan ^a,b,c   Campbell, Katrina L ^a,c   Johnson, David W ^a,b,c   Stanton, Tony ^a,c   Vesey, David A ^a,b   Coombes, Jeff S ^a   Weston, Kassia S ^a   Hawley, Carmel M ^a,c   McWhinney, Brett C ^d   Ungerer, Jacobus P J ^d   Isbel, Nicole ^a,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b TRANSLATIONAL RESEARCH INSTITUTE   (Australia)

^c PRINCESS ALEXANDRA HOSPITAL   (Australia)

^d Department of Cardiology Princess Alexandra Hospital ^*  (Australia)

Author keywords

Indoxyl sulfate; Inflammation; Oxidative stress; P cresyl sulfate; Uremic toxins

Indexed keywords

ALBUMIN; CHOLESTEROL; GAMMA INTERFERON; GLUTATHIONE PEROXIDASE; HEMOGLOBIN A1C; INDICAN; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOPROSTANE DERIVATIVE; P CRESYL SULFATE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UREMIC TOXIN;

ADULT; AGE; ALBUMIN BLOOD LEVEL; ARTERIAL STIFFNESS; ARTICLE; BODY HEIGHT; BODY MASS; BODY WEIGHT; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CHRONIC KIDNEY DISEASE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATIONAL STUDY; CROSS-SECTIONAL STUDY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DIASTOLIC BLOOD PRESSURE; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; GENDER; GLOMERULONEPHRITIS; GLOMERULUS FILTRATION RATE; HUMAN; HYPERTENSION; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; OBSERVATIONAL STUDY; OXIDATIVE STRESS; PULSE WAVE; REFLUX NEPHROPATHY; SYSTOLIC BLOOD PRESSURE; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

INDOXYL SULFATE; INFLAMMATION; OXIDATIVE STRESS; P-CRESYL SULFATE; UREMIC TOXINS;

AGED; ANTIOXIDANTS; BIOLOGICAL MARKERS; BLOOD PROTEINS; CARDIOVASCULAR DISEASES; CRESOLS; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; INDICAN; INFLAMMATION; INTERLEUKIN-6; MALE; MIDDLE AGED; OXIDATIVE STRESS; RENAL INSUFFICIENCY, CHRONIC; RISK REDUCTION BEHAVIOR; SULFURIC ACID ESTERS; TOXINS, BIOLOGICAL; UREMIA; VASCULAR STIFFNESS;

EID: 84901794277     PISSN: 01884409     EISSN: 18735487     Source Type: Journal    
DOI: 10.1016/j.arcmed.2014.04.002     Document Type: Article

References (46)

