P-Cresyl sulphate has pro-inflammatory and cytotoxic actions on human proximal tubular epithelial cells

Nephrology Dialysis Transplantation

Volumn 29, Issue 1, 2014, Pages 56-64

  Poveda, Jonay ^a   Sanchez Niño, Maria D ^b   Glorieux, Griet ^c,d   Sanz, Ana B ^a   Egido, Jesús ^a,e   Vanholder, Raymond ^c,d   Ortiz, Alberto ^a,d,e  

^a 28400 Madrid   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d EUTOX   (France)

^e IRSIN   (Spain)

Author keywords

apoptosis; cell death; fn14; inflammation; tweak; uraemic toxins

Indexed keywords

4 CRESYL GLUCURONIDE; 4 CRESYL SULFATE; ALBUMIN; CXCL16 CHEMOKINE; CYTOKINE RECEPTOR; FN14 RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; UNCLASSIFIED DRUG; UREMIC TOXIN;

APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY TUBULE CELL; LONG TERM EXPOSURE; PRIORITY JOURNAL;

APOPTOSIS; CELL DEATH; FN14; INFLAMMATION; TWEAK; URAEMIC TOXINS;

ANIMALS; APOPTOSIS; CELL DEATH; CELLS, CULTURED; CRESOLS; DISEASE PROGRESSION; EPITHELIAL CELLS; HUMANS; KIDNEY TUBULES, PROXIMAL; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, TUMOR NECROSIS FACTOR; RENAL INSUFFICIENCY, CHRONIC; SULFURIC ACID ESTERS;

EID: 84892170272     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gft367     Document Type: Article

References (70)

