American Journal of Kidney Diseases
Volume 53, Issue 1 , Pages 138-150 , January 2009

Accumulation of Advanced Glycation End Products and Chronic Complications in ESRD Treated by Dialysis

  • Robbert Meerwaldt, MD, PhD

      Affiliations

    • Department of Surgery, Isala Clinics, Zwolle, The Netherlands
    • Corresponding Author InformationAddress correspondence to Robbert Meerwaldt, MD, PhD, Department of Surgery, Isala Clinics, Dr Heesweg 2, 8025 AB, Zwolle, The Netherlands
  • ,
  • Clark J. Zeebregts, MD, PhD

      Affiliations

    • Department of Surgery, Division of Vascular Surgery, University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • Gerjan Navis, MD, PhD

      Affiliations

    • Department of Internal Medicine, Division of Nephrology, University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • Jan-Luuk Hillebrands, PhD

      Affiliations

    • Department of Cell Biology, University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • Joop D. Lefrandt, MD, PhD

      Affiliations

    • Department of Internal Medicine, Division of Vascular Medicine, University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • Andries J. Smit, MD, PhD

      Affiliations

    • Department of Internal Medicine, Division of Vascular Medicine, University Medical Center Groningen, Groningen, The Netherlands

Received 20 May 2008 ,Accepted 29 August 2008.