1. Lekawanvijit S., Kompa A.R., Wang B.H., et al. Cardiorenal syndrome: the emerging role of protein-bound uremic toxins. Circ Res 2012, 111:1470-1483.
2. Meijers B.K.I., Evenepoel P. The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression. Nephrol Dial Transplant 2011, 26:759-761.
3. Vaziri N.D., Wong J., Pahl M., et al. Chronic kidney disease alters intestinal microbial flora. Kidney Int 2013, 83:308-315.
4. Fukuuchi F., Hida M., Aiba Y., et al. Intestinal bacteria-derived putrefactants in chronic renal failure. Clin Exp Nephrol 2002, 6:99-104.
5. Evenepoel P., Meijers B.K., Bammens B.R., et al. Uremic toxins originating from colonic microbial metabolism. Kidney Int 2009, 76:S12-S19.
6. De Smet R., David F., Sandra P., et al. A sensitive HPLC method for the quantification of free and total p-cresol in patients with chronic renal failure. Clin Chim Acta 1998, 278:1-21.
7. Shimizu H., Bolati D., Adijiang A., et al. NF-kappaB plays an important role in indoxyl sulfate-induced cellular senescence, fibrotic gene expression, and inhibition of proliferation in proximal tubular cells. Am J Physiol Cell Physiol 2011, 301:C1201-C1212.
8. Watanabe H., Miyamoto Y., Honda D., et al. p-Cresyl sulfate causes renal tubular cell damage by inducing oxidative stress by activation of NADPH oxidase. Kidney Int 2013, 83:582-592.
9. Yisireyili M., Shimizu H., Saito S., et al. Indoxyl sulfate promotes cardiac fibrosis with enhanced oxidative stress in hypertensive rats. Life Sci 2013, 92:1180-1185.
10. Lekawanvijit S., Kompa A.R., Manabe M., et al. Chronic kidney disease-induced cardiac fibrosis is ameliorated by reducing circulating levels of a non-dialysable uremic toxin, indoxyl sulfate. PLoS One 2012, 7:e41281.
11. Motojima M., Hosokawa A., Yamato H., et al. Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int 2003, 63:1671-1680.
12. Yu M., Kim Y.J., Kang D.H. Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress. Clin J Am Soc Nephrol 2011, 6:30-39.
13. Barreto F.C., Barreto D.V., Liabeuf S., et al. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol 2009, 4:1551-1558.
14. Liabeuf S., Barreto D.V., Barreto F.C., et al. Free p-cresylsulphate is a predictor of mortality in patients at different stages of chronic kidney disease. Nephrol Dial Transplant 2010, 25:1183-1191.
15. Bammens B., Evenepoel P., Keuleers H., et al. Free serum concentrations of the protein-bound retention solute p-cresol predict mortality in hemodialysis patients. Kidney Int 2006, 69:1081-1087.
16. Mathew T.H., Johnson D.W., Jones G.R. Chronic kidney disease and automatic reporting of estimated glomerular filtration rate: revised recommendations. Med J Aust 2007, 187:459-463.
17. Pretorius C.J., McWhinney B.C., Sipinkoski B., et al. Reference ranges and biological variation of free and total serum indoxyl- and p-cresyl sulphate measured with a rapid UPLC fluorescence detection method. Clin Chim Acta 2013, 419:122-126.
18. Chowdhury F., Williams A., Johnson P. Validation and comparison of two multiplex technologies, Luminex and Mesoscale Discovery, for human cytokine profiling. J Immunol Methods 2009, 340:55-64.
19. Rice-Evans C., Miller N.J. Total antioxidant status in plasma and body fluids. Methods Enzymol 1994, 234:279-293.
20. Mullins A.L., van Rosendal S.P., Briskey D.R., et al. Variability in oxidative stress biomarkers following a maximal exercise test. Biomarkers 2013, 18:446-454.
21. Laurent S., Cockcroft J., Van Bortel L., et al. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 2006, 27:2588-2605.
22. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 1995, 854:1-452.
23. Levin A., Rigatto C., Brendan B., et al. Cohort profile: Canadian study of prediction of death, dialysis and interim cardiovascular events (CanPREDDICT). BMC Nephrol 2013, 14:121.
24. Sun C.Y., Hsu H.H., Wu M.S. p-Cresol sulfate and indoxyl sulfate induce similar cellular inflammatory gene expressions in cultured proximal renal tubular cells. Nephrol Dial Transplant 2012, 28:70-78.