1. Vanholder R, De SR. Pathophysiologic effects of uremic retention solutes. J Am Soc Nephrol 1999; 10: 1815-1823
2. Vanholder R, De SR, Hsu C et al. Uremic toxicity: the middle molecule hypothesis revisited. Semin Nephrol 1994; 14: 205-218
3. Duranton F, Cohen G, De SR et al. Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol 2012; 23: 1258-1270
4. Neirynck N, Vanholder R, Schepers E et al. An update on uremic toxins. Int Urol Nephrol 2013; 45: 139-150
5. 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
6. Vanholder R, Schepers E, Pletinck A et al. An update on protein-bound uremic retention solutes. J Ren Nutr 2012; 22: 90-94
7. Ortiz A, Massy ZA, Fliser D et al. Clinical usefulness of novel prognostic biomarkers in patients on hemodialysis. Nat Rev Nephrol 2012; 8: 141-150
8. 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
9. Meert N, Schepers E, Glorieux G et al. Novel method for simultaneous determination of p-cresylsulphate and p-cresylglucuro-nide: clinical data and pathophysiological implications. Nephrol Dial Transplant 2012; 27: 2388-2396
10. Meijers BK, Van KS, Verbeke K et al. The uremic retention solute p-cresyl sulfate and markers of endothelial damage. Am J Kidney Dis 2009; 54: 891-901
11. Ruggenenti P, Cravedi P, Remuzzi G. Mechanisms and treatment of CKD. J Am Soc Nephrol 2012; 23: 1917-1928
12. Hatakeyama S, Yamamoto H, Okamoto A et al. Effect of an oral adsorbent, AST-120, on dialysis initiation and survival in patients with chronic kidney disease. Int J Nephrol 2012; 2012: 376128
13. Shoji T, Wada A, Inoue K et al. Prospective randomized study evaluating the efficacy of the spherical adsorptive carbon AST-120 in chronic kidney disease patients with moderate decrease in renal function. Nephron Clin Pract 2007; 105: c99-c107
14. Konishi K, Nakano S, Tsuda S et al. AST-120 (Kremezin) initiated in early stage chronic kidney disease stunts the progression of renal dysfunction in type 2 diabetic subjects. Diabetes Res Clin Pract 2008; 81: 310-315
15. Berlanga JR, Marron B, Reyero A et al. Peritoneal dialysis retardation of progression of advanced renal failure. Perit Dial Int 2002; 22: 239-242
16. Nakamura T, Sato E, Fujiwara N et al. Oral adsorbent AST-120 ameliorates tubular injury in chronic renal failure patients by reducing proteinuria and oxidative stress generation. Metabolism 2011; 60: 260-264
17. Vanholder R, Meert N, Van BW et al. Why do patients on peritoneal dialysis have low blood levels of protein-bound solutes? Nat Clin Pract Nephrol 2009; 5: 130-131
18. Pham NM, Recht NS, Hostetter TH et al. Removal of the protein-bound solutes Indican and p-cresol sulfate by peritoneal dialysis. Clin J Am Soc Nephrol 2008; 3: 85-90
19. Evenepoel P, Bammens B, Verbeke K et al. Superior dialytic clearance of beta(2)-microglobulin and p-cresol by high-flux hemodialysis as compared to peritoneal dialysis. Kidney Int 2006; 70: 794-799
20. Sun CY, Chang SC, Wu MS. Uremic toxins induce kidney fibrosis by activating intrarenal renin-angiotensin-aldosterone system associated epithelial-to-mesenchymal transition. PLoS One 2012; 7: e34026
21. Sun CY, Chang SC, Wu MS. Suppression of Klotho expression by protein-bound uremic toxins is associated with increased DNA methyltransferase expression and DNA hypermethylation. Kidney Int 2012; 81: 640-650
22. Sanchez-Nino MD, Sanz AB, Ihalmo P et al. The MIF receptor CD74 in diabetic podocyte injury. J Am Soc Nephrol 2009; 20: 353-362
23. Justo P, Sanz AB, Sanchez-Nino MD et al. Cytokine cooperation in renal tubular cell injury: the role of TWEAK. Kidney Int 2006; 70: 1750-1758
24. Sanchez-Nino MD, Sanz AB, Lorz C et al. BASP1 promotes apop-tosis in diabetic nephropathy. J Am Soc Nephrol 2010; 21: 610-621
25. Lorz C, Ortiz A, Justo P et al. Proapoptotic Fas ligand is expressed by normal kidney tubular epithelium and injured glomeruli. J Am Soc Nephrol 2000; 11: 1266-1277
26. Sanz AB, Justo P, Sanchez-Nino MD et al. The cytokine TWEAK modulates renal tubulointerstitial inflammation. J Am Soc Nephrol 2008; 19: 695-703
27. Sanz AB, Sanchez-Nino MD, Ramos AM et al. NF-kappaB in renal inflammation. J Am Soc Nephrol 2010; 21: 1254-1262
28. Molano A, Lakhani P, Aran A et al. TWEAK stimulation of kidney resident cells in the pathogenesis of graft versus host induced lupus nephritis. Immunol Lett 2009; 125: 119-128
29. Ortiz A, Lorz C, Catalan MP et al. Expression of apoptosis regulatory proteins in tubular epithelium stressed in culture or following acute renal failure. Kidney Int 2000; 57: 969-981
30. Baines RJ, Brunskill NJ. Tubular toxicity of proteinuria. Nat Rev Nephrol 2011; 7: 177-180
31. Eloot S, Schepers E, Barreto DV et al. Estimated glomerular filtration rate is a poor predictor of concentration for a broad range of uremic toxins. Clin J Am Soc Nephrol 2011; 6: 1266-1273
32. Grgic I, Campanholle G, Bijol V et al. Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int 2012; 82: 172-183
33. Izquierdo MC, Sanz AB, Mezzano S et al. TWEAK (tumor necrosis factor-like weak inducer of apoptosis) activates CXCL16 expression during renal tubulointerstitial inflammation. Kidney Int 2012; 81: 1098-1107
34. Lorz C, Benito A, Ucero AC et al. Trail and kidney disease. Front Biosci 2009; 14: 3740-3749
35. Lorz C, Benito-Martin A, Boucherot A et al. The death ligand TRAIL in diabetic nephropathy. J Am Soc Nephrol 2008; 19: 904-914