References 

  1. Rayner HC, Pisoni RL, Bommer J, et al. Mortality and hospitalization in haemodialysis patients in five European countries: Results from the Dialysis Outcomes and Practice Patterns Study (DOPPS). Nephrol Dial Transplant. 2004;19:108–120
  2. Foley RN, Parfrey PS, Sarnak MJ. Epidemiology of cardiovascular disease in chronic renal disease. J Am Soc Nephrol. 1998;9(suppl 12):S16–S23
  3. Stack AG, Bloembergen WE. Prevalence and clinical correlates of coronary artery disease among new dialysis patients in the United States: A cross-sectional study. J Am Soc Nephrol. 2001;12:1516–1523
  4. Schwenger V, Zeier M, Henle T, Ritz E. Advanced glycation endproducts (AGEs) as uremic toxins. Nahrung. 2001;45:172–176
  5. Shaw S, Akyol M, Bell J, Briggs JD, Dominiczak MH. Effects of continuous ambulatory peritoneal dialysis and kidney transplantation on advanced glycation endproducts in the skin and peritoneum. Cell Mol Biol (Noisy-le-grand). 1998;44:1061–1068
  6. Miyata T, Ueda Y, Yoshida A, et al. Clearance of pentosidine, an advanced glycation end product, by different modalities of renal replacement therapy. Kidney Int. 1997;51:880–887
  7. Gugliucci A, Bendayan M. Renal fate of circulating advanced glycated end products (AGE): Evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia. 1996;39:149–160
  8. Makita Z, Yanagisawa K, Kuwajima S, et al. Advanced glycation endproducts and diabetic nephropathy. J Diabetes Complications. 1995;9:265–268
  9. Ceballos-Picot I, Witko-Sarsat V, Merad-Boudia M, et al. Glutathione antioxidant system as a marker of oxidative stress in chronic renal failure. Free Radic Biol Med. 1996;21:845–853
  10. Genuth S, Sun W, Cleary P, et al. Glycation and carboxymethyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the Diabetes Control and Complications Trial and epidemiology of diabetes interventions and complications participants with type 1 diabetes. Diabetes. 2005;54:3103–3111
  11. Gerrits EG, Lutgers HL, Kleefstra N, et al. Skin autofluorescence: A tool to identify type 2 diabetic patients at risk for developing microvascular complications. Diabetes Care. 2008;31:517–521
  12. Friedlander MA, Wu YC, Elgawish A, Monnier VM. Early and advanced glycosylation end products (Kinetics of formation and clearance in peritoneal dialysis). J Clin Invest. 1996;97:728–735
  13. Friedlander MA, Wu YC, Schulak JA, Monnier VM, Hricik DE. Influence of dialysis modality on plasma and tissue concentrations of pentosidine in patients with end-stage renal disease. Am J Kidney Dis. 1995;25:445–451
  14. Lin CL, Huang CC, Yu CC, Yang HY, Chuang FR, Yang CW. Reduction of advanced glycation end product levels by on-line hemodiafiltration in long-term hemodialysis patients. Am J Kidney Dis. 2003;42:524–531
  15. Gerdemann A, Wagner Z, Solf A, et al. Plasma levels of advanced glycation end products during haemodialysis, haemodiafiltration and haemofiltration: Potential importance of dialysate quality. Nephrol Dial Transplant. 2002;17:1045–1049
  16. Monnier VM, Cerami A. Nonenzymatic browning in vivo: Possible process for aging of long-lived proteins. Science. 1981;211:491–493
  17. Thorpe SR, Baynes JW. Maillard reaction products in tissue proteins: New products and new perspectives. Amino Acids. 2003;25:275–281
  18. Wolff SP, Dean RT. Glucose autoxidation and protein modification (The potential role of ‘autoxidative glycosylation’ in diabetes). Biochem J. 1987;245:243–250
  19. Miyata T, Wada Y, Cai Z, et al. Implication of an increased oxidative stress in the formation of advanced glycation end products in patients with end-stage renal failure. Kidney Int. 1997;51:1170–1181
  20. Vaziri ND. Oxidative stress in uremia: Nature, mechanisms, and potential consequences. Semin Nephrol. 2004;24:469–473
  21. Diepeveen SH, Verhoeven GH, van der PJ, et al. Oxidative stress in patients with end-stage renal disease prior to the start of renal replacement therapy. Nephron Clin Pract. 2004;98:c3–c7