25. Pecoits-Filho R., Barany P., Lindholm B., et al. Interleukin-6 is an independent predictor of mortality in patients starting dialysis treatment. Nephrol Dial Transplant 2002, 17:1684-1688.
26. Kanda T., Takahashi T. Interleukin-6 and cardiovascular diseases. Jpn Heart J 2004, 45:183-193.
27. Chiu C.A., Lu L.F., Yu T.H., et al. Increased levels of total P-cresylsulphate and indoxyl sulphate are associated with coronary artery disease in patients with diabetic nephropathy. Rev Diabet Stud 2010, 7:275-284.
28. Wu I.W., Hsu K.H., Hsu H.J., et al. Serum free p-cresyl sulfate levels predict cardiovascular and all-cause mortality in elderly hemodialysis patients-a prospective cohort study. Nephrol Dial Transplant 2012, 27:1169-1175.
29. Lekawanvijit S., Adrahtas A., Kelly D.J., et al. Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes?. Eur Heart J 2010, 31:1771-1779.
30. Zhang H., Park Y., Wu J., et al. Role of TNF-alpha in vascular dysfunction. Clin Sci (Lond) 2009, 116:219-230.
31. Faure V., Dou L., Sabatier F., et al. Elevation of circulating endothelial microparticles in patients with chronic renal failure. J Thromb Haemost 2006, 4:566-573.
32. Lonnemann G., Novick D., Rubinstein M., et al. Interleukin-18, interleukin-18 binding protein and impaired production of interferon-gamma in chronic renal failure. Clin Nephrol 2003, 60:327-334.
33. Hsu C.C., Lu Y.C., Chiu C.A., et al. Levels of indoxyl sulfate are associated with severity of coronary atherosclerosis. Clin Invest Med 2013, 36:E42-E49.
34. Vaddi K., Nicolini F.A., Mehta P., et al. Increased secretion of tumor necrosis factor-alpha and interferon-gamma by mononuclear leukocytes in patients with ischemic heart disease-Relevance in superoxide anion generation. Circulation 1994, 90:694-699.
35. Lin C.J., Liu H.L., Pan C.F., et al. Indoxyl sulfate predicts cardiovascular disease and renal function deterioration in advanced chronic kidney disease. Arch Med Res 2012, 43:451-456.
36. Avissar N., Ornt D.B., Yagil Y., et al. Human kidney proximal tubules are the main source of plasma glutathione peroxidase. Am J Physiol 1994, 266:C367-C375.
37. Shimizu H., Bolati D., Higashiyama Y., et al. Indoxyl sulfate upregulates renal expression of MCP-1 via production of ROS and activation of NF-kappaB, p53, ERK, and JNK in proximal tubular cells. Life Sci 2012, 90:525-530.
38. El-Far M.A., Bakr M.A., Farahat S.E., et al. Glutathione peroxidase activity in patients with renal disorders. Clin Exp Nephrol 2005, 9:127-131.
39. Ghiselli A., Serafini M., Natella F., et al. Total antioxidant capacity as a tool to assess redox status: critical view and experimental data. Free Radic Biol Med 2000, 29:1106-1114.
40. Small D.M., Coombes J.S., Bennett N., et al. Oxidative stress, anti-oxidant therapies and chronic kidney disease. Nephrology 2012, 17:311-321.
41. Brunet P., Gondouin B., Duval-Sabatier A., et al. Does uremia cause vascular dysfunction?. Kidney Blood Press Res 2011, 34:284-290.
42. Meijers B.K., Van Kerckhoven S., Verbeke K., et al. The uremic retention solute p-cresyl sulfate and markers of endothelial damage. Am J Kidney Dis 2009, 54:891-901.
43. Schepers E., Meert N., Glorieux G., et al. P-cresylsulphate, the main in vivo metabolite of p-cresol, activates leucocyte free radical production. Nephrol Dial Transplant 2007, 22:592-596.
44. Meijers B.K., Claes K., Bammens B., et al. p-Cresol and cardiovascular risk in mild-to-moderate kidney disease. Clin J Am Soc Nephrol 2010, 5:1182-1189.
45. Namikoshi T., Tomita N., Satoh M., et al. Oral adsorbent AST-120 ameliorates endothelial dysfunction independent of renal function in rats with subtotal nephrectomy. Hypertens Res 2009, 32:194-200.
46. Fujii H., Nishijima F., Goto S., et al. Oral charcoal adsorbent (AST-120) prevents progression of cardiac damage in chronic kidney disease through suppression of oxidative stress. Nephrol Dial Transplant 2009, 24:2089-2095.