European Journal of Vascular & Endovascular Surgery
Volume 36, Issue 2 , Pages 125-131 , August 2008

Clinical Relevance of Advanced Glycation Endproducts for Vascular Surgery

  • R. Meerwaldt

      Affiliations

    • Department of Surgery, Isala Clinics, Zwolle, The Netherlands
  • ,
  • M.G. van der Vaart

      Affiliations

    • Department of Surgery (Division of Vascular Surgery), University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • G.M. van Dam

      Affiliations

    • Department of Surgery (Division of Vascular Surgery), University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • R.A. Tio

      Affiliations

    • Department of Cardiology, University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • J.-L. Hillebrands

      Affiliations

    • Department of Cell Biology (University of Groningen), University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • A.J. Smit

      Affiliations

    • Department of Internal Medicine (Division of Vascular Medicine), University Medical Center Groningen, Groningen, The Netherlands
  • ,
  • C.J. Zeebregts

      Affiliations

    • Department of Surgery (Division of Vascular Surgery), University Medical Center Groningen, Groningen, The Netherlands
    • Corresponding Author InformationCorresponding author. C. J. Zeebregts, MD, PhD, Department of Surgery, Division of Vascular Surgery, University Medical Center Groningen, P.O. Box 30 001, 9700 RB Groningen, The Netherlands. Tel.: +31 503613382; fax: +31 503611745.

Received 27 November 2007 ,Accepted 16 January 2008.