  22. Kosch M, Levers A, Fobker M, et al. Dialysis filter type determines the acute effect of haemodialysis on endothelial function and oxidative stress. Nephrol Dial Transplant. 2003;18:1370–1375
  23. Niwa T. 3-Deoxyglucosone: Metabolism, analysis, biological activity, and clinical implication. J Chromatogr B Biomed Sci Appl. 1999;731:23–36
  24. Thornalley PJ, Glyoxalase I. —Structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans. 2003;31:1343–1348
  25. Miyata T, van Ypersele dS, Imasawa T, et al. Glyoxalase I deficiency is associated with an unusual level of advanced glycation end products in a hemodialysis patient. Kidney Int. 2001;60:2351–2359
  26. Waanders F, Greven WL, Baynes JW, et al. Renal accumulation of pentosidine in non-diabetic proteinuria-induced renal damage in rats. Nephrol Dial Transplant. 2005;20:2060–2070
  27. Koschinsky T, He CJ, Mitsuhashi T, et al. Orally absorbed reactive glycation products (glycotoxins): An environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci U S A. 1997;94:6474–6479
  28. Cerami C, Founds H, Nicholl I, et al. Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A. 1997;94:13915–13920
  29. Bakker SJ, Gans RO, ter Maaten JC, Teerlink T, Westerhoff HV, Heine RJ. The potential role of adenosine in the pathophysiology of the insulin resistance syndrome. Atherosclerosis. 2001;155:283–290
  30. Bakker SJ, IJzerman RG, Teerlink T, Westerhoff HV, Gans RO, Heine RJ. Cytosolic triglycerides and oxidative stress in central obesity: The missing link between excessive atherosclerosis, endothelial dysfunction, and beta-cell failure?. Atherosclerosis. 2000;148:17–21
  31. Monnier VM, Vishwanath V, Frank KE, Elmets CA, Dauchot P, Kohn RR. Relation between complications of type I diabetes mellitus and collagen-linked fluorescence. N Engl J Med. 1986;314:403–408
  32. Onorato JM, Thorpe SR, Baynes JW. Immunohistochemical and ELISA assays for biomarkers of oxidative stress in aging and disease. Ann N Y Acad Sci. 1998;854:277–290
  33. Taneda S, Monnier VM. ELISA of pentosidine, an advanced glycation end product, in biological specimens. Clin Chem. 1994;40:1766–1773
  34. Slowik-Zylka D, Safranow K, Dziedziejko V, Bukowska H, Ciechanowski K, Chlubek D. A sensitive and specific HPLC method for the determination of total pentosidine concentration in plasma. J Biochem Biophys Methods. 2004;61:313–329
  35. Pamplona R, Portero-Otin M, Ruiz C, et al. Thyroid status modulates glycoxidative and lipoxidative modification of tissue proteins. Free Radic Biol Med. 1999;27:901–910
  36. Ahmed MU, Thorpe SR, Baynes JW. Identification of N epsilon-carboxymethyllysine as a degradation product of fructoselysine in glycated protein. J Biol Chem. 1986;261:4889–4894
  37. Hricik DE, Wu YC, Schulak A, Friedlander MA. Disparate changes in plasma and tissue pentosidine levels after kidney and kidney-pancreas transplantation. Clin Transplant. 1996;10:568–573
  38. Dorrian CA, Cathcart S, Clausen J, Shapiro D, Dominiczak MH. Factors in human serum interfere with the measurement of advanced glycation endproducts. Cell Mol Biol (Noisy-le-grand). 1998;44:1069–1079
  39. Kessel L, Sander B, Dalgaard P, Larsen M. Lens fluorescence and metabolic control in type 1 diabetic patients: A 14 year follow up study. Br J Ophthalmol. 2004;88:1169–1172
  40. Meerwaldt R, Graaff R, Oomen PH, et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia. 2004;47:1324–1330
  41. Meerwaldt R, Links T, Graaff R, et al. Simple noninvasive measurement of skin autofluorescence. Ann N Y Acad Sci. 2005;1043:290–298
  42. Meerwaldt R, Hartog JW, Graaff R, et al. Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol. 2005;16:3687–3693
  43. Maynard JD, Rohrscheib M, Way JF, Nguyen CM, Ediger MN. Noninvasive type 2 diabetes screening: Superior sensitivity to fasting plasma glucose and A1C. Diabetes Care. 2007;30:1120–1124
  44. Wu T, Willett WC, Rifai N, Rimm EB. Plasma fluorescent oxidation products as potential markers of oxidative stress for epidemiologic studies. Am J Epidemiol. 2007;166:552–560