36. Bonventre JV. Can we target tubular damage to prevent renal function decline in diabetes? Semin Nephrol 2012; 32: 452-462
37. Lowenstein J. The angler fish and uremic toxins. FASEB J 2011; 25: 1781-1785
38. Ortiz A, Ziyadeh FN, Neilson EG. Expression of apoptosis-regu-latory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. J Investig Med 1997; 45: 50-56
39. Rodriguez-Iturbe B, Johnson RJ, Herrera-Acosta J. Tubulointer-stitial damage and progression of renal failure. Kidney Int Suppl 2005; 99: S82-S86
40. Rodriguez-Iturbe B, Garcia GG. The role of tubulointerstitial inflammation in the progression of chronic renal failure. Nephron Clin Pract 2010; 116: c81-c88
41. Lorz C, Justo P, Sanz A et al. Paracetamol-induced renal tubular injury: a role for ER stress. J Am Soc Nephrol 2004; 15: 380-389
42. Lorz C, Justo P, Sanz AB et al. Role of Bcl-xL in paracetamol-induced tubular epithelial cell death. Kidney Int 2005; 67: 592-601
43. Fored CM, Ejerblad E, Lindblad P et al. Acetaminophen, aspirin, and chronic renal failure. N Engl J Med 2001; 345: 1801-1808
44. Ortiz A, Justo P, Sanz A et al. Tubular cell apoptosis and cidofo-vir-induced acute renal failure. Antivir Ther 2005; 10: 185-190
45. Fernandez-Fernandez B, Montoya-Ferrer A, Sanz AB et al. Teno-fovir nephrotoxicity: 2011 update. AIDS Res Treat 2011; 2011: 354908
46. Miyamoto Y, Watanabe H, Noguchi T et al. Organic anion transporters play an important role in the uptake of p-cresyl sulfate, a uremic toxin, in the kidney. Nephrol Dial Transplant 2011; 26: 2498-2502
47. Liabeuf S, Barreto DV, Barreto FC 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
48. Yamamoto H, Tsuruoka S, Ioka T et al. Indoxyl sulfate stimulates proliferation of rat vascular smooth muscle cells. Kidney Int 2006; 69: 1780-1785
49. Wang CP, Lu LF, Yu TH et al. Serum levels of total p-cresylsul-phate are associated with angiographic coronary atherosclerosis severity instable angina patients with early stage of renal failure. Atherosclerosis 2010; 211: 579-583
50. Barreto FC, Barreto DV, 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
51. Meijers BK, Bammens B, De MB et al. Free p-cresol is associated with cardiovascular disease in hemodialysis patients. Kidney Int 2008; 73: 1174-1180
52. Ueda H, Shibahara N, Takagi S et al. AST-120, an oral adsorbent, delays the initiation of dialysis in patients with chronic kidney diseases. Ther Apher Dial 2007; 11: 189-195
53. Akizawa T, Asano Y, Morita S et al. Effect of a carbonaceous oral adsorbent on the progression of CKD: a multicenter, randomized, controlled trial. Am J Kidney Dis 2009; 54: 459-467
54. Izquierdo MC, Perez-Gomez MV, Sanchez-Nino MD et al. Klotho, phosphate and inflammation/ageing in chronic kidney disease. Nephrol Dial Transplant 2012; 27: iv6-iv10
55. Sanchez-Nino MD, Sanz AB, Ortiz A. Klotho to treat kidney fi-brosis. J Am Soc Nephrol 2013; 24: 687-689
56. Carracedo J, Buendia P, Merino A et al. Klotho modulates the stress response in human senescent endothelial cells. Mech Ageing Dev 2012; 133: 647-654
57. Moreno JA, Izquierdo MC, Sanchez-Nino MD et al. The inflammatory cytokines TWEAK and TNFalpha reduce renal klotho expression through NFkappaB. J Am Soc Nephrol 2011; 22: 1315-1325
58. Sanz AB, Sanchez-Nino MD, Ortiz A. TWEAK, a multifunctional cytokine in kidney injury. Kidney Int 2011; 80: 708-718
59. 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
60. Shimizu H, Yisireyili M, Higashiyama Y et al. Indoxyl sulfate up-regulates renal expression of ICAM-1 via production of ROS and activation of NF-kappaB and p53 in proximal tubular cells. Life Sci 2013; 92: 143-148
61. Shimizu H, Bolati D, Higashiyama Y et al. Indoxyl sulfate upre-gulates 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
62. Kim SH, Yu MA, Ryu ES et al. Indoxyl sulfate-induced epithelial-to- mesenchymal transition and apoptosis of renal tubular cells as novel mechanisms of progression of renal disease. Lab Invest 2012; 92: 488-498
63. Shimizu H, Yisireyili M, Nishijima F et al. Indoxyl Sulfate Enhances p53-TGF-beta(1)-Smad3 pathway in proximal tubular cells. Am J Nephrol 2013; 37: 97-103
64. Sun CY, Hsu HH, Wu MS. p-Cresol sulfate and indoxyl sulfate induce similar cellular inflammatory gene expressions in cultured proximal renal tubular cells. Nephrol Dial Transplant 2013; 28: 70-78
65. Bolati D, Shimizu H, Higashiyama Y et al. Indoxyl sulfate induces epithelial-to-mesenchymal transition in rat kidneys and human proximal tubular cells. Am J Nephrol 2011; 34: 318-323
66. Shimizu H, Bolati D, Adijiang A et al. Senescence and dysfunction of proximal tubular cells are associated with activated p53 expression by indoxyl sulfate. Am J Physiol Cell Physiol 2010; 299: C1110-C1117
67. Taki K, Nakamura S, Miglinas M et al. Accumulation of indoxyl sulfate in OAT1/3-positive tubular cells in kidneys of patients with chronic renal failure. J Ren Nutr 2006; 16: 199-203
68. Mutsaers HA, Wilmer MJ, van den Heuvel LP et al. Basolateral transport of the uraemic toxin p-cresyl sulfate: role for organic anion transporters? Nephrol Dial Transplant 2011; 26: 4149
69. Marron B, Remon C, Perez-Fontan M et al. Benefits of preserving residual renal function in peritoneal dialysis. Kidney Int Suppl 2008; 108: S42-S51
70. Vanholder R, Bammens B, de LH et al. Warning: the unfortunate end of p-cresol as a uraemic toxin. Nephrol Dial Transplant 2011; 26: 1464-1467