References 

  1. Monnier VM, Mustata GT, Biemel KL, Reihl O, Lederer MO, Zhenyu D, et al. Cross-linking of the extracellular matrix by the Maillard reaction in aging and diabetes: an update on “a Puzzle Nearing Resolution”. Ann N Y Acad Sci. 2005;1043:533–544
  2. 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(3):235–246
  3. Miyata T, Wada Y, Cai Z, Iida Y, Horie K, Yasuda Y, 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(4):1170–1181
  4. Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes. 1999;48(1):1–9
  5. Monnier VM. Nonenzymatic glycosylation, the Maillard reaction and the aging process. J Gerontol. 1990;45(4):B105–B111
  6. Baynes JW, Thorpe SR. Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med. 2000;28(12):1708–1716
  7. Thorpe SR, Baynes JW. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids. 2003;25(3–4):275–281
  8. Miyata T, Ueda Y, Yoshida A, Sugiyama S, Iida Y, Jadoul M, et al. Clearance of pentosidine, an advanced glycation end product, by different modalities of renal replacement therapy. Kidney Int. 1997;51(3):880–887
  9. Koschinsky T, He CJ, Mitsuhashi T, Bucala R, Liu C, Buenting C, et al. Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci U S A. 1997;94(12):6474–6479
  10. Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, et al. Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A. 1997;94(25):13915–13920
  11. 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(6):1308–1315
  12. Klein DJ, Oegema TR, Brown DM. Release of glomerular heparan-35so4 proteoglycan by heparin from glomeruli of streptozocin-induced diabetic rats. Diabetes. 1989;38(1):130–139
  13. 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
  14. 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(7):1013–1023
  15. Wautier JL, Schmidt AM. Protein glycation: a firm link to endothelial cell dysfunction. Circ Res. 2004;95(3):233–238
  16. 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(7):403–408
  17. 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
  18. 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(6 Pt 1):568–573
  19. Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, 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(12):3687–3693
  20. Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia. 2004;47(7):1324–1330
  21. Yoshida N, Okumura K, Aso Y. High serum pentosidine concentrations are associated with increased arterial stiffness and thickness in patients with type 2 diabetes. Metabolism. 2005;54(3):345–350
  22. Suliman ME, Stenvinkel P, Jogestrand T, Maruyama Y, Qureshi AR, Barany P, 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(6):418–425
  23. Crauwels HM, Herman AG, Bult H. Local application of advanced glycation end products and intimal hyperplasia in the rabbit collared carotid artery. Cardiovasc Res. 2000;47(1):173–182
  24. Cipollone F, Iezzi A, Fazia M, Zucchelli M, Pini B, Cuccurullo C, et al. The receptor RAGE as a progression factor amplifying arachidonate-dependent inflammatory and proteolytic response in human atherosclerotic plaques: role of glycemic control. Circulation. 2003;108(9):1070–1077
  25. Katakami N, Matsuhisa M, Kaneto H, Matsuoka TA, Sakamoto K, Nakatani Y, et al. Decreased endogenous secretory advanced glycation end product receptor in type 1 diabetic patients: its possible association with diabetic vascular complications. Diabetes Care. 2005;28(11):2716–2721
  26. Koyama H, Shoji T, Yokoyama H, Motoyama K, Mori K, Fukumoto S, et al. Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25(12):2587–2593
  27. Wang K, Zhou Z, Zhang M, Fan L, Forudi F, Zhou X, et al. Peroxisome proliferator-activated receptor gamma down-regulates receptor for advanced glycation end products and inhibits smooth muscle cell proliferation in a diabetic and nondiabetic rat carotid artery injury model. J Pharmacol Exp Ther. 2006;317(1):37–43
  28. Yoshida S, Yamada K, Hamaguchi K, Nishimura M, Hatakeyama E, Tsuchida H, 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(5):273–280
  29. McNulty M, Mahmud A, Feely J. Advanced glycation end-products and arterial stiffness in hypertension. Am J Hypertens. 2007;20(3):242–247
  30. Akira K, Amano M, Okajima F, Hashimoto T, Oikawa S. Inhibitory effects of amlodipine and fluvastatin on the deposition of advanced glycation end products in aortic wall of cholesterol and fructose-fed rabbits. Biol Pharm Bull. 2006;29(1):75–81
  31. Lapolla A, Piarulli F, Sartore G, Ceriello A, Ragazzi E, Reitano R, et al. Advanced glycation end products and antioxidant status in type 2 diabetic patients with and without peripheral artery disease. Diabetes Care. 2007;30(3):670–676
  32. Blaauw J, Smit AJ, van Pampus MG, van Doormaal JJ, Aarnoudse JG, Rakhorst G, et al. Skin autofluorescence, a marker of advanced glycation end products and oxidative stress, is increased in recently preeclamptic women. Am J Obstet Gynecol. 2006;195(3):717–722
  33. Kiuchi K, Nejima J, Takano T, Ohta M, Hashimoto H. Increased serum concentrations of advanced glycation end products: a marker of coronary artery disease activity in type 2 diabetic patients. Heart. 2001;85(1):87–91
  34. Falcone C, Emanuele E, D'Angelo A, Buzzi MP, Belvito C, Cuccia M, et al. Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men. Arterioscler Thromb Vasc Biol. 2005;25(5):1032–1037
  35. Fuellen G, Foell D, Nacken W, Sorg C, Kerkhoff C. Absence of S100A12 in mouse: implications for RAGE-S100A12 interaction. Trends Immunol. 2003;24(12):622–624
  36. Burke AP, Kolodgie FD, Zieske A, Fowler DR, Weber DK, Varghese PJ, et al. Morphologic findings of coronary atherosclerotic plaques in diabetics: a postmortem study. Arterioscler Thromb Vasc Biol. 2004;24(7):1266–1271
  37. Mulder DJ, van Haelst PL, Gross S, de Leeuw K, Bijzet J, Graaff R, et al. Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products. Atherosclerosis. 2007;