  45. Kollias N, Gillies R, Moran M, Kochevar IE, Anderson RR. Endogenous skin fluorescence includes bands that may serve as quantitative markers of aging and photoaging. J Invest Dermatol. 1998;111:776–780
  46. Sakata N, Imanaga Y, Meng J, et al. Increased advanced glycation end products in atherosclerotic lesions of patients with end-stage renal disease. Atherosclerosis. 1999;142:67–77
  47. Yoshida S, Yamada K, Hamaguchi K, et al. Immunohistochemical study of human advanced glycation end-products (AGE) and growth factors in cardiac tissues of patients on maintenance dialysis and with kidney transplantation. Clin Nephrol. 1998;49:273–280
  48. Taki K, Takayama F, Tsuruta Y, Niwa T. Oxidative stress, advanced glycation end product, and coronary artery calcification in hemodialysis patients. Kidney Int. 2006;70:218–224
  49. Suliman ME, Stenvinkel P, Jogestrand T, et al. Plasma pentosidine and total homocysteine levels in relation to change in common carotid intima-media area in the first year of dialysis therapy. Clin Nephrol. 2006;66:418–425
  50. Sell DR, Nelson JF, Monnier VM. Effect of chronic aminoguanidine treatment on age-related glycation, glycoxidation, and collagen cross-linking in the Fischer 344 rat. J Gerontol A Biol Sci Med Sci. 2001;56:B405–B411
  51. Wolffenbuttel BH, Boulanger CM, Crijns FR, et al. Breakers of advanced glycation end products restore large artery properties in experimental diabetes. Proc Natl Acad Sci U S A. 1998;95:4630–4634
  52. Hartog JW, Voors AA, Bakker SJ, Smit AJ, van Veldhuisen DJ. Advanced glycation end-products (AGEs) and heart failure: Pathophysiology and clinical implications. Eur J Heart Fail. 2007;9:1146–1155
  53. Smit AJ, Lutgers HL. The clinical relevance of advanced glycation endproducts (AGE) and recent developments in pharmaceutics to reduce AGE accumulation. Curr Med Chem. 2004;11:2767–2784
  54. Monnier VM, Sell DR, Genuth S. Glycation products as markers and predictors of the progression of diabetic complications. Ann N Y Acad Sci. 2005;1043:567–581
  55. Klein DJ, Oegema TR, Brown DM. Release of glomerular heparan-35SO4 proteoglycan by heparin from glomeruli of streptozocin-induced diabetic rats. Diabetes. 1989;38:130–139
  56. Tarsio JF, Reger LA, Furcht LT. Decreased interaction of fibronectin, type IV collagen, and heparin due to nonenzymatic glycation (Implications for diabetes mellitus). Biochemistry. 1987;26:1014–1020
  57. Drueke TB, Khoa TN, Massy ZA, Witko-Sarsat V, Lacour B, Descamps-Latscha B. Role of oxidized low-density lipoprotein in the atherosclerosis of uremia. Kidney Int Suppl. 2001;78:S114–S119
  58. Oranje WA, Wolffenbuttel BH. Lipid peroxidation and atherosclerosis in type II diabetes. J Lab Clin Med. 1999;134:19–32
  59. Stocker R, Keaney JF. Role of oxidative modifications in atherosclerosis. Physiol Rev. 2004;84:1381–1478
  60. Sobal G, Menzel J, Sinzinger H. Why is glycated LDL more sensitive to oxidation than native LDL? (A comparative study). Prostaglandins Leukot Essent Fatty Acids. 2000;63:177–186
  61. Bucala R, Makita Z, Vega G, et al. Modification of low density lipoprotein by advanced glycation end products contributes to the dyslipidemia of diabetes and renal insufficiency. Proc Natl Acad Sci U S A. 1994;91:9441–9445
  62. Thornalley PJ. Cell activation by glycated proteins (AGE receptors, receptor recognition factors and functional classification of AGEs). Cell Mol Biol (Noisy-le-grand). 1998;44:1013–1023
  63. Schmidt AM, Hasu M, Popov D, et al. Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci U S A. 1994;91:8807–8811
  64. Basta G, Schmidt AM, De Caterina R. Advanced glycation end products and vascular inflammation: Implications for accelerated atherosclerosis in diabetes. Cardiovasc Res. 2004;63:582–592
  65. Yan SF, Ramasamy R, Naka Y, Schmidt AM. Glycation, inflammation, and RAGE: A scaffold for the macrovascular complications of diabetes and beyond. Circ Res. 2003;93:1159–1169
  66. Tanji N, Markowitz GS, Fu C, et al. Expression of advanced glycation end products and their cellular receptor RAGE in diabetic nephropathy and nondiabetic renal disease. J Am Soc Nephrol. 2000;11:1656–1666
  67. Schwedler S, Schinzel R, Vaith P, Wanner C. Inflammation and advanced glycation end products in uremia: Simple coexistence, potentiation or causal relationship?. Kidney Int Suppl. 2001;78:S32–S36
  68. Hogan M, Cerami A, Bucala R. Advanced glycosylation endproducts block the antiproliferative effect of nitric oxide (Role in the vascular and renal complications of diabetes mellitus). J Clin Invest. 1992;90:1110–1115
  69. Obrenovich ME, Monnier VM. Glycation stimulates amyloid formation. Sci Aging Knowledge Environ. 2004;e3, (abstr)
  70. Gejyo F, Odani S, Yamada T, et al. Beta 2-microglobulin: A new form of amyloid protein associated with chronic hemodialysis. Kidney Int. 1986;30:385–390
  71. Gejyo F, Narita I. Current clinical and pathogenetic understanding of beta2-m amyloidosis in long-term haemodialysis patients. Nephrology (Carlton). 2003;8(suppl):S45–S49
  72. Ogawa H, Saito A, Oda O, Nakajima M, Chung TG. Detection of novel beta 2-microglobulin in the serum of hemodialysis patients and its amyloidogenic predisposition. Clin Nephrol. 1988;30:158–163
  73. Miyata T, Taneda S, Kawai R, et al. Identification of pentosidine as a native structure for advanced glycation end products in beta-2-microglobulin-containing amyloid fibrils in patients with dialysis-related amyloidosis. Proc Natl Acad Sci U S A. 1996;93:2353–2358
  74. Brancaccio D, Gallieni M, Niwa T, Braidotti P, Coggi G. Ultrastructural localization of advanced glycation end products and beta2-microglobulin in dialysis amyloidosis. J Nephrol. 2000;13:129–136
  75. Niwa T, Katsuzaki T, Miyazaki S, et al. Amyloid beta 2-microglobulin is modified with imidazolone, a novel advanced glycation end product, in dialysis-related amyloidosis. Kidney Int. 1997;51:187–194
  76. Du YS, Zhu H, Fu J, et al. Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: A proinflammatory pathway in Alzheimer disease. Proc Natl Acad Sci U S A. 1997;94:5296–5301
  77. Miyata T, Hori O, Zhang J, et al. The receptor for advanced glycation end products (RAGE) is a central mediator of the interaction of AGE-beta2microglobulin with human mononuclear phagocytes via an oxidant-sensitive pathway (Implications for the pathogenesis of dialysis-related amyloidosis). J Clin Invest. 1996;98:1088–1094
  78. Owen WF, Hou FF, Stuart RO, et al. Beta 2-microglobulin modified with advanced glycation end products modulates collagen synthesis by human fibroblasts. Kidney Int. 1998;53:1365–1373
  79. Miyata T, Kawai R, Taketomi S, Sprague SM. Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant. 1996;11(suppl 5):S54–S57
  80. Combet S, Ferrier ML, Van Landschoot M, et al. Chronic uremia induces permeability changes, increased nitric oxide synthase expression, and structural modifications in the peritoneum. J Am Soc Nephrol. 2001;12:2146–2157
  81. De Vriese AS, Flyvbjerg A, Mortier S, Tilton RG, Lameire NH. Inhibition of the interaction of AGE-RAGE prevents hyperglycemia-induced fibrosis of the peritoneal membrane. J Am Soc Nephrol. 2003;14:2109–2118
  82. Nakamura S, Tachikawa T, Tobita K, et al. Role of advanced glycation end products and growth factors in peritoneal dysfunction in CAPD patients. Am J Kidney Dis. 2003;41(suppl 1):S61–S67
  83. Nakayama M, Yoshimura K, Maruyama Y, Numata M, Hosoya T, Izumi G. Possible involvement of cross-linking advanced glycation endproducts in long-term CAPD peritoneal degeneration. Nephrol Dial Transplant. 2004;19:1664–1665
  84. Nakayama M, Kawaguchi Y, Yamada K, et al. Immunohistochemical detection of advanced glycosylation end-products in the peritoneum and its possible pathophysiological role in CAPD. Kidney Int. 1997;51:182–186
  85. Kjellstrand P, Erixon M, Wieslander A, Linden T, Martinson E. Temperature: The single most important factor for degradation of glucose fluids during storage. Perit Dial Int. 2004;24:385–391
  86. Linden T, Cohen A, Deppisch R, Kjellstrand P, Wieslander A. 3,4-Dideoxyglucosone-3-ene (3,4-DGE): A cytotoxic glucose degradation product in fluids for peritoneal dialysis. Kidney Int. 2002;62:697–703