  38. Berg TJ, Snorgaard O, Faber J, Torjesen PA, Hildebrandt P, Mehlsen J, et al. Serum levels of advanced glycation end products are associated with left ventricular diastolic function in patients with type 1 diabetes. Diabetes Care. 1999;22(7):1186–1190
  39. Zoccali C, Mallamaci F, Asahia K, Benedetto FA, Tripepi G, Tripepi R, et al. Pentosidine, carotid atherosclerosis and alterations in left ventricular geometry in hemodialysis patients. J Nephrol. 2001;14(4):293–298
  40. Simm A, Wagner J, Gursinsky T, Nass N, Friedrich I, Schinzel R, et al. Advanced glycation endproducts: a biomarker for age as an outcome predictor after cardiac surgery?. Exp Gerontol. 2007;42(7):668–675
  41. Koyama Y, Takeishi Y, Arimoto T, Niizeki T, Shishido T, Takahashi H, et al. High serum level of pentosidine, an advanced glycation end product (AGE), is a risk factor of patients with heart failure. J Card Fail. 2007;13(3):199–206
  42. Kilhovd BK, Juutilainen A, Lehto S, Ronnemaa T, Torjesen PA, Hanssen KF, et al. Increased serum levels of advanced glycation endproducts predict total, cardiovascular and coronary mortality in women with type 2 diabetes: a population-based 18 year follow-up study. Diabetologia. 2007;50(7):1409–1417
  43. Meerwaldt R, Lutgers HL, Links TP, Graaff R, Baynes JW, Gans RO, et al. Skin autofluorescence is a strong predictor of cardiac mortality in diabetes. Diabetes Care. 2007;30(1):107–112
  44. Goldberg T, Cai W, Peppa M, Dardaine V, Baliga BS, Uribarri J, et al. Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc. 2004;104(8):1287–1291
  45. Fung F, Sherrard DJ, Gillen DL, Wong C, Kestenbaum B, Seliger S, et al. Increased risk for cardiovascular mortality among malnourished end-stage renal disease patients. Am J Kidney Dis. 2002;40(2):307–314
  46. Wu T, Rifai N, Willett WC, Rimm EB. Plasma fluorescent oxidation products: independent predictors of coronary heart disease in men. Am J Epidemiol. 2007;166(5):544–551
  47. Cuccurullo C, Iezzi A, Fazia ML, De Cesare D, Di Francesco A, Muraro R, et al. Suppression of RAGE as a basis of simvastatin-dependent plaque stabilization in type 2 diabetes. Arterioscler Thromb Vasc Biol. 2006;26(12):2716–2723
  48. Kolodgie FD, Narula J, Haider N, Virmani R. Apoptosis in atherosclerosis. Does it contribute to plaque instability?. Cardiol Clin. 2001;19(1):127–139ix
  49. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, et al. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 2002;106(22):2827–2835
  50. Sugimoto K, Nishizawa Y, Horiuchi S, Yagihashi S. Localization in human diabetic peripheral nerve of N(epsilon)-carboxymethyllysine-protein adducts, an advanced glycation endproduct. Diabetologia. 1997;40(12):1380–1387
  51. Cellek S, Qu W, Schmidt AM, Moncada S. Synergistic action of advanced glycation end products and endogenous nitric oxide leads to neuronal apoptosis in vitro: a new insight into selective nitrergic neuropathy in diabetes. Diabetologia. 2004;47(2):331–339
  52. Meerwaldt R, Links TP, Graaff R, Hoogenberg K, Lefrandt JD, Baynes JW, et al. Increased accumulation of skin advanced glycation end-products precedes and correlates with clinical manifestation of diabetic neuropathy. Diabetologia. 2005;48(8):1637–1644
  53. Veves A, Akbari CM, Primavera J, Donaghue VM, Zacharoulis D, Chrzan JS, et al. Endothelial dysfunction and the expression of endothelial nitric oxide synthetase in diabetic neuropathy, vascular disease, and foot ulceration. Diabetes. 1998;47(3):457–463
  54. Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, et al. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol. 2001;159(2):513–525
  55. Zhou Z, Wang K, Penn MS, Marso SP, Lauer MA, Forudi F, et al. Receptor for AGE (RAGE) mediates neointimal formation in response to arterial injury. Circulation. 2003;107(17):2238–2243
  56. Takeda R, Suzuki E, Satonaka H, Oba S, Nishimatsu H, Omata M, et al. Blockade of endogenous cytokines mitigates neointimal formation in obese zucker rats. Circulation. 2005;111(11):1398–1406
  57. Choi EY, Kwon HM, Ahn CW, Lee GT, Joung B, Hong BK, et al. Serum levels of advanced glycation end products are associated with in-stent restenosis in diabetic patients. Yonsei Med J. 2005;46(1):78–85
  58. Cai W, Zhu L, Chen X, Uribarri J, Peppa M. Association of advanced glycoxidation end products and inflammation markers with thrombosis of arteriovenous grafts in hemodialysis patients. Am J Nephrol. 2006;26(2):181–185
  59. Weiss MF, Scivittaro V, Anderson JM. Oxidative stress and increased expression of growth factors in lesions of failed hemodialysis access. Am J Kidney Dis. 2001;37(5):970–980
  60. Monnier VM, Bautista O, Kenny D, Sell DR, Fogarty J, Dahms W, et al. Skin collagen glycation, glycoxidation, and crosslinking are lower in subjects with long-term intensive versus conventional therapy of type 1 diabetes: relevance of glycated collagen products versus HbA1c as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes. 1999;48(4):870–880
  61. 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(1):41–49
  62. Alderson NL, Chachich ME, Youssef NN, Beattie RJ, Nachtigal M, Thorpe SR, et al. The AGE inhibitor pyridoxamine inhibits lipemia and development of renal and vascular disease in Zucker obese rats. Kidney Int. 2003;63(6):2123–2133
  63. Sebekova K, Gazdikova K, Syrova D, Blazicek P, Schinzel R, Heidland A, 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(4):265–270
  64. Wolffenbuttel BH, Boulanger CM, Crijns FR, Huijberts MS, Poitevin P, Swennen GN, et al. Breakers of advanced glycation end products restore large artery properties in experimental diabetes. Proc Natl Acad Sci U S A. 1998;95(8):4630–4634

PII: S1078-5884(08)00108-1

doi: 10.1016/j.ejvs.2008.01.030

European Journal of Vascular & Endovascular Surgery
Volume 36, Issue 2 , Pages 125-131 , August 2008