  87. Wieslander A, Linden T, Kjellstrand P. Glucose degradation products in peritoneal dialysis fluids: How they can be avoided. Perit Dial Int. 2001;21(suppl 3):S119–S124
  88. Mortier S, Faict D, Schalkwijk CG, Lameire NH, De Vriese AS. Long-term exposure to new peritoneal dialysis solutions: Effects on the peritoneal membrane. Kidney Int. 2004;66:1257–1265
  89. Rippe B, Simonsen O, Heimburger O, et al. Long-term clinical effects of a peritoneal dialysis fluid with less glucose degradation products. Kidney Int. 2001;59:348–357
  90. Lowrie EG, Lew NL. Death risk in hemodialysis patients: The predictive value of commonly measured variables and an evaluation of death rate differences between facilities. Am J Kidney Dis. 1990;15:458–482
  91. Makita Z, Radoff S, Rayfield EJ, et al. Advanced glycosylation end products in patients with diabetic nephropathy. N Engl J Med. 1991;325:836–842
  92. Baynes JW, Thorpe SR. Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med. 2000;28:1708–1716
  93. Schwedler SB, Metzger T, Schinzel R, Wanner C. Advanced glycation end products and mortality in hemodialysis patients. Kidney Int. 2002;62:301–310
  94. Busch M, Franke S, Muller A, et al. Potential cardiovascular risk factors in chronic kidney disease: AGEs, total homocysteine and metabolites, and the C-reactive protein. Kidney Int. 2004;66:338–347
  95. Roberts MA, Thomas MC, Fernando D, Macmillan N, Power DA, Ierino FL. Low molecular weight advanced glycation end products predict mortality in asymptomatic patients receiving chronic haemodialysis. Nephrol Dial Transplant. 2006;21:1611–1617
  96. Wagner Z, Molnar M, Molnar GA, et al. Serum carboxymethyllysine predicts mortality in hemodialysis patients. Am J Kidney Dis. 2006;47:294–300
  97. He C, Sabol J, Mitsuhashi T, Vlassara H. Dietary glycotoxins: Inhibition of reactive products by aminoguanidine facilitates renal clearance and reduces tissue sequestration. Diabetes. 1999;48:1308–1315
  98. Koyama H, Shoji T, Yokoyama H, et al. Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:2587–2593
  99. Koyama H, Shoji T, Fukumoto S, et al. Low circulating endogenous secretory receptor for AGEs predicts cardiovascular mortality in patients with end-stage renal disease. Arterioscler Thromb Vasc Biol. 2007;27:147–153
  100. Gross S, van Ree RM, Oterdoom LH, et al. Low levels of sRAGE are associated with increased risk for mortality in renal transplant recipients. Transplantation. 2007;84:659–663
  101. Onorato JM, Jenkins AJ, Thorpe SR, Baynes JW. Pyridoxamine, an inhibitor of advanced glycation reactions, also inhibits advanced lipoxidation reactions (Mechanism of action of pyridoxamine). J Biol Chem. 2000;275:21177–21184
  102. Metz TO, Alderson NL, Thorpe SR, Baynes JW. Pyridoxamine, an inhibitor of advanced glycation and lipoxidation reactions: A novel therapy for treatment of diabetic complications. Arch Biochem Biophys. 2003;419:41–49
  103. Voziyan PA, Metz TO, Baynes JW, Hudson BG. A post-Amadori inhibitor pyridoxamine also inhibits chemical modification of proteins by scavenging carbonyl intermediates of carbohydrate and lipid degradation. J Biol Chem. 2002;277:3397–3403
  104. Degenhardt TP, Alderson NL, Arrington DD, et al. Pyridoxamine inhibits early renal disease and dyslipidemia in the streptozotocin-diabetic rat. Kidney Int. 2002;61:939–950
  105. Stitt A, Gardiner TA, Alderson NL, et al. The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes. Diabetes. 2002;51:2826–2832
  106. Waanders F, van den BE, Nagai R, van V I, Navis G, van Goor H. Renoprotective effects of the AGE-inhibitor pyridoxamine in experimental chronic allograft nephropathy in rats. Nephrol Dial Transplant. 2008;23:518–524
  107. Williams ME, Bolton WK, Khalifah RG, Degenhardt TP, Schotzinger RJ, McGill JB. Effects of pyridoxamine in combined phase 2 studies of patients with type 1 and type 2 diabetes and overt nephropathy. Am J Nephrol. 2007;27:605–614
  108. Bolton WK, Cattran DC, Williams ME, et al. Randomized trial of an inhibitor of formation of advanced glycation end products in diabetic nephropathy. Am J Nephrol. 2004;24:32–40
  109. Zheng F, Zeng YJ, Plati AR, et al. Combined AGE inhibition and ACEi decreases the progression of established diabetic nephropathy in B6 db/db mice. Kidney Int. 2006;70:507–514
  110. Bakris GL, Bank AJ, Kass DA, Neutel JM, Preston RA, Oparil S. Advanced glycation end-product cross-link breakers: A novel approach to cardiovascular pathologies related to the aging process. Am J Hypertens. 2004;17(12 Pt 2):23S–30S
  111. Kass DA, Shapiro EP, Kawaguchi M, et al. Improved arterial compliance by a novel advanced glycation end-product crosslink breaker. Circulation. 2001;104:1464–1470
  112. Yang S, Litchfield JE, Baynes JW. AGE-breakers cleave model compounds, but do not break Maillard crosslinks in skin and tail collagen from diabetic rats. Arch Biochem Biophys. 2003;412:42–46
  113. Alderson NL, Chachich ME, Frizzell N, et al. Effect of antioxidants and ACE inhibition on chemical modification of proteins and progression of nephropathy in the streptozotocin diabetic rat. Diabetologia. 2004;47:1385–1395
  114. Yamagishi S, Takeuchi M. Nifedipine inhibits gene expression of receptor for advanced glycation end products (RAGE) in endothelial cells by suppressing reactive oxygen species generation. Drugs Exp Clin Res. 2004;30:169–175
  115. Sebekova K, Gazdikova K, Syrova D, et al. Effects of ramipril in nondiabetic nephropathy: Improved parameters of oxidatives stress and potential modulation of advanced glycation end products. J Hum Hypertens. 2003;17:265–270
  116. Miyata T, van Ypersele dS, Ueda Y, et al. Angiotensin II receptor antagonists and angiotensin-converting enzyme inhibitors lower in vitro the formation of advanced glycation end products: Biochemical mechanisms. J Am Soc Nephrol. 2002;13:2478–2487
  117. Uribarri J, Cai W, Sandu O, Peppa M, Goldberg T, Vlassara H. Diet-derived advanced glycation end products are major contributors to the body's AGE pool and induce inflammation in healthy subjects. Ann N Y Acad Sci. 2005;1043:461–466
  118. Uribarri J, Peppa M, Cai W, et al. Restriction of dietary glycotoxins reduces excessive advanced glycation end products in renal failure patients. J Am Soc Nephrol. 2003;14:728–731
  119. Hricik DE, Schulak JA, Sell DR, Fogarty JF, Monnier VM. Effects of kidney or kidney-pancreas transplantation on plasma pentosidine. Kidney Int. 1993;43:398–403
  120. Hartog JW, Smit AJ, van Son WJ, et al. Advanced glycation end products in kidney transplant patients: A putative role in the development of chronic renal transplant dysfunction. Am J Kidney Dis. 2004;43:966–975
  121. Hartog JW, de Vries AP, Bakker SJ, et al. Risk factors for chronic transplant dysfunction and cardiovascular disease are related to accumulation of advanced glycation end-products in renal transplant recipients. Nephrol Dial Transplant. 2006;21:2263–2269
  122. Fleischmann EH, Bower JD, Salahudeen AK. Are conventional cardiovascular risk factors predictive of two-year mortality in hemodialysis patients?. Clin Nephrol. 2001;56:221–230
  123. Malatino LS, Benedetto FA, Mallamaci F, et al. Smoking, blood pressure and serum albumin are major determinants of carotid atherosclerosis in dialysis patients (CREED Investigators. Cardiovascular Risk Extended Evaluation in Dialysis patients). J Nephrol. 1999;12:256–260
  124. Blacher J, London GM, Safar ME, Mourad JJ. Influence of age and end-stage renal disease on the stiffness of carotid wall material in hypertension. J Hypertens. 1999;17:237–244
  125. Baynes JW. From life to death—The struggle between chemistry and biology during aging: The Maillard reaction as an amplifier of genomic damage. Biogerontology. 2000;1:235–246

 Originally published online as doi:10.1053/j.ajkd.2008.08.031 on November 26, 2008.

PII: S0272-6386(08)01423-6

doi: 10.1053/j.ajkd.2008.08.031

American Journal of Kidney Diseases
Volume 53, Issue 1 , Pages 138-150 , January 